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The inheritance of components of resistance to bacterial leaf spot of pepper (Capsicum annum L.)

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Title:
The inheritance of components of resistance to bacterial leaf spot of pepper (Capsicum annum L.)
Creator:
Hibberd, Allen Maxwell, 1950-
Publication Date:
Language:
English
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xvi, 218 leaves : ill. ; 28 cm.

Subjects

Subjects / Keywords:
Bacteria ( jstor )
Diameters ( jstor )
Hypersensitivity ( jstor )
Inoculation ( jstor )
Leaves ( jstor )
Lesions ( jstor )
Memory interference ( jstor )
Peppers ( jstor )
Stall ( jstor )
Xanthomonas campestris ( jstor )
Bacterial diseases of plants ( lcsh )
Leaf spots ( lcsh )
Peppers -- Disease and pest resistance -- Genetic aspects ( lcsh )
Genre:
bibliography ( marcgt )
theses ( marcgt )
non-fiction ( marcgt )

Notes

Thesis:
Thesis (Ph. D.)--University of Florida, 1985.
Bibliography:
Includes bibliographical references (leaves 208-217).
General Note:
Typescript.
General Note:
Vita.
Statement of Responsibility:
by Allen Maxwell Hibberd.

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University of Florida
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University of Florida
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Copyright [name of dissertation author]. Permission granted to the University of Florida to digitize, archive and distribute this item for non-profit research and educational purposes. Any reuse of this item in excess of fair use or other copyright exemptions requires permission of the copyright holder.
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ACY0465 ( NOTIS )
13568361 ( OCLC )
AA00003401_00001 ( sobekcm )

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THE INHERITANCE OF COMPONENTS OF RESISTANCE TO BACTERIAL LEAF
SPOT OF PEPPER (Capsicum annuum L.)











BY

ALLEN MAXWELL HIBBERD


A DISSERTATION PRESENTED TO THE GRADUATE SCHOOL
OF THE UNIVERSITY OF FLORIDA IN
PARTIAL FULFILLMENT OF THE REQUIREMENTS
FOR THE DEGREE OF DOCTOR OF PHILOSOPHY



UNIVERSITY OF FLORIDA


1985
















The efficient discharge of responsibilities in breeding

disease resistant pepper is dedicated to

ALLYN AUSTIN COOK












ACKNOWLEDGMENTS

I owe a debt of gratitude to many individuals and organizations.

To the Queensland Department of Primary Industries for generous

and sustained support, in particular,

to Mr. Robin Barke, for unwavering support;

to Mr. Gary Nahrung for his work;

to Mr. Bob Hall for work behind the scenes.

To the Vegetable Sectional Group of the Committee of Direction of

Fruit Marketing, Queensland, for their farsightedness and

financial support.

To Dr. Allyn Cook for pointing the way on many an occasion.

To the University of Florida, in particular,

to Dr. Don Maynard for his overall support;

to Dr. S. Subramanya for financial assistance, interest and

encouragement. It is impossible to do in three years all

that is desirable;

to Dr. Jack Fry for his fairness;

to the Vegetable Crops Department for my assistantship;

to my supervisory committee, Drs. M. J. Bassett, R. E. Stall,

and C. B. Hall for their perseverance with me;

Thank you Professor Stall

to Ms. Diane Jack, Mr. Gerald Minsavage, and Mr. Ralph Rice

for tireless helping hands;









to others of the faculty of the Vegetable Crops and Plant

Pathology Departments.

To Arthur Yates and Company, Sydney, Australia, for their thought-

ful interest and most generous gift.

To Mrs. Irma Smith for thoughtful dedication to preparing the

manuscript,

My thanks.

Thank you Jo-Anne, for life, forever.












TABLE OF CONTENTS

Page

ACKNOWLEDGMENTS. .. .. iii

LIST OF TABLES .. vii

LIST OF FIGURES. .. xiii

ABSTRACT .. xv

Chapters

1. INTRODUCTION. 1

2. REVIEW OF LITERATURE. .. .. 5

Hypersensitive Resistance 6
Variations in the Pepper--Xanthomonas campestris
pv. vesicatoria System. 9
Hypersensitivity in Other Pathosystems. 12
Nonhypersensitive Resistance to Xcv in Pepper 14
Nonhypersensitive Resistance in Other Pathosystems. 15
Summary .. 18

3. THREE INDEPENDENT GENES FOR RESISTANCE TO BACTERIAL LEAF
SPOT IN A PLANT INTRODUCTION OF PEPPER (Capsicum
annuum L.). .. 19

Materials and Methods 21
Results and Discussion. 26

4. DIFFERENTIATION OF PATHOTYPES OF Xanthomonas campestris
pv. vesicatoria PATHOGENIC ON PEPPER (Capsicum
annuum L.) .... 63

Materials and Methods 65
Results and Discussion. 67

5. ALLELISM OF RACE SPECIFIC GENES FOR HYPERSENSITIVE
RESISTANCES TO Xanthomonas campestris pv. vesicatoria
IN TWO LINES OF PEPPER (Capsicum annuum L.) 87

Materials and Methods 88
Results and Discussion. 93










Page

6. INHERITANCE OF RESISTANCE TO BACTERIAL SPOT IN PEPPER
PLANT INTRODUCTION 163189 105

Materials and Methods ... 106
Results and Discussion. 110

7. INHERITANCE OF NONHYPERSENSITIVE RESISTANCE TO BACTERIAL
SPOT IN A PLANT INTRODUCTION OF PEPPER (Capsicum
annuum L.). 141

Materials and Methods 142
Results and Discussion. 145

8. FIELD RESISTANCE TO BACTERIAL SPOT IN PEPPER CORRELATED
WITH COMPONENTS OF RESISTANCE MEASURED IN GREENHOUSE
PLANTINGS 171

Materials and Methods 172
Results 175
Discussion. 186

9. DISCUSSION. .. 188

Comparison of Hypersensitive and Nonhypersensitive
Resistances .. 189
Inheritance of Nonhypersensitive Resistance 192

10. SUMMARY AND CONCLUSIONS 203

LITERATURE CITED .. 208

BIOGRAPHICAL SKETCH. ........ .218











LIST OF TABLES

Tables Page

3-1. Number of lesions per 2 cm2 of leaf at timed intervals,
and diameter per lesion at 32 days after inoculation
of peppers Early Calwonder and PI 271322 with four
isolates of Xanthomonas campestris pv. vesicatoria 27

3-2. Hypersensitivity in plants of PI 271322 to inoculation
with four isolates of race 1 and eight isolates of
race 2 of Xanthomonas campestris pv. vesicatoria 29

3-3. Number of lesions per 2 cm2 of leaf and diameter per
lesion in peppers 271-4, Early Calwonder, and 10 R
15 days after inoculation with races 1, 2, and 3 of
Xanthomonas campestris pv. vesicatoria 33

3-4. Segregation for hypersensitivity in progenies of peppers
271-4 and Delray Bell inoculated with races 1 and 2 of
Xanthomonas campestris pv. vesicatoria 35

3-5. Segregation for hypersensitivity in progenies of peppers
271-4 and Early Calwonder inoculated with races 1 and
2 of Xanthomonas campestris pv. vesicatoria. 37

3-6. Segregation for hypersensitivity in progenies of the second
backcross to Early Calwonder which, with controls, were
inoculated with races 1 and 2 of Xanthomonas campestris
pv. vesicatoria. 38

3-7. Segregation for hypersensitivity in progenies of the third
backcross which, with controls, were inoculated with
races 1 and 2 of Xanthomonas campestris pv.
vesicatoria. .. 39

3-8. Lesions per 2 cm2 of leaf in peppers with four combinations
of genes BsI and Bs3 following inoculation with races
1 and 2 of Xanthomonas campestris pv. vesicatoria. 42

3-9. Diameters per lesion in peppers with four combinations of
genes Bs1 and Bs1 following inoculation with races 1
and 2 of Xanthomonas campestris pv. vesicatoria. 43

3-10. Lesions per 2 cm2 of leaf and diameter per lesion in pepper
control lines, and second backcross breeding progenies
of genotype Bs1 Bs_ inoculated with races 1 and 2 of
Xanthomonas campestris pv. vesicatoria 45












3-11. Lesions per 2 cm2 of leaf and diameter per lesion in
parents 271-4 and Early Calwonder, F2, and back-
crosses and control line 10 R in two plantings inocu-
lated with race 3 of Xanthomonas campestris pv.
vesicatoria. .. ... .. 47

3-12. Frequency distribution of lesions per 2 cm2 of leaf
occurring in parents 271-4, Early Calwonder, F1, F2,
and backcrosses in two plantings inoculated with race
3 of Xanthomonas campestsris pv. vesicatoria .. 48

3-13. Frequency distribution of diameter per lesion in parents
271-4 and Early Calwonder, Fl, F2, and backcrosses in
two plantings inoculated with race 3 of Xanthomonas
campestris pv. vesicatoria 49

3-14. Analysis of transformed, weighted generation means of
number of lesions per 2 cm of leaf and diameter per
lesion for one planting of progenies of peppers Early
Calwonder and 271-4 inoculated with race 3 of
Xanthomonas campestris pv. vesicatoria 51

3-15. Analysis of transformed, weighted, generation means
of number of lesions per 2 cm of leaf and
diameter per lesion for the second planting of
progenies of peppers Early Calwonder and 271-4
inoculated with race 3 of Xanthomonas campestris
pv. vesicatoria. .. ... 52

3-16. Number of lesions per 2 cm2 of leaf and diameter per lesion
in control lines and progenies of the second backcross
to Early Calwonder inoculated with race 3 of Xanthomonas
campestris pv. vesicatoria. All backcross progeny
plants were of genotype Bs1 Bs3. 54

3-17. Frequency distribution of lesions per 2 cm2 of leaf and
diameter per lesion in pepper control lines and
progenies of genotype Bsi Bs from second backcross
to Early Calwonder inoculated with race 3 of Xanthomonas
campestris pv. vesicatoria 55

4-1. Conductivity as a measure of electrolyte loss at two
temperatures from pepper leaf tissue inoculated with
races 1, 2, and 3 of Xanthomonas campestris pv.
vesicatoria. .. 68


viii


Tables


Page









4-2. Conductivity as a measure of electrolyte loss from leaf
tissue of parents Early Calwonder, 271-4, and their
hybrids inoculated with races 1, 2, and 3 of Xanthomonas
campestris pv. vesicatoria 69

4-3. Sequence of reactions of peppers Early Calwonder, 271-4,
and their hybrid progeny inoculated with races 1, 2,
and 3 of Xanthomonas campestris pv. vesicatoria. 75

5-1. Reaction of pepper lines and tomato to inoculation with
races of Xanthomonas campestris pv. vesicatoria. 90

5-2. Conductivity as a measure of electrolyte loss at two
temperatures from pepper leaf tissues inoculated with
races 1, 2, and 3 of Xanthomonas campestris pv.
vesicatoria. 94

5-3. Segregation for hypersensitive reactions in a pepper test-
cross population inoculated with races 1, 2, and 3 of
Xanthomonas campestris pv. vesicatoria 98

5-4. Number of lesions per 2 cm2 of leaf and diameter per
lesion in parents, F1, test-cross progeny and line
10 R inoculated with race 3 isolate Xv 69-1 of
Xanthomonas campestris pv. vesicatoria 100

5-5. Number of lesions per 2 cm2 of leaf and diameter per
lesion in samples of plants of parents, F1, test-
cross progeny, and check line 10 R inoculated with
race 1 isolate Xv 80-5 of Xanthomonas campestris
pv. vesicatoria. ... 102

6-1. Lesions per 2 cm2 of leaf at four sampling times and mean
diameter per lesion 35 days after inoculation of
peppers with races 1, 2, and 3 of Xanthomonas
campestris pv. vesicatoria 112

6-2. Conductivity as a measure of electrolyte loss from pepper
leaf tissue inoculated with race 2 of Xanthomonas
campestris pv. vesicatoria and incubated at either
of two temperatures. 117

6-3. Number of lesions per 2 cm2 and diameter per lesion in
leaves of 189-5, and check lines Early Calwonder and
10 R 15 days after inoculation with races 1, 2, and
3 of Xanthomonas campestris pv. vesicatoria. 118

6-4. Number of lesions per 2 cm2 of leaf and diameter per lesion
of parents, F1, F2, both backcrosses, and check lines
two weeks after inoculation with 1.1 x 103 cfu ml" of
isolate Xv 82-7 of race 2 of Xanthomonas campestris
pv. vesicatoria. ... 123


Tables


Page









6-5. Frequency distribution of number of lesions per 2 cm2 of
leaf in parental, F1, F2, and both backcross gener-
ations inoculated with race 1 isolate Xv 82-8 of
Xanthomonas campestris pv. vesicatoria 124

6-6. Frequency distribution of diameter per lesion in parental,
F1, FT, and both backcross generations inoculated with
race isolate Xv 82-8 of Xanthomonas campestris pv.
vesicatoria. .. 125

6-7. Frequency distribution of number of lesions per 2 cm2 of
leaf in parental, F1, Fg, and both backcross generations
inoculated with race 3 isolate Xv-77-3A of Xanthomonas
campestris pv. vesicatoria .. 126

6-8. Frequency distribution of diameter per lesion in parental,
F1, F2, and both backcross generations inoculated with
race isolate Xv 77-3A of Xanthomonas campestris pv.
vesicatoria. .. 127

6-9. Number of lesions per 2 cm2 of leaf and diameter per lesion
in resistant and susceptible plants in parental, F1,
F2, both backcros es, and check lines inoculated with
1.5 x 10i cfu ml" of race 3 isolate Xv 77-3A of
Xanthomonas campestris pv. vesicatoria 129

6-10. Generation means analysis of number of lesions per 2 cm2
of leaf and lesion diameter from Florida VR-4 x 189-5
progenies inoculated with isolate Xv 82-8 of race 1 of
Xanthomonas campestris pv. vesicatoria .. 132

6-11. Generation means analysis of number of lesions per 2 cm2
of leaf and mean lesion diameter from Florida
VR-4 x 189-5 progenies inoculated with isolate
Xv 77-3A of Xanthomonas campestris pv. vesicatoria 133

7-1. Number of lesions per 2 cm2 of leaf at timed intervals
and diameter per lesion at 32 days after inoculation
of peppers Early Calwonder and PI 246331 with four
isolates of Xanthomonas campestris pv. vesicatoria 146

7-2. Estimated bacterial populations per cm2 of leaf in samples
from peppers 246-4 and Early Calwonder inoculated with
races 1, 2, and 3 of Xanthomonas campestris pv.
vesicatoria. 149

7-3. Lesions per 2 cm2 of leaf and diameter per lesion in
peppers Early Calwonder and 246-4 15 days after
inoculation with races 1, 2 and 3 of Xanthomonas
campestris pv. vesicatoria 150


Tables


Page










7-4. Number of lesions per 2 cm2 of leaf and diameter per lesion
in leaves of parental, F1, F2, and backcross populations
of the cross between peppers Early Calwonder and 246-4
inoculated with races 1, 2, and 3 of Xanthomonas
campestris pv. vesicatoria 151

7-5. Frequency distribution of lesions per 2 cm2 of leaf in
parents Early Calwonder and 246-4, and F1, F2 and race
1 of Xanthomonas campestris pv. vesicatoria. 154

7-6. Frequency distribution of lesions per 2 cm2 of leaf in
parents Early Calwonder and 246-4, and F1, F and
backcross populations inoculated with races and 3
of Xanthomonas campestris pv. vesicatoria. 155

7-7. Analysis of weighted generations means of number of
lesions per 2 cm of leaf and diameter per lesion
in progenies of peppers Early Calwonder and 246-4
inoculated with isolate Xv 77-3A of Xanthomonas
campestris pv. vesicatoria 156

7-8. Analysis of weighted generation means of numbers of
lesions per 2 cm of leaf and diameter per lesion
in progenies of peppers Early Calwonder and 246-4
inoculated with isolate Xv 82-8 of Xanthomonas
campestris pv. vesicatoria 158

7-9. Frequency distribution of lesion diameter in parents
Early Calwonder and 246-4, and Fl, F2, and backcross
populations inoculated with race 1 and Xanthomonas
campestris pv. vesicatoria 159

7-10. Frequency distribution of lesion diameter in parents
Early Calwonder and 246-4, F1, F2, and backcross
populations inoculated with races 2 and 3 of
Xanthomonas campestris pv. vesicatoria 160

7-11. Comparison of means of lesions per 2 cm2 of leaf and
diameter per lesion for each of three isolates of
Xanthomonas campestris pv. vesicatoria among plants of
the F2 and first backcross to the susceptible parent
selected only for high numbers of leaves of one of the
isolates ... .. 163

7-12. Analysis of weighted generation means of numbers of lesions
per 2 cm2 of leaf and diameter per leasion for progenies
of peppers Early Calwonder and 246-4 inoculated with
isolate Xv 77-3 of Xanthomonas campestris pv.
vesicatoria. .... .... .. 165


Page


Tables










7-13. Analysis of weighted generation means of number of lesions
per 2 cm2 of leaf and diameter per lesion for progenies
of peppers Early Calwonder and 246-4 with isolate
Xv 83-1 of Xanthomonas campestris pv. vesicatoria. 166

8-1. Lesions per 2 cm2 of leaf and diameter per lesion at 32 days
after inoculating pepper plant introductions and control
cultivar with races 1, 2, and 3 of Xanthomonas
campestris pv. vesicatoria 177

8-2. Lesions per 2 cm2 of leaf and diameter per lesion 21 days
after inoculating inbred pepper plant introductions,
breedling lines, and control cultivar with race 3 of
Xanthomonas campestris pv. vesicatoria 179

8-3. Lesions per 2 cm2 of leaf and diameter per lesion in two
pepper lines at timed intervals after inoculation
with races 1 and 2 of Xanthomonas campestris pv.
vesicatoria. .. 183

8-4. Estimated bacterial populations in leaf samples from
six pepper lines at timed intervals after inoculating
with races 1, 2, and 3 of Xanthomonas campestris pv.
vesicatoria. 184

8-5. Disease severity (area under disease progress curve) in
field planted pepper lines inoculated with three races
of Xanthomonas campestris pv. vesicatoria. 185


Tables


Page












LIST OF FIGURES


Figures Page

3-1. Populations of bacteria per cm2 of leaf of peppers Early
Calwonder and 271-4 inoculated with races 1, 2, and
3, and pepper 10 R inoculated with race 2 of
Xanthomonas campestris pv. vesicatoria 32

3-2. Generation means of lesions per 2 cm2 of leaf and diameter
per lesion related to theoretical frequency of the
allele for susceptibility in parents, Fl, F? and
backcross pepper populations inoculated with race 3 of
Xanthomonas campestris pv. vesicatoria .... 58

3-3. Generation means of lesions per 2 cm2 of leaf and diameter
per lesion related to theoretical frequency of the
allele for susceptibility in parents and second
backcross breeding progenies inoculated with race 3
of Xanthomonas campestris pv. vesicatoria. 60

4-1. Conductivity as a measure of electrolyte loss from leaf
tissue of peppers inoculated with races 1, 2, and 3
of Xanthomonas campestris pv. vesicatoria. 71

4-2. Conductivity as a measure of electrolyte loss from leaf
tissue of peppers Early Calwonder, 271-4 and their
hybrids inoculated with races 1 and 2 of Xanthomonas
campestris pv. vesicatoria .. .. 73

4-3. Populations of bacteria per cm2 of leaf of peppers Early
Calwonder, 271-4, and their reciprocal hybrids (pooled
data) inoculated with race 1 isolate Xv 71-21 of
Xanthomonas campestris pv. vesicatoria 79

4-4. Populations of bacteria per cm2 of leaf of peppers Early
Calwonder, 271-4, and their reciprocal hybrids (pooled
data) inoculated with race 2 isolate Xv E3 of
Xanthomonas campestris pv. vesicatoria 81

4-5. Populations of bacteria per cm2 of leaf of peppers Early
Calwonder, 271-4, and their reciprocal hybrids (pooled
data) inoculated with race 3 isolate Xv 69-1 of
Xanthomonas campestris pv. vesicatoria 83

5-1. Conductivity as a measure of electrolyte loss from pepper
leaf tissues inoculated with three races of Xanthomonas
campestris pv. vesicatoria ... .. 96


xiii











6-1. Electrical conductivity as a measure of electrolyte loss
from leaf tissue of peppers inoculated with sterile
water and race 2 of Xanthomonas campestris pv.
vesicatoria. 115

6-2. Bacterial populations in pepper leaves inoculated with
isolates of races 1, 2, and 3 of Xanthomonas
campestris pv. vesicatoria 120

6-3. Variation in number of lesions per 2 cm2 of leaf related to
theoretical frequency of the allele for susceptibility
in pepper generations inoculated with two isolates of
Xanthomonas campestris pv. vesicatoria 135

6-4. Variation in lesion diameters related to theoretical
frequency of the allele for susceptibility in pepper
generations inoculated with two isolates of Xanthomonas
campestris pv. vesicatoria 137

8-1. Relation between number of lesions per 2 cm2 of leaf and
diameter per lesion in resistant and susceptible peppers
inoculated with race 3 of Xanthomonas campestris pv.
vesicatoria. 181


Figures


Page











Abstract of Dissertation Presented to the Graduate School
of the University of Florida in Partial Fulfillment of the
Requirements for the Degree of Doctor of Philosophy

THE INHERITANCE OF COMPONENTS OF RESISTANCE TO BACTERIAL LEAF
SPOT OF PEPPER (Capsicum annuum L.)

By

Allen Maxwell Hibberd

December 1985

Chairman: Dr. M. J. Bassett
Major Department: Horticultural Science

Inheritance of resistance to bacterial leaf spot of pepper

(Capsicum annuum L.) incited by Xanthomanas campestris pv. vesicatoria

(Doidge) Dye was evaluated in progenies of resistant germplasm crossed

with susceptible bell pepper.

The basis for designating pathogenic races was avirulence on

plants with genes derived from PI 271322. Race 1 induced a hyper-

sensitive response (HR) in plants with Bs3, race 2 induced HR in plants

with Bsl, and race 3 did not induce HR. Race 3 occurred frequently in

laboratory cultures of races 1 and 2.

Eighteen PI and 6 breeding lines had genetic resistance to races

1, 2, and 3. In addition, plants of PI 163189 had gene Bsj, and PI

271322 had Bsi and Bs3.

Resistance to race 1 and to race 2 was detected after injections

of leaves of plants with BsI and Bs3 with high concentrations of inocula

(>108 cells ml-1). Collapse of tissues occurred within 24 hours with












race 1 and 12 hours with race 2. Concomitantly, electrolyte losses

occurred and bacterial multiplication was inhibited. Both genes were

incompletely dominant in heterozygotes of PI 271322 crossed with

susceptible pepper.

The gene Bs2 in cv. Florida XVR 3-25 controlled HR to both races 1

and 3. Genes Bsi, Bs2, and Bs3 segregated independently in crosses.

Resistance to race 3 and concomitantly to races 1 and 2 was iden-

tified after injections of leaves with low concentrations of inocula

(2 x 103 cells ml-1). In resistant plants, lesions were fewer and always

smaller than in susceptible plants. Lesion diameter and field resist-

ance to race 3 were correlated (r=0.99).

Monogenic additive-gene action controlled resistances to race 3 in

PI 163189, 246331, and 271322. Lesion diameters in heterozygotes varied

around mid-parent values. Parental values varied according to the

bacterial isolates used for inoculation. Lesion numbers in heterozy-

gotes were few with weak isolates, but equalled the susceptible parent

with aggressive isolates. The proposed symbol for this gene in PI

271322 is Bs4. Gene Bs4 segregated independently of Bs1 and Bs3 in

crosses. Bell pepper stocks with all four genes were produced.











CHAPTER 1
INTRODUCTION

Bacterial leaf spot, incited by the gram negative, motile

bacterium, Xanthomonas campestris pv. vesicatoria (Doidge, 1920), Dye

1978 (hereafter designated Xcv), is the most destructive leaf disease of

bell pepper (Capsicum annuum L.) in warm humid environments. Disease

severity varies with the time of primary infection and may extend from

loss of a few lower leaves to complete defoliation of susceptible culti-

vars. Yield loss accrues from failure to set fruit, and from undersized

and sunburnt fruit. Refoliation and additional flowering can occur but

fruit set are later maturing and smaller. Quantitative yield data to

assess the effects of disease are uncommon, but, overall, a loss of 10%

to production in the state of Florida may be average. This translates

to a fruit value of $7.5 million on 1983-84 figures (Hochmuth and

Maynard, 1985).

The bacterial spot organism is endemic in warm humid environments.

A prime source of inoculum is overwintering and oversummering volunteer

peppers and tomatoes (Krupka and Crossan, 1956; Person, 1965; Pohronezny,

1984). Inoculum dispersal is aided by a continuum over time of pepper

and tomato crops in many regions, and frequent wind driven rains

(Vakili, 1967). Disease control by sanitation has been insufficient to

eliminate the need for chemical and genetic control of Xcv. Chemical

control relies on frequent sprays with copper and mancozeb mixture

(Marco and Stall, 1983). However, the most strictly applied spray

regime is expected to be less effective than genetic resistance to the






2

pathogen. Resistant cultivars are the more energy efficient method of

disease control, and they contribute to major savings in crop production

costs.

Several releases of bell pepper (Cook, 1984; Cook et al., 1976;

Cook et al., 1977) were selected in part for the dominant genes for

hypersensitive resistance, BsI (Cook and Stall, 1963), and Bs2 (Cook and

Guevara, 1984). Race 2 of the strain of Xcv pathogenic on pepper (Cook

and Stall, 1969) induced the hypersensitive reaction (HR) in plants with

Bs1, but virulence of race 1 was not affected by this gene (Cook and

Stall, 1968; 1969; 1982). The gene Bs2 controlled hypersensitivity to

race 1 (Cook and Guevara, 1982; 1984), and isolates virulent on plants

with BsI and Bs2 were not observed in limited testing. Recently, Kim

and Hartmann (1985) reported a third gene Bs3, which also controls HR to

isolates of race 1. The relation between Bs2 and Bs3 is unknown, and

Kim and Hartmann (1985) assumed they were different loci. Releases of

bell pepper with Bs3 have not been made, and testing for pathogenic

variability in relation to Bs3 was not extensive (Kim and Hartmann,

1985).

Race 2 of Xcv occurs with race 1 in Florida but has been detected

in few other pepper producing areas of the world (Cook and Stall, 1982;

F.R.J.B. Reifschneider, 1985, personal communication to R.E. Stall).

Nevertheless, BsI was useful in delaying disease progress in Florida

(Dahlbeck et al., 1979). The Bs3 gene appeared to contribute much to

low disease severity in field plantings infected with race 1 (Kim and








3

Hartmann, 1985). Resistance to race 1 controlled by both Bs2 and Bs3

together, if indeed the genes are different, may be long lasting.

Stable resistance to Xcv is found in many pepper plant

introductions (PI lines) (Adamson and Sowell, 1983; Borchers, 1965;

Dempsey, 1953; Hibberd et al., 1979; Hibberd and Gillespie, 1982a; Kim,

1983; Sowell and Dempsey, 1977; Stall, 1981). Most sources lack

hypersensitive responses to races 1 and 2 (Cook and Stall, 1969; Kim,

1983; Stall, 1981). Nevertheless, disease severity was consistently

very low on these lines. No releases of bell pepper have yet been made

using these sources of resistance. Borchers (1965) used several PI

lines, and made progress by selecting among naturally infected plantings

of inbred backcrosses. Breeding was discontinued, however, and seed is

no longer available (E.A. Borchers, 1978, personal communication).

Progress has been slow in other breeding programs (Adamson and Sowell,

1983; Hibberd and Gillespie, 1982a). There are several reasons for

this:

1. Some plant breeders are unwilling to use race specific genes

for fear of instability of resistance (Adamson and Sowell, 1983; Hibberd

and Gillespie, 1982a).

2. Inoculation techniques that are frequently used fail to

introduce the bacteria directly into the mesophyll of leaves, which is

the site of bacterial activity (Stall and Cook, 1966). Using these

techniques, consistent, quantifiable data are not reliable and estimates

of heritability of resistance are reduced accordingly (Adamson and

Sowell, 1983; Hibberd and Gillespie, 1982a).











3. Genetics of resistance is often assumed to be complex and

quantitative.

4. Guiding plant pathologists may regard the hypersensitive

reaction as an artifact of the unnaturally high inoculum density used to

detect it most easily (Klement et al., 1964). This has the effect of

enforcing a selection task more difficult than necessary on unsuspecting

plant breeders.

5. More than one resistance mechanism occurring in single plants

may not be recognized unless appropriate inoculation techniques are

used. Inheritance studies may be confounded unless variability in host

responses is recognized (Adamson and Sowell, 1983; Kim and Hartmann,

1985; Stall, 1981).

It is important that genes responsible for stable, effective

resistance be identified and characterized. Knowledge of efficient

selection methods will simultaneously accrue. Research was undertaken

with these views in mind. Particular attention was given to two

aspects. These were allelism and characterization of known genes for

hypersensitive resistance, and the inheritance of genes for nonhyper-

sensitive resistance. As a consequence, efficient selection procedures

were defined, and resistance genes were moved from commercially

unadapted germplasm to bell pepper.

This research is comprised of a series of related topics and

experiments. They are described in several discreet chapters. The

reader is forewarned that this was achieved at the expense of some

repetition.













CHAPTER 2
REVIEW OF LITERATURE

Apparently healthy plants may harbor a wide range of bacteria

(Leben, 1974). These gain entry through natural plant openings, such as

stomata and hydathodes, and through wounds such as those induced by wind

and rain driven sand particles (Goodman, 1982; Vakili, 1967). The bac-

terium, after entering, may induce the following to happen: If the bac-

terium is a saprophyte, bacteria may multiply little if at all, and no

host tissue damage occurs. If the bacterium is a parasite, numbers may

increase over a short time span (often measured in hours) and subse-

quently stabilize or decline slowly with no visible damage occurring.

This sequence of events is associated with localized hypersensitive

death of host cells. A second reaction type may occur with parasitic

bacteria in that populations continue to increase to high levels, which

is associated with extensive and visible host tissue necrosis. This is

the susceptible reaction.

Resistance to a parasitic bacterium is usually observed as lower

disease severity consistent with lower bacterial populations. Low

populations of bacteria are often associated with hypersensitivity, but

other forms of resistance may occur which are not typically hypersens-

itive (Klement, 1982). Nevertheless, hypersensitivity appears to be a

general resistance mechanism in plants to bacterial parasites (Klement,

1982).








Hypersensitive Resistance

Hypersensitivity in plants is commonly observed after inoculation

of species of pseudomonads and xanthomonads among phytopathogenic bac-

teria. Its development in plants after inoculation has been useful both

as an aid to identification of bacterial species (Lelliott et al.,

1966) and determination of host ranges (Klement, 1982). A hypersensi-

tive reaction (HR) occurs in plant species which normally are not sus-

ceptible to the bacterial species. In all examples studied, HR was

found associated with vastly fewer bacteria per unit area of leaf than

occurring in compatible, susceptible reactions (Allington and Chamber-

lain, 1949; Ercolani and Crosse, 1966; Klement et al., 1964; Lyon and

Wood, 1976; Roebuck et al., 1978).

As a consequence, HR was sought also in pathosystems involving

normally compatible bacteria, and many examples of its occurrence can

now be cited (Brinkerhoff et al., 1984; Cook, 1973; Cook and Guevara,

1984; Cook and Stall, 1968, 1969; Fallik et al., 1984; Gitaitis, 1983;

Kim and Hartmann, 1985; Lawson and Summers, 1984; Long et al., 1985;

Mukherjee et al., 1966; Patel, 1982; Smith and Mansfield, 1981; Walker

and Patel, 1964). In those cases studied closely, HR was found to

function in the same manner as that occurring between parasitic bacteria

and nonhost species (Al-Mousawi et al., 1982; Cook and Stall, 1968; Lyon

and Wood, 1976; Roebuck et al., 1978; Stall and Cook, 1966); that is,

host cell metabolism was severely disrupted and death soon followed.

Concomitantly, bacterial populations were much lower than in susceptible

reactions.

The HR is inducible (Meadows and Stall, 1981; Klement, 1982).

Cell-to-cell contact between living host and bacterial cells is required







7

for induction of HR but not the susceptible reaction (Lyon and Woods,

1976; Stall and Cook, 1979; Young, 1974). However, Keen and Holliday

(1982) and Long et al. (1985) argued against the requirement for cell-to-

cell contact. A specific recognition event is presumed to occur during

this phase (Keen, 1982) but its nature is unknown (Staskawicz et al.,

1984). The recognition is under genetic control (Stall, 1985; Staska-

wicz et al., 1984) according to the model of a locus in the pathogen

interacting with a complementary locus in the host (Flor, 1955). Induc-

tion time for HR varies in part with inoculum concentration. In some

pathosystems a longer time is required for symptoms of HR to occur when

low concentrations of bacteria are used than with high concentrations

(Essenberg et al., 1979). This implies a minimum concentration of

interacting gene products is essential for HR to proceed. Length of the

induction period is usually measured in plant tissues inoculated with

high concentrations of bacteria. In such tests, induction time varies

between approximately 1 and 5 h after inoculation after which HR usually

proceeds irreversibly (Klement, 1982).

Once HR is induced, host cell collapse follows a latent period of

variable length, during which biochemical events leading to cell col-

lapse are presumed to occur (Klement, 1982). The cell-collapse phase of

HR occurs with an irreversible breakdown of membranes and plastids, and

the mixing of cytoplasmic and vacuolar contents (Al-Mousawi et al.,

1982; Cook and Stall, 1968; Lyon and Wood, 1976; Roebuck et al., 1978;

Stall and Cook, 1966). Inoculated leaf tissues lose turgor as metabol-

ism is disrupted, and loss of electrolytes increases greatly (Cook and

Stall, 1968; Cook and Guevara, 1984). Electrolyte losses also occur







8

from tissues in the susceptible reaction but the rate of increase is

slow and gradual in comparison with HR-induced losses. Concomitantly,

bacteria cease multiplying (Klement et al., 1964), and their numbers may

progressively decline over time (Cook and Guevara, 1984). Host cells

may accumulate large amounts of antibiotic phytoalexins prior to tissue

collapse (Long et al., 1985). Release of these and acid vacuolar

contents during cell collapse imposes a localized environment which

inhibits further bacterial multiplication (Klement et al., 1964; Long et

al., 1985), and bacteria may die.

High inoculum concentration is vital to detect HR easily. All

host cells in the inoculated tissue collapse in response to inoculum

containing 107 to 108 cells ml-1. Genes in pepper for hypersensitivity

were not identified and characterized as such until their phenotypes

were clearly visualized by using such high concentrations (Cook and

Guevara, 1984; Cook and Stall, 1963; Kim and Hartmann, 1985; Stall and

Cook, 1966). Necrotic hypersensitive flecks will develop occasionally

in leaves that are surface sprayed with the same high concentration of

bacteria. Bacteria may have entered through some stomata in sufficient

numbers for isolated visible HR-necroses to develop (Cook and Stall,

1963). When leaves are infiltrated with low concentrations of bacteria,

occasional small necrotic flecks may result from limited bacterial

multiplication (Essenberg et al., 1979), but visible necroses often do

not occur.

Hypersensitivity appears to be under genetic control. The host

genes that are responsible for its induction in cultivars or plant

introduction (PI) lines of a normally susceptible species can be

explored by genetic crosses. However, inheritance of surprisingly










few reactions has been examined (Long et al., 1985), and much of the

knowledge of HR stems from the work of Cook and Stall with pepper

(Capsicum annuum L.) and Xanthomonas campestris pv. vesicatoria (Doidge,

1920), Dye 1978 (hereafter designated as Xcv).

Variation in the Pepper--Xanthomonas campestris
pv. vesicatoria System

Three dominant genes for HR to Xcv have been described in pepper.

Subscripts following gene designation follow the terminology of Lippert

et al. (1965). The first gene, Bsl, was found in a heterogenous PI line

(Cook and Stall, 1963). Hypersensitivity induced by Bs1 was confirmed

by observations of ultrastructure (Sasser, Stall, and Cook, 1968),

leakage of ions from inoculated tissue (Cook and Stall, 1968), and

changes in bacterial populations in vivo (Cook, 1973; Stall and Cook,

1966). The gene was incorporated by standard backcrossing with

selection into releases of several bell peppers (Cook, 1984; A.A. Cook,

1979 and 1982, personal communications).

From an early stage of selection for BsI in segregating progeny,

variants of Xcv were noted which induced a susceptible reaction rather

than HR. Two races were clearly differentiated by plants with this

gene. Race 1 induced the susceptible reaction, and race 2 induced HR.

Near isogenic lines of pepper, with the difference based on Bs1, were

produced. These have found extensive use in studies of the physiology

of HR (Cook, 1973; Cook and Stall, 1968, 1971; Stall et al., 1981),

induction of HR (Meadows and Stall, 1981; Stall et al., 1974; Stall and

Cook, 1979), racial instability in Xcv (Dahlbeck and Stall, 1979;

Dahlbeck et al., 1979; Stall et al., 1984), influence of BsI on







10

disease progress and pathogenesis (Dahlbeck et al., 1979; Stall, 1985)

and the distribution in nature of races of Xcv (Cook and Stall, 1982).

The HR to race 2 was observed in several other PI lines (Cook and Stall,

1969) but allelism of genes was not tested.

Races 1 and 2 of the pepper strain of Xcv occur in Florida's

pepper producing areas, but race 1 and not race 2 appears to predominate

in other regions of the world (Cook and Stall, 1982). Resistance to

race 1 is essential for control of bacterial spot. Cook reported a

dominant gene, Bs2, for HR to race 1, which he found in a plant intro-

duction of C. chacoense L. (Cook and Guevara, 1982; 1984). A recent

bell pepper release (Cook, 1984) was produced by selecting for Bs2 in

recurrent backcrosses to a cultivar with Bs1. The HR controlled

by Bs2 differed symptomatically from that controlled by Bs1 (Cook and

Guevara, 1982), and Cook (1977) suggested linkage of resistance to both

races 1 and 2 occurred in the C. chacoense line. Kim and Hartmann

(1985) assumed that Bs2 controlled HR to both races 1 and 2, but their

assumption was based on a mis-interpretation of the Cook and Guevara

(1982) abstract. Isolates of race 1 virulent on plants with Bs2 were

not detected in limited testing (A.A. Cook, 1984, personal communica-

tion). The extensive studies of HR controlled by Bsl have not been

repeated with Bs2.

Recently Kim and Hartmann (1985) reported another dominant gene,

Bs3, in C. annuum that controls HR to race 1 of the pepper strain.

Hypersensitivity induced by this gene was not characterized. The few

isolates tested induced HR in plants with B_3. The genetic relationship

between Bs2 and Bs3 is unknown.






11

Concomitantly with this work, other isolates of Xcv were noted

that induced hypersensitivity in all tested peppers, irrespective of the

presence of Bs1, Bs2, or Bs3. Susceptibility occurred in tomato, and

these isolates were designated as the tomato strain of Xcv to

distinguish them from races 1 and 2 of the pepper strain (Cook and

Stall, 1969). The HR to the tomato strain differed in several ways from

HR of plants with BsI to race 2 of the pepper strain (Cook, 1973). The

HR to the tomato strain was symptomatically different and was visibly

slow in developing. The loss of ions from leaf tissue infiltrated with

the tomato strain was intermediate to losses occurring with HR in plants

with Bsi inoculated with race 2 and the susceptible reaction. Bacterial

populations were correspondingly higher with the tomato strain than with

race 2 in plants with Bsl, but lower than in the fully susceptible

reaction. Several environmental variables (light, darkness, and Ca

(NO3)2-infiltrated leaves) had contrasting influences on the two forms

of HR. These comparisons are evidence that HR induced by distinct

pathotypes may involve quite different biological processes. One

process is inherited as a dominant, single-gene trait, but genetic

variability could not be determined for the other.

The tomato strain of Xcv is a variant based on the reaction of two

host species. It may more appropriately be regarded as a pathovar of

Xanthomonas campestris distinct from Xcv in that pepper does not appear

to be its natural host. Similarly, Kimura et al. (1972) mentioned

Brazilian isolates of Xcv which induced HR in tomato and susceptibility

in pepper irrespective of the presence of Bsi (F.R.J.B. Reifschneider,

1985, personal communication to R.E. Stall). Two profitable areas for







12

future research may involve identifying the genetic factors in pepper

and tomato responsible for these two differential host-pathogen inter-

actions, and transferring them reciprocally between plant species.

Nevertheless, Capsicum is a diverse genus which may yield many other

forms of HR to Xcv that are transferrable by crossing within C. annuum.

Hypersensitivity in Other Pathosystems

The HR in the pepper and Xcv system is a model because of the

extent of its characterization and usage. Other pathosystems have been

treated to varying extents. The HR in soybean to the bacterial blight

organism has also been intensively studied (Keen, 1982; Staskawicz et

al., 1984; Long et al., 1985) but with relatively little effort directed

to inheritance of resistance (Mukherjee et al., 1966). Patel (1982)

reported two race-specific dominant genes in cowpea for HR to bacterial

pustule. The reaction to one race developed consistently slower by

several hours than HR to the other race in the same plant, but both

appeared typical of HR. Genes in cotton for hypersensitivity to bacter-

ial blight also are dominant (Brinkerhoff et al., 1984), appear to be

race specific (Bayles and Johnson, 1985), and have been recombined in

useful releases. The races of the blight bacterium have not been

characterized extensively. Dominant, race-specific genes for HR in

several other pathosystems have found commercial use (Walker and Patel,

1964; Taylor et al., 1978; Innes et al., 1984; Fallik et al., 1984;

Lawson and Summers, 1984). Those and others have been characterized to

varying extents (Ercolani and Crosse, 1966; Lyon and Woods, 1976;

Roebuck et al., 1978; Young, 1974). Slow developing or atypical hyper-

sensitivity has been reported also in several pathosystems besides

pepper with Xcv. Both Patel (1982) and Gitaitis (1983) reported that







13

isolates of the bacterial pustule organism in cowpea induced a slow

developing atypical HR. Ersek and Hevesi (1983), Jones and Fett (1985),

and Long et al. (1985) reported intermediate, that is, slow developing

HR in soybean inoculated with the bacterial blight organism, and Smith

and Mansfield (1981) characterized some effects of slow HR in oats to

the halo blight bacterium. Cucumber reacted to the angular leaf spot

bacterium with atypical HR (Dessert et al., 1982). In all cases, atypi-

cal HR represented a high degree of resistance to the pathogen and

resembled the description of HR in pepper to the tomato strain of Xcv

(Cook, 1973).

Commonly, typical HR is race-specific (Keen, 1982). This may not

be so for atypical or slow developing HR (Cook, 1973). Patel (1982)

preferred to select for the slow developing HR since it appeared func-

tional against all races. However, in the few cases studied, these

resistances were recessively inherited in contrast to dominance of typi-

cal, race-specific HR (Dessert et al., 1982; Jones and Scott, 1985;

Patel, 1982). Consequently, inbred backcross progenies may be necessary

for selection purposes. This effectively doubles the number of genera-

tions required in breeding for these resistances. Despite these acknowl-

edged variations, hypersensitivity is considered a qualitative trait of

major effect. It is functional at widely different plant maturities

(Laurence and Kennedy, 1974; Bayles and Johnson, 1985; Cook and Stall,

1968), and inoculum concentrations (Essenberg et al., 1979; Turner and

Novacky, 1974), and is significantly influenced only by extremes of

environmental conditions (Cook, 1973; Stall and Cook, 1979; Keen, 1982;

Klement, 1982).









Nonhypersensitive Resistances to Xcv in Pepper

Genes for HR in pepper were found in a few PI lines only after ex-

tensive testing of germplasm derived mainly from the Indian subcontinent

(Cook, 1977; Cook and Stall, 1963; Kim and Hartmann, 1985; Sowell,

1980). Many other PI lines were found which also are highly resistant

to Xcv (Borchers, 1965; Dempsey, 1953; Greenleaf, 1960; Hibberd et al.,

1979; Hibberd and Gillespie, 1982a; Kim, 1983; Sowell, 1960; Sowell and

Dempsey, 1977). These lines either lacked HR entirely or were hetero-

geneous for HR to races 1 or 2 (Cook and Stall, 1969; Kim and Hartmann,

1985). No PI line, with the possible exception of the above mentioned

C. chacoense line with Bs2, was observed with HR to both races. Several

nonhypersensitively resistant PI lines have been used in breeding.

Borchers (1965) and Hibberd and Gillespie (1982a) selected resistant

segregates from among field-grown, naturally infected F3 and inbred

backcross progenies. By implication, this resistance was not inherited

as a dominant trait, but as a recessive or incomplete recessive (Hibberd

and Gillespie, 1982a). Two independent resistance genes were detected

only in F3 progenies of crosses between resistant PI lines and suscept-

ible bell pepper (Adamson and Sowell, 1983).

Substantial progress was made in breeding for nonhypersensitive

resistance, but releases of bell pepper have not eventuated. Several

reasons contributed to slow progress. Selection in field-planted

progenies was, not unexpectedly, effective only in environments highly

conducive to disease spread (Hibberd and Gillespie, 1982a). Similarly,

selection was ineffective in some greenhouse-grown experiments of short

duration. In these, bacteria were applied only superficially to leaves








15

(Adamson and Sowell, 1983). The inoculum dosage actually received at

the mesophyll where bacteria multiply cannot be standardized in such

tests. Heritability of resistance was low.

These problems were circumvented by examining components of

resistance (Stall, 1981; Stall et al., 1982b). Initial numbers of bac-

teria per unit of leaf area are directly proportional to their concen-

tration in inoculum used to infiltrate leaves (Klement et al., 1964;

Essenberg et al., 1979; Dahlbeck and Stall, 1979; Turner and Novacky,

1974; Stall et al., 1982b). Bacterial colonies develop in the mesophyll

from single bacteria (Essenberg et al., 1979). These may grow to form

lesions, and their frequency per unit area of leaf reflects resistance

(Stall, 1981; Stall et al., 1982b). Nonhypersensitive resistance in

pepper assessed by this method was recessive but continuously distrib-

uted (Stall, 1981). Resistance selected in an F2 progeny was highly

heritable, and F3 lines were identified which were homozygous and

and homogeneous (R.E. Stall, 1982, personal communication). Nonhyper-

sensitive resistance was more clearly and effectively identified by this

technique than any other (compare Cook and Stall, 1969; and Stall,

1981). Replication within plants was necessary to quantify resistance.

Seedlings were therefore required to be at a more mature stage than was

necessary to identify qualitative genes for HR, and the workload per

selection cycle increased correspondingly.

Nonhypersensitive Resistance in Other Pathosystems

Hypersensitivity is not known or recognized in some other patho-

systems involving xanthomonad bacteria, for example common blight of

bean and bacterial blight of rice. Pathogenic races sensu Cook and

Stall (1969) are not known in these cases. Instead isolates may be







16

clustered into groups by their degree of virulence on standard sets of

cultivars (Mew et al., 1982; Schuster and Coyne, 1971, 1975). The

degree of resistance varies with the bacterial isolates, test environ-

ment, stage of plant growth, and the plant tissue (Coyne et al., 1973;

Coyne and Schuster, 1974a, 1974b; Valladares-Sanchez et al., 1979; Sidhu

and Khush, 1978; Yoshimura et al., 1984).

Inheritance of these resistances may be additive, dominant, or

recessive. Dominance often is incomplete. Resistance is quantitative

in all cases. Relatively discreet classes of resistant and susceptible

plants in segregating populations were observed with some systems (Yosh-

imura et al., 1983, 1984), but not others (Coyne and Schuster, 1979;

Coyne et al., 1973). More accurate classification of single plants

occurred where at least one important component of resistance was reli-

ably measured. For example, the bacterial blight pathogen was applied

directly to exposed rice leaf tissue by damaging leaves. Lesion length

developed in a given time from these inoculation sites accurately re-

flected resistance (Yoshimura et al., 1984). Diffuse chlorosis in other

pathosystems may preclude accurate measurements of disease development

(Coyne and Schuster, 1974b). In that event, quantitative resistance was

better assessed in terms of quantitative genetics (Valladares-Sanchez,

1979). Additive gene dosage effects appear to be important in these

examples of nonhypersensitive resistances (Valladares-Sanchez, 1979).

Heterozygotes but not necessarily homozygotes may interact strongly with

many environmental factors (Sidhu and Khush, 1978; Mew et al., 1982).

This strongly implies an effect of gene dosage on degree of resistance.

There are several similarities between nonhypersensitive resistance

in pepper to Xcv and other pathosystems. Nonhypersensitive resistance








17

may be durable, but the degree of resistance may vary between host lines

(Mew et al., 1982; Schuster and Coyne, 1975; Sowell, 1960; Sowell and

Dempsey, 1977). Bacterial isolates also may vary in their degree of

virulence (Cook, 1973; Mew et al., 1982). Nonhypersensitive resistance

to a broad range of bacterial isolates may be controlled by one or a few

genetic loci in the host (Brinkerhoff et al., 1984; Cook and Stall,

1969; Patel, 1982; Sowell and Dempsey, 1977; Stall, 1981; Yoshimura et

al., 1984). More than one locus may exist in any one host (Adamson and

Sowell, 1983; Patel, 1982; Yoshimura et al., 1984). The degree of

resistance controlled by these loci in heterozygotes may vary with the

test conditions (Adamson and Sowell, 1983; Hibberd and Gillespie, 1982a;

Sidhu and Kush, 1978; Valladarez-Sanchez et al., 1979; Yoshimura et al.,

1984) so that inbred progenies may be necessary to identify resistant

homozygotes (Adamson and Sowell, 1983; Brinkerhoff et al., 1984; Patel,

1982; Stall, 1981). Accurate quantification of resistance requires

measuring its components (Mew et al., 1982; Stall, 1981; Yoshimura et

al., 1984), and few nonhypersensitive resistances have been well

characterized.

Nonhypersensitive resistances have found greatest use in supple-

menting race specific genes for HR (Fallik et al., 1984; Innes et al.,

1984; Lawson and Summers, 1984; Patel, 1982; Walker and Patel, 1964).

It is probable that genes for nonhypersensitive resistance are funda-

mentally of greater importance than genes for race-specific HR, and that

the latter should be used to supplement the former. Finally, the dis-

tinguishing difference in physiology of HR in its various forms and non-

hypersensitive resistance has never been established.









Summary

The following conclusions may be drawn. Breeding for resistance

to bacterial leaf spot in pepper is necessary. Genes for HR, found

infrequently in Capsicum, are qualitative in their effect. They control

highly useful resistance that is easily selected in breeding progenies.

The genetic relation between two of the three reported genes for HR in

pepper is unknown. The gene Bs, controls race-specific HR, but the

degree of racial specialization, if any, of the genes Bs2 and Bs3 is

unknown. Measurably different hypersensitive reactions may occur in

pepper. Collectively these may control durable resistance. Durable

resistance may also be controlled by simply inherited genes which do not

mediate HR. This resistance is quantitative, and its inheritance may be

basically additive. Poor understanding of the mode of inheritance of

resistance may be resolved by assessing components of resistance in

segregating progenies inoculated by infiltration of leaves with a

carefully standardized low concentration of bacteria.












CHAPTER 3
THREE INDEPENDENT GENES FOR RESISTANCE TO BACTERIAL LEAFSPOT
IN A PLANT INTRODUCTION OF PEPPER (Capsicum annuum L.)

Bacterial leaf spot, incited by Xanthomonas campestris pv.

vesicatoria (Doidge, 1920), Dye 1978 (herein designated as Xcv) is the

most destructive foliar disease of bell peppers in warm humid environ-

ments. Three strains of Xcv have been differentiated by their reaction

after inoculation of pepper and tomato (Lycopersicon esculentum Mill.)

plants. Isolates of the tomato strain are avirulent on pepper which

reacts with hypersensitivity (Cook and Stall, 1969; Cook, 1973). Iso-

lates virulent on pepper are divided into two strains, namely one to

which tomato reacts with hypersensitivity, and the pepper strain which

is virulent on both plant species (Cook and Stall, 1969; 1982). The

pepper strain occurs world wide (Cook and Stall, 1982), while that which

is avirulent on tomato has been reported from Brazil (Kimura et al., 1972).

Two races of the pepper strain were differentiated by inoculation

of pepper plants carrying the resistance gene BsI. Race 2 induces a

hypersensitive reaction (HR) in plants with BsI but race 1 does not

(Cook and Stall, 1969). The gene Bs1 was first discovered in plants of

pepper plant introduction PI 163192 (Cook and Stall, 1963). Releases of

bell pepper Florida VR-2, Florida VR-4, and Delray Bell have BsI (A.A.

Cook, 1979, and 1982, personal communications). However, these are

susceptible to race 1 so that gene Bsj alone is insufficient for disease

control (Cook and Guevara, 1984; Cook and Stall, 1982; Dahlbeck et al.,

1979).










Plants of PI 271322 were more resistant than others in tests by

Sowell and Dempsey (1977). Resistance proved durable in diverse environ-

ments (Hibberd et al., 1979; Kim and Hartmann, 1985; Stall, 1981). Two

inherited resistances to race 1 were identified in PI 271322. The line

was heterogeneous for gene Bs which controlled hypersensitivity

(Kim and Hartmann, 1985). Stall (1981) reported recessively inherited

resistance controlled by one or two genes. This resistance was atypi-

cally hypersensitive and occurred in plants of PI 271322 lacking Bs3.

The difference between these resistances was observed only when

leaves were infiltrated with appropriate concentrations of bacteria (Kim

and Hartmann, 1985; Klement et al., 1964; Stall, 1981). Confluent

necrosis controlled by Bs3 occurs within 24 h with inoculum density of

108 cfu (colony forming units) ml-1. Necrosis occurs after 2 to 3 days

in resistant plants which lack Bs3 (Cook and Stall, 1969; Kim and Hart-

mann, 1985). Recessively inherited resistance in segregating progenies

derived from PI 271322 was assessed as fewer discreet lesions per unit

area of leaf 2 to 3 weeks after inoculating with low concentrations of

approximately 2.5 x 103 cfu ml-1 (Stall, 1981). Lesions also were

smaller in resistant than in susceptible plants. Occasional flecks of

small size may develop in plants with genes for HR when challenged with

low inoculum concentration (Essenberg et al., 1979; Klement et al.,

1964; Turner and Novacky, 1974).

Race 2 of the pepper strain of Xcv is the more common race in

Florida and occurs with race 1 (Cook and Stall, 1982). Sowell and







21

Dempsey (1977) originally reported resistance to race 2 in PI 271322. I

observed HR to race 2 in PI 271322 in addition to previously described

responses, and postulated that three resistances were functional within

the line, and all contribute to durable resistance. This chapter pre-

sents evidence for independent inheritance of three resistance mechan-

isms in PI 271322, and genetic evidence for a new race 3 of the pepper

strain of Xcv.

Materials and Methods

Inoculum Preparation

The Xcv isolates used in these studies were stored frozen in 15%

glycerol or in refrigerated, sterilized water. Inocula were prepared

from agitated (24 h) nutrient broth cultures. After centrifugation,

bacterial pellets were resuspended in sterile tap water, and standard-

ized colorimetrically to 50% light transmittance to approximate a dens-

ity of 5 x 108 cfu ml-1. These suspensions were either used

directly for observing HR, or, for other experiments, were serially

diluted to final concentrations of 1 x 103 to 3 x 103 cfu m1-1, con-

firmed by replicated colony counts from 0.05 ml subsamples spread on

nutrient agar plates. Inoculation with each race was by hypodermic

infiltration of intercostal leaf tissues. Confirmation of race was by

reaction of pepper lines near isogenic for Bsi after infiltrating them

with 5 x 108 cfu ml-1 inocula (Cook and Stall, 1969).

Heterogeneity of Resistance in PI 271322

An estimate of the variability in resistance of PI 271322 to two

races of Xcv was obtained from a small population. Plants of this line,

the susceptible control Early Calwonder (ECW), and its near isogenic







22

line 10 R with Bs1 gene (Dahlbeck et al., 1979), were raised in steamed

peat-vermiculite mix in 10-cm plastic pots arranged in a greenhouse

(temperature range 20 to 35 C). Rows of 8 plants were randomized.

Plants were watered as required and treated four times during the

experiment with approximately 0.4 g per pot of soluble 20:20:20

fertilizer.

Four fully expanded leaves per plant of PI 271322 and ECW were

each inoculated with approximately 2.5 x 103 cfu ml-1 of each of four

isolates Xv 0623, Xv 77-3A, and Xv 82-8 (all race 1), and Xv 82-7 (race

2). Each leaf was inoculated with all four isolates. A spot about 2 cm

diameter was infiltrated with inoculum.

A single leaf was sampled from each plant at 11, 14, 21 and 32

days following inoculation. The numbers of lesions per 2 cm2 of leaf

within a perimeter imprinted by a cork-borer were counted at each

inoculation site viewed under a dissecting microscope (magnified 2.5 X).

The diameters of five randomly chosen lesions at each site, or of all

lesions where fewer than five existed, were measured at day 32 using a

graduated eyepiece. In addition to this test, all plants of PI 271322,

ECW, and 10 R were observed for development of HR at 24 h after inocu-

lating two additional leaves per plant with 5 x 108 cfu ml-1 of each

isolate. A single plant, designated 271-4, was selected for hypersensi-

tivity to both races 1 and 2, as well as for a high degree of resistance

to all isolates. The progeny of this plant was used in studies of

inheritance of resistances.

Hypersensitivity to a total of 16 isolates belonging to races 1

and 2 was observed in a subsequent 166 plant population of PI 271322.







23

All plants in this test were inoculated with 5 x 108 cfu ml-1 inocula

and reactions were compared with those of inbred progeny of 271-4.

Bacterial Populations in vivo

Low disease severity in PI 271322 was expected to correlate with

lower populations of bacteria in mesophyll. Plants of 271-4, ECW, and

10 R were raised in a greenhouse as described above. Three fully

expanded leaves per plant were each inoculated with three isolates each

at approximately 1.5 x 108 cfu ml-1: Xv 80-5 (race 1), Xv E3 (race 2),

and Xv 69-1 which does not induce typical HR in 271-4. Single plants of

each host were sampled at 0, 2, 5, 8, 11, and 14 days after inoculation.

Populations of bacteria of each race were determined from replicated 1.0

cm2 (i.e., 2 x 0.5 cm2) leaf samples. Samples were triturated in 0.5 ml

sterile water, the suspensions serially diluted where appropriate, and

0.05 ml subsamples of the final dilutions spread on nutrient agar

plates. Colonies were counted after 2 to 3 days incubation at 30C, and

mean values converted to logl0 (cfu cm-2) of leaf. The numbers of

lesions per 2 cm2 of leaf and diameters of a maximum of 5 lesions per

inoculation site were obtained on additional plants 15 days after

inoculation. The experiment was repeated.

Inheritance of Resistances

A single inbred progeny plant of 271-4 was crossed with single

plants of cultivars Delray Bell (with the BsI gene) and ECW. Single F1

plants of both crosses were self-pollinated to yield F2 seed, and cross-

pollinated with additional plants of respective parents to give back-

cross progenies.







24

Several experiments were completed. The first was to test the

allelism of BsI to HR of race 2 observed in 271-4, and to verify mono-

genic inheritance of Bs3. Population sizes were 12 plants of both

parents Delray Bell and 271-4, 20 of F1, 241 of F2, 20 to 40 of the two

backcrosses, and 5 each of control lines ECW and 10 R. Plants were grown

in seedling flats in a greenhouse. The following inoculations were

applied to the eight populations. When the cotylendonary leaves were

fully expanded, one cotyledon on each plant was inoculated with isolate

Xv 82-7 of race 2. Inoculum density was 5 x 108 cfu ml-1. Hypersensi-

tivity was observed 24 h after inoculation (Cook and Stall, 1969). On

completion of that test, seedlings were transplanted to pots as de-

scribed above. Isolates Xv 82-8 of race 1 and Xv 82-7 of race 2 were

used to inoculate all seedlings at a more mature stage. A fully expand-

ed leaf was infiltrated with inoculum at 5 x 108 cfu ml-1 and observed

for hypersensitivity after 24 hours. The test was repeated on the same

plants.

A second experiment comprised a series of plantings. The experi-

mental goals were to investigate the inheritance of nonhypersensitive

resistance in 271-4, to study any possible interaction of this resist-

ance with genes for hypersensitivity to races 1 and 2, and to transfer

resistance genes to a bell pepper background. Two separate plantings of

the following seven populations were made in a greenhouse: parents

271-4 and ECW, F1, F2, backcrosses, and control line 10 R. Rows of 8

plants were randomized. Poor seed germination in the first planting

prompted the second, and population sizes varied. Only mature leaves

were inoculated. Isolates Xv 82-8 of race 1 and Xv 82-7 of race 2 were

used to observe hypersensitivity as described above. All plants in







25

both plantings were inoculated with a low concentration (approximately

1.5 x 103 cfu ml-1) of an isolate (Xv 77-3A) which does not induce

typical HR in 271-4. Three fully expanded leaves adjacent the fork on

the main stem were inoculated and harvested after 2.5 weeks. Lesions

were counted and measured as described above, and mean values were

obtained for each plant.

Genes for HR to races 1 and 2, whether in homozygous or hetero-

zygous condition, were expected to result in few, small lesions in

plants inoculated with low concentrations of bacteria (Essenberg et al.,

1979; Turner and Novacky, 1974). All plants in the second planting were

inoculated with approximately 1.5 x 103 cfu ml-1 of isolates Xv 82-8

(race 1) and Xv 82-7 (race 2). Lesions were counted and measured as

described above, and mean values from three leaves per plant were

obtained for each isolate.

Single plants of the first backcross to ECW were selected for all

three resistance reactions. These were inbred and crossed with pollen

from ECW plants. Resistant plants were selected in progenies of two

successive cycles of recurrent backcrosses and inbred backcrosses. Pop-

ulation sizes varied. The same inoculation, evaluation, and selection

procedures described above were used throughout. Cotyledon leaves also

were inoculated in one set of progenies (i.e., third backcross). The

following isolates were used in various tests: Xv 71-21, Xv 80-5, and

Xv 82-8 of race 1, Xv 81-23, Xv 82-7, and Xv E3 of race 2, and Xv 69-1

of race 3.

Hypersensitivity to races 1 and 2 was expected to be qualitative

(Cook and Stall, 1969; Kim and Hartmann, 1985). Nonhypersensitive







26

resistance is quantitative, and segregation may not result in discreet

classes of plants (Adamson and Sowell, 1983; Hibberd and Gillespie,

1982a; Stall, 1981). In that event, data were evaluated by analyses of

generation means weighted by their variances (Basford and De Lacy, 1979;

Hayman, 1958; Mather and Jinks, 1971). This analysis requires no a

priori assumption of the degree of dominance. The matrix parameter

specification of Fisher (1918) was used, where m is the theoretical pop-

ulation mean at F.; a is the value of additivity, and d is value of dom-

inance deviation. The analysis applies a X2 goodness-of-fit test to

computed parameters for a single-gene, additive-dominance model. In the

event of poor fit, the analysis fits a digenic model with interactions

(Basford and De Lacy, 1979). Specific comparisons of means were per-

formed by t-test.

Results and Discussion

Heterogeneity of Resistances in PI 271322

All inoculated plants of PI 271322 were resistant to four isolates

of Xcv comprising races 1 and 2. Only a few lesions per 2 cm2 of

leaf developed in leaves of PI 271322 infiltrated with approximately

2.5 x 103 cfu ml-1 (Table 3-1). This contrasted with relatively many

lesions in ECW. Lesion diameter 32 days after inoculation was approxi-

mately 8 times as great in ECW as in PI 271322. Variation in lesion

numbers but not in lesion diameter occurred among plants of PI 271322,

and plants were identified with very few lesions with all four isolates.

Plants of 10 R were uniformly hypersensitive within 24 h after inoculat-

ing with 5 x 108 cfu ml-1 of isolate Xv 82-7 of race 2. A susceptible

reaction occurred in leaves of 10 R inoculated with race 1, and in

leaves of ECW with both races. In these, watersoaked appearance of the









27






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28

inoculated tissue occurred in 24 to 36 h after inoculation. This was

followed by necrosis of the tissue in 2.5 to 3 days.

Heterogeneity for HR to both races 1 and 2 occurred among plants

of PI 271322. Fourteen of 15 plants showed HR to isolates Xv 0623 and

Xv 82-8 of race 1, four plants showed HR to isolate Xv 82-7 of race 2,

and no plant was hypersensitive to isolate Xv 77-3A of race 1. One

plant did not have HR to any isolate. The plants of PI 271322 and iso-

lates of Xcv which together did not produce typical HR resulted instead

in necrosis which differed also from the susceptible reaction in 10 R

and ECW. This necrosis, which occurred in 2 to 3 days after inocula-

tion, was dry and brown, and was not preceded by a watersoaked appear-

ance. It will be designated as intermediate necrosis. Several single

plants of PI 271322 were selected. One plant, designated 271-4, had HR

with isolates Xv 0623, Xv 82-8, and Xv 82-7 of races 1 and 2 and very

few lesions with isolate Xv 77-3A. Inbred progeny of 271-4 were homozy-

gous for their reactions to these same isolates.

In a larger planting of PI 271322 (Table 3-2), four isolates of

race 1, namely Xv 69-1, Xv 77-3A, Xv 81-18, and Xv 82-15 induced the

intermediate necrosis in all plants of PI 271322 and four other isolates

of race 1, namely Xv 0623, Xv 71-71, Xv 80-5, and Xv 82-8 induced

typical HR in 123 (or 74.1%) plants. All 8 isolates of race 2, Xv

61-38, Xv 65-1, Xv 70-7, Xv 80-6, Xv 82-7, Xv 83-3, and Xv E3 induced HR

in 65 (or 39.2%) plants. All other reactions occurring in PI 271322

were of the intermediate necrosis type. The frequencies of typical HR

to isolates of races 1 and 2 were independent of each other (Table 3-2).

The HR to some isolates of race 1 was taken to represent the

effect of gene 8s3 (Kim and Hartmann, 1985). The race 1 isolates which











Table 3-2.


Hypersensitivity in plants of PI 271322 to inoculation with
four isolates of race 1 and eight isolates of race 2 of
Xanthomonas campestris pv. vesicatoria.


Race 2 Race 1 hypersensitivity
hypersensitivity Present Absent Totals


Present 47 18 65 (39.2%)b

Absent 76 25 101 (60.8%)

Totals 123 (74.1%) 43 (25.9%) 166


aInoculum concentration approximately
percentage of total number of plants


5 x 108 cfu ml-1.
in parentheses.







30

did not induce typical confluent HR were classified temporarily as a new

race 3. It was clear however that plants of PI 271322 were resistant to

isolates of race 3. Plants which lacked HR to races 1 and 2 were never-

theless resistant to both of these races (Table 3-1). The HR reactions

to races 1 and 2 therefore occurred in plants which already were resist-

ant to all isolates. In fact, Stall (1981) used isolate Xv 80-5 to

evaluate nonhypersensitive resistance in PI 271322. This isolate induced

typical HR in plants with gene Bs3. The genetic relation of Bs1 (orig-

inally from PI 163192 and which controls HR to race 2) with the locus

controlling HR to race 2 in PI 271322 is unknown.

Bacterial Population in vivo.

Populations of bacteria of races 1, 2, and 3 reached approximately

5 x 106 to 108 cfu cm-2 in leaves of ECW 10 to 14 days after infiltra-

tion with low inoculum concentration (Figure 3-1). In contrast, popula-

tions in leaves of 271-4, were 104 to 105 times lower than in leaves of

ECW. Populations of isolate Xv E3 of race 2 were about 10 to 50 times

higher in leaves of 10 R than in 271-4, and 103 to 104 times lower than

in leaves of ECW. Changes in populations of races 1, 2, and 3 in leaves

of 271-4 were consistent with hypersensitivity, that is, bacterial

multiplication occurred for 2 to 3 days after which it ceased, and

populations declined slowly (Cook and Guevara, 1984; Stall and Cook,

1968; Klement et al., 1964).

Many lesions of relatively large diameter developed in leaves of

ECW inoculated with races 1, 2, and 3, and in 10 R leaves with races 1

and 3 (Table 3-3). Lesions were visible between 5 and 6 days after

inoculation, corresponding to populations of 5 x 105 to 5 x 106 cfu per






























Figure 3-1. Populations of bacteria per cm2 of leaf of
peppers Early Calwonder and 271-4 inoculated with races 1, 2, and 3,
and pepper 10 R inoculated with race 2 of Xanthomonas campestris pv.
vesicatoria. Points represent means of 6 replicates.

















---- Race 1 Isolate Xv 80-5

Race 2 Isolate Xv E3
----- Race 3 Isolate Xv 69-1

Early Calwonder
2 10 R
x 271-4


4 6 8
Days after inoculation


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34

cm2 (Figure 3-1). Only a few small lesions occurred in leaves of 271-4

with any isolate. Necrotic hypersensitive flecks developed in leaves of

10 R with isolate Xv E3 of race 2. Their higher frequency in 10 R than

in 271-4 corresponded with bacterial populations approximately 10 times

higher in 10 R (Figure 3-1).

Resistance to race 3 in 271-4 was clearly present and effective

but was difficult to distinguish from hypersensitivity following inocu-

lation with a low concentration of bacteria (Table 3-3, Figure 3-1).

Interpretation of the mechanism underlying race 3 resistance should come

from ultrastructural and physiological studies (Jones and Fett, 1985).

Inheritance of Resistance

Hypersensitivity to races 1 and 2

All plants of parents 271-4 and Delray Bell, and their F1, F2, and

backcross progenies, and line 10 R, but none of ECW, were hypersensitive

to isolate Xv 82-7 of race 2 (Table 3-4). This result occurred at two

stages of plant maturity, namely in cotyledons of young seedlings and in

fully expanded leaves of mature seedlings. This is consistent with the

hypothesis that gene Bs1 is present in homozygous condition in both par-

ents 271-4 and Delray Bell.

All plants of 271-4, the F1, and backcross (F1 x 271-4) popula-

tions, but no plants of Delray Bell, 10 R, and ECW were hypersensitive to

isolate Xv 82-8 of race 1 (Table 3-4). Segregation occurred in the F2

and backcross (F1 x Delray Bell) populations. Segregation was consist-

ent with a ratio in the F2 of 3:1 (X2 = 1.33, P = 0.30 to 0.20), and a

ratio in the backcross of 1:1 (X2 = 0.71, P = 0.50 to 0.30). These

ratios were expected if a single, homozygous gene, Bs3, is in 271-4 (Kim

and Hartmann, 1985).











Table 3-4.


Segregation for hypersensitivity in progenies of peppers
271-4 and Delray Bell inoculated with races 1 and 2 of
Xanthomonas campestris pv. vesicatoria.


Numbers of plants

Race 1 isolate Xv 82-8 Race 2 isolate Xv 82-7

Generation HRb non-HR HR non-HR


271-4 12 0 12 0

Delray Bell 0 12 12 0

F1 (271-4 x
Delray Bell) 20 0 20 0

F2 173 68 241 0

F1 x 271-4 18 0 18 0

F1 x Delray Bell 15 20 35 0

Controls

Early Calwonder 0 5 0 5

10 R 0 5 5 0


aInoculum concentration approximately 5
bHR = hypersensitive reaction.


x 108 cfu m-1.







36

Independent segregation of BsI and Bs3 occurred in progenies of 271-4

and ECW (Table 3-5). The F1 progeny was hypersensitive to both races

1 and 2. Four combinations of HR to races 1 and 2 occurred in the F2

populations (Table 3-5). In one planting, segregation was consistent

with a ratio of 9 plants with HR to races 1 and 2:3 plants HR to race 1

only:3 plants HR to race 2 only:l plant lacking HR. Segregation margin-

ally failed to fit this ratio in the second planting (P = 0.05 to 0.02)

(Table 3-5). Failure to fit resulted from unexpectedly few plants

hypersensitive to isolate Xv 82-7 of race 2. Independent segregation of

Bsl and Bs was supported by data from backcross progenies in both
plantings. All plants of the backcross (F1 x 271-4) were hypersensi-

tive to both races 1 and 2. Segregation in the backcross (F1 x ECW) was

consistent (P = 0.5 to 0.1) with the occurrence of equal frequencies of

plants with each of the four possible combinations of hypersensitivity

to races 1 and 2.

Single plants with both BsI and Bs3 were selected from the back-

cross (F1 x ECW). These were both self-pollinated and backcrossed to

ECW. Selection for Bs1 and Bs3 was subsequently made in progenies of

two successive recurrent backcrosses to ECW (Tables 3-6 and 3-7).

Observed segregation ratios adequately fitted those expected for

independent assortment of both genes in all populations except one

(Table 3-7). Significantly fewer plants hypersensitive to isolate Xv

81-23 of race 2 occurred in that population than expected. Similar

deviations from expectation did not occur in any population inoculated

with isolates of race 1. The results of inoculating leaves at two

stages of plant maturity, namely recently fully expanded cotyledons and

leaves of mature plants, agreed to within 98.5% (Table 3-7).


















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41

The genes Bs1 and Bs3 are inherited independently. Their pheno-

types are dominant and observable in plants at two maturity stages. Use

of cotyledon leaves to select BsI and Bs should contribute to effi-

cient use of labor and time in backcross breeding. The low frequency of

error in the cotyledon test with heterozygotes (Table 3-7) is not

sufficient deterrent to its use. Selected plants may be reinoculated at

a more mature stage.

Significantly fewer F2 plants of the cross between 271-4 and ECW

were hypersensitive to isolate Xv 82-7 of race 2 in one of two plantings

(Table 3-5). In contrast, an excellent fit occurred in both plantings

with isolate Xv 82-8 of race 1. It was possible that mutation of iso-

late Xv 82-7 occurred during inoculum preparation (Dahlbeck and Stall,

1979), and that plants in one test were consequently inoculated with a

mixture of races. Two colony types in about equal frequency occurred

in subsamples of inoculum which were cultured on nutrient agar plates.

They proved to be races 2 and 3 by inoculating peppers 271-4, 10 R, and

ECW (Chapter 4, this dissertation). Hypersensitivity to race 2 con-

trolled by BsI predominates in plants inoculated with a mixture of

races 1 and 2 (Stall et al., 1974). However, it is likely that HR

developed slowly in this test in some plants with Bs1, and these were

classified as nonhypersensitive (Table 3-5).

Inocula of isolate Xv 82-8 of race 1 and impure Xv 82-7, both at

low concentration, were used to inoculate mature leaves of all plants.

Low disease severity was expected in plants with BsI and Bs3 compared

with those lacking these genes. Only a few lesions of small diameter

occurred with isolate Xv 82-8 of race 1 in all plants of 271-4 and in

its progeny which had Bs3 (Tables 3-8 and 3-9). In contrast, many





























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lesions of large diameter occurred in ECW and backcross (F1 x ECW)

plants lacking Bs3.

Few lesions of small diameter with impure isolate Xv 82-7 of race

2 occurred in plants of 271-4, F1 and backcross (F1 x 271-4) progenies

(Tables 3-8 and 3-9). In contrast, relatively many lesions of large

diameter occurred in plants of ECW and in backcross (F1 x ECW) plants

lacking Bs1. Significantly fewer lesions of smaller diameter (P<0.05)

occurred in F2 and backcross (F1 x ECW) plants with BsI than in sister

plants lacking Bsl, but much overlap occurred between groups for both

attributes. In addition, F2 and backcross (F1 x ECW) plants with Bs1

had significantly more and larger lesions (P<0.05) than plants of the

parent 271-4, F1, and backcross (F1 x 271-4) populations. The F2 and

backcross (F1 x ECW) plants with BsI appeared relatively far more

diseased with impure isolate Xv 82-7 of race 2 than did sister plants

with Bs_ inoculated with pure isolate Xv 82-8 of race 1.

Both BsI and Bs3 controlled dominant phenotypes with two widely

different concentrations of inoculum. Mutation of race 2 to race 3

however confounded the degree of dominance with Bsi, and race 3 resist-

ance varied independently of Bs1.

In a further test of the penetrance of Bsi and B_3, control lines

and second backcross breeding progenies heterozygous for BsI and Bs3

were inoculated with low concentrations of isolates Xv 80-5 of race 1

and Xv E3 of race 2. Many lesions of relatively large diameter

developed in leaves of ECW with both isolates, and in leaves of 10 R

with isolate Xv 80-5 of race 1 (Table 3-10). In contrast, only a few

lesions of small diameter developed in leaves of 10 R with isolate Xv

E3, and with both isolates in 271-4 and hypersensitive backcross




















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progenies. Significantly more lesions of both isolates occurred in

backcross progenies heterozygous for Bsl and Bs than in 271-4, but

lesion diameters were equally small. The dominance of Bsj and Bs3 was

therefore slightly incomplete with low concentration inoculum.

Nonhypersensitive resistance to race 3

Plants of 271-4 were resistant to isolates of race 3 (Tables 3-1

and 3-2, Figure 3-1). Their reaction to inoculum containing 108 to

5 x 108 cfu ml-1 was distinguishable from the susceptible reaction by

careful scrutiny, but the difference was not instantly recognizable

(Cook and Stall, 1969). Segregates in F2 progenies that were resistant

to race 3 were not recognized with certainty, however, in preliminary

tests with this inoculum density. It was necessary to quantify resist-

ance in terms of two of its components, namely, number of lesions per 2

cm2 of leaf (Stall, 1981) and diameter per lesion, following inocula-

tion with low inoculum density. These components together reflected

resistance to race 3 better than either alone (Figure 3-1, Table 3-3,

and Chapter 8 of this dissertation).

The same experimental populations discussed above were inoculated

with isolates of race 3 at low inoculum density. Large differences in

means of both components occurred among the populations of parents 271-4

and ECW, F1, F2, backcrosses, and control line 10 R in two plantings

inoculated with isolate XV 77-3A of race 3 (Table 3-11). Few lesions of

small diameter occurred in plants of 271-4, F1, and backcross

(F1 x 271-4) populations, and all plants appeared resistant (Tables 3-12,
and 3-13). Relatively many lesions of large diameter occurred in plants

of ECW and 10 R, but variation in lesion number in ECW was unexpectedly

great in the second planting (Tables 3-11, 3-12 and 3-13). Wide varia-
tion in both components occurred among F2 and backcross (F1 x ECW) plants











Table 3-11.


Lesions per 2 cm2 of leaf and diameter per lesion in
parents 271-4 and Early Calwonder, F1, F2, and back-
crosses and control line 10 R in two plantings
inoculated with race 3 of Xanthomonas campestris pv.
vesicatoria.


Number Lesionsa Diameter
of per per lesion
Generation plants 2 cm2 (mm x 10)


271-4 50b 0.5 0.17c 1.3 0.14
44 0.8 0.20 1.2 0.08

ECWd 42 14.3 0.48 7.1 0.55
42 19.0 0.92 4.8 0.16

F1 (271-4 x ECW) 51 2.2 0.47 1.7 0.14
36 0.5 0.11 1.3 0.07

F2 116 5.8 0.54 2.2 0.16
236 4.6 0.33 2.3 0.07

F1 x 271-4 60 1.8 0.33 1.3 0.07
77 1.0 + 0.22 1.3 0.05

F1 x ECW 22 12.0 1.56 4.0 0.60
94 12.4 0.85 3.3 0.12

10 R 14 18.5 0.75 5.3 0.70
8 15.1 1.59 4.7 0.65

alsolate Xv 77-3A of race with inoculum concentration in first plant-
ings of 1.1 x 10J cfu ml and 1.5 x 10 cfu ml- in second planting.
bUpper value from first planting, lower value from second.
CMean standard error of mean.
dECW = Early Calwonder.

















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50

in both plantings. Distinct, nonoverlapping classes of resistant and

susceptible plants did not occur, and the F2 distribution was strongly

skewed toward resistance in both plantings (Tables 3-12, and 3-13).

However, distribution of lesion numbers in the backcross (F1 x ECW)

populations suggested two classes of plants, one resistant or partly so,

and one susceptible (Table 3-12). The pattern of variation among gener-

ations strongly implied simple genetic control with a high degree of

dominance for low values of components of resistance.

Analysis of generation means weighted by their error variances

were computed for both components. Data were first transformed by

square root of (x + 0.5) to account for the large number of zero values

in some populations. Single gene models marginally failed to fit the

transformed means of both components from the first planting (Table

3-14). However, digenic models with additive epistasis fitted adequately

Epistasis was negative for log lesion numbers and positive for log

lesion diameter. Digenic models were necessary to fit data from the

second planting. Estimated parameters however still reflected a high

component of dominance for low numbers of lesions, and additivity for

lesion diameter (Table 3-15). Unexpectedly wide variation in both

attributes occurred in nonsegregating generations (Tables 3-12 and

3-13). This probably contributed to failure of data to fit single gene

models.

A combination of additive and incompletely dominant gene action

for components of resistance basically explained continuous variation in

these populations. Dominance was incomplete for low lesion numbers.

Stall (1981), however, reported dominance for high lesion numbers in

related progenies. Additional data to resolve this contrast were























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collected from second backcross progenies inoculated with isolate Xv

69-1 of race 3. Parental selections crossed with ECW to produce these

populations were highly resistant to isolate Xv 77-3A of race 3, and

possessed BsI and Bs3.

No lesions developed in plants of 271-4 in 2 weeks after inocula-

tion. In contrast, many lesions of relatively large diameter developed

in leaves of ECW and 10 R (Table 3-16). Mean values of both components

in backcross progenies were lower than in control lines ECW and 10 R but

wide variation occurred (Table 3-17). Mean values from the inbred back-

cross population were significantly lower than from the noninbred back-

crosses and susceptible control lines (P<0.05), and wide variation also

occurred (Tables 3-16 and 3-17). The numbers of lesions per 2 cm2 of

leaf separated basically into groups in both the noninbred and inbred

backcross progenies (Table 3-17). Three groups of plants were evident

in the inbred backcross. These were resistant plants with very few

lesions, an intermediate group, and a susceptible group with many

lesions. The group of highly resistant plants did not occur in nonin-

bred backcross progenies. The number of lesions per 2 cm2 and diameter

per lesion were positively correlated (r = 0.65, P<0.05). These data

are consistent with a single additive gene for resistance being ex-

pressed in this experiment. Additivity is reflected in intermediate

disease severity in heterozygotes (Tables 3-16 and 3-17).

Both resistance and susceptibility to race 3 isolates occurred

among plants with genes Bsi and Bs3 (Table 3-16) or with any other

combination of these genes (Tables 3-5, 3-12, and 3-13). Progenies with

any combination of resistances could be recovered. Resistance to races

1, 2, and 3 are independent of each other.









Table 3-16.


Number of lesions per 2 cm2 of leaf and diameter per
lesion in control lines and progenies of the second back-
cross to Early Calwonder inoculated with race 3 of
Xanthomonas campestris pv. vesicatoria. All backcross
progeny plants were of genotype Bs. Bs3.


Number Lesionsa Diameter
of per per lesion
Generation plants 2 cm2 (mm x 10)

Controls
271-4 7 0

ECWC 8 18.6 3.15b 5.4 0.64

10 R 3 20.3 1.43 5.4 1.00

Backcrosses
(BC 11-2)u x ECW 40 13.5 1.24 4.1 0.28

(BC 31-1) x ECW 35 12.9 1.22 3.8 0.32

(BC 31-4) x ECW 13 12.2 1.33 4.9 0.58

(BC 31-4) selfed 60 7.5 0.88 2.6 0.17

aIsolate Xv 69-1 of race 3 used with inoculum concentration 1.3 x 103
cfu ml-1.
bMean standard error of mean.
cECW = Early Calwonder.
dFemale parents refer to single plant selections from first backcross.














4-1
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-o o







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4- Ci
* m







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56

To illustrate additive and dominant gene action with race 3, data

from two different experiments are plotted and compared with data from

Stall (1981) in Figures 3-2 and 3-3. The theoretical frequency of an

allele in F1 and F2 progenies is 0.5, and is 0.25 and 0.75 in respective

backcross populations. Generation means of both components of resist-

ance from 6 populations are plotted against these frequencies for iso-

late Xv 77-3A in Figure 3-2, and for four populations with isolate Xv

69-1 in Figure 3-3. In addition, the generation means of lesion numbers

observed by Stall (1981) are plotted in Figure 3-3. Resistance to iso-

late Xv 77-3A was incompletely dominant, and generation means of both

components were not strictly related linearly to the frequency of the

allele from ECW (Figure 3-2, Tables 3-14 and 3-15). However, means with

isolate Xv 69-1 were linearly related to allele frequency (Figure 3-3,

Tables 3-16 and 3-17). In contrast, dominance occurred for high lesion

numbers in data from Stall (1981), and generation means increased non-

linearly with frequency of the allele for susceptibility (Figure 3-3).

The three sets of experiments are not strictly comparable since

different plants, growing conditions, and bacterial isolates were used.

However, a general pattern emerged to explain inheritance of resistance

to race 3. Dominance reversal of lesion numbers with nontypically

hypersensitive resistance can be explained as a reduced rate of bacter-

ial multiplication. The potential number of lesions is controlled by

inoculum concentration (Essenberg et al., 1979; Stall et al., 1982;

Turner and Novacky, 1974). Bacteria multiply in situ to populations

controlled, in part, by the resistance mechanism functioning in the host

(Chapter 4, this dissertation). A small increase in bacterial popula-

tions may be associated with a large increase in the number of lesions




























Figure 3-2. Generation means of lesions per 2 cm2 of leaf
and diameter per lesion related to theoretical frequency of the
allele for susceptibility in parents, F1, F2 and backcross pepper
populations inoculated with race 3 of Xanthomonas campestris pv.
vesicatoria. Data are from the first of two plantings.















*-21
7 x Lesions per 2 cm2 of leaf /
Diameter per lesion ,/

6- Dotted lines linking parental means / -18
are theoretical for additivity
with no dominance or epistasis. /

/ / -
5- / x-15


a



O / /- C
x x




34 / x, -20
0 / -
S13 9 0 -



2 / -6 0
E


4- x
o ,o

0 0.25 0.50 0.75 1.00
Theoretical frequency of allele for susceptibility





























Figure 3-3. Generation means of lesions per 2 cm2 of leaf
and diameter per lesion related to theoretical frequency of the
allele for susceptibility in parents and second backcross breeding
progenies inoculated with race 3 of Xanthomonas campestris pv.
vesicatoria. Data of lesion numbers from Stall (1981) included for
comparison.






60


25.0

-A 22.5



S- 20.0


/ 17.5

/
/ /5.o-


/ X

5- / -12.5oM
"- / a-
0.
E /
E4
E 4/- 10.0 C0

0. 0
o / _i
3 / X 7
o3- x -7.5

0. /
.62- -5.0
/ x Lesions per 2 cm2 50
a Diameter per lesion with
S / isolate Xv 69-1
1 A Lesions per 2 cm2 from -2.5
Stall (1981)

0 x 1 \ 0
0 0.25 0.50 0.75 1.00
Theoretical frequency of allele for susceptibility








61

that become visible (Chapter 8, this dissertation). Lesion expansion

will continue whether few or all the potential lesions have become vis-

ible. The rate of lesion expansion will vary with the degree of resist-

ance and aggressiveness of the isolate. Lesion diameter should approxi-

mate the mid-parent value characteristic of each isolate (see also Chap-

ters 6 and 7 of this dissertation). It is clear that heterozygotes were

identified in two successive recurrent backcrosses. These plants were

identified by their components of resistance which reflect bacterial

populations in host mesophyll (Figure 3-1, Table 3-3).

Reports of reversal of dominance and recessively inherited resist-

ance to bacterial pathogens are common in the literature. For example

Brinkerhoff et al. (1984), Chand and Walker (1964a and b), Fallik et al.

(1984), Hibberd and Gillespie (1982a), Innes et al. (1982), Kim (1983),

Patel (1982), Patel and Walker (1966), Sidhu and Khush (1978), Taylor et

al. (1978), Valladares-Sanchez (1979), and Yoshimura (1984) have re-

ported them. It is possible that underlying additivity may be occurring

with many quantitatively-assessed resistance genes.

The PI 271322 is unique among investigated peppers in having three

independent resistance mechanisms. All plants were resistant to all

tested isolates of Xcv, but the line was heterogeneous for race-specific

genes BsI and Bs3. In fact, both Bs and Bs3 were unnecessary for

resistance to Xcv in PI 271322 and its progeny from crosses with bell

pepper (Chapter 8, this dissertation; and R.E. Stall, 1982, personal

communication). Resistance to race 3 therefore appeared to be general-

ized against all races. Nevertheless, all three genes contributed to

make PI 271322 the most resistant observed by Sowell and Dempsey (1977).








62

These are useful either singly (Dahlbeck et al., 1979; Kim and Hartmann,

1985; Stall, 1981) or collectively. It should be noted, however, that

plants with Bs1 and Bs3 may be highly susceptible to bacterial spot

unless selected for resistance to race 3 (Table 3-17).

Efficient selection of resistance genes in segregating populations

is vitally important in plant breeding. Genes Bsl and Bs3 may be ident-

ified by infiltrating cotyledons with high concentration inocula. Sin-

gle plants with resistance to race 3 were efficiently identified by

inoculating fully expanded leaves with low concentration inoculum

(Stall, 1981). The dominance reversal of race 3 resistance is of con-

cern, and three approaches to selection are possible. Commonly, inbred

backcross progenies are inoculated (Brinkerhoff et al., 1984; Hibberd

and Gillespie, 1982; Innes et al., 1984; Patel, 1982; Stall, 1981), but

two generations per cycle are required. Single generation cycles may be

accomplished by progeny testing presumed heterozygotes (Hanson, 1959).

Alternatively, heterozygotes may be identified by inoculating with a

relatively weak growing isolate.

Clearly, dominant hypersensitivity is easier to select than nonhy-

persensitive resistance. Cook reported a single gene, Bs2, for hyper-

sensitivity to race 1 of Xcv in a PI of C. chacoense L. (Cook and

Guevara, 1982; 1984). The genetic relation between Bs2 and Bs3 and the

reaction of race 3 on plants with BS2 are the subject of a subsequent

investigation (Chapter 5, this dissertation).

The designation Bs4 is proposed for the additively inherited,

nonhypersensitive gene for resistance to race 3 of Xcv.













CHAPTER 4
DIFFERENTIATION OF PATHOTYPES OF Xanthomonas campestris pv.
vesicatoria PATHOGENIC ON PEPPER (Capsicum annuum L.)

Pathogenicity on its host is the single most important charact-

eristic of a pathogen. Races occur as variants which are virulent on

plants with resistance genes. Two races of Xanthomonas campestris pv.

vesicatoria (Doidge, 1920) Dye, 1978 (referred to here as Xcv) were

recognized as pathogenic on pepper (Capsicum annuum L.) (Cook and Stall,

1969, 1982). Race 2 induced a typical rapid hypersensitive reaction

(HR) in plants with gene Bsj (Cook and Stall, 1963; Stall and Cook,

1966), and race 1 did not. The gene Bjs was found first in plant

introduction (PI) 163192 (Cook and Stall, 1963) and was recently

confirmed to be also in PI lines 163189 and 271322 (this dissertation,

Chapters 3 and 6).

Recently, Kim and Hartmann (1985) reported that PI 271322 has an

independent gene, Bs3, for HR to isolates of race 1. However, I ob-

served variants of race 1 which did not induce typical HR in plants of

PI 271322 with Bs3 and presented genetic evidence for race 3 (this dis-

sertation, Chapter 3). The PI 271322 was also resistant to race 3 but

in an atypical hypersensitive way, and this resistance was inherited as

a single additive gene Bsa in crosses with susceptible bell pepper. The

three resistance genes in PI 271322 segregated independently (Stall,

1981; this dissertation, Chapter 3), and the line was resistant to Xcv

irrespective of the presence or absence of Bsi and Bs3.







64

The HR induced by race 2 in plants with Bs1 was characterized by

drastic host cell membrane disorganization and collapse within 24 h

after inoculation (Stall and Cook, 1966). This change was reflected in

rapidly increasing loss of electrolytes from the mesophyll inoculated

with 108 cfu (colony forming units) ml-1 (Cook and Stall, 1968). Bac-

terial populations ceased to grow with these changes and sometimes

progressively declined. Previously (Kim and Hartmann, 1985), no

physiological evidence was presented to confirm the HR to race 1 in PI

271322, nor to distinguish between races 1 and 3 (this dissertation,

Chapter 3). Changes in bacterial populations in vivo presented earlier

(this dissertation, Chapter 3) were consistent with hypersensitivity to

all races 1, 2, and 3.

The time from inoculation to observable hypersensitivity to fungal

pathogens varies with the host gene for HR in several pathosystems (Day,

1974; Ellingboe, 1982; Keen, 1982). Evidence is accumulating for simi-

lar variations in time to cell collapse with HR to bacterial plant path-

ogens. Patel (1982) described two race-specific genes for HR with bac-

terial pustule in cowpea. The cell collapse with one race occurred

later than cell collapse with the other race in the one plant with both

resistances. Both Patel (1982) and Gitaitis (1983) described a third

resistance to the same pathogen of cowpea. This response was character-

istically more slowly developing than usually expected for HR, but was

associated with low bacterial populations in vivo. Ersek and Hevesi

(1983) and Long et al. (1985) noted slow developing hypersensitivity in

soybean to bacterial blight. Cook (1973) characterized the slow devel-

oping HR in pepper to isolates of Xcv which are pathogenic only on






65

tomato. Electrolyte loss from inoculated leaf tissues was slower than

with HR in the interaction between BS1 and race 2, and populations of

bacteria were correspondingly higher.

A definite sequence of events occurs in inoculated pepper plants

with all three resistance genes (Bs1, Bs3 and Bs4) derived from PI

271322. Hypersensitivity occurs most rapidly with race 2 in 9 to 18 h,

followed by HR with race 1 in 20 to 24 h, and lastly, atypical hyper-

sensitive necrosis with race 3 in about 2 days after inoculating with

108 cfu ml-1. In addition, HR in heterozygotes for Bs and Bs3

was delayed for 2 to several hours in comparison with homozygotes,

although both genes control dominant phenotypes (Cook and Stall, 1963;

Kim and Hartmann, 1985). Small necrotic lesions develop occasionally in

hypersensitively resistant cotton (Essenberg et al., 1979), and pepper

plants (this dissertation, Chapter 3) when challenged with low inoculum

concentrations. Pepper plants heterozygous for Bs1 and Bs3 often

developed more numerous but equally small lesions compared with homozy-

gotes. This chapter presents evidence for races 1, 2, and 3 of Xcv, for

differences in time to host reaction with the three resistance genes,

and for incomplete dominance of genes Bsl and Bs3 in pepper.

Materials and Methods

Inocula were prepared from agitated, late log phase, nutrient

broth cultures. After centrifugation, pellets were resuspended in

sterile tap water and standardized colorimetrically to 50% light

transmittance to approximate a density of 5 x 108 cfu ml-1. These

suspensions were used either directly for observing HR and measuring

electrolyte loss, or were serially diluted to 5 x 103 cfu ml-1 for

determination of bacterial populations in vivo. Inoculation with







66

each race was by hypodermic infiltration of intercostal leaf tissues on

each of three fully expanded leaves per plant. The following isolates

were used as representative of Xcv: Xv 71-21 and Xv 80-5 of race 1,

Xv E3 of race 2, and Xv 69-1 of race 3. They had been maintained frozen

in 15% glycerol or on sealed nutrient agar plates at 3 to 4 C.

The single plant selection from PI 271322, designated 271-4, was

used. Inbred progeny of 271-4 were homozygous for genes Bs1, Bs3, and

Bs1 (this dissertation, Chapter 3). The susceptible cultivar Early

Calwonder (ECW), and its near isogenic line 10 R with the Bs1 gene

(Dahlbeck et al., 1979) were also used. Single plants of 271-4 and ECW

were raised, self-pollinated, and reciprocally cross-pollinated. Plants

of 10 R, and inbred and hybrid progeny of ECW and 271-4 were raised in a

greenhouse (temperature range 18 to 35 C) in steamed peat-vermiculite

mix in 10-cm plastic pots, and fertilized four times during the experi-

ments with 0.4 g per pot of soluble 20:20:20 fertilizer.

Two repeated experiments were completed. The first was to deter-

mine differences in rates of electrolyte loss from leaves of peppers

271-4, ECW, and 10 R inoculated with representative cultures of races 1,

2, and 3. After inoculation, plants were maintained in constant

temperature chambers at 25 0.25 and 30 0.25 C and illuminated for

18 h per day by fluorescent and incandescent lamps. The second

experiment was to determine the degree of dominance of the three

resistance genes in 271-4 and its hybrids with ECW by 3 methods. These

methods were time after inoculation to visible plant reactions at 25 C,

loss of electrolytes from inoculated leaf tissue of plants at 25 C, and

bacterial populations in vivo in the same plants reinoculated after

returning them to the greenhouse.







67

Electrolyte losses were determined with samples of 3.0 cm2 of

leaf tissue harvested at timed intervals after inoculation with 5 x 108

cfu m1-1. Samples were suspended in 3.0 ml deionized water and conduct-

ivity in Umho of the suspending solution was recorded immediately.

Conductivity was recorded again after vacuum infiltration at 63 cm Hg

for 60 second and followed by agitation for 1 h at 30 C. The difference

in conductivity between the two readings was taken to represent the

influence of bacteria on host tissue (Cook and Stall, 1968). There were

three replicates and the experiment was repeated.

Bacterial populations in vivo were determined from 1.0 cm2 (i.e.,

2 x 0.5 cm2) samples of inoculated leaf tissue harvested at timed

intervals after inoculation with 5 x 108 cfu ml-1. Samples were

triturated in 0.5 ml sterile tap water, the suspensions serially diluted

where appropriate, and 0.05 ml of the final dilutions spread on nutrient

agar plates. The resulting colonies were counted 2 to 3 days after

incubation at 30 C, and numbers converted to log10 (cfu cm-2) of leaf.

Means of three replicates were recorded, and the experiment was

repeated.

Results and Discussion

Electrical conductivity of the solutions containing discs from

inoculated leaves increased slowly with all isolates in ECW, and with

isolates Xv 80-5 (race 1) and Xv 69-1 (race 3) in 10 R (Tables 4-1 and

4-2; Figures 4-1 and 4-2). Greater increases occurred at 30 than 25 C.

Averages of the means from two temperatures are shown in Figures 4-1 and

4-2. Visible watersoaking occurred at about 30 h accompanied by large

increases in conductivity between 36 and 48 h.










Table 4-1.


Conductivity as a measure of electrolyte loss at two temperatures
from pepper leaf tissue inoculated with races 1, 2, and 3 of
Xanthomonas campestris pv. vesicatoria.


Electrical conductivity (pmho)a

Hours after infiltration
Host Xcv
variety isolate 1 6 12 24 30 36 48

Early Calwonder Xv 80-5 28c 43 48 110 149 150 351d
race 1 39 26 47 63 91 123 198

Xv E3 27 40 42 114 155 135 255d
race 2 30 20 37 67 86 89 189

Xv 69-1 30 42 48 112 145 129 261d
race 3 38 21 41 67 85 107 192

10 R Xv 80-5 37 48 65 82 87 92
30 33 33 46 74 77 152d

Xv E3 34 234 251 -
34 159 298 -

Xv 69-1 27 43 41 88 120 120
41 17 38 46 85 118 176d

271-4 Xv 80- 5 65 61 84 274 338 -
72 59 81 294 348

Xv E3 68 193 263 -
72 95 346 -

Xv 69-1 66 58 77 103 121 125 225d
65 85 60 144 148 245 173


aValues are means of 6 replicates except where indicated.
bInoculum concentration 5 x 10A cfu ml"
cUpper value from 30 C treatment, lower value from 25 C.
dMeans of 3 replicates.











Table 4-2.


Conductivity as a measure of electrolyte loss from leaf tissue of
parents Early Calwonder, 271-4, and their hybrids inoculated with
races 1, 2, and 3 of Xanthomonas campestris pv. vesicatoria.


Electrical conductivity (Pmho)a

Hours after infiltration
Host Xcv
variety isolate 0 9 15 21 23 26.5 31 36

Early Calwonder Xv 71-21 19 25 47 61 87 104 144 124
race 1

Xv E3 24 34 60 85 107 127 185 190
race 2

Xv 69-1 24 30 48 64 109 108 177 184
race 3

271-4 Xv 71-21 34 60 94 164 341 -

Xv E3 39 347 -

Xv 69-1 45 60 97 94 101 107 140 165

Reciprocal Xv 71-21 26 42 76 127 194 221 -
hybrids (pooled
data) Xv E3 29 143 295 -

Xv 69-1 29 38 69 73 115 107 125 141

aValues are means of 6 replicates for Early Calwonder and 271-4, and of
12 reps (pooled data) for hybrids between them.
bInoculum concentration 5 x 10 cfu ml-
CPlants held at 25 1 C




























Figure 4-1. Conductivity as a measure of electrolyte loss
from leaf tissue of peppers inoculated with races 1, 2, and 3 of
Xanthomonas campestris pv. vesicatoria. Data were averaged for
temperature treatments of 25 and 30 C, and points represent means
of 12 replicates.




















x
I


1/
I?
I'

I/
I,
//


/I
j I
II
I

I I
I
I
;7


x


/
/
/
/
/
/
I
I
/ J


---Isolate
----Isolate
-----Isolate


* Early Calwonder
10 R
x 271-4

Xv 80-5 of race 1
Xv E3 of race 2
Xv 69-1 of race 3


16 24 32
Hours after inoculation


40 48


360


320-


280W-


2401-


0
-C
E
200 -



D 160-
-o
o
C
0

120-



80



40c


0 8



























Figure 4-2. Conductivity as a measure of electrolyte loss
from leaf tissue of peppers Early Calwonder, 271-4 and their
hybrids inoculated with races 1 and 2 of Xanthomonas campestris
pv. vesicatoria. Points represent means of 6 or 12 replicates.











360
x
I X
/
320-


oI
280

I I
240 -
I I
I I /
,1 /

. 200- I /
E I
>. I I I
4-I I
S160- I / /


S120 I
/ /

80 /
80 / Early Calwonder
I /







0 8 16 24 32 40 48
Hours after inoculation16 24 32 40 48
Hours after inoculation








74

The lines 10 R and 271-4 were hypersensitive to isolate Xv E3 of

race 2. The cell collapse appeared complete by 9 h after inoculation

and was reflected by large increases in conductivity of the solution

containing the leaf discs (Tables 4-1 and 4-2, and Figures 4-1 and 4-2).

Slightly more rapid collapse occurred at 30 than 25 C (Table 4-1).

Inoculated leaf tissue of both hybrids between 271-4 and ECW wilted

after 9 h, and cell collapse was visibly complete by 13 to 14 h after

inoculation (Tables 4-2 and 4-3, Figure 4-2). No difference occurred

between the two hybrids and data from them were pooled.

The line 271-4, but not 10 R, was hypersensitive to isolates

Xv 71-21 and Xv 80-5 of race 1 (Tables 4-1, 4-2, and 4-3). Wilting

occurred in the inoculated tissue from about 15 h, and cell collapse was

visibly complete within 24 h in all experiments. No marked difference

in time to necrosis occurred between temperatures of 25 and 30 C. At

25 C, conductivity increased greatly between 21 and 23 h after inocula-

tion (Table 4-2, Figure 4-2). Hypersensitivity was delayed several

hours in hybrid plants. Wilting of the inoculated tissue occurred after

17 h in hybrids, and cell collapse was visibly complete by 27 h (Tables

4-2 and 4-3, Figure 4-2). No difference occurred between hybrids.

Typical HR with isolate Xv 69-1 of race 3 did not occur in plants

of 271-4 in any experiment (Tables 4-1, 4-2, and 4-3, Figure 4-1).

However, inoculated leaf tissue appeared wilted between 15 and 22 h

after infiltration, in unison with race 1 isolates. After that time the

difference between races became apparent. Most leaf tissue infiltrated

with isolate Xv 69-1 of race 3 ceased to appear wilted and returned to

apparent full turgidity by 23 h (Table 4-3). Approximately 10% of the

















U)

4r- -4-

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(u *0 4J
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oc
S 0 0 X *
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.0 >L C-4 5
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tissue appeared as randomly scattered hypersensitive flecks. This

appearance did not alter subsequently. Conductivity of the solution

containing leaf discs increased slowly with time (Tables 4-1 and 4-2,

Figure 4-1), but watersoaked necrosis and a large increase in conductiv-

ity between 36 and 48 h, characteristics of the susceptible reaction,

did not occur. A similar response, but which was delayed by several

hours, occurred with both hybrids (Tables 4-2 and 4-3). However, no

hypersensitive flecks occurred in hybrids.

Isolates of races 1 and 2 were clearly differentiated by inocula-

tion of plants of 271-4 and 10 R. Races 1 and 3 in 10 R resulted in

susceptible reactions. The HR in 271-4 to race 1 occurred about 14 h

later than HR to race 2. Race 3 was clearly differentiated in plants of

271-4 by not inducing typical HR. Plants of ECW and 10 R were suscept-

ible to race 3. The reaction in 271-4 to race 3 may be a modified or

incomplete HR (Klement, 1982). Host cell metabolism appeared to be

influenced by this reaction, and electrolyte loss occurred to an extent

possibly sufficient to be associated with both restricted bacterial pop-

ulation increase (this dissertation, Chapter 3), and death of a small

proportion of host tissue. The majority of host cells appeared to

recover to a non-necrotic, turgid condition. This aspect needs verifi-

cation by means of ultrastructural observations.

The phenotypes of BSl and Bs3 in heterozygotes were incompletely

dominant following inoculation with high concentrations of bacteria. At

25 C the relative time delay in developing confluent HR necroses in

heterozygotes compared with homozygous 271-4 was approximately 20% with

Bsl, and 50% with BS3. Hybrids were therefore expected to support







77

higher bacterial populations than in 271-4 (Klement et al., 1964), which

did occur (Figures 4-3, 4-4, and 4-5).

Numerous discreet lesions with isolates of races 1, 2, and 3 were

visible in leaves of ECW between 5 and 6 days after infiltration with

low concentrations of inoculum. Lesions were not seen in 271-4. Occas-

ional small lesions with isolate Xv E3 of race 2, and relatively many

lesions with isolate Xv 69-1 of race 3 occurred in hybrids. Atmospheric

conditions were at dew point during the nights of day 8 to 10. This en-

couraged natural watersoaking of the mesophyll by root pressure flow

(Johnson, 1947). Watersoaking of leaf-tissue was noted at and adjacent

to those inoculated sites where lesions were visible and bacterial popu-

lations were intermediate to high, but not where populations were low.

Populations of bacteria of races 1, 2, and 3 were 104 to 105

times lower in leaves of 271-4 than in ECW 10 to 14 days after inocula-

tion (Figures 4-3, 4-4, and 4-5). No large or consistent differences

occurred between the two hybrids, and data from them were pooled. High-

er populations occurred in heterozygotes than in 271-4 but the degree of

difference varied with the isolate. There was a small difference 4 to

10 days after inoculation with isolate Xv 71-21 of race 1 (Figure 4-3)

but no difference remained after 12 to 14 days. The hybrid progeny had

bacterial populations that were intermediate between the two parents

with isolate Xv E3 of race 2 (Figure 4-4), and only 10-fold or less

fewer than in ECW with isolate Xv 69-1 of race 3 (Figure 4-5).

The patterns of increase in populations of isolates Xv 71-21 and

Xv E3 in 271-4 and heterozygotes were consistent with hypersensitivity

controlled by Bs3 and Bs1, respectively (Cook and Guevara, 1984;



























Figure 4-3. Populations of bacteria per cm2 of leaf of
peppers Early Calwonder, 271-4, and their reciprocal hybrids
(pooled data) inoculated with race 1 isolate Xv 71-21 of
Xanthomonas campestris pv. vesicatoria. Points represent means
of 6 or 12 replicates.


















SEarly Calwonder
x 271-4
* Reciprocal hybrids .J- '


6 8 10
Days after inoculation


12 14


0
Cm
E

C
L









0
a,
0

4-


0
E


0
L
0


O
4-
O
O

O
>


o.




























Figure 4-4. Populations of bacteria per cm2 of leaf of
peppers Early Calwonder, 271-4, and their reciprocal hybrids
(pooled data) inoculated with race 2 isolate Xv E3 of Xanthomonas
campestris pv. vesicatoria. Points represent means of 6 or 12
replicates.



















* Early Calwonder
x 271-4
* Reciprocal hybrids


after inoculation


,*


a5
06







c4
L.
a)


c






>3
.4-

0


o
0



O
-.J




























Figure 4-5. Populations of bacteria per cm2 of leaf of
peppers Early Calwonder, 271-4, and their reciprocal hybrids
(pooled data) inoculated with race 3 isolate Xv 69-1 of
Xanthomonas campestris pv. vesicatoria. Points represent means
of 6 or 12 replicates.















* Early Calwonder
x 271-4
* Reciprocal hybrids


x






xx


3-


0 2


6
Days after


8
inoculation


10 12







84

Klement et al., 1964; Stall and Cook, 1966). Populations increased for

approximately 2 days at rates similar to those in ECW leaves, but stabi-

lized or declined slowly thereafter. Cell collapse within 27 h at 25 C

in both homozygotes and heterozygotes followed infiltration of leaves

with races 1 and 2 at high inoculum concentrations. Bacteria multiplied

for two days in the variable greenhouse environment after which multi-

plication ceased with low inoculum concentrations. In contrast to these

results, populations of isolate Xv 69-1 of race 3 in 271-4 and heterozy-

gotes increased for 4 to 6 days after inoculation before resistance was

noted. Populations decreased greatly in leaves of 271-4 after day 6

(Figure 4-5) but continued to increase in heterozygotes, which appeared

susceptible.

Natural watersoaking probably contributed to relatively high popu-

lations in heterozygotes with isolates Xv E3 and Xv 69-1 of races 2 and

3, respectively (Klement, 1982). The HR to race 2 controlled by Bsl

is inhibited and a susceptible reaction occurs where constant watersoak-

ing is enforced (Stall and Cook, 1979; and personal observations).

Hypersensitive flecks with race 2 occurred in some leaves in noninocu-

lated tissue adjacent to the inoculated zone. This implied free move-

ment and multiplication of bacteria in a continuum of water. It should

be noted however that intermediate populations occurred from day 4

before watersoaking was observed. The population of isolate Xv E3 was

about 10 times lower at day 14 than at days 10 as 12. This is consist-

ent with populations stabilizing in the absence of watersoaking.

Resistance to race 3 in PI 271322 is variously inherited as a

recessive (Stall, 1981), partially dominant, or purely additive trait




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