Group Title: BMC Ecology
Title: Phenotypic plasticity of fine root growth increases plant productivity in pine seedlings
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Title: Phenotypic plasticity of fine root growth increases plant productivity in pine seedlings
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Language: English
Creator: Wu, Rongling
Grissom, James
McKeand, Steven
O'Malley, David
Publisher: BMC Ecology
Publication Date: 2004
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Abstract: BACKGROUND:The plastic response of fine roots to a changing environment is suggested to affect the growth and form of a plant. Here we show that the plasticity of fine root growth may increase plant productivity based on an experiment using young seedlings (14-week old) of loblolly pine. We use two contrasting pine ecotypes, "mesic" and "xeric", to investigate the adaptive significance of such a plastic response.RESULTS:The partitioning of biomass to fine roots is observed to reduce with increased nutrient availability. For the "mesic" ecotype, increased stem biomass as a consequence of more nutrients may be primarily due to reduced fine-root biomass partitioning. For the "xeric" ecotype, the favorable influence of the plasticity of fine root growth on stem growth results from increased allocation of biomass to foliage and decreased allocation to fine roots. An evolutionary genetic analysis indicates that the plasticity of fine root growth is inducible, whereas the plasticity of foliage is constitutive.CONCLUSIONS:Results promise to enhance a fundamental understanding of evolutionary changes of tree architecture under domestication and to design sound silvicultural and breeding measures for improving plant productivity.
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BMC Ecology


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BioMed Central


Research article

Phenotypic plasticity of fine root growth increases plant
productivity in pine seedlings
Rongling Wu* 1,2,3, James E Grissom2, Steven E McKeand2 and
David M O'Malley2


Address: 'School of Life Sciences, Zhejiang Forestry University, Lin'an, Zhejiang 311300, People's Republic of China, 2Department of Forestry,
North Carolina State University, Raleigh, NC 27695, USA and 3Institute of Food and Agricultural Sciences, University of Florida, Gainesville, FL
32611, USA
Email: Rongling Wu* Rwu@stat.ufl.edu; James E Grissom jimgrissom@ncsu.edu; Steven E McKeand steve_mckeand@ncsu.edu;
David M O'Malley davido@unity.ncsu.edu
* Corresponding author


Published: 07 September 2004
BMC Ecology 2004, 4:14 doi:10.1 186/1472-6785-4-14


Received: 29 April 2004
Accepted: 07 September 2004


This article is available from: http://www.biomedcentral.com/1472-6785/4/14
2004 Wu et al; licensee BioMed Central Ltd.
This is an open-access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0),
which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.



Abstract
Background: The plastic response of fine roots to a changing environment is suggested to affect
the growth and form of a plant. Here we show that the plasticity of fine root growth may increase
plant productivity based on an experiment using young seedlings (14-week old) of loblolly pine. We
use two contrasting pine ecotypes, mesicc" and xericc", to investigate the adaptive significance of
such a plastic response.
Results: The partitioning of biomass to fine roots is observed to reduce with increased nutrient
availability. For the mesicc" ecotype, increased stem biomass as a consequence of more nutrients
may be primarily due to reduced fine-root biomass partitioning. For the xericc" ecotype, the
favorable influence of the plasticity of fine root growth on stem growth results from increased
allocation of biomass to foliage and decreased allocation to fine roots. An evolutionary genetic
analysis indicates that the plasticity of fine root growth is inducible, whereas the plasticity of foliage
is constitutive.
Conclusions: Results promise to enhance a fundamental understanding of evolutionary changes
of tree architecture under domestication and to design sound silvicultural and breeding measures
for improving plant productivity.


Background
The use of chemical fertilizers has been responsible for
dramatic increase in the stem wood production of forest
trees [1-4]. In an 8-year-old stand of loblolly pine growing
on an infertile site in Scotland County, North Carolina,
for example, stem volume increment increased 152% after
the fourth year of fertilization treatment [4]. However, lit-
tle is known about the mechanistic basis for such favora-
ble effects of fertilization. One hypothesis is that


improved nutrient availability leads to increases in leaf
area growth and photosynthetic capacity, thus producing
more photosynthate that can be allocated to the stem
wood. This hypothesis has been supported by a number
of physiological studies [5-7] and used as a conceptual
model for plant nitrogen acquisition and cycling [8].
However, forest trees can consume as much as 60-80% of
annual net primary productivity in the turnover of fine
roots [3]. Fine roots are a tissue with high maintenance


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respiration tissue whose primary function is to absorb and
metabolize water and nutrients from the soil [9-121. A
number of previous studies have shown that the produc-
tion of fine roots is sensitive to the availability and distri-
bution of nutrients within the soil [1,4,13,14]. In this
study, we test a second hypothesis that the capacity of fine
roots to respond to nutrient availability, referred to as phe-
notypic plasticity, can potentially increase forest-tree
productivity.

Phenotypic plasticity is the potential of an organism to
alter its phenotype in changing environments [15-19].
Phenotypic plasticity may play an important role in plant
adaptation and evolution by combining a physiological
buffering to poor environmental conditions with an
improved response to favorable conditions [20]. The
understanding of how phenotypic diversity is generated
by the coherent change of other integrated traits is a key
challenge in evolutionary biology. In much plant litera-
ture, studies of adaptive phenotypic plasticity have
focused mainly on morphological and fitness traits above
ground [16]. It is unclear how phenotypic plasticity exerts
a significant effect on plant growth and production
through the alteration of root systems below ground.
Studies strongly suggest that plant root systems are
adapted to different environments [14], and their diver-
sity represents one important form of morphological evo-
lution [12]. Fine roots are unique organs with great
environmental and developmental plasticity which are
subject to strong natural selection and are amenable to
genetic and developmental study [10].

Loblolly pine is the most important tree species for fiber
production in the southern US [21]. Because of its wide
natural distribution from the moist Atlantic Coastal Plain
to the dry "Lost Pines" region of Texas, this species dis-
plays strong adaptability to a range of environmental con-
ditions. However, detailed ecophysiological and
developmental mechanisms for the adaptive response of
loblolly pine from a perspective of fine roots remain
unknown. In the study, we integrate the conceptual theory
of phenotypic plasticity into the test of the hypothesis that
the reduced production of fine roots under high fertiliza-
tion can increase stem productivity in loblolly pine.

Results and Discussion
After 4 weeks of treatment, trees receiving the high nutri-
ent treatment displayed 22% xericic") and 47% mesicic")
greater stem biomass than those under the low fertilizer
treatment (P < 0.001). These values increased to 102%
and 199% for these two ecotypes, respectively, when the
trees were treated for 14 weeks (P < 0.001).

Allometric analysis was used to evaluate the influences of
foliage and fine-root biomass partitioning on stem growth
which arise from differences in nutrient supply. On both


, ...................
A "mesic"
7 .. ... -. ---. --.. --. -
6 .----------.------.--


Low nutrient High nutrient


................................-- ---


Low nutrient High nutrient


0.5

0.4

0.3

20.2
0.1
A-


Low nutrient High nutrient Low nutrient High nutrient


Figure I
Different plant performance under the low and high nutrient
treatments measured at 14 weeks of treatment. (A) Stem
biomass. (B) The proportions of foliage (open bars) and fine-
root (solid bars) biomass to total plant biomass.





harvesting dates, the proportion of foliage biomass to
total plant biomass increased markedly, whereas the pro-
portion of fine root biomass decreased significantly, with
better nutrient supplies. As an illustration, we use Figure 1
to demonstrate the phenotypic plasticity of stem growth
(Fig. 1A) and biomass partitioning between two treat-
ments (Fig. 1 B) on the second harvesting date. However,
the degree of plasticity, defined as the absolute difference
between the two treatments [16], was strikingly greater for
the fine-root proportion than foliage proportion, espe-
cially for the xericc" ecotype. The significance levels for the
treatment effect on stem biomass decreased when the pro-
portion of foliage or fine-root biomass was held constant
(P < 0.01), as compared to the significance level when the
proportion was not held constant (P < 0.0001). These
dependent relationships suggest that increased stem bio-
mass due to better nutrient supplies was attributable to
both increased foliage investment and decreased energetic
costs of fine root construction.




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xericc"


Figure 2
Path diagrams representing the cause-and-effect relationship between the two predictor variables, foliage biomass and fine-
root biomass proportions, and the response variable, stem biomass, that results from differences in nutrient supply. The varia-
ble residual is the undetermined portion. p and r denote path coefficients and correlation coefficients, respectively.


We analyzed genetic differences in how foliage and fine-
root biomass partitioning affect stem biomass through
changes in nutrient level. We used correlations of family
means in the two treatments to calculate path coefficients
of the nutrient-induced plasticity of foliage and fine-root
biomass partitioning to the plasticity of stem biomass. For
mesicc" families, the plasticity of foliage biomass parti-
tioning did not give rise to a change in stem biomass (py,,
= -0.09), whereas the plasticity of fine-root biomass parti-
tioning, i.e., decreased partitioning of biomass to fine
roots under higher fertilization, had a significant impact
on the corresponding increase of stem biomass (py,, = -
0.99, Fig. 2A). For xericc" families, both increased bio-
mass partitioning to foliage and decreased partitioning to
fine roots as a consequence of more nutrients favorably
affected stem biomass. The path coefficients derived from
foliage and fine-root biomass partitioning accounted for
most of the variation in stem biomass as indicated by a
small residual effect (0.09-0.12), suggesting that no addi-
tional traits are required to explain stem biomass. Results
from path analysis suggest that the two ecotypes have dif-
ferent physiological mechanisms that determine the
nutrient-dependent influences of foliage and fine-root
biomass partitioning on stem growth.

Foliage and fine roots have complementary roles in
uptake of resources; the former in energy and carbon


uptake and the latter in water and nutrient uptake [ 12,22].
Mechanistic modeling of resource uptake suggests that the
most efficient deployment of plant biomass is to form
minimal fine roots that supply water and nutrients for the
production of maximum leaf area [11]. However, there
are important trade-offs in generating few fine roots. We
used the ratio of foliage biomass to fine-root biomass
(RFF) as an architectural trait to describe the allocation of
biomass within ephemeral tissues. This ratio reflects the
degree to which plants display a balance of resource
investment vs. resource acquisition. It was highly plastic
to nutritional levels and tree development. The ratio was
larger in the high nutrient treatment (RFF = 6.0-7.0) than
in the low treatment (RFF = 3.0-3.5). Under the higher
nutrient treatment, trees tended to invest increased energy
on foliage with their growth. All these trends differed
between the two ecotypes, as shown by significant interac-
tion effects between ecotypes, treatments and harvesting
dates (P < 0.001). Plasticity between different growth
stages indicates the dependence of plastic responses on
the timing and sequences of developmental events. Eco-
typic variation in developmental plasticity represents
different genetic bases involved in relevant developmental
events [23].

Ecotypic differentiation of loblolly pine could be
explained by limits of plasticity. Quantitative evolution-

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0.05 0.06 0.07 0.08 0.09

Plasticity of biomass partitioning to foliage


0.06 0.09 0.12 0.15 0.18

Plasticity of biomass partitioning to fine roots


Figure 3
The relationships of shoot biomass residuals with the degree of the plasticity of biomass partitioning to foliage (A) and fine
roots (B). In this study, shoot biomass is used as a surrogate of fitness, because great capacity of vegetative growth at early
stages is advantageous for competing for growth resources and is suggested to be favored by natural selection [15]. The resid-
uals of shoot biomass were calculated by differences between its observations and predictions estimated from foliage and fine-
root biomass proportions using polynomial equations (see ref. 24 for a detailed description of this calculation approach). The
degree of plasticity was represented as family difference between the nutrient treatments.


ary genetic models predict that the phenotypic plasticity
of a trait is costly or physiologically limiting when the trait
is forced to respond to environmental variation ("passive"
response). DeWitt et al. [24] delineated five costs (main-
tenance costs, production costs, information acquisition
costs, developmental stability costs and genetic costs) and
three limits (information reliability limits, lag-time limits
and developmental range limits) of plasticity. A limit of
plasticity occurs when facultative development cannot
produce a trait mean as near the optimum as can fixed
development. A negative relationship between the degree
of plasticity and the fitness residuals (calculated from the
regression of fitness on mean phenotype) identifies a
limit of plasticity.

Our analysis suggests that the plasticity of fine-root bio-
mass proportion is physiologically limiting, whereas the
plasticity of foliage biomass proportion is not. The rela-
tionship of the shoot biomass residuals was positive with
the degree of plasticity of foliage biomass proportion (Fig.
3A), but negative with the degree of plasticity of fine-root
biomass proportion (Fig. 3B). Thus, when nutrient supply


changes, foliage and fine roots will respond in different
ways, with the former in a constitutive (active) way and
the latter in an inducible (passive) way [24]. For both
xericc" and mesicc" ecotypes, the families that reduced
fine root biomass the least had the highest stem biomass
on the high nutrient treatment. Larger limits of fine-root
plasticity for xericc" than mesicc" (Fig. 3B) could explain
why the stronger plasticity of fine root growth for the
former ecotype did not result in more stem growth as
expected (see Fig. 1A). Perhaps, for these "Lost Pines"
from infertile sites, under improved nutritional
conditions there is strong conflict between energetic sav-
ings due to reduced fine root production and energetic
costs associated with higher efficiency of absorbing and
metabolizing nutrients with fewer fine roots.

Forest tree form (biomass partitioning) is highly plastic in
response to changes in nutrient levels. The carbon budgets
for forest trees show a surprisingly large role of roots.
Under low nutrient conditions that predominate in
natural forests, 60-80% of photosynthate is allocated
below ground, compared with 30% for high nutrient lev-


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els [3]. Our path analysis for loblolly pine seedlings
showed that phenotypic plasticity of roots had a major
influence on the plasticity of stem biomass, supporting
the hypothesis that roots play a crucial role in forest pro-
ductivity. Current selections when grown on high nutrient
sites could have relative proportions of roots and stems
and foliage that are unfavorable for high yield.

Progress towards domestication in trees will be slowed by
long generation times, but is likely to be based on the
exploitation of interactions between genotypes and yield
associated with various types of agronomic methods (e.g.,
fertilizer levels), as have been shown for herbaceous crop
plants. However, the environmental uncertainties during
the long life span of trees have caused some breeders to
consider the value of plasticity as a trait itself. And plastic-
ity could obscure the relationship between phenotype and
genotype, making selection less efficient. Efforts to
domesticate forest trees will be enhanced by a deeper
knowledge of phenotypic plasticity [20].

Conclusions
Our study of biomass partitioning in relation to varying
nutritional levels in loblolly pine supports the previous
hypothesis, proposed by Linder and Axelson [1], that the
reduced production of fine roots under fertilization
results in the increase of stem production through the
optimal use of energy. Yet, supporting this hypothesis
does not imply that we should reject a more commonly
accepted hypothesis that greater plant production due to
fertilization stems from increased foliage and
photosynthetic capacity. We explained the discrepancy of
these two hypotheses from an ecophysiological perspec-
tive using a well-established conceptual model of pheno-
typic plasticity. The pattern of biomass partitioning is
under environmental control and exhibits considerable
ecotypic differentiation for the best utilization of available
resources. In this study, we observed that biomass parti-
tioning in loblolly pine is also under ontogenetic control,
as well documented in other species [25,26]. Although
our study of fine roots was performed using young
loblolly pine seedlings in controlled conditions, results
promise to enhance a fundamental understanding of evo-
lutionary changes of tree architecture under domestica-
tion and to design sound silvicultural and breeding
measures for improving plant productivity.

Methods
Plant material
Phenotypic plasticity was evaluated for fine roots and bio-
mass partitioning of a commercially important forest tree
species, loblolly pine (Pinus taeda L.). We used two con-
trasting loblolly pine ecotypes from regions that differ in
soil resource availability. One of the ecotypes, known as
the "Lost Pines" of Texas, is adapted to drought condi-


tions and low soil fertility and is denoted by xericc",
whereas the other, Atlantic Coastal Plain, is adapted to
more moderate conditions and is denoted by mesicc".
Adaptive differentiation between the contrasting xericc"
and mesicc" ecotypes has been previously characterized
[21].

In May 1997, the seeds from the two ecotypes of loblolly
pine were germinated in vermiculite, the seedlings were
transplanted to 40 cm deep by 20 cm diameter plastic pots
filled with pure sand, and placed in an open site at the
Horticulture Field Laboratory at North Carolina State Uni-
versity, Raleigh. Pine seedlings from each ecotype were
assigned to two different treatments: low nutrients and
high nutrients [4]. The experiment was laid out in a com-
plete randomized design with two different nutritional
treatments and with five half-sib families from each
ecotype in each level (8 seedlings were included per fam-
ily per ecotype in each treatment). The seedlings in the
high nutrient regime were fertilized at 50 ppm N solution
(Peters 15-16-17) every morning, and those in the low
nutrient level at 10 ppm N every other morning. The two
treatments received the same amount of water. Half of the
trees were harvested after 4 weeks of treatment, whereas
the other half, after 14 weeks of treatment. Plants were
separated into foliage, branches, stem, tap root, coarse
roots and fine roots. Fine roots are defined as those of
diameter < 2 mm.

Data analysis
The differences of stem biomass between the two nutri-
tional levels were statistically analyzed using an allometric
model that characterizes allometric relationships between
plant parts and wholes. The model is based on an expo-
nential function, y = axb, where x and y are total plant bio-
mass and stem biomass, respectively, and a and b
represent the coefficient and exponent of the allometric
equation, respectively [27].

Path analysis was used to identify the cause-effect rela-
tionships in a complex system [281. Path analysis parti-
tions the correlation of component traits with a yield trait
into two parts, direct and indirect. We performed path
analysis to detect the direct and indirect effects of the plas-
ticity of foliage biomass and fine root biomass on the
plasticity of stem biomass. The path coefficients for foli-
age biomass (play) and fine root biomass (p2-y) to stem
biomass through the change of nutritional levels were
estimated by solving the following regular equations:

Pl-y + rl22Py = ly

rl12Ply + P2~y = r2y


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where ry and r2y are the family correlation coefficients of
the plasticity of foliage biomass and fine-root biomass
with the plasticity of stem biomass, respectively, and r12 is
the family correlation coefficient between the plasticity of
foliage biomass and fine-root biomass. Residuals were
estimated to evaluate the degree of determination for the
path analysis [28]. All data analyses were performed using
software SAS (SAS Institute 1988).


Authors' Contributions
RW designed the study, carried out the experiment, ana-
lyzed the data and drafted the manuscript. JEG partici-
pated in the experiment. SEM participated in the design of
the study. DMO participated in the design and coordina-
tion. All authors read and approved the final manuscript.


Acknowledgements
We thank Wen Zeng, Zhigang Lian, Anthony McKeand, Yi Li, Hongxiu Liu,
Helen Chen, Paula Zanker and Jun Lu for technical assistance, Scot Surles
for tipmoth control, and Mary Topa and Bill Retzlaff for helpful discussion
regarding this study. We are especially grateful to Mary Topa and Bill Ret-
zlaff for constructive comments on early versions of this manuscript. This
research was supported by the United States Department of Energy. The
publication of this manuscript was approved as Journal Series No. R-10425
by the Florida Agricultural Experiment Station.

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