Plant phenotypic plasticity in a changing climate

Plant phenotypic plasticity in a changing climate

Plant phenotypic plasticity plays a crucial role in how species adapt to climate change. This research explores the genetic and molecular mechanisms that enable plants to exhibit phenotypic plasticity in response to environmental changes. Authored by A.B. Nicotra and colleagues, the study synthesizes current knowledge on how plants can adjust their traits to survive in shifting climates. It emphasizes the importance of understanding these adaptive responses for both native species and agricultural crops. This document is essential for ecologists, biologists, and agricultural scientists interested in plant resilience and adaptation strategies.

Key Points

  • Explains the genetic mechanisms behind phenotypic plasticity in plants.
  • Discusses the role of environmental factors in shaping plant traits.
  • Analyzes the implications of climate change on plant adaptation strategies.
  • Highlights the importance of phenotypic plasticity for agricultural resilience.
  • newtopiccyclegrowin
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Plant phenotypic plasticity in a
changing climate
A.B. Nicotra
1
, O.K. Atkin
1
, S.P. Bonser
2
, A.M. Davidson
1
, E.J. Finnegan
3
, U. Mathesius
1
,
P. Poot
4
, M.D. Purugganan
5
, C.L. Richards
6
, F. Valladares
7
and M. van Kleunen
8
1
Research School of Biology, The Australian National University, Canberra, ACT, Australia
2
Evolution and Ecology Research Centre & School of Biological, Earth and Environmental Sciences University of New South Wales
Sydney, Australia
3
CSIRO Plant Industry, Canberra, ACT, Australia
4
School of Plant Biology, Faculty of Natural and Agricultural Sciences, University of Western Australia, Crawley, WA, Australia, and
Science Division, Department of Environment and Conservation, Locked Bag 104, Bentley Delivery Centre, WA, Australia
5
Department of Biology, Center for Genomics and Systems Biology, New York University, New York, NY, USA
6
Department of Integrative Biology, University of South Florida, Tampa, FL, USA
7
Instituto de Recursos Naturales. CSIC, Madrid, Spain
8
Institute of Plant Sciences and Oeschger Centre, University of Bern, Bern, Switzerland
Climate change is altering the availability of resources
and the conditions that are crucial to plant performance.
One way plants will respond to these changes is through
environmentally induced shifts in phenotype (phenotyp-
ic plasticity). Understanding plastic responses is crucial
for predicting and managing the effects of climate
change on native species as well as crop plants. Here,
we provide a toolbox with definitions of key theoretical
elements and a synthesis of the current understanding of
the molecular and genetic mechanisms underlying plas-
ticity relevant to climate change. By bringing ecological,
evolutionary, physiological and molecular perspectives
together, we hope to provide clear directives for future
research and stimulate cross-disciplinary dialogue on
the relevance of phenotypic plasticity under climate
change.
Climate change and plant adaption
Climate change is altering the environments in which all
organisms develop. Plant species can adjust to these novel
conditions through phenotypic plasticity (see Glossary),
adapt through natural selection or migrate to follow con-
ditions to which they are adapted; these options are not
mutually exclusive. For any given plant species or popula-
tion, determining responses to environmental changes will
require an understanding of the environmentally induced
variation in the phenotype of individual plants. Once
regarded as noise, phenotypic plasticity is now understood
to be genetically controlled, heritable and of potential
importance to species’ evolution [1,2]. With mounting evi-
dence from molecular and developmental biology, we are
now at the threshold of gaining a sophisticated under-
standing of the mechanisms of plasticity, which will be
crucial for predicting changes in species distributions,
community composition and crop productivity under cli-
mate change [3,4].
Some authors have argued that plastic responses to
rapid climate change are less important than adaptation
Review
Glossary
Adaptive plasticity: Phenotypic plasticity that increases the global fitness of a
genotype (Figure 2).
Environmental sensing loci: Genes or gene regions that encode sensors, or
receptors, for environmental signals, e.g. genes encoding photoreceptors or
receptors detecting microbial signals.
Epialleles: Different forms or alleles of a gene that are identical in DNA
sequence but differ in epigenetic markers. These epigenetic differences are
usually associated with differing expressions of the epialleles. The causes of
their formation are as yet poorly understood.
Epigenetic: Includes the mechanisms of gene regulation that lead to heritable,
but potentially reversible, changes in gene expression without changing the
DNA sequence of the gene (Box 1).
Fitness: The fitness of an individual is taken as the relative abundance and
success of its genes (often measured as the number of surviving offspring)
over multiple generations. In many cases, especially with large or long-lived
species, direct estimates of fitness are not feasible and total biomass, seed
number or biomass, survivorship or growth rates of a single generation are
used as proxies.
Genome plasticity: A change in genome structure or organization associated
with environmental signals, leading to the evolution of new phenotypes, might
result from mutational hotspots, genome expansion, transposable elements or
somatic recombination.
Genotype: When we refer to a genotype we do so in a population genetic
sense, not in reference to a molecular sequence of a single gene, but to the
complete genome.
Phenotype: The appearance or characteristics of an organism resulting
from both genetic and environmental influences. In our terms, all organisms
have a phenotype not just those expressing a mutation in a given gene of
interest.
Phenotypic plasticity: The range of phenotypes a single genotype can express
as a function of its environment.
Plant functional traits: Quantitative traits related to the fitness and success of
individuals in a given environment, they provide good indicators about
species’ ecologies (e.g. what growth rates they are likely to exhibit, what
recruitment strategy they rely on) and are often related to competitive status,
commonness/rarity or dominance in the community (Box 2).
Plant functional types: Categorical assessments enabling plant species to be
grouped according to functional position in a community or ecosystem. For
example, classifications can be based on growth form (e.g. herb, grass, shrub),
nitrogen fixing status, photosynthetic pathway or leaf longevity.
Post-transcriptional and post-translational modifications: Chemical modifica-
tions to mRNA or proteins that are made after an mRNA or protein is
transcribed or translated, respectively (e.g. the phosphorylation of proteins).
Regulatory gene transcription: The process of making mRNA of a regulatory
gene. The RNA is subsequently translated to form a protein, the product of the
gene.
Signaling cascades: These are cascades of events that mediate cellular
responses to external signals, for example the cascades of protein phosphor-
ylation and second messenger generation following the perception of a signal
by a receptor kinase.
Corresponding author: Nicotra, A.B. (adrienne.nicotra@anu.edu.au).
684
1360-1385/$ – see front matter ß 2010 Elsevier Ltd. All rights reserved. doi:10.1016/j.tplants.2010.09.008 Trends in Plant Science, December 2010, Vol. 15, No. 12
or shifts in the geographic range of distribution [5,6]. These
studies argue that the failure to expand beyond current
limits demonstrates that a species’ adaptive potential has
been largely exhausted, or argue that plasticity will be an
unimportant factor because the cues that signaled the
plastic responses in the first place might no longer be
‘reliable’ in changed climates [7]. However, as we show
below, plastic changes in seed longevity, phenology, leaf
lifespan and the temperature responses of metabolic pro-
cesses are all well documented in response to elevated CO
2
and climate change factors.
There is general acceptance that high levels of genetic
variation within natural populations improve the potential
to withstand and adapt to novel biotic and abiotic environ-
mental changes including the tolerance of climatic change
[8]. A portion of this genetic variation determines the
ability of plants to sense changes in the environment
and produce a plastic response. For example, genetic vari-
ation in genes encoding temperature sensors and tran-
scription factors regulating vernalization (see below)
could help plant populations adapt to changes in tempera-
ture. Plasticity, therefore, can both provide a buffer against
rapid climate changes and assist rapid adaption [2,9].
Thus, we argue that, in the context of rapid climate change,
phenotypic plasticity can be a crucial determinant of plant
responses, both short- and long-term.
Here, we provide a conceptual toolbox with definitions of
the key theoretical elements and a synthesis of the current
understanding of the molecular and genetic mechanisms
underlying phenotypic plasticity, as relevant to climate
change. We discuss how new developments in our under-
standing of signaling cascades and epigenetics in particu-
lar hold promise for interdisciplinary approaches to
understanding the evolution of plasticity and for predicting
how plasticity will influence the responses of native plants
and agricultural systems to climate change. We aim to
provide background on the ecological and evolutionary
literature on phenotypic plasticity and outline emerging
techniques in molecular biology. By bringing these per-
spectives together, we hope to stimulate crucial cross-
disciplinary dialogues on the topic of plasticity and plant
responses to climate change [2,9] (Box 1).
Molecular basis of plastic responses in key traits
The ability of an organism to express plasticity in a given
trait must be mediated at the molecular level [10] (See
[()TD$FIG]
Phenotype
regulated by
environment,
genotypes react
similarly
Signal received e.g.
by perceiving light
with a photoreceptor
Signal is transduced
into increased
transcription of genes,
e.g. of the
anthocyanin
biosynthesis pathway
Results in a phenotype
with enhanced enzyme
activity and products , e.g.
increased anthocyanin
content in different
environment
No environmental
response
Signal receptor may
be missing or mutated
Mutation of
transcription factor, or
genes encoding these
proteins may be
silenced by epigenetic
mechanisms.
Genotypes differ
constitutively in trait,
no environmentally
induced change
Phenotype
regulated by
environment,
genotypes react
differently.
One genotype has
more sensitive
receptor than the
other
One genotype
increases
transcription more in
response to signal
than the other
Genotypes differ in
amount of product
produced in response to
environment, but both
show response
Epigenetic, transcriptional or post-
transcriptional regulation
Environment
Phenotype
(e.g. synthesis of
anthocyanin)
Signal cascade
(e.g. induction of
transcription
factors)
Receptor
(e.g.
photoreceptor)
Signal
(e.g. light)
(a)
(c)
Env1
Trait value
Plasticity
E*
G
GxE
1
E
G*
GxE
2
E*
G*
GxE*
3
(b)
Env1 Env2 Env2
TRENDS in Plant Science
Figure 1. Anthocyanins are produced in leaves in response to excess light and temperature and osmotic extremes, and serve as a reversible plastic mechanism forthe
protection of photosynthetic machinery [86–88]. Here, we use an anthocyanin example to illustrate (a) the points in the molecular machinery, which translate an environmental
signal (excess light in this case) into a phenotype. (b) In the evolutionary and ecological literature, these responses are commonly presented as reaction norms. Here, the blue
and red lines indicate the reaction norms of two different genotypes responding to a change from a low light environment (Env1) to a high light one (Env2). The extent of
phenotypic change in response to a signal is its phenotypic plasticity. Asterisks in the panels denote whether there is a significant effect of environment (E) or genotype (G), and
whether there is a significant genotype by environment interaction (G E). (c) Likely examples of the mechanisms underlying the cases depicted in panels 1–3 are given
separately for each point in the signal pathway. The leaves on the left and right represent the phenotypes in Env1 and Env2, respectively.
Review
Trends in Plant Science Vol.15 No.12
685
Figure 1 and Figure I in Box 2). For example, developmen-
tal transformations have been shown to be controlled by
environmental signaling pathways that sense abiotic cues
such as light and nitrogen [11] and drought [12], as well as
biotic signals such as Nod factors that cause nodulation in
legumes under low nitrogen conditions [13]. For many
other environmentally induced phenotypic responses,
the mechanisms of how environmental signals are sensed
and processed are still largely unknown [e.g. 14,15].An
improved understanding of the molecular basis of environ-
mentally induced changes in plant traits will yield insight
into possible ecological and evolutionary responses in wild
species and will be useful for engineering plasticity in crop
species (Box 1, Q1).
Flowering time is a good example of a crucial trait that
has been shown to be both under genetic control and plastic
(see below). Under climate change, the temperature cues
triggering the chain of events leading to flowering might
cease to be reliable if they occur at the wrong time with
respect to the lifecycle and ecology of the species. Such
changes in cue, signal or response schemes might thereby
elicit maladaptive responses [7]. Alternatively, they can
lead to the expression of phenotypic responses that are
currently hidden [16]. Current techniques in molecular
biology and genetics allow for studies of plastic trait
responses that scale from a description of molecular mecha-
nism to the assessment of adaptive value under current or
simulated future climates [17]. Thus far the genetic basis of
plasticity has been examined in greatest depth in model and
crop species. As new tools become available, the extension of
these studies to more non-model species becomes increas-
ingly possible and will help us determine the extent to which
there are genetic homologs in other species (Box 2).
Plasticity in key plant functional traits in response to
climate change
Plasticity is a characteristic of a given trait in response to a
given environmental stimulus, rather than a characteristic
of an organism as a whole. Likewise, some responses are
examples of adaptive plasticity, providing a fitness benefit,
whereas others are inevitable responses to physical pro-
cesses or resource limitations [18,19] (Figure 2). Both
adaptive and non-adaptive plasticity will play a role in
the context of plant responses to climate change. Differen-
tiating between the two is important to our understanding
of both the current value and the evolution of plasticity
(Box 1, Q2). The consensus from the theoretical literature
is that adaptive phenotypic plasticity should evolve in
heterogeneous environments where signals of environmen-
tal conditions are reliable [19,20]. Hypotheses about what
sort of species will be most plastic also abound in the
literature [21–26], yet our ability to predict patterns of
plasticity in key traits in response to climate change
remains limited.
Given that it is not feasible to assess plastic responses to
current or future environments on all species, it is impor-
tant to identify which traits are likely to show important
plastic responses to particular changing environmental
conditions and to develop predictors to enable us to gener-
alize about the sorts of species likely to exhibit these plastic
responses [9]. Those traits can then be examined in current
or projected climate conditions to determine the extent of
plasticity and assess the extent to which the underlying
molecular and genetic pathways are shared (Box 2).
Plasticity in plant functional traits
In recent years, ecologists have categorized species accord-
ing to plant functional types and have also identified
several continuous plant functional traits that vary in
predictable ways along environmental gradients. Func-
tional types are widely used in global climate models to
group species according to their function in the ecosystem
or community (e.g. C3 or C4 grasses, herbs, shrubs, decid-
uous trees, N-fixing legumes, etc.). Functional traits are
those that help describe the ecology of species using a few,
easily quantified variables (e.g. seed size, plant height, leaf
lifespan, leaf mass per area, etc.) [27]. Functional traits are
relevant to both global climate models and mechanistic
models of plant distributions (see below). Considering their
probable importance, we advocate that plant functional
traits should have priority for the investigation of (adap-
tive) phenotypic plasticity and identification of molecular
and genetic mechanisms across species (Box 3).
Adaptive plasticity in functional traits is likely to assist
rapid adaptation to new conditions. Thus, a natural ques-
Box 1. Outstanding questions
Modern techniques and the potential for cross-disciplinary ap-
proaches mean that we are now in a position to address the
following questions effectively.
Q1: Molecular basis of plasticity:
What is the genetic control of plasticity and how is it linked to
epigenetics?
Can we identify ‘plasticity genes’?
Does identifying such plasticity genes improve our ability to
predict the longer term responses of traits and species to climate
change?
Q2: Adaptive plasticity:
What traits are likely to show adaptive plasticity?
Will species with differing ecologies (i.e. differing functional
types) exhibit adaptive plasticity in different traits?
Will the incidence of adaptive plasticity vary among types of traits
(e.g. those related to anatomy versus allocation versus physiol-
ogy)?
Q3: Functional traits:
Are the traits most commonly identified as plant functional traits
also those that show adaptive plasticity?
Is plasticity in functional traits important in determining response
to climate change under future climates, regardless of current
adaptive value?
Q4: Plasticity and evolution:
How has plasticity contributed to the diversification of lineages
and can the evidence of this contribution be found by comparing
the distribution of adaptive plasticity or relevant plasticity genes
with population or species phylogenies?
How will plasticity contribute to rapid evolution in response to
climate change?
How much variation is there for plasticity and how does it respond
to selection?
Q5: Plasticity in crop species:
Has breeding led to reductions in adaptive plasticity in contem-
porary crop varieties relative to older ones or wild ancestors?
Can we breed for plasticity in key traits in agricultural systems to
improve yield stability under climate change?
Review
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FAQs of Plant phenotypic plasticity in a changing climate

What is phenotypic plasticity in plants?
Phenotypic plasticity refers to the ability of a single genotype to express different phenotypes in response to varying environmental conditions. This adaptability allows plants to optimize their growth and reproduction based on the specific challenges they face, such as changes in temperature, light, and water availability. Understanding phenotypic plasticity is crucial for predicting how plant species will respond to ongoing climate change and for developing strategies to enhance crop resilience.
How does climate change affect plant phenotypic plasticity?
Climate change alters the environmental conditions that plants experience, which can trigger phenotypic plasticity. For instance, increased temperatures and altered precipitation patterns can lead to changes in flowering time, leaf longevity, and seed dormancy. These shifts can either enhance a plant's ability to thrive in new conditions or, conversely, lead to maladaptive responses if the environmental cues become unreliable. Thus, studying these plastic responses is vital for understanding future plant distributions and ecosystem dynamics.
What are the implications of phenotypic plasticity for agriculture?
Phenotypic plasticity has significant implications for agriculture, particularly in the context of climate change. By understanding how crops can adjust their traits in response to environmental stressors, farmers and scientists can develop more resilient varieties that maintain productivity under changing conditions. This research can inform breeding programs aimed at enhancing traits such as drought resistance and nutrient use efficiency, ultimately contributing to food security in a warming world.
What key traits are associated with plant functional plasticity?
Key traits associated with plant functional plasticity include leaf mass per area, flowering time, seed size, and root-to-shoot ratio. These traits help determine how well a plant can adapt to its environment and compete for resources. For example, variations in flowering time can affect reproductive success, while changes in leaf structure can influence photosynthetic efficiency. Understanding these traits is crucial for predicting how different species will respond to environmental changes.

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