REVIEW ARTICLE
Shaped by the environment – adaptation in plants
Meeting report based on the presentations at the FEBS Workshop
‘Adaptation Potential in Plants’ 2009 (Vienna, Austria)
Maria F. Siomos
Gregor Mendel Institute of Molecular Plant Biology, Austrian Academy of Sciences, Vienna, Austria
Introduction
Two hundred years after the birth of the British natu-
ralist and writer Charles Darwin (1809–1882)
(Fig. 1A), and 150 years after his seminal publication
On the Origin of Species by Means of Natural Selec-
tion, or the Preservation of Favoured Races in the
Struggle for Life [1], Darwin’s theory of evolution, in
which natural selection acting on heritable variation
in populations is responsible for biological diversity,
has been widely accepted by biologists. As written by
Theodosius Dobzhansky, ‘Nothing in biology makes
sense, except in the light of evolution’ [2]. The magni-
tude of Darwin’s insight into evolutionary processes
can only be fully grasped when reflecting that Darwin
was aware of neither Gregor Mendel’s laws of inheri-
tance [3] (which went all but unnoticed until their
rediscovery at the turn of the 20th century) nor of
what the physical basis underlying variation within
populations might be. Since the discovery of the
structure of DNA [4] and the ability to analyse DNA
by sequencing and other molecular methods, we now
know that genetic variation and epigenetic mecha-
nisms form the basis of phenotypic variation. It is,
however, only recently that the necessary tools have
been developed to study the evolutionary process

FLOWERING LOCUS C; FRI, FRIGIDA; HTH, HOTHEAD; QTL, quantitative trait locus; R, Resistance; siRNA, small interfering RNA.
FEBS Journal 276 (2009) 4705–4714 ª 2009 The Author Journal compilation ª 2009 FEBS 4705
molecular mechanisms by which plants, as sessile
organisms, adapt to local environmental conditions
(Fig. 1B), as this allows insights into the processes of
speciation and evolution of life on earth as well as
providing the potential to generate crop varieties that
are adapted to defined environmental conditions. This
will be an important strategy in reducing the number
of people at risk of hunger as a result of global cli-
mate change. The presentations at the FEBS Work-
shop ‘Adaptation Potential in Plants’ covered a broad
range of topics concerning adaptation, including the
control of genomic variability, mechanisms of epige-
netic variability, ecological genomics, mechanisms of
speciation, non-Mendelian inheritance and the response
of plants to environmental stress.
Controlling genomic variability
As genetic variation is the ultimate source of pheno-
typic variation within populations, it is the driving
force for creating the raw materials on which natural
selection can work to cause adaptation. Although
Neo-Darwinian evolution holds that genetic variation
is random, it is beginning to emerge that the timing or
location of heritable genomic variability can be con-
trolled [5].
An example of temporal control of genomic variabil-
ity in bacteria was given in the Workshop’s broad
introductory lecture to the topic of adaptation by Ivan
Matic from INSERM U571, Paris, France. In asexu-

A
B
C
D
Fig. 1. Flower shape adapts to maximize pollination. (A) Charles Robert Darwin: copy by John Collier, 1883 (1881) (National Portrait Gallery,
London, UK). (B) The colouring of the labellum (specialized median petal) of the flowers of the orchid Ophrys speculum closely resembles
the female wasp Colpa aurea, thus males of the species are attracted to the flower and pick up pollen during their attempts at mating
(image courtesy of the Encyclopaedia Britannica online from the article ‘Mimicry – biology’). (C) Small, red flower of Mimulus aurantiacus
var. puniceus adapted for bird pollination. Scale bar: 1 cm. (D) Large, yellow flower of M. aurantiacus var. australis adapted for insect pollina-
tion. Scale bar: 1 cm (images of Mimulus flowers courtesy of Rolf Baumberger).
Adaptation in plants M. F. Siomos
4706 FEBS Journal 276 (2009) 4705–4714 ª 2009 The Author Journal compilation ª 2009 FEBS
is a morphological derivative, originating from a loss
of the epigenetic regulator DDM1 in the Columbia
background, characterized by a dwarf phenotype,
twisted leaves and decreased seed production. The bal
variant is partially resistant to Pseudomonas syringae –
a situation that, under certain environmental condi-
tions, could represent enhanced fitness, even though
mutant plants are less fertile. Richards’ results show
that the bal phenotype, rather than resulting from an
epiallele as previously thought, is due to a genetic
alteration that leads to overexpression of the SNC1
gene from within the R-gene cluster (H. Yi & E. Rich-
ards, unpublished results). If bal is not an epiallele
but is due to a genetic mutation, how can bal revert
to BAL at an unusually high frequency upon ethane
methyl sulfonate treatment? The explanation appar-
ently lies in locus-specific hypermutation of the SNC1
gene (H. Yi & E. Richards, unpublished results).

recessive locus with a sporophytic maternal effect,
which suggests that it acts specifically in the seed coat.
Uniparental expression was the central theme in the
presentation of Rebecca Mosher from the University
of Cambridge, UK, who talked about a 24-nucleotide
class of plant small interfering RNAs (siRNAs) in
Arabidopsis. There are 4000–10 000 such siRNA loci
in floral tissue, corresponding to at least 1% of the
Arabidopsis genome, 90% of which require plant-
specific RNA polymerase IV, which is involved in the
RNA-dependent DNA methylation pathway [17]. The
function of 24-nucleotide siRNAs is elusive, as there
are no overt phenotypes associated with mutations in
RNA polymerase IV. However, these siRNAs accu-
mulate in developing seeds, and are only expressed
from maternal genes as seeds develop [18]. Mosher
speculated that the evolutionary role of this uniparen-
tal expression could be adaptation to divergent pollen
donors.
Ecological genomics
In the emerging field of ecological genomics, genomics
and molecular approaches are combined for the study
of adaptation of organisms in their natural habitats.
The recent advent of high-throughput deep sequencing
[19], as well as of other genomic methods, including
quantitative trait locus (QTL) analysis [20], is allowing
research to move away from conventional model or
crop organisms to ecologically relevant species, either
in their natural habitats or isolated from natural habi-
tats. The genomes of 10 closely related Drosophila spe-

sequencing, whole genome resequencing using Perlegen
technology, single nucleotide polymorphism genotyp-
ing and Solexa shotgun sequencing of over 1000 Ara-
bidopsis lines, and has already generated data about
loci associated with flowering [28], pathogen resistance
[28], and developmental and ionomic phenotypes
(M. Nordborg, unpublished results). The development
of a browser for the research community, displaying
such association results, is in progress.
Caroline Dean talked about the regulation of flower-
ing time, a key trait in adaptation to different environ-
ments that is vital for reproductive success. Many
genes and pathways are involved in regulating flower-
ing in Arabidopsis, including the floral repressor gene
FLOWERING LOCUS C (FLC) [29,30]. FLC expres-
sion is repressed by vernalization, the acceleration of
flowering by a period of exposure to cold, thus pro-
moting flowering, whereas FRIGIDA (FRI) activates
FLC expression, resulting in inhibition of flowering.
FRI and FLC together ensure that flowering does not
commence until winter has passed. As there is varia-
tion in both the requirement for and response to ver-
nalization across natural accessions of Arabidopsis
from different geographical locations, it is of interest
to understand the molecular basis underlying this vari-
ation. Allelic variation at FRI is the major determinant
of vernalization requirement, and rapid-cycling Arabid-
opsis accessions (i.e. those not needing vernalization),
such as the commonly used Columbia ecotype, carry
loss of function of FRI alleles [31]. QTL analysis of

sinolate biosynthesis and which was identified by QTL
analysis [33]. B. stricta plants producing methionine-
derived glucosinolates are resistant to the generalist
lepidopteran herbivore Trichoplusia ni, whereas plants
with BCAA-derived glucosinolates are susceptible [33].
As herbivory levels influence the fitness of the host
plant, herbivores can act as agents of natural selection.
To test whether the BCMA locus is under selection,
over 2000 plants nearly isogenic for the BCMA locus
were planted in two different natural habitats in the
Rocky Mountains, and herbivore resistance and indi-
vidual fitness were measured. Whereas high herbivore
pressure at the southern site caused a reduction in
fitness and strong selection for resistance (i.e. the
methionine allele), at the northern site, lower herbi-
vore pressure resulted in no selection for resistance
(i.e. the BCAA allele) (T. Mitchell-Olds, unpublished
results).
Ecological epigenetics
Traditionally, it has been held that genomic variability
forms the basis for variation in populations upon
which natural selection can act. However, epigenetic
mechanisms, which are heritable, can form stable
states that contribute to natural variation [34] and,
thus, also to evolution. A possible role for epigenetics
in evolution was put forward by Ueli Grossniklaus
from the University of Zurich, Switzerland, who intro-
duced ongoing research in collaboration with Rolf
Baumberger into shrubs of the Mimulus aurantiacus
species complex, which are endemic in southern Cali-

genetic (including hybridization and polyploidy) and
epigenetic variation, and natural selection, does not
remain static but can evolve. According to Ernst
Mayr’s ‘biological species concept’ [37] (one of several
different definitions of a species [38]), different species
are reproductively isolated from each other. An exam-
ple of reproductive isolation is the negative heterosis
(hybrid sterility or lethality) observed in the offspring
of crosses between divergent parents in many species,
including A. thaliana, which is proving to be a promi-
nent model for speciation studies [39]. Three talks at
the Workshop addressed molecular mechanisms
involved in the early stages of plant speciation.
Luca Comai from the Department of Plant Biology
and Genome Center, UC Davis, CA, USA gave a talk
about the genetic and molecular factors that affect the
success of newly formed polyploid Arabidopsis plants.
Interploidy crosses of A. thaliana can result in F
1
lethality due to dosage-sensitive incompatibility [40].
One of the factors highlighted that can control such
lethality is the WRKY transcription factor, TTG2 [41],
which controls seed development through expression in
the maternal sporophyte. Roosa Laitinen from the
Max Planck Institute for Developmental Biology,
Tubingen, Germany focused on a single locus that
causes F
1
hybrid incompatibilities in A. thaliana
(R. Laitinen, unpublished results). This locus was iden-

other  10% ‘revert’ to a wild-type phenotype. One
trivial explanation for the existence of these ‘rever-
tants’ is outcrossing with pollen from wild-type plants,
which could be plausible, owing to the fused reproduc-
tive organs in the hth mutants, and this is the explana-
tion preferred by some researchers [47,48]. According
to Lolle, however, in large-scale experiments, detect-
able outcrossing events are too low in number to
account for the high levels of reversion seen in the hth
mutants. As even indel mutations revert to a perfect
wild-type sequence (S. Lolle, unpublished results), Lolle
believes that there is a template mechanism involved,
and that the templates may be in the form of an RNA
cache. Her latest argument supporting non-Mendelian
inheritance in hth mutants concerns rare mosaic plants
in which some sectors are wild type and others mutant
(S. Lolle, unpublished results). The jury is still out on
this potentially revolutionary new mechanism of inher-
itance, and the scientific community is eagerly awaiting
publication of further evidence.
The environment stresses plants
The science and society lecture of William Easterling,
Pennsylvania State University, PA, USA addressed the
question of how agriculture will be affected by climate
change in response to global warming. Easterling
M. F. Siomos Adaptation in plants
FEBS Journal 276 (2009) 4705–4714 ª 2009 The Author Journal compilation ª 2009 FEBS 4709
reported that moderate increases in global tempera-
tures of up to +3 °C will benefit temperate mid-lati-
tude to high-latitude regions, whereas even slight

gene expression that result in stress tolerance. In Ara-
bidopsis, the CBF cold acclimation pathway includes
action of the transcription factors CBF1, CBF2 and
CBF3 (members of the AP2 ⁄ EREBP family of DNA-
binding proteins) [50]. The CBF1–3 genes are induced
within 15 min of low-temperature exposure, and their
induction is also gated by the circadian clock, with the
extent of transcript accumulation upon cold exposure
depending on the time of day of the exposure [51].
Cold induction of CBF2 involves multiple cis-acting
regulatory elements, one of which binds members of
the calmodulin-binding transcription activator (CAM-
TA) family of transcription factors [52,53]. CAMTA3
is a positive regulator of both CBF2 and CBF1 expres-
sion, and plants carrying a camta1 ⁄ 3 double mutation
are impaired in freezing tolerance [52]. These results
establish a role for CAMTA proteins in cold acclima-
tion and provide a possible point of integrating low-
temperature calcium and calmodulin signalling with
cold-regulated gene expression.
Elizabeth Vierling from the University of Arizona,
Tucson, AZ, USA discussed signalling networks
involved in plant responses to high temperature. In a
similar manner as for freezing tolerance, many plants
are able to acclimate to high temperatures that would
otherwise be lethal to plants upon direct exposure.
This process requires a complex network of factors,
ranging from components involved in sensing and sig-
nal transduction, to transcription factors and effector
molecules, with heat shock proteins playing a crucial

genes in the roots [57].
The energy transmitted by sunlight is the ultimate
source of energy for life on earth, and can be har-
nessed by photosynthesis in plants, blue-green algae
and certain bacteria. As sunlight is an extremely
changeable, abiotic environmental factor, several
aspects of plant responses to sunlight were addressed
at the Workshop. Ferenc Nagy from the Biological
Research Centre, Szeged, Hungary elaborated on the
signalling mechanisms of the phytochrome group of
Arabidopsis photoreceptors (PHYA, PHYB, PHYC,
PHYD, PHYE), which regulate growth and develop-
mental processes such as hypocotyl growth, flower
induction, flavonoid synthesis, root growth, shade
avoidance and greening through signal transduction
Adaptation in plants M. F. Siomos
4710 FEBS Journal 276 (2009) 4705–4714 ª 2009 The Author Journal compilation ª 2009 FEBS
cascades [58]. All of the phytochrome pathways share
a common feature, namely that light alters their
nucleo-cytoplasmic distribution in a quantity-depen-
dent and quality-dependent manner [59]. Nagy concen-
trated his discussion on PHYA and PHYB, and
provided evidence that the molecular machinery medi-
ating light-regulated nuclear import of these photore-
ceptors is substantially different and that FHY1 ⁄ FHL
are rate-limiting factors for PHYA relocalization into
the nucleus [60]. He also stressed the importance of
light-induced protein degradation in phytochrome-con-
trolled signalling and showed data on mutants, isolated
in a custom-designed genetic screen, that are impaired

¨
gre from the School of Bio-
logical Sciences, Royal Holloway, University of Lon-
don, UK, who talked about signalling pathways
regulating the extent and directionality of plant growth
in response to environmental stress factors during devel-
opment [66,67]. The third talk on plant responses to
light was that of Jean Molinier from IBMP-CNRS,
Strasbourg, France, who presented data on the role of
one of the CUL4-based E3 ligase complexes, CUL4–
DDB1–DDB2, in the control of genome integrity in
response to UV radiation in Arabidopsis. Plants are in
the precarious position of, on the one hand, requiring
sunlight that contains UV radiation to undergo photo-
synthesis and, on the other hand, of having to ensure
that UV radiation does not induce irreversible DNA
damage. Molinier showed that the CUL4–DDB1–
DDB2 complex plays a role in nucleotide excision repair
of UV-C-induced DNA damage and that this activity is
controlled by the ATR kinase [68]. In addition,
preliminary data show that the CUL4-based E3 ligase
complex may be involved in the control of chromatin
structure and dynamics, which also contributes to the
maintenance of genome integrity and flexibility.
Conclusion
The FEBS Workshop ‘Adaptation Potential in Plants’
was a great success, with talks and posters covering
top-quality research, much of which was unpublished.
A large number of young researchers were given the
opportunity to discuss their projects at the Workshop,

Arabidopsis hth mutants, were discussed, with expertise
from one field being applied to another. It is only with
collaboration at this level that knowledge of plant biol-
ogy will be advanced and that the potential that such
knowledge offers will be unleashed and applied to
solving societal problems such as provision of food
and energy. This point was highlighted in the science
M. F. Siomos Adaptation in plants
FEBS Journal 276 (2009) 4705–4714 ª 2009 The Author Journal compilation ª 2009 FEBS 4711
and society lecture about the effect of climatic change
on agriculture, and is crucial at a time when the cli-
mate is changing at an unprecedented rate because of
human activity.
Acknowledgements
The organizers of the Workshop ‘Adaptation Poten-
tial in Plants’ (O. Mittelsten Scheid, W. Aufsatz,
C. Jonak, K. Riha, D. Schweizer and M. Siomos
from the Gregor Mendel Institute of Molecular Plant
Biology, Vienna, Austria) acknowledge the funding
awarded by FEBS and the Austrian Federal Ministry
of Science and Research in support of the Work-
shop. M. Siomos thanks U. Grossniklaus (University
of Zurich, Switzerland), O. Mittelsten Scheid and K.
Riha for critically reading the review, and R. Baum-
berger, the Encyclopaedia Britannica and the
National Portrait Gallery, London, UK for provid-
ing images.
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