Tài liệu Báo cáo khoa học: Shaped by the environment – adaptation in plants Meeting report based on the presentations at the FEBS Workshop ‘Adaptation Potential in Plants’ 2009 (Vienna, Austria) pdf

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

in action. It is of particular interest from both a
scientific and societal perspective to understand the
Keywords
adaptation; Arabidopsis; climate change;
Darwin; ecology; environment; evolution;
genomic variability; speciation; stress
Correspondence
M. F. Siomos, Gregor Mendel Institute of
Molecular Plant Biology, Austrian Academy
of Sciences, Dr. Bohr-Gasse 3, 1030 Vienna,
Austria
Fax: +43 1 79044 23 9101
Tel: +43 1 79044 9101
E-mail:
Website:
(Received 25 May 2009, revised 18 June
2009, accepted 25 June 2009)
doi:10.1111/j.1742-4658.2009.07170.x
As sessile organisms that are unable to escape from inhospitable environ-
ments, plants are at the mercy of the elements. Nonetheless, plants have
managed to adapt, evolve and survive in some of the harshest conditions
on earth. The FEBS Workshop ‘Adaptation Potential in Plants’, held at
the Gregor Mendel Institute of Molecular Plant Biology, Vienna, Austria
from 19 to 21 March 2009, provided a forum (including 18 invited talks,
8 selected short talks and 69 posters) for about 100 plant biologists from
32 countries, working in the diverse fields of genetics, epigenetics, stress
signalling, and growth and development, to come together and discuss
adaptation potential in plants at all its levels.
Abbreviations
BCAA, branched chain amino acid; BCMA, branched chain methionine allocation; CAMTA, calmodulin-binding transcription activator; FLC,

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-

ally reproducing organisms, which have low rates of
gene transfer and recombination, adaptation can be
limited by the availability of genetic variation. Con-
trolling genomic variability allows bacteria to circum-
vent this problem and, thus, thrive in almost all
ecological niches. Recent research on both laboratory
and natural isolates of the bacterium Escherichia coli
from diverse ecological niches, including commensal
and pathogenic isolates, has revealed that mutation
rates vary between isolates [6,7] and, furthermore, that
mutation rates are not constant but can increase in
response to environmental stress [8]. For example,
antibiotic treatment contributes to selection of bacte-
rial strains with higher than average mutation rates,
known as ‘mutator’ strains, on antibiogram tests [9]
and in the gut of germ-free mice (I. Matic, unpublished
results). E. coli mutator strains with the highest rates
of mutagenesis – in the range of 10–100 times that of
the average mutation rate – have been found to have
mutations in the mismatch repair genes mutS and
mutL [8]. By increasing global mutation rates, bacteria
improve their chance of survival under stressful envi-
ronmental conditions, despite the cost associated with
lethal and deleterious mutations.
Locus-specific genomic variability at the BAL locus
in Arabidopsis thaliana, which contains a cluster of dis-
ease Resistance (R)-genes [10,11] implicated in plant
innate immunity, was the subject of the talk of Eric
Richards from the Boyce Thompson Institute at Cor-
nell University, NY, USA. The A. thaliana bal variant

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).

Mechanisms of epigenetic variability
In addition to genetic variation, epigenetic variability
can also contribute to phenotypic variation, upon
which evolutionary forces can act [12]. A major con-
tributor to epigenetic variability is the state of chroma-
tin, which can be altered, for instance, by ATP-
dependent chromatin remodelling [13,14]. This was the
focus of the talk of Andrzej Jerzmanowski from the
Laboratory of Plant Molecular Biology, University of
Warsaw ⁄ Institute of Biochemistry and Biophysics, Pol-
ish Academy of Sciences, Warsaw, Poland. Brande
Wulff from IBMP-CNRS, Strasbourg, France dis-
cussed environmentally induced seed dormancy in Ara-
bidopsis. Seed dormancy, a trait that is found in many
plant species and is defined as the inability of viable
seeds to germinate under favourable conditions, can be
overcome by environmental stimuli, which are also
able to induce new dormant states referred to as sec-
ondary dormancy. Sixty-seven epigenetic recombinant
inbred lines, which are nearly isogenic but differ in
their DNA methylation polymorphisms [15,16], were
used to isolate Arabidopsis lines with quantitative dif-
ferences in secondary dormancy. An epigenetic recom-
binant inbred line was identified that was unable to
germinate in the presence of the gibberellic acid bio-
synthesis inhibitor paclobutrazol. This line was found
not to be affected in primary dormancy, but rather
was more sensitive to certain environmental stimuli
that provoke secondary dormancy (B. Wulff, unpub-
lished results). This phenotype behaves as a single

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-

cies were, for example, recently sequenced [21]. The
value and importance of developing genomics tools,
including genotyping and complete genome sequencing
for diverse A. thaliana accessions [22–24] as well as for
non-model species of Arabidopsis, such as Arabidopsis
lyrata, has also become clear [25]. This gives research-
ers the unprecedented ability to combine advanced
genomics techniques with the genetic and molecular
toolkits available for model organisms to study adap-
tation processes in nature.
Magnus Nordborg from the Gregor Mendel Insti-
tute of Molecular Plant Biology, Vienna, Austria ⁄ Uni-
versity of Southern California, Los Angeles, CA, USA,
Caroline Dean from the John Innes Centre, Norwich,
UK and Thomas Mitchell-Olds from Duke University,
Durham, NC, USA discussed different aspects of eco-
logical genomics. Magnus Nordborg provided an over-
view of genome-wide association studies in A. thaliana.
Although such studies have been primarily applied to
humans to identify disease-related genes of multifacto-
rial diseases, such as diabetes or rheumatoid arthritis,
based on data generated by the HapMap project [26],
genome-wide association studies also provide a power-
ful means of identifying alleles and loci responsible for
M. F. Siomos Adaptation in plants
FEBS Journal 276 (2009) 4705–4714 ª 2009 The Author Journal compilation ª 2009 FEBS 4707
natural variation in model organisms such as A. thali-
ana [27]. To this end, Nordborg has joined forces with
other laboratories to undertake an ‘Arabidopsis Hap-
Map’ project that involves a combination of dideoxy

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

the variation in vernalization response has also been
undertaken, and it was found that the trans-factors
involved in vernalization, namely VRN2, VRN1,
VIN3 and VRN5, which act to cause histone modifica-
tions characteristic of PcG-induced chromatin silenc-
ing, did not map under the QTL. The variation in
vernalization response appears to be due to quantita-
tive differences in the epigenetic silencing of FLC, and
is potentially mediated by cis-elements within FLC.
This variation is important in the adaptation of Ara-
bidopsis to different winter climates [32]. To determine
whether the variation in vernalization response is an
adaptation specific for each microclimate, Dean
intends to monitor Arabidopsis plants from three
Swedish sites. To look at this more generally, she is
performing genome-wide association studies in collabo-
ration with Magnus Nordborg.
Thomas Mitchell-Olds presented a project about the
evolution and fitness of a complex trait involved in
plant chemical defence against insect herbivores.
A. thaliana and Brassica crops constitutively produce
leaf glucosinolates, mostly derived from the amino acid
methionine, which are broken down to form products
that are toxic to insects, thus providing resistance to
herbivory. In Boechera stricta, a close wild relative of
Arabidopsis, a set of glucosinolates can either be pre-
dominantly methionine-derived or branched chain
amino acid (BCAA)-derived, depending on the poly-
morphism at the BCMA (branched chain methionine
allocation) locus, which encodes an enzyme in gluco-

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-

fornia and show a high degree of phenotypic plasticity.
Flower phenotypes in different regions range from
small, red, bird-pollinated flowers (Fig. 1C), through
orange flowers to large, yellow, insect-pollinated flow-
ers (Fig. 1D). Until now, these phenotypic differences
have been attributed to natural hybridization at the
subspecies level. However, by monitoring the flower
phenotypes of these populations in field studies over
the past 13 years, Grossniklaus and Baumberger have
observed that the transition in flower phenotype occurs
Adaptation in plants M. F. Siomos
4708 FEBS Journal 276 (2009) 4705–4714 ª 2009 The Author Journal compilation ª 2009 FEBS
during the lifespan of individual plants (unpublished
results), thus ruling out the hybrids explanation. Further
research has revealed that this phenotypic transition
bears the hallmarks of an epigenetic transition (U. Gross-
niklaus & R. Baumberger, unpublished results). What
makes this transition all the more remarkable is that it
does not occur in plants grown under controlled labora-
tory conditions but only in the field, suggesting that an
environmental factor is triggering the transition. As the
transition from yellow, insect-pollinated flowers to red,
bird-pollinated flowers leads to reproductive isolation,
this is an example of how epigenetics could play a
pivotal role in adaptation and speciation.
Mechanisms of speciation
A species, the lowest taxonomic category in the hierar-
chical classification of living organisms introduced by
Carolus Linnaeus in the 18th century [35,36], refers to
a group of ‘like’ organisms, which, as a result of

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-

tified from a large-scale survey of intraspecific crosses,
approximately 2% of which showed necrosis, and from
which a gene homologous to the TIR–NB–LRR family
of R-genes was previously identified that caused hybrid
necrosis [42]. Ovidiu Paun from the Royal Botanic
Gardens, Kew, UK discussed how genetic and epige-
netic responses to allopolyploidization drive adaptation
in a series of independently formed, ecologically diver-
gent wild Dactylorhiza allopolyploids (Orchidaceae)
with the same diploid parentage (O. Paun, unpublished
results). Fingerprinting-based methods indicate that
recurrent allopolyploidy significantly increases gene
expression range and methylation variation, resulting
in higher levels of evolutionary flexibility. Moreover,
allopolyploid individuals express significantly more
gene variants (including novel ones) than their parents,
providing strong evidence that hybridization and poly-
ploidy increase biological complexity [43].
Non-Mendelian inheritance in hothead
mutants
Susan Lolle from the University of Waterloo, Ontario,
Canada provided an update on her exciting but con-
troversial findings on the HOTHEAD (HTH) organ
fusion mutants in A. thaliana [44]. Homozygous hth
mutants exhibit fusions between floral organs [45,46]
and, when allowed to self-fertilize, manifest segregation
patterns that are dramatically different from those
expected according to Mendelian laws of inheritance.
Instead of 100% mutant progeny being segregated,
 90% of the resulting plants are mutants, while the

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

warming will decrease yields in the tropics and sub-
tropics; temperature increases beyond this level will
have negative effects in all regions [49]. Patterns of glo-
bal rainfall will also be altered, with water becoming a
limiting resource and, according to Easterling, the ‘oil
of the 21st century’. Although the number of people
globally at risk of hunger in 2080 is projected to
decrease relative to today’s levels, global warming is
predicted to increase this number relative to the situa-
tion without global warming [49]. In light of these pre-
dictions, Easterling stressed the importance of
agriculture adapting to these new climatic conditions,
including by making use of the full pallet of genetic
tools available to generate crop plants that are better
able to cope with stresses such as heat, cold, drought
and high salinity. In subsequent Workshop talks, plant
mechanisms for responding to cold, heat, canopy
shade, phosphate starvation and UV stresses were dis-
cussed.
Michael Thomashow from Michigan State Univer-
sity, MI, USA presented research on gene regulons
and regulatory pathways involved in freezing tolerance
in Arabidopsis. Freezing tolerance increases in many
plants in response to low, non-freezing temperature, a
process known as cold acclimation. Cold acclimation
in Arabidopsis involves a network of regulatory genes,
starting from the upstream ‘thermometer’ genes that,
through signal transduction pathways, lead to induc-
tion of a first wave of genes encoding transcriptional
activators. This is followed by additional waves of

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

role [54]. Vierling’s research group has been using com-
plementary experimental approaches, including tran-
scriptome profiling, and forward and reverse genetics,
to identify mechanisms involved in acquired thermotol-
erance in plants. Transcriptome profiling revealed 57
transcripts specifically upregulated in acclimated
plants, including heat shock proteins, transcription
factors and immunophilins, as well as downregulated
transcripts, including biotic stress-responsive genes
[55]. Forward genetic screens yielded mutants defective
in thermotolerance (‘hot’ mutants), including the heat
shock protein Hsp101, whose promoter responds to
heat like a thermometer [56]. An Hsp101 suppressor
screen has identified a mitochondrial transcription ter-
mination factor-related protein that is able to restore
thermotolerance, not only in the presence of the
Hsp101 allele used for the screen but also of the null
allele and other heat-sensitive mutants (E. Vierling,
unpublished results).
Margarete Mu
¨
ller from the Leibniz Institute of Plant
Genetics and Crop Plant Research, Gatersleben,
Germany talked about local and systemic regulation of
phosphate starvation responses in Arabidopsis. With
plants that either had a phosphate-sufficient or phos-
phate-deficient shoot, a split root system was used to
investigate phosphate deficiency responses such as root
growth inhibition, increase in root hair number and
the expression of 51 phosphate starvation-inducible

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

in the light-induced, rapid and conformation-depen-
dent degradation of PHYA. The presentation of Ida
Ruberti from the Institute of Molecular Biology and
Pathology, National Research Council, Rome, Italy
was on the molecular mechanisms involved in the
shade avoidance response, which leads to a stimulation
of elongation growth as well as to inhibition of root
and leaf development. Auxin signalling plays a crucial
role in all of these responses [61,62]. The persistence of
a low ratio of red to far-red signal results in the down-
regulation of several genes that are rapidly upregulated
in the shade avoidance response, including the auxin-
related genes IAA19 and IAA29 [63]. The negative reg-
ulator of the shade avoidance response, HFR1 ⁄ SICS1,
is also induced in response to shade, so as to ensure
that an exaggerated reaction does not occur if a plant is
unsuccessful in escaping canopy shade. Ruberti reported
that HFR1 ⁄ SICS1 functions in the PHYB signal trans-
duction pathway and acts in concert with other tran-
scription factors modulated through PHYA in response
to canopy shade [63]. The many facets of auxin signal-
ling in plant growth and development [64,65] were
explained by Eva Zazˇ ı
´
malova
´
from the Institute of
Experimental Botany, Academy of Sciences of the Czech
Republic, Prague, Czech Republic. This subject was also
touched upon by Laszlo Bo

¨
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,

mostly in poster presentations, but also in short talks.
In recognition of their efforts, three poster prizes were
awarded to young scientists: Sascha Laubinger (Max
Planck Institute for Developmental Biology, Tubingen,
Germany) for his poster about the dual roles of the
nuclear cap-binding complex and SERRATE in pre-
mRNA splicing and microRNA processing; Maria
Novokreshchenova (Moscow State University, Russian
Federation) for her poster about the responses of the
Arabidopsis NFZ24 mutant to cold and high-light
treatment; and Tom Turner (Gregor Mendel Institute
of Molecular Plant Biology, Vienna, Austria ⁄ Univer-
sity of Southern California, Los Angeles, CA, USA)
for his poster about local adaptation of A. lyrata to
serpentine soils revealed by population resequencing.
Numerous different levels of adaptation mechanisms
have enabled plants to conquer some of the most
inhospitable habitats on earth. Gaining an overall
understanding of how these mechanisms interact to
allow plants to adapt to ever-changing environmental
conditions requires interdisciplinary approaches, with
scientists from different fields combining their expertise
to tackle unanswered questions. The Workshop left its
participants with much food for thought by providing
just such an interdisciplinary forum, in which research
results, including novel concepts such as environmen-
tally induced increases in mutation rates in bacteria
and a heritable, epigenetic, environmentally-induced
switch of pollination syndromes in Mimulus, or contro-
versial findings such as non-Mendelian inheritance in

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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