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: maria.siomos@gmi.oeaw.ac.at Website: http://www.gmi.oeaw.ac.at (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. 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The presentations at the FEBS Work- shop Adaptation Potential in Plants covered a broad range of topics concerning adaptation, including