TY - JOUR
AU - Eckardt, Nancy A.
AB - Conway Morris (2000)wrote that the only point of agreement among biologists discussing organic evolution seems to be “It happened.” Until recently, those attempting to forge links between evolutionary and functional plant genetics might have responded that discussions of any kind would be nice. Thomas Mitchell-Olds (Max Planck Institute for Chemical Ecology, Jena, Germany) and Montserrat Aguadé (University of Barcelona, Spain) are two such scientists amid a growing group who are beginning to realize the benefits of discussions and collaboration between functional geneticists (such as developmental molecular biologists) and evolutionary geneticists (such as those studying population genetics and ecology). Mitchell-Olds and Aguadé organized a recent workshop on Functional Evolutionary Genetics and Plant Adaptation, held in Jena, Germany, on March 9 through 11, 2001, to promote interactions between these fields. The workshop was sponsored by the European Science Foundation Scientific Program on Plant Adaptation. Judging by the enthusiasm of the participants and the high quality of the presentations, the meeting was an unqualified success. This report presents a general overview of the meeting and summarizes the major themes that emerged. See http://www.ice.mpg.de/departments/Gen/conferences/esf_2001/ for a full listing of speakers and abstracts. LINKAGE DISEQUILIBRIUM AND SINGLE NUCLEOTIDE POLYMORPHISMS One of the most important concepts in studies of both functional and evolutionary genetics is linkage disequilibrium (LD). The extent and ramifications of LD in Arabidopsis thaliana was a topic of great interest at the workshop and was discussed in detail in talks given by Magnus Nordborg (University of Southern California, Los Angeles) and Karl Schmid (Max Planck Institute for Chemical Ecology). In a population with several polymorphic loci, LD occurs when alleles at two loci occur together more often than expected (Figure 1) Figure 1. Open in new tabDownload slide Two Populations Are Depicted with Polymorphisms at the A Locus and the B Locus. In the first population, allelic state at the A locus is independent of alleles at the B locus. Genotypes at the two loci are independent, hence the population is in linkage equilibrium. In the second population, A alleles are paired with B alleles (and a alleles occur with b alleles) more often than would be expected if they were independent. Such correlation (or nonindependence) among loci is called linkage disequilibrium. Linkage disequilibrium is important in genomics because marker loci may be correlated with functional variants (such as disease genes). This permits identification of disease genes and the prediction of disease risk. Figure 1. Open in new tabDownload slide Two Populations Are Depicted with Polymorphisms at the A Locus and the B Locus. In the first population, allelic state at the A locus is independent of alleles at the B locus. Genotypes at the two loci are independent, hence the population is in linkage equilibrium. In the second population, A alleles are paired with B alleles (and a alleles occur with b alleles) more often than would be expected if they were independent. Such correlation (or nonindependence) among loci is called linkage disequilibrium. Linkage disequilibrium is important in genomics because marker loci may be correlated with functional variants (such as disease genes). This permits identification of disease genes and the prediction of disease risk. . LD is a statistical measure that quantifies the nonindependence of genotypes at several loci. When genotypes are correlated between loci, the information from a marker may predict genotypic function at another locus—hence, the importance of LD in functional genomics and studies of hu-man disease. In some instances, the occurrence of LD suggests that selection favors chromosomes carrying particular multilocus genotypes. However, Nordborg pointed out that the extent of LD is a result of a complex historical process (M. Nordborg and S. Tavaré provide a comprehensive discussion of this topic in an unpublished review available at http://www-hto.usc.edu/papers/abstracts/tig.html). LD is expected to vary greatly because of the randomness of history, but the average rate of decay of LD (i.e., the genetic or physical distance over which LD can be measured) depends on the demographic history of the population and a number of other factors. In particular, in plant populations, the extent of selfing versus outcrossing can have a strong effect. Nordborg showed that LD is more extensive in selfing species, which is expected because populations of self-pollinating individuals tend to be largely homozygous (Nordborg, 2000). What was of great interest to those at the meeting was that Nordborg also showed that although LD is extensive in A. thaliana, it is far from genome wide (as had been considered by many to be the case). He presented evidence that LD in A. thaliana decays over a distance of 100 to 200 kb. This has significance for those interested in using single nucleotide polymorphisms (SNPs) in association studies (i.e., linking phenotype with a SNP marker). A genome-wide “SNP chip” for conducting association studies with A. thaliana could be constructed using ∼2000 SNPs spaced at 50- to 100-kb intervals, a prospect that is possible with currently available resources and technologies. Nordborg favored the idea of sequencing 500- to 1000-bp segments every 50 to 100 kb (1% of the genome) in 100 individuals, which could be used to produce a SNP chip with 10 or so tightly linked SNPs every 50 to 100 kb. Schmid discussed efforts of the Max Planck SNP Consortium to develop a database of 1300 SNPs, evenly spaced at 100 kb, by using a selection of 12 A. thaliana accessions that are among the most highly diverged (based on previous amplified fragment length polymorphism studies) plus data from the closely related species Arabidopsis lyrata and Arabis drummondii. GENETIC VARIATION AND THE MATING GAME One of the major topics of discussion was the idea that the type of mating system (i.e., selfing versus outcrossing) can have a significant effect on the evolution of plant genes. A high degree of selfing produces highly homozygous populations, which effectively reduces recombination (as discussed above) and complicates efforts to determine the adaptive significance of a particular trait or gene. Because A. thaliana is a highly selfing species, a number of evolutionary geneticists have turned to the closely related outcrossing species A. lyrata as a model for investigating adaptive variation (North American and European subspecies formerly known as Arabis lyrata, Arabis petraea, and Cardaminopsis petraea are now considered subspecies of Arabidopsis lyrata [O'Kane and Al-Shehbaz, 1997]). Work with A. lyrata comes with the disadvantage that very little genomic sequence is available. However, its close relationship with A. thaliana makes it particularly amenable to studies of “candidate genes,” in which genes that are suspected of being associated with important phenotypic traits (e.g., based on the biochemical function of the protein) are selected as possible candidates influencing adaptively signifi-cant variation. Candidate genes can be identified (mapped, cloned, and sequenced) in A. lyrata quite easily because of the high degree of homology and colinearity between the two species. Associations between the candidate gene and the phenotypic trait may sometimes be easier to demonstrate in the outcrossing A. lyrata; thus, the adaptive role of the specific candidate could be confirmed. Because of the wealth of genetic and genomic information available regarding A. thaliana, comparisons between A. lyrata and A. thaliana can be expected to provide critical information not only about the importance of mating system in shaping evolutionary outcomes but also about the possible adaptive and functional significance of various genetic loci. The effect of mating system on DNA variation was discussed in a number of presentations. Because selfing produces populations of homozygotes and reduces the effective recombination rate, it is commonly thought that selfing reduces DNA variation. However, selfing actually has little effect on the overall amount of DNA variation within a species. Rather, it affects how variation is structured. DNA variation in a selfing species tends to be structured into distinct haplotypes coupled with extensive LD (a haplotype is a specific multilocus combination of alleles that occurs in an individual, such as A1B1). Conversely, recombination among heterozygotes in an outcrossing species reduces LD and breaks up haplotypes. Outi Savolainen (University of Oulu, Finland) compared sequence variation in A. lyrata and A. thaliana for alcohol dehydrogenase (Adh), the model gene of sequence variation in plants, and the candidate genes CONSTANS (CO) and FRIGIDA (FRI), which have been associated with flowering time in a number of species. The overall (within-species) level of variation was about the same in both species; however, a higher degree of within-population polymorphism was found in A. lyrata compared with that of A. thaliana populations. Selfing is expected to decrease the effective population size, and thus within-population variation, by twofold relative to outcrossing species, but within-population variation was decreased more than twofold in A. thaliana relative to A. lyrata. In addition to the effect of selfing, the recent and rapid expansion of A. thaliana from Asia to other parts of the world, leading to founder effects or so-called bottlenecks, is seen as an important factor leading to low within-population variation in A. thaliana (Savolainen et al., 2000). This idea was echoed by a number of other speakers. Interestingly, CO and FRI showed more sequence divergence between the two species than did Adh, suggesting that different constraints may be acting on these genes. The difficulty of inferring the action of natural selection in selfing species was raised in several presentations. For example, Aguadé presented data on sequence variation in genes encoding enzymes of the phenylpropanoid pathway in A. thaliana. Two patterns of variation emerged: in some genes (typified by FAH1), variation was structured into two highly divergent haplotypes that exhibited little within-haplotype diversity, whereas in other genes (typified by CHI), there was no clear evidence for two haplotypes. In outcrossing species, the presence of two highly divergent haplotypes in regions with normal levels of recombination can be a strong indication of balancing selection in that region. However, in a selfing species, this pattern could equally be attributable to genetic drift, given that recombination is effectively reduced (Aguadé, 2001). Information about the potential adaptive significance of genes can come from examining patterns of DNA variation in the context of gene function and phenotype. Michael Purugganan (North Carolina State University, Raleigh) presented data on DNA variation among genes involved in flower development, which again suggested that two basic patterns of variation exist in A. thaliana: genes that are somehow organized into distinct haplotypes versus those that are not. Thus, one group of genes, including TFL, showed a low amount of variation in the coding sequence, but high levels of variation organized into distinct haplotypes in the promoter region; other genes showed either low (LFY) or normal (AP3, PI) levels of variation throughout coding sequence and promoter regions. The low level of variation in the LFY floral meristem identity gene is consistent with the idea that natural selection has driven an advantageous LFY mutation to fixation in all A. thaliana populations (directional selection). But selection on the LFY coding region also could be attributable to genetic “hitchhiking” (e.g., directional selection on a nearby locus, resulting in reduced nucleotide variation for a chromosomal region surrounding the selected locus). The size of the affected region depends on LD; thus, it will be larger in a selfing population. TFL1, which appears to function by repressing LFY, is perhaps even more complex. Although the low amount of variation in the coding sequence may suggest directional (purifying) selection (as for LFY), two distinct promoter haplotypes suggest balancing (diversifying) selection acting on the promoter region. Association studies with 21 A. thaliana accessions suggest that the TFL promoter types are associated with different numbers of inflorescence meristems. Moreover, Purugganan presented results from field experiments conducted by his collaborators, the Arabidopsis ecologists Johanna Schmitt and Cynthia Weinig (Brown University, Providence, RI), which suggest that the number of inflorescence branches has an impact on overall plant fitness. Wolfgang Stephan (Ludwig-Maxi-milians-Universität, Munich, Germany) presented data on the effects of recombination and mating system on DNA variation in the tomato genus Lycopersicon. His group has studied patterns of nucleotide diversity in the selfing species L. chmielewski and L. pimpinellifolium and the outcrossers L. peruvianum, L. chilense, and L. hirsutum. Although the amount of within-population polymorphism was much lower in the selfing relative to the outcrossing species, the level of nucleotide diversity was not highly correlated with recombination rate, as it is in Drosophila. Thus, there is a strong effect of mating system on the structure of nucleotide diversity, but it is by no means the only factor. Stephan suggested that demographic factors, such as population subdivision and population size, also have dramatic effects on the structure of nucleotide diversity (Stephan and Langley, 1998). DOES EVOLUTION PLAY FAVORITES? A number of speakers presented evidence that certain loci have been “recruited” for a particular function inde-pendently multiple times, either in different species or within a single species. This pattern has been observed before. For example, Paterson et al. (1995)reported on independent mutations at corresponding (e.g., homeologous) genetic loci among different cereal crop species. Mark Rausher (Duke University, Durham, NC) stated that the reasons for apparently nonrandom patterns of substitution are unclear. Has it occurred simply by chance? Do some genes have excessively high mutation rates (for unknown reasons)? Or is the answer that mutations in many genes impinging on a particular pathway are detrimental or lethal, whereas mutation in one of the genes is allowed? Morning glory (Ipomoea spp) has a tremendous amount of variation in flower color. Rausher's group examined the phylogeny of 40 Ipomoea spp and found that white flower color has evolved independently many times. Furthermore, transitions in flower color were found to be highly asymmetric; for example, there are many cases of purple to white transitions but not of the opposite transition of white to purple. The data collected so far suggest that this pattern may be the result of “knockout” mutations. For example, I. purpurea (normally purple flower) produces some variants at the W locus that produce white flowers in homozygous individuals and white-purple flowers in heterozygotes. W was cloned and found to be homologous with the myb transcription factor An2 in petunia, which is known to be involved in flower color. The white-flowered I. purpurea variants seem to have frameshift deletions and an introduced stop codon in this gene. Rausher's group will test the knockout hypothesis by introducing a wild-type copy of W, presumably the functional gene, into white-flowered plants. There are at least eight genetic routes that can produce white-flowered plants in Ipomoea. Rausher's group is collecting data to determine the genetic changes associated with flower color in 15 independently evolved white-flowered species. They also will test various hypotheses that the pattern of knockout mutations is not random. For example, there may be fewer deleterious pleiotropic effects associated with regulatory genes that are highly specifically expressed only in certain tissues (such as An2, which is expressed specifically in flower petals in petunia) relative to structural genes or other reg-ulatory genes that are more widely expressed throughout the plant. Another hypothesis is that there are fewer deleterious pleiotropic effects associated with mutations in downstream compared with upstream structural genes. The data collected so far suggest that downstream structural genes may be more subject to mutations that persist than are upstream structural genes. Caroline Dean (John Innes Centre, Norwich, UK) gave another example of nonrandom occurrence of mutations at the FRI locus in A. thaliana, which is a major determinant of flowering time (Johanson et al., 2000). The majority of A. thaliana accessions are winter annuals that are late-flowering plants that require vernalization, or a prolonged cold period, to flower. Winter annualism in A. thaliana is chiefly a monogenic trait that maps to the FRI locus. FRI encodes a novel protein with no strong homology with any other known proteins. It is a single gene that appears to confer a vernalization requirement by overriding flowering promotion pathways. The rapid-cycling accessions Columbia and Landsberg erecta carry loss-of-function FRI alleles. Interestingly, early flowering appears to have evolved multiple times in A. thaliana through loss of FRI function. This is quite surprising, because fri mutations account for relatively few vernalization and flowering time mutants obtained through mutagenesis experiments. Further analysis of FRI over a wide range of populations in A. lyrata could prove to be extremely interesting as well. THE HOLY GRAIL: LINKING PHENOTYPE AND GENOTYPE Significant progress has been made toward linking phenotype and genotype for a number of plant traits and genes. In addition to the research on genes involved in flower development and flowering time discussed above, numerous presentations were given linking genes to a wide variety of phenotypic characteristics, such as trichome development, hypocotyl length and seedling development, seed storage lipids, insect and pathogen resistance, and salt tolerance. A few of these presentations are summarized here. Flower Shape Enrico Coen (John Innes Centre) spoke on the evolution of floral characters and what determines whether flowers are asymmetrical, as in Antirrhinum (snapdragon), or symmetrical, as in the Asteraceae (daisies). The wild-type Antirrhinum flower has two dorsal, one ventral, and two lateral petals and emerges from an indeterminate meristem. A peloric mutant of Antirrhinum, which carries a mutation in a gene named CYCLOIDIA, has radially symmetrical flowers comprising five ventral petals produced from a determinate meristem. In the early stages of flower development, when the bud appears radially symmetrical, CYCLOIDIA is expressed quite specifically only in the dorsal petal regions. Daisies and other members of the Asteraceae (composites) have what appear to be radially symmetrical flowers. However, the composite flower consists of inner disc florets and outer ray florets, and although the disc florets are symmetrical, each ray floret is asymmetrical. Coen reported on research on Senecio spp conducted in collaboration with Richard Abbott and Amanda Gillies (University of St. Andrews, UK) and Pilar Cubas (Universidad Autónoma de Madrid, Spain). Senecio vulgaris, a composite native to the United Kingdom, has yellow disc florets but no ray florets. The Italian species S. squalidus, which has yellow disc and ray florets, escaped from the Oxford botanical gardens 300 years ago and is now widespread throughout the United Kingdom. The two species interbred, and a rayed variant of S. vulgaris appeared. Restriction fragment length polymorphism analysis has shown polymorphism cosegregating with the rayed and nonrayed forms of Senecio that is tightly linked to a CYCLOIDIA-like gene, which is expressed only in floral meristem tissue that forms into ray florets. Future work will focus on providing definitive evidence that this gene is responsible for the rayed versus the nonrayed phenotype. In another example, Coen showed a striking mutant of Cosmos, another composite with ray and disc florets, in which the ray florets formed tubes instead of flattened petals. Floral symmetry is thought to have evolved independently many times. It will be very interesting to determine if the Cosmos mutation is associated with a CYCLOIDIA-like gene and if a similar mutant can be created in Senecio. Insect Resistance Juergen Kroymann (Max Planck Institute for Chemical Ecology) provided evidence for almost complete association of phenotype and genotype for genes involved with insect resistance in A. thaliana, from work done in collaboration with others in the Mitchell- Olds group (Kliebenstein et al., 2001a, 2001b; Kliebenstein and Mitchell-Olds, 2001). They identified candidate genes through subtractive hybridization and gene expression analysis from plants damaged by insect herbivores compared with mechanically wounded control plants and analyses of a number of mutants and different accessions of A. thaliana showing variation in insect resistance. They chose to focus attention on genes involved in glucosinolate biosynthesis, because glucosinolates are known to be associated with insect interactions (the breakdown of various glucosinolates leads to the accumulation of toxic products) and glucosinolate composition and accumulation is highly variable among A. thaliana accessions. Quantitative trait loci for insect resistance and aliphatic glucosinolate composition were mapped, and a complete association was found between glucosinolate profiles and the expression of two genes, AOP2 and AOP3. Accessions such as Col-0 that appear to have both genes knocked out, based on sequence analysis and expression studies, accumulate a methylsulfinylalkyl glucosinolate precursor. Accessions found to express a functional AOP2 accumulated an alkenyl glucosinolate and did not express AOP3, and AOP3 was expressed only in those ecotypes that produce hydroxyalkyl glucosinolates. None of the accessions examined was found to express both genes. Work is in progress to determine the extent to which these genes influence insect resistance. Pathogen Resistance Pathogens exert tremendous selection pressure on plants. It is well known that pathogens produce recognition (avirulence) factors that trigger rapid defense signaling cascades in plants. Recognition by the plant is conferred by so-called R (resistance) genes, a large group of genes that share sequence motifs including leucine-rich repeat (LRR), Toll/Interleukin-1 receptor, nucleotide binding (NB), and serine/threonine kinase domains. There is evidence for tremendous sequence exchange that produces a diversity of NB-LRR–type R proteins, which may provide plants with a mechanism for maintaining resistance against rapidly evolving pathogen populations. Although R loci are highly polymorphic, resistance-signaling genes appear to be rather more conserved. Jane Parker (Sainsbury Laboratory, Norwich, UK) presented data on two genes, PAD4 and EDS1, that are required for R gene–mediated resistance to a range of microbial pathogens. These two genes function upstream of defenses mediated by the phenolic signaling molecule salicylic acid and appear to be necessary for the induction of systemic immunity. Both genes encode lipase-like proteins and thus may function by hydrolyzing a lipid-based substrate (Parker et al., 2000). Starch Biosynthesis Barbara Schaal (Washington University, St. Louis, MO) spoke about the search for genes that have played a role in the evolution of carbohydrate metabolism and starch synthesis in cassava (Manihot esculenta). Very little research has been conducted on cassava, although it is an essential staple crop for 600 million people, particularly in Africa. Schaal's group has pinpointed the probable progenitor of the cultivated crop as the wild species M. flabelifolia, the natural range of which is in the Amazon basin (Olsen and Schaal, 2001). Luis Carvalho, a longtime collaborator of Schaal's, has made some striking discoveries about cassava by examining how people in this area grow and use the crop. Unlike most other parts of the world, where cassava is grown as a monoculture and used mainly for its starchy tuber, in the Amazon it is in-tercropped and there are many uses for the plant. Numerous cultivars are grown; some are grown for the leaves as well as the tubers, and others are used to make juice, alcohol, or flour for bread. Analysis of carbohydrate content in the different varieties showed that some of the Amazon cultivars contain very little starch but high levels of free sugars, compared with the levels in world germbank varieties. This was an important discovery because people in other parts of the world are trying to engineer cassava for higher sugar content, thus far with little success. Schaal hypothesized that a mutation in the starch biosynthesis pathway led to a new biochemistry, and she plans to look more carefully at M. esculenta and M. flabelifolia in the Amazon basin to understand the evolution of these genes. In summary, the renewed interest in collaborations among functional and evolutionary geneticists is highly promising for plant genetics research. Functional geneticists can provide information and ideas about genes and mechanisms that may be ecologically significant targets of natural selection. Evolutionary geneticists can provide information on the degree and structure of DNA variation, which can form the basis for the development of new tools, such as mapped recombinant inbred lines and marker densities for LD mapping, and the isolation of new genes involved in development and physiology. A number of plant geneticists began studying the outcrossing species A. lyrata with the idea that it might provide a plant equivalent of Drosophila, which has large random mating populations in which levels of within-population DNA variation are correlated with recombination rate in local chromosomal regions. The structure of variation in A. lyrata may resemble that of Drosophila more than that of A. thaliana does. However, Nordborg pointed out that the main reason Drosophila is a “good model” for population genetics is that it can fly, so there is random mating on a global scale, and that population structure, perhaps more than the type of mating system, has a critical influence on patterns of DNA variation. Thus, it should not be surprising to find that the pattern of DNA variation in A. lyrata does not resemble that of Drosophila very closely. Nonetheless, evolutionary genetics should benefit greatly from more extensive analyses and comparisons of A. lyrata and A. thaliana. Perhaps the joint efforts of plant functional and evolutionary geneticists will redefine what it means to be a “good model” for population genetics. ACKNOWLEDGMENTS I thank Monserrat Aguadé, Magnus Nordborg, Thomas Mitchell-Olds, and Michael Purugganan for helpful discussions and comments. REFERENCES Aguadé, M. ( 2001 ). 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TI - Functional Evolutionary Genetics and Plant AdaptationLinking Phenotype and Genotype
JO - The Plant Cell
DO - 10.1105/tpc.13.6.1249
DA - 2001-06-01
UR - https://www.deepdyve.com/lp/oxford-university-press/functional-evolutionary-genetics-and-plant-adaptationlinking-phenotype-zEdm010uPR
SP - 1249
EP - 1254
VL - 13
IS - 6
DP - DeepDyve
ER -