7 Genomics, Adaptation, and the Evolution of Plant Form
Kristen Shepard
Department of Biological Sciences, Barnard College, New York, NY, USA
Search for more papers by this authorKristen Shepard
Department of Biological Sciences, Barnard College, New York, NY, USA
Search for more papers by this authorAbstract
A central question in the evolution of plant development is to understand how modifications of plant form contribute to adaptation within a species. Molecular population genomics and quantitative genetics offer complementary tools for answering this question. Quantitative trait locus mapping identifies genetic variation that underlies variation in plant form, while analyses of nucleotide diversity illuminate the evolutionary history of developmentally relevant genes. By combining these tools with developmental genetic characterization of natural sequence variants and with ecological experiments that test adaptive hypotheses, recent studies have begun to tease apart the genetic basis of adaptation. This chapter includes an overview of genome-wide mapping and population genomic methods, as well as case studies detailing the application of these techniques in root development, plant domestication, phytochrome-mediated phenotypic variation, and regulation of flowering time.
References
- Adzhubei, I.A., Schmidt, S., Peshkin, L., et al. (2010) A method and server for predicting damaging missense mutations. Nature Methods, 7, 248–249.
- Alonso-Blanco, C., Aarts, M.G.M., Bentsink, L., et al. (2009) What has natural variation taught us about plant development, physiology, and adaptation? Plant Cell, 21, 1877–1896.
- Amasino, R. (2010) Seasonal and developmental timing of flowering. The Plant Journal, 61, 1001–1013.
- Balasubramanian, S., Sureshkumar, S., Agrawal, M., et al. (2006) The PHYTOCHROME C photoreceptor gene mediates natural variation in flowering and growth responses of Arabidopsis thaliana . Nature Genetics, 38, 711–715.
- Beaumont, M.A. & Balding, D.J. (2004) Identifying adaptive genetic divergence among populations from genome scans. Molecular Ecology, 13, 969–980.
- Becker, A. & Lange, M. (2010) VIGS - genomics goes functional. Trends in Plant Science, 15, 1–4.
- Beuchat, J., Li, S.W., Ragni, L., et al. (2010) A hyperactive quantitative trait locus allele of Arabidopsis BRX contributes to natural variation in root growth vigor. Proceedings of the National Academy of Sciences of the United States of America, 107, 8475–8480.
- Blázquez, M.A. & Weigel, D. (1999) Independent regulation of flowering by Phytochrome B and gibberellins in Arabidopsis . Plant Physiology, 120, 1025–1032.
- Borevitz, J.O., Maloof, J.N., Lutes, J., et al. (2002) Quantitative trait loci controlling light and hormone response in two accessions of Arabidopsis thaliana . Genetics, 160, 683–696.
- Bossdorf, O., Richards, C.L. & Pigliucci, M. (2008) Epigenetics for ecologists. Ecology Letters, 11, 106–115.
- Buckler, E.S., Holland, J.B., Bradbury, P.J., et al. (2009) The genetic architecture of maize flowering time. Science, 325, 714–718.
- Bustamante, C.D., Nielsen, R., Sawyer, S.A., et al. (2002) The cost of inbreeding in Arabidopsis . Nature, 416, 531–534.
- Caicedo, A.L., Stinchcombe, J.R., Olsen, K.M., et al. (2004) Epistatic interaction between Arabidopsis FRI and FLC flowering time genes generates a latitudinal cline in a life history trait. Proceedings of the National Academy of Sciences of the United States of America, 101, 15670–15675.
- Chapman, M.A., Pashley, C.H., Wenzler, J., et al. (2008) A genomic scan for selection reveals candidates for genes involved in the evolution of cultivated sunflower (Helianthus annuus). Plant Cell, 20, 2931–2945.
- Clack, T., Shokry, A., Moffet, M., et al. (2009) Obligate heterodimerization of Arabidopsis Phytochromes C and E and interaction with the PIF3 basic helix-loop-helix transcription factor. Plant Cell, 21, 786–799.
- Clark, R.M., Wagler, T.N., Quijada, P., et al. (2006) A distant upstream enhancer at the maize domestication gene tb1 has pleiotropic effects on plant and inflorescent architecture. Nature Genetics, 38, 594–597.
- Clark, R.M., Schweikert, G., Toomajian, C., et al. (2007) Common sequence polymorphisms shaping genetic diversity in Arabidopsis thaliana . Science, 317, 338–342.
- Cong, B., Barrero, L.S. & Tanksley, S.D. (2008) Regulatory change in YABBY-like transcription factor led to evolution of extreme fruit size during tomato domestication. Nature Genetics, 40, 800–804.
- Cong, B., Liu, J.P. & Tanksley, S.D. (2002) Natural alleles at a tomato fruit size quantitative trait locus differ by heterochronic regulatory mutations. Proceedings of the National Academy of Sciences of the United States of America, 99, 13606–13611.
- Cubas, P., Vincent, C. & Coen, E. (1999) An epigenetic mutation responsible for natural variation in floral symmetry. Nature, 401, 157–161.
- Deschamps, S. & Campbell, M.A. (2010) Utilization of next-generation sequencing platforms in plant genomics and genetic variant discovery. Molecular Breeding, 25, 553–570.
- Ehrenreich, I.M., Hanzawa, Y., Chou, L., et al. (2009) Candidate gene association mapping of Arabidopsis flowering time. Genetics, 183, 325–335.
- Engelmann, K. & Purugganan, M. (2006) The molecular evolutionary ecology of plant development: flowering time in Arabidopsis thaliana . Advances in Botanical Research: Incorporating Advances in Plant Pathology, 44, 507–526.
- Fay, J.C. & Wu, C.I. (2000) Hitchhiking under positive Darwinian selection. Genetics, 155, 1405–1413.
- Filiault, D.L., Wessinger, C.A., Dinneny, J.R., et al. (2008) Amino acid polymorphisms in Arabidopsis phytochrome B cause differential responses to light. Proceedings of the National Academy of Sciences of the United States of America, 105, 3157–3162.
- Fitz Gerald, J.N., Lehti-Shiu, M.D., Ingram, P.A., et al. (2006) Identification of quantitative trait loci that regulate Arabidopsis root system size and plasticity. Genetics, 172, 485–498.
- Flowers, J.M., Hanzawa, Y., Hall, M.C., et al. (2009) Population genomics of the Arabidopsis thaliana flowering time gene network. Molecular Biology and Evolution, 26, 2475–2486.
- Franklin, K.A. & Quail, P.H. (2010) Phytochrome functions in Arabidopsis development. Journal of Experimental Botany, 61, 11–24.
- Frewen, B.E., Chen, T.H.H., Howe, G.T., et al. (2000) Quantitative trait loci and candidate gene mapping of bud set and bud flush in Populus . Genetics, 154, 837–845.
- Fu, Y.X. & Li, W.H. (1993) Statistical tests of neutrality of mutations. Genetics, 133, 693–709.
- García-Gil, M.R., Mikkonen, M. & Savolainen, O. (2003) Nucleotide diversity at two phytochrome loci along a latitudinal cline in Pinus sylvestris . Molecular Ecology, 12, 1195–1206.
- Gaut, B.S. & Long, A.D. (2003) The lowdown on linkage disequilibrium. Plant Cell, 15, 1502–1506.
- Gore, M.A., Chia, J.-M., Elshire, R.J., et al. (2009) A first-generation haplotype map of maize. Science, 326, 1115–1117.
- He, Y. (2009) Control of the transition to flowering by chromatin modifications. Molecular Plant, 2, 554–564.
- Hilscher, J., Schlötterer, C. & Hauser, M.T. (2009) A single amino acid replacement in ETC2 shapes trichome patterning in natural Arabidopsis populations. Current Biology, 19, 1747–1751.
- Holland, J.B. (2007) Genetic architecture of complex traits in plants. Current Opinion in Plant Biology, 10, 156–161.
- Hudson, R.R., Kreitman, M. & Aguade, M. (1987) A test of neutral molecular evolution based on nucleotide data. Genetics, 116, 153–159.
- Ikeda, H., Fujii, N. & Setoguchi, H. (2009) Molecular evolution of phytochromes in Cardamine nipponica (Brassicaceae) suggests the involvement of PHYE in local adaptation. Genetics, 182, 603–614.
- Ingvarsson, P.K., Garcia, M.V., Luquez, V., et al. (2008) Nucleotide polymorphism and phenotypic associations within and around the phytochrome B2 locus in European aspen (Populus tremula, Salicaceae). Genetics, 178, 2217–2226.
- Jiménez-Gómez, J.M., Alonso-Blanco, C., Borja, A., et al. (2007) Quantitative genetic analysis of flowering time in tomato. Genome, 50, 303–315.
- Johannes, F., Porcher, E., Teixeira, F.K., et al. (2009) Assessing the impact of transgenerational epigenetic variation on complex traits. PLoS Genetics, 5, e1000530.
- Johanson, U., West, J., Lister, C., et al. (2000) Molecular analysis of FRIGIDA, a major determinant of natural variation in Arabidopsis flowering time. Science, 290, 344–347.
- Jones, N., Ougham, H., Thomas, H., et al. (2009) Markers and mapping revisited: finding your gene. New Phytologist, 183, 935–966.
-
Kimura, M. (1983) The Neutral Theory of Molecular Evolution, Cambridge University Press, Cambridge.
10.1017/CBO9780511623486 Google Scholar
- Kliebenstein, D. (2009) Quantitative genomics: Analyzing intraspecific variation using global gene expression polymorphisms or eQTLs. Annual Review of Plant Biology, 60, 93–114.
- Kover, P.X., Valdar, W., Trakalo, J., et al. (2009) A multiparent advanced generation inter-cross to fine-map quantitative traits in Arabidopsis thaliana . PLoS Genetics 5, e1000551.
- Lempe, J., Balasubramanian, S., Sureshkumar, S., et al. (2005) Diversity of flowering responses in wild Arabidopsis thaliana strains. PLoS Genetics 1, e6.
- Li, W.-H. (1997) Molecular Evolution, Sinauer Associates, Inc., Sunderland, MA.
- Librado, P. & Rozas, J. (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics, 25, 1451–1452.
- Loudet, O., Gaudon, V., Trubuil, A., et al. (2005) Quantitative trait loci controlling root growth and architecture in Arabidopsis thaliana confirmed by heterogeneous inbred family. Theoretical and Applied Genetics, 110, 742–753.
- Luquez, V., Hall, D., Albrectsen, B.R., et al. (2008) Natural phenological variation in aspen (Populus tremula): the SwAsp collection. Tree Genetics & Genomes, 4, 279–292.
- Mackay, T.F.C. (2001) Quantitative trait loci in Drosophila . Nature Reviews Genetics, 2, 11–20.
- Maloof, J.N., Borevitz, J.O., Dabi, T., et al. (2001) Natural variation in light sensitivity of Arabidopsis . Nature Genetics, 29, 441–446.
- Mathews, S. & McBreen, K. (2008) Phylogenetic relationships of B-related phytochromes in the Brassicaceae: Redundancy and the persistence of phytochrome D. Molecular Phylogenetics and Evolution, 49, 411–423.
- McDonald, J.H. & Kreitman, M. (1991) Adaptive protein evolution at the Adh locus in Drosophila . Nature, 351, 652–654.
- McNally, K.L., Childs, K.L., Bohnert, R., et al. (2009) Genomewide SNP variation reveals relationships among landraces and modern varieties of rice. Proceedings of the National Academy of Sciences of the United States of America, 106, 12273–12278.
- Mitchell-Olds, T. & Schmitt, J. (2006) Genetic mechanisms and evolutionary significance of natural variation in Arabidopsis . Nature, 441, 947–952.
- Monte, E., Alonso, J.M., Ecker, J.R., et al. (2003) Isolation and characterization of phyC mutants in Arabidopsis reveals complex crosstalk between phytochrome signaling pathways. Plant Cell, 15, 1962–1980.
- Mouchel, C.F., Briggs, G.C. & Hardtke, C.S. (2004) Natural genetic variation in Arabidopsis identifies BREVIS RADIX, a novel regulator of cell proliferation and elongation in the root. Genes & Development, 18, 700–714.
- Mouchel, C.F., Osmont, K.S. & Hardtke, C.S. (2006) BRX mediates feedback between brassinosteroid levels and auxin signalling in root growth. Nature, 443, 458–461.
- Myles, S., Peiffer, J., Brown, P.J., et al. (2009) Association mapping: Critical considerations shift from genotyping to experimental design. Plant Cell, 21, 2194–2202.
- Nordborg, M., Hu, T.T., Ishino, Y., et al. (2005) The pattern of polymorphism in Arabidopsis thaliana . PloS Biology, 3, e196.
- Nordborg, M. & Innan, H. (2003) The genealogy of sequences containing multiple sites subject to strong selection in a subdivided population. Genetics, 163, 1201–1213.
- Nordborg, M. & Weigel, D. (2008) Next-generation genetics in plants. Nature, 456, 720–723.
- Oleksyk, T.K., Smith, M.W. & O'Brien, S.J. (2010) Genome-wide scans for footprints of natural selection. Philosophical Transactions of the Royal Society B-Biological Sciences, 365, 185–205.
- Olsen, K.M., Womack, A., Garrett, A.R., et al. (2002) Contrasting evolutionary forces in the Arabidopsis thaliana floral developmental pathway. Genetics, 160, 1641–1650.
- Ossowski, S., Schwab, R. & Weigel, D. (2008) Gene silencing in plants using artificial microRNAs and other small RNAs. Plant Journal, 53, 674–690.
- Przeworski, M. (2002) The signature of positive selection at randomly chosen loci. Genetics, 160, 1179–1189.
- Putterill, J., Laurie, R. & Macknight, R. (2004) It's time to flower: the genetic control of flowering time. Bioessays, 26, 363–73.
- Richards, E.J. (2011) Natural epigenetic variation in plant species: a view from the field. Current Opinion in Plant Biology, 14, 204–209.
- Rockwell, N.C., Su, Y.-S. & Lagarias, J.C. (2006) Phytochrome structure and signaling mechanisms. Annual Review of Plant Biology, 57, 837–858.
- Ross-Ibarra, J., Morrell, P.L. & Gaut, B.S. (2007) Plant domestication, a unique opportunity to identify the genetic basis of adaptation. Proceedings of the National Academy of Sciences of the United States of America, 104, 8641–8648.
- Saïdou, A.A., Mariac, C., Luong, V., et al. (2009) Association studies identify natural variation at PHYC linked to flowering time and morphological variation in pearl millet. Genetics, 182, 899–910.
- Salvi, S. & Tuberosa, R. (2005) To clone or not to clone plant QTLs: present and future challenges. Trends in Plant Science, 10, 297–304.
- Samis, K.E., Heath, K.D. & Stinchcombe, J.R. (2008) Discordant longitudinal clines in flowering time and PHYTOCHROME C in Arabidopsis thaliana . Evolution, 62, 2971–2983.
- Schlötterer, C. (2002) Towards a molecular characterization of adaptation in local populations. Current Opinion in Genetics & Development, 12, 683–687.
-
Schlötterer, C. & Dieringer, D. (2005) A novel test statistic for the identification of local selective sweeps based on microsatellite gene diversity. In: Selective Sweep (ed. D Niurminsky). pp. 55–64. Kluwer Academic Publishers, Boston.
10.1111/j.1365-294X.2006.03190.x Google Scholar
- Schneeberger, K. & Weigel, D. (2011) Fast-forward genetics enabled by new sequencing technologies. Trends in Plant Science, 16, 282–288.
- Shepard, K.A. (2007) The molecular population genetics of shoot development in Arabidopsis thaliana . Genetica, 129, 19–36.
- Shepard, K.A. & Purugganan, M.D. (2003) Molecular population genetics of the Arabidopsis CLAVATA2 region: The genomic scale of variation and selection in a selfing species. Genetics, 163, 1083–1095.
- Shindo, C., Bernasconi, G. & Hardtke, C.S. (2007) Natural genetic variation in Arabidopsis: tools, traits and prospects for evolutionary ecology. Annals of Botany, 99, 1043–1054.
- Shindo, C., Bernasconi, G. & Hardtke, C.S. (2008) Intraspecific competition reveals conditional fitness effects of single gene polymorphism at the Arabidopsis root growth regulator BRX . New Phytologist, 180, 71–80.
- Stenøien, H.K., Fenster, C.B., Kuittinen, H., et al. (2002) Quantifying latitudinal clines to light responses in natural populations of Arabidopsis thaliana (Brassicaceae). American Journal of Botany, 89, 1604–1608.
- Stinchcombe, J.R. & Hoekstra, H.E. (2008) Combining population genomics and quantitative genetics: finding the genes underlying ecologically important traits. Heredity, 100, 158–170.
- Tajima, F. (1983) Evolutionary relationship of DNA sequences in finite populations. Genetics, 105, 437–460.
- Tajima, F. (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics, 123, 585–595.
- Toomajian, C., Hu, T.T., Aranzana, M.J., et al. (2006) A nonparametric test reveals selection for rapid flowering in the Arabidopsis genome. PLoS Biology 4, e137.
- Tuinstra, M.R., Ejeta, G. & Goldsbrough, P.B. (1997) Heterogeneous inbred family (HIF) analysis: a method for developing near-isogenic lines that differ at quantitative trait loci. Theoretical and Applied Genetics, 95, 1005–1011.
- Van Eeuwijk, F.A., Bink, M.C.A.M., Chenu, K., et al. (2010) Detection and use of QTL for complex traits in multiple environments. Current Opinion in Plant Biology, 13, 193–205.
- Vaughn, M.W., Tanurdžíc, M., Lippman, Z., et al. (2007) Epigenetic natural variation in Arabidopsis thaliana . PLoS Biology, 5, e174.
- Wang, R.L. & Hey, J. (1996) The speciation history of Drosophila pseudoobscura and close relatives: Inferences from DNA sequence variation at the Period locus. Genetics, 144, 1113–1126.
- Watterson, G.A. (1975) Number of segregating sites in genetical models without recombination. Theoretical Population Biology, 7, 256–276.
- Weigel, D. & Mott, R. (2009) The 1001 Genomes Project for Arabidopsis thaliana . Genome Biology, 10, 107.
- Weigel, D. & Nordborg, M. (2005) Natural variation in Arabidopsis. How do we find the causal genes? Plant Physiology, 138, 567–568.
- Weinig, C., Ungerer, M.C., Dorn, L.A., et al. (2002) Novel loci control variation in reproductive timing in Arabidopsis thaliana in natural environments. Genetics, 162, 1875–1884.
- Weinthal, D., Tovkach, A., Zeevi, V., et al. (2010) Genome editing in plant cells by zinc finger nucleases. Trends in Plant Science, 15, 308–321.
- Werner, J.D., Borevitz, J.O., Warthmann, N., et al. (2005) Quantitative trait locus mapping and DNA array hybridization identify an FLM deletion as a cause for natural flowering-time variation. Proceedings of the National Academy of Sciences of the United States of America, 102, 2460–2465.
- White, G.M., Hamblin, M.T. & Kresovich, S. (2004) Molecular evolution of the phytochrome gene family in sorghum: Changing rates of synonymous and replacement evolution. Molecular Biology and Evolution, 21, 716–723.
- Wright, S.I., Bi, I.V., Schroeder, S.G., et al. (2005) The effects of artificial selection on the maize genome. Science, 308, 1310–1314.
- Wright, S.I. & Charlesworth, B. (2004) The HKA test revisited: a maximum-likelihood-ratio test of the standard neutral model. Genetics, 168, 1071–1076.
- Wright, S.I. & Gaut, B.S. (2005) Molecular population genetics and the search for adaptive evolution in plants. Molecular Biology and Evolution, 22, 506–519.
- Yamamoto, Y.Y. & Obokata, J. (2008) PPDB: a plant promoter database. Nucleic Acids Research, 36, D977–D981.
- Yu, J., Holland, J.B., McMullen, M.D., et al. (2008) Genetic design and statistical power of nested association mapping in maize. Genetics, 178, 539–551.
- Yu, J., Pressoir, G., Briggs, W.H., et al. (2006) A unified mixed-model method for association mapping that accounts for multiple levels of relatedness. Nature Genetics, 38, 203–208.
- Zhou, L., Zhang, J., Yan, J., et al. (2011) Two transposable element insertions are causative mutations for the major domestication gene teosinte branched 1 in modern maize. Cell Research, 21, 1267--1270.
Browse other articles of this reference work: