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  • Review Article
  • Published:

Beyond the thale: comparative genomics and genetics of Arabidopsis relatives

Nature Reviews Genetics volume 16, pages 285–298 (2015)Cite this article

Subjects

Key Points

  • Although Arabidopsis thaliana has traditionally been the primary model organism in plants, several closely related species have recently become a focal point for comparative genomic studies and have led to an expansion of the spectrum of traits under study.

  • The availability and analysis of several high-quality whole-genome sequences from species closely related to A. thaliana within the Brassicaceae family have shed light on the processes of genome evolution in plants, including the emergence and evolution of polyploids.

  • Comparative genomic studies across species of the Brassicaceae family have identified an important role for local gene duplications and deletions in generating evolutionary diversity and diversification of gene function in plants.

  • Several species of the Brassicaceae family are better subjects for field studies than A. thaliana itself. The use of these species as models has enabled researchers to identify the genetic basis for fitness in the real field conditions.

  • The accelerated production of high-quality whole-genome sequences from a range of plant species, and the emergence of genome-editing technologies, will continue to facilitate advances in the study of non-model species in the Brassicaceae family.

Abstract

For decades a small number of model species have rightly occupied a privileged position in laboratory experiments, but it is becoming increasingly clear that our knowledge of biology is greatly improved when informed by a broader diversity of species and evolutionary context. Arabidopsis thaliana has been the primary model organism for plants, benefiting from a high-quality reference genome sequence and resources for reverse genetics. However, recent studies have made a group of species also in the Brassicaceae family and closely related to A. thaliana a focal point for comparative molecular, genomic, phenotypic and evolutionary studies. In this Review, we emphasize how such studies complement continued study of the model plant itself, provide an evolutionary perspective and summarize our current understanding of genetic and phenotypic diversity in plants.

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Figure 1: Phylogeny of Brassicaceae with genome sequences that have been published or that are being processed.
Figure 2: The effects of mating-system shifts.
Figure 3: The evolution of development.

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References

  1. Karl, R. & Koch, M. A. A world-wide perspective on crucifer speciation and evolution: phylogenetics, biogeography and trait evolution in tribe Arabideae. Ann. Bot. 112, 983–1001 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  2. O'Kane, S. L. & Al-Shehbaz, I. A. A synopsis of Arabidopsis (Brassicaceae). Novon 7, 323–327 (1997).

    Article  Google Scholar 

  3. Koch, M., Haubold, B. & Mitchell-Olds, T. Molecular systematics of the Brassicaceae: evidence from coding plastidic matK and nuclear Chs sequences. Am. J. Bot. 88, 534–544 (2001).

    Article  CAS  PubMed  Google Scholar 

  4. Beilstein, M. A., Nagalingum, N. S., Clements, M. D., Manchester, S. R. & Mathews, S. Dated molecular phylogenies indicate a Miocene origin for Arabidopsis thaliana. Proc. Natl Acad. Sci. USA 107, 18724–18728 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Bailey, C. D. et al. Toward a global phylogeny of the Brassicaceae. Mol. Biol. Evol. 23, 2142–2160 (2006).

    Article  CAS  PubMed  Google Scholar 

  6. Al-Shehbaz, I. A., Beilstein, M. A. & Kellogg, E. A. Systematics and phylogeny of the Brassicaceae (Cruciferae): an overview. Plant Systemat Evol. 259, 89–120 (2006).

    Article  Google Scholar 

  7. Couvreur, T. L. et al. Molecular phylogenetics, temporal diversification, and principles of evolution in the mustard family (Brassicaceae). Mol. Biol. Evol. 27, 55–71 (2010).

    Article  CAS  PubMed  Google Scholar 

  8. Franzke, A., Lysak, M. A., Al-Shehbaz, I. A., Koch, M. A. & Mummenhoff, K. Cabbage family affairs: the evolutionary history of Brassicaceae. Trends Plant Sci. 16, 108–116 (2011). This is a very readable, pleasantly non- Arabidopsis -centric summary of evolutionary trends in the Brassicaceae.

    Article  CAS  PubMed  Google Scholar 

  9. Kiefer, M. et al. BrassiBase: introduction to a novel knowledge database on brassicaceae evolution. Plant Cell Physiol. 55, e3 (2014).

    Article  PubMed  CAS  Google Scholar 

  10. Al-Shehbaz, I. A. A generic and tribal synopsis of the Brassicaceae (Cruciferae). Taxon 61, 931–954 (2012).

    Article  Google Scholar 

  11. Lysak, M. A. Live and let die: centromere loss during evolution of plant chromosomes. New Phytol. 203, 1082–1089 (2014).

    Article  Google Scholar 

  12. Lysak, M. A., Koch, M. A., Beaulieu, J. M., Meister, A. & Leitch, I. J. The dynamic ups and downs of genome size evolution in Brassicaceae. Mol. Biol. Evol. 26, 85–98 (2009).

    Article  CAS  PubMed  Google Scholar 

  13. Schranz, M. E., Lysak, M. A. & Mitchell-Olds, T. The ABC's of comparative genomics in the Brassicaceae: building blocks of crucifer genomes. Trends Plant Sci. 11, 535–542 (2006). This review provides a simple system of 24 conserved chromosomal blocks as a foundation for understanding genome evolution in the Brassicaceae.

    Article  CAS  PubMed  Google Scholar 

  14. Oyama, R. K. et al. The shrunken genome of Arabidopsis thaliana. Plant Systemat. Evol. 273, 257–271 (2008).

    Article  CAS  Google Scholar 

  15. Ahmad, S. et al. Genetic dissection of basal defence responsiveness in accessions of Arabidopsis thaliana. Plant Cell Environ. 34, 1191–1206 (2011).

    Article  CAS  PubMed  Google Scholar 

  16. Koch, M. A. & Kiefer, M. Genome evolution among cruciferous plants: a lecture from the comparison of the genetic maps of three diploid species — Capsella rubella, Arabidopsis lyrata subsp. petraea, and A. thaliana. Am. J. Bot. 92, 761–767 (2005).

    Article  PubMed  Google Scholar 

  17. Slotte, T. et al. The Capsella rubella genome and the genomic consequences of rapid mating system evolution. Nature Genet. 45, 831–835 (2013).

    Article  CAS  PubMed  Google Scholar 

  18. Haudry, A. et al. An atlas of over 90,000 conserved noncoding sequences provides insight into crucifer regulatory regions. Nature Genet. 45, 891–898 (2013). This paper represents a major milestone in Brassicaceae comparative genomics, identifying tens of thousands of potential regulatory sequences from the combined analysis of nine genome assemblies.

    Article  CAS  PubMed  Google Scholar 

  19. Piegu, B. et al. Doubling genome size without polyploidization: dynamics of retrotransposition-driven genomic expansions in Oryza australiensis, a wild relative of rice. Genome Res. 16, 1262–1269 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Long, Q. et al. Massive genomic variation and strong selection in Arabidopsis thaliana lines from Sweden. Nature Genet. 45, 884–890 (2013).

    Article  CAS  PubMed  Google Scholar 

  21. Seymour, D. K., Koenig, D., Hagmann, J., Becker, C. & Weigel, D. Evolution of DNA methylation patterns in the Brassicaceae is driven by differences in genome organization. PLoS Genet. 10, e1004785 (2014). This paper reports that there is little conservation of DNA methylation in the Brassicaceae family, even between closely related species, because most methylated sequences are evolutionarily short lived.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  22. Willing, E.-M. et al. Genome expansion of Arabis alpina linked with retrotransposition and reduced symmetric DNA methylation. Nature Plants 1, 14023 (2015).

    Article  CAS  PubMed  Google Scholar 

  23. Dassanayake, M. et al. The genome of the extremophile crucifer Thellungiella parvula. Nature Genet. 43, 913–918 (2011).

    Article  CAS  PubMed  Google Scholar 

  24. Wu, H. J. et al. Insights into salt tolerance from the genome of Thellungiella salsuginea. Proc. Natl Acad. Sci. USA 109, 12219–12224 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Yang, R. L. et al. The reference genome of the halophytic plant Eutrema salsugineum. Front. Plant Sci. 4, 46 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  26. Otto, S. P. The evolutionary consequences of polyploidy. Cell 131, 452–462 (2007).

    Article  CAS  PubMed  Google Scholar 

  27. Comai, L. The advantages and disadvantages of being polyploid. Nature Rev. Genet. 6, 836–846 (2005).

    Article  CAS  PubMed  Google Scholar 

  28. Marhold, K. & Lihova, J. Polyploidy, hybridization and reticulate evolution: lessons from the Brassicaceae. Plant Syst. Evol. 259, 143–174 (2006).

    Article  Google Scholar 

  29. Joly, S., Heenan, P. B. & Lockhart, P. J. A. Pleistocene inter-tribal allopolyploidization event precedes the species radiation of Pachycladon (Brassicaceae) in New Zealand. Mol. Phylogenet. Evol. 51, 365–372 (2009). This study presents evidence for an apparent allopolyploidization event between two unknown species that belonged to two different lineages in the Brassicaceae.

    Article  CAS  PubMed  Google Scholar 

  30. Blanc, G., Barakat, A., Guyot, R., Cooke, R. & Delseny, M. Extensive duplication and reshuffling in the Arabidopsis genome. Plant Cell 12, 1093–1102 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Vision, T. J., Brown, D. G. & Tanksley, S. D. The origins of genomic duplications in Arabidopsis. Science 290, 2114–2117 (2000).

    Article  CAS  PubMed  Google Scholar 

  32. Simillion, C., Vandepoele, K., Van Montagu, M. C., Zabeau, M. & Van de Peer, Y. The hidden duplication past of Arabidopsis thaliana. Proc. Natl Acad. Sci. USA 99, 13627–13632 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Schranz, M. E., Kantama, L., de Jong, H. & Mitchell-Olds, T. Asexual reproduction in a close relative of Arabidopsis: a genetic investigation of apornixis in Boechera (Brassicaceae). New Phytol. 171, 425–438 (2006).

    Article  PubMed  Google Scholar 

  34. Barker, M. S., Vogel, H. & Schranz, M. E. Paleopolyploidy in the Brassicales: analyses of the Cleome transcriptome elucidate the history of genome duplications in Arabidopsis and other Brassicales. Genome Biol. Evol. 1, 391–399 (2009).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  35. Mayrose, I. et al. Recently formed polyploid plants diversify at lower rates. Science 333, 1257 (2011).

    Article  CAS  PubMed  Google Scholar 

  36. Comai, L. et al. Phenotypic instability and rapid gene silencing in newly formed Arabidopsis allotetraploids. Plant Cell 12, 1551–1567 (2000).

    CAS  PubMed  PubMed Central  Google Scholar 

  37. Wang, J. et al. Genomewide nonadditive gene regulation in Arabidopsis allotetraploids. Genetics 172, 507–517 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Schranz, M. E. & Osborn, T. C. Novel flowering time variation in the resynthesized polyploid Brassica napus. J. Hered. 91, 242–246 (2000).

    Article  CAS  PubMed  Google Scholar 

  39. Schranz, M. E. & Osborn, T. C. De novo variation in life-history traits and responses to growth conditions of resynthesized polyploid Brassica napus (Brassicaceae). Am. J. Bot. 91, 174–183 (2004).

    Article  PubMed  Google Scholar 

  40. Lee, H. S. & Chen, Z. J. Protein-coding genes are epigenetically regulated in Arabidopsis polyploids. Proc. Natl Acad. Sci. USA 98, 6753–6758 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Ha, M. et al. Small RNAs serve as a genetic buffer against genomic shock in Arabidopsis interspecific hybrids and allopolyploids. Proc. Natl Acad. Sci. USA 106, 17835–17840 (2009). This study implicates small RNAs as a major factor in the reconciliation of gene expression programmes after allopolyploidization.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Scannell, D. R., Byrne, K. P., Gordon, J. L., Wong, S. & Wolfe, K. H. Multiple rounds of speciation associated with reciprocal gene loss in polyploid yeasts. Nature 440, 341–345 (2006).

    Article  CAS  PubMed  Google Scholar 

  43. Bikard, D. et al. Divergent evolution of duplicate genes leads to genetic incompatibilities within A. thaliana. Science 323, 623–626 (2009).

    Article  CAS  PubMed  Google Scholar 

  44. Song, K., Lu, P., Tang, K. & Osborn, T. C. Rapid genome change in synthetic polyploids of Brassica and its implications for polyploid evolution. Proc. Natl Acad. Sci. USA 92, 7719–7723 (1995).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Xiong, Z., Gaeta, R. T. & Pires, J. C. Homoeologous shuffling and chromosome compensation maintain genome balance in resynthesized allopolyploid Brassica napus. Proc. Natl Acad. Sci. USA 108, 7908–7913 (2011). This paper reports an amazingly fluid genome after allopolyploidization, with rampant aneuploidy, intergenomic and intragenomic rearrangements, chromosome breakage and fusion, rDNA changes and loss of repeat sequences.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Henry, I. M. et al. The BOY NAMED SUE quantitative trait locus confers increased meiotic stability to an adapted natural allopolyploid of Arabidopsis. Plant Cell 26, 181–194 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Yant, L. et al. Meiotic adaptation to genome duplication in Arabidopsis arenosa. Curr. Biol. 23, 2151–2156 (2013).

    Article  CAS  PubMed  Google Scholar 

  48. Hollister, J. D. et al. Genetic adaptation associated with genome-doubling in autotetraploid Arabidopsis arenosa. PLoS Genet. 8, e1003093 (2012).

    Article  PubMed  PubMed Central  Google Scholar 

  49. Wendel, J. F. Genome evolution in polyploids. Plant Mol. Biol. 42, 225–249 (2000).

    Article  CAS  PubMed  Google Scholar 

  50. Wang, X. et al. The genome of the mesopolyploid crop species Brassica rapa. Nature Genet. 43, 1035–1039 (2011).

    Article  CAS  PubMed  Google Scholar 

  51. Liu, S. et al. The Brassica oleracea genome reveals the asymmetrical evolution of polyploid genomes. Nature Commun. 5, 3930 (2014).

    Article  CAS  Google Scholar 

  52. Darwin, C. The Effects of Cross and Self Fertilisation in the Vegetable Kingdom (John Murray, 1876).

    Book  Google Scholar 

  53. Charlesworth, D. & Charlesworth, B. The evolution and breakdown of S-allele systems. Heredity 43, 41–55 (1979).

    Article  Google Scholar 

  54. Baker, H. Self-compatibility and establishment after 'long-distance' dispersal. Evolution 9, 347–349 (1955).

    Google Scholar 

  55. Stebbins, G. Self fertilization and population variability in the higher plants. Am. Nat. 91, 337–354 (1957).

    Article  Google Scholar 

  56. Hedrick, P. W. Adaptive introgression in animals: examples and comparison to new mutation and standing variation as sources of adaptive variation. Mol. Ecol. 22, 4606–4618 (2013).

    Article  PubMed  Google Scholar 

  57. Bateman, A. J. Self-incompatibility systems in angiosperms: III. Cruciferae. Heredity 9, 53–68 (1955).

    Article  Google Scholar 

  58. Takayama, S. & Isogai, A. Self-incompatibility in plants. Annu. Rev. Plant Biol. 56, 467–489 (2005).

    Article  CAS  PubMed  Google Scholar 

  59. Ivanov, R., Fobis-Loisy, I. & Gaude, T. When no means no: guide to Brassicaceae self-incompatibility. Trends Plant Sci. 15, 387–394 (2010).

    Article  CAS  PubMed  Google Scholar 

  60. Chantha, S. C., Herman, A. C., Platts, A. E., Vekemans, X. & Schoen, D. J. Secondary evolution of a self-incompatibility locus in the Brassicaceae genus Leavenworthia. PLoS Biol. 11, e1001560 (2013). This report describes a neofunctionalization event resulting in de novo evolution of self-incompatibility.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Tang, C. et al. The evolution of selfing in Arabidopsis thaliana. Science 317, 1070–1072 (2007).

    Article  CAS  PubMed  Google Scholar 

  62. Sherman-Broyles, S. et al. S locus genes and the evolution of self-fertility in Arabidopsis thaliana. Plant Cell 19, 94–106 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Guo, Y. L. et al. Recent speciation of Capsella rubella from Capsella grandiflora, associated with loss of self-incompatibility and an extreme bottleneck. Proc. Natl Acad. Sci. USA 106, 5246–5251 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Foxe, J. P. et al. Recent speciation associated with the evolution of selfing in Capsella. Proc. Natl Acad. Sci. USA 106, 5241–5245 (2009). References 63 and 64 report on the recent speciation and evolution of self-compatibility of C. rubella.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Busch, J. W., Joly, S. & Schoen, D. J. Demographic signatures accompanying the evolution of selfing in Leavenworthia alabamica. Mol. Biol. Evol. 28, 1717–1729 (2011).

    Article  CAS  PubMed  Google Scholar 

  66. Tsuchimatsu, T., Kaiser, P., Yew, C. L., Bachelier, J. B. & Shimizu, K. K. Recent loss of self-incompatibility by degradation of the male component in allotetraploid Arabidopsis kamchatica. PLoS Genet. 8, e1002838 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Shimizu, K. K., Shimizu-Inatsugi, R., Tsuchimatsu, T. & Purugganan, M. D. Independent origins of self-compatibility in Arabidopsis thaliana. Mol. Ecol. 17, 704–714 (2008).

    Article  CAS  PubMed  Google Scholar 

  68. Nasrallah, J. B., Liu, P., Sherman-Broyles, S., Schmidt, R. & Nasrallah, M. E. Epigenetics mechanisms for breakdown of self-incompatibility in inter-specific hybrids. Genetics 175, 1965–1973 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Schmickl, R., Jorgensen, M. H., Brysting, A. K. & Koch, M. A. The evolutionary history of the Arabidopsis lyrata complex: a hybrid in the amphi-Beringian area closes a large distribution gap and builds up a genetic barrier. BMC Evol. Biol. 10, 98 (2010).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  70. Koch, M. A. & Matschinger, M. Evolution and genetic differentiation among relatives of Arabidopsis thaliana. Proc. Natl Acad. Sci. USA 104, 6272–6277 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Ross-Ibarra, J. et al. Patterns of polymorphism and demographic history in natural populations of Arabidopsis lyrata. PLoS ONE 3, e2411 (2008).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  72. Wright, S. I., Lauga, B. & Charlesworth, D. Subdivision and haplotype structure in natural populations of Arabidopsis lyrata. Mol. Ecol. 12, 1247–1263 (2003).

    Article  CAS  PubMed  Google Scholar 

  73. Clauss, M. J. & Mitchell-Olds, T. Population genetic structure of Arabidopsis lyrata in Europe. Mol. Ecol. 15, 2753–2766 (2006).

    Article  CAS  PubMed  Google Scholar 

  74. Mable, B. K., Robertson, A. V., Dart, S., Di Berardo, C. & Witham, L. Breakdown of self-incompatibility in the perennial Arabidopsis lyrata (Brassicaceae) and its genetic consequences. Evolution 59, 1437–1448 (2005).

    Article  PubMed  Google Scholar 

  75. Griffin, P. C. & Willi, Y. Evolutionary shifts to self-fertilisation restricted to geographic range margins in North American Arabidopsis lyrata. Ecol. Lett. 17, 484–490 (2014).

    Article  CAS  PubMed  Google Scholar 

  76. Willi, Y. & Määttänen, K. The relative importance of factors determining genetic drift: mating system, spatial genetic structure, habitat and census size in Arabidopsis lyrata. New Phytol. 189, 1200–1209 (2011).

    Article  PubMed  Google Scholar 

  77. Willi, Y. & Maattanen, K. Evolutionary dynamics of mating system shifts in Arabidopsis lyrata. J. Evol. Biol. 23, 2123–2131 (2010).

    Article  CAS  PubMed  Google Scholar 

  78. Hoebe, P. N., Stift, M., Tedder, A. & Mable, B. K. Multiple losses of self-incompatibility in North-American Arabidopsis lyrata?: Phylogeographic context and population genetic consequences. Mol. Ecol. 18, 4924–4939 (2009).

    Article  CAS  PubMed  Google Scholar 

  79. Foxe, J. P. et al. Reconstructing origins of loss of self-incompatibility and selfing in North American Arabidopsis lyrata: a population genetic context. Evolution 64, 3495–3510 (2010).

    Article  PubMed  Google Scholar 

  80. Brandvain, Y., Slotte, T., Hazzouri, K. M., Wright, S. I. & Coop, G. Genomic identification of founding haplotypes reveals the history of the selfing species Capsella rubella. PLoS Genet. 9, e1003754 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. Slotte, T., Hazzouri, K. M., Stern, D., Andolfatto, P. & Wright, S. I. Genetic architecture and adaptive significance of the selfing syndrome in Capsella. Evolution 66, 1360–1374 (2012).

    Article  PubMed  PubMed Central  Google Scholar 

  82. St Onge, K. R., Kallman, T., Slotte, T., Lascoux, M. & Palme, A. E. Contrasting demographic history and population structure in Capsella rubella and Capsella grandiflora, two closely related species with different mating systems. Mol. Ecol. 20, 3306–3320 (2011).

    Article  PubMed  Google Scholar 

  83. Hurka, H., Friesen, N., German, D. A., Franzke, A. & Neuffer, B. 'Missing link' species Capsella orientalis and Capsella thracica elucidate evolution of model plant genus Capsella (Brassicaceae). Mol. Ecol. 21, 1223–1238 (2012).

    Article  PubMed  Google Scholar 

  84. Vekemans, X., Poux, C., Goubet, P. M. & Castric, V. The evolution of selfing from outcrossing ancestors in Brassicaceae: what have we learned from variation at the S-locus? J. Evolution Biol. 27, 1372–1385 (2014).

    Article  CAS  Google Scholar 

  85. Charlesworth, D. & Willis, J. H. The genetics of inbreeding depression. Nature Rev. Genet. 10, 783–796 (2009).

    Article  CAS  PubMed  Google Scholar 

  86. Sicard, A. & Lenhard, M. The selfing syndrome: a model for studying the genetic and evolutionary basis of morphological adaptation in plants. Ann. Bot. Lond. 107, 1433–1443 (2011).

    Article  Google Scholar 

  87. Sicard, A. et al. Genetics, evolution, and adaptive significance of the selfing syndrome in the genus Capsella. Plant Cell 23, 3156–3171 (2011). References 81 and 87 report that different strains of C. rubella share several loci for selfing-associated traits, suggesting that these evolved early during the species' history.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Böcher, T. W. Cytological and Embryological Studies in the Amphi-Apomictic Arabis holboellii Complex (Ejnar Minksgaard, 1951).

    Google Scholar 

  89. Koch, M., Al-Shehbaz, I. A. & Mummenhoff, K. Molecular systematics, evolution, and population biology in the mustard family (Brassicaceae). Ann. Mo. Bot. Gard. 90, 151–171 (2003).

    Article  Google Scholar 

  90. Rushworth, C. A., Song, B. H., Lee, C. R. & Mitchell-Olds, T. Boechera, a model system for ecological genomics. Mol. Ecol. 20, 4843–4857 (2011).

    Article  PubMed  PubMed Central  Google Scholar 

  91. Sharbel, T. F., Mitchell-Olds, T. M., Dobes, C., Kantama, L. & de Jong, H. Biogeographic distribution of polyploidy and B chromosomes in the apomictic Boechera holboellii complex. Cytogenet. Genome Res. 109, 283–292 (2005).

    Article  CAS  PubMed  Google Scholar 

  92. Kantama, L. et al. Diploid apomicts of the Boechera holboellii complex display large-scale chromosome substitutions and aberrant chromosomes. Proc. Natl Acad. Sci. USA 104, 14026–14031 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. Mau, M. et al. The conserved chimeric transcript UPGRADE2 is associated with unreduced pollen formation and is exclusively found in apomictic Boechera species. Plant Physiol. 163, 1640–1659 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. Corral, J. M. et al. A conserved apomixis-specific polymorphism is correlated with exclusive exonuclease expression in premeiotic ovules of apomictic Boechera species. Plant Physiol. 163, 1660–1672 (2013). References 93 and 94 report the first molecular factors that were identified to be involved in natural apomixis.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  95. Champagne, C. & Sinha, N. Compound leaves: equal to the sum of their parts? Development 131, 4401–4412 (2004).

    Article  CAS  PubMed  Google Scholar 

  96. Piazza, P. et al. Arabidopsis thaliana leaf form evolved via loss of KNOX expression in leaves in association with a selective sweep. Curr. Biol. 20, 2223–2228 (2010). This study suggests that the simple leaf form of A. thaliana arose by relatively recent strong selection.

    Article  CAS  PubMed  Google Scholar 

  97. Hay, A. S. et al. Cardamine hirsuta: a versatile genetic system for comparative studies. Plant J. 78, 1–15 (2014).

    Article  CAS  PubMed  Google Scholar 

  98. Hay, A. & Tsiantis, M. The genetic basis for differences in leaf form between Arabidopsis thaliana and its wild relative Cardamine hirsuta. Nature Genet. 38, 942–947 (2006).

    Article  CAS  PubMed  Google Scholar 

  99. Bharathan, G. et al. Homologies in leaf form inferred from KNOXI gene expression during development. Science 296, 1858–1860 (2002).

    Article  CAS  PubMed  Google Scholar 

  100. Long, J. A., Moan, E. I., Medford, J. I. & Barton, M. K. A member of the KNOTTED class of homeodomain proteins encoded by the STM gene of Arabidopsis. Nature 379, 66–69 (1996).

    Article  CAS  PubMed  Google Scholar 

  101. Royer, D. L., Wilf, P., Janesko, D. A., Kowalski, E. A. & Dilcher, D. L. Correlations of climate and plant ecology to leaf size and shape: potential proxies for the fossil record. Am. J. Bot. 92, 1141–1151 (2005).

    Article  PubMed  Google Scholar 

  102. Barkoulas, M., Hay, A., Kougioumoutzi, E. & Tsiantis, M. A developmental framework for dissected leaf formation in the Arabidopsis relative Cardamine hirsuta. Nature Genet. 40, 1136–1141 (2008).

    Article  CAS  PubMed  Google Scholar 

  103. Blein, T. et al. A conserved molecular framework for compound leaf development. Science 322, 1835–1839 (2008).

    Article  CAS  PubMed  Google Scholar 

  104. Rubio-Somoza, I. et al. Temporal control of leaf complexity by miRNA-regulated licensing of protein complexes. Curr. Biol. 24, 2714–2719 (2014).

    Article  CAS  PubMed  Google Scholar 

  105. Nakayama, H. et al. Regulation of the KNOX-GA gene module induces heterophyllic alteration in North American lake cress. Plant Cell 26, 4733–4748 (2014). This paper reveals the molecular mechanisms underlying intra-individual differences in leaf shape in a non-model species.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  106. Vlad, D. et al. Leaf shape evolution through duplication, regulatory diversification, and loss of a homeobox gene. Science 343, 780–783 (2014). This study describes the genetic basis for leaf complexity differences among Arabidopsis relatives and highlights the importance of gene duplications during morphological evolution.

    Article  CAS  PubMed  Google Scholar 

  107. Saddic, L. A. et al. The LEAFY target LMI1 is a meristem identity regulator and acts together with LEAFY to regulate expression of CAULIFLOWER. Development 133, 1673–1682 (2006).

    Article  CAS  PubMed  Google Scholar 

  108. Sicard, A. et al. Repeated evolutionary changes of leaf morphology caused by mutations to a homeobox gene. Curr. Biol. 24, 1880–1886 (2014).

    Article  CAS  PubMed  Google Scholar 

  109. Kougioumoutzi, E. et al. SIMPLE LEAF3 encodes a ribosome-associated protein required for leaflet development in Cardamine hirsuta. Plant J. 73, 533–545 (2013).

    Article  CAS  PubMed  Google Scholar 

  110. Weigel, D. Natural variation in Arabidopsis: from molecular genetics to ecological genomics. Plant Physiol. 158, 2–22 (2012).

    Article  CAS  PubMed  Google Scholar 

  111. Guo, Y. L., Todesco, M., Hagmann, J., Das, S. & Weigel, D. Independent FLC mutations as causes of flowering-time variation in Arabidopsis thaliana and Capsella rubella. Genetics 192, 729–739 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  112. Kuittinen, H., Niittyvuopio, A., Rinne, P. & Savolainen, O. Natural variation in Arabidopsis lyrata vernalization requirement conferred by a FRIGIDA indel polymorphism. Mol. Biol. Evol. 25, 319–329 (2008).

    Article  CAS  PubMed  Google Scholar 

  113. Wang, R. H. et al. PEP1 regulates perennial flowering in Arabis alpina. Nature 459, 423–U138 (2009). A gene controlling the singular onset of flowering in A. thaliana is required for cycles of flowering and vegetative growth in A. alpina.

    Article  CAS  PubMed  Google Scholar 

  114. Albani, M. C. et al. PEP1 of Arabis alpina is encoded by two overlapping genes that contribute to natural genetic variation in perennial flowering. PLoS Genet. 8, e1003130 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  115. Bergonzi, S. et al. Mechanisms of age-dependent response to winter temperature in perennial flowering of Arabis alpina. Science 340, 1094–1097 (2013).

    Article  CAS  PubMed  Google Scholar 

  116. Wu, G. et al. The sequential action of miR156 and miR172 regulates developmental timing in Arabidopsis. Cell 138, 750–759 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  117. Zhou, C. M. et al. Molecular basis of age-dependent vernalization in Cardamine flexuosa. Science 340, 1097–1100 (2013). References 115 and 117 describe different ways to 'rewire' regulatory networks controlling age- and temperature-dependent flowering.

    Article  CAS  PubMed  Google Scholar 

  118. Wang, J. W., Czech, B. & Weigel, D. miR156-regulated SPL transcription factors define an endogenous flowering pathway in Arabidopsis thaliana. Cell 138, 738–749 (2009).

    Article  CAS  PubMed  Google Scholar 

  119. Melzer, S. et al. Flowering-time genes modulate meristem determinacy and growth form in Arabidopsis thaliana. Nature Genet. 40, 1489–1492 (2008).

    Article  CAS  PubMed  Google Scholar 

  120. Clauss, M. J. & Koch, M. A. Poorly known relatives of Arabidopsis thaliana. Trends Plant Sci. 11, 449–459 (2006).

    Article  CAS  PubMed  Google Scholar 

  121. Sasidharan, R. et al. Root transcript profiling of two Rorippa species reveals gene clusters associated with extreme submergence tolerance. Plant Physiol. 163, 1277–1292 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  122. Inan, G. et al. Salt cress. A halophyte and cryophyte Arabidopsis relative model system and its applicability to molecular genetic analyses of growth and development of extremophiles. Plant Physiol. 135, 1718–1737 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  123. Turner, T. L., Bourne, E. C., Von Wettberg, E. J., Hu, T. T. & Nuzhdin, S. V. Population resequencing reveals local adaptation of Arabidopsis lyrata to serpentine soils. Nature Genet. 42, 260–263 (2010). This paper reports one of the first uses of short-read resequencing to detect candidates for adaptation in a wild plant.

    Article  CAS  PubMed  Google Scholar 

  124. Kramer, U. Metal hyperaccumulation in plants. Annu. Rev. Plant Biol. 61, 517–534 (2010).

    Article  PubMed  CAS  Google Scholar 

  125. Verbruggen, N., Hermans, C. & Schat, H. Molecular mechanisms of metal hyperaccumulation in plants. New Phytol. 181, 759–776 (2009).

    Article  CAS  PubMed  Google Scholar 

  126. Kazemi-Dinan, A., Thomaschky, S., Stein, R. J., Krämer, U. & Müller, C. Zinc and cadmium hyperaccumulation act as deterrents towards specialist herbivores and impede the performance of a generalist herbivore. New Phytol. 202, 628–639 (2014).

    Article  CAS  PubMed  Google Scholar 

  127. Becher, M., Talke, I. N., Krall, L. & Kramer, U. Cross-species microarray transcript profiling reveals high constitutive expression of metal homeostasis genes in shoots of the zinc hyperaccumulator Arabidopsis halleri. Plant J. 37, 251–268 (2004). The innovative use of microarrays in a close relative of A. thaliana revealed broad trends in gene expression shifts linked to metal hyperaccumulation.

    Article  CAS  PubMed  Google Scholar 

  128. Talke, I. N., Hanikenne, M. & KrÄmer, U. Zinc-dependent global transcriptional control, transcriptional deregulation, and higher gene copy number for genes in metal homeostasis of the hyperaccumulator Arabidopsis halleri. Plant Physiol. 142, 148–167 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  129. Weber, M., Harada, E., Vess, C., Roepenack-Lahaye, E. & Clemens, S. Comparative microarray analysis of Arabidopsis thaliana and Arabidopsis halleri roots identifies nicotianamine synthase, a ZIP transporter and other genes as potential metal hyperaccumulation factors. Plant J. 37, 269–281 (2004).

    Article  CAS  PubMed  Google Scholar 

  130. Willems, G. et al. Quantitative trait loci analysis of mineral element concentrations in an Arabidopsis halleri x Arabidopsis lyrata petraea F2 progeny grown on cadmium-contaminated soil. New Phytol. 187, 368–379 (2010).

    Article  CAS  PubMed  Google Scholar 

  131. Courbot, M. et al. A major quantitative trait locus for cadmium tolerance in Arabidopsis halleri colocalizes with HMA4, a gene encoding a heavy metal ATPase. Plant Physiol. 144, 1052–1065 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  132. Willems, G. et al. The genetic basis of zinc tolerance in the metallophyte Arabidopsis halleri ssp. halleri (Brassicaceae): an analysis of quantitative trait loci. Genetics 176, 659–674 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  133. Frerot, H. et al. Genetic architecture of zinc hyperaccumulation in Arabidopsis halleri: the essential role of QTL x environment interactions. New Phytol. 187, 355–367 (2010).

    Article  CAS  PubMed  Google Scholar 

  134. Hanikenne, M. et al. Evolution of metal hyperaccumulation required cis-regulatory changes and triplication of HMA4. Nature 453, 391–395 (2008). This report describes how a series of changes were needed to increase expression of a transporter, HMA4, that is required for metal hyperaccumulation.

    Article  CAS  PubMed  Google Scholar 

  135. Hanikenne, M. et al. Hard selective sweep and ectopic gene conversion in a gene cluster affording environmental adaptation. PLoS Genet. 9, e1003707 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  136. Craciun, A. R. et al. Variation in HMA4 gene copy number and expression among Noccaea caerulescens populations presenting different levels of Cd tolerance and accumulation. J. Exp. Bot. 63, 4179–4189 (2012).

    Article  CAS  PubMed  Google Scholar 

  137. Deinlein, U. et al. Elevated nicotianamine levels in Arabidopsis halleri roots play a key role in zinc hyperaccumulation. Plant Cell 24, 708–723 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  138. Shahzad, Z. et al. The five AhMTP1 zinc transporters undergo different evolutionary fates towards adaptive evolution to zinc tolerance in Arabidopsis halleri. PLoS Genet. 6, e1000911 (2010).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  139. Mirouze, M. et al. A putative novel role for plant defensins: a defensin from the zinc hyper-accumulating plant, Arabidopsis halleri, confers zinc tolerance. Plant J. 47, 329–342 (2006).

    Article  CAS  PubMed  Google Scholar 

  140. Roux, C. et al. Does speciation between Arabidopsis halleri and Arabidopsis lyrata coincide with major changes in a molecular target of adaptation? PLoS ONE 6, e26872 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  141. Weinig, C., Ewers, B. E. & Welch, S. M. Ecological genomics and process modeling of local adaptation to climate. Curr. Opin. Plant Biol. 18, 66–72 (2014).

    Article  PubMed  Google Scholar 

  142. Kliebenstein, D. J., Kroymann, J. & Mitchell-Olds, T. The glucosinolate–myrosinase system in an ecological and evolutionary context. Curr. Opin. Plant Biol. 8, 264–271 (2005).

    Article  CAS  PubMed  Google Scholar 

  143. Schranz, M. E., Manzaneda, A. J., Windsor, A. J., Clauss, M. J. & Mitchell-Olds, T. Ecological genomics of Boechera stricta: identification of a QTL controlling the allocation of methionine- versus branched-chain amino acid-derived glucosinolates and levels of insect herbivory. Heredity 102, 465–474 (2009).

    Article  CAS  PubMed  Google Scholar 

  144. Prasad, K. V. et al. A gain-of-function polymorphism controlling complex traits and fitness in nature. Science 337, 1081–1084 (2012). This paper describes a prime example of biochemical innovation through gene duplication and divergent selection.

    Article  CAS  PubMed  Google Scholar 

  145. Reintanz, B. et al. bus, a bushy Arabidopsis CYP79F1 knockout mutant with abolished synthesis of short-chain aliphatic glucosinolates. Plant Cell 13, 351–367 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  146. Chen, S. X. et al. CYP79F1 and CYP79F2 have distinct functions in the biosynthesis of aliphatic glucosinolates in Arabidopsis. Plant J. 33, 923–937 (2003).

    Article  CAS  PubMed  Google Scholar 

  147. Koch, M. A. et al. BrassiBase: tools and biological resources to study characters and traits in the Brassicaceae-version 1.1. Taxon 61, 1001–1009 (2012).

    Article  Google Scholar 

  148. Lyons, E. & Freeling, M. How to usefully compare homologous plant genes and chromosomes as DNA sequences. Plant J. 53, 661–673 (2008).

    Article  CAS  PubMed  Google Scholar 

  149. Goodstein, D. M. et al. Phytozome: a comparative platform for green plant genomics. Nucleic Acids Res. 40, D1178–D1186 (2012).

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

The authors thank D. Seymour and four anonymous reviewers for their comments on this manuscript. The authors' work on phenotypic diversity in the Brassicaceae has been supported by a Human Frontier Science Program long-term fellowship (D.K.), Deutsche Forschungsgemeinschaft (German Research Foundation) Priority Program 1529 – 'Adaptomics' (WE 2897; D.W.) and the Max Planck Society (D.W.).

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    Daniel Koenig & Detlef Weigel

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Correspondence to Detlef Weigel.

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FURTHER INFORMATION

BrassiBase

CoGe

Phytozome

PowerPoint slides

Glossary

Copy number variation

Local expansion or contraction through tandem duplication of single-copy sequences or deletion of recently duplicated sequences.

Homeologous

Pertaining to ancestrally related genes or chromosomes that arose through duplication during polyploidization.

Subfunctionalization

The partitioning of ancestral function between recently duplicated gene copies.

Neofunctionalization

The acquisition of a new function by a paralogue that has arisen through gene duplication.

Inbreeding depression

The loss of vigour resulting from mating between related individuals and commensurate loss of heterozygosity.

Sporophytic genetic incompatibility

Incompatibility determined by the parental genotype (that is, the sporophyte).

Haplotype

Genetic variants that are inherited together, usually because of physical linkage on the same chromosome.

Balancing selection

The selective forces that maintain genetic variation for longer than expected by random chance. Well-known examples include negative frequency-dependent selection and overdominance.

Selfing syndrome

The suite of floral modifications associated with the transition from outcrossing to selfing. Most changes are thought to result from reduced investment in pollinator attraction and increased selfing efficiency.

Apomixis

A form of plant asexual reproduction via the formation of seeds.

Life history

The timing of key events such as germination and flowering.

Meristem

Stem cell reservoir in plants.

Metalliferous soils

Soils with high levels of potentially toxic trace elements.

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Koenig, D., Weigel, D. Beyond the thale: comparative genomics and genetics of Arabidopsis relatives. Nat Rev Genet 16, 285–298 (2015). https://doi.org/10.1038/nrg3883

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