A bountiful harvest: genomic insights into crop domestication phenotypes.

Human selection during crop domestication has resulted in remarkable transformations of plant phenotypes, providing a window into the genetic basis of morphological evolution. Recent progress in our understanding of the genetic architecture of novel plant traits has emerged from combining advanced molecular technologies with improved experimental designs, including nested association mapping, genome-wide association studies, population genetic screens for signatures of selection, and candidate gene approaches. These studies reveal a diversity of underlying causative mutations affecting phenotypes important in plant domestication and crop improvement, including coding sequence substitutions, presence/absence and copy number variation, transposon activation leading to novel gene structures and expression patterns, diversification following gene duplication, and polyploidy leading to altered combinatorial capabilities. The genomic regions unknowingly targeted by human selection include both structural and regulatory genes, often with results that propagate through the transcriptome as well as to other levels in the biosynthetic and morphogenetic networks.

[1]  J. Bailey-Serres Microgenomics: genome-scale, cell-specific monitoring of multiple gene regulation tiers. , 2013, Annual review of plant biology.

[2]  P. Tak,et al.  The resolution of inflammation , 2012, Nature Reviews Immunology.

[3]  Saravanaraj N. Ayyampalayam,et al.  The banana (Musa acuminata) genome and the evolution of monocotyledonous plants , 2012, Nature.

[4]  Qian Qian,et al.  Control of grain size, shape and quality by OsSPL16 in rice , 2012, Nature Genetics.

[5]  M. Hufford,et al.  Historical genomics of North American maize , 2012, Proceedings of the National Academy of Sciences.

[6]  R. Guigó,et al.  The genome of melon (Cucumis melo L.) , 2012, Proceedings of the National Academy of Sciences.

[7]  Nathan M. Springer,et al.  Reshaping of the maize transcriptome by domestication , 2012, Proceedings of the National Academy of Sciences.

[8]  J. Chen,et al.  Genome-wide genetic changes during modern breeding of maize , 2012, Nature Genetics.

[9]  Peter J. Bradbury,et al.  Maize HapMap2 identifies extant variation from a genome in flux , 2012, Nature Genetics.

[10]  T. Close,et al.  Genome wide linkage disequilibrium in Chinese asparagus bean (Vigna. unguiculata ssp. sesquipedialis) germplasm: implications for domestication history and genome wide association studies , 2012, Heredity.

[11]  Xun Xu,et al.  Comparative population genomics of maize domestication and improvement , 2012, Nature Genetics.

[12]  Doreen Ware,et al.  ZmCCT and the genetic basis of day-length adaptation underlying the postdomestication spread of maize , 2012, Proceedings of the National Academy of Sciences.

[13]  Xianran Li,et al.  Presence of tannins in sorghum grains is conditioned by different natural alleles of Tannin1 , 2012, Proceedings of the National Academy of Sciences.

[14]  Cheng-Ting Yeh,et al.  Parallel domestication of the Shattering1 genes in cereals , 2012, Nature Genetics.

[15]  Y. Xing,et al.  Evolution and Association Analysis of Ghd7 in Rice , 2012, PloS one.

[16]  M. Stitt,et al.  Genome-wide association mapping of leaf metabolic profiles for dissecting complex traits in maize , 2012, Proceedings of the National Academy of Sciences.

[17]  M. Navascués,et al.  Evolution of Neutral and Flowering Genes along Pearl Millet (Pennisetum glaucum) Domestication , 2012, PloS one.

[18]  J. Dvorak,et al.  The origin of spelt and free-threshing hexaploid wheat. , 2012, The Journal of heredity.

[19]  T. Giraud,et al.  New Insight into the History of Domesticated Apple: Secondary Contribution of the European Wild Apple to the Genome of Cultivated Varieties , 2012, PLoS genetics.

[20]  Daniel W. A. Buchan,et al.  The tomato genome sequence provides insights into fleshy fruit evolution , 2012, Nature.

[21]  H. Sommer,et al.  Molecular genetic basis of pod corn (Tunicate maize) , 2012, Proceedings of the National Academy of Sciences.

[22]  Y. Vigouroux,et al.  Evolutionary history of pearl millet (Pennisetum glaucum [L.] R. Br.) and selection on flowering genes since its domestication. , 2012, Molecular biology and evolution.

[23]  D. Laurie,et al.  Copy Number Variation Affecting the Photoperiod-B1 and Vernalization-A1 Genes Is Associated with Altered Flowering Time in Wheat (Triticum aestivum) , 2012, PloS one.

[24]  James C. Schnable,et al.  Escape from Preferential Retention Following Repeated Whole Genome Duplications in Plants , 2012, Front. Plant Sci..

[25]  T. Zerjal,et al.  Maize genetic diversity and association mapping using transposable element insertion polymorphisms , 2012, Theoretical and Applied Genetics.

[26]  Edward S. Buckler,et al.  Crop genomics: advances and applications , 2011, Nature Reviews Genetics.

[27]  M. Purugganan,et al.  Natural selection in gene-dense regions shapes the genomic pattern of polymorphism in wild and domesticated rice. , 2012, Molecular biology and evolution.

[28]  Qian Qian,et al.  Genome-wide association study of flowering time and grain yield traits in a worldwide collection of rice germplasm , 2011, Nature Genetics.

[29]  Huanming Yang,et al.  Draft genome sequence of pigeonpea (Cajanus cajan), an orphan legume crop of resource-poor farmers , 2011, Nature Biotechnology.

[30]  D. Soltis,et al.  Polyploidy and Genome Evolution , 2012, Springer Berlin Heidelberg.

[31]  Lin Fang,et al.  Resequencing 50 accessions of cultivated and wild rice yields markers for identifying agronomically important genes , 2011, Nature Biotechnology.

[32]  P. Wittkopp,et al.  Cis-regulatory elements: molecular mechanisms and evolutionary processes underlying divergence , 2011, Nature Reviews Genetics.

[33]  Lex E. Flagel,et al.  Parallel up-regulation of the profilin gene family following independent domestication of diploid and allopolyploid cotton (Gossypium) , 2011, Proceedings of the National Academy of Sciences.

[34]  Lijun Luo,et al.  Natural variation in GS5 plays an important role in regulating grain size and yield in rice , 2011, Nature Genetics.

[35]  Jeffrey Ross-Ibarra,et al.  Genetic Architecture of Maize Kernel Composition in the Nested Association Mapping and Inbred Association Panels1[W] , 2011, Plant Physiology.

[36]  Jeffrey Ross-Ibarra,et al.  Identification of a functional transposon insertion in the maize domestication gene tb1 , 2011, Nature Genetics.

[37]  Edward S. Buckler,et al.  Distinct Genetic Architectures for Male and Female Inflorescence Traits of Maize , 2011, PLoS genetics.

[38]  Cécile Huneau,et al.  Duplication and partitioning in evolution and function of homoeologous Q loci governing domestication characters in polyploid wheat , 2011, Proceedings of the National Academy of Sciences.

[39]  Mark H. Wright,et al.  Genome-wide association mapping reveals a rich genetic architecture of complex traits in Oryza sativa , 2011, Nature communications.

[40]  M. Fontaine,et al.  Cereal Domestication and Evolution of Branching: Evidence for Soft Selection in the Tb1 Orthologue of Pearl Millet (Pennisetum glaucum [L.] R. Br.) , 2011, PloS one.

[41]  J. Reif,et al.  Genome-wide association mapping of agronomic traits in sugar beet , 2011, Theoretical and Applied Genetics.

[42]  M. Yamasaki,et al.  Artificial selection for a green revolution gene during japonica rice domestication , 2011, Proceedings of the National Academy of Sciences.

[43]  R. Hudson,et al.  Two Evolutionary Histories in the Genome of Rice: the Roles of Domestication Genes , 2011, PLoS genetics.

[44]  Claude W. dePamphilis,et al.  Ancestral polyploidy in seed plants and angiosperms , 2011, Nature.

[45]  Robert J. Elshire,et al.  A Robust, Simple Genotyping-by-Sequencing (GBS) Approach for High Diversity Species , 2011, PloS one.

[46]  Peter J. Bradbury,et al.  Genome-wide nested association mapping of quantitative resistance to northern leaf blight in maize , 2011, Proceedings of the National Academy of Sciences.

[47]  J. Rogers,et al.  Crop genome sequencing: lessons and rationales. , 2011, Trends in plant science.

[48]  William T B Thomas,et al.  INTERMEDIUM-C, a modifier of lateral spikelet fertility in barley, is an ortholog of the maize domestication gene TEOSINTE BRANCHED 1 , 2011, Nature Genetics.

[49]  Peter J. Bradbury,et al.  Genome-wide association study of quantitative resistance to southern leaf blight in the maize nested association mapping population , 2011, Nature Genetics.

[50]  Peter J. Bradbury,et al.  Genome-wide association study of leaf architecture in the maize nested association mapping population , 2011, Nature Genetics.

[51]  Q. Qian,et al.  Genetic Control of a Transition from Black to Straw-White Seed Hull in Rice Domestication1[C][W][OA] , 2011, Plant Physiology.

[52]  Detlef Weigel,et al.  Transposable elements and small RNAs contribute to gene expression divergence between Arabidopsis thaliana and Arabidopsis lyrata , 2011, Proceedings of the National Academy of Sciences.

[53]  Edward S. Buckler,et al.  Genetic structure and domestication history of the grape , 2011, Proceedings of the National Academy of Sciences.

[54]  David A. Rasmussen,et al.  Contributions of Flowering Time Genes to Sunflower Domestication and Improvement , 2011, Genetics.

[55]  J. Doebley,et al.  Genetic signals of origin, spread, and introgression in a large sample of maize landraces , 2010, Proceedings of the National Academy of Sciences.

[56]  J. Dvorak,et al.  Nucleotide diversity maps reveal variation in diversity among wheat genomes and chromosomes , 2010, BMC Genomics.

[57]  Ryan A. Rapp,et al.  Gene expression in developing fibres of Upland cotton (Gossypium hirsutum L.) was massively altered by domestication , 2010, BMC Biology.

[58]  Bo Wang,et al.  Resequencing of 31 wild and cultivated soybean genomes identifies patterns of genetic diversity and selection , 2010, Nature Genetics.

[59]  Qifa Zhang,et al.  Genome-wide association studies of 14 agronomic traits in rice landraces , 2010, Nature Genetics.

[60]  Peter Tiffin,et al.  Pervasive gene content variation and copy number variation in maize and its undomesticated progenitor. , 2010, Genome research.

[61]  K. Olsen,et al.  Genetic perspectives on crop domestication. , 2010, Trends in plant science.

[62]  J. Specht,et al.  Artificial selection for determinate growth habit in soybean , 2010, Proceedings of the National Academy of Sciences.

[63]  Jared L. Strasburg,et al.  The Role of Recently Derived FT Paralogs in Sunflower Domestication , 2010, Current Biology.

[64]  Haibao Tang,et al.  Domestication and plant genomes. , 2010, Current opinion in plant biology.

[65]  E. Vollbrecht,et al.  Evidence of selection at the ramosa1 locus during maize domestication , 2010, Molecular ecology.

[66]  T. Lacombe,et al.  Evolution of the VvMybA gene family, the major determinant of berry colour in cultivated grapevine (Vitis vinifera L.) , 2010, Heredity.

[67]  Tomas W. Fitzgerald,et al.  Origins and functional impact of copy number variation in the human genome , 2010, Nature.

[68]  Kazuhiko Sugimoto,et al.  Molecular cloning of Sdr4, a regulator involved in seed dormancy and domestication of rice , 2010, Proceedings of the National Academy of Sciences.

[69]  Nicola Pecchioni,et al.  CBF gene copy number variation at Frost Resistance-2 is associated with levels of freezing tolerance in temperate-climate cereals , 2010, Theoretical and Applied Genetics.

[70]  C. Howe,et al.  Molecular Basis of the Waxy Endosperm Starch Phenotype in Broomcorn Millet (Panicum miliaceum L.) , 2010, Molecular biology and evolution.

[71]  林鹭 Duplication and independent selection of cell-wall invertase genes GIF1 and OsCIN1 during rice evolution and domestication , 2010 .

[72]  N. Goncharov,et al.  Molecular characterization of vernalization loci VRN1 in wild and cultivated wheats , 2010, BMC Plant Biology.

[73]  C. Helliwell,et al.  RESEARCH ARTICLE Open Access Research article Sequence variation and selection of small RNAs in domesticated rice , 2022 .

[74]  K. Matsushima,et al.  Waxy strains of three amaranth grains raised by different mutations in the coding region , 2010, Molecular Breeding.

[75]  K. Olsen,et al.  Novel Phr1 mutations and the evolution of phenol reaction variation in US weedy rice (Oryza sativa). , 2009, The New phytologist.

[76]  Luis Herrera-Estrella,et al.  The Palomero Genome Suggests Metal Effects on Domestication , 2009, Science.

[77]  Dawn H. Nagel,et al.  The B73 Maize Genome: Complexity, Diversity, and Dynamics , 2009, Science.

[78]  Barbara Pickersgill fls Domestication of plants revisited – Darwin to the present day , 2009 .

[79]  Patrick S. Schnable,et al.  Maize Inbreds Exhibit High Levels of Copy Number Variation (CNV) and Presence/Absence Variation (PAV) in Genome Content , 2009, PLoS genetics.

[80]  L. Fan,et al.  Post-Domestication Selection in the Maize Starch Pathway , 2009, PloS one.

[81]  M. Fitzgerald,et al.  The origin and evolution of fragrance in rice (Oryza sativa L.) , 2009, Proceedings of the National Academy of Sciences.

[82]  Lex E. Flagel,et al.  Parallel expression evolution of oxidative stress-related genes in fiber from wild and domesticated diploid and polyploid cotton (Gossypium) , 2009, BMC Genomics.

[83]  M. McMullen,et al.  Genetic Properties of the Maize Nested Association Mapping Population , 2009, Science.

[84]  Peter J. Bradbury,et al.  The Genetic Architecture of Maize Flowering Time , 2009, Science.

[85]  C. Bustamante,et al.  Evolutionary History of GS3, a Gene Conferring Grain Length in Rice , 2009, Genetics.

[86]  Lex E. Flagel,et al.  Gene duplication and evolutionary novelty in plants. , 2009, The New phytologist.

[87]  Y. Vigouroux,et al.  Association Studies Identify Natural Variation at PHYC Linked to Flowering Time and Morphological Variation in Pearl Millet , 2009, Genetics.

[88]  S. Boué,et al.  Recent amplification and impact of MITEs on the genome of grapevine (Vitis vinifera L.) , 2009, Genome biology and evolution.

[89]  Y. Okumoto,et al.  Multiple alleles at Early flowering 1 locus making variation in the basic vegetative growth period in rice (Oryza sativa L.) , 2009, Theoretical and Applied Genetics.

[90]  Pamela S Soltis,et al.  The role of hybridization in plant speciation. , 2009, Annual review of plant biology.

[91]  Z. Chen,et al.  Altered circadian rhythms regulate growth vigor in hybrids and allopolyploids , 2008, Nature.

[92]  André Beló,et al.  Allelic genome structural variations in maize detected by array comparative genome hybridization , 2009, Theoretical and Applied Genetics.

[93]  J. Dubcovsky,et al.  Genetic and Molecular Characterization of the VRN2 Loci in Tetraploid Wheat1[W][OA] , 2008, Plant Physiology.

[94]  Ryan A. Rapp,et al.  Evolutionary genetics of genome merger and doubling in plants. , 2008, Annual review of genetics.

[95]  D. Luo,et al.  Genetic control of rice plant architecture under domestication , 2008, Nature Genetics.

[96]  S. Knapp,et al.  A Genomic Scan for Selection Reveals Candidates for Genes Involved in the Evolution of Cultivated Sunflower (Helianthus annuus)[W] , 2008, The Plant Cell Online.

[97]  Marta Matvienko,et al.  Multiple paleopolyploidizations during the evolution of the Compositae reveal parallel patterns of duplicate gene retention after millions of years. , 2008, Molecular biology and evolution.

[98]  Xianran Li,et al.  Control of a key transition from prostrate to erect growth in rice domestication , 2008, Nature Genetics.

[99]  Chung-I Wu,et al.  Independent Losses of Function in a Polyphenol Oxidase in Rice: Differentiation in Grain Discoloration between Subspecies and the Role of Positive Selection under Domestication[W] , 2008, The Plant Cell Online.

[100]  Wei He,et al.  Control of rice grain-filling and yield by a gene with a potential signature of domestication , 2008, Nature Genetics.

[101]  J. Casacuberta,et al.  Genome-Wide Analysis of the “Cut-and-Paste” Transposons of Grapevine , 2008, PloS one.

[102]  S. Carroll Evo-Devo and an Expanding Evolutionary Synthesis: A Genetic Theory of Morphological Evolution , 2008, Cell.

[103]  Kaworu Ebana,et al.  Deletion in a gene associated with grain size increased yields during rice domestication , 2008, Nature Genetics.

[104]  Lex E. Flagel,et al.  Parallel Domestication, Convergent Evolution and Duplicated Gene Recruitment in Allopolyploid Cotton , 2008, Genetics.

[105]  Lei Wang,et al.  Natural variation in Ghd7 is an important regulator of heading date and yield potential in rice , 2008, Nature Genetics.

[106]  L. Kruglyak,et al.  Breeding Designs for Recombinant Inbred Advanced Intercross Lines , 2008, Genetics.

[107]  S. Tanksley,et al.  Regulatory change in YABBY-like transcription factor led to evolution of extreme fruit size during tomato domestication , 2008, Nature Genetics.

[108]  L. Fan,et al.  Molecular evidence for post-domestication selection in the Waxy gene of Chinese waxy maize , 2008, Molecular Breeding.

[109]  E. Stockinger,et al.  A Retrotransposon-Mediated Gene Duplication Underlies Morphological Variation of Tomato Fruit , 2008, Science.

[110]  H. Kanamori,et al.  Barley grain with adhering hulls is controlled by an ERF family transcription factor gene regulating a lipid biosynthesis pathway , 2008, Proceedings of the National Academy of Sciences.

[111]  M. Chapman,et al.  Molecular insights into the evolution of crop plants. , 2008, American journal of botany.

[112]  Lex E. Flagel,et al.  The Evolution of Spinnable Cotton Fiber Entailed Prolonged Development and a Novel Metabolism , 2008, PLoS genetics.

[113]  P. Leroy,et al.  Soft selective sweep near a gene that increases plant height in wheat , 2008, Molecular ecology.

[114]  M. McMullen,et al.  Genetic Design and Statistical Power of Nested Association Mapping in Maize , 2008, Genetics.

[115]  M. Chapman,et al.  Crop evolution: from genetics to genomics. , 2007, Current opinion in genetics & development.

[116]  W. Zhai,et al.  TAC1, a major quantitative trait locus controlling tiller angle in rice. , 2007, The Plant journal : for cell and molecular biology.

[117]  Ryan D. Hernandez,et al.  Genome-Wide Patterns of Nucleotide Polymorphism in Domesticated Rice , 2007, PLoS genetics.

[118]  Jan Dvorak,et al.  Genome Plasticity a Key Factor in the Success of Polyploid Wheat Under Domestication , 2007, Science.

[119]  J. Coyne,et al.  THE LOCUS OF EVOLUTION: EVO DEVO AND THE GENETICS OF ADAPTATION , 2007, Evolution; international journal of organic evolution.

[120]  Wei Huang,et al.  A QTL for rice grain width and weight encodes a previously unknown RING-type E3 ubiquitin ligase , 2007, Nature Genetics.

[121]  Sarah Hake,et al.  The heterochronic maize mutant Corngrass1 results from overexpression of a tandem microRNA , 2007, Nature Genetics.

[122]  J. Lupski Structural variation in the human genome. , 2007, The New England journal of medicine.

[123]  M. Thomas,et al.  White grapes arose through the mutation of two similar and adjacent regulatory genes. , 2007, The Plant journal : for cell and molecular biology.

[124]  A. Amores,et al.  Rapid and cost-effective polymorphism identification and genotyping using restriction site associated DNA (RAD) markers. , 2007, Genome research.

[125]  Andreas Graner,et al.  Six-rowed barley originated from a mutation in a homeodomain-leucine zipper I-class homeobox gene , 2007, Proceedings of the National Academy of Sciences.

[126]  Bruce D. Smith,et al.  The Molecular Genetics of Crop Domestication , 2006, Cell.

[127]  H. Dooner,et al.  Remarkable variation in maize genome structure inferred from haplotype diversity at the bz locus , 2006, Proceedings of the National Academy of Sciences.

[128]  F. Feltus,et al.  Many gene and domain families have convergent fates following independent whole-genome duplication events in Arabidopsis, Oryza, Saccharomyces and Tetraodon. , 2006, Trends in genetics : TIG.

[129]  Jonathan F. Wendel,et al.  Polyploidy and Crop Improvement , 2006 .

[130]  Carene Rizzon,et al.  Striking Similarities in the Genomic Distribution of Tandemly Arrayed Genes in Arabidopsis and Rice , 2006, PLoS Comput. Biol..

[131]  Bin Han,et al.  GS3, a major QTL for grain length and weight and minor QTL for grain width and thickness in rice, encodes a putative transmembrane protein , 2006, Theoretical and Applied Genetics.

[132]  B. Gill,et al.  Molecular Characterization of the Major Wheat Domestication Gene Q , 2006, Genetics.

[133]  Takuji Sasaki,et al.  The map-based sequence of the rice genome , 2005, Nature.

[134]  Steven G. Schroeder,et al.  The Effects of Artificial Selection on the Maize Genome , 2005, Science.

[135]  Robert J Henry,et al.  The gene for fragrance in rice. , 2005, Plant biotechnology journal.

[136]  K. Hammer Das Domestikationssyndrom , 1984, Die Kulturpflanze.

[137]  H. Hirochika,et al.  Association of VvmybA1 gene expression with anthocyanin production in grape (Vitis vinifera) skin-color mutants , 2005 .

[138]  Kazuyuki Doi,et al.  Ehd1, a B-type response regulator in rice, confers short-day promotion of flowering and controls FT-like gene expression independently of Hd1. , 2004, Genes & development.

[139]  O. Anderson,et al.  Sequencing of the Triticum monococcum Hardness locus reveals good microcolinearity with rice , 2004, Molecular Genetics and Genomics.

[140]  M. Schranz,et al.  De novo variation in life-history traits and responses to growth conditions of resynthesized polyploid Brassica napus (Brassicaceae). , 2004, American journal of botany.

[141]  R. Shapley,et al.  The Wheat VRN2 Gene Is a Flowering Repressor Down-Regulated by Vernalization , 2004 .

[142]  Jonathan F. Wendel,et al.  Genome evolution in polyploids , 2004, Plant Molecular Biology.

[143]  A. Paterson Polyploidy, evolutionary opportunity, and crop adaptation , 2005, Genetica.

[144]  Douglas E. Soltis,et al.  Advances in the study of polyploidy since Plant speciation , 2003 .

[145]  L. Yan,et al.  Positional cloning of the wheat vernalization gene VRN1 , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[146]  Edward S. Buckler,et al.  Dwarf8 polymorphisms associate with variation in flowering time , 2001, Nature Genetics.

[147]  The Arabidopsis Genome Initiative Analysis of the genome sequence of the flowering plant Arabidopsis thaliana , 2000, Nature.

[148]  Jody Hey,et al.  The limits of selection during maize domestication , 1999, Nature.

[149]  J. Doebley,et al.  The evolution of apical dominance in maize , 1997, Nature.

[150]  Andrew H. Paterson,et al.  Convergent Domestication of Cereal Crops by Independent Mutations at Corresponding Genetic Loci , 1995, Science.

[151]  J. Doebley,et al.  Genetic and morphological analysis of a maize-teosinte F2 population: implications for the origin of maize. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[152]  N. Pierce Origin of Species , 1914, Nature.