title: Selection on grain shattering genes and rates of rice domestication.
abstract: Molecular cloning of major quantitative trait loci (QTLs) responsible for the reduction of rice grain shattering, a hallmark of cereal domestication, provided opportunities for in-depth investigation of domestication processes. Here, we studied nucleotide variation at the shattering loci, sh4 and qSH1, for cultivated rice, Oryza sativa ssp. indica and Oryza sativa ssp. japonica, and the wild progenitors, Oryza nivara andOryza rufipogon. The nonshattering sh4 allele was fixed in all rice cultivars, with levels of sequence polymorphism significantly reduced in both indica and japonica cultivars relative to the wild progenitors. The sh4 phylogeny together with the neutrality tests and coalescent simulations suggested that sh4 had a single origin and was fixed by artificial selection during the domestication of rice. Selection on qSH1 was not detected in indica and remained unclear in japonica. Selection on sh4 could be strong enough to have driven its fixation in a population of cultivated rice within a period of c. 100 yr. The slow fixation of the nonshattering phenotype observed at the archeological sites might be a result of relatively weak selection on mutations other than sh4 in early rice cultivation. The fixation of sh4 could have been achieved later through strong selection for the optimal phenotype.
authors.affiliation: State Key Laboratory of Systematic and Evolutionary Botany, Institute of Botany, Chinese Academy of Sciences, Beijing, 100093, China.
authors.forename: Lin-Bin
authors.initials: LB
authors.lastname: Zhang
authors.affiliation: State Key Laboratory of Systematic and Evolutionary Botany, Institute of Botany, Chinese Academy of Sciences, Beijing, 100093, China.
authors.forename: Qihui
authors.initials: Q
authors.lastname: Zhu
authors.affiliation: State Key Laboratory of Systematic and Evolutionary Botany, Institute of Botany, Chinese Academy of Sciences, Beijing, 100093, China.
authors.forename: Zhi-Qiang
authors.initials: ZQ
authors.lastname: Wu
authors.affiliation: Department of Ecology and Evolutionary Biology, University of California, Irvine, CA 92697, USA.
authors.forename: Jeffrey
authors.initials: J
authors.lastname: Ross-Ibarra
authors.affiliation: Department of Ecology and Evolutionary Biology, University of California, Irvine, CA 92697, USA.
authors.forename: Brandon S
authors.initials: BS
authors.lastname: Gaut
authors.affiliation: State Key Laboratory of Systematic and Evolutionary Botany, Institute of Botany, Chinese Academy of Sciences, Beijing, 100093, China.
authors.forename: Song
authors.initials: S
authors.lastname: Ge
authors.affiliation: Department of Plant Biology, Michigan State University, East Lansing, MI 48824, USA.
authors.forename: Tao
authors.initials: T
authors.lastname: Sang
mesh_terms: D000383:Agriculture / Q000266:history; D001483:Base Sequence; D001947:Breeding / Q000266:history; D003001:Cloning, Molecular; D018744:DNA, Plant / Q000235:genetics; D017343:Genes, Plant; D014644:Genetic Variation; D049690:History, Ancient; D008957:Models, Genetic; D012275:Oryza / Q000145:classification / Q000235:genetics* / Q000254:growth & development / Q000266:history; D010641:Phenotype; D010802:Phylogeny; D020641:Polymorphism, Single Nucleotide; D040641:Quantitative Trait Loci; D012641:Selection, Genetic; D013997:Time Factors
chemical_list: D018744:DNA, Plant
references.citation: Allaby RG, Fuller DQ, Brown TA. 2008. The genetic expectations of a protracted model for the origins of domesticated crops. Proceedings of the National Academy of Sciences, USA 105: 13982-13986.
references.citation: Azhaguvel P, Komatsuda T. 2007. A phylogenetic analysis based on nucleotide sequence of a marker linked to the brittle rachis locus indicates a diphyletic origin of barley. Annals of Botany 100: 1009-1015.
references.citation: Caicedo A, Williamson S, Hernandez RD, Boyko A, Fledel-Alon A, York T, Polato N, Olsen K, Nielsen R, McCouch SR et al . 2007. Genome-wide patterns of nucleotide polymorphism in domesticated rice. PLoS Genetics 3: e163.
references.citation: Cheng C, Motohashi R, Tsuchimoto S, Fukuta Y, Ohtsubo H, Ohstubo E. 2003. Polyphyletic origin of cultivated rice: based on the interspersion pattern of SINEs. Molecular Biology and Evolution 20: 67-75.
references.citation: Clark RM, Linton E, Messing J, Doebley JF. 2004. Pattern of diversity in the genomic region near the maize domestication gene tb1. Proceedings of the National Academy of Sciences, USA 101: 700-707.
references.citation: Das A, Mohanty S, Stephan W. 2004. Inferring the population structure and demography of Drosophila ananassae from multilocus data. Genetics 168: 1975-1985.
references.citation: Diamond J. 2002. Evolution, consequences and future of plant and animal domestication. Nature 418: 700-707.
references.citation: Doebley JF, Gaut BS, Smith BD. 2006. The molecular genetics of crop domestication. Cell 127: 1309-1321.
references.citation: Feng Q, Zhang Y, Hao P, Wang S, Fu G, Huang Y, Li Y, Zhu J, Liu Y, Hu X et al . 2002. Sequence and analysis of rice chromosome 4. Nature 420: 316-320.
references.citation: Fu YX, Li WH. 1993. Statistical tests of neutrality of mutations. Genetics 133: 693-709.
references.citation: Fuller DQ. 2007. Contrasting patterns in crop domestication and domestication rates: recent archaeobotanical insights from the Old World. Annals of Botany 100: 903-924.
references.citation: Fuller DQ, Qin L, Zheng Y, Zhao Z, Chen X, Hosoya LA, Sun GP. 2009. The domestication process and domestication rate in rice: spikelet bases from the lower Yangtze. Science 323: 1607-1610.
references.citation: Gao LZ, Innan H. 2008. Nonindependent domestication of the two rice subspecies, Oryza sativa ssp. indica and ssp. japonica, demonstrated by multilocus microsatellites. Genetics 179: 965-976.
references.citation: Garris A, Tai T, Coburn J, Kresovich S, McCouch SR. 2005. Genetic structure and diversity in Oryza sativa L. Genetics 169: 1631-1638.
references.citation: Gaut BS, Morton BR, McCaig BC, Clegg MT. 1996. Substitution rate comparisons between grasses and palms: synonymous rate differences at the nuclear gene Adh parallel rate differences at the plastid gene rbcL. Proceedings of the National Academy of Sciences, USA 93: 10274-10279.
references.citation: Harlan JR. 1992. Crops and man, 2nd edn. Madison, WI, USA: American Society of Agronomy and Crop Science Society of America.
references.citation: Hu CH, Kao KN, Chang CC. 1964. Histological and genetic studies on shedding and lodging habits of rice plants. Botanical Bulletin of Academia Sinica 5: 170-180.
references.citation: Huelsenbeck JP, Ronquist F. 2001. MrBayes: Bayesian inference of phylogeny. Bioinformatics 17: 754-755.
references.citation: Innan H, Kim Y. 2004. Pattern of polymorphism after strong artificial selection in a domestication event. Proceedings of the National Academy of Sciences, USA 101: 10667-10672.
references.citation: Ji H-S, Chu S-H, Jiang W, Cho Y-I, Hahn J-H, Eun M-Y, McCouch SR, Koh H-J. 2006. Characterization and mapping of a shattering mutant in rice that corresponds to a block of domestication genes. Genetics 173: 995-1005.
references.citation: Kaplan NL, Hudson RR, Langley CH. 1989. The ‘hitchhiking effect’ revisited. Genetics 123: 887-899.
references.citation: Khush GS. 1997. Origin, dispersal, cultivation and variation of rice. Plant Molecular Biology 35: 25-34.
references.citation: Kimura M, Ohta T. 1969. The average number of generations until fixation of a mutant gene in a finite population. Genetics 61: 763-771.
references.citation: Komatsuda T, Pourkheirandish M, He C, Azhaguvel P, Kanamori H, Perovic D, Stein N, Graner A, Wicker T, Tagiri A et al . 2007. Six-rowed barley originated from a mutation in a homeodomain-leucine zipper I-class homeobox gene. Proceedings of the National Academy of Sciences, USA 104: 1424-1429.
references.citation: Konishi S, Ebana K, Izawa T. 2008. Inference of the japonica rice domestication process from the distribution of six functional nucleotide polymorphisms of domestication-related genes in various landraces and modern cultivars. Plant Cell Physiology 49: 1283-1293.
references.citation: Konishi S, Izawa T, Lin SY, Ebana K, Fukuta Y, Sasaki T, Yano M. 2006. An SNP caused loss of seed shattering during rice domestication. Science 312: 1392-1396.
references.citation: Kovach MJ, Sweeney MT, McCouch SR. 2007. New insights into the history of rice domestication. Trends in Genetics 23: 578-587.
references.citation: Li C, Zhou A, Sang T. 2006a. Rice domestication by reducing shattering. Science 311: 1936-1939.
references.citation: Li C, Zhou A, Sang T. 2006b. Genetic analysis of rice domestication syndrome with the wild annual species, Oryza nivara. New Phytologist 170: 185-194.
references.citation: Lin Z, Griffith M, Li X, Zhu Z, Tan L, Fu Y, Zhang W, Wang X, Xie D, Sun C. 2007. Origin of seed shattering in rice (Oryza sativa L.). Planta 226: 11-20.
references.citation: Londo JP, Chiang YC, Hung KH, Chiang TY, Schaal BA. 2006. Phylogeography of Asian wild rice, Oryza rufipogon, reveals multiple independent domestications of cultivated rice, Oryza sativa. Proceedings of the National Academy of Sciences, USA 103: 9578-9583.
references.citation: Matsuoka Y, Vigouroux Y, Goodman MM, Sanchez GJ, Buckler E, Doebley J. 2002. A single domestication for maize shown by multilocus microsatellite genotyping. Proceedings of the National Academy of Sciences, USA 99: 6080-6084.
references.citation: Morrell PL, Clegg MT. 2007. Genetic evidence for a second domestication of barley (Hordeum vulgare) east of the Fertile Crescent. Proceedings of the National Academy of Sciences, USA 104: 3289-3294.
references.citation: Nei M, Li WH. 1979. Mathematical model for studying genetic variation in terms of restriction endonucleases. Proceedings of the National Academy of Sciences, USA 76: 5269-5273.
references.citation: Nielsen R. 2001. Statistical tests of selective neutrality in the age of genomics. Heredity 86: 641-647.
references.citation: Onishi K, Takagi K, Kontani M, Tanaka T, Sano Y. 2007. Different patterns of genealogical relationships found in the two major QTL causing reduction of seed shattering during rice domestication. Genome 50: 757-766.
references.citation: Posada D, Crandall KA. 1998. Modeltest: testing the model of DNA substitution. Bioinformatics 14: 817-818.
references.citation: Purugganan MD, Fuller DQ. 2009. The nature of selection during plant domestication. Nature 457: 843-848.
references.citation: Rieseberg LH, Raymond O, Rosenthal DM, Lai Z, Livingstone K, Nakazato T, Durphy JL, Schwarzbach AE, Donovan LA, Lexer C. 2003. Major ecological transitions in wild sunflowers facilitated by hybridization. Science 301: 1211-1216.
references.citation: Ronquist F, Huelsenbeck JP. 2003. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572-1574.
references.citation: Ross-Ibarra J, Gaut BS. 2008. Multiple domestications do not appear monophyletic. Proceedings of the National Academy of Sciences, USA 105: E105.
references.citation: Rozas J, Sánchez-Delbarrio JC, Messeguer X, Rozas R. 2003. DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19: 2496-2497.
references.citation: Sakamoto Y, Ishiguro M, Kitagawa G. 1986. Akaike Information Criterion Statistics. Tokyo, Japan/Dordrecht, the Netherlands: KTK Scientific Publishers/D. Reidel Publishing.
references.citation: Sang T. 2009. Genes and mutations underlying domestication transitions in grasses. Plant Physiology 149: 63-70.
references.citation: Sang T, Ge S. 2007a. The puzzle of rice domestication. Journal of Integrative Plant Biology 49: 760-768.
references.citation: Sang T, Ge S. 2007b. Genetics and phylogenetics of rice domestication. Current Opinion in Genetics & Development 17: 533-538.
references.citation: Second G. 1982. Origin of the genic diversity of cultivated rice (Oryza spp.): study of the polymorphism scored at 40 isozyme loci. Japanese Journal of Genetics 57: 25-57.
references.citation: Stephan W, Wiehe T, Lenz MW. 1992. The effect of strongly selected substitutions on neutral polymorphism - analytical results based on diffusion-theory. Theoretical Population Biology 41: 237-254.
references.citation: Sweeney M, McCouch S. 2007. The complex history of the domestication of rice. Annals of Botany 100: 951-957.
references.citation: Sweeney MT, Thomson MJ, Cho YG, Park YJ, Williamson SH, Bustamante CD, McCouch SR. 2007. Global dissemination of a single mutation conferring white pericarp in rice. PLoS Genetics 3: 1418-1425.
references.citation: Sweeney MT, Thomson MJ, Pfeil BE, McCouch SR. 2006. Caught red-handed: Rc encodes a basic helix-loop-helix protein conditioning red pericarp in rice. Plant Cell 18: 283-294.
references.citation: Swofford DL. 2002. paup*: phylogenetic analysis using parsimony (*and other methods), version 4.0. Sunderland, MA, USA: Sinauer Associates.
references.citation: Tajima F. 1989. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123: 585-595.
references.citation: Tanno KI, Willcox G. 2006. How fast was wild wheat domesticated? Science 311: 1886.
references.citation: Tenaillon MI, U’Ren J, Tenaillon O, Brandon SG. 2004. Selection versus demography: a multilocus investigation of the domestication process in maize. Molecular Biology and Evolution 21: 1214-1225.
references.citation: Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG. 1997. The Clustal X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research 25: 4876-4882.
references.citation: Thornton KR, Jensen JD. 2007. Controlling the false positive rate in multilocus genome scans for selection. Genetics 175: 737-750.
references.citation: Vaughan DA, Lu B-R, Tomooka N. 2008. The evolving story of rice evolution. Plant Science 174: 394-408.
references.citation: Wang RL, Stec A, Hey J, Lukens L, Doebley J. 1999. The limits of selection during maize domestication. Nature 398: 236-239.
references.citation: Watterson GA. 1975. On the number of segregating sites in genetical models without recombinations. Theoretical Population Biology 7: 256-276.
references.citation: White S, Doebley J. 1999. The molecular evolution of terminal ear1, a regulatory gene in the genus Zea. Genetics 153: 1455-1462.
references.citation: Wright SI, Charlesworth B. 2004. The HKA test revisited: a maximum-likelihood-ratio test of the standard neutral model. Genetics 168: 1071-1076.
references.citation: Wright SI, Bi IV, Schroeder SG, Yamasaki M, Doebley JF, McMullen MD, Gaut BS. 2005. The effects of artificial selection on the maize genome. Science 308: 1308-1310.
references.citation: Yamasaki M, Tenaillon MI, Vroh Bi I, Schroeder SG, Sanchez-Villeda H, Doebley JF, Brandon SG, McMullen MD. 2005. A large-scale screen for artificial selection in maize identifies candidate agronomic loci for domestication and crop improvement. Plant Cell 17: 2859-2872.
references.citation: Zeder MA. 2006. Central questions in the domestication of plants and animals. Evolutionary Anthropology: Issues, News, and Reviews 15: 105-117.
references.citation: Zhao Z, Piperno DR. 2000. Late Pleistocene/Holocene environments in the middle Yangtze River Valley, China and rice (Oryza sativa L.) domestication: the phytolith evidence. Geoarchaeology 15: 203-222.
references.citation: Zhao Q, Zhang Y, Cheng Z, Chen M, Wang S, Feng Q, Huang Y, Li Y, Tang Y, Zhou B et al . 2002. A fine physical map of the rice chromosome 4. Genome Research 12: 817-823.
references.citation: Zhu Q, Ge S. 2005. Phylogenetic relationships among A-genome species of the genus Oryza revealed by intron sequences of four nuclear genes. New Phytologist 167: 249-265.
references.citation: Zhu Q, Zheng X, Luo J, Gaut BS, Ge S. 2007. Multilocus analysis of nucleotide variation of Oryza sativa and its wild relatives: severe bottleneck during domestication of rice. Molecular Biology and Evolution 24: 875-888.
references.citation: Zong Y, Chen Z, Innes JB, Chen C, Wang Z, Wang H. 2007. Fire and flood management of coastal swamp enabled first rice paddy cultivation in east China. Nature 449: 459-462.