Molecular cloning of Sdr4, a regulator involved in seed dormancy and domestication of rice

Seed dormancy provides a strategy for flowering plants to survive adverse natural conditions. It is also an important agronomic trait affecting grain yield, quality, and processing performance. We cloned a rice quantitative trait locus, Sdr4, which contributes substantially to differences in seed dormancy between japonica (Nipponbare) and indica (Kasalath) cultivars. Sdr4 expression is positively regulated by OsVP1, a global regulator of seed maturation, and in turn positively regulates potential regulators of seed dormancy and represses the expression of postgerminative genes, suggesting that Sdr4 acts as an intermediate regulator of dormancy in the seed maturation program. Japonica cultivars have only the Nipponbare allele (Sdr4-n), which endows reduced dormancy, whereas both the Kasalath allele (Srd4-k) and Sdr4-n are widely distributed in the indica group, indicating prevalent introgression. Srd4-k also is found in the wild ancestor Oryza rufipogon, whereas Sdr4-n appears to have been produced through at least two mutation events from the closest O. rufipogon allele among the accessions examined. These results are discussed with respect to possible selection of the allele during the domestication process.

[1]  M. Yano,et al.  Molecular identification of a major quantitative trait locus, qLTG3–1, controlling low-temperature germinability in rice , 2008, Proceedings of the National Academy of Sciences.

[2]  SnRK,et al.  In vitro reconstitution of an abscisic acid signalling pathway , 2009 .

[3]  R. Finkelstein,et al.  Abscisic Acid Signaling in Seeds and Seedlings Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.010441. , 2002, The Plant Cell Online.

[4]  S. Mccouch,et al.  New insights into the history of rice domestication. , 2007, Trends in genetics : TIG.

[5]  M. Yano,et al.  DNA changes tell us about rice domestication. , 2009, Current opinion in plant biology.

[6]  T. Hattori,et al.  Regulation of the Osem gene by abscisic acid and the transcriptional activator VP1: analysis of cis-acting promoter elements required for regulation by abscisic acid and VP1. , 1995, The Plant journal : for cell and molecular biology.

[7]  M. Nei,et al.  MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. , 2007, Molecular biology and evolution.

[8]  X. Lan,et al.  Mapping QTLs for pre-harvest sprouting tolerance on chromosome 2D in a synthetic hexaploid wheat x common wheat cross. , 2008, Journal of applied genetics.

[9]  Christian A. Ross,et al.  Computational Prediction and Experimental Verification of HVA1-like Abscisic Acid Responsive Promoters in Rice (Oryza sativa) , 2006, Plant Molecular Biology.

[10]  T. Hattori,et al.  ACGT-containing abscisic acid response element (ABRE) and coupling element 3 (CE3) are functionally equivalent. , 1999, The Plant journal : for cell and molecular biology.

[11]  S. Lin,et al.  Mapping quantitative trait loci controlling seed dormancy and heading date in rice, Oryza sativa L., using backcross inbred lines , 1998, Theoretical and Applied Genetics.

[12]  M. Kawase,et al.  Development of an RFLP-based Rice Diversity Research Set of Germplasm , 2005 .

[13]  I. Romagosa,et al.  Verification of barley seed dormancy loci via linked molecular markers , 2004, Theoretical and Applied Genetics.

[14]  Amanda J. Garris,et al.  Genetic Structure and Diversity in Oryza sativa L. , 2005, Genetics.

[15]  M. E. Foley,et al.  Multiple Loci and Epistases Control Genetic Variation for Seed Dormancy in Weedy Rice (Oryza sativa) , 2004, Genetics.

[16]  M. Koornneef,et al.  Cloning of DOG1, a quantitative trait locus controlling seed dormancy in Arabidopsis , 2006, Proceedings of the National Academy of Sciences.

[17]  S. Cutler,et al.  In vitro Reconstitution of an ABA Signaling Pathway , 2009, Nature.

[18]  H. Yoshida,et al.  A role of OsGA20ox1, encoding an isoform of gibberellin 20-oxidase, for regulation of plant stature in rice , 2004, Plant Molecular Biology.

[19]  Lihuang Zhu,et al.  QTL analysis of seed dormancy in rice (Oryza sativa L.) , 2004, Euphytica.

[20]  T. Sang,et al.  Rice Domestication by Reducing Shattering , 2007 .

[21]  F. Myouga,et al.  Type 2C protein phosphatases directly regulate abscisic acid-activated protein kinases in Arabidopsis , 2009, Proceedings of the National Academy of Sciences.

[22]  Bin Han,et al.  Collection and Comparative Analysis of 1888 Full-length cDNAs from Wild Rice Oryza rufipogon Griff. W1943 , 2008, DNA research : an international journal for rapid publication of reports on genes and genomes.

[23]  G. Sécond.  Origin of the genic diversity of cultivated rice (Oryza spp.): study of the polymorphism scored at 40 isozyme loci , 1982 .

[24]  Kazumasa Murata,et al.  A large-scale collection of phenotypic data describing an insertional mutant population to facilitate functional analysis of rice genes , 2006, Plant Molecular Biology.

[25]  K. Shinozaki,et al.  A stress-inducible gene for 9-cis-epoxycarotenoid dioxygenase involved in abscisic acid biosynthesis under water stress in drought-tolerant cowpea. , 2000, Plant physiology.

[26]  R. Laskey,et al.  Two interdependent basic domains in nucleoplasmin nuclear targeting sequence: Identification of a class of bipartite nuclear targeting sequence , 1991, Cell.

[27]  M. Yano,et al.  An SNP Caused Loss of Seed Shattering During Rice Domestication , 2006, Science.

[28]  Björn Usadel,et al.  Mapping Metabolic and Transcript Temporal Switches during Germination in Rice Highlights Specific Transcription Factors and the Role of RNA Instability in the Germination Process1[W][OA] , 2008, Plant Physiology.

[29]  T. Hattori,et al.  Sequence and functional analyses of the rice gene homologous to the maize Vp1 , 1994, Plant Molecular Biology.

[30]  Xin-Yao Yu,et al.  The role of water channel proteins and nitric oxide signaling in rice seed germination , 2007, Cell Research.

[31]  S. Wessler,et al.  Filler DNA is associated with spontaneous deletions in maize. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[32]  S. Oka,et al.  Early infection of scutellum tissue with Agrobacterium allows high-speed transformation of rice. , 2006, The Plant journal : for cell and molecular biology.

[33]  H. Kende,et al.  Expression of beta-expansins is correlated with internodal elongation in deepwater rice. , 2001, Plant physiology.

[34]  Michael J Holdsworth,et al.  Seed after-ripening is a discrete developmental pathway associated with specific gene networks in Arabidopsis , 2007, The Plant journal : for cell and molecular biology.

[35]  Zheng You-liang,et al.  Mapping QTLs for pre-harvest sprouting tolerance on chromosome 2D in a synthetic hexaploid wheat×common wheat cross , 2010, Journal of Applied Genetics.

[36]  D. McCarty,et al.  Signaling from the embryo conditions Vp1-mediated repression of alpha-amylase genes in the aleurone of developing maize seeds. , 1999, The Plant journal : for cell and molecular biology.

[37]  K. Bradford,et al.  Seed development, dormancy and germination , 2007 .

[38]  Yoshihiro Kawahara,et al.  The Rice Annotation Project Database (RAP-DB): 2008 update , 2007, Nucleic Acids Res..

[39]  Maarten Koornneef,et al.  The Absence of Histone H2B Monoubiquitination in the Arabidopsis hub1 (rdo4) Mutant Reveals a Role for Chromatin Remodeling in Seed Dormancy[W][OA] , 2007, The Plant Cell Online.

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

[41]  F. Gubler,et al.  Anatomical and Transcriptomic Studies of the Coleorhiza Reveal the Importance of This Tissue in Regulating Dormancy in Barley1[W] , 2009, Plant Physiology.

[42]  C. M. Karssen,et al.  In Vivo Inhibition of Seed Development and Reserve Protein Accumulation in Recombinants of Abscisic Acid Biosynthesis and Responsiveness Mutants in Arabidopsis thaliana. , 1989, Plant physiology.

[43]  Q. Shen,et al.  Modular nature of abscisic acid (ABA) response complexes: composite promoter units that are necessary and sufficient for ABA induction of gene expression in barley. , 1996, The Plant cell.

[44]  Masaharu Suzuki,et al.  Quantitative Statistical Analysis of cis-Regulatory Sequences in ABA/VP1- and CBF/DREB1-Regulated Genes of Arabidopsis1[w] , 2005, Plant Physiology.

[45]  Mark E. Sorrells,et al.  RFLP Analysis of Genomic Regions Associated with Resistance to Preharvest Sprouting in Wheat , 1993 .

[46]  R. Motohashi,et al.  Polyphyletic origin of cultivated rice: based on the interspersion pattern of SINEs. , 2003, Molecular biology and evolution.

[47]  C. Bustamante,et al.  Global Dissemination of a Single Mutation Conferring White Pericarp in Rice , 2007, PLoS genetics.

[48]  Masako Totsuka,et al.  Experimentally determined sequence requirement of ACGT-containing abscisic acid response element. , 2002, Plant & cell physiology.

[49]  Kazuo N. Watanabe,et al.  Identification of SNPs in the waxy gene among glutinous rice cultivars and their evolutionary significance during the domestication process of rice , 2004, Theoretical and Applied Genetics.

[50]  P. McCourt,et al.  Isolation of an internal deletion mutant of the Arabidopsis thaliana ABI3 gene. , 1994, Plant & cell physiology.

[51]  J. Suttle,et al.  The qSD12 underlying gene promotes abscisic acid accumulation in early developing seeds to induce primary dormancy in rice , 2010, Plant Molecular Biology.

[52]  D. Inzé,et al.  Cis-analysis of a seed protein gene promoter: the conservative RY repeat CATGCATG within the legumin box is essential for tissue-specific expression of a legumin gene. , 1992, The Plant journal : for cell and molecular biology.

[53]  D. McCarty,et al.  The Viviparous-1 developmental gene of maize encodes a novel transcriptional activator , 1991, Cell.

[54]  M T Clegg,et al.  Genome comparisons reveal a dominant mechanism of chromosome number reduction in grasses and accelerated genome evolution in Triticeae , 2009, Proceedings of the National Academy of Sciences.