Genomic adaptation of flowering‐time genes during the expansion of rice cultivation area

The diversification of flowering time in response to natural environments is critical for the spread of crops to diverse geographic regions. In contrast with recent advances in understanding the molecular basis of photoperiodic flowering in rice (Oryza sativa), little is known about how flowering-time diversification is structured within rice subspecies. By analyzing genome sequencing data and a set of 429 chromosome segment substitution lines (CSSLs) originating from 10 diverse rice accessions with wide distributions, we revealed diverse effects of allelic variations for common flowering-time quantitative trait loci in the recipient's background. Although functional variations associated with a few loci corresponded to standing variations among subspecies, the identified functional nucleotide polymorphisms occurred recently after rice subgroup differentiation, indicating that the functional diversity of flowering-time gene sequences was not particularly associated with phylogenetic relationship between rice subspecies. Intensive analysis of the Hd1 genomic region identified the signature of an early introgression of the Hd1 with key mutation(s) in aus and temperate japonica accessions. Our data suggested that, after such key introgressions, new mutations were selected and accelerated the flowering-time diversity within subspecies during the expansion of rice cultivation area. This finding may imply that new genome-wide changes for flowering-time adaptation are one of the critical determinants for establishing genomic architecture of local rice subgroups. In-depth analyses of various rice genomes coupling with the genetically confirmed phenotypic changes in a large set of CSSLs enabled us to demonstrate how rice genome dynamics has coordinated with the adaptation of cultivated rice during the expansion of cultivation area.

[1]  Dong Cao,et al.  Natural variation at the soybean J locus improves adaptation to the tropics and enhances yield , 2017, Nature Genetics.

[2]  E. Buckler,et al.  A study of allelic diversity underlying flowering-time adaptation in maize landraces , 2017, Nature Genetics.

[3]  Kaworu Ebana,et al.  Hd18, Encoding Histone Acetylase Related to Arabidopsis FLOWERING LOCUS D, is Involved in the Control of Flowering Time in Rice. , 2016, Plant & cell physiology.

[4]  M. Yamasaki,et al.  Genome-wide association study using whole-genome sequencing rapidly identifies new genes influencing agronomic traits in rice , 2016, Nature Genetics.

[5]  M. Yano,et al.  Advanced backcross QTL analysis reveals complicated genetic control of rice grain shape in a japonica × indica cross , 2015, Breeding science.

[6]  F. Taguchi-Shiobara,et al.  Genetic architecture of variation in heading date among Asian rice accessions , 2015, BMC Plant Biology.

[7]  Haiyang Wang,et al.  Days to heading 7, a major quantitative locus determining photoperiod sensitivity and regional adaptation in rice , 2014, Proceedings of the National Academy of Sciences.

[8]  Björn Usadel,et al.  Trimmomatic: a flexible trimmer for Illumina sequence data , 2014, Bioinform..

[9]  Cai-guo Xu,et al.  Grain Number, Plant Height, and Heading Date7 Is a Central Regulator of Growth, Development, and Stress Response1[W][OPEN] , 2014, Plant Physiology.

[10]  Rachel S. Meyer,et al.  Evolution of crop species: genetics of domestication and diversification , 2013, Nature Reviews Genetics.

[11]  M. Yano,et al.  Natural Variation of the RICE FLOWERING LOCUS T 1 Contributes to Flowering Time Divergence in Rice , 2013, PloS one.

[12]  M. Yano,et al.  Detection of QTLs to reduce cadmium content in rice grains using LAC23/Koshihikari chromosome segment substitution lines , 2013, Breeding science.

[13]  Kaworu Ebana,et al.  Hd16, a gene for casein kinase I, is involved in the control of rice flowering time by modulating the day-length response , 2013, The Plant journal : for cell and molecular biology.

[14]  Zhijun Cheng,et al.  Association of functional nucleotide polymorphisms at DTH2 with the northward expansion of rice cultivation in Asia , 2013, Proceedings of the National Academy of Sciences.

[15]  D. Schwartz,et al.  Improvement of the Oryza sativa Nipponbare reference genome using next generation sequence and optical map data , 2013, Rice.

[16]  Haiyang Wang,et al.  Ehd4 Encodes a Novel and Oryza-Genus-Specific Regulator of Photoperiodic Flowering in Rice , 2013, PLoS genetics.

[17]  M. Yano,et al.  Roles of the Hd5 gene controlling heading date for adaptation to the northern limits of rice cultivation , 2012, Theoretical and Applied Genetics.

[18]  A. Fujiyama,et al.  A map of rice genome variation reveals the origin of cultivated rice , 2012, Nature.

[19]  Kaworu Ebana,et al.  Natural variation in Hd17, a homolog of Arabidopsis ELF3 that is involved in rice photoperiodic flowering. , 2012, Plant & cell physiology.

[20]  M. Nei,et al.  MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. , 2011, Molecular biology and evolution.

[21]  Makoto Takano,et al.  Molecular Dissection of the Roles of Phytochrome in Photoperiodic Flowering in Rice1[C][W][OA] , 2011, Plant Physiology.

[22]  K. Shimamoto,et al.  Heading date 1 (Hd1), an ortholog of Arabidopsis CONSTANS, is a possible target of human selection during domestication to diversify flowering times of cultivated rice. , 2011, Genes & genetic systems.

[23]  John Quackenbush,et al.  Defining an informativeness metric for clustering gene expression data , 2011, Bioinform..

[24]  M. Yano,et al.  Germplasm enhancement by developing advanced plant materials from diverse rice accessions , 2010 .

[25]  M. DePristo,et al.  The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. , 2010, Genome research.

[26]  Tomoko Ito,et al.  Multiple introgression events surrounding the Hd1 flowering-time gene in cultivated rice, Oryza sativa L. , 2010, Molecular Genetics and Genomics.

[27]  M. Yano,et al.  A pair of floral regulators sets critical day length for Hd3a florigen expression in rice , 2010, Nature Genetics.

[28]  Jianmin Wan,et al.  DTH8 Suppresses Flowering in Rice, Influencing Plant Height and Yield Potential Simultaneously1[W][OA] , 2010, Plant Physiology.

[29]  M. Yano,et al.  Detection of quantitative trait loci controlling pre-harvest sprouting resistance by using backcrossed populations of japonica rice cultivars , 2010, Theoretical and Applied Genetics.

[30]  M. Yano,et al.  The Role of Casein Kinase II in Flowering Time Regulation Has Diversified during Evolution1[W][OA] , 2009, Plant Physiology.

[31]  Kenneth L. McNally,et al.  Genomewide SNP variation reveals relationships among landraces and modern varieties of rice , 2009, Proceedings of the National Academy of Sciences.

[32]  Gonçalo R. Abecasis,et al.  The Sequence Alignment/Map format and SAMtools , 2009, Bioinform..

[33]  H. Kanamori,et al.  Molecular and Evolutionary Analysis of the Hd6 Photoperiod Sensitivity Gene Within Genus Oryza , 2009, Rice.

[34]  T. Izawa,et al.  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. , 2008, Plant & cell physiology.

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

[36]  Shojiro Tamaki,et al.  Hd3a and RFT1 are essential for flowering in rice , 2008, Development.

[37]  T. Izawa,et al.  Adaptation of flowering-time by natural and artificial selection in Arabidopsis and rice. , 2007, Journal of experimental botany.

[38]  M. Yano,et al.  Development of Chromosome Segment Substitution Lines Derived from Backcross between indica Donor Rice Cultivar ‘Nona Bokra’ and japonica Recipient Cultivar ‘Koshihikari’ , 2007 .

[39]  E. Ohtsubo,et al.  Phylogenetic analysis of Oryza rufipogon strains and their relations to Oryza sativa strains by insertion polymorphism of rice SINEs. , 2007, Genes & genetic systems.

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

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

[42]  Yoshinobu Takeuchi,et al.  Construction and evaluation of chromosome segment substitution lines carrying overlapping chromosome segments of indica rice cultivar 'Kasalath' in a genetic background of japonica elite cultivar 'Koshihikari' , 2005 .

[43]  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.

[44]  Takashi Araki,et al.  Hd3a, a rice ortholog of the Arabidopsis FT gene, promotes transition to flowering downstream of Hd1 under short-day conditions. , 2002, Plant & cell physiology.

[45]  M. Yano,et al.  Genetic control of flowering time in rice, a short-day plant. , 2001, Plant physiology.

[46]  M. Yano,et al.  Hd1, a Major Photoperiod Sensitivity Quantitative Trait Locus in Rice, Is Closely Related to the Arabidopsis Flowering Time Gene CONSTANS , 2000, Plant Cell.

[47]  G. Khush Origin, dispersal, cultivation and variation of rice , 1997, Plant Molecular Biology.

[48]  M. Kimura,et al.  The neutral theory of molecular evolution. , 1983, Scientific American.

[49]  M. Kimura A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences , 1980, Journal of Molecular Evolution.

[50]  W. F. Thompson,et al.  Rapid isolation of high molecular weight plant DNA. , 1980, Nucleic acids research.

[51]  T. Satake,et al.  Male Sterility Caused by Cooling Treatment at the Young Microspore Stage in Rice Plants : V. Estimations of pollen developmental stage and the most sensitive stage to coolness , 1970 .

[52]  T. Nagata STUDIES ON THE SIGNIFICANCE OF INDETERMINATE GROWTH HABIT IN BREEDING SOYBEANS. : IV. Varietal difference in the fruiting process attributable to the habit. -b. Internal development of the seeds. , 1967 .

[53]  Kaworu Ebana,et al.  HapRice, an SNP haplotype database and a web tool for rice. , 2014, Plant & cell physiology.

[54]  Claude-Alain H. Roten,et al.  Theoretical and practical advances in genome halving , 2004 .

[55]  T. Katayama Photoperiodism in the Genus Oryza : IV. Combinations of plant age, day length and number of treatment , 1974 .