Massive gene losses in Asian cultivated rice unveiled by comparative genome analysis

BackgroundRice is one of the most important food crops in the world. With increasing world demand for food crops, there is an urgent need to develop new cultivars that have enhanced performance with regard to yield, disease resistance, and so on. Wild rice is expected to provide useful genetic resources that could improve the present cultivated species. However, the quantity and quality of these unexplored resources remain unclear. Recent accumulation of the genomic information of both cultivated and wild rice species allows for their comparison at the molecular level. Here, we compared the genome sequence of Oryza sativa ssp. japonica with sets of bacterial artificial chromosome end sequences (BESs) from two wild rice species, O. rufipogon and O. nivara, and an African rice species, O. glaberrima.ResultsWe found that about four to five percent of the BESs of the two wild rice species and about seven percent of the African rice could not be mapped to the japonica genome, suggesting that a substantial number of genes have been lost in the japonica rice lineage; however, their close relatives still possess their counterpart genes. We estimated that during evolution, O. sativa has lost at least one thousand genes that are still preserved in the genomes of the other species. In addition, our BLASTX searches against the non-redundant protein sequence database showed that disease resistance-related proteins were significantly overrepresented in the close relative-specific genomic portions. In total, 235 unmapped BESs of the three relatives matched 83 non-redundant proteins that contained a disease resistance protein domain, most of which corresponded to an NBS-LRR domain.ConclusionWe found that the O. sativa lineage appears to have recently experienced massive gene losses following divergence from its wild ancestor. Our results imply that the domestication process accelerated large-scale genomic deletions in the lineage of Asian cultivated rice and that the close relatives of cultivated rice have the potential to restore the lost traits.

[1]  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.

[2]  C. Tebaldi,et al.  Prioritizing Climate Change Adaptation Needs for Food Security in 2030 , 2008, Science.

[3]  Jianxin Ma,et al.  Rapid recent growth and divergence of rice nuclear genomes. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[4]  G S Khush,et al.  HARNESSING SCIENCE AND TECHNOLOGY FOR SUSTAINABLE RICE-BASED PRODUCTION SYSTEM , 2004 .

[5]  Jinhua Xiao,et al.  Through the genetic bottleneck: O. rufipogon as a source of trait-enhancing alleles for O. sativa , 2007, Euphytica.

[6]  Qihui Zhu,et al.  Phylogenetic relationships among A-genome species of the genus Oryza revealed by intron sequences of four nuclear genes. , 2005, The New phytologist.

[7]  S. Jackson,et al.  The Oryza bacterial artificial chromosome library resource: construction and analysis of 12 deep-coverage large-insert BAC libraries that represent the 10 genome types of the genus Oryza. , 2005, Genome research.

[8]  Kanako O. Koyanagi,et al.  Curated genome annotation of Oryza sativa ssp. japonica and comparative genome analysis with Arabidopsis thaliana. , 2007, Genome research.

[9]  K. Devos,et al.  Plant comparative genetics after 10 years. , 1998, Science.

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

[11]  J. Thompson,et al.  CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. , 1994, Nucleic acids research.

[12]  Rolf Apweiler,et al.  InterProScan: protein domains identifier , 2005, Nucleic Acids Res..

[13]  Xing Wang Deng,et al.  Rice 2020: a call for an international coordinated effort in rice functional genomics. , 2008, Molecular plant.

[14]  M. Kovach,et al.  Leveraging natural diversity: back through the bottleneck. , 2008, Current opinion in plant biology.

[15]  Katsuhiko Murakami,et al.  Evola: Ortholog database of all human genes in H-InvDB with manual curation of phylogenetic trees , 2007, Nucleic Acids Res..

[16]  B. Lu,et al.  A comparative study of genetic relationships among the AA-genome Oryza species using RAPD and SSR markers , 2003, Theoretical and Applied Genetics.

[17]  C. Soderlund,et al.  The Oryza Map Alignment Project: The Golden Path to Unlocking the Genetic Potential of Wild Rice Species , 2005, Plant Molecular Biology.

[18]  Dawei Li,et al.  The Genomes of Oryza sativa: A History of Duplications , 2005, PLoS biology.

[19]  D. Roze,et al.  Self-Fertilization and the Evolution of Recombination , 2005, Genetics.

[20]  S. Tanksley,et al.  Seed banks and molecular maps: unlocking genetic potential from the wild. , 1997, Science.

[21]  M. Yano,et al.  Expression of Xa1, a bacterial blight-resistance gene in rice, is induced by bacterial inoculation. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[22]  D. Leister.  Tandem and segmental gene duplication and recombination in the evolution of plant disease resistance gene. , 2004, Trends in genetics : TIG.

[23]  Jun Wang,et al.  Analysis of 142 genes resolves the rapid diversification of the rice genus , 2008, Genome Biology.

[24]  L. Stein,et al.  Construction, alignment and analysis of twelve framework physical maps that represent the ten genome types of the genus Oryza , 2008, Genome Biology.

[25]  Li Yang,et al.  MIPSPlantsDB—plant database resource for integrative and comparative plant genome research , 2007, Nucleic Acids Res..

[26]  B C Meyers,et al.  Clusters of resistance genes in plants evolve by divergent selection and a birth-and-death process. , 1998, Genome research.

[27]  M. Nei,et al.  Molecular Evolution and Phylogenetics , 2000 .

[28]  R. Michelmore,et al.  Recombination and spontaneous mutation at the major cluster of resistance genes in lettuce (Lactuca sativa). , 2001, Genetics.

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

[30]  N. Saitou,et al.  The neighbor-joining method: a new method for reconstructing phylogenetic trees. , 1987, Molecular biology and evolution.

[31]  B. Keller,et al.  Molecular evolution of receptor-like kinase genes in hexaploid wheat. Independent evolution of orthologs after polyploidization and mechanisms of local rearrangements at paralogous loci. , 2001, Plant physiology.

[32]  M T Clegg,et al.  Substitution rate comparisons between grasses and palms: synonymous rate differences at the nuclear gene Adh parallel rate differences at the plastid gene rbcL. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[33]  M. Nei,et al.  Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. , 1986, Molecular biology and evolution.

[34]  E. Eichler,et al.  Structural Dynamics of Eukaryotic Chromosome Evolution , 2003, Science.

[35]  G. Khush.  Green revolution: the way forward , 2001, Nature Reviews Genetics.

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

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

[38]  M. Thomson,et al.  Caught Red-Handed: Rc Encodes a Basic Helix-Loop-Helix Protein Conditioning Red Pericarp in Rice[W][OA] , 2006, The Plant Cell Online.

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

[40]  Zuofeng Zhu,et al.  Construction of introgression lines carrying wild rice (Oryza rufipogon Griff.) segments in cultivated rice (Oryza sativa L.) background and characterization of introgressed segments associated with yield-related traits , 2006, Theoretical and Applied Genetics.

[41]  Takuji Nishimura,et al.  Mersenne twister: a 623-dimensionally equidistributed uniform pseudo-random number generator , 1998, TOMC.

[42]  S. Jackson,et al.  Doubling genome size without polyploidization: dynamics of retrotransposition-driven genomic expansions in Oryza australiensis, a wild relative of rice. , 2006, Genome research.

[43]  Sequence variation in the gene encoding the 10-kDa prolamin in Oryza (Poaceae). I. Phylogenetic Implications , 2002, Theoretical and Applied Genetics.

[44]  M. Yano,et al.  The Pib gene for rice blast resistance belongs to the nucleotide binding and leucine-rich repeat class of plant disease resistance genes. , 1999, The Plant journal : for cell and molecular biology.

[45]  Jing Wang,et al.  Identification of a New Rice Blast Resistance Gene, Pid3, by Genomewide Comparison of Paired Nucleotide-Binding Site–Leucine-Rich Repeat Genes and Their Pseudogene Alleles Between the Two Sequenced Rice Genomes , 2009, Genetics.

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

[47]  D. Haussler,et al.  Human-mouse alignments with BLASTZ. , 2003, Genome research.

[48]  H. Mori,et al.  Evolutionary instability of operon structures disclosed by sequence comparisons of complete microbial genomes. , 1999, Molecular biology and evolution.

[49]  G. Khush.  Challenges for meeting the global food and nutrient needs in the new millennium , 2001, The Proceedings of the Nutrition Society.

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

[51]  D. Swofford.  PAUP*: Phylogenetic analysis using parsimony (*and other methods), Version 4.0b10 , 2002 .

[52]  李佩芳.  International Rice Genome Sequencing Project. 2005. The map-based sequence of the rice genome. , 2005 .

[53]  Q. Sun,et al.  Resistance gene complexes: evolution and utilization. , 2001, Annual review of phytopathology.

[54]  M. Kreitman,et al.  Fitness costs of R-gene-mediated resistance in Arabidopsis thaliana , 2003, Nature.

[55]  M. Nei,et al.  Concerted and birth-and-death evolution of multigene families. , 2005, Annual review of genetics.

[56]  B. Charlesworth,et al.  Selection for recombination in partially self-fertilizing populations. , 1979, Genetics.

[57]  J. Soussana,et al.  Crop and pasture response to climate change , 2007, Proceedings of the National Academy of Sciences.

[58]  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.