Through the genetic bottleneck: O. rufipogon as a source of trait-enhancing alleles for O. sativa

This paper summarizes results from a decade of collaborative research using advanced backcross (AB) populations to a) identify quantitative trait loci (QTL) associated with improved performance in rice and to b) clone genes underlying key QTLs of interest. We demonstrate that AB-QTL analysis is capable of (1) successfully uncovering positive alleles in wild germplasm that were not obvious based on the phenotype of the parent (2) offering an estimation of the breeding value of exotic germplasm, (3) generating near isogenic lines that can be used as the basis for gene isolation and also as parents for further crossing in a variety development program and (4) providing gene-based markers for targeted introgression of alleles using marker-assisted-selection (MAS). Knowledge gained from studies examining the population structure and evolutionary history of rice is helping to illuminate a long-term strategy for exploiting and simultaneously preserving the well-partitioned gene pools in rice.

[1]  Cai-guo Xu,et al.  Identification of quantitative trait loci and epistatic interactions for plant height and heading date in rice , 2002, Theoretical and Applied Genetics.

[2]  J. Zhu,et al.  Impact of epistasis and QTL×environment interaction on the developmental behavior of plant height in rice (Oryza sativa L.) , 2001, Theoretical and Applied Genetics.

[3]  A. McClung,et al.  An Improved Method for Using a Microsatellite in the Rice Waxy Gene to Determine Amylose Class , 2001 .

[4]  A. Price,et al.  Marker-assisted selection to introgress rice QTLs controlling root traits into an Indian upland rice variety , 2006, Theoretical and Applied Genetics.

[5]  R. Henry,et al.  A Perfect Marker for Fragrance Genotyping in Rice , 2005, Molecular Breeding.

[6]  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.

[7]  L. Stein,et al.  Plant Ontology (PO): a Controlled Vocabulary of Plant Structures and Growth Stages , 2005, Comparative and functional genomics.

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

[9]  A. Paterson,et al.  Epistasis for three grain yield components in rice (Oryza sativa L.). , 1997, Genetics.

[10]  P. Christou,et al.  ‘Green revolution’ genes encode mutant gibberellin response modulators , 1999, Nature.

[11]  H. Oka,et al.  VARIATIONS IN THE BREEDING SYSTEMS OF A WILD RICE, ORYZA PERENNIS , 1967, Evolution; international journal of organic evolution.

[12]  E. Hammond,et al.  Inheritance of Oil Percentage in Interspecific Crosses of Hexaploid Oats , 1975 .

[13]  K. Ishihara,et al.  Science of the rice plant , 1993 .

[14]  J. Hawkes Significance of wild species and primitive forms for potato breeding , 1958, Euphytica.

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

[16]  J. Londo,et al.  Phylogeography of Asian wild rice, Oryza rufipogon, reveals multiple independent domestications of cultivated rice, Oryza sativa. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[17]  T. Oki,et al.  Polymeric procyanidins as radical-scavenging components in red-hulled rice. , 2002, Journal of agricultural and food chemistry.

[18]  K. Zheng,et al.  Genetic differentiation of wild relatives of rice as assessed by RFLP analysis , 2002, Theoretical and Applied Genetics.

[19]  N. Tomooka,et al.  On the phylogeny and biogeography of the genus Oryza , 2005 .

[20]  A. Iyer-Pascuzzi,et al.  Functional markers for xa5-mediated resistance in rice (Oryza sativa, L.) , 2007, Molecular Breeding.

[21]  G. S. Khush,et al.  Green revolution: A mutant gibberellin-synthesis gene in rice , 2002, Nature.

[22]  Zhonghua Wang,et al.  Development of a SNLP marker from the Pi-ta blast resistance gene by tri-primer PCR , 2004, Euphytica.

[23]  S. Tanksley,et al.  Advanced backcross QTL analysis: a method for the simultaneous discovery and transfer of valuable QTLs from unadapted germplasm into elite breeding lines , 1996, Theoretical and Applied Genetics.

[24]  E. Septiningsih,et al.  Identification of quantitative trait loci for yield and yield components in an advanced backcross population derived from the Oryza sativa variety IR64 and the wild relative O. rufipogon , 2003, Theoretical and Applied Genetics.

[25]  S. Mccouch,et al.  Identification of QTLs for domestication‐related and agronomic traits in an Oryza sativa×O. rufipogon BC1F7 population , 2005 .

[26]  J. Harlan Our vanishing genetic resources. , 1975, Science.

[27]  P. R. Jennings,et al.  Inheritance and Significance of Dwarfism in an Indica Rice Variety , 1966 .

[28]  Michael J. Thomson,et al.  Mapping quantitative trait loci for yield, yield components and morphological traits in an advanced backcross population between Oryza rufipogon and the Oryza sativa cultivar Jefferson , 2003, Theoretical and Applied Genetics.

[29]  R. Dilday Contribution of ancestral lines in the development of new cultivars of rice. , 1990 .

[30]  Jane Lomax,et al.  It's All GO for Plant Scientists1 , 2005, Plant Physiology.

[31]  P. Marri,et al.  Identification and mapping of yield and yield related QTLs from an Indian accession of Oryza rufipogon , 2005, BMC Genetics.

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

[33]  L. Stein,et al.  Development and mapping of 2240 new SSR markers for rice (Oryza sativa L.). , 2002, DNA research : an international journal for rapid publication of reports on genes and genomes.

[34]  J. Léon,et al.  Advanced backcross QTL analysis in barley (Hordeum vulgare L.) , 2003, Theoretical and Applied Genetics.

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

[36]  J. Glaszmann Isozymes and classification of Asian rice varieties , 1987, Theoretical and Applied Genetics.

[37]  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.

[38]  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.

[39]  T. Dobzhansky STUDIES ON HYBRID STERILITY. 11. LOCALIZATION OF STERILITY FACTORS I N DROSOPHILA PSEUDOOBSCURA HYBRIDS , 2003 .

[40]  Peter Hedden,et al.  The genes of the Green Revolution. , 2003, Trends in genetics : TIG.

[41]  J. Tohme,et al.  QTL mapping of grain quality traits from the interspecific cross Oryza sativa × O. glaberrima , 2004, Theoretical and Applied Genetics.

[42]  D. Mackill,et al.  Quantitative trait locus analysis for rice panicle and grain characteristics , 1998, Theoretical and Applied Genetics.

[43]  L. Lipovich,et al.  Computational and experimental analysis of microsatellites in rice (Oryza sativa L.): frequency, length variation, transposon associations, and genetic marker potential. , 2001, Genome research.

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

[45]  D. Mackill,et al.  Evaluation of Genetic Diversity in Rice Subspecies Using Microsatellite Markers , 2002 .

[46]  Zhikang Li,et al.  Genome-wide Introgression Lines and their Use in Genetic and Molecular Dissection of Complex Phenotypes in Rice (Oryza sativa L.) , 2005, Plant Molecular Biology.

[47]  Z. Zeng Precision mapping of quantitative trait loci. , 1994, Genetics.

[48]  P. Moncada,et al.  Quantitative trait loci for yield and yield components in an Oryza sativa×Oryza rufipogon BC2F2 population evaluated in an upland environment , 2001, Theoretical and Applied Genetics.

[49]  R. Doerge,et al.  Empirical threshold values for quantitative trait mapping. , 1994, Genetics.

[50]  M. Ferreira,et al.  QTL mapping and introgression of yield-related traits from Oryza glumaepatula to cultivated rice (Oryza sativa) using microsatellite markers , 2002, Theoretical and Applied Genetics.

[51]  G. Khush,et al.  RFLP analysis of rice (Oryza sativa L.) introgression lines , 1992, Theoretical and Applied Genetics.

[52]  B. Burr,et al.  The maize repressor-like gene intensifier1 shares homology with the r1/b1 multigene family of transcription factors and exhibits missplicing. , 1996, The Plant cell.

[53]  Richard M. Bruskiewich,et al.  Linking genotype to phenotype: the International Rice Information System (IRIS) , 2003, ISMB.

[54]  B. D. Webb,et al.  Registration of 'Jefferson' rice , 1997 .

[55]  S. Tanksley,et al.  Advanced backcross QTL analysis of tomato. II. Evaluation of near-isogenic lines carrying single-donor introgressions for desirable wild QTL-alleles derived from Lycopersicon hirsutum and L. pimpinellifolium , 1998, Theoretical and Applied Genetics.

[56]  K. Devos,et al.  Comparative genetics in the grasses. , 1998, Plant molecular biology.

[57]  Cai-guo Xu,et al.  Importance of epistasis as the genetic basis of heterosis in an elite rice hybrid. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[58]  B. W. Shirley Flavonoids in seeds and grains: physiological function, agronomic importance and the genetics of biosynthesis , 1998, Seed Science Research.

[59]  T. Nishio,et al.  Mutation detection in rice waxy mutants by PCR-RF-SSCP , 2003, Theoretical and Applied Genetics.

[60]  P. R. Jennings Plant Type as a Rice Breeding Objective1 , 1964 .

[61]  H. Nguyen,et al.  Identification and mapping of the QTL for aluminum tolerance introgressed from the new source, ORYZA RUFIPOGON Griff., into indica rice (Oryza sativa L.) , 2003, Theoretical and Applied Genetics.

[62]  Cai-guo Xu,et al.  Characterization of the main effects, epistatic effects and their environmental interactions of QTLs on the genetic basis of yield traits in rice , 2002, Theoretical and Applied Genetics.

[63]  S. Tanksley,et al.  Identification of trait-improving quantitative trait loci alleles from a wild rice relative, Oryza rufipogon. , 1998, Genetics.

[64]  X. Yong Mapping Quantitative Trait Loci for Grain Appearance Traits of Rice Using a Recombinant Inbred Line Population , 2001 .

[65]  M. Ellis,et al.  Semidwarf (sd-1), “green revolution” rice, contains a defective gibberellin 20-oxidase gene , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[66]  B. Valent,et al.  Direct interaction of resistance gene and avirulence gene products confers rice blast resistance , 2000, The EMBO journal.

[67]  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.

[68]  T. Ishii,et al.  Molecular tagging of genes for brown planthopper resistance and earliness introgressed from Oryza australiensis into cultivated rice, O. sativa. , 1994, Genome.

[69]  Jinhua Xiao,et al.  QTL detection for rice grain quality traits using an interspecific backcross population derived from cultivated Asian (O. sativa L.) and African (O. glaberrima S.) rice. , 2004, Genome.

[70]  Kazuo Tsugane,et al.  Efficient gene targeting by homologous recombination in rice , 2002, Nature Biotechnology.

[71]  Masatomo Kobayashi,et al.  Loss-of-function of a Rice Gibberellin Biosynthetic Gene, GA20 oxidase (GA20ox-2), Led to the Rice ‘Green Revolution’ , 2002 .

[72]  L. Stein,et al.  Development and mapping of 2240 new SSR markers for rice (Oryza sativa L.) (supplement). , 2002, DNA research : an international journal for rapid publication of reports on genes and genomes.

[73]  G. Sécond Molecular Markers in Rice Systematics and the Evaluation of Genetic Resources , 1991 .

[74]  E. Sánchez-Monge European plant science: a field of opportunities. , 2005, Journal of experimental botany.

[75]  J. Rutger,et al.  Inheritance of Semidwarfism in Rice, ORYZA SATIVA L. , 1978, Genetics.

[76]  Jeremy D. Edwards,et al.  Substitution Mapping of dth1.1, a Flowering-Time Quantitative Trait Locus (QTL) Associated With Transgressive Variation in Rice, Reveals Multiple Sub-QTL , 2006, Genetics.

[77]  Xiangkun Wang,et al.  Genetic differentiation for nuclear, mitochondrial and chloroplast genomes in common wild rice (Oryza rufipogon Griff.) and cultivated rice (Oryza sativa L.) , 2002, Theoretical and Applied Genetics.

[78]  Xing Yong-zhong,et al.  Mapping and isolation of quantitative trait loci controlling plant height and heading date in rice , 2001 .

[79]  S. Iida,et al.  Modification of Endogenous Natural Genes by Gene Targeting in Rice and Other Higher Plants , 2005, Plant Molecular Biology.

[80]  Y. Sano,et al.  Differentiation of perennial and annual types due to habitat conditions in the wild riceOryza perennis , 1984, Plant Systematics and Evolution.

[81]  Fan Zhang,et al.  GL3 encodes a bHLH protein that regulates trichome development in arabidopsis through interaction with GL1 and TTG1. , 2000, Genetics.

[82]  M. E. Foley,et al.  Phenotypic Selection for Dormancy Introduced a Set of Adaptive Haplotypes From Weedy Into Cultivated Rice , 2005, Genetics.

[83]  Wei Zhao,et al.  Gramene: a bird's eye view of cereal genomes , 2005, Nucleic Acids Res..

[84]  I. Paran,et al.  Mapping of yield-related QTLs in pepper in an interspecific cross of Capsicum annuum and C. frutescens , 2003, Theoretical and Applied Genetics.

[85]  S. C. Roy A preliminary classification of the wild rice of C. P. & Berar. , 1921 .

[86]  Xing Yong-zhong,et al.  Mapping Quantitative Trait Loci for Grain Appearance Traits of Rice Using a Recombinant Inbred Line Population , 2001 .

[87]  M. E. Foley,et al.  Genetic analysis of adaptive syndromes interrelated with seed dormancy in weedy rice (Oryza sativa) , 2005, Theoretical and Applied Genetics.

[88]  L. Xiong,et al.  Identification of genetic factors controlling domestication-related traits of rice using an F2 population of a cross between Oryza sativa and O. rufipogon , 1999, Theoretical and Applied Genetics.

[89]  J. Harlan Genetic Resources in Wild Relatives of Crops 1 , 1976 .

[90]  M. Yano,et al.  Diverse variation of reproductive barriers in three intraspecific rice crosses. , 2002, Genetics.

[91]  T. Dobzhansky,et al.  Studies on hybrid sterility , 2004, Zeitschrift für Zellforschung und Mikroskopische Anatomie.

[92]  S. S. Virmani,et al.  Identification and transfer of a new cytoplasmic male sterility source from Oryza perennis into indica rice (O. sativa) , 2004, Euphytica.

[93]  S. Mccouch,et al.  Fine Mapping of a Grain-Weight Quantitative Trait Locus in the Pericentromeric Region of Rice Chromosome 3 , 2004, Genetics.

[94]  J. Mol,et al.  ANTHOCYANIN1 of Petunia Controls Pigment Synthesis, Vacuolar pH, and Seed Coat Development by Genetically Distinct Mechanisms Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.003772. , 2002, The Plant Cell Online.

[95]  Hong Lu,et al.  Population structure and breeding patterns of 145 U.S. rice cultivars based on SSR marker analysis , 2005 .

[96]  K. Zheng,et al.  RFLP-based phylogenetic analysis of wide compatibility varieties in Oryza sativa L. , 1994, Theoretical and Applied Genetics.

[97]  V. Grant,et al.  Origin of Cultivated Rice , 1988 .

[98]  P. Hedden,et al.  Gibberellin metabolism: new insights revealed by the genes. , 2000, Trends in plant science.

[99]  R. A. Forsberg,et al.  Constraints in using wild relatives in breeding: lack of basic knowledge on crop gene pools. , 1993 .

[100]  C. Sneller,et al.  Identification of red rice, rice, and hybrid populations using microsatellite markers , 2002, Weed Science.

[101]  R. Stettler,et al.  Molecular genetics of growth and development in populus. IV. Mapping QTLs with large effects on growth, form, and phenology traits in a forest tree. , 1995, Genetics.

[102]  Bao Liu,et al.  Extensive de Novo Genomic Variation in Rice Induced by Introgression From Wild Rice (Zizania latifolia Griseb.) , 2005, Genetics.

[103]  D. Brar,et al.  Alien introgression in rice , 1997, Plant Molecular Biology.

[104]  Jing Ma,et al.  Red and black rice decrease atherosclerotic plaque formation and increase antioxidant status in rabbits. , 2001, The Journal of nutrition.

[105]  J. Li,et al.  Identification of QTLs affecting traits of agronomic importance in a recombinant inbred population derived from a subspecific rice cross , 1996, Theoretical and Applied Genetics.

[106]  M. Ganal,et al.  Advanced backcross QTL analysis for the identification of quantitative trait loci alleles from wild relatives of wheat (Triticum aestivum L.) , 2003, Theoretical and Applied Genetics.

[107]  Y. Minobe,et al.  Positional cloning of rice semidwarfing gene, sd-1: rice "green revolution gene" encodes a mutant enzyme involved in gibberellin synthesis. , 2002, DNA research : an international journal for rapid publication of reports on genes and genomes.

[108]  K. Shimamoto Picking genes in the rice genome , 2002, Nature Biotechnology.