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O. Rufipogon As a Source of Trait-Enhancing Alleles for O. Sativa

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O. Rufipogon As a Source of Trait-Enhancing Alleles for O. Sativa Euphytica (2007) 154:317–339 DOI 10.1007/s10681-006-9210-8 Through the genetic bottleneck: O. rufipogon as a source of trait-enhancing alleles for O. sativa Susan R. McCouch Æ Megan Sweeney Æ Jiming Li Æ Hui Jiang Æ Michael Thomson Æ Endang Septiningsih Æ Jeremy Edwards Æ Pilar Moncada Æ Jinhua Xiao Æ Amanda Garris Æ Tom Tai Æ Cesar Martinez Æ Joe Tohme Æ M. Sugiono Æ Anna McClung Æ Long Ping Yuan Æ Sang-Nag Ahn Received: 23 February 2006 / Accepted: 9 June 2006 / Published online: 17 October 2006 Ó Springer Science+Business Media B.V. 2006 Abstract This paper summarizes results from a performance in rice and to b) clone genes decade of collaborative research using advanced underlying key QTLs of interest. We demonstrate backcross (AB) populations to a) identify quan- that AB-QTL analysis is capable of (1) success- titative trait loci (QTL) associated with improved fully uncovering positive alleles in wild germ- S. R. McCouch (&) Æ M. Sweeney Æ H. Jiang Æ Present Address: M. Thomson Æ E. Septiningsih Æ J. Edwards Æ A. Garris P. Moncada Æ J. Xiao Æ A. Garris USDA/ARS, Geneva, NY, USA Department of Plant Breeding & Genetics, Cornell University, 162 Emerson Hall, Ithaca, NY 14853, Present Address: USA T. Tai e-mail: [email protected] University of California, Davis, CA, USA J. Li C. Martinez Æ J. Tohme Pioneer Hybrid International, Johnston, Iowa 50131, CIAT, Cali, Colombia USA M. Sugiono Present Address: ICABIOGRAD, 16111 Bogor, Indonesia M. Thomson Æ E. Septiningsih International Rice Research Institute, Los Ban˜ os, A. McClung Laguna, Philippines USDA-ARS, DBNRRC & Beaumont Rice Research Unit, Beaumont, TX 77713, USA Present Address: J. Edwards L. P. Yuan University of Arizona, Tucson, AZ, USA China National Hybrid Rice Research & Development Center, Changsha, Hunan 41025, P.R. Present Address: China P. Moncada Cenicafe, Apartado aereo 2427, Manizales, Caldas, S.-N. Ahn Colombia Dept of Agronomy, College of Agriculture, Chungnam National University, Daejeon, Republic of Present Address: Korea J. Xiao Monsanto Corp, St. Louis, MO, USA 123 318 Euphytica (2007) 154:317–339 plasm that were not obvious based on the phe- in China, India and Vietnam (Matsuo 1997) notype of the parent (2) offering an estimation of suggests that differentiation of the indica and the breeding value of exotic germplasm, (3) gen- japonica gene pools pre-dates the domestication erating near isogenic lines that can be used as the of O. sativa by several hundred thousand years. basis for gene isolation and also as parents for This is consistent with the belief that rice was further crossing in a variety development pro- independently domesticated on at least two gram and (4) providing gene-based markers for occasions from a pre-differentiated ancestral pool targeted introgression of alleles using marker-as- (Cheng et al. 2003; Garris et al. 2005; Roy 1921; sisted-selection (MAS). Knowledge gained from Second 1991, 1982). studies examining the population structure and In a recent study by Garris et al. (2005), five evolutionary history of rice is helping to illumi- sub-populations were clearly identified in a col- nate a long-term strategy for exploiting and lection of 234 landrace varieties of O. sativa using simultaneously preserving the well-partitioned 169 simple sequence repeat (SSR) markers and gene pools in rice. two chloroplast sequences. The basic number and identity of the sub-populations identified by Keywords Inter-specific cross Æ Transgressive Garris et al. (2005) using 169 SSRs were consis- variation Æ Quantitative trait loci (QTL) Æ Rice tent with those detected by Glaszmann (1987) (Oryza sativa L.) Æ Marker assisted selection Æ using only 15 isozyme markers. The same groups Molecular breeding were also identified by intronic SNP’s assayed at 112 random genetic loci (A. Caicedo, NCSU and Abbreviations S. Williamson, Cornell Univ, pers. comm.). Con- AB Advanced backcross sistent with Glaszmann’s earlier study (1987), QTL Quantitative trait loci nuclear and chloroplast SSR data supported a MAS Marker-assisted-selection close evolutionary relationship between the in- NIL Near isogenic line dica and aus groups, and between the tropical japonica, temperate japonica and aromatic groups (Fig. 1). A more complete evaluation of the population sub-structure of O. sativa is currently Introduction underway as part of the Generation Challenge Program (McNally pers. comm., IRRI) using a Evolutionary history and population diverse set of molecular markers and several sub-structure of O. sativa thousand accessions. Preliminary results suggest that the same groups identified by Garris et al. Rice, Oryza sativa, is a cultivated, inbreeding (2005) and Glaszmann (1987) are emerging in this species. It is estimated to have been domesticated study, providing strong support for the underlying in Asia approximately 10,000 years ago from a population sub-structure described to date. complex ancestral species, O. rufipogon, that inhabits diverse environments throughout Asia Population structure of O. rufipogon (Oka 1988; Vaughan et al. 2005). Two major sub- species within O. sativa have been recognized O. rufipogon is considered to be the progenitor of since ancient times, namely indica and japonica O. sativa and this is consistent with the fact that it (Matsuo et al. 1997). The time since divergence of is genetically more diverse than O. sativa (Sun the indica and japonica gene pools has been et al. 2002). It is found dispersed throughout a estimated as approximately 0.44 million years wide range of habitats across most of tropical and based on comparisons of genome sequence sub-tropical Asia. O. rufipogon, like O. sativa,is between Nipponbare (japonica) and cv 9311 comprised of genetically identifiable sub-popula- (indica) (Ma and Bennetzen 2004). This time tions that show strong geographical and ecological estimate, in conjunction with evidence from differentiation (Edwards 2005; Lu et al. 2002; fossilized remains of rice grains found in tombs Morishima et al. 1984; Oka and Morishima 1967). 123 Euphytica (2007) 154:317–339 319 Indica Tropical Japonica Aus Temperate Japonica Aromatic Fig. 1 Modified from Garris et al. (2005) showing unroot- (color < in the online version of this figure > ) of the ed Neighbor-joining (NJ) tree (Cavalli-Sforza 1967) branches of the tree corresponds to the observed chloro- developed using 169 nuclear SSRs and 234 landrace plast haplotype. Copyright permission granted by the accessions of O. sativa; the intensity of the grey shading Genetics Society of America There is recent evidence that the ancestry of exclusively on crosses between members of the the indica and japonica subgroups of O. sativa same sub-population (indica–indica) or between can be traced to specific geographically-defined related sub-populations (i.e., tropical japonica · O. rufipogon populations (Cheng et al. 2003; temperate japonica) (Lu et al. 2004; Ni et al. 2002; Edwards 2005; Londo et al. 2006). However, Sano 1993). This is largely due to the prevalence of admixture and introgression hybridization among sub-population incompatibilities that make it sub-populations and between cultivated and wild difficult to obtain a random array of fertile populations can obscure the picture (Cheng et al. recombinants from indica–japonica crosses 2003; Edwards 2005). Further, movement of wild (Harushima et al. 2002; Oka 1988; Sano 1993). rice seed accompanying that of landrace or elite Breeding programs based on indica–japonica O. sativa varieties complicates our understanding hybridization boast a few success stories, such as of ancestor–descendent relationships (Lu et al. the Tongil rice in Korea (Choi 1978; Choi et al. 2002). 1974) but are inevitably plagued by genome-wide incompatibilities that lead to hybrid breakdown Intra-specific breeding in rice and a persistent loss of recombinants in successive generations (Oka 1988). The phenomenon is A majority of the world’s rice is produced from reminiscent of Dobzhansky–Muller incompatibil- inbred (pure line) varieties and historically inbred ities (Dobzhansky 1936; Muller 1942) in which variety development has focused almost there is a gradual accumulation of mutations that 123 320 Euphytica (2007) 154:317–339 cause incompatible epistatic interactions when two for intra-specific crosses; when useful genes are species (or sub-species) are hybridized. The long- transferred from genetically distant (non AA- term consequences for rice breeders of restricting genome) species, the process is often encumbered crossing and population development to within by serious sterility barriers and anomalous patterns sub-population materials is that there is a limited of recombination (Ishii et al. 1994; Jena et al. 1992; pool of genetic variation available for identifying Wang et al. 2005). However, crosses within the AA new and useful combinations of genes. Over time, genome species are relatively easy to make and this aggravates the genetic bottlenecks that were avoid the major problems of sterility encountered initially created during the process of domestica- in more divergent crosses. In cases where linkage tion and leads to a cryptic form of genetic erosion drag is a problem, the use of molecular markers to that dramatically slows the rate of genetic gain. identify selected recombinant individuals that In contrast to the programs devoted to inbred retain only a very small piece of wild chromosome variety development, hybrid rice breeders have can greatly facilitate the transfer of desirable genes. explored a much larger portion of the genetic A major
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