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Evolutionary History of GS3, a Gene Conferring Grain Length in Rice

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Evolutionary History of GS3, a Gene Conferring Grain Length in Rice Copyright Ó 2009 by the Genetics Society of America DOI: 10.1534/genetics.109.103002 Evolutionary History of GS3, a Gene Conferring Grain Length in Rice Noriko Takano-Kai,*,1 Hui Jiang,†,1,2 Takahiko Kubo,*,3 Megan Sweeney,†,4 Takashi Matsumoto,§ Hiroyuki Kanamori,** Badri Padhukasahasram,†† Carlos Bustamante,†† Atsushi Yoshimura,* Kazuyuki Doi*,5 and Susan McCouch†,6 *Faculty of Agriculture, Kyushu University, Fukuoka 812-8581, Japan, †Department of Plant Breeding and Genetics, Cornell University, Ithaca, New York 14853, §Division of Genome and Biodiversity Research, National Institute of Agrobiological Sciences, Tsukuba, Ibaraki 305-8602, Japan, **Institute of Society for Techno-Innovation of Agriculture, Forestry, and Fisheries, Tsukuba, 305-0854, Japan and ††Department of Biological Statistics and Computational Biology, Cornell University, Ithaca, New York 14853 Manuscript received March 27, 2009 Accepted for publication May 24, 2009 ABSTRACT Unlike maize and wheat, where artificial selection is associated with an almost uniform increase in seed or grain size, domesticated rice exhibits dramatic phenotypic diversity for grain size and shape. Here we clone and characterize GS3, an evolutionarily important gene controlling grain size in rice. We show that GS3 is highly expressed in young panicles in both short- and long-grained varieties but is not expressed in leaves or panicles after flowering, and we use genetic transformation to demonstrate that the dominant allele for short grain complements the long-grain phenotype. An association study revealed that a C to A mutation in the second exon of GS3 (A allele) was associated with enhanced grain length in Oryza sativa but was absent from other Oryza species. Linkage disequilibrium (LD) was elevated and there was a 95.7% reduction in nucleotide diversity (up) across the gene in accessions carrying the A allele, suggesting positive selection for long grain. Haplotype analysis traced the origin of the long-grain allele to a Japonica- like ancestor and demonstrated introgression into the Indica gene pool. This study indicates a critical role for GS3 in defining the seed morphologies of modern subpopulations of O. sativa and enhances the potential for genetic manipulation of grain size in rice. EED size and seed number are the major determi- that are sold largely in processed forms, the physical S nants of crop yield in both the cereals and the properties of rice grains are immediately obvious to grain legumes. Seed size was also a target of artificial consumers (Fitzgerald et al. 2009). Thus, rice offers a selection during domestication, where large seeds are unique opportunity to investigate the genetics and generally favored due to ease of harvesting and en- evolutionary history of seed size and shape. hanced seedling vigor (Harlan et al. 1972). In rice, Cultivated rice (Oryza sativa) was domesticated in Asia traits related to grain size and appearance have a large from the wild progenitor O. rufipogon Griff. and/or O. impact on market value and play a pivotal role in the nivara Sharma (Ishii et al. 1988; Oka 1988; Dally and adoption of new varieties (Champagne et al. 1999; Second 1990; Nakano et al. 1992; Chen et al. 1993). Juliano 2003). However, different grain quality traits Classical studies of the subpopulation structure of O. are prized by different local cultures and cuisines and, sativa have identified two primary subspecies or varietal unlike other cereals such as wheat, barley, and maize groups, namely Indica and Japonica (Oka 1988; Wang and Tanksley 1989; Sun et al. 2002). Studies that have dated the divergence between the Indica and the Sequence data from this article have been deposited with the DDBJ/ Japonica groups indicate that it predates rice domestica- GenBank Data Libraries under accession nos. AB488612–AB488665. tion by at least 100,000 years (Ma and Bennetzen 2004; Supporting information is available online at http://www.genetics.org/ Vitte et al. 2004; Zhu and Ge 2005), suggesting that at cgi/content/full/genetics.109.103002/DC1. least two genetically distinct gene pools of O. rufipogon 1 These authors contributed equally to this work. were cultivated and subsequently domesticated. 2Present address: Chengdu Institute of Biology, Chinese Academy of Sciences, Chengdu, Sichuan 610041, P. R. China. Isozyme and DNA studies revealed that there is 3Present address: Plant Genetics Laboratory, National Institute of additional genetic structure within these two groups, Genetics, Mishima, Shizuoka 411-8540, Japan. with three subpopulations composing the Japonica 4Present address: Department of Plant Sciences, University of Arizona, varietal group (temperate japonica, tropical japonica, and Tucson, Arizona, 85721. aromatic, written all in lowercase) and two subpopula- 5 Present address: Graduate School of Bioagricultural Sciences, Nagoya tions composing the Indica group (indica and aus) University, Chikusa, Nagoya 464-8601, Japan. econd laszmann arris 6Corresponding author: Cornell University, 162 Emerson Hall, Ithaca, (S 1985; G 1987; G et al. 2005; NY 14853-1901. E-mail: [email protected] Caicedo et al. 2007). While there is great diversity of Genetics 182: 1323–1334 (August 2009) 1324 N. Takano-Kai et al. seed size and shape both within and between the dominant allele for small seed size at this locus. Com- different subpopulations of O. sativa, each subpopula- parative mapping of QTL controlling seed weight in tion is popularly associated with a characteristic seed rice, maize, and sorghum further suggested that orthol- morphology. Temperate japonica varieties are known for ogous seed size genes at this locus might be associated their short, round grains, indica and aus for slender with domestication in all three crops (Paterson et al. grains, and within the aromatic subpopulation [hereaf- 1995). ter referred to as Group V varieties, according to the In the current study, we used positional cloning and isozyme group designation (Glaszmann 1987)] the transformation to demonstrate that the GS3 gene group of basmati varieties is highly valued for their very underlies both the gw3.1 QTL (Thomson et al. 2003; long, slender grains (Juliano and Villareal 1993). Li et al. 2004) and the lk3 QTL (Kubo et al. 2001). In Identification of the genes that control the range of transformation experiments, we demonstrated for the seed size variation in rice will offer opportunities to first time that the dominant allele for small grain size study the evolutionary history and phenotypic diversifi- complements the long-grain phenotype and we charac- cation of the five subpopulations within O. sativa and terized the spatial expression patterns of the gene at also provide valuable targets for genetic manipulation. different developmental stages. We undertook an asso- In rice, four genes contributing to seed or grain size ciation analysis to examine the relationship between the have been identified and characterized. The first, grain alleles at GS3 and the observed variation for grain size 3 (GS3), was isolated from an indica 3 indica length/size in both wild and cultivated rice. Finally, we population and found to encode a novel protein with examined sequence haplotypes across the GS3 region to several conserved domains including a phosphatidyl- look for evidence of selection and to identify the origin ethanolamine-binding protein (PEBP)-like domain, a of the mutation leading to increased grain length in transmembrane region, a putative tumor necrosis factor O. sativa. receptor/nerve growth factor receptor (TNFR/NGFR) family domain, and a von Willebrand factor type C (VWFC) domain (Fan et al. 2006). A second gene, grain MATERIALS AND METHODS weight 2 (GW2), was found to encode an unknown RING- Fine mapping of gw3.1 and lk3: A total of 4148 BC5F2 type protein with E3 ubiquitin ligase activity (Song et al. individuals derived from a cross between Jefferson 3 O. 2007). The third, grain incomplete filling 1 (GIF1), rufipogon and 1641 BC3F3 plants derived from a cross between encodes a cell-wall invertase required for carbon parti- Asominori 3 IR24 were screened for recombinants within ang target regions defined by the QTL gw3.1 and lk3, respectively. tioning during early grain filling (W et al. 2008). Plants from the Jefferson 3 O. rufipogon population were Finally, the recently characterized seed width 5 (SW5) has grown in 2-inch-deep pots in the Guterman greenhouse of no apparent homolog in the database but was shown to Cornell University. Plants from the Asominori 3 IR24 pop- interact with polyubiquitin in a yeast two-hybrid assay; ulation were grown at University Farm, Kyushu University, thus it likely acts in the ubiquitin–proteasome pathway Japan. Once informative recombinants were identified, seed- lings of recombinants and parental controls were transplanted to regulate cell division during seed development and allowed to set seeds. The seed length phenotype was (Shomura et al. 2008; Weng et al. 2008). evaluated using seeds harvested from primary panicles. Seeds Many genes controlling seed size have also been from the gw3.1 population were measured using a digital identified in Arabidopsis and tomato, providing a frame- caliper as described (Li et al. 2004) and seed lengths from the work for assembling the genetic pathway that determines lk3 population were determined by visual observation. Prog- haudhury eny testing was conducted as necessary. this trait in dicotyledonous plants (C et al. Additional DNA markers were designed and used to detect 2001; Jofuku et al. 2005; Ohto et al. 2005; Sundaresan recombination break points. Simple sequence repeat (SSR) 2005; Schruff et al. 2006; Yoine et al. 2006; Roxrud et al. markers were designed using the SSRIT tool [(Temnykh et al. 2007; Li et al. 2008; Xiao et al. 2008; Orsi and Tanksley 2000) http://www.gramene.org/db/markers/ssrtool] and the 2009; Zhou et al. 2009). Several of these genes show publicly available Nipponbare genome sequence (http:// rice.plantbiology.msu.edu/). SSR and indel markers were maternal control by regulating endosperm and/or ovule amplified using standard PCR protocols. Cleaved amplified development (Garcia et al.
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