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The Complex History of the Domestication of Rice

The Complex History of the Domestication of Rice Annals of Botany 100: 951–957, 2007 doi:10.1093/aob/mcm128, available online at www.aob.oxfordjournals.org REVIEW MEGAN SWEENEY and SUSAN McCOUCH* Department of Plant Breeding and Genetics, Cornell University, 161 Emerson Hall, Ithaca, NY 14850, USA Received: 13 December 2006 Returned for revision: 1 February 2007 Accepted: 22 May 2007 Published electronically: 6 July 2007 † Background Rice has been found in archaeological sites dating to 8000 BC, although the date of rice domestication is a matter of continuing debate. Two species of domesticated rice, Oryza sativa (Asian) and Oryza glaberrima (African) are grown globally. Numerous traits separate wild and domesticated rices including changes in: pericarp colour, dormancy, shattering, panicle architecture, tiller number, mating type and number and size of seeds. † Scope Genetic studies using diverse methodologies have uncovered a deep population structure within domesti- cated rice. Two main groups, the indica and japonica subspecies, have been identified with several subpopulations existing within each group. The antiquity of the divide has been estimated at more than 100 000 years ago. This date far precedes domestication, supporting independent domestications of indica and japonica from pre-differentiated pools of the wild ancestor. Crosses between subspecies display sterility and segregate for domestication traits, indi- cating that different populations are fixed for different networks of alleles conditioning these traits. Numerous dom- estication QTLs have been identified in crosses between the subspecies and in crosses between wild and domesticated accessions of rice. Many of the QTLs cluster in the same genomic regions, suggesting that a single gene with pleiotropic effects or that closely linked clusters of genes underlie these QTL. Recently, several domes- tication loci have been cloned from rice, including the gene controlling pericarp colour and two loci for shattering. The distribution and evolutionary history of these genes gives insight into the domestication process and the relation- ship between the subspecies. † Conclusions The evolutionary history of rice is complex, but recent work has shed light on the genetics of the transition from wild (O. rufipogon and O. nivara) to domesticated (O. sativa) rice. The types of genes involved and the geographic and genetic distribution of alleles will allow scientists to better understand our ancestors and breed better rice for our descendents. Key words: Oryza sativa, domestication, shattering, pericarp colour, QTL, subpopulation structure, subspecies. INTRODUCTION concentration in Asia, while O. glaberrima is grown in West Africa. Oryza rufipogon can be found throughout Rice is the world’s largest food crop, providing the caloric Asia and Oceania. Oryza barthii and O. longistaminata needs of millions of people daily. There are two distinct are African species, O. barthii endemic in West Africa types of domesticated rice, Oryza sativa, or Asian rice and O. longistaminata is found throughout Africa. Oryza and Oryza glaberrima, African rice, both of which have meridionalis is native to Australia and O. glumaepatula is unique domestication histories. In order to examine the endemic in Central and South America. Given these distri- variation selected by humans over our long relationship butions, it is easy to locate the ancestral pools from with rice, we must first look at the ancestors of our which modern rice were extracted. The African cultivars modern cultivars. The genus Oryza contains 21 wild rela- were domesticated from O. barthii (formally called tives of the domesticated rices (Vaughan et al., 2003). O. breviligulata) and O. sativa was domesticated The genus is divided into four species complexes: the from O. rufipogon. There is still continuing debate over O. sativa, O. officialis, O. ridelyi and O. granulata species whether O. rufipogon, the perennial species, O. nivara, complexes. All members of the Oryza genus have n ¼ the annual species, or possibly both were the direct ances- 12 chromosomes and while interspecific crossing is poss- tors of O. sativa. For the purpose of this review we will ible within each complex, it is difficult to recover fertile off- reserve judgment and refer to both the annual and perennial spring from crosses across complexes (Vaughan et al., forms as O. rufipogon. 2003). The O. sativa complex contains two domesticated Many phenotypic differences are obvious between species: O. sativa and O. glaberrima, and five or six wild O. sativa and its wild relatives (Xiao et al., 1998; Xiong species: O. rufipogon, O. nivara (also considered to be an et al., 1999; Bres-Patry et al., 2001; Cai and Morishima, ecotype of O. rufipogon), O. barthii, O. longistaminata, 2002; Thomson et al., 2003; Uga et al., 2003; Li et al., O. meridionalis and O. glumaepatula, all of which are 2006a) (Fig. 1). Wild rices typically display long awns diploids. Oryza sativa is distributed globally with a high and severe shattering for seed dispersal, whereas the dome- sticated type have short awns if any and reduced shattering to maximize the number of seeds that can be harvested. * For correspondence. E-mail srm4@cornell.edu # 2007 The Author(s) This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http:// creativecommons.org/licenses/by-nc/2.0/uk/) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited. 952 Sweeney and McCouch — Rice Domestication that can carry larger numbers of seeds than the wild ancestors. These phenotypes are not perfectly partitioned between wild and cultivated plants. While we refer to domestication ‘events’ it is important to remember that domestication was a process that occurred over an extended period of time. Genetic loci that were selected from existing genetic vari- ation in the wild species may appear fixed within domesti- cated rice, but will show variation within the wild rices. Although domestication traits are not favoured by natural selection, many of these traits are polygenic. A single allele promoting a more domesticated phenotype could be masked in the wild by a dominant allele at the same locus, or by alleles at other loci in the pathway, until a chance combination of different pre-existing wild alleles produces a plant with a domestication phenotype. This domesticated genotype would not survive long without arti- ficial selection, but the parents contributing the variation leading to the domesticated phenotype can have wild phenotypes which would not be selected against. Positive mutations that occurred later in the domestication process may be absent from the wild gene pool or early landraces, but would be ubiquitous among more recently developed cultivars. On-going gene flow between domesticated and wild rice further complicates the picture. We consider dom- estication traits to be those that are favoured by humans, occur at significantly higher frequencies in domesticated compared with wild rices, and adversely affect a plant’s ability to survive and reproduce without human assistance. Genes influencing these traits and showing signs of ancient selection are considered domestication genes. DOMESTICATION OF O. GLABERRIMA Linguistic evidence supports an African origin of O. glaberrima, as rice words in several west African language families (malo, maro, mano, etc.) predate the Portuguese-derived words associated with Asian rice FIG. 1. Wild and domesticated rice phenotypes. (A) Immature panicle (Blench, 2006; Porteres, 1970). Archaeologists have found from O. rufipogon showing open panicle structure; arrows indicate ceramic impressions of rice grains dating from 1800 BC to extruded stigmas. (B) Mature panicle from O. rufipogon showing dark 800 BC in Ganjigana located in north-east Nigera. These hulls and long awns; arrows indicate positions of seeds that have shattered. (C, F) Dehulled seed from O. rufipogon (C) and O. sativa (F). (D, E) go back to 1800 BC and continue through to 800 BC.At Grain-bearing O. sativa ssp. japonica (D) and ssp. indica (E) panicles the neighbouring site of Kursakata, scientist have uncovered with straw-coloured hulls with a closed panicle structure. abundant charred grains of rice dating from 1200 BC through to AD 0 (Klee et al., 2000). However, there is no evidence that the grains from either of these sites are dom- Dormancy levels are higher in the wild rices, allowing esticated and not wild rices. The oldest documented dom- viable seeds to persist for years before germination, but esticated O. glaberrima dates between 300 BC and 200 BC these have been reduced in cultivars to give uniform germi- and comes from Jenne-Jeno, Mali on the Inland Niger nation. The pericarp and seed coat of wild grains contain a Delta (McIntosh, 1995). Molecular data beginning with pigment giving them a red colour which modern Asian cul- isozyme studies and confirmed by simple sequence repeat tivars lack, but which many African cultivars retain. Seeds (SSR) and single nucleotide polymorphism (SNP) data, hulls are straw coloured in the domesticated but dark in the unequivocally demonstrate the uniqueness of African rice wilds. Mating habits differ, O. rufipogon and O. barthii are and its close genetic relationship to O. barthii (Second, partially outcrossing, with estimates ranging from 10 to 50 %, 1982; Semon et al., 2005). The centre of diversity for while O. sativa and O. glaberrima are almost entirely O. glaberrima is thought to be the upper Niger River inbreeding. Wild grains are consistently small while dome- Delta. Porteres (1970) hypothesized that O. glaberrima sticated grains vary in size. The panicle structure has was first cultivated in the floodwaters using floating rice changed from an open panicle with few secondary branches cultivars. Rice culture then spread to the brackish waters bearing relatively few grains, to a densely packed panicle using non-floating cultivars and subsequently further Sweeney and McCouch — Rice Domestication 953 selections were used to plant upland fields watered only by below 2 mm it is unlikely that they represent mature dom- rainfall. Asian rice was introduced into O. glaberrima’s esticated grains. Whether harvested as immature grains range after the initial domestication and the two species from a highly shattering plant or as mature grains from a are now sown side by side in West Africa (Dresch, 1949). non-shattering plant with thin O. rufipogon-type seeds Recently, breeders have crossed O. sativa and cannot be determined by this method. What can be docu- O. glaberrima, combining the stress-tolerance traits of mented is that seeds with measurements similar to O. glaberrima with the yield potential of O. sativa (Jones mature, modern O. sativa do not appear until 4500 BC at et al., 1997; Gridley et al., 2002). Known as NERICAs Chengtoushan in the Middle Yangzte and approx. 4000 BC (NEw RICe for Africa) these varieties have become in the Lower Yangzte area (Fuller et al., 2007). These popular among West African farmers. The remainder of seeds are certainly domesticated. Before this time the this review will focus on O. sativa, about which much genetic changes conditioning a lack of shattering and/or more is known. the mutations leading to thicker grains had not been selected. While these mutations are genetically indepen- dent, they result in the same grain width phenotype. ARCHAEOLOGICAL EVIDENCE OF Rice moved north to the Yellow River basin in Central O. SATIVA DOMESTICATION China beginning in 3000–2000 BC (Crawford, 2005). South The oldest archaeological evidence of rice use by humans of the Yangzi River, work in Taiwan and Vietnam date the has been found in the middle and lower Yangzi River earliest rice finds there to roughly the same time period, Valley region of China. Phytoliths, silicon microfossils of 2500–2000 BC (Higham and Lu, 1998). Archaeological plant cell structures, from rice have been found at the work in India uncovered the Neolithic site Lahuradewa in Xianrendong and Diotonghuan sites and dated to 11 000– the Ganges Valley containing evidence of rice consumption 12 000 BC (Zhao, 1998). Scientists have uncovered other dating to 7000–5000 BC (discussed in Fuller, 2006). sites in this region, including Shangshan, and Bashidang Archaeological studies have not yet been able to determine with significant quantities of rice remains, some dating whether this dispersal primarily consisted of a transfer of cul- back to 8000 BC (Higham and Lu, 1998; Pei, 1998; Jiang tivation technology that was applied to local wild rices, or if and Liu, 2006; Fuller, 2007). There is much debate over the domesticated varieties travelled with the paddy techno- whether or not the rice discovered at these sites represents logy. For the moment we turn to other lines of evidence to domesticated, cultivated rice, cultivated wild rices or if address the question of how many times rice was they are wild rices, which had been foraged from nature. domesticated. As improvements continue to be made in ancient DNA amplification techniques and more rice domestication POPULATION STRUCTURE IN ASIAN RICE genes are cloned, it may soon be possible to answer these questions directly. However, at present we must infer As early as the Chinese Han dynasty in China (approx. AD from indirect evidence. 100) there are have records of two different types of rice A few bone ‘spades’ were recovered at Kuahuqiao in the called Hsien and Keng (Matsuo et al., 1997). Today these lower Yangzi (6000–5400 BC), although the design indi- groups are commonly referred to the indica and japonica cates they would not have been used for heavy tillage subspecies respectively. The distinctness of these groups (Zhejiang Provincial Institute of Cultural Relics and has been confirmed by many different approaches over Archaeology, 2004; discussed in Fuller et al., 2007). the course of rice research. There are distinguishing mor- However the nearby Hemudu site (5000–4000 BC) contains phological features, including leaf colour, seed size and api- many bone scapulas which would be useful as spades or culus hair length, but the variation for these traits precludes hoes and are thought to have been used in rice cultivation using them to definitively classify varieties into subspecies (Chang, 1986; Fuller et al., 2007). Rice grains sieved (Kato et al., 1928; Oka, 1988). Researchers have also from the oldest known paddy fields in the lower Yangzi observed that progeny derived from crosses between these River Valley date to 4000 BC (Cao et al., 2006), giving groups exhibited sterility (Kato et al., 1928). A third clear-cut evidence for rice cultivation at this point in time. group or subpopulation was identified based on morphology Genetic changes causing the shift from wild to domesti- and was referred to as javanica (Matsuo, 1952). This group cated rice are harder to pinpoint. Mutations leading to a is now known as the tropical japonica subpopulation reduction in the degree of grain shattering are a perquisite (Glaszmann, 1987; Garris et al., 2005). Genetic analysis for domestication. Communities that foraged wild, shatter- by Morishima and Oka (1970, 1988), in addition to ing rice seeds would likely gather them before maturity Engle’s cytological studies (Engle, 1969), corroborated since most of the mature grains quickly fall to the the distinctness of the three rice groups previously estab- ground. Immature rice grains have a smaller width than lished by morphology. fully mature seeds, because rice grains reach their full Modern molecular methods have confirmed the ancient length early in seed development, and subsequent grain observations about divisions within O. sativa and added filling increases the width of the seeds. A survey of new levels of clarity to questions concerning the origins diverse modern rices has shown that mature modern culti- of rice. Isozymes were used to clearly differentiate the vated grains rarely have a width ,2 mm, although some indica and japonica groups within O. sativa, and suggested mature wild grains do (Fuller et al., 2007). Therefore, if further division within these two groups (Second, 1982; width of the assemblage of ancient grains from a site falls Glaszmann, 1987). Glazmann’s landmark study using 15 954 Sweeney and McCouch — Rice Domestication polymorphic loci on nearly 1700 diverse O. sativa varieties patterns of retrotransposon insertion (Ma and Bennetzen, identified six different groupings or subpopulations, indica, 2004; Vitte et al., 2004; Zhu and Ge, 2005). These dates japonica, aus, aromatic, rayada and ashina. This level of significantly predate the earliest archaeological evidence differentiation was not confirmed by the RFLP studies for rice consumption by humans. Taken together, the data which distinguish only the indica and japonica subspecies suggests that the O. rufipogon ancestor must have contained (Wang and Tanksley, 1989). A recent study using SSR at least two, possibly four, differentiated subgroups from markers examined 169 nuclear loci in 234 diverse acces- which different subpopulations were independently dom- sions of rice (Garris et al., 2005). This work identified esticated (Chang, 1976; Second, 1982; Wang et al., 1992; five major subpopulations: aus and indica, grouping Cheng et al., 2003; Garris et al., 2005). More research is within the traditional indica subspecies while the temperate needed to fully understand the domestication history of japonica, tropical japonica and aromatic subpopulations the different rice subpopulations. Understanding this popu- grouped within the japonica subspecies. These groupings lation structure is important because these gene pools rep- corresponded well with Glazmann’s original classification, resent valuable reservoirs of genetic variation and their and support the idea that O. sativa contains many geneti- effective use by both breeders and geneticists requires a cally distinct groups. The data from nuclear and chloroplast deeper understanding of the relationships between them. SSRs, as well as the isozymes, demonstrated that the In an effort to identify the geographical locations of aromatic subpopulation (associated with Basmati and different domestication events, Londo et al. (2006) exam- other types of high quality rice) was much more closely ined the geographical distribution of the sequence haplo- related genetically to the japonica subpopulations then to types at three genetic loci using a large collection of wild indica or aus. This is contrary to traditional classification, and domesticated rices (Londo et al., 2006). Looking at which had placed the aromatic group within the indica the sequence of the atpB-rbcL, p-VATPase and SAM subspecies based on the long-thin grains for which the genes, they compared indica and japonica haplotypes basmatic aromatics are known. with haplotypes from a geographically diverse panel of The F values provide a quantitative estimate of the degree O. rufipogon. While conclusions drawn from a sample of st of differentiation between subpopulations (Remington et al., three genes cannot be considered definitive, the data show 2001), The F values calculated in the Garris study are much an association between japonica-like haplotypes and wild st higher than those typically found for maize or other crops accessions from China and indica-like haplotypes and wild with a single domestication event (Garris et al., 2005). The accessions collected across the Himalayan Mountains in genetic divergence between the indica and japonica group- Thailand, India and neighbouring countries. Interestingly, ings have led many to conclude that these subspecies may some domesticated japonicas do not share a haplotype represent independent domestications from divergent pools with any O. rufipogon accessions, suggesting either that of O. rufipogon that had differentiated over thousands of the wild population that was ancestral to these japonicas years of geographical isolation. As more data about the was not sampled in this survey, or that it is now extinct. genetic distinctiveness of the aromatic and aus groups is This work suggests the subspecies separation was enforced gathered it has been proposed that these subpopulations by significant geographical barriers in addition to the may have also been independently domesticated from genetic sterility barriers. unique subpopulations of O. rufipogon (McCouch et al., 2006). Specifically, the fact that these groups contain QTLs between wild and domesticated unique alleles not found in other subpopulations of O. sativa argues against them having been selected from Many researches have made crosses between within these subpopulations (Jain et al., 2004; Garris et al., O. rufipogon and O. sativa cultivars looking for genes con- 2005). In contrast, the close genetic relationship between trolling domestication traits (Xiao et al., 1998; Xiong et al., the temperate and tropical japonica subpopulations (shared 1999; Bres-Patry et al., 2001; Cai and Morishima, 2002; alleles, though at different frequencies) suggests that these Thomson et al., 2003; Uga et al., 2003; Li et al., 2006a). groups are selections from a single genetic pool that have These studies have shown that domestication traits are influ- been adapted to different climatic conditions (Garris et al., enced by many different loci. Several researchers have 2005). Whether there are two or more than two domestication noted that QTLs for domestication traits tend to cluster events in O. sativa, independent domestications of the two within certain regions of the rice genome. The centromere major subspecies are supported by several lines of evidence. region of chromosome 7 is the site of QTLs for seed Genotyping of domesticated rice and wild relatives using colour, panicle structure, dormancy and shattering, among isozymes and RFLPs demonstrated that indica and japonica others (Xiong et al., 1999; Li et al., 2006a). Other clusters accessions were more closely related to different accessions for domestication traits have been reported on rice chromo- of O. rufipogon than to each other (Second, 1982; Wang somes 3, 4, 6, 8, 9, 11 and 12 (Cai and Morishima, 2002; Li et al., 1992). A recent study confirmed this result using et al., 2006a). This positional convergence may represent sequence haplotype analysis at three genetic loci (Londo clusters of domestication loci, or possibly major domesti- et al., 2006). With the complete genomic sequence from cation genes with pleiotrophic effects on many traits. both ‘Nipponbare’ ( japonica) and ‘9311’ (indica), three Based on the previously presented evidence of indepen- groups estimated that the indica and japonica subgroups dent domestications for indica and japonica we would diverged between 200 000 and 400 000 years ago (0 2– expect that different suites of genes and corresponding 0 4 mya) based on intronic sequence from four genes and mutations influencing domestication traits would have Sweeney and McCouch — Rice Domestication 955 been selected within the different subspecies or subpopu- Curiously, the non-shattering allele was present in all the lations. Therefore, when crosses are made between the O. sativa varieties surveyed, including members of indica, two subspecies, the offspring should segregate for wild tropical and temperate japonica subpopulations. If in fact alleles at several loci and wild characteristics should the domestications of the indica and japonica subspecies re-appear among sub-specific populations. This has, in were completely independent, we might expect mutations fact, been observed. Most notably for traits like dormancy at the same locus, but would not expect to see the same and shattering, intra-specific crosses between parents with functional polymorphisms at domestication loci. It is low dormancy and shattering give rise to progeny that highly unlikely that the same SNP would independently have higher levels of dormancy and shattering than either arise in both subspecies, and the likelihood decreases dra- parent (Lin et al., 1998; Miura et al., 2002; Longbiao matically when we consider the fact that all O. sativa varie- et al., 2004; Konishi et al., 2006). However, levels of dor- ties surveyed shared not only the functional SNP but five mancy and shattering in these crosses are not as high as other SNPs within the gene that differed among wild haplo- wild accessions, suggesting either that indica and japonica types. Independent mutations occurring in different genetic share some domestication alleles or that independent backgrounds would be expected to carry different signature mutations within the same domestication loci occurred in haplotypes across the target region. The fact that both the each subspecies which fail to compliment when crossed. FNP and the corresponding haplotypes were identical in Another confirmation that different domestication genes both indica and japonica cultivars at the sh4 locus provides were under selection in different subpopulations comes strong evidence for the conclusion that the allele arose once from QTL studies. Populations derived from crosses and then crossed the geographic and genetic barriers that between a single wild accession and diverse cultivars divide the two subspecies. Why the allele for non-shattering often identity different QTLs for domestication traits and not the non-shattering plants themselves was dispersed (Xiao et al., 1998; Moncada et al., 2001; Septiningsih is an interesting puzzle, suggesting that early farmers were et al., 2003; Thomson et al., 2003; McCouch et al., 2006; selecting for the non-shattering trait in combination with Xie et al., 2006). additional traits not found in the original non-shattering plants. Cloning other domestication genes and tracing their evolutionary history and patterns of distribution will allow us to determine whether introgression across subspe- Domestication genes that have been cloned cies is a common occurrence in the domestication of rice, or The large number of resources currently available to rice an isolated case for sh4. It is possible that one subspecies researches, not the least of which is genome sequence from was domesticated and subsequently was crossed to local representatives of both japonica (Nipponbare) and indica wild rices as it was carried to new locations. Heavy (93–11) cultivars (Goff et al., 2002; Yu et al., 2002), has natural and artificial selective pressures combined with resulted in an increase in the pace of gene cloning in rice. loss of progeny due to intra-specific sterility barriers Recently several groups have reported the cloning of between the indica and japonica genomes would give rise genes influencing traits associated with the domestication to plants that resembled the locally adapted wild species syndrome. but that contained a few valuable introgressions harbouring Two of these papers report the cloning of genes affecting domestication genes from the new introductions. shattering. The first of these papers looked at a cross Alternatively, domestication events in the subspecies may between the wild species O. nivara and an indica cultivar have been truly independent and when the early domesti- (Li et al., 2006b). QTL analysis of the F progeny from cates were grown in close proximity, they crossed. this cross identified three genomic regions affecting shatter- Beneficial alleles with a clear advantage were thus trans- ing. One of these regions, sh4, explained 69 % of the ferred and would have been the targets of selection by observed variation, and mapped to the same position early agriculturalists. where other large-effect shattering QTLs had been Despite a fixed sh4 allele within O. sativa there is signifi- mapped in previous studies. The effect of the locus was cant variation between and within subpopulations for so great that a single allele caused all mature grain on the degree of shattering. Traditionally, indicas have been panicle to drop when the panicle was simply tapped, reported to have higher shattering levels than japonicas while the absence of this allele required shaking to induce and, as mentioned above, crosses between indica and shattering. Fine mapping identified the gene underlying japonica display transgressive segregation for shattering this QTL as a Myb transcription factor and association (Konishi et al., 2006). This suggests that shattering alleles and transformation studies pinpointed the functional at loci other than sh4 are differentially fixed within each nucleotide polymorphism (FNP) to a single base pair of the two populations. The second group to clone a shatter- within the DNA binding domain of this gene. The non- ing gene worked with a cross between the aus variety, shattering allele was also found in several non-shattering Kasalath, and the temperate japonica variety, Nipponbare accessions of O. nivara. These accessions most likely rep- (Konishi et al., 2006). The mapped QTL, called qSH1 resent outcrosses with domesticated plants that transferred again explained 69 % of the variation between these two the non-shattering allele back into the wild germplasm, as domesticated groups. Fine mapping pinpointed the FNP to the non-shattering wild plants which were selected and an SNP 12 kb upstream of a BEL1-type homeobox gene further modified by human selections would have faced and the function of this promoter polymorphism was strong negative selective pressures in the wild. confirmed using transformation. In situ hybridization 956 Sweeney and McCouch — Rice Domestication temperate japonica weedy rice. Theoretical and Applied Genetics demonstrated that this change in the promoter region elimi- 102: 118–126. nated the expression of the homeobox gene at the provi- Cai W, Morishima H. 2002. 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The Complex History of the Domestication of Rice

Annals of Botany , Volume 100 (5) – Jul 6, 2007

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Annals of Botany 100: 951–957, 2007 doi:10.1093/aob/mcm128, available online at www.aob.oxfordjournals.org REVIEW MEGAN SWEENEY and SUSAN McCOUCH* Department of Plant Breeding and Genetics, Cornell University, 161 Emerson Hall, Ithaca, NY 14850, USA Received: 13 December 2006 Returned for revision: 1 February 2007 Accepted: 22 May 2007 Published electronically: 6 July 2007 † Background Rice has been found in archaeological sites dating to 8000 BC, although the date of rice domestication is a matter of continuing debate. Two species of domesticated rice, Oryza sativa (Asian) and Oryza glaberrima (African) are grown globally. Numerous traits separate wild and domesticated rices including changes in: pericarp colour, dormancy, shattering, panicle architecture, tiller number, mating type and number and size of seeds. † Scope Genetic studies using diverse methodologies have uncovered a deep population structure within domesti- cated rice. Two main groups, the indica and japonica subspecies, have been identified with several subpopulations existing within each group. The antiquity of the divide has been estimated at more than 100 000 years ago. This date far precedes domestication, supporting independent domestications of indica and japonica from pre-differentiated pools of the wild ancestor. Crosses between subspecies display sterility and segregate for domestication traits, indi- cating that different populations are fixed for different networks of alleles conditioning these traits. Numerous dom- estication QTLs have been identified in crosses between the subspecies and in crosses between wild and domesticated accessions of rice. Many of the QTLs cluster in the same genomic regions, suggesting that a single gene with pleiotropic effects or that closely linked clusters of genes underlie these QTL. Recently, several domes- tication loci have been cloned from rice, including the gene controlling pericarp colour and two loci for shattering. The distribution and evolutionary history of these genes gives insight into the domestication process and the relation- ship between the subspecies. † Conclusions The evolutionary history of rice is complex, but recent work has shed light on the genetics of the transition from wild (O. rufipogon and O. nivara) to domesticated (O. sativa) rice. The types of genes involved and the geographic and genetic distribution of alleles will allow scientists to better understand our ancestors and breed better rice for our descendents. Key words: Oryza sativa, domestication, shattering, pericarp colour, QTL, subpopulation structure, subspecies. INTRODUCTION concentration in Asia, while O. glaberrima is grown in West Africa. Oryza rufipogon can be found throughout Rice is the world’s largest food crop, providing the caloric Asia and Oceania. Oryza barthii and O. longistaminata needs of millions of people daily. There are two distinct are African species, O. barthii endemic in West Africa types of domesticated rice, Oryza sativa, or Asian rice and O. longistaminata is found throughout Africa. Oryza and Oryza glaberrima, African rice, both of which have meridionalis is native to Australia and O. glumaepatula is unique domestication histories. In order to examine the endemic in Central and South America. Given these distri- variation selected by humans over our long relationship butions, it is easy to locate the ancestral pools from with rice, we must first look at the ancestors of our which modern rice were extracted. The African cultivars modern cultivars. The genus Oryza contains 21 wild rela- were domesticated from O. barthii (formally called tives of the domesticated rices (Vaughan et al., 2003). O. breviligulata) and O. sativa was domesticated The genus is divided into four species complexes: the from O. rufipogon. There is still continuing debate over O. sativa, O. officialis, O. ridelyi and O. granulata species whether O. rufipogon, the perennial species, O. nivara, complexes. All members of the Oryza genus have n ¼ the annual species, or possibly both were the direct ances- 12 chromosomes and while interspecific crossing is poss- tors of O. sativa. For the purpose of this review we will ible within each complex, it is difficult to recover fertile off- reserve judgment and refer to both the annual and perennial spring from crosses across complexes (Vaughan et al., forms as O. rufipogon. 2003). The O. sativa complex contains two domesticated Many phenotypic differences are obvious between species: O. sativa and O. glaberrima, and five or six wild O. sativa and its wild relatives (Xiao et al., 1998; Xiong species: O. rufipogon, O. nivara (also considered to be an et al., 1999; Bres-Patry et al., 2001; Cai and Morishima, ecotype of O. rufipogon), O. barthii, O. longistaminata, 2002; Thomson et al., 2003; Uga et al., 2003; Li et al., O. meridionalis and O. glumaepatula, all of which are 2006a) (Fig. 1). Wild rices typically display long awns diploids. Oryza sativa is distributed globally with a high and severe shattering for seed dispersal, whereas the dome- sticated type have short awns if any and reduced shattering to maximize the number of seeds that can be harvested. * For correspondence. E-mail srm4@cornell.edu # 2007 The Author(s) This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http:// creativecommons.org/licenses/by-nc/2.0/uk/) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited. 952 Sweeney and McCouch — Rice Domestication that can carry larger numbers of seeds than the wild ancestors. These phenotypes are not perfectly partitioned between wild and cultivated plants. While we refer to domestication ‘events’ it is important to remember that domestication was a process that occurred over an extended period of time. Genetic loci that were selected from existing genetic vari- ation in the wild species may appear fixed within domesti- cated rice, but will show variation within the wild rices. Although domestication traits are not favoured by natural selection, many of these traits are polygenic. A single allele promoting a more domesticated phenotype could be masked in the wild by a dominant allele at the same locus, or by alleles at other loci in the pathway, until a chance combination of different pre-existing wild alleles produces a plant with a domestication phenotype. This domesticated genotype would not survive long without arti- ficial selection, but the parents contributing the variation leading to the domesticated phenotype can have wild phenotypes which would not be selected against. Positive mutations that occurred later in the domestication process may be absent from the wild gene pool or early landraces, but would be ubiquitous among more recently developed cultivars. On-going gene flow between domesticated and wild rice further complicates the picture. We consider dom- estication traits to be those that are favoured by humans, occur at significantly higher frequencies in domesticated compared with wild rices, and adversely affect a plant’s ability to survive and reproduce without human assistance. Genes influencing these traits and showing signs of ancient selection are considered domestication genes. DOMESTICATION OF O. GLABERRIMA Linguistic evidence supports an African origin of O. glaberrima, as rice words in several west African language families (malo, maro, mano, etc.) predate the Portuguese-derived words associated with Asian rice FIG. 1. Wild and domesticated rice phenotypes. (A) Immature panicle (Blench, 2006; Porteres, 1970). Archaeologists have found from O. rufipogon showing open panicle structure; arrows indicate ceramic impressions of rice grains dating from 1800 BC to extruded stigmas. (B) Mature panicle from O. rufipogon showing dark 800 BC in Ganjigana located in north-east Nigera. These hulls and long awns; arrows indicate positions of seeds that have shattered. (C, F) Dehulled seed from O. rufipogon (C) and O. sativa (F). (D, E) go back to 1800 BC and continue through to 800 BC.At Grain-bearing O. sativa ssp. japonica (D) and ssp. indica (E) panicles the neighbouring site of Kursakata, scientist have uncovered with straw-coloured hulls with a closed panicle structure. abundant charred grains of rice dating from 1200 BC through to AD 0 (Klee et al., 2000). However, there is no evidence that the grains from either of these sites are dom- Dormancy levels are higher in the wild rices, allowing esticated and not wild rices. The oldest documented dom- viable seeds to persist for years before germination, but esticated O. glaberrima dates between 300 BC and 200 BC these have been reduced in cultivars to give uniform germi- and comes from Jenne-Jeno, Mali on the Inland Niger nation. The pericarp and seed coat of wild grains contain a Delta (McIntosh, 1995). Molecular data beginning with pigment giving them a red colour which modern Asian cul- isozyme studies and confirmed by simple sequence repeat tivars lack, but which many African cultivars retain. Seeds (SSR) and single nucleotide polymorphism (SNP) data, hulls are straw coloured in the domesticated but dark in the unequivocally demonstrate the uniqueness of African rice wilds. Mating habits differ, O. rufipogon and O. barthii are and its close genetic relationship to O. barthii (Second, partially outcrossing, with estimates ranging from 10 to 50 %, 1982; Semon et al., 2005). The centre of diversity for while O. sativa and O. glaberrima are almost entirely O. glaberrima is thought to be the upper Niger River inbreeding. Wild grains are consistently small while dome- Delta. Porteres (1970) hypothesized that O. glaberrima sticated grains vary in size. The panicle structure has was first cultivated in the floodwaters using floating rice changed from an open panicle with few secondary branches cultivars. Rice culture then spread to the brackish waters bearing relatively few grains, to a densely packed panicle using non-floating cultivars and subsequently further Sweeney and McCouch — Rice Domestication 953 selections were used to plant upland fields watered only by below 2 mm it is unlikely that they represent mature dom- rainfall. Asian rice was introduced into O. glaberrima’s esticated grains. Whether harvested as immature grains range after the initial domestication and the two species from a highly shattering plant or as mature grains from a are now sown side by side in West Africa (Dresch, 1949). non-shattering plant with thin O. rufipogon-type seeds Recently, breeders have crossed O. sativa and cannot be determined by this method. What can be docu- O. glaberrima, combining the stress-tolerance traits of mented is that seeds with measurements similar to O. glaberrima with the yield potential of O. sativa (Jones mature, modern O. sativa do not appear until 4500 BC at et al., 1997; Gridley et al., 2002). Known as NERICAs Chengtoushan in the Middle Yangzte and approx. 4000 BC (NEw RICe for Africa) these varieties have become in the Lower Yangzte area (Fuller et al., 2007). These popular among West African farmers. The remainder of seeds are certainly domesticated. Before this time the this review will focus on O. sativa, about which much genetic changes conditioning a lack of shattering and/or more is known. the mutations leading to thicker grains had not been selected. While these mutations are genetically indepen- dent, they result in the same grain width phenotype. ARCHAEOLOGICAL EVIDENCE OF Rice moved north to the Yellow River basin in Central O. SATIVA DOMESTICATION China beginning in 3000–2000 BC (Crawford, 2005). South The oldest archaeological evidence of rice use by humans of the Yangzi River, work in Taiwan and Vietnam date the has been found in the middle and lower Yangzi River earliest rice finds there to roughly the same time period, Valley region of China. Phytoliths, silicon microfossils of 2500–2000 BC (Higham and Lu, 1998). Archaeological plant cell structures, from rice have been found at the work in India uncovered the Neolithic site Lahuradewa in Xianrendong and Diotonghuan sites and dated to 11 000– the Ganges Valley containing evidence of rice consumption 12 000 BC (Zhao, 1998). Scientists have uncovered other dating to 7000–5000 BC (discussed in Fuller, 2006). sites in this region, including Shangshan, and Bashidang Archaeological studies have not yet been able to determine with significant quantities of rice remains, some dating whether this dispersal primarily consisted of a transfer of cul- back to 8000 BC (Higham and Lu, 1998; Pei, 1998; Jiang tivation technology that was applied to local wild rices, or if and Liu, 2006; Fuller, 2007). There is much debate over the domesticated varieties travelled with the paddy techno- whether or not the rice discovered at these sites represents logy. For the moment we turn to other lines of evidence to domesticated, cultivated rice, cultivated wild rices or if address the question of how many times rice was they are wild rices, which had been foraged from nature. domesticated. As improvements continue to be made in ancient DNA amplification techniques and more rice domestication POPULATION STRUCTURE IN ASIAN RICE genes are cloned, it may soon be possible to answer these questions directly. However, at present we must infer As early as the Chinese Han dynasty in China (approx. AD from indirect evidence. 100) there are have records of two different types of rice A few bone ‘spades’ were recovered at Kuahuqiao in the called Hsien and Keng (Matsuo et al., 1997). Today these lower Yangzi (6000–5400 BC), although the design indi- groups are commonly referred to the indica and japonica cates they would not have been used for heavy tillage subspecies respectively. The distinctness of these groups (Zhejiang Provincial Institute of Cultural Relics and has been confirmed by many different approaches over Archaeology, 2004; discussed in Fuller et al., 2007). the course of rice research. There are distinguishing mor- However the nearby Hemudu site (5000–4000 BC) contains phological features, including leaf colour, seed size and api- many bone scapulas which would be useful as spades or culus hair length, but the variation for these traits precludes hoes and are thought to have been used in rice cultivation using them to definitively classify varieties into subspecies (Chang, 1986; Fuller et al., 2007). Rice grains sieved (Kato et al., 1928; Oka, 1988). Researchers have also from the oldest known paddy fields in the lower Yangzi observed that progeny derived from crosses between these River Valley date to 4000 BC (Cao et al., 2006), giving groups exhibited sterility (Kato et al., 1928). A third clear-cut evidence for rice cultivation at this point in time. group or subpopulation was identified based on morphology Genetic changes causing the shift from wild to domesti- and was referred to as javanica (Matsuo, 1952). This group cated rice are harder to pinpoint. Mutations leading to a is now known as the tropical japonica subpopulation reduction in the degree of grain shattering are a perquisite (Glaszmann, 1987; Garris et al., 2005). Genetic analysis for domestication. Communities that foraged wild, shatter- by Morishima and Oka (1970, 1988), in addition to ing rice seeds would likely gather them before maturity Engle’s cytological studies (Engle, 1969), corroborated since most of the mature grains quickly fall to the the distinctness of the three rice groups previously estab- ground. Immature rice grains have a smaller width than lished by morphology. fully mature seeds, because rice grains reach their full Modern molecular methods have confirmed the ancient length early in seed development, and subsequent grain observations about divisions within O. sativa and added filling increases the width of the seeds. A survey of new levels of clarity to questions concerning the origins diverse modern rices has shown that mature modern culti- of rice. Isozymes were used to clearly differentiate the vated grains rarely have a width ,2 mm, although some indica and japonica groups within O. sativa, and suggested mature wild grains do (Fuller et al., 2007). Therefore, if further division within these two groups (Second, 1982; width of the assemblage of ancient grains from a site falls Glaszmann, 1987). Glazmann’s landmark study using 15 954 Sweeney and McCouch — Rice Domestication polymorphic loci on nearly 1700 diverse O. sativa varieties patterns of retrotransposon insertion (Ma and Bennetzen, identified six different groupings or subpopulations, indica, 2004; Vitte et al., 2004; Zhu and Ge, 2005). These dates japonica, aus, aromatic, rayada and ashina. This level of significantly predate the earliest archaeological evidence differentiation was not confirmed by the RFLP studies for rice consumption by humans. Taken together, the data which distinguish only the indica and japonica subspecies suggests that the O. rufipogon ancestor must have contained (Wang and Tanksley, 1989). A recent study using SSR at least two, possibly four, differentiated subgroups from markers examined 169 nuclear loci in 234 diverse acces- which different subpopulations were independently dom- sions of rice (Garris et al., 2005). This work identified esticated (Chang, 1976; Second, 1982; Wang et al., 1992; five major subpopulations: aus and indica, grouping Cheng et al., 2003; Garris et al., 2005). More research is within the traditional indica subspecies while the temperate needed to fully understand the domestication history of japonica, tropical japonica and aromatic subpopulations the different rice subpopulations. Understanding this popu- grouped within the japonica subspecies. These groupings lation structure is important because these gene pools rep- corresponded well with Glazmann’s original classification, resent valuable reservoirs of genetic variation and their and support the idea that O. sativa contains many geneti- effective use by both breeders and geneticists requires a cally distinct groups. The data from nuclear and chloroplast deeper understanding of the relationships between them. SSRs, as well as the isozymes, demonstrated that the In an effort to identify the geographical locations of aromatic subpopulation (associated with Basmati and different domestication events, Londo et al. (2006) exam- other types of high quality rice) was much more closely ined the geographical distribution of the sequence haplo- related genetically to the japonica subpopulations then to types at three genetic loci using a large collection of wild indica or aus. This is contrary to traditional classification, and domesticated rices (Londo et al., 2006). Looking at which had placed the aromatic group within the indica the sequence of the atpB-rbcL, p-VATPase and SAM subspecies based on the long-thin grains for which the genes, they compared indica and japonica haplotypes basmatic aromatics are known. with haplotypes from a geographically diverse panel of The F values provide a quantitative estimate of the degree O. rufipogon. While conclusions drawn from a sample of st of differentiation between subpopulations (Remington et al., three genes cannot be considered definitive, the data show 2001), The F values calculated in the Garris study are much an association between japonica-like haplotypes and wild st higher than those typically found for maize or other crops accessions from China and indica-like haplotypes and wild with a single domestication event (Garris et al., 2005). The accessions collected across the Himalayan Mountains in genetic divergence between the indica and japonica group- Thailand, India and neighbouring countries. Interestingly, ings have led many to conclude that these subspecies may some domesticated japonicas do not share a haplotype represent independent domestications from divergent pools with any O. rufipogon accessions, suggesting either that of O. rufipogon that had differentiated over thousands of the wild population that was ancestral to these japonicas years of geographical isolation. As more data about the was not sampled in this survey, or that it is now extinct. genetic distinctiveness of the aromatic and aus groups is This work suggests the subspecies separation was enforced gathered it has been proposed that these subpopulations by significant geographical barriers in addition to the may have also been independently domesticated from genetic sterility barriers. unique subpopulations of O. rufipogon (McCouch et al., 2006). Specifically, the fact that these groups contain QTLs between wild and domesticated unique alleles not found in other subpopulations of O. sativa argues against them having been selected from Many researches have made crosses between within these subpopulations (Jain et al., 2004; Garris et al., O. rufipogon and O. sativa cultivars looking for genes con- 2005). In contrast, the close genetic relationship between trolling domestication traits (Xiao et al., 1998; Xiong et al., the temperate and tropical japonica subpopulations (shared 1999; Bres-Patry et al., 2001; Cai and Morishima, 2002; alleles, though at different frequencies) suggests that these Thomson et al., 2003; Uga et al., 2003; Li et al., 2006a). groups are selections from a single genetic pool that have These studies have shown that domestication traits are influ- been adapted to different climatic conditions (Garris et al., enced by many different loci. Several researchers have 2005). Whether there are two or more than two domestication noted that QTLs for domestication traits tend to cluster events in O. sativa, independent domestications of the two within certain regions of the rice genome. The centromere major subspecies are supported by several lines of evidence. region of chromosome 7 is the site of QTLs for seed Genotyping of domesticated rice and wild relatives using colour, panicle structure, dormancy and shattering, among isozymes and RFLPs demonstrated that indica and japonica others (Xiong et al., 1999; Li et al., 2006a). Other clusters accessions were more closely related to different accessions for domestication traits have been reported on rice chromo- of O. rufipogon than to each other (Second, 1982; Wang somes 3, 4, 6, 8, 9, 11 and 12 (Cai and Morishima, 2002; Li et al., 1992). A recent study confirmed this result using et al., 2006a). This positional convergence may represent sequence haplotype analysis at three genetic loci (Londo clusters of domestication loci, or possibly major domesti- et al., 2006). With the complete genomic sequence from cation genes with pleiotrophic effects on many traits. both ‘Nipponbare’ ( japonica) and ‘9311’ (indica), three Based on the previously presented evidence of indepen- groups estimated that the indica and japonica subgroups dent domestications for indica and japonica we would diverged between 200 000 and 400 000 years ago (0 2– expect that different suites of genes and corresponding 0 4 mya) based on intronic sequence from four genes and mutations influencing domestication traits would have Sweeney and McCouch — Rice Domestication 955 been selected within the different subspecies or subpopu- Curiously, the non-shattering allele was present in all the lations. Therefore, when crosses are made between the O. sativa varieties surveyed, including members of indica, two subspecies, the offspring should segregate for wild tropical and temperate japonica subpopulations. If in fact alleles at several loci and wild characteristics should the domestications of the indica and japonica subspecies re-appear among sub-specific populations. This has, in were completely independent, we might expect mutations fact, been observed. Most notably for traits like dormancy at the same locus, but would not expect to see the same and shattering, intra-specific crosses between parents with functional polymorphisms at domestication loci. It is low dormancy and shattering give rise to progeny that highly unlikely that the same SNP would independently have higher levels of dormancy and shattering than either arise in both subspecies, and the likelihood decreases dra- parent (Lin et al., 1998; Miura et al., 2002; Longbiao matically when we consider the fact that all O. sativa varie- et al., 2004; Konishi et al., 2006). However, levels of dor- ties surveyed shared not only the functional SNP but five mancy and shattering in these crosses are not as high as other SNPs within the gene that differed among wild haplo- wild accessions, suggesting either that indica and japonica types. Independent mutations occurring in different genetic share some domestication alleles or that independent backgrounds would be expected to carry different signature mutations within the same domestication loci occurred in haplotypes across the target region. The fact that both the each subspecies which fail to compliment when crossed. FNP and the corresponding haplotypes were identical in Another confirmation that different domestication genes both indica and japonica cultivars at the sh4 locus provides were under selection in different subpopulations comes strong evidence for the conclusion that the allele arose once from QTL studies. Populations derived from crosses and then crossed the geographic and genetic barriers that between a single wild accession and diverse cultivars divide the two subspecies. Why the allele for non-shattering often identity different QTLs for domestication traits and not the non-shattering plants themselves was dispersed (Xiao et al., 1998; Moncada et al., 2001; Septiningsih is an interesting puzzle, suggesting that early farmers were et al., 2003; Thomson et al., 2003; McCouch et al., 2006; selecting for the non-shattering trait in combination with Xie et al., 2006). additional traits not found in the original non-shattering plants. Cloning other domestication genes and tracing their evolutionary history and patterns of distribution will allow us to determine whether introgression across subspe- Domestication genes that have been cloned cies is a common occurrence in the domestication of rice, or The large number of resources currently available to rice an isolated case for sh4. It is possible that one subspecies researches, not the least of which is genome sequence from was domesticated and subsequently was crossed to local representatives of both japonica (Nipponbare) and indica wild rices as it was carried to new locations. Heavy (93–11) cultivars (Goff et al., 2002; Yu et al., 2002), has natural and artificial selective pressures combined with resulted in an increase in the pace of gene cloning in rice. loss of progeny due to intra-specific sterility barriers Recently several groups have reported the cloning of between the indica and japonica genomes would give rise genes influencing traits associated with the domestication to plants that resembled the locally adapted wild species syndrome. but that contained a few valuable introgressions harbouring Two of these papers report the cloning of genes affecting domestication genes from the new introductions. shattering. The first of these papers looked at a cross Alternatively, domestication events in the subspecies may between the wild species O. nivara and an indica cultivar have been truly independent and when the early domesti- (Li et al., 2006b). QTL analysis of the F progeny from cates were grown in close proximity, they crossed. this cross identified three genomic regions affecting shatter- Beneficial alleles with a clear advantage were thus trans- ing. One of these regions, sh4, explained 69 % of the ferred and would have been the targets of selection by observed variation, and mapped to the same position early agriculturalists. where other large-effect shattering QTLs had been Despite a fixed sh4 allele within O. sativa there is signifi- mapped in previous studies. The effect of the locus was cant variation between and within subpopulations for so great that a single allele caused all mature grain on the degree of shattering. Traditionally, indicas have been panicle to drop when the panicle was simply tapped, reported to have higher shattering levels than japonicas while the absence of this allele required shaking to induce and, as mentioned above, crosses between indica and shattering. Fine mapping identified the gene underlying japonica display transgressive segregation for shattering this QTL as a Myb transcription factor and association (Konishi et al., 2006). This suggests that shattering alleles and transformation studies pinpointed the functional at loci other than sh4 are differentially fixed within each nucleotide polymorphism (FNP) to a single base pair of the two populations. The second group to clone a shatter- within the DNA binding domain of this gene. The non- ing gene worked with a cross between the aus variety, shattering allele was also found in several non-shattering Kasalath, and the temperate japonica variety, Nipponbare accessions of O. nivara. These accessions most likely rep- (Konishi et al., 2006). The mapped QTL, called qSH1 resent outcrosses with domesticated plants that transferred again explained 69 % of the variation between these two the non-shattering allele back into the wild germplasm, as domesticated groups. Fine mapping pinpointed the FNP to the non-shattering wild plants which were selected and an SNP 12 kb upstream of a BEL1-type homeobox gene further modified by human selections would have faced and the function of this promoter polymorphism was strong negative selective pressures in the wild. confirmed using transformation. In situ hybridization 956 Sweeney and McCouch — Rice Domestication temperate japonica weedy rice. Theoretical and Applied Genetics demonstrated that this change in the promoter region elimi- 102: 118–126. nated the expression of the homeobox gene at the provi- Cai W, Morishima H. 2002. 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Published: Jul 6, 2007

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