The species of the genus Oryza and transfer of useful genes from wild species into cultivated rice, O. sativa
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1 Breeding Science 60: (2010) doi: /jsbbs Review The species of the genus Oryza and transfer of useful genes from wild species into cultivated rice, O. sativa Kshirod K. Jena* 1) 1) Plant Breeding, Genetics and Biotechnology Division, International Rice Research Institute, C/o National Institute of Crop Science, Rural Development Administration, Suwon , Republic of Korea The genus Oryza has 24 species out of which two are cultivated (O. sativa and O. glaberrima) and 22 are wild species. Of the 22 wild species, six are in the primary gene pool of O. sativa complex and these wild species are easily crossable with the major cultivated species. These have the same AA genome as O. sativa. However, there are 10 wild species under O. officinalis complex having BB, CC, BBCC, CCDD, EE and FF genomes. The wild species of this complex are in the secondary gene pool and are cross incompatible with O. sativa. There are six most distantly related wild species with either diploids or tetraploids of GG, HHJJ and HHKK genomes and are highly cross incompatible with O. sativa. All the 22 wild species of Oryza are a vast reservoir of genes for biotic and abiotic stresses resistance. Some of the yield enhancing traits/genes from AA genome wild species have been identified and mapped with molecular markers for their integration into O. sativa genome. A broad-spectrum resistance gene for bacterial blight resistance (Xa21) has been identified in O. longistaminata and introduced into many rice cultivars. Advances in biotechnology have facilitated the development of interspecific hybrids between O. sativa and wild species of secondary and tertiary gene pools. Some important genes Pi40 and Bph18 for resistance to blast and brown planthopper, respectively, have been successfully transferred into elite cultivars from O. australiensis and the function of one blast resistance gene (Pi9) derived from O. minuta is elucidated. Many important genes from the most distantly related wild species such as O. alta, O. granulata, O. longiglumis and O. coarctata are expected to be transferred into cultivated rice in the future using the latest tools of molecular genetics and biotechnology. Key Words: Rice, wild species, genus Oryza, genes. Introduction Communicated by H. Yasui Received September 30, Accepted October 31, *Corresponding author ( k.jena@cgiar.org) Rice (Oryza sativa L.) is the most economically important food crop in the world and provides two third of calorie intake of more than three billion people in Asia and one-third of calorie intake of nearly 1.5 billion people in Africa and Latin America (Khush 2005). Rice is cultivated worldwide under various agro-climatic conditions. However, rice production in recent years has been affected seriously by major biotic and abiotic stresses due to adverse climatic change and breakdown of resistance genes in elite cultivars (Normile 2008). The genetic variability for resistance or tolerance to biotic stresses is limited in cultivated rice gene pool but abundantly present in the gene pools of wild species belonging to the genus Oryza. There is an urgent need to broaden the gene pool of cultivated rice by transferring valuable genes from wild species for enhancing resistance/tolerance to biotic and abiotic stresses and eventually increase yield potential of modern cultivars. The objective of this paper is to discuss the status of the species in the genus Oryza and the transfer of high value genes present in wild species into rice cultivars using the tools of modern biotechnology and genetics. Wild species of Oryza The genus Oryza of the Gramineae family has 24 species. Two of the 24 species, O. sativa L. and O. glaberrima Steud., are cultivated cereals and 22 are wild species distributed in different geographic locations worldwide (Khush 1997, Vaughan 1989). O. sativa is cultivated as a major cereal crop in most parts of Asia and consumed as a staple food. The African cultivated rice, O. glaberrima is grown in small areas in West Africa. O. sativa has two subspecies: japonica and indica. The subspecies japonica has a narrow genetic resources compared to indica subspecies which has a wide genetic diversity. Oryza wild species were classified into three main groups or complexes based on the ease of
2 Genus Oryza and transfer of useful genes from wild species 519 gene transfer from wild species into cultivated rice. These are: (1) O. sativa complex, (2) O. officinalis complex. (3) O. meyeriana and O. ridleyi complex (Morishima and Oka 1960). These groups/complexes were later named as primary, secondary and tertiary gene pools of Oryza, respectively (Khush 1997). The O. sativa complex has two cultivated species and six wild species with the AA genome (Table 1). These species are diploid, cross compatible and show homologous chromosome pairing. The perennial wild species, O. rufipogon is the progenitor of the cultivated Asian rice O. sativa while O. barthii is the progenitor of the cultivated African rice O. glaberrima (Chang 1976, Oka 1988, Vaughan et al. 2008, Zhu and Ge 2005). Of the two Asian wild species, the perennial O. rufipogon is distributed throughout tropical Asia and Oceania, whereas the annual O. nivara is restricted to tropical continental Asia. The other wild species endemic to Africa, O. longistaminata is perennial and rhizomatous. Two other perennial wild species, O. meridionalis and O. glumaepatula are endemic to tropical Australia, and South and Central America, respectively. Many useful genes from these AA genome species have been transferred by interspecific hybridization and selection. There are ten wild species in O. officinalis complex which have a wide geographical distribution. The species are either diploid or tetraploid with six different types of genomes: BB (O. punctata), CC (O. officinalis, O. rhizomatis and O. eichingeri), BBCC (O. punctata and O. minuta), CCDD (O. latifolia, O. alta and O. grandiglumis), EE (O. australiensis) and FF (O. brachyantha). These species are cross incompatible with the cultivated species, O. sativa and show non-homologous chromosome pairing making gene transfer into cultivated rice difficult. There are two diploid wild species, O. granulata and O. meyeriana under O. meyeriana complex and possess the GG genome. These two species are cross incompatible with O. sativa. Two tetraploid (O. longiglumis and O. ridleyi) wild species with HHJJ genome on the other hand are included in the O. ridleyi complex and these species are highly cross-incompatible with the cultivated species, O. sativa. Two more wild species such as O. coarctata which was previously called Porteresia coarctata and another species O. schlechteri are similarly included in the tertiary gene pools. These two species are tetraploid with the HHKK genome (Ge et al. 1999, Khush 1997). Useful genes of wild species of Oryza The wild species of Oryza contains numerous genes of economic importance and are being used as alternate sources of resistance or tolerance to biotic and abiotic stresses to enrich the cultivated rice gene pool (Table 2). The wild species of AA genome have useful genes such as resistance to grassy stunt and tungro viruses and bacterial blight, source of cytoplasmic male sterility for hybrid rice production, and resistance to flooding (Brar and Khush 1997). However, the wild species belonging to secondary gene pool of Oryza are distantly related to O. sativa. The wild species of this gene pool have a wealth of valuable genes needed for rice improvement. These species have genes conferring resistance to brown planthopper, white-backed planthopper, green leafhopper, leaf and neck blast, bacterial leaf blight (BB), yellow stem borer, sheath blight and genes for adaptation to aerobic soil, and high biomass production to increase yield potential Table 1. Wild species of Oryza with chromosome number, genome composition and their origin Wild species Chromosome Number Genome Origin O. rufipogon Griff. 24 AA Tropical Asia O. nivara Sharma et Shastry 24 AA Tropical Asia O. longistaminata Chev. et Roehr 24 AA Africa O. barthii Chev. et Roehr 24 AA Africa O. meridionalis Ng 24 AA Tropical Australia O. glumaepatula Steud. 24 AA South and Central America O. punctata Kotschy ex Steud. 24, 48 BB, BBCC Africa O. minuta J.S. Presl. ex C.B. Presl. 48 BBCC Philippines and Papua New Guinea O. officinalis Wall ex. Watt 24 CC Tropical Asia O. rhizomatis Vaughan 24 CC Sri Lanka O. eichingeri Peter 24 CC South Asia and East Africa O. latifolia Desv. 48 CCDD South America O. alta Swallen 48 CCDD South America O. grandiglumis Prod. 48 CCDD South America O. australiensis Domin. 24 EE Tropical Australia O. brachyantha Chev. et Roehr 24 FF Africa O. granulata Nees et Arn. ex. Watt 24 GG Southeast Asia O. meyeriana Baill 24 GG Southeast Asia O. longiglumis Jansen 48 HHJJ Indonesia O. ridleyi Hook 48 HHJJ South Asia O. schlechteri Pilger 24 HHKK Papua New Guinea O. coarctata Roxb. 48 HHKK India
3 520 Jena Table 2. Wild species of Oryza with useful traits Wild species Genome Useful traits a O. rufipogon AA Source of CMS, stem elongation ability, resistance to BB, and tungro tolerance O. nivara AA Resistance to grassy stunt virus and BB O. longistaminata AA Resistance to BB O. meridionalis AA Stem elongation ability O. punctata BB, BBCC Resistance to BPH and ZLH O. minuta BBCC Resistance to sheath blight, blast, BB, BPH O. officinalis CC Resistance to BPH, WBPH and GLH O. eichingeri CC Resistance to BPH, WBPH and GLH O. latifolia CCDD Resistance to BPH, Higher biomass for yield O. alta CCDD Resistance to stem borer and high biomass O. grandiglumis CCDD Higher biomass for yield O. australiensis EE Resistance to BPH and blast O. brachyantha FF Resistance to yellow stem borer O. granulata GG Adaptation to aerobic soil O. longiglumis HHJJ Resistance to blast and BB O. ridleyi HHJJ Resistance to blast, BB and stemborer O. coarctata HHKK Salt tolerance a CMS = cytoplasmic male sterility; BB = bacterial leaf blight; BPH = brown planthopper; WBPH = white backed planthopper; GLH = green leafhopper; ZLH = zigzag leafhopper of cultivated rice. The most distantly related wild species, O. granulata, O. meyeriana, O. longiglumis, O. ridleyi and O. coarctata have most valuable genes such as adaptation to aerobic soil and salinity tolerance, and resistance to bacterial blight, blast and stem borer (Brar and Khush 1997, Ge et al. 1999, Khush 1997). Transfer of useful genes from wild species into cultivated rice Fig. 1. Scheme for gene transfer from wild species into cultivated rice through production of monosomic alien addition lines (MAAL). *WW = genome of wild species in parenthesis It is easy to transfer valuable genes from AA genome wild species into cultivated rice by conventional breeding methods. Valuable traits of wild species are either controlled by major genes or controlled by multiple genes or polygenes. Nevertheless, quantitative trait loci (QTL) controlling yield and its component traits, grain quality traits, aluminum tolerance and tungro virus resistance (Brar, unpublished) have been successfully transferred from O. rufipogon (Acc ; Acc ) into indica rice cultivars (Nguyen et al. 2003, Septiningsih et al. 2003a, 2003b, Xiao et al. 1996). Genes for grassy stunt virus resistance have also been transferred from the wild species O. nivara (Acc ) into many indica cultivars (Brar and Khush 1997). Many distantly related wild species were identified as novel sources of biotic stresses resistance (Heinrichs et al. 1985). However, useful genes from distantly related wild species belonging to secondary and tertiary gene pools are difficult to transfer into cultivated rice because of cross compatibility barriers, non-homologous chromosome pairing and linkage drags. Advances in biotechnology have provided opportunities to generate inter-specific hybrids from the crosses between cultivated rice and distantly related wild species by means of embryo rescue (Jena and Khush 1984; Fig. 1). Specific chromosomes of wild species from secondary gene pool can be successfully transferred into cultivated rice through embryo rescue, production of allotriploids followed by development of monosomic alien addition lines having full chromosome complement of O. sativa and single chromosomes of wild species (Jena and Khush 1989, Jena et al. 1991). Useful genes of wild species, O. officinalis (Acc.
4 Genus Oryza and transfer of useful genes from wild species ) and O. australiensis (Acc ) have been eventually transferred into rice cultivars through production of disomic lines by rare recombinational events (Jena and Khush 1990, Jena et al. 1991) (Table 3). Molecular characterization of introgressed chromosome segments transferred from wild species into cultivated rice genome has also been demonstrated (Jena et al. 1992). Tagging of useful genes with DNA markers Valuable genes and QTL of wild species have been identified in AA, BB, CC, BBCC, CCDD, EE, FF, GG, HHJJ and HHKK genomes through evaluation under different stress conditions. Some of the genes/qtls associated with different agronomic traits for yield and yield components, aluminum tolerance and grain quality are derived from O. rufipogon ((Nguyen et al. 2003, Septiningsih et al. 2003a, 2003b, Xiao et al. 1996). The BB resistance gene, Xa21 from O. longistaminata has been tagged with molecular markers Ronald et al. 1992). The Xa21 gene has been cloned and reported to encode a serine threonine kinase like receptor protein (Song et al. 1995). Many valuable genes for major biotic stresses of rice were also identified in distantly related wild species belonging to secondary and tertiary gene pools and some genes for brown planthopper (BPH) resistance derived from O. officinalis (Acc ), O. minuta (101141), O. latifolia (Acc ) and O. australiensis (Acc ) were like wise tagged with molecular markers (Hirabayashi et al. 1998, Jena et al. 2002, 2006, Jena and Kim 2010, Rahman et al. 2009, Renganayaki et al. 2002, Yang et al. 2002, 2004). Moreover, blast resistance genes derived from O. minuta (Acc ) and O. australiensis (Acc ) were similarly tagged with molecular markers (Jeung et al. 2007, Liu et al. 2002). The blast resistance gene Pi40 from O. australiensis conferred broad-spectrum durable resistance to blast isolates of different countries (Fig. 2). BPH and blast resistance genes from O. minuta and O. australiensis were fine mapped using sequence information of O. sativa cv Nipponbare (Jena et al. 2006, Jeung et al. 2007, Qu et al. 2006). The gene, Bph14 derived from O. officinalis conferring resistance to BPH biotype of China and the blast resistance gene, Pi9 from O. minuta have been successfully cloned and found to encode CC-NBS-LRR and NBS-LRR proteins, respectively (Du et al. 2009, Zhou et al. 2006). The resistance genes from CC, BBCC and EE genomes are localized on different chromosomes (Table 3) and these genes are expected to further enhance resistance to BPH and blast after their transfer into elite rice cultivars. Conclusions The wild species of the genus Oryza are a wealth of genetic resources for rice improvement. These valuable germplasm are available in the gene bank of the International Rice Research Institute, Los Baños, Philippines. From several of these species, many useful genes have been identified and some important genes for increasing yield and resistance to biotic stresses have been mapped, and transferred into elite cultivars. Monosomic alien addition lines with single chromosomes of wild species of secondary genepool and introgression lines with genes of wild species have been developed at the International Rice Research Institute, Los Baños, Table 3. Useful genes of wild species of Oryza tagged with DNA markers and transferred into cultivated rice, O. sativa Wild species Useful traits a Identified genes/qtl Marker types b Chromosome location c Reference O. rufipogon Amylose content QTL SSR/RFLP 6S Septiningsih et al. (2003b) Yield QTL SSR 1L Xiao et al. (1996) QTL SSR 2S Xiao et al. (1996) Yield QTL SSR 1L, 2L, 9L Septiningsih et al. (2003a) Grain weight QTL SSR 8L Septiningsih et al. (2003a) Aluminum tolerance QTL RFLP 1S, 3S, 9L Nguyen et al. (2003) O. longistaminata BB Xa21 STS 11L Ronald et al. (1992) O. officinalis BPH Bph6 RAPD 11L Jena et al. (2002) bph11 RFLP 3L Hirabayashi et al. (1998) Bph13 RAPD 3S Renganyaki et al. (2002) Bph14 STS 3L Huang et al. (2001) Bph15 STS 4S Yang et al. (2004) O. minuta BPH Bph20 STS 4S Rahman et al. (2009) BPH Bph21 STS 12L Rahman et al. (2009) Blast Pi9 STS 6S Liu et al. (2002) O. latifolia BPH Bph12 SSR 4S Yang et al. (2002) O. australiensis BPH Bph10 RFLP 12L Ishii et al. (1994) BPH Bph18 STS 12L Jena et al. (2006) Leaf and neck blast Pi40 CAPS 6S Jeung et al. (2007) a BPH = brown planthopper; BB = bacterial leaf blight b SSR = simple sequence repeat; RAPD = randomly amplified polymorphic DNA; RFLP = restriction fragment length polymorphism; STS = sequence tagged site; CAPS = cleaved amplified polymorphic segment; QTL = quantitative trait loci c S = short arm, L = long arm
5 522 Jena Fig. 2. A. Blast resistance gene, Pi40 transferred from O. australiensis (D) into susceptible cultivated rice (RP) and produced blast resistant backcross progenies (BC), C = Susceptible check. B. Blast resistant BC lines tagged with DNA markers ( ) which is absent in susceptible BC progenies. Philippines. Seeds of these valuable materials are freely available to researchers worldwide to introduce useful genes into cultivated rice to improve rice production. Recent advances in biotechnology have provided opportunities to use genome sequence information in conjunction with precise strategies for genetic analysis to transfer agriculturally important genes from distantly related wild species. Further research is needed to identify genes controlling homoeologous chromosome pairing in the genus Oryza and to use these for precisely transferring valuable genes from distantly related wild species into cultivated rice, and incorporate the genes into elite cultivars by marker-assisted selection and backcross breeding. Acknowledgements I thank Dr. Suk-Man Kim and Ms. Seung-Hee Han of IRRI- Korea Office at National Institute of Crop Science, RDA for carefully formatting the manuscript. Literature Cited Brar, D.S. and G.S. Khush (1997) Alien introgression in rice. Plant Mol. Biol. 35: Chang, T.T. (1976) The origin, evolution, cultivation, dissemination and diversification of Asian and African rices. Euphytica 25: Du, B., W. Zhang, B. Liu, J. Hu, Z. Wei, Z. Shi, R. He, L. Zhu, R. Chen, B.Han et al. (2009) Identification and characterization of Bph14, a gene conferring resistance to brown planthopper in rice. Proc. Natl. Acad. Sci. USA 106: Ge, S., T. Sang, B.R. Lu and D.Y. Hong (1999) Phylogeny of rice genomes with emphasis on origins of allotetraploid species. Proc. Natl. Acad. Sci. USA 96: Heinrichs, E.A., F.G. Medrano and H.R. Rapusas (1985) Genetic evaluation of insect resistance in rice. International Rice Research Institute, Manila, Philippines, p Hirabayshi, H., E.R. Angeles, R. Kaji, T. Ogawa, D.S. Brar and G.S. Khush (1998) Identification of brown planthopper resistance gene derived from O. officinalis using molecular markers in rice. Breed. Sci. 48 (Suppl. 1): 82. Huang, Z., G. He, L. Shu, X. Li and Q. Zhang (2001) Identification and mapping of two brown planthopper resistance genes in rice. Theor. Appl. Genet. 102: Ishii, T., D.S. Brar, D.S. Multani and G.S. Khush (1994) Molecular tagging of genes for brown planthopper resistance and earliness introgressed from Oryza australiensis into cultivated rice, O. sativa. Genome 37: Jena, K.K. and G.S. Khush (1984) Embryo rescue of interspecific hybrids and its scope in rice improvement. Rice Genet. Newsl. 1: Jena, K.K. and G.S. Khush (1989) Monosomic alien addition lines of rice: production, morphology, cytology, and breeding behavior. Genome 37:
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