Breeding Science 60: 518–523 (2010) doi:10.1270/jsbbs.60.518

Review

The species of the and transfer of useful genes from wild species into cultivated , O. sativa

Kshirod K. Jena*1)

1) Breeding, Genetics and Biotechnology Division, International Rice Research Institute, C/o National Institute of Crop Science, Rural Development Administration, Suwon 441-857, 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 iden- tified in O. longistaminata and introduced into many rice . Advances in biotechnology have facili- tated 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, respective- ly, 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 trans- ferred into cultivated rice in the future using the latest tools of molecular genetics and biotechnology.

Key Words: Rice, wild species, genus Oryza, genes.

Introduction ance to biotic and abiotic stresses and eventually increase yield potential of modern cultivars. The objective of this pa- Rice ( L.) is the most economically important per is to discuss the status of the species in the genus Oryza food crop in the world and provides two third of calorie in- and the transfer of high value genes present in wild species take of more than three billion people in Asia and one-third into rice cultivars using the tools of modern biotechnology of calorie intake of nearly 1.5 billion people in Africa and and genetics. Latin America (Khush 2005). Rice is cultivated worldwide under various agro-climatic conditions. However, rice pro- Wild species of Oryza duction in recent years has been affected seriously by major biotic and abiotic stresses due to adverse climatic change The genus Oryza of the Gramineae family has 24 species. and breakdown of resistance genes in elite cultivars Two of the 24 species, O. sativa L. and O. glaberrima (Normile 2008). The genetic variability for resistance or tol- Steud., are cultivated cereals and 22 are wild species distrib- erance to biotic stresses is limited in cultivated rice gene uted in different geographic locations worldwide (Khush pool but abundantly present in the gene pools of wild species 1997, Vaughan 1989). O. sativa is cultivated as a major ce- belonging to the genus Oryza. There is an urgent need to real crop in most parts of Asia and consumed as a staple broaden the gene pool of cultivated rice by transferring valu- food. The African cultivated rice, O. glaberrima is grown in able genes from wild species for enhancing resistance/toler- small areas in West Africa. O. sativa has two subspecies: japonica and indica. The subspecies japonica has a narrow Communicated by H. Yasui genetic resources compared to indica subspecies which has Received September 30, 2010. Accepted October 31, 2010. a wide genetic diversity. Oryza wild species were classified *Corresponding author (e-mail: [email protected]) into three main groups or complexes based on the ease of Genus Oryza and transfer of useful genes from wild species 519 gene transfer from wild species into cultivated rice. These gene transfer into cultivated rice difficult. are: (1) O. sativa complex, (2) O. officinalis complex. (3) There are two diploid wild species, O. granulata and O. meyeriana and O. ridleyi complex (Morishima and Oka O. meyeriana under O. meyeriana complex and possess the 1960). These groups/complexes were later named as prima- GG genome. These two species are cross incompatible with ry, secondary and tertiary gene pools of Oryza, respectively O. sativa. Two tetraploid (O. longiglumis and O. ridleyi) (Khush 1997). wild species with HHJJ genome on the other hand are in- The O. sativa complex has two cultivated species and six cluded in the O. ridleyi complex and these species are highly wild species with the AA genome (Table 1). These species cross-incompatible with the cultivated species, O. sativa. are diploid, cross compatible and show homologous chro- Two more wild species such as O. coarctata which was mosome pairing. The perennial wild species, O. rufipogon is previously called coarctata and another species the progenitor of the cultivated Asian rice O. sativa while O. schlechteri are similarly included in the tertiary gene O. barthii is the progenitor of the cultivated African rice pools. These two species are tetraploid with the HHKK ge- O. glaberrima (Chang 1976, Oka 1988, Vaughan et al. nome (Ge et al. 1999, Khush 1997). 2008, Zhu and Ge 2005). Of the two Asian wild species, the perennial O. rufipogon is distributed throughout tropical Useful genes of wild species of Oryza Asia and Oceania, whereas the annual O. nivara is restricted to tropical continental Asia. The other wild species endemic The wild species of Oryza contains numerous genes of eco- to Africa, O. longistaminata is perennial and rhizomatous. nomic importance and are being used as alternate sources of Two other perennial wild species, O. meridionalis and resistance or tolerance to biotic and abiotic stresses to enrich O. glumaepatula are endemic to tropical Australia, and the cultivated rice gene pool (Table 2). The wild species of South and Central America, respectively. Many useful genes AA genome have useful genes such as resistance to grassy from these AA genome species have been transferred by stunt and tungro viruses and bacterial blight, source of cyto- interspecific hybridization and selection. plasmic male sterility for hybrid rice production, and resis- There are ten wild species in O. officinalis complex tance to flooding (Brar and Khush 1997). However, the wild which have a wide geographical distribution. The species are species belonging to secondary gene pool of Oryza are dis- either diploid or tetraploid with six different types of ge- tantly related to O. sativa. The wild species of this gene pool nomes: BB (O. punctata), CC (O. officinalis, O. rhizomatis have a wealth of valuable genes needed for rice improve- and O. eichingeri), BBCC (O. punctata and O. minuta), ment. These species have genes conferring resistance to CCDD (O. latifolia, O. alta and O. grandiglumis), EE brown planthopper, white-backed planthopper, green leaf- (O. australiensis) and FF (O. brachyantha). These species hopper, leaf and neck blast, bacterial leaf blight (BB), yellow are cross incompatible with the cultivated species, O. sativa stem borer, sheath blight and genes for adaptation to aerobic and show non-homologous chromosome pairing making 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 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 520 Jena

Table 2. Wild species of Oryza with useful traits Wild species Genome Useful traitsa 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 leaf- hopper; 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 cultivat- ed rice

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 toler- ance and tungro virus resistance (Brar, unpublished) have been successfully transferred from O. rufipogon (Acc. 105491; Acc. 106424) 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 trans- ferred from the wild species O. nivara (Acc. 101508) into many indica cultivars (Brar and Khush 1997). Many distantly related wild species were identified as Fig. 1. Scheme for gene transfer from wild species into cultivated rice novel sources of biotic stresses resistance (Heinrichs et al. through production of monosomic alien addition lines (MAAL). 1985). However, useful genes from distantly related wild *WW = genome of wild species in parenthesis species belonging to secondary and tertiary gene pools are difficult to transfer into cultivated rice because of cross com- patibility barriers, non-homologous chromosome pairing ary gene pool can be successfully transferred into cultivated and linkage drags. Advances in biotechnology have provid- rice through embryo rescue, production of allotriploids fol- ed opportunities to generate inter-specific hybrids from the lowed by development of monosomic alien addition lines crosses between cultivated rice and distantly related wild having full chromosome complement of O. sativa and single species by means of embryo rescue (Jena and Khush 1984; chromosomes of wild species (Jena and Khush 1989, Jena et Fig. 1). Specific chromosomes of wild species from second- al. 1991). Useful genes of wild species, O. officinalis (Acc. Genus Oryza and transfer of useful genes from wild species 521

100896) and O. australiensis (Acc. 100882) have been even- O. minuta (Acc. 101141) and O. australiensis (Acc. 100882) tually transferred into rice cultivars through production of were similarly tagged with molecular markers (Jeung et al. disomic lines by rare recombinational events (Jena and 2007, Liu et al. 2002). The blast resistance gene Pi40 from Khush 1990, Jena et al. 1991) (Table 3). Molecular charac- O. australiensis conferred broad-spectrum durable resis- terization of introgressed chromosome segments transferred tance to blast isolates of different countries (Fig. 2). BPH and from wild species into cultivated rice genome has also been blast resistance genes from O. minuta and O. australiensis demonstrated (Jena et al. 1992). were fine mapped using sequence information of O. sativa cv Nipponbare (Jena et al. 2006, Jeung et al. 2007, Qu et al. Tagging of useful genes with DNA markers 2006). The gene, Bph14 derived from O. officinalis confer- ring resistance to BPH biotype of China and the blast resis- Valuable genes and QTL of wild species have been identi- tance gene, Pi9 from O. minuta have been successfully fied in AA, BB, CC, BBCC, CCDD, EE, FF, GG, HHJJ and cloned and found to encode CC-NBS-LRR and NBS-LRR HHKK genomes through evaluation under different stress proteins, respectively (Du et al. 2009, Zhou et al. 2006). The conditions. Some of the genes/QTLs associated with differ- resistance genes from CC, BBCC and EE genomes are local- ent agronomic traits for yield and yield components, alumi- ized on different chromosomes (Table 3) and these genes are num tolerance and grain quality are derived from O. rufipogon expected to further enhance resistance to BPH and blast after ((Nguyen et al. 2003, Septiningsih et al. 2003a, 2003b, their transfer into elite rice cultivars. Xiao et al. 1996). The BB resistance gene, Xa21 from O. longistaminata has been tagged with molecular markers Conclusions Ronald et al. 1992). The Xa21 gene has been cloned and re- ported to encode a serine threonine kinase like receptor pro- The wild species of the genus Oryza are a wealth of genetic tein (Song et al. 1995). Many valuable genes for major biotic resources for rice improvement. These valuable germplasm stresses of rice were also identified in distantly related wild are available in the gene bank of the International Rice species belonging to secondary and tertiary gene pools and Research Institute, Los Baños, Philippines. From several of some genes for brown planthopper (BPH) resistance derived these species, many useful genes have been identified and from O. officinalis (Acc. 100896), O. minuta (101141), some important genes for increasing yield and resistance to O. latifolia (Acc. 100914) and O. australiensis (Acc. 100882) biotic stresses have been mapped, and transferred into elite were like wise tagged with molecular markers (Hirabayashi cultivars. Monosomic alien addition lines with single chro- et al. 1998, Jena et al. 2002, 2006, Jena and Kim 2010, mosomes of wild species of secondary genepool and intro- Rahman et al. 2009, Renganayaki et al. 2002, Yang et al. gression lines with genes of wild species have been devel- 2002, 2004). Moreover, blast resistance genes derived from oped 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 traitsa Identified genes/QTL Marker typesb Chromosome locationc 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 522 Jena

Fig. 2. A. Blast resistance gene, Pi40 transferred from O. australiensis (D) into susceptible cultivated rice (RP) and produced blast resistant back- cross progenies (BC), C = Susceptible check. B. Blast resistant BC lines tagged with DNA markers (→) which is absent in susceptible BC progenies.

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