Grass!.: Systematicsand Evolution. (2000). Eds S.W.L. Jacobs and J. Everett. (CSIRO: Melbourne)

PRELIMINARY STUDIES ON AND BIOSYSTEMATICS OF THE AA GENOME SPECIES ()

Bao-Rong Lu, Ma. Elizabeth B. Naredo, Amita B. Juliano, and Michael 7: Jackson

GeneticResources Center, International Research Institute, P.O. Box 933, 1099Manila, Philippines.

Abstract The Oryza L () include$ 22 wild species and two cultivated species-a. sativa L (Asian rice) and O. glaberrima Steud. (African rice). Asian rice is an economically important crop; it is the staple food for half of the world's population. Eight taxa, including the cultivated ones, are classified In the O. sativa complex on the basis of their morphological similarity and their common AA genome. Wild species in this complex are the most accessible and valuable genetic resources for rice breeding. Because of considerable variation in the mor- phology and habitat preferences of these rice species, taxonomy in this complex has long been a problem in terms of species delimitation and nomenclature. This paper summarizes recent biosystematic studies of the AA genome Oryza species through interspecific hybridization and meiotic analysis of F I hybrids and their P!ir'ental species. It concludes that most of the AA genome species in the O. sativa complex. such as O. rufipogon, O. bar- th;;, O. g/umaepatula, O. meridiana/is, and O. /ong;staminata, are distinct species with prominent reproductive bar- riers between them, although differentiation of the AA genome is limited between different species in the complex. A hypothetical biosystematic relationship of the AA genome Oryza species is proposed.

Key words: Poaceae, Oryza, , taxonomy,. biosystematics, meiotic pairing. differentiation.

INTRODUCTION bution of Dryza species,the taxonomy has long been a prob- lem, particularly in the D. sativa complex, in terms of species The genus Oryza L. is classified in the tribe Oryzeae,which delimitation and nomenclature. contains 12 genera (Table 1), and includes 22 specieswidely distributed throughout the tropics. Great diversity in morphol- There are two cultivated rice speciesthat originated independ- ogy and habitats has been observedfor the various Oryzaspe- ently from differentwild ancestralspecies in Asia and Africa. The cies. Following the taxonomic treatment of Vaughan (1989), Asian cultivated rice (Dryza sativa L.) is an economicallyimpor- speciesin this genusare classifiedin four complexes,with some tant world cerealcrop and is the staplefood for about half of the speciesnot yet placed in any (Table 2). Six basic genomes,AA, world's population. This speciesprobably originated acrossa BB, CC, EE, FF, and GG, as well as three genomic combina- broad areaextending over the foothills of the Himalayasand its tions, BBCC, CCDD, and HHJJ, have beendesignated respec- adjacent.mountain regions in Asia,and is now grownworldwide. tively in diploid and tetraploid Oryza species,although the The African cultivated rice (D. glaberrima Steud.)was domesti- origin of DD, HH, and JJ is still unknown. This reflects cated in West Africa and is still cultivated in some farming remarkablegenetic variation in the genus.Because of consider- systemstoday. Rapid expansion of human populations and able morphological variability, the frequent occurrence of decreasesin agricultural land require much higher rice produc- intermediate types betweensome species,and the wide distri- tion than that which is now achieved.Wild relatives of rice,

51 Baa-RangLu et at.

Table I. Genera, number of species, distribution, and chromosome number in the tribe Oryzeae (adapted from Vaughan 1989).

China, japan (t) a Chikusiochloo 3 24 Hygroryzo I Asia (t + T) 24 17 worldwide (t + T) 48.60. 96 II North and South America (t + T) 24 Maltebrunia 5 tropical and southern Africa (T) Unknown Oryza 24 pan-tropics (T) 24.48 South Asia (T) 48 ProsPhytochloa southern Africa (t) Unknown Australia (t + T) 24 Rhynchoryza South America (t) 24 Zizania 3 Europe, Asia, N. America (t + T) 30.34 5 North and South America (t + T) 24 aT; tropical area.t ; temperate area. particularly thosehaving the AA genome,are extremelyvaluable speciesin this complex from different continents have been geneticresources that serveto broadenthe geneti~background of reported to have considerablemorphological similarities and cultivated tice becausethe two cultivated tice speciesalso have intermediatetypes arealso found betweenspecies occurring sym- the samegenome. They aretherefore the most accessiblegenetic patrically. This hasled to considerabletaxonomic and nomencla- resourcesin the tice genepool. ture changesin the wild speciesin this complex.

Eight Oryza species,including the two cultigens,have the AA genome and are classified in the O. sativa complex (Table 2). NOMENCLATURE AND TAXONOMIC CHANGES IN AA Theseare O. rufipogon,O. nivara,and O. sativa,which arenative GENOME ORYZA SPECIES to Asia, although the Asian cultivated tice is now grown world- The two cultivated rice specieshave beengiven a large numberof wide; O. longistaminata,O. barthii, and O. glaberrima,which are namesand undergoneconsiderable nomenclature revision (see endemic to Africa; and O. meridionalisand O. glumaepatula, Sampath1962; Harlan and de Wet 1971; Vaughan 1989 for a which are only found in Australia and Latin America, respec- review), but L. and O. glaberrima'Steud. have tively (Fig. I). Although geographicallyand geneticallyisolated, becomewell acceptedand widely adoptednames.

...". ~~~r.:£:F~;"""=~--'-~~~pQ CJ:.o"'"J\) ~ Q ~ ~ ~. ~ <:) .. '\") " _J ,c- -""

~ L.I~ ( ~ """""""'."" I '0. ~ ~ -- " ~ ~ ~<::)J'~

'\ -:1 oryza sat,va . warId WI' d e O. barthii ~~~J_D -~ o. nivara 1111111111.O. glaberrima I'////J. o. glumaepatula (::::::::::::]O. rufipogon Q

r---" I o. longistaminata o. meridiana/is

Fig. I. Distribution of the AA genome Oryza species in different geographical regions.

52 TAXONOMY AND BIOSYSTEMATICS OF AA GENOME ORYZA

Table 2. Chromosome number, genome content, and distribution of species in the genus Oryza (modified from Vaughan 1989)

O. sativa complex O. barthi; A. Chev. 24 AA Africa O. glaberr;ma Steud. 24 AA West Africa O. glumaepatula Steud. 24 AA South & Central America O. lang;staminata Chev. et Roehr. 24 AA Africa O. meridiana/is Ng 24 AA tropical Australia O. n;vara Sharma et Shastry 24 AA tropical & subtropical Asia O. rufipogon Griff. 24 AA tropical & subtropical Asia. & tropical Australia O. sativa L. 24 AA worldwide O. officina/is complex O. alto Swallen 48 CCDD South & Central America O. australiensisDomin. 24 EECC. tropical Australia O. eichingeri Peter 24, 48 South Asia & East Africa O. grandig/umis (Doell) Prod. 48 CCDD South & Central America O. latifolia Desv. 48 CCDD South & Central America O. minuta J. S. Presl. et C. B Presl. 48 BBCCCC. Philippines & Papua New Guinea O. officina/isWall. ex Watt 24, 48 tropical & subtropical Asia, & tropical Australia O. punctata Kotechy ex Steud. 24, 48 BB & BBCC Africa O. rhizomatis Vaughan 24 CC Sri Lanka O. meyeriana complex O. granulata Nees et Arn. ex Watt 24 GG South & Southeast Asia O. meyeriana (Zoll. et Mor. ex Steud.) Baill. 24 GG Southeast Asia O. ridleyi complex

O. longiglum;sJansen 48 HHJJ Irian Jaya, Indonesia. & Papua New Guinea

O. ridley; Hook. f. 48 HHJJ South Asia Species not assigned to any complex O. brachyantha Chev. et Roehr. 24 FF Africa O. neoca!edon;caMorat 24 Unknown New Caledonia O. schlechter; Pilger 48 Unknown Papua New Guinea a A tetraploid fonT1 with 48 chromosomes has also been found in the species

The closerelatives of O. sativahave beennamed differently over (Morishima etat. 1961)and intermediateperennial-annual pop- time. The speciesname O. perennisMoech was widely used for ulations havealso beenfound in nature (Morishima 1986). Our wild speciesin the O. sativa complex (Sampath1962; Oka and morphologicalanalysis also demonstrated a greatdegree of over- Morishima 1967; Morishima 1969). The perennialO. rufipogon lapping betweenthese two speciesQuliano et at. 1998). was referred to asAsian O. perennis,in line with other wild spe- ciesof the complex from different continents,which were called There has also been considerabletaxonomic and nomenclature Mrican, American,and OceanianO. perennis.This influencehas confusionwith the African wild rice species,although morpholog- been so significant that many scientistsstill use O. perennisin ical differencesbetween these species are significant. The annual their recent publications (Pental and Barnes 1985; Oka 1988; O. barthii, which has beenwidely acceptedas the ancestorof the Morishima et al. 1992; Ishii et al. 1996). The annual specieswas Mrican cultivatedrice O. glaberrima(Chang 1976),was referred called O. fatua Koenig ex A. Chev. or O. sativa f. spontanea to as O. brevitigulataChev. et Roehr. (Sampath1962; aka and Roshev.,and was describedas O. nivara by Sharmaand Shastry Morishima 1967; Second1982; Ishii etaL 1996)or asAfrican O. (1965) to distinguish it from O. rUfipogon.But the name O. perennisby someauthors (Pental and Barnes1985). The perennial nivara has been interpreted differently. Some scientists have speciesO. longistarninatawas called O. barthii (Sampath1962; acceptedO. nivara as an independentspecies (Chatterjee 1951; Clayton 1968) or O. perennissubsp. barthii (aka and Morishima Chang 1976; Vaughan 1989, 1994) and considered it as the 1967; Clayton 1968). It was alsocommon to namethis perennial ancestorof the Asian cultivated rice. Others, however,treated O. speciesas Mrican O. perennis (Morishima 1969; aka 1988; nivara as a synonym of O. sativa (Duistermaat 1987) or the Morishima et aL 1992). In the Philippines we useO. barthii for annual form of O. rufipogon (Asian O. perennis)(Morishima the annualspecies and O. longistarninatafor the perennialspecies. 1969; Oka 1988; Morishima et al. 1992). Nevertheless,O. Our unpublished data from morphologicalstUdies show a clear rufipogonand O. nivara showa continuous array of intergrades separationof the two speciessampled from diff~rentlocalities.

53

TAXONOMY AND BIOSYSTEMATICS OF AA GENOME OR~

Table 3. Seed set (%) from intraspecific and reciprocal interspecific crosses amongAA genome rice species (modified from Naredo et 01.1997. 1998,and our unpublished data).

Fig. JA-B. Meiotic chromosome pairing at metaphase I of the O. barth;; x O. glumaepatula hybrid with 10 ring and 2 rod bivalents in A and the O. barthii x O. n;vara hybrid with 12 ring bivalents in B. betweenvarious AA genome rice species,particularly between GENOME RELATIONSHIP THROUGH MEIOTIC those from different continents,and betweencertain populations CHROMOSOME PAIRING of the samespecies. Figure 2 summarizesdata for spikeletfertiliry It is generally agreed that species in the O. sativa complex have of the F Jinterspecific hybrids which was generallyless than 10%, essentiallythe same M genome (Richharia 1960; Chu et at. 1969; except for the FJ hybrids among 0.. rufipogon, O. nivara, and Morishima et at. 1992). Some authors have used different super- o. sativa,and those between O. glaberrimaand O. barthii, for scriptS to differentiate the M genomes in some species,such as O. which more than 50% spikelet fertiliry was observedin each longistaminata{A'A'),O. glumaepatula(AgpAgp),and O. meridiona- combination (Naredo et at. 1997, 1998; Naredo et at..,unpub- lis (AffiAffi) (Chang 1985; Vaughan 1989). However, this differen- lished data). In contrast, spikeletfertiliry of the parental species tiatioh cannot be supported from cytogenetic studies. To assess included varied between 60%-80%. This indicates diffecent genomic relationships, particularly between the wild M genome degreesof reproductive isolation betweendifferent AA genome rice species,we analyzed all the available F 1 hybrids generated from species,and comparativelystrong isolation betweenthose from the interspecific crosses.Dara from chromosome configurations in different continents, supporting previous studies on hybrid fer- meioses of different interspecific hybrids showed almost full pair- tilities of O. perennis from different geographical origins ing between the parental genomes (Figure 3A-B), except for some (Morishima 1969; aka 1988). hybrids with O. meridionalis, in which a slightly lower value of

55 Baa-RangLu et at.

O. meridiana/is

Fig. 4. Meiotic pairing of the F I hybrids between various AA genome Oryza species. Numbers in the middle box indicate chiasma frequency per pollen mother cell (PMC), and numbers in the small boxes indicate chiasma frequency per PMC of the wild parental species.

chromosomepairing wasobserved. Figure 4 summarizesthe aver- them. A similar situation is found betweenthe Afri~ cultivated agechiasma frequencies per pollen mother cell (PMC) at meiotic rice O. glaberrimaand its ancestorO. barthii. metaphaseI in the availableFJ hybrids (including the reciprocal crosses)between different AA genomerice species,and in the wild The differentiation of the AA genome in rice speciesof the O. parentalspecies (Lu etal. 1997,1998; Lu et al.,unpublished data). sativa complex is extremelylimited judging from the chromo- The chiasmafrequencies are generally higher than 20 per PMC in some pairing ability of the parental genomes in interspecific the FJhybrids (many FJhybrids had more than 23 chiasmataper hybrids. More detailed studies at the molecular level should be PMC). The chromosomepairing levelis almostas high as in their conducted to determine the degreeof homology shared by the parentalaccessions, although it is slightly lower in a few combina- AA genomein different speciesin the O. sativacomplex. tions. This result suggestslimited differentiation of the AA genomein the differentspecies of the O. sativacomplex, regardless Basedon the results from our morphological studies, interspe- of the geographicalisolation of thesespecies. cific hybridization, and meiotic analysis of the interspecific hybrids, in combination with reports from other molecular stud- ies (Doi etal. 1996; Ishii etal. 1996; Martin etal. 1997),a tenta- CONCLUSIONS tive biosystematicrelationship of the M genomespecies in the The wild AA genomespecies in the O. sativacomplex, such as O. O. sativacomplex is illustrated in Figure 5. The Asian O. sativa, rufipagan,O. barthii, O. g/umaepatuta,O. meridiana/is,and O. O. nivara, and 9. rufipogonshare close biosystematicrelation- longistaminata,are distinct specieswith ptominent degreesof ships.The MricanO. glaberrimaand o. barthii havethe highest reproductive isolation betweenthem. Our interspecific hybridi- affinity, and the Latin American O. glumaepatulajoins this Mri- zation studies (Naredo eta/. 1997,1998; Naredo eta/., unpub- can group. O. longistaminataand the Australian o. meridionalis lished data) strongly support the conclusion that thesewild rice have relatively distant relationshipswith the other AA genome specieswarrant specifictaxonomic status. rice species.

The Asian cultivated tice O. sativaand its putative ancestraltaxa, O. rufipogonand O. nivara,have verylimited reproductiveisola- REFERENCES tion, although the 'typical' samplesof O. sativa,O. rufipogon, Brar, S. D. and Khush, G. S. 1997. Alien introgression in rice: and O. nivara are morphologically distinct. But intermediate Molecular Biology 35, 35-47. types from introgressionof the three taxaare found in nature and Chat:Jg.T.T. (1976). The origin, evolution, cultivation, dissemination. continuous morphological variation can be observed between and diversification of AsiananqAfrican nces. Euphytica 25,435-411.

56 TAXONOMY AND BIOSYSTEMATICS OF AA GENOME aRYZA

O. sativa O. nivara

O. barlhii

O. meridiana/is

Fig. 5. A tentative biosystematic relationship of the AA genome Oryza species.

Chang, T. T. (1985). Crop history and genetic conservation: Rice -a Majumder. N. D.. Ram. T.. and Sharma, A. C. (1997). Cytological and case study. Iowa Statejoumal of Research 59,425-455. morphological variation in hybrid swarms and introgressed popula- Chatterjee, D. (1951). Note on the origin and distribution of wild and tion of interspecific hybrids (Oryza ruppogon Griff. x Oryza sativa L) cultivated rice. Indian Journal of Agricultural Sciences 18, I 85- I92. and its impact on evolution of intermediate types. Euphytica 94, Chu, Y. E., Morishima, H.. and aka, H. I. (1969). Reproductive baniero 295-302. distributed in cultivated rice species and their wild relatives. japa- Morishima, H. (1969). Phenetic similarity and phylogenetic relationships nesejoumal of Genetics 44, 225-229. among strains of Oryza perenn;s, estimated by methods of numerical Clayton, w. D. (1968). Studies in Gramineae. XVII. West African wild taxonomy. Evolution 23.429-443. rice. Kew Bulletin 21, 487-488. Morishima, H. (1986). Wild progenrtors of cultivated rice and their Doi, K Yoshimura, A.. Nakano, M.. and Iwata, N. (1996). Classification population dynamics. In 'Rice Genetics.' (Ed. IRRI) pp. 3-14. (IRRI: of A genome species in the genus Oryza using nuclear DNA mark- Los Banos, Philippines.) ero. International Rice Research Notes 21...8-10. Morishima. H.. Oka. H. I.. and Chang W. T. (1961). Direction of differ- Duistermaat, H. .( 1987). A revision of Oryza (Gramineae) in Malaysia entiation in populations of wild rice. Oryza perennis and O. sativa t: and Australia. Blumea 32, 157-193. spontanea. Evolution 15, 326-339. Harlan, J. R, and de Wet, J. M. J. (1971), Toward a rational classification of cultivated . Taxon 20, 509-5 17. Morishima, H.. Sano. Y.. and Oka. H. I. (1992). Evolutionary studies in Ishii, T.. Nakano, T.. Maeda, H.. and Kamijjma, ~. (1996), Phylogenetic cultivated rice and its wild relatives. Oxford Surveys in Evolutionary relationships in A-genome species of rice as revealed by RAPD Biology8,135-184. analysis. Genes and Genetic Systems 71, 195-20 I. Naredo M. E. B.. juliano. A. B.. Lu, B. R, and jackson. M...T. (1997). Juliano, A. B.. Naredo, M. E. B.. and Jackson, M. T. (1998). Taxonomic Hybridization of AA genome rice species from Asia and Australia. I. Status of Oryza g/umaepatula Steud. I. Comparative morphological Crosses and development of hybrids. Genetic Resources and Crop studies of New World diploids and Asian M gehome species. Evolution 44, 17-23. Genetic Resourcesand Crop Evolution 45, 197-203. Naredo, M. E. B.. juliano. A B.. Lu. B. R, and jackson. M. T. (1998). Tax- Lu, B. R, Naredo, M. E. B.. Juliano, A. B.. and Jackson, M.T. (1997). onomic status of Oryza glumaepatula Steud. II. Hybridization Hybridization of M genome rice species from Asia and Australia. II. between New World diploids and AA genome species from Asia Meiotic analysis of Oryza meridionalis and its hybrids. Genetic and Australia. Genetic Resources and Crop Evolution 45.. 205-214. Resourcesand Crop Evolution 44, 25-31. Ng. N. Q.. Chang. T. T.. Williams. j. T.. and Hawkes. j. G. (1981). Mor- Lu, B. R, Naredo, M. E. B.. Juliano, AB.. and Jackson, M. T. (1998). T axo- phological studies of Asian rice and its related wild species and the nomic Status of Oryza glumaepatula Steud. III. Assessment of genomic recognrtion of a new Australian taxon. Botanic journal of Unnean affinity among M genome species from the New World, Asia, and Society ..6, 303-313. Australia. Genetic Resourcesand Crop Evolution 45, 205-214. Martin, C. A.. Juliano, A. B.. Newbury, H. J.. Lu, B. R, Jackson, M.T.. and aka. H. I. (1988). 'Origin of cultivated rice.' O~ Scientific Societies Ford-Uoyd, B. V. (1997). The use of RAPD markero to faCilitate the Press: Tokyo. japan.) identification of Oryza species wrthin a germ plasm collection. aka. H. I.. and Morishima, H. (1967). Variations in the breeding systems Genetic Resourcesand Crop Evolution 44, 175-183. of a wild rice. Oryza perennis. Evolution 21. 249-258.

57

~ Baa-Rang Lu et al.

Penta/, D., and Barnes. S. R. (1985). Interrelationship of cultivated rice Shalma, S, D. and Shasjry. S. V. S. (1965). Taxonomic studies in Oryza sativa and O. giaberrima with Wild O. perennis complex. Theo- genus Oryza L III. O. rufipogon Griff. sensu stricto and O. nivara retical and Applied Genetics 70, j 85-191. Shalma and Shasjry nom. novo Indian journal of Plant Breeding 25, Richharia. R. H. (1960). Origins of cultivated . Indian Journal of 157-167. i Genetics and Plant Breeding 20. l- 14, T ateoka, T, (1962.). : ~ono~ic studies of Oryza, II, Several species Sampath, S. (1962). The genus Oryza: Its taxonomy and species interre- complexes. Botarnc MagazIne Tokyo 75, 455-461. lationships. Oryza I, I -29. Vaugb~.. D. A (1989). The genus Oryza L: cun-ent status of taxonomy. Second. G. (1982). Origin of the genetic diversitY of cultivated rice IRRI Research paper Series 138, IRRI, Los '"Banos:Philippines. (Oryza spp.): study of the polymorphism scored at 40 isozyme loci. Vaughan,D. A., ( 1994), 'The wild relatives of rice: A genetic resources japanesejoumal of Genetics 57,25-57. handbook' (IRRI: Los Banos: Philippines.)

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