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

PRELIMINARY STUDIES ON TAXONOMY AND BIOSYSTEMATICS OF THE

AA GENOME ORYZA SPECIES (POACEAE)

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

Genetic Resources Center, International Rice Research Institute,P.O. Box 933, 1099 Manila, Philippines.

AbstractThe genus Oryza L (Oryzeae) 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, wild rice, taxonomy,. biosystematics, meiotic pairing. differentiation.

INTRODUCTION

The genus Oryza L. is classified in the tribe Oryzeae, whichcontains 12 genera (Table 1), and includes 22 species widelydistributed throughout the tropics. Great diversity in morphol-ogy and habitats has been observed for the various Oryza spe-cies. Following the taxonomic treatment of Vaughan (1989),species in this genus are classified in four complexes, with somespecies not yet placed in any (Table 2). Six basic genomes, AA,BB, CC, EE, FF, and GG, as well as three genomic combina-tions, BBCC, CCDD, and HHJJ, have been designated respec-tively in diploid and tetraploid Oryza species, although theorigin of DD, HH, and JJ is still unknown. This reflectsremarkable genetic variation in the genus. Because of consider-able morphological variability, the frequent occurrence ofintermediate types between some species, and the wide distri-

bution of Dryza species, the taxonomy has long been a prob-lem, particularly in the D. sativa complex, in terms of speciesdelimitation and nomenclature.

There are two cultivated rice species that originated independ-ently from different wild ancestral species in Asia and Africa. TheAsian cultivated rice (Dryza sativa L.) is an economically impor-tant world cereal crop and is the staple food for about half of theworld's population. This species probably originated across abroad area extending over the foothills of the Himalayas and itsadjacent .mountain regions in Asia, and is now grown worldwide.The African cultivated rice (D. glaberrima Steud.) was domesti-cated in West Africa and is still cultivated in some farmingsystems today. Rapid expansion of human populations anddecreases in agricultural land require much higher rice produc-tion than that which is now achieved. Wild relatives of rice,

51

Baa-Rang Lu et at.

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

Chikusiochloo

Hygroryzo

Leersia

Luziola

Maltebrunia

Oryza

Porteresia

ProsPhytochloa

Potamophila

RhynchoryzaZizania

Zizaniopsis

3

I

17

II

5

24

24

24

48. 60. 9624

Unknown

24.48

48

Unknown

24

24

30.3424

3

5

China, japan (t) a

Asia (t + T)

worldwide (t + T)

North and South America (t + T)

tropical and southern Africa (T)

pan-tropics (T)

South Asia (T)

southern Africa (t)

Australia (t + T)

South America (t)

Europe, Asia, N. America (t + T)

North and South America (t + T)

aT; tropical area. t ; temperate area.

species in this complex from different continents have beenreported to have considerable morphological similarities andintermediate types are also found between species occurring sym-patrically. This has led to considerable taxonomic and nomencla-ture changes in the wild species in this complex.

particularly those having the AA genome, are extremely valuablegenetic resources that serve to broaden the geneti~ background ofcultivated tice because the two cultivated tice species also havethe same genome. They are therefore the most accessible geneticresources in the tice genepool.

Eight Oryza species, including the two cultigens, have the AAgenome and are classified in the O. sativa complex (Table 2).These are O. rufipogon, O. nivara, and O. sativa, which are nativeto Asia, although the Asian cultivated tice is now grown world-wide; O. longistaminata, O. barthii, and O. glaberrima, which areendemic to Africa; and O. meridionalis and O. glumaepatula,which are only found in Australia and Latin America, respec-tively (Fig. I). Although geographically and genetically isolated,

NOMENCLATURE AND TAXONOMIC CHANGES IN AA

GENOME ORYZA SPECIES

The two cultivated rice species have been given a large number ofnames and undergone considerable nomenclature revision (seeSampath 1962; Harlan and de Wet 1971; Vaughan 1989 for areview), but Oryza sativa L. and O. glaberrima'Steud. havebecome well accepted and widely adopted names.

...". ~~~r.:£:F~ ;"""=~--'-~~~ p Q CJ:.o "'"J\) ~ Q~ ~ ~. ~

..'\") " _J

,c- -""

<:)

L.I~I

~( ~

"--~ """""""'.""

'0.~ ~

<::)J'~~

~

O. barthii

1111111111. O. glaberrima

I'////J. o. glumaepatula

r---" I o. longistaminata

Q

~~~J_Do t. Id ' d'\ -:1 ryza sa ,va war WI e

-~ o. nivara

(::::::::::::] O. rufipogon

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)

24

24

24

24

24

24

24

24

AA

AA

AA

AA

AA

AA

AA

AA

O. sativa complex

O. barthi; A. Chev.

O. glaberr;ma Steud.

O. glumaepatula Steud.

O. lang;staminata Chev. et Roehr.

O. meridiana/is Ng

O. n;vara Sharma et Shastry

O. rufipogon Griff.

O. sativa L.

Africa

West Africa

South & Central America

Africa

tropical Australia

tropical & subtropical Asia

tropical & subtropical Asia. & tropical Australia

worldwide

48

24

24,

48

48

48

24,

24,

24

CCDDEECC.

CCDDCCDDBBCCCC.

BB & BBCC

CC

O. officina/is complex

O. alto Swallen

O. australiensis Domin.

O. eichingeri Peter

O. grandig/umis (Doell) Prod.

O. latifolia Desv.

O. minuta J. S. Presl. et C. B Presl.

O. officina/is Wall. ex Watt

O. punctata Kotechy ex Steud.

O. rhizomatis Vaughan

South & Central America

tropical Australia

South Asia & East Africa

South & Central America

South & Central America

Philippines & Papua New Guinea

tropical & subtropical Asia, & tropical Australia

Africa

Sri Lanka

O. meyeriana complex

O. granulata Nees et Arn. ex Watt

O. meyeriana (Zoll. et Mor. ex Steud.) Baill.

24

24

GG

GG

South & Southeast Asia

Southeast Asia

O. ridleyi complex

O. longiglum;s Jansen

O. ridley; Hook. f.

48

48

HHJJ

HHJJ

Irian Jaya, Indonesia. & Papua New Guinea

South Asia

Species not assigned to any complex

O. brachyantha Chev. et Roehr.

O. neoca!edon;ca Morat

O. schlechter; Pilger

24

24

48

FF

Unknown

Unknown

Africa

New Caledonia

Papua New Guinea

a A tetraploid fonT1 with 48 chromosomes has also been found in the species

The close relatives of O. sativa have been named differently overtime. The species name O. perennis Moech was widely used forwild species in the O. sativa complex (Sampath 1962; Oka andMorishima 1967; Morishima 1969). The perennial O. rufipogonwas referred to as Asian O. perennis, in line with other wild spe-cies of the complex from different continents, which were calledMrican, American, and Oceanian O. perennis. This influence hasbeen so significant that many scientists still use O. perennis intheir recent publications (Pental and Barnes 1985; Oka 1988;Morishima et al. 1992; Ishii et al. 1996). The annual species wascalled O. fatua Koenig ex A. Chev. or O. sativa f. spontaneaRoshev., and was described as O. nivara by Sharma and Shastry(1965) to distinguish it from O. rUfipogon. But the name O.nivara has been interpreted differently. Some scientists haveaccepted O. nivara as an independent species (Chatterjee 1951;Chang 1976; Vaughan 1989, 1994) and considered it as theancestor of the Asian cultivated rice. Others, however, treated O.nivara as a synonym of O. sativa (Duistermaat 1987) or theannual form of O. rufipogon (Asian O. perennis) (Morishima1969; Oka 1988; Morishima et al. 1992). Nevertheless, O.rufipogon and O. nivara show a continuous array of intergrades

(Morishima et at. 1961) and intermediate perennial-annual pop-ulations have also been found in nature (Morishima 1986). Ourmorphological analysis also demonstrated a great degree of over-lapping between these two species Quliano et at. 1998).

There has also been considerable taxonomic and nomenclatureconfusion with the African wild rice species, although morpholog-ical differences between these species are significant. The annualO. barthii, which has been widely accepted as the ancestor of theMrican cultivated rice O. glaberrima (Chang 1976), was referredto as O. brevitigulata Chev. et Roehr. (Sampath 1962; aka andMorishima 1967; Second 1982; Ishii et aL 1996) or as African O.perennis by some authors (Pental and Barnes 1985). The perennialspecies O. longistarninata was called O. barthii (Sampath 1962;Clayton 1968) or O. perennis subsp. barthii (aka and Morishima1967; Clayton 1968). It was also common to name this perennialspecies as Mrican O. perennis (Morishima 1969; aka 1988;Morishima et aL 1992). In the Philippines we use O. barthii forthe annual species and O. longistarninata for the perennial species.Our unpublished data from morphological stUdies show a clearseparation of the two species sampled from diff~rent localities.

53

48

48

48

TAXONOMY AND BIOSYSTEMATICS OF AA GENOME OR~

Table 3. Seed set (%) from intraspecific and reciprocal interspecific crosses amongAA genome rice species (modified from Naredoet 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. barthiix O. n;vara hybrid with 12 ring bivalents in B.

between various AA genome rice species, particularly betweenthose from different continents, and between certain populationsof the same species. Figure 2 summarizes data for spikelet fertiliryof the F J interspecific hybrids which was generally less than 10%,except for the FJ hybrids among 0.. rufipogon, O. nivara, ando. sativa, and those between O. glaberrima and O. barthii, forwhich more than 50% spikelet fertiliry was observed in eachcombination (Naredo et at. 1997, 1998; Naredo et at.., unpub-lished data). In contrast, spikelet fertiliry of the parental speciesincluded varied between 60%-80%. This indicates diffecentdegrees of reproductive isolation between different AA genomespecies, and comparatively strong isolation between those fromdifferent continents, supporting previous studies on hybrid fer-tilities of O. perennis from different geographical origins(Morishima 1969; aka 1988).

GENOME RELATIONSHIP THROUGH MEIOTIC

CHROMOSOME PAIRING

It is generally agreed that species in the O. sativa complex have

essentially the same M genome (Richharia 1960; Chu et at. 1969;Morishima et at. 1992). Some authors have used different super-scriptS to differentiate the M genomes in some species, such as O.

longistaminata{A'A'),O. glumaepatula(AgpAgp), and O. meridiona-lis (AffiAffi) (Chang 1985; Vaughan 1989). However, this differen-

tiatioh cannot be supported from cytogenetic studies. To assess

genomic relationships, particularly between the wild M genomerice species, we analyzed all the available F 1 hybrids generated fromthe interspecific crosses. Dara from chromosome configurations inmeioses of different interspecific hybrids showed almost full pair-ing between the parental genomes (Figure 3A-B), except for somehybrids with O. meridionalis, in which a slightly lower value of

55

Baa-Rang Lu et at.

chromosome pairing was observed. Figure 4 summarizes the aver-age chiasma frequencies per pollen mother cell (PMC) at meioticmetaphase I in the available FJ hybrids (including the reciprocalcrosses) between different AA genome rice species, and in the wildparental species (Lu et al. 1997, 1998; Lu et al., unpublished data).The chiasma frequencies are generally higher than 20 per PMC inthe FJ hybrids (many FJ hybrids had more than 23 chiasmata perPMC). The chromosome pairing level is almost as high as in theirparental accessions, although it is slightly lower in a few combina-tions. This result suggests limited differentiation of the AAgenome in the different species of the O. sativa complex, regardlessof the geographical isolation of these species.

them. A similar situation is found between the Afri~ cultivatedrice O. glaberrima and its ancestor O. barthii.

The differentiation of the AA genome in rice species of the O.sativa complex is extremely limited judging from the chromo-some pairing ability of the parental genomes in interspecifichybrids. More detailed studies at the molecular level should beconducted to determine the degree of homology shared by theAA genome in different species in the O. sativa complex.

Based on the results from our morphological studies, interspe-cific hybridization, and meiotic analysis of the interspecifichybrids, in combination with reports from other molecular stud-ies (Doi etal. 1996; Ishii etal. 1996; Martin etal. 1997), a tenta-tive biosystematic relationship of the M genome species in theO. sativa complex is illustrated in Figure 5. The Asian O. sativa,O. nivara, and 9. rufipogon share close biosystematic relation-ships. The MricanO. glaberrima and o. barthii have the highestaffinity, and the Latin American O. glumaepatula joins this Mri-can group. O. longistaminata and the Australian o. meridional ishave relatively distant relationships with the other AA genomerice species.

CONCLUSIONS

The wild AA genome species in the O. sativa complex, such as O.rufipagan, O. barthii, O. g/umaepatuta, O. meridiana/is, and O.longistaminata, are distinct species with ptominent degrees ofreproductive isolation between them. Our interspecific hybridi-zation studies (Naredo eta/. 1997,1998; Naredo eta/., unpub-lished data) strongly support the conclusion that these wild ricespecies warrant specific taxonomic status.

The Asian cultivated tice O. sativa and its putative ancestral taxa,O. rufipogon and O. nivara, have very limited reproductive isola-tion, although the 'typical' samples of O. sativa, O. rufipogon,and O. nivara are morphologically distinct. But intermediatetypes from introgression of the three taxa are found in nature andcontinuous morphological variation can be observed between

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TAXONOMY AND BIOSYSTEMATICS OF AA GENOME aRYZA

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