2) Gene symbols and information on male sterility
T. K.INOSHITA
Professor Kmeritus. Hokkaido University. Sapporo. 060 Japan
Male sterility is an important character for hybrid seed production on a large scale. Information on genes responsible for various types of male sterility in rice is summarized as shown in Tables, 1, 2 and 3, which were partly transposed from the data of rice genes mentioned in Rice Genetics Newsletter Vol. 12 (Kinoshita 1995).
1. Cytoplasmic male sterility (CMS)
CMS was first reported by Katsuo and Mizushima (1958). They introduced nuclear genome of Fujisaka 5 into the cytoplasm of 'Chinese wild rice' (Oryza f. spontanea=0. rufipogon) by successive backcrosses. In hybrid rice breeding 'Chinsurah boro' cyto-
Table 1. Male sterile cytoplasms |
||||
Cytoplasm |
Name |
Maintainer |
Restorer |
Reference |
[cms-bo] |
Chinsurah boro II cytoplasm |
Taichung 65 |
Rfl-a Rfl-a |
Shinjyo 1969 1975, |
etc. |
Kadowaki et al. 1988, 1990 |
|||
[cms-ld] |
Lead rice cytoplasm |
Fujisaka 5 |
Rf2 Rf2 |
Watanabe 1971 |
[cms-TA] |
TA820 (Tadukan) cytoplasm |
Norm 8 |
Kitamura 1962a, 1962b |
|
[cms-CW] |
Chinese wild rice cytoplasm |
Fujisaka 5 |
Katsuo & Mizushima |
|
1958 |
||||
[cms-WA] |
Wild abortive cytoplasm |
IR24 etc. |
Rf3 Rf3 |
Lin & Yuan 1980. |
Rf4 Rf4 |
Kakowaki et al. 1988, |
|||
Virmarn et al. 1989 |
||||
[cms-HL] |
Red awned wild cytoplasm |
IR54753A etc. |
Lin & Yuan 1980 |
|
[cms-ak] |
Akebono cytoplasm |
Lien-Tong-Tao |
Rfak Rfak |
Yabuno 1977, |
([cms-jp]) |
Sakamoto et al. 1990 |
|||
[cms-ARC]* |
ARC13829-16 cytoplasm |
IR54755 |
IR42 etc. |
Virmani et al. 1989 |
[cms-GAM]* |
Gambiaca cytoplasm |
Chao Yang 1 |
IR58 etc. |
Lin & Yuan 1980, |
etc. |
Kakowaki et al. 1988, |
|||
Virmani et al. 1989 |
||||
[cms-sp] * |
MS577A cytoplasm |
IR42 etc. |
Kakowaki et al. 1988, |
|
Virmani et al. 1989 |
||||
[cms-UR89]* |
UR89F cytoplasm |
Taichung 65 |
Rfl-b Rfl-b |
Kakowaki et al. 1988, |
Shinjyo 1990 |
||||
[cms-UR102]* |
UR102F cytoplasm |
Taichung 65 |
Rfl-c Rfl-c |
Kakowaki et al. 1988, |
Shiniyo 1990 |
||||
[cms-UR104]* |
UR104F cytoplasm |
Taichung 65 |
Rfl-d Rfl-d |
Kakowaki et al. 1988, |
Shinjyo 1990 |
||||
[cms-UR106]* |
UR106F cytoplasm |
Taichung 65 |
Rfl-e Rfl-e |
Kakowaki et al. 1988, |
Shinjyo 1990 |
||||
[cms- UR27]* |
UR27F cytoplasm |
Taichung 65 |
Shinjyo 1990 |
|
[cms-54257]* |
54257 cytoplasm |
Ling et al. 1989 |
||
[cms-Khiaboro] * |
Khiaboro cytoplasm |
Akibare |
Nagamine et al. 1995 |
|
[cms-IR66707A]* |
Oryza perennis Ace 104823 |
IR64 |
Dalmacio et al. 1992, 1995 |
|
cytoplasm |
*Cytoplasm symbols are not registered in RGC.
Rice Genetics Newsletter Vol. 14
Table 2. Fertility restoring genes |
|||
Gene |
Explanation (Name/Cytoplasm/Origin) |
Locus |
Reference |
Rfl |
Pollen fertility restoration-1 /[cms-bo]/Chinsurah boro II/Rfl-a, Rfl-b, Rfl-c, Rfl-d (multiple alleles) |
Chr.l0:12 7.5cM to XNpb291, 3.7cM to OSRRf, 1.5% to fL601 Close to fL60lB |
Shinjyo 1975,1990, Sato el at. 1985, Vimiani & Shinjyo 1988, Fukuta rial. 1992, YueiaJ. 1995, Afaigielal. 1996, Yokomla et al. 1996 Ichikawa n al. 1997 |
Rf2 |
Pollen fertility restoration-2 /[cms-ld]/Fukuyama |
chr.2:132 |
Watanabe 1971, Shinjyo & Sato 1994 |
Rf3* (R2, Rf2)
Rf4* (Rl, Rfl, RfWAl) |
Fertility restoration-3/[cms-WA] /IR24 etc.
Fertility restoralion-4/ [cms-WA] /IR24 etc. |
chr.l: 1.9cMtoRG532
chr.7: near XNpb379 |
Lu & Zhang 1986, Bharaj et al. 1991,1995,Teng& Shen 1994, Chang a al. 1994, 1997, Zhang & Lu 1996 |
RfWA2 |
Weaker fertility restoration/ [cms-WA]/IR36 |
triplo-10 |
Bharaj et al. 1995 |
Rf2, 3,4, 5 |
[cms-Wa]DH from ZYQ/JX |
chr.2: RZ404C-RG241B chr3: RG694-RG413 chr 5: C22-RG449D chr.5: RG435-RG172A |
Zhu et al. 1996 |
Rf5(t)" (Rf(t)) |
Fertility restoration-5/[cms-WA] /Fen. revertant from 1132A (WA-tpe) |
chr.l: 5.3cm to OPB07-640 |
Shen et al. 1993a, 1996a 1996b |
Rfa. b, c |
Pollen fertility restoration/[cms-bo] /H-406/complernentary |
Maekawa 1982 |
|
Rja, b', c', d' |
Pollen fertility restoraton/[cms-bo] /H-103/complementary |
Maekawa 1982 |
|
Rfak (Rfjp) |
Pollen fertility restoration-ak/[cms-ak] /Akebono |
Yabuno 1977 |
|
lfr |
Induction of fertility restoration /[cms-bo]/partially sterile mutant from Taichung 65CMS |
Sano et al. 1992 |
* Gene symbols are not registered in RGC.
plasm or BT cytoplasm designated as {cms-bo] is extensively used for japonica hybrid rice development. The mode of inheritance of fertility restoring genes and molecular nature of mtDNA have been studied as a basis for breeding (Shinjyo 1975: Kadowaki et al. 1986, 1988, 1990-, Shikanai et al. 1989; Yamato et al. 1992 etc.). On the other hand, the cytoplasm of a male sterile line, 'wild abortive' designated as [cms-WA] is also successfully used for indica hybrid rice development (Lin and Yuan 1980). There are several cyto-plasmic sources as mentioned by Virmani and Shinjyo (1988). Virmani et al. (1989) demonstrated the cytoplasmic diversity among five cytoplasms, cms-bo, cms-WA, cms-GAM, cms-ARC and cms-sp depending on the spikelet fertilities of the progenies from test-crosses with a set of 28 cultivars. As to the utilization of wild Oryza species, Shinjyo (1990) classified at least four kinds of new cytoplasms derived from UR-lines belonging to 0. rufipogon depending on the interaction with different genotypes of Rf1 alleles. Ling et al. (1989) also found a CMS line, 54257 among somaclonal variants regenerated from anther culture and the mutant CMS was controlled by a cytoplasmic factor designated as
Report of Committee on Gene Symbolization
Table 3. Genetic male sterility |
||
Gene |
Name/Origin/Mutagen Locus |
Reference |
Ms1 (sf) |
male sterile-l/Fukukame/spontaneous chr.6:27 |
Hara 1946 |
ms2 |
male sterile-2/md-strain/spontaneous |
Group A (ms2-ms6), |
ms3 |
male sterile-3/Bufumochi/spontaneous |
Shibuya 1973 |
ms4 |
male sterile-4/Fujiminori/spontaneous |
|
ms5 |
male sterile-5/Otori/spontaneous |
|
ms6 |
male sterile-6/Bufumochi/spontaneous |
|
ms7 |
male sterile-7/K-l:Koshihikari/EI chr.3:80 |
Group B (ms -ms6); |
ms8 |
male sterile-8/K-2:Koshihikari/EI chr.7:20% to rfs |
Ko & Yamagata 1987, 1989 |
ms9 |
male sterile-9a/RTI-3aT65/spontaneous chr.6:100 |
Sato & Shinjyo 1991 |
ms9 |
male sterile-9b/E-l:Etsunan 77/EI |
|
ms10 |
male sterile-10/T-l:Toyonishiki/EI chr.9:5% to Dn1 |
|
msll |
male sterile-ll/T-2:Toyonishiki/EI |
|
msl2 |
male sterile-12/T-3:Toyoi1ishiki/EI |
|
msl3 |
male sterile-13/S-32:Sasanishiki/EI |
|
msl4 |
male sterile-14/S-40:Sasanishiki/7-ray chr.5:11% to nl1 |
|
ms15 |
male sterile-15/S-55:Sasanishiki/EI |
|
msl6 |
male sterile-16/S-59:Sasanishiki/EI |
|
msl7 |
male sterile-17/S-81:Sasanishiki/7-ray chr.2:35% to gh2 |
|
ms18* |
male sterile- 18/MS27: Nihonmasari/EI |
Group C (msl8~ms45); |
msl9* |
male sterile-19/MS28:Nihonmasari/ γ-ray |
Fujimaki et al. 1977, |
ms20* |
male sterile-20a/MS15:Nihonmasari/EI |
Hiraiwa & Tanaka 1980, |
ms20* |
male sterile-20b/MS29:Nihonmasari/ γ-ray |
Fujimaki & Hiraiwa |
ms2l*-ms23* |
male sterile 21-23/MS:Nihonmasari/γ-ray |
1986, Tamaru 1994 |
ms24* |
male sterile-24a/MS4:Nihonmasari/ γ-ray |
|
ms24* |
male sterile-24b/MS9:Nihonmasari/ γ-ray |
|
ms25*-ms30* |
male sterile 25-30/MS5-10:Nihonmasari/γ-ray |
|
ms31 * ~ms45* |
male sterile 31-45/MSII-26:Nihonmasari/EI |
|
ms46* |
male sterile-46/M201/streptomycin |
Group D (ms46~ms63); |
ms47*, ms48* |
male sterile-47, 48/MIOI/γ-ray |
Trees & Rutger 1978, |
ms49* |
male sterile-49/M201/EMS |
Mese et al. 1984, Hu & |
ms50* |
male sterile-50a/Calady/spontaneous |
Rutger 1992 |
ms50* |
male sterile-50b/Earirose/spontaneous |
|
ms51* |
male sterile-51/M201/EMS |
|
ms52* |
male sterile-52/MIOI/γ-ray |
|
ms52* |
male sterile-53a/MIOI/γ-ray |
|
ms53* |
male sterile-53b/M201/EMS |
|
ms54*~ms56* |
male sterile 54-56/M201/EMS |
|
ms57* |
male sterile-57/MIOI/γ-ray |
|
ms58* |
male sterile-58/M201/EMS |
|
ms59* |
male sterile-59a/MIOI/γ-ray |
|
ms59* |
male sterile-59b/M201/EMS |
|
ms60* |
male sterile-60a/MIOI/γ-ray |
|
rns60* |
male sterile-60b/M201/EMS |
|
ms60* |
male sterile-60c/Calrose 76 |
|
/anther culture |
||
ms61* |
male sterile-61/M201/EI |
|
ms62* |
male sterile-62/MIOI/7-ray |
|
ms63* |
male sterile-63/Caloro |
|
/spontaneous |
||
msIR36* |
male sterile (ms-IR36)/IR36/EI |
Group E (mslR36 ~ |
msIR36* |
male sterile (5495ms)/Line5495 |
msm77(t)); |
/spontaneous |
Singh & Ikehashi 1981, |
|
msIR36* |
male sterile (5683ms)/Line5683 |
Suh et at. 1989, 1991 |
/spontaneous |
||
mslR36* |
male sterile (Milyang 54ms) |
|
/Milyang 54/spontaneous |
Rice Genetics Newsletter Vol. 14
(Continued)
Gene |
Name/Origin/Mutagen |
Locus |
Reference |
msm55(t) *
msm 67(t)*
msm 77(t)* |
male sterile (Milyang 55ms) /Milyang- 55/spontaneous male sterile (Milyang 67ms) /Mi]yang 67/spontaneous male sterile (Milyang 77ms) /Milyang 77/spontaneous |
chr.l:31
chr.l:15% to mp1 |
|
ms2(t)*' |
male sterile/Co40XVaigai F1 /anther culture male sterile/Co40XVaigai F1 /anther culture |
Group F (ms1(t). Kaul 1986 |
|
oms |
open hull male sterile/spontaneous |
Takeda 1987 |
|
tmsl |
thermosensitive male sterility-I /5460:IR54/spontaneous |
chr.8: Sun et al. 1989. 6.7cMtoTGMSI,2 Yang et al. 1992 (OPB-19) Wang et al. 1995. 1996 |
|
tms2 |
thermosensitive male sterility-2 /Reimei/ γ-ray |
Maruyama et al. 1991 |
|
tms3(t)* |
thermosensitive male sterility-3 /IR32364/ γ-ray |
chr.6: 7.7cM to OPAC3-640 |
Borkakati & Virmani 1993, Subudhi et al. 1995, 1996, 1997 |
thermosensitive male sterility /26 Zhaizao S/ γ-ray |
Shen et al. 1993b |
||
pms1* (pgms, ms1P)
pms2* (ms2P) |
IP) photoperiod-sensitive male sterility-I /Nongken 58s/spontaneous
photoperiod-sensitive male sterility-2/Nongken 58s/spontaneous |
chr.7: 4.3cM to RG477
chr.8: near RG191 |
Group G (pms1, pms2); Zhu & Yu 1989, Wang et al. 1991, Shao Zhang et al. 1993 |
Pms(t)* |
photoperiod-sensitive male sterility /M201/EMS |
Oard & Hu 1995 |
Allelism tests were carried out only within each group.
*Gene symbols are not registered in RGC.
[cms-54257].
Following this, Dalmacio et al. (1992, 1995) produced a CMS line, IR66707A as a new source in the combination between the cytoplasm from (O. perennis Ace 104823 and the nuclear genome of IR64. Nagamine et al. (1995) also selected a new cytoplasmic source from boro varieties introduced from Bangladesh. The cytoplasm was different from [cms-boro] using test-crosses with several restorers and molecular structure of mtDNA, and was named as [cms-Khiaboro]. These new CMS systems are useful to enlarge the cytoplasmic diversity in hybrid rice breeding.Many kinds of somatic and cytoplasmic hybrids were produced by protoplast fusion using Ory'w species (Kyozuka et al. 1989). Transfer of [cms-bo] cytoplasm was achieved by donor-recipient method (Aviv et al. 1984) in japonica varieties. It is effectively used not only to shorten the time for breeding of CMS lines, but also to elucidate the genetic nature of CMS. Later it was demonstrated that a new chimeric gene, rpsi is also responsible for CMS in mtDNA besides atp6 (Kinoshita and Mori 1996).
Report of Committee on Gene Symbolization 17
It is generally accepted that Rf followed by a numeral is used to designate the fertility restoring genes. Hitherto Rfl and Rf2 located on chromosomes 10 and 2 respectively are used for the restorer genes for {cms-bo} and {cms-ld} (Table 2). It is indicated that two dominant restorer genes have additive effects for the restoration of fertility in [cm^-W^]. The two genes are located on chromosomes I and 7 respectively (Zhang and Lu 1996; Zhang et al. 1994, 1997). These genes were named as Rf3 and Rf4 by Zhang et al. ( 1997) replacing Rf2(R2) and Rf] (/?/) which were formerly used in several papers (Bharaj et al. 1991.1995: Teng and Shen 1994; Zhang et al. 1994). Teng and Shen ( 1994) showed that there is no evidence for interaction and pleiotropic effects between the fertility restoring genes for {cms-bo} and [cm^-W4]. In addition, a male fertile revertant was induced with Co"" gamma ray treatment from a CMS line, 11-32A having [c»M-W4] and the mutant acted as a fertility restoring gene (tentatively named as Rf5(t)) and is different from Rf3 and Rf4 present in IR24 and Minghui 63 (Shen et al. 1993a, 1996a, b). Fine mapping of these genes is progressing by using RFLP markers around OPB07-640 (chromosome 1) which are closely linked with the gene (Shen et al. 1996a). DNA markers closely linked to /?/-genes provide useful tools in marker-aided selection for the sterile maintainer and fertility restoring genes (Akagi et al. 1996).
Induction of partial male fertility in {cms-bo} Taichung 65 was controlled by the gene designated lfr (Sano and Eiguchi 1991: Sano et al. 1992). II. Genetic male sterility (GMS)
Usually single recessive genes condition male sterility and number over 70 in rice. As shown in Table 3, a numeral attached to ms were assigned without the coordinated allelism tests by the respective research group. In a few cases, duplicate recessive genes were reported, while no dominant genes have been reported. Type and stage of pollen abortion are various among the mutants (Hu and Rutger 1992; Tamaru 1994).
Environmentally conditioned male sterility (EGMS) can be efficiently used for hybrid seed production and 'two lines method' (EGMS and pollen parent) is gradually replacing 'three lines method' (CMS, maintainer and restorer). Sometimes EGMS are divided into thermosensitive MS (TGMS) and photoperiod-sensitive MS (PGMS or PSMS) depending upon their mode of response.
In the case of TGMS, male sterility is conditioned under high temperature but returns to normal under low temperature. Three single recessive genes, tmsl, tms2 and tms3(t) have been reported (Sun et al. 1989; Yang et al. 1992; Maruyama et al. 1991; Subudhi et al. 1995). Both tms2 and tms3(l) were induced with gamma irradiations, while tmsl occurred as a spontaneous mutant. The TGMS line containing tms3(t) shows complete male sterility at day and night temperatures of 32° and 24°C, but is partially fertile at 27° and 21 °C or 24°C and 18°C in the phytotron (Borkakati and Virmani 1993). In RFLP analysis, tmsl and tms3(t) were located on chromosome 8 and 6 respectively (Wang et al. 1995, 1996:Subudhicf<3/. 1995, 1996, 1997). ApromisingTGMSmutantnamedas26 Zhaizao S was induced by gamma-rays and the mutant showed low fertility especially at 30°C though there is no inheritance data (Shen et al. 1993b). In the case of PGMS, a spontaneous mutant was found in the field of Nongken 58.
Rice Genetics Newsletter Vol. 14
The mutant exhibited various types of pollen abortion under the restricted condition of long day (14hr/day) (Wang et al. 1991). Genetic analysis indicated that at least two recessive genes, pins I and pms2 are responsible for the trait and are located on chromosomes 7 and 3 respectively (Shao and Tang 1992; Zhang et al. 1993). Main effects of pmsl were about three times larger in the average than that of pms2 showing a considerable interaction between these two loci (Zhang et al. 1993). There is a possibility that one of the two sterility inducing genes from Nong-Ken 58S (NK58s) is allelic to one of the fertility restoring genes for [cw.s'-lVA] (Shao and Tang 1995). Similar PGMS mutants were found in progenies of the ethyl methanesulfonate-treated materials of the rice cultivar M-201 (Oard et al. 1991). Pollen fertility increased 3 to 44-fold when the mutant plants were ratooned and grown in a growth chamber with a 12hr daylength. PGMS was governed by one to three recessive genes. From the experiments with red or far-red light treatments, it was found that phytochrome is involved in regulation of pollen fertility (Oard and Hu 1995).
A spontaneous mutant named as open hull male sterile was controlled by a single recessive gene, oms. The pleiotropic effects of mutant gene resulted in lower seed fertility, smaller caryopsis, darker leaf color and good ratooning (Takeda 1987).
In order to promote gene identification and allelism tests, free exchange of the germplasm of male sterile mutants among different research groups is urgently needed.
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Rice Genetics Newsletter Vol. 14
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