1. Plant Cell Physiol. 46(1): 48–62 (2005)
doi:10.1093/pcp/pci506, available online at www.pcp.oupjournals.org
JSPP © 2005
Mini Review
Rice Mutants and Genes Related to Organ Development, Morphogenesis and
Physiological Traits
Nori Kurata 1, 4, 5, Kazumaru Miyoshi 3, Ken-Ichi Nonomura 1, 4, Yukiko Yamazaki 2, 4 and Yukihiro Ito 1, 4
1
Genetic Strains Research Center, National Institute of Genetics, Mishima, 411-8540 Japan
2
Center for Genetic Resource Information, National Institute of Genetics, Mishima, 411-8540 Japan
3
Graduate School of Agricultural and Life Sciences, University of Tokyo, Tokyo, 11-8657 Japan
4
School of Life Science, Graduate University for Advanced Studies (SOKENDAI), Mishima, 411-8540 Japan
;
Recent advances in genomic studies and the sequenced have been used primarily for genetic studies such as identifica-
genome information have made it possible to utilize pheno- tion of genes that regulate rice morphogenesis or physiological
typic mutants for characterizing relevant genes at the traits, and linkage analysis for gene mapping. In 1998, the rice
molecular level and reveal their functions. Various mutants genetics committee reported 571 mutant genes (Nagato and
and strains expressing phenotypic and physiological varia- Yoshimura 1998). To date, nearly 2,000 trait genes including
tions provide an indispensable source for functional analy- both single Mendelian loci/genes and quantitative trait loci
sis of genes. In this review, we cover almost all of the rice (QTLs) have been recorded. Even at the present status where
mutants found to date and the variant strains that are im- tens of thousands of cDNAs and expressed sequence tags
portant in developmental, physiological and agronomical (ESTs) have been isolated as genetic codes, most trait genes
studies. Mutants and genes showing defects in vegetative specific for rice mutants and variant/strains have not been iso-
organs, i.e. leaf, culm and root, inflorescence reproductive lated. In this review, 1,698 rice genes reported to date based on
organ and seeds with an embryo and endosperm are de- the mutant or variant phenotypes are listed. Most of these
scribed with regards to their phenotypic and molecular genes are mapped on one of the 12 rice chromosomes. Classifi-
characteristics. A variety of alleles detected by quantitative cation of the 1,698 genes into phenotypic categories is summa-
trait locus analysis, such as heading date, disease/insect re- rized in Table 1. Mutant phenotypes and gene classification fit
sistance and stress tolerance, are also shown. into particular categories for rice development, as described by
Itoh et al. in this issue. In this review, genes and mutants of key
Keywords: Developmental mutant — Phenotype — Physio- or interesting functions in relation to rice organ development
logical mutant — Rice organ — Trait gene. and biological/physiological reactions have been selected from
the gene list of Table 1. The genes described in this study
Abbreviations: ARGM, Asian rice gall midge; bHLH, basic should be important sources for functional genetic studies to
helix–loop–helix; BPH, brown planthopper; CMS, cytoplasmic male
connect gene structure with gene functions. In fact, enormous
sterility; EST, expressed sequence tag; GLH, green leafhopper; GO,
gene ontology; GRH, green rice leafhopper; LRR, leucine-rich repeat; progress in rice genome mapping and sequencing has pro-
NBS, nucleotide-binding site; NIL, near isogenic line; PMS, photope- moted map-based cloning of these trait genes during the last
riod-sensitive genic male sterility; PO, plant ontology; QTL, quantita- decade.
tive trait locus; RIL, recombinant inbred line; SAM, shoot apical In addition to the positional cloning approach, systematic
meristem; TGMS, thermosensitive genic male sterility; TO, trait ontol-
ogy; WBPH, whitebacked planthopper; WCVs, wide-compatibility
functional genomics approaches to screen mutants using inser-
varieties. tion mutagenesis have been developed (Hirochika et al. 1996,
An et al. 2003, Ito et al. 2004b, Kim et al. 2004, Sallaud et al.
2004). Several mutants and genes from Tos17-transposed lines
and T-DNA insertion lines are included in this review. Tagged
Introduction flanking sequence databases generated for most mutant popula-
tions are used in reverse genetics approaches. The MNU-
The discovery and isolation of useful natural mutants and induced mutant population established by Satoh and Omura
their variants in rice breeding has taken many years and consid- (1981) is thought to possess a very frequent point mutation
erable effort. In the latter quarter of the 20th century, many ratio and so could also be a powerful source for identifying
studies were conducted to generate artificial mutants by using mutant lines by applying reverse genetic approaches such as
γ-ray irradiation or chemical mutagens, e.g. methylnitrosourea the TILLING system (Till et al. 2003). The mutant strains of
(MNU) and ethyl methanesulfonate (EMS). These mutants both types are collected on a large scale, and their classifica-
5
Corresponding author: E-mail, nkurata@lab.nig.ac.jp; Fax, +81-55-981-6808.
48

2. Rice mutants and trait genes 49
Table 1 Classification and number of mutant/variant genes
Class of genes No. of genes Class of genes No. of genes
Vegetative organ 276 Seed 236
SAM 30 Morphological traits 55
Leaf 53 • Embryo 28
Culm 141 • Endosperm 3
Root 52 • Grain shape 24
Reproductive organ 464 Physiological traits 181
Heading date 115 • Dormancy 30
Inflorescence 111 • Longevity 3
Spikelet 46 • Storage substances 80
Pollination, fertilization, fertility 238 • Shattering 28
• Fertility restoration 16 • Taste 40
• Segregation distortion 15 Tolerance, resistance 288
• Hybrid sterility, 58 Disease resistance 134
• Hybrid weakness 22 Insect resistance 72
• Male sterility 107 Stress tolerance 82
• Female sterility 3 Characters as QTLs 297
• Meiosis 12 Grain quality 47
• Other sterilities 5 Yield and productivity 134
Heterochrony 4 Plant growth activity 72
Coloration 133 Germination 11
Anthocyanin 40 Root activity 11
Chlorophyll 77 Seed sterility 22
Others 16 Total 1698
tion according to phenotype is underway; see Appendix 1 (1) Genes specifically expressed in the SAM
for Tos17 tagging mutants and Appendix 1 (2) for the MNU- In the vegetative development of rice, the SAM maintains
induced mutants. itself and simultaneously generates lateral organs such as
In this review, rice trait genes important for the under- leaves and tillers. Several different families of homeobox genes
standing of rice are documented. Detailed data including chro- have been cloned and analysed in plants. One of them is a
mosomal locations, trait ontology (TO)/plant ontology (PO) KNOX class 1 homeobox gene family which is a pivotal regula-
and gene ontology (GO) IDs and reference for all 1,698 trait tor of SAM formation and maintenance in plants. In rice there
genes are available in the Oryzabase [see Appendix 1 (3)]. are six KNOX class 1 genes, OSH1, OSH3, OSH6, OSH15,
Such information could be useful for comparative studies of OSH43 and OSH71, in its genome (Sentoku et al. 1999). Five
organ development, and for structural variation of genes among of these genes are expressed in the SAM. Their constitutive
species and genera. expression results in inhibition of regeneration from the callus
by maintaining the cells in an undifferentiated state or results in
Mutants and Genes in Vegetative Organ Development abnormal morphology of regenerated shoots mainly on the
leaves (Sentoku et al. 2000, Ito et al. 2001). Among these
In vegetative development, leaves are generated succes- genes, only the mutant of OSH15 has been analyzed (Sato et al.
sively from flanks of the shoot apical meristem (SAM) with an 1999). The osh15 mutant shows reduced plant height and is
alternate phyllotaxy. Culm, crown roots and lateral roots are allelic to the dwarf mutant, d6. Thus, OSH15 is involved in the
also formed in this developmental phase. A large number of control of normal plant height in addition to SAM formation
mutants defective in development of various organs have been and maintenance. Another gene family that plays a role in
reported in rice, and in several cases causal genes have been SAM is the NAC gene family that shares an evolutionarily con-
cloned. Mutants and genes associated with vegetative organ served NAC domain. Expression analysis suggests diverse
development are categorized into four groups: (i) genes specifi- functions for each member of this family (Kikuchi et al. 2000).
cally expressed in the SAM; (ii) leaf mutants; (ii) culm
mutants; and (iv) root mutants. Leaf mutants
In leaf development, various types of mutants have been
identified and can be categorized into two large groups; a leaf

3. 50 Rice mutants and trait genes
morphology group and a leaf color group. The leaf morphol- 2001). Mutants lacking each of these gene activities show spe-
ogy group contains seven types of mutants: rolled leaves, drip- cific patterns in reducing internode length. These gibberellin
ping-wet leaves, narrow leaves, drooping leaves, blade–sheath synthesis genes form small gene families in the rice genome,
boundary defect leaves, glabrous leaves and hairy leaves; and and the members of each gene family show different expres-
QTLs controlling leaf angle, leaf length and leaf width. sion patterns.
Mutants of three loci have been categorized in the droop- In addition to gibberellin synthesis genes, several gib-
ing leaf subgroup. Among them, DROOPING LEAF (DL) has berellin signaling genes have been cloned and a signaling
been thoroughly analyzed (Nagasawa et al. 2003, Yamaguchi et mechanism has been studied. These genes are, D1, GA-INSEN-
al. 2004). DL is expressed in the central region of the develop- SITIVE DWARF2 (GID2) and SLENDER RICE1 (SLR1). Loss-
ing young leaf and its loss-of-function mutation results in a of-function mutants of D1 and GID2 show a dwarf phenotype,
defective midrib formation and drooping leaves. DL encodes a whereas a loss-of function mutant of SLR1 resembles the phe-
putative transcription factor of the YABBY family. DL is a notype of an exogenous application of gibberellins on plants
pleiotropic gene and also specifies carpel identity during flower (Ashikari et al. 1999, Fujisawa et al. 1999, Ikeda et al. 2001).
development (see Organ Identity section). Detailed analyses of D1 and GID2 encode positive regulators for gibberellin signal-
other mutants remain to be carried out. ing, whilst SLR1 encodes a negative regulator. GID2 is
Seven lamina joint angle QTLs, two leaf length QTLs, involved in the degradation of SLR1 (Sasaki et al. 2003). GID2
five leaf width QTLs and one leaf length mutant have been encodes an F-box protein in a component of ubiquitin ligase E3
identified. In a coleoptile photomorphogenesis1 (cpm1) mutant, named SCFGID2.
coleoptiles elongate more than wild-type coleoptiles under red D1 encodes an α-subunit of the trimeric G protein, which
light or in the darkness (Biswas et al. 2003). is localized in the plasma membrane as a complex with the β-
There are three mutants affecting leaf blade–sheath and the γ-subunits (Ashikari et al. 1999, Fujisawa et al. 1999,
boundary, auricleless (aul), liguleless (lg) and collarless (col). Kato et al. 2004). The d1 mutant is insensitive to low concen-
The auricleless (aul) mutant lacks auricles and the ligule is trations of gibberellins, but still shows a response to high con-
rudimentary, whereas liguleless (lg) lacks ligule, auricle and centrations of gibberellins (Ueguchi-Tanaka et al. 2000).
leaf collar (Maekawa 1988). The collarless mutant lacks collar Two genes have been cloned which encode proteins cata-
(Sanchez and Khush 1998). Another two classes of mutants, lyzing brassinosteroid synthesis. In d2 mutants, the second
two glabrous leaf and two hairy leaf mutants were also found in internode from the top has been shown to be shortened,
the leaf mutants. The other leaf mutant group has abnormali- whereas elongation of the other internodes is rarely affected
ties in leaf color including lesion mimic spotted phenotype. (Hong et al. 2003). The d2 mutant also shows an erect leaf phe-
notype. D2 encodes brassinosteroid C-3 oxidase (also called
Culm mutants CYP90D2, a member of cytochrome P450), which catalyzes a
Culm mutants can be categorized into eight groups; C-3 oxidation step of brassinosteroid synthesis. In the rice
dwarfism/elongation, floating, tiller formation, tiller angle, brit- genome, one homolog of D2 has been found, which is
tleness, thickness, twisted and others. The dwarfism/elonga- expressed mainly in the root.
tion group includes mutants impaired in gibberellin synthesis, BRASSINOSTEROID-DEPENDENT1/BRASSINOSTEROID-
gibberellin signaling, brassinosteroid synthesis and brassinos- DEFICIENT DWARF1 (BRD1) encodes a brassinosteroid C-6
teroid signaling. oxidase (OsDWARF), which catalyzes the C-6 oxidation step
of brassinosteroid synthesis (Hong et al. 2002, Mori et al.
DWARFISM/ELONGATION 2002). The brd1 mutant shows almost no internode elongation,
Since plant height in rice is an agronomically important a reduced ratio of leaf sheath to leaf blade, and a short root.
trait for breeding high-yielding cultivars, numerous dwarf and The brd1 mutant also shows constitutive photomorphogenesis
semi-dwarf mutants have been collected. Some of them have in the dark.
been shown to be gibberellin- or brassinosteroid-related In the brassinosteroid signaling pathway in rice, only one
mutants. gene has been cloned. D61 encodes a receptor-like protein
D35, SD1 and D18 genes encode gibberellin biosynthesis kinase with extensive sequence identity to the Arabidopsis
enzymes which catalyze specific steps. D35 encodes ent-kau- brassinosteroid receptor BRI1 (Yamamuro et al. 2000). This
rene oxidase which catalyzes the early three steps of gibberel- suggests that D61 is the receptor for brassinosteroid in rice.
lin synthesis (ent-kaurene→ent-kaurenol→ent-kaurenal→ent- The d61 mutant shows less sensitivity to exogenously applied
kaurenoic acid) (Itoh et al. 2004). SD1, the ‘green revolution’ brassinosteroid. More endogenous brassinosteroids accumulate
gene, encodes GA20 oxidase which catalyzes three steps in the d61 mutant than the wild-type plant. The relative ratio of
(GA53→GA44→GA19→GA20) (Sasaki et al. 2002). D18 leaf blade to sheath length is also smaller compared with the
encodes GA3 β-hydroxylase that catalyzes the step from GA20 wild type. The results of these phenotypic analyses are consist-
to GA1, which is an active form of gibberellin (Itoh et al. ent with the idea that D61 is the brassinosteroid receptor.

4. Rice mutants and trait genes 51
FLOATING
Another group of mutants are related to floating characters
or deep water tolerance. These genes exist in the floating rice
strains, and are involved in reactions mainly for extreme elon-
gation of the internodes. These genes are analyzed as QTLs and
are described in the Stress tolerance section.
TILLER FORMATION
Seven mutants with a reduced number of tillers have been
identified. Among them, MONOCULM1 (MOC1) has been
shown to be involved in tiller bud initiation (Li et al. 2003a).
The moc1 mutant shows no tillering owing to a defect in tiller
bud formation during the vegetative phase, and produces no
rachis branches in the inflorescence. MOC1 encodes a tran- Fig. 1 Histological characterization of seminal roots of the crl1, crl2,
scription factor of the plant-specific GRAS family. Expression rrl1 and rrl2 mutants in rice. (A–C) Transverse sections of the nodes
of MOC1 starts in the presumptive region of the axillary bud of wild type (A), crl1 (B) and crl2 (C). In crl1, no crown root primor-
formation, and continues until maturation of the tiller buds. dia is initiated (B), and in crl2 development of crown roots is impaired
(C). (D–G) Longitudinal sections of seminal roots of the wild type (D
and F), rrl1 (E) and rrl2 (G). In rrl1, the cortical cell length is signifi-
BRITTLE cantly reduced (E), and in rrl2 the root apical meristem is small and
Six mutants with brittle culm have been identified. Brittle the root cell length is reduced (G). Photographs are kind gifts from H.
mutants are easily broken by bending. Among them, BRITTLE Kitano and Y. Inukai (Nagoya University).
CULM1 (BC1) has been studied most extensively (Li et al.
2003b). The bc1 mutant has less cellulose and more lignin than
the wild-type plant. Monosaccharide composition is also Mutants and Genes in Reproductive Organ Development
affected in the bc1 mutant. Thus, BC1 controls the mechanical
strength of plants through the cell wall composition. BC1 Heading date
encodes a COBRA-like protein and is expressed mainly in Rice is a model plant for analysis of flowering of short-
developing sclerenchyma cells and in vascular bundles. day plants, and also for comparative studies of flowering with
long-day plants such as Arabidopsis. A large number of QTLs
TILLER ANGLE AND THICKNESS have been identified from a cross between wild and cultivated
Seven genes identified as mutations or QTLs are catego- rice strains and between japonica and indica strains. In one
rized in the tiller angle group. However, detailed morphological combination, detailed analyses of every QTL have been car-
and molecular analyses of these genes have not yet been ried out using near isogenic lines (NILs) (Yano et al. 2001).
reported. Big uppermost culm (Buc) is categorized in the thick- Heading date1 (Hd1) encodes a zinc-finger transcription factor
ness group. closely related to the Arabidopsis flowering gene product
CONSTANS (CO), and Hd3a encodes a protein closely related
Root mutants to Arabidopsis FLOWERING LOCUS T (FT) (Yano et al.
In contrast to the understanding of shoot development, 2000, Kojima et al. 2002). Under short-day conditions, Hd1
analysis of root development lags behind, even though a activates expression of Hd3a and induces flowering. Under
number of mutants have been isolated which affect various long-day conditions, Hd1 suppresses the expression of Heading
aspects of root development. These include mutants for root date 3a (Hd3a) and inhibits transition to a reproductive phase.
number, root branching, root length, root thickness, root This pattern of regulation contrasts with that of Arabidopsis in
weight, root pulling force and rhizome formation. The crl1 which under long-day conditions CO (Hd1) induces flowering
(crown rootless1) mutant forms radicle and lateral roots through expression of FT (Hd3a) (Hayama et al. 2003).
normally, but is impaired in the initiation of crown root primor- Early heading date1 (Ehd1) encodes a B-type response
dia (Fig. 1A, B) (Inukai et al. 2001a). Thus, CRL1 specifically regulator of a two-component signaling system and confers
regulates initiation of crown root primordia. CROWN early flowering, especially under short-day conditions (Doi et
ROOTLESS2 (CRL2) regulates various aspects of rice develop- al. 2004). The effect of Ehd1 is observed in the hd1 mutant
ment including initiation and subsequent growth of crown root background, but in the ehd1 mutant background Hd1 functions
primordia (Fig. 1C, D, Inukai et al. 2001a). The reduced root normally as a floral inducer under short-day conditions and
length1 (rrl1) and reduced root length2 (rrl2) mutations cause also as a floral repressor under long-day conditions. Under
short roots (Inukai et al. 2001b). In the rrl1 mutant, only the short-day conditions, expression of Hd3a is higher in the Ehd1
cortical cell length is significantly reduced, whilst in the rrl2 background than in the ehd1 background. This indicates that
mutant, the root apical meristem is also small (Fig. 1E, G). Ehd1 and Hd1 function independently and that the two path-

5. 52 Rice mutants and trait genes
Fig. 3 Flower mutants of rice. (A) Wild-type flower. (B) fon1-2
flower. (C) spw1 flower. (D) dl flower. Photographs are kind gifts from
H. Hirano and Y. Nagato (University of Tokyo).
In the panicle phytomer1 (pap1) mutant, the numbers of
Fig. 2 Inflorescence images of lax and fzp mutants of rice. (A) Wild-
type inflorescence. (B) Inflorescence images of lax mutants. (C) Inflo-
primary branches are increased. In addition, internode length
rescence of fzp mutant. (D) Terminal spikelet of wild-type branch. (E) and number of rachis are reduced, and rudimentary and empty
Apical region of fzp branches. Photographs are kind gifts from J. Kyo- glumes are elongated (Takahashi et al. 1998).
zuka (University of Tokyo).
LATERAL MERISTEM IDENTITY
This group of mutants fails to specify the identity of the
ways are integrated into a flowering pathway with Hd3a. lateral branch meristem as the spikelet or flower meristem.
Heading date 6 (Hd6) delays flowering under long-day condi- This group includes FRIZZY PANICLE (FZP). In fzp mutants,
tions but not short-day conditions. Although Hd6 has been primary rachis branch meristems develop normally, but spike-
shown to encode an α-(catalytic) subunit of protein kinase CK2 lets are replaced by branch meristems (Fig. 2C–E, Komatsu et
(Takahashi et al. 2001), interaction with other flowering genes al. 2003b). As a result, branch meristems are continuously gen-
and alleles remains to be studied. erated in the inflorescence of the fzp mutant. FZP encodes a
In addition to these excellent examples of QTL analysis, transcriptional activator with the ERF domain, and is expressed
other QTL analyses have revealed many trait genes from a in a region where the rudimentary glume primordia develop.
variety of strains. Several QTLs are introduced in this mini-
review; however, QTLs showing growth activities in vegeta- FLOWER ORGANIZATION
tive and reproductive organs are not incorporated. They are This group of mutants has defects in flower organization.
agronomically important traits, such as grain quality, yield and A mutant flower of this group has an abnormal number or
productivity, plant growth activity, germination, root activity arrangement of whorls. Although some mutants are known,
and seed sterility, and are listed in the rice genes and mutants of such as extra glume-1 (eg1) and extra glume-2 (eg2), their
Oryzabase [see Appendix 1 (3)]. detailed analyses remain to be carried out.
Inflorescence ORGAN NUMBER
Inflorescence and flower mutants can be categorized into This group of mutants has defects in controlling the
seven groups according to the developmental step at which number of organs developed in each whorl. In these mutants,
mutant phenotypes are observed, such as lateral branching, lat- only the number of floral organs is affected, whereas flower
eral meristem identity, flower organization, organ number, organization and organ identity are normal. floral organ
organ identity, organ development and others. number1 (fon1) and fon2 are mutants in this group. In these
mutants, the number of floral organs such as carpel, stamen and
LATERAL BRANCHING lodicule is increased, whereas the number of glumes such as
This group of mutants has defects in the formation and lemma and palea is not affected (Fig. 3B, Nagasawa et al.
elongation of lateral branches. The mutants of this group form 1996). fon1 and fon2 control organ numbers by regulating mer-
fewer numbers of rachis branches and spikelets or compact istem size or number of meristem cells. The FON1 gene
panicle(s). In this group, LAX PANICLE (LAX) has been stud- encodes a receptor-like protein kinase with a high homology to
ied most extensively. In lax mutants, spikelets are formed only Arabidopsis CLAVATA1 (CLV1) (Suzaki et al. 2004).
on the apices of rachis branches, and no lateral spikelets are
formed (Fig. 2A, B, Komatsu et al. 2001, Komatsu et al. ORGAN IDENTITY
2003a). LAX is necessary for initiation of lateral meristem for- This group of mutants has defects in specification of the
mation. LAX encodes a putative transcription factor with a identity of organs. In rice, several genes involved in organ
plant-specific basic helix–loop–helix (bHLH) domain and is identification have been identified. Among them, SUPER-
expressed at the boundary between the lateral meristem and WOMAN (SPW) specifies lodicules and stamens. In spw mutant
apical meristem. flowers, lodicules and stamens are homeotically transformed

6. Rice mutants and trait genes 53
into palea-like organs and carpels, respectively (Fig. 3C, CMS lines require combination with the fertility restorer lines
Nagasawa et al. 2003). The SPW gene has been shown to be to maintain a hybrid system, whereas alteration of environmen-
identical to OsMADS16, a rice MADS-box gene. SPW is tal conditions, such as day length and temperature shift, can
expressed in the lodicules and stamens. These analyses indi- restore fertility in PMS and TGMS (Liu et al. 2001, Wang et al.
cate that SPW is a class B gene and the ABC model is applica- 2003).
ble, at least in part, to rice. In Oryza sativa, only a single CMS system has been thor-
DROOPING LEAF (DL), which plays a role in leaf devel- oughly studied using cybrids with the cytoplasm of cv. Chinsu-
opment (see Leaf mutants section), also specifies carpel iden- rah Boro II (Boro, indica rice) and the nuclear genome of cv.
tity (Nagasawa et al. 2003, Yamaguchi et al. 2004). In the dl Taichung 65 (T65, japonica rice), called ms-bo type or BT type
mutant, the carpel has been homeotically transformed into the CMS (Shinjo 1975, Shinjo 1984). A mitochondrial atp6 and a
stamens (Fig. 3D). In flower development, expression of DL unique sequence orf79 downstream of atp6 are known to relate
starts in the presumptive region where carpel primordium is to CMS (Kadowaki et al. 1990, Iwabuchi et al. 1993, Akagi et
initiated, and continues in the carpel primordium. Thus, DL al. 1994). The Rf-1 gene has been reported to encode a protein
specifies the identity of only a single whorl. In this respect, the with a mitochondrial transit peptide and pentatricopeptide
ABC model is modified in rice. repeat (PPR) (Kazama and Toriyama 2003, Komori et al.
Another gene involved in specification of organ identity is 2004). On the other hand, neither PMS nor TGMS genes have
LEAFY HULL STERILE1 (LHS1) (Jeon et al. 2000). In the lhs1 been isolated as yet. Ku et al. (2003) reported that pro-
mutant flower, lemma and palea show a leaf-like appearance. grammed cell death of premature tapetum is associated with
Lodicules also become leafy. The number of stamens is TGMS in rice.
reduced. In some flowers, a new abnormal flower is formed in Several other genic mutations exhibiting pollen sterility or
the whorl of the stamens, indicating that specification of floral abnormal anther development have also been reported (mostly
meristem identity is incomplete. LHS1 is identical to designated ms). Recently, the aid1 mutant showing a defect in
OsMADS1, a close member of Arabidopsis AP1. LHS pro- anther dehiscence was identified using an Ac/Ds transposon
motes determination of the floral meristem identity and specifi- tagging system (Zhu et al. 2004). The AID1 gene encodes a
cation of the lemma, palea and lodicules. Other genes have novel protein with a single MYB DNA-binding domain.
been cloned which have resulted in homeotic transformation of
floral organs when they are ectopically expressed or their anti- Hybrid sterility and reproductive barrier
sense is expressed (Kang et al. 1998, Kyozuka and Shimamoto Although there are several genic models for hybrid steril-
2002). ity, only two models are applied to interspecific rice hybrids.
One is the ‘single locus sporo-gametophytic interaction’ model,
ORGAN DEVELOPMENT AND OTHERS and the other is the ‘duplicate loci gametic lethal’ model (Oka
Mutants of the organ development group have defects in 1974, Sano et al. 1979).
development of each organ and show abnormal development of Gamete eliminator genes play key functions in preferen-
awn, lemma and palea after specification of their organ iden- tial inheritance of one of the alleles in the heterozygous F1
tity. Twenty genes or QTLs involved in awn development are plants, and support the former model. The Mendelian segrega-
known, whilst six genes are known for each of lemma and tion of marker genes linked with the gamete eliminator is dis-
palea. In malformed lemma1 (mls1) and mls2, morphological torted in progenitors. Many gamete eliminator loci, designated
abnormalities in the lemma and low pollen fertility are as S in most cases, have been identified in various cross-combi-
observed, and in mls3, lemma and palea are malformed (Taka- nations among the Oryza species. In the cross-combination
mure and Kinoshita 1992). Mutants involved in gametophyte between O. sativa and O. glaberrima, at least seven S loci have
development are described below. been identified using NILs of a T65 background (Sano 1983,
Sano 1990, Doi et al. 1998, Doi et al. 1999, Taguchi et al.
Sexual Reproduction Processes 1999). The loci S1, S3, S19 and S20 act to abort pollen carry-
ing the T65 haplotype, and the loci S2 and S21 act to abort
In this section, we describe the genes and mutations asso- pollen carrying the glaberrima haplotype (Fig. 4A–D). Hetero-
ciated with gamete or seed sterility. zygous plants in the S18 locus probably exhibit a defect in male
sporocyte development. In addition to the gamete eliminator
Male sterility and fertility restoration alleles, Ikehashi and Araki (1986) have reported the existence
Male sterility, for which a large number of mutants are of a neutral S allele (S5n) in javanicas, called wide-compatibil-
found, is classified into four major groups: male sterility ity varieties (WCVs). The WCVs enable generation of fertile
caused by cytoplasmic male sterility (CMS), photoperiod-sen- F1 plants when crossed with japonica and indica, whilst
sitive genic male sterility (PMS), thermosensitive genic male japonica–indica hybrids exhibit high sterility and are primarily
sterility (TGMS) and other genic male sterilities. CMS, PMS attributed to the S5 locus. Thus the WCVs have actually con-
and TGMS can be used for practical hybrid production. The tributed to overcoming hybrid sterility (Wan et al. 1993). In

7. 54 Rice mutants and trait genes
Fig. 4 Hybrid sterility found in the genus Oryza. (A–D) Pollen from
cross-combination between O. sativa L. and O. glaberrima Steud.
stained with I2-KI solution. (A) O. sativa L. cv. T65. (B) O. glaber-
rima Steud. (IRGC1104038). (C) An F1 hybrid. (D) A near isogenic
line heterozygous for the S21 locus. (E and F) Paraffin sections of the
matured embryo sac in the F1 plants between cv. Asominori (japonica)
and cv. IR24 (indica). (E) Asominori (wild type). (F) A collapsed
embryo sac in the double recessive plants for the hsa1and hsa2 loci.
(G) Hybrid weakness segregated in the F2 population between O.
sativa L. and O. glumaepatula Steud. From left to right, O. sativa
(T65), a vigorous progeny, two progenies exhibiting hybrid weakness Fig. 5 Phenotypes of pair1 and msp1 mutants of rice. (A) Twelve
(indicated by arrows), and O. glumaepatula (IRGC1105688). Photo- bivalents at diakinesis in the wild type. (B) Twenty-four univalents in
graphs are kind gifts from K. Doi (Kyushu University) and T. Kubo the pair1 mutant. (C) Normal anaphase I in the wild type. Magenta and
(Cancer Institute). green represent chromosomes and tubulin fibers, respectively. (D)
Chromosome non-disjunction at anaphase I of the pair1 mutant. (E) A
addition to S genes, many loci or genes distorting Mendelian normal megaspore mother cell (MMC, arrowhead) formed in an ovule
segregation of flanking marker genes in interspecific hybrids of the wild type. (F) Plural MMCs (arrowheads) in a single ovule of
the msp1 mutant. (G and H) In situ hybridization of the MSP1 mRNA
have been identified, many of which are designated ga. against a longitudinal section of the wild-type anther (G) and ovule
Recently, Harushima et al. (2002) reported that many map posi- (H). (G) PMC, pollen mother cell; Ta, tapetum; Ml, middle layer; En,
tions for numerous segregation distorter loci of japonica and endothecium; Ep, epidermis. The tapetum layer is intensely stained,
indica strains differed with cross-combinations, suggesting but the PMCs are not. (H) The nucellar cells are stained, but the MMC
rapid evolution of reproductive barrier genes. (arrow) is not.
Only a few pairs of loci involved in complementary F2
hybrid sterility support another genic model. Recently, Kubo chromosome 8. The double recessive plant causes female ste-
and Yoshimura (1999) reported a pair of complementary loci rility (Fig. 4E, F), whilst the single recessive homozygotes of
for F2 hybrid sterility, hsa1 on chromosome 12 and hsa2 on each locus exhibit moderate sterility.

8. Rice mutants and trait genes 55
Hybrid weakness regulator of gibberellin-dependent α-amylase (Gubler et al.
Hybrid weakness or hybrid breakdown is not directly 1995). Even though OsGAMYB is also highly expressed in the
related to sexual reproduction, but is worth noting in this sec- aleurone layer of rice seeds, one of its essential functions might
tion because they are one of the components of the reproduc- be in pollen development (Kaneko et al. 2004).
tive barriers. All hw loci reported so far (Hwa, hwb, Hwc, hwd
and hwe) complementarily affect viability of F1 or F2 plants Large-scale monitoring of specific gene expression in reproduc-
(Oka 1957, Amemiya and Akamine 1963, Chu and Oka 1972, tive organs
Fukuoka et al. 1998, Kubo and Yoshimura 2002). The plants Using cDNA microarray analyses and in situ hybridiza-
affected by the complementary gene sets generally show a tion techniques, Endo et al. (2004) revealed 259 non-redun-
small number of tillers, short culms and panicles, chlorosis or dant cDNA clones specifically or predominantly expressed in
necrosis of leaves, absence of seed sets, root growth inhibition, rice anthers, and classified into four groups. Lan et al. (2004)
and so on (Fig. 4G). reported the 253 ESTs exhibiting differential expression dur-
ing pollination and fertilization.
MEIOSIS
In the majority of eukaryotes, chromosome synapsis is Genes and Mutants Identified as Seed Characters
mediated by an evolutionarily conserved, tripartite, protein
structure called the synaptonemal complex (SC) (Wettstein et Embryo and endosperm mutants are divided into catego-
al. 1984, Zickler and Kleckner 1999). Synaptic mutants are ries of embryo, endosperm and grain shape for the morphologi-
classified into two categories, asynaptic and desynaptic cal characters, and dormancy, longevity, storage substances,
mutants (Li et al. 1945). The former class is characterized by shattering and taste for the physiological characters.
partial or complete inhibition of the synapsis of homologous
chromosomes, whereas the latter shows precocious separation Embryo
of bivalents following chromosome pairing. In O. sativa, many A large number of mutations affecting various aspects of
asynaptic (as) and desynaptic (ds) mutants have been isolated seed development have been reported in rice. Rice seeds con-
so far (Katayama 1963, Kitada and Omura 1983). sist of two distinct parts, an embryo and an endosperm. Over
Recently, Nonomura et al. (Nonomura et al. 2004a, Non- 200 embryo mutants reported to date (Nagato et al. 1989,
omura et al. 2004b) identified the rice meiotic genes PAIR1 and Kitano et al. 1993, Hong et al. 1995a) are categorized into five
PAIR2 from sterile mutant lines tagged with Tos17 (Hirochika groups: embryoless, deletion of embryonic organs, altered
et al. 1996). The loss-of-function mutations of two PAIR genes embryo size, modified organ position and aberrant morphology.
result in asynapsis and chromosome non-disjunction in male
and female meiocytes (Fig. 5A–D). The PAIR1 gene encodes a EMBRYOLESS AND ORGAN DELETION
novel nuclear protein (Nonomura et al. 2004a). PAIR2 encodes The embryoless1 (eml1) mutant develops seeds that lack
a protein homologous to the yeast HOP1 and Arabidopsis an embryo (Fig. 6A) (Hong et al. 1995a, Hong et al. 1995b).
ASY1 (Nonomura, K., Eiguchi, M., Nakano, M., Suzuki, T. and The eml1 embryo degenerates at the early stage (∼3 d after pol-
Kurata, N. unpublished data). lination), but endosperm development seems normal. Notably,
manifestation of an embryoless phenotype depends on the
OTHER STERILITIES growing temperature.
There are only a few other genes or mutations that are The globular embryo (gle) mutants develop embryos with
involved in sexual reproduction but not classified in the above a globular shape and completely lack embryonic organs (Fig.
categories. In the msp1 mutant flowers, the number of male and 6B). At least four loci (gle1–gle4) cause this phenotype. Analy-
female sporocytes increases abnormally (Fig. 5F) (Nonomura sis of a gle4 embryo using molecular markers indicates that
et al. 2003). The MSP1 gene encodes a putative leucine-rich GLE4 plays a role in radial pattern formation during rice
repeat (LRR) receptor-like protein kinase, and is expressed in embryogenesis, but not in formation of embryonic organs
the nurse cells surrounding the male and female sporocytes (Kamiya et al. 2003). The club-shaped embryo (cle) mutants
(Fig. 5G, H). Lee et al. (2004) identified the OsCP1 gene from fail to form both a shoot and a radicle, as does the gle muta-
T-DNA-tagged mutant lines. The oscp1 mutant showed a sig- tions (Fig. 6C). Unlike the gle embryos, palisade-shaped cells
nificant defect in pollen development, in addition to dwarfism. characteristic of the scutellar epithelium are formed in the
OsCP1 expression is observed mainly in anther locules but not whole epidermis of cle. Since the palisade-shaped cells of cle
in vegetative tissues. OsCP1 encodes the papain family express an α-amylase gene, it is considered that the most cle
cysteine protease. embryo comprises the scutellum (Hong et al. 1995a).
Kaneko et al. (2004) identified a MYB domain gene The organless (orl) mutants also lack both a shoot and a
OsGAMYB, from the Tos17-tagged lines. The osgamyb mutant radicle (Fig. 6D). Unlike cle1, the orl1 embryo differentiates
exhibits defects especially in anther and pistil development, but palisade-shaped cells in the epidermis-facing endosperm, sug-
not in vegetative tissues. GAMYB is a positive transcriptional gesting that embryonic polarity is not affected in orl1. Consist-

9. 56 Rice mutants and trait genes
Fig. 6 Phenotypes of rice embryo mutants from median longitudinal sections. (A) eml1 seed showing no embryo. (B) gle1 embryo without
organs. (C) cle1 embryo without organs. (D) orl1 without organs. (E) shl1 embryo lacking a shoot but with a normal radicle. (F) sho1 embryo
with an aberrant shoot lacking a coleoptile but with a normal radicle. (G) Wild-type embryo (left), ge embryo with enlarged scutellum (center)
and re1 embryo in which every organ is reduced (right). (H) apd1 embryo with apically displaced shoot and radicle. (I) enl large embryo lacking
endosperm. S, shoot; Sc, scutellum; R, radicle. Photographs are kind gifts from Y. Nagato (University of Tokyo).
ently, tissue specificity of OSH1 gene expression is maintained chron, resulting in deformed shoot architecture (Itoh et al.
in orl1 (Sato et al. 1996). 2000).
Four shootless (shl) mutants, shl1, shl2, shl3 and shl4,
have been reported to be indispensable in shoot formation dur- EMBRYO SIZE
ing embryogenesis (Satoh et al. 1999). Of these, shl1, shl2 and Two types of mutations causing either a reduction or
shl4 exhibit indistinguishable phenotypes; complete loss of enlargement of embryo size have been reported (Hong et al.
shoots, coleoptile and epiblast and normal radicle formation 1996). The giant embryo (ge) mutants have a 1.2–1.5 times
(Fig. 6E). In another mutant, shl3, in addition to deletion of the longer embryo and reduced endosperm (Fig. 6G). The scutel-
shoot, the radicle is exogenously produced and cells in the lum is enlarged but the sizes of the shoot and radicle are not
remaining tissues are highly vacuolated. SHL1, SHL2 and affected (Hong et al. 1996). Three reduced embryo (re)
SHL4 function upstream of OSH1 (Satoh et al. 1999). At least mutants, re1, re2 and re3, exhibit a reduction in embryo size.
two loci, RAL1 and RAL2, are required for radicle formation. The re embryo is less than half the length of the wild-type
The ral embryo seems to be truncated in the apical–basal direc- embryo, and shows a reduction in all embryonic organs includ-
tion but develops a shoot. After germination, the ral plant pro- ing the apical meristems and the enlarged endosperm (Fig. 6G)
duces normal crown roots. Thus, it is supposed that the ral (Hong et al. 1996). Anatomical and double mutant analyses
phenotype bears root-producing ability, but is caused by dele- using ge, re and other mutants suggest that the primary func-
tion of the basal embryonic region where the radicle develops. tion of GE and RE resides in endosperm development, not in
In addition, ral1 affects vascular pattern formation (Scarpella et embryogenesis (Hong et al. 1996).
al. 2003).
ORGAN POSITION
ORGAN MORPHOGENESIS The APD1 locus is related to organ position. In the apical
Two shoot organization (sho) mutants, sho1 and sho2, displacement (apd) mutant embryo, the shoot is formed at the
show severe defects in embryonic organ development. In sho apex of the embryo and the radicle at the center of the embryo
embryos, the first to the third leaves are malformed, but the (Fig. 6H). This phenotype is due mostly to an enlargement of
radicle develops normally (Fig. 6F). The sho1 plant produces the basal region of the embryo and underdevelopment of the
malformed leaves with a random phyllotaxy and a short plasto- scutellum (Hong et al. 1995a).

10. Rice mutants and trait genes 57
Endosperm Seed dormancy
Because the cereal endosperm is an important staple diet Since seed dormancy is a complex and quantitative char-
in many countries, studies on genes acting in the endosperm acter influenced by both genetic and environmental factors, the
are important issues for both basic research and plant breeding. regulatory mechanism of dormancy is not well understood.
Although a large number of genes that are associated with stor- OsVP1 is a rice ortholog of VP1 in maize and ABI3 in Arabi-
age substances in the endosperm, such as protein and starch, dopsis (Hattori et al. 1994). Molecular analysis and in situ
have been identified, analysis of genes regulating endosperm expression patterns indicate the involvement of OsVP1 in seed
development is limited. Only one mutant affecting endosperm maturation processes including dormancy, as in maize and Ara-
development has been reported. The endospermless (enl) bidopsis (Hattori et al. 1995, Miyoshi et al. 2002). The rice
mutant fails to form an endosperm (Fig. 6I) (Kageyama et al. vivipary (riv) mutants, riv1 and riv2, exhibit precocious germi-
1991). After fertilization, the enl1 endosperm starts to develop nation before harvesting and reduced sensitivity to abscisic
but degenerates at an early stage (∼3 d after pollination), result- acid (Miyoshi et al. 2000).
ing in the production of a very large embryo (Kageyama et al. QTL analysis has detected dormancy-related genes. By
1991, Miyoshi et al. 2000). The mutations associated with using RILs (recombinant inbred lines) between cultivated and
embryo size, ge and re, are also supposed to affect endosperm wild rice strains, 17 QTLs have been detected (Cai and
growth (Hong et al. 1996). Morishima 2000). In addition, five QTLs have been detected
using BILs (backcross inbred lines) derived from a backcross
SEED MATURATION of Nipponbare/Kasalath/Nipponbare (Miura et al. 2002).
To date, a large number of rice genes related to seed matu-
ration processes, mainly starch and storage protein synthesis
Heterochrony
and their accumulation, have been identified.
The heterochronic genes control the temporal regulation
Rice seeds accumulate various kinds of substances as
of development and greatly affect plant architecture. Two hete-
nutrients to support seedling growth. Starch, which consists of
rochronic genes have been identified and characterized in rice.
amylose and amylopectin, is the major source of nutrition for
One is PLASTOCHRON1 (PLA1) (Itoh et al. 1998). In the pla1
seedling growth. The Waxy (Wx) gene encodes a granule-bound
mutant, primary rachis branches in the panicle are converted
starch synthase involved in amylose synthesis (Nelson and Pan
into vegetative shoots (Fig. 7B). Because vegetative to repro-
1995). Two naturally occurring Wx alleles, Wxa and Wxb, are
ductive phase transition occurs normally, the vegetative phase
known (Sano 1984, Sano et al. 1986). Rice cultivars (mainly is elongated and both vegetative and reproductive programs are
japonica cultivars) with a Wxb allele produce lower amounts of expressed simultaneously in the pla1 mutant. Thus, PLA1 is a
Wx protein than those (mainly indica cultivars) carrying Wxa heterochronic gene controlling proper termination of the vege-
(Sano et al. 1986). Wxb carries a substitution mutation at the 5′ tative phase. The pla1 mutant also shows short plastochron, an
spliced site of the first intron, and causes a low content of amy- enlarged SAM, small leaves, bending of the lamina joint and
lose (Cai et al. 1998, Isshiki et al. 1998). The dull (du) muta- dwarfism (Fig. 7A). PLA1 encodes a member of CYP78A, a
tions also affect amylose content. In du-1 and du-2, the amount subfamily of the large cytochrome P450 family, and is
of spliced Wxb mature transcript, but not Wxa transcript, is expressed in young leaves and bracts (Fig. 7C, D, Miyoshi et
reduced (Isshiki et al. 2000). al. 2004).
Cereal seed proteins have been classified into four types, The mori1 mutant reiterates the wild-type second leaf
water-soluble albumin, salt-soluble globulin, alcohol-soluble stage and fails to induce adult phase (Asai et al. 2002). MORI1
prolamin and acidic or basic solution-soluble glutelins. Among is a heterochronic gene playing an important role in juvenile to
them, glutelin has been studied intensively because it is the adult phase transition.
most abundant storage protein occupying 60–80% of the total
endosperm protein. Glutelin precursors are encoded by a multi- Tolerance and Resistance
gene family that consists of the GluA and GluB subfamilies
(Takaiwa et al. 1991). Mutations showing a reduction or lack of Rice has evolved many kinds of resistance or tolerance
a particular subunit or precursor polypeptide have been identi- genes against biotic and abiotic stresses. Almost all of the
fied. Three loss-of-function mutants, gulutelin1 (glu1), glu2 resistance or tolerance genes have been found as variant alleles
and glu3, have defects in subunits 1a, 2a and 3a, respectively. in a variety of cultivated and wild strains.
A dominant mutation of Low glutelin content1 (Lgc1) causes a
reduction in glutelin content. Unlike the above glu mutations, Disease resistance
the Lgc1 mutation has been found to influence the amount of A large number of resistant genes or alleles specific to
most glutelin subunits (Iida et al. 1997). It is revealed that Lgc1 individual races of fungi and bacteria have been identified.
suppresses accumulation of glutelin gene family transcripts via Two serious and well-studied rice diseases are rice blast, a fun-
RNA silencing (Kusaba et al. 2003). gal disease caused by Magnaporthe grisea, and bacterial bright

11. 58 Rice mutants and trait genes
avilurence gene that is interactive with Pi-ta has also been iso-
lated (Orback et al. 2000). In addition, an intensive gene-for-
gene analysis has been carried out of the multiple steps of the
infectious process of Magnaporthe in rice (Sesuma and
Osbourn 2004), and a variety of cDNAs induced during the
defense steps in the rice blast-resistant mutant have also been
identified (Han et al. 2004).
Recently, an approach has been used to identify mutants
which confer breakdown of Xa21-mediated resistance from
thousands of mutant strains (Wang et al. 2004). Xa21 is a wide
spectrum resistance gene for multiple varieties of X. oryzae.
Therefore, findings of the breakdown mutants for Xa21 resist-
ance would clarify genes composed of the Xa21 multispectrum
defense pathway.
A hundred disease-resistant or defense-response gene-like
sequences have been mapped into several clusters on the rice
chromosomes, and some of them coincide with QTLs or major
resistance genes (Wang et al. 2001). The NBS family has
around 400 members in the rice genome (Monosi et al. 2004),
and the receptor-like kinase (RLK) family has about 1,200
members (Shiu et al. 2004).
Lesion mimic mutants
The lesion mimic mutants show symptom-like spots on
leaves and sometimes on the panicles. Over 11 mutants have
been identified and are classified as spotted leaves (spl) or cell
death and resistance (cdr) (Fig. 8A). Most of them are thought
to have defects in genes with roles in the disease defense path-
ways against attack from fungi, bacteria or viruses, althought a
Fig. 7 Expression and mutant phenotype of PLA1. (A) Seedlings of few spl mutants do not show resistance. Some mutant genes
the pla1 mutant and the wild type. Due to the shortened plastochron,
which produce lesions mimicking symptoms are well charac-
the pla1 mutant produces more leaves than the wild type. (B) Panicles
of the pla1 mutant and the wild type. Primary rachis branches of pla1 terized (Takahashi et al. 1999, Yamanouchi et al. 2002). Two
are converted into vegetative shoots. (C and D) In situ hybridization of genes cloned from spl mutants are the heat stress transcription
PLA1 mRNA in wild-type leaves. (C) Expression of PLA1 at the base factor (HSF) gene (Kawasaki et al. 1999), and a U-box/Arma-
of young leaves. (D) Expression of PLA1 in bracts. dillo repeat protein gene involved in the ubiqitination pathway
(Zeng et al. 2004).
caused by Xanthomonas oryzae. Most resistance genes identi- Insect resistance
fied for bacterial and fungal pathogens have nucleotide-bind- More than 200 species of insects are associated with rice
ing sites/LRRs (NBS-LRR) and/or serine/threonine receptor plants as pests. Among them, the brown planthopper (BPH;
kinase domains. In total, >20 resistance genes to Xanthomonus Nilaparvata lugens Stål), whitebacked planthopper (WBPH;
are identified, and three genes are cloned; Xanthomonus resist- Sogatella furcifera Horvath), green leafhopper (GLH; Nepho-
ance gene 1 (Xa1), Xa21 and Xa26, encoding LRR receptor tettix virescens Distant), green rice leafhopper (GRH; Nepho-
kinase proteins (Yoshimura et al. 1998, Wang et al. 1998, Sun tettix cincticeps Uhler) and Asian rice gall midge (ARGM;
et al. 2004). Among >60 blast resistance genes/alleles includ- Orseolia oryzae Wood-Mason) are the worst pests for which
ing QTLs, two genes are cloned: Pyricularia oryzae (Mag- the major host resistance genes have been well studied. Most of
naporthe grisea) resistance gene ta (Pi-ta) encoding NBS-LLR the >70 resistance genes reported so far have been identified
and a gene found in a resistant strain Zhai Ye Qing8 (ZYQ8) using RILs, NILs or detected as QTLs.
encoding a protein carrying a low homology to the serine/thre- More than 13 resistance genes against BPH and six genes
onine kinase domain and a calmodulin-binding domain (Wang against WBPH have been identified, and several BPH resist-
et al. 1999, Zheng et al. 2004). ance genes have been tagged on a molecular linkage map. An
A single base change in Pi-ta confers a difference between example of antibiosis is shown in Fig. 8B–D. Rice ovicidal
resistance and susceptibility (Bryan et al. 2000). Avirulence response to WBPH is characterized by the formation of watery
genes in the infectious blast fugi are also characterized. An lesions and production of an ovicidal substance, benzyl ben-

12. Rice mutants and trait genes 59
RILs or NILs is the most convenient way to detect multiple
loci for tolerance and sensitivity (Nguyen et al. 2004). Instead
of identification of stress tolerance genes using genetic meth-
ods, another molecular approach to identify and isolate such
tolerance-related genes is employed (de los Reyes et al. 2003,
Dubouzet et al. 2003). Dubouzet et al. (2003) isolated five
stress responsible rice genes of the DREB/CBF transcription
factor by homolog hunting of Arabidopsis genes. The cloned
genes are expressed under cold or dehydration and high-salt
stress and then activate a number of target genes. Attempts to
generate stress-tolerant transgenic rice with stress tolerance-
related genes have also been made (Garg et al. 2002, Mukho-
Fig. 8 (A) Leaf phenotypes of spl2, spl4 and spl9 mutants. (B) A padhyay et al. 2004). Recently, a more sophisticated genomic
watery lesion attacked by WBPH. (C) Resistance response of a approach has become available involving combinational analy-
japonica cultivar Asominori with dead eggs. (D) Susceptible response sis of expression profiling using microarray analysis with seg-
of an indica cultivar IR24 with live eggs. Photographs are kind gifts
regated progeny from a cross of tolerant and sensitive parent
from A. Yoshimura and H. Yasui (Kyushu University).
strains (Cooper et al. 2003, Hazen et al. 2004).
Stress tolerance is tightly related to the developmental
zoate, which causes high egg mortality of WBPH (Seino et al. stages and specific organs. For instance, metal ion and salinity
1996, Suzuki et al. 1996). A gene with ovicidal activity to tolerance is expressed mainly in the root during the process of
WBPH, Ovc, and four ovicidal QTLs, qOVA-1–3, qOVA-4, ion absorption through water uptake. Cold tolerance is espe-
qOVA-5–1 and qOVA-5–2, have been identified (Yamasaki et cially needed during the germinating and flowering stages. It
al. 2003). Ovc was the first gene to be identified that kills might be possible to identify tolerant mutants/genes in the
insect eggs in plants. mutant/variant groups of these organs. Submergence tolerance
Another type of antibiosis is found in resistant varieties may be specifically important in rice, a character enabling sur-
against GLH and GRH. The resistant plants cause delayed vival during deep water stress. A group of wild rice strains and
growth and eventual death of infesting insects. The resistance landraces show submergence tolerance, which results in rapid
may be concerned with sucking inhibition after their infesta- internode elongation. This specific character must also be regu-
tion. So far, six loci for resistance to GRH, Grh1–Grh6, are lated by a genetic program for culum development. A recent
known. NILs carrying single resistance genes show weak review and a QTL analysis for submergence sensitivity have
resistance (Grh1and Grh2) and susceptibility (Grh4). On the shown various aspects of this reaction (Jackson and Ram 2003,
other hand, NILs carrying two resistance genes, Grh2 and Toojinda et al. 2003).
Grh4, express strong resistance to GRH and GLH. The interac-
tion of Grh2 and Grh4 expresses a strong resistance against Coloration
two leafhopper species in rice.
Gm2 is a dominant gene conferring resistance to biotype 1 Coloration is one of the most important characters of
of ARGM (Diptera: Cecidomyiidae), the major dipteran pest. plants, especially in relation to the chlorophyll biosynthesis
Tissue necrosis, represented by a typical hypersensitive reac- pathway. Tissue-specific coloration with anthocyanin is an
tion accompanied by maggot mortality, is observed within 4 d interesting phenomenon, which is partly integrated in the organ
after infestation of avirulent biotype 1 of the ARGM (Bentur developmental program. A large number of mutants and vari-
and Kalode 1996). Two other resistance genes, Gm6 and Gm7 ants have been identified in these categories.
(both may be identical), are tightly linked to Gm2 (Katiyar et
al. 2001, Sardesai et al. 2002). Anthocyanin and other colorations
Wild rice species are excellent genetic resources for resist- More than 40 mutants and/or variants have been found to
ance genes and can also be used to integrate their resistance possess purple coloration genes/alleles by modifying anthocy-
loci into cultivated rice (Brar and Khush 1997). Some loci have anin biosynthesis in rice. The divergent pattern of anthocyanin
been confirmed as being transferred successfully into culti- coloration in specific organs, e.g. coleoptile, leaf axil, leaf
vated rice via homologous chromosome recombination. None sheath, leaf blade, leaf margin, midrib, leaf apex, internode,
of the rice resistance genes to insects have yet been cloned. nodal ring, pericarp and stigma, is detected in the mutants/vari-
ants. It has been reported that these specific patterns in expres-
Stress tolerance sion of anthocyanin are attributed to dysfunction of the key
Sensitivities to various stresses such as drought, cold (low regulator of anthocyanin biosynthesis R genes/alleles in rice. R
temperature), salt/osmotic stress, herbicides and metals vary genes encode bHLH protein transcription factors and regulate
from strain to strain. QTL analysis using an F2 population, pigmentation in specific organs. One of the rice R loci, purple

13. 60 Rice mutants and trait genes
leaf (PI), has a complex allele PI(w) composed of at least two Mutant and Variant Genes in Future Functional Genom-
genes of the bHLH proteins (Sakamoto et al. 2001). The com- ics of Rice
plex nature of multiple alleles of the R loci may be involved in
a variety of organ/tissue-specific regulations of anthocyanin As shown in this mini-review, many trait genes revealed
biosynthesis. Sixteen mutants for coloration with substances by mutant and QTL analyses have been accumulated. In the
other than anthocyanin have been reported: Brown furrows of next decade, full genome sequence information should help to
hull (Bf), gold furrows of hull (gf1and2), gold hull and inter- promote the rapid growth in isolation and characterization of
node (gh1-3), redpericarp and seed coat (Rd), and so on. These these trait genes. The collection and positioning of many pieces
mutants also show organ-specific coloration. of genes in the developmental and physiological pathways will
decipher the many gene networks and thus determine the mor-
Chlorophyll phological and developmental regulations for those gene net-
Chlorophyll synthesis is very important to all plants in works. Morphological mutants play an indispensable role in the
relation to photosynthesis. Chlorophyll and its encasing study of rice development and of QTLs with regards to plant
organelle, the chloroplast, are both synthesized from chloro- growth reactions. However, individual gene characterization is
plast- and nucleus-encoded genes. Studies on chlorophyll and not enough to achieve such kinds of studies, but systematic
chloroplast biosynthesis pathways have been extensively com- work using genomic and bioinformatic approaches is required.
piled for many plants. In rice, >70 chlorophyll mutants exhibit- Generation of a search system for knock-out mutants for all
ing albino, chlorina, stripe, virescent, yellow-green and zebra rice genes, microarray analysis for mutant and variant strains,
leaves have been recorded. Albino has no chlorophyll, com- gene/genome comparative studies with Arabidopsis, wild rice
and other cereal species, and an ideal analytical system for
pletely lacks any green color and dies soon after germination.
handling large quantities of data using bioinformatic tools will
Chlorina mutants have light green leaves and a low ability for
together promote functional genomic studies in the very near
photosynthesis, thus growing weakly and depending on the
future.
gene locus or allele. The stripe phenotype appears as a white
sectored leaf in the longitudinal direction, and is different in
Appendix 1
size and number of white stripes among the loci. On the con-
trary, zebra has a white or yellow transverse banding phenotype
(1) http://tos.nias.affrc.go.jp/~miyao/pub/tos17/
in the green leaves. This phenotype is highly variegated in (2) http://www.shigen.nig.ac.jp/rice/oryzabase/nbrpStrains/kyushu-
band size, frequency and color at every stage of plant growth. Grc.jsp
Virescent mutants also show conditional chlorosis in the leaf to (3) http://www.shigen.nig.ac.jp/rice/oryzabase/genes/geneClasses.jsp
different degrees depending on the temperature, strength and
wavelength of light. One of the virescent mutant inhibits the Acknowledgments
translation of plastid transcripts during chloroplast differentia-
tion (Sugimoto et al. 2004). These analyses indicate there are We are grateful to Dr. Y. Nagato (The Univeristy of Tokyo) for
his valuable discussions and helpful comments, and also for kindly
several components used in chlorophyll synthesis and the pho-
providing photographs. We would also like to thank Drs. A.
tosynthesis pathways. Most classes of chlorophyll mutants are Yoshimura, H. Yasui, K. Doi (Kyushu University), T. Kubo (Cancer
composed of >10 independent loci, suggesting that each bio- Institute, Tokyo), J. Kyozuka, H. Hirano (The University of Tokyo),
synthesis pathway is constructed with at least 10 proteins that and Y. Inukai, H. Kitano, M. Matsuoka (Nagoya University) for their
are necessary to complete chlorophyll/chloroplast biogenesis. useful advice and kindly providing photographs. Finally, we would
like to thank Dr. S. Iyama (National Institute of Genetics) for his huge
One chrolina mutant has been revealed to encode OsCHLH, a
effort in selecting and gathering information for rice genes and
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(Received October 30, 2004; Accepted November 10, 2004)