Recent Progress on Rice Genetics in China - CiteSeerX

Journal of Integrative Plant Biology 2007, 49 (6): 776−790

.Invited Review.

Recent Progress on Rice Genetics in China Hua Jiang1, 2, Long-Biao Guo1 and Qian Qian1* ( 1State Key Laboratory of Rice Biology, China National Rice Research Institute, Hangzhou 310006, China; 2

The Agricultural College, Yangzhou University, Yangzhou 225006, China)

Abstract Through thousands of years of evolution and cultivation, tremendously rich genetic diversity has been accumulated in rice (Oryza sativa L.), developing a large germplasm pool from which people can select varieties with morphologies of interest and other important agronomic traits. With the development of modern genetics, scientists have paid more attention to the genetic value of these elite varieties and germplasms, and such rich rice resources provide a good foundation for genetic research in China. Approximately 100 000 accessions of radiation-, chemical- or insertion-induced mutagenesis have been generated since the 1980s, and great progress has been made on rice molecular genetics. So far at least 16 variant/mutant genes including MOC1, BC1, SKC1, and Rf genes have been isolated and characterized in China. These achievements greatly promote the research on functional genomics, understanding the mechanism of plant development and molecular design breeding of rice in China. Here we review the progress of three aspects of rice genetics in China: moving forward at the molecular level, genetic research on elite varieties and germplasms, and new gene screening and genetic analysis using mutants. The prospects of rice genetics are also discussed. Key words: functional genomics; genetics; germplasm resources; rice (Oryza sativa). Jiang H, Guo LB, Qian Q (2007). Recent progress on rice genetics in China. J. Integr. Plant Biol. 49(6), 776−790.

Available online at www.blackwell-synergy.com/links/toc/jipb, www.jipb.net

As the major force of evolution, variance exhibits plants’ perfect adaptation to environments. Thousands of different traits and alleles emerge, because of genetic variance; they form a large germplasm pool from which people can select varieties with morphologies of interest and other important agronomic traits that best serve crop modification and plant breeding. Since Mendel’s careful choice of traits led to the illustrious Mendel’s Law, scientists not only pay attention to

Received 1 Dec. 2006

Accepted 27 Feb. 2007

Supported by the High-Tech Research and Development (863) Program of China (2006AA10A102) and the State Key Basic Research and Development Program of China (2005CB120805). Publication of this paper is supported by the National Natural Science Foundation of China (30624808). *Author for correspondence. Tel: +86 (0)571 6337 0537; Fax: +86 (0)571 6337 0389; E-mail: . © 2007 Institute of Botany, the Chinese Academy of Sciences doi: 10.1111/j.1672-9072.2007.00492.x

plant breeding through artificial selection and steering natural selection, but also show great interest in the genetic value of these variant morphologies. Rice (Oryza sativa L.) is one of the most important staple crops in the world and more than half of the world’s population depends on it as a main source of nuturition (Figure 1). Owing to its small genome size (~389 Mb), the known genome sequence (International Rice Genome Sequencing Project (IRGSP), 2005), ease of Agrobacterium-mediated transformation (Hiei et al. 1994), and genetic synteny with other cereal genomes (i.e. barley, wheat, maize and sorghum) (Bennetzen and Ma 2003), rice is not only a model monocotyledon for research on plant development, but also a model crop for research on cereals’ genomics and evolution. Numerous scientists worldwide contributed great efforts to developments such as Mendelian segregation in rice (van der Stok 1908), an agreed system of rice chromosome numbering, and linkage groups and nomenclature for gene symbolization reported in succession (Kadam and Ramiah 1943; Nagao and Takahashi 1963) to make rice a favored higher plant for molecular and cellular genetic studies before 1980. With the development of molecular biology and molecular genetics, much

Recent Progress on Rice Genetics in China 777

genetic research has been carried out on all schematic aspects of the rice life-cycle (Figure 1) in China, and great progress has been achieved, especially in the past 5 years (Han and Xue 2003; Xue et al. 2003; Wang and Li 2005b). Whole genome shotgun sequencing of indica rice 9311, and also the sequencing of chromosome 4 of japonica rice Nipponbare, which is a part of the International Rice Genome Sequencing Project (IRGSP), have been completed by Chinese scientists and published online (Feng et al. 2002; Yu et al. 2002). In the present paper, we summarize recent progress made by scientists in China on rice genetics, especially in gene mapping and cloning from three basic aspects, for example, moving forward at the molecular level, genetics research on elite varieties and germplasms, and new gene screening and genetic analysis using mutants. Finally, we present our strategy for resolving the existing problems surrounding rice genetics and speculate on the development of rice genetics in the future.

Moving Forward at the Molecular Level Many researchers in China are currently engaged in rice genetics to illuminate the mechanism of plant development. Great efforts are being made to try to keep up with research being conducted overseas. However, genetic research in China lagged behind and the development of rice genetics was also full of setbacks. Although the earliest studies on rice genetics can be traced back to the 1930s, the research on it was almost stagnated because of the Anti-Japanese War and the Civil War from the 1930s to the 1940s. From the 1950s to the 1960s, most efforts were made on rice breeding for high-yielding varieties, and the development of rice genetics was very slow. Since the 1970s, due to the largely successful hybrid rice breeding, rice genetics has been revived. For a long time the studies on rice had still been concentrated on classic genetics, and the research objectives had been focused mainly on semidwarf, disease resistance and other morphologies that are important for rice breeding. Many researchers focused on the

Figure 1. The life circle of rice. The figure exhibits the cycle by showing some landmark events that have occurred in rice. MS, male sterility; PSGMS, photoperiod-sensitive genic male-sterile; TGMS, thermo sensitive genic male-sterile.

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description of the morphology, the inheritance analysis, the chromosome location using maker stocks and trisomic lines as tools through cross testing and the basic karyotype analysis to unify the chromosome numbering system in rice (Qian and Cheng 2006). With the development of modern molecular biology and molecular genetics, and in virtue of the published sequence information, much progress has been made in China, and some has reached the advanced international level. Since the 1990s, the chromosome numbering system in rice had been unified, and many young scientists have returned from overseas and taken part in genetic research at the cellular and molecular levels, which has pushed forward the development of rice genetics in China.

Genetics Research on Elite Varieties and Germplasms There are about 120 000 accessions of rice germplasms all over the world, and about 80 000 of them are in China. Such richness in rice germplasms provides a good resource for genetic research. Although rice genetic research lagged behind in our country, with the help of our resource advantages, our progresses is catching up with the world’s top level. In this section, we emphasize agronomically important traits in grain production and their genetic studies by using elite varieties and germplasm resources. Identification and use of elite rice gemplasm Plant height Definitely, the most important gene resource in rice genetics and breeding worldwide is the semi-dwarf gene SD1. The exploitation and use of semi-dwarf genes in the 1960s led to the great achievement that was widely known as the “green revolution”, stimulating a major increase in rice production in China (Gu 1980). Many semi-dwarf resources were derived from the special germplasm resources Ai-Jio-Nan-Te or Deo Geo Woo Gen. Since then, scientists in China have paid more attention to semi-dwarf genetics than ever before (Liang et al. 1996; Wang et al. 2002), and many researchers have focused on the investigation of the inheritance and identification of linkage groups of the semi-dwarf genes using cross tests, marker stocks and the production of trisomic lines (Li et al. 2001, 2002). Since the 1980s, three semi-dwarf genes sd-g, sdt2 and a small grain dwarf d162 (t), were primarily or finely mapped on chromosomes 4, 5 and 3, respectively (Li et al. 2003c; Liang et al. 2004; Zhao et al. 2005). Except the semi-dwarf genes, two other plant-height genes were also cloned or fine-mapped. The ELONGATED UPMOST INTERNODE1 (EUI1) gene, an important germplasm for seed production of hybrid rice, was cloned

on chromosome 5 (Luo et al. 2006a; Zhu et al. 2006), which encodes cytochrome P450 protein related to gibberellin acids (GA) biosynthesis (Zhu et al. 2006). Another EUI2 gene was fine-mapped on chromosome 10 (Wei 2006b). Except for the recessive plant-height genes mentioned above, three dominant plant-height genes also have been mapped. Deng et al. (2004) reported a new long-culm mutant “d111” and the gene LC (t) conferring this mutation was located on chromosome 1. Liu et al. (2006) mapped a DOMINANT SEMI-DWARF (DSD) gene on chromosome 7. Wei et al. (2006a) mapped a dominant dwarf gene D-53 on chromosome 11. However, only a few kinds of dwarf resources have been used in rice breeding, and moreover, most indica varieties extensively used in the current rice production were derived from the semi-dwarf varieties (Ai-Jio-Nan-Te) controlled by sd1 or its alleles. Therefore, identification and use of new semi-dwarf resources/genes are important subjects for rice breeding. On the other hand, we will be able to get much more information about the pathway controlling the rice plant height by using new semi-dwarf germplasm resources. Male sterility An important resource in genetics and breeding is male sterility genes. There are two types of male sterility: genic male sterility (GMS) and cytoplasmic male sterility (CMS). CMS is a maternally-inherited character that can be found in over 150 plant species. CMS/restoration systems which are considered to be an ideal model for study of the interactions between nuclear and organellar genomes, serve as an important tool for hybrid seed production. In rice, there are three major types of CMS/restoration systems, including CMS-BT (borotype), CMS-WA (wild abortive), and CMS-HL (Honglian). The first commercially used CMS-WA germplasm was discovered by Chinese scientist Longping Yuan in the 1970s, and was used to develope the three-line system hybrid rice. As a gametophytic system, CMS-BT is the most widely investigated rice CMS system at the genetic level, and is originally derived from the cytoplasm of an indica rice variety Chinsurash BoroII. Recently, Dr Yaoguang Liu’s laboratory published the results of a study, in which they cloned the CMS and two Rf genes in the CMS-BT/restoration system and elucidated the molecular mechanism for male sterility and fertility restoration (Wang et al. 2006d). This is a significant contribution to hybrid rice dedicated by Chinese scientists. A number of fertility restorer genes that are involved in other CMS systems have been studied genetically. Two Rf loci, Rf5 and Rf6 (t), responding to CMS-HL, have been located in different regions of chromosome 10 (Liu et al. 2004). Both the CMSDT restorer gene Rf-d1 (t) and the CMS-DA restorer gene Rf-d (t) were also detected on chromosome 10 (Xie et al. 2001; Tan et al. 2004). Two CMS-WA restorer genes Rf3 (t) and Rf4 (t) have been located on chromosomes 1 and 10, respectively


(Yang et al. 2002a). Moreover, elite germplasm Hubei photoperiod sensitive genic male-sterile rice (HPCMR) Nongkeng 58S was discovered by Chinese scientist Mingsong Shi in 1973, resulting in the twoline system hybrid rice. Recently, the significant advances have been taking place in genetic research on photoperiod-sensitive genic male sterility (PSGMS) and thermo-sensitive genic male sterility (TGMS). Three major genes conferring PSGMS or TGMS, pms1, pms3 and tms5, were finely mapped on chromosomes 12, 7 and 2 (Liu et al. 2001; Lu et al. 2005; Yang et al. 2006). Li et al. (2006a) cloned another nuclear male-sterile gene, TDR from japonica cultivar 9522 on chromosome 2, which is responsible for tapetum degradation. Biotic stress resistance Biotic stress mainly includes two aspects: disease stress and insect stress. Throughout the world, bacterial blight, blast and sheath blight are the three most destructive diseases to rice and have been a focus of breeding efforts for decades. The studies on disease tolerance were focused on the identification of new resistant strains with systematic and standardized naming of the identified resistant genes and the resistant genes’ allelic tests. Since the bacterial blight-resistant gene Xa21 became the first cloned gene through a map-based cloning strategy in rice (Song et al. 1995), research on disease resistances has became an area of great interest. To date, two blight-resistant genes, Xa26 and Xa13, have been cloned by Chinese scientists (Sun et al. 2004a; Chu et al. 2006b). Xa26 on chromosome 11 encodes an leucine rich repeat (LRR) receptor kinase-like protein (Sun et al. 2004a). xa13, a recessive allele conferring disease resistance against bacterial blight, plays a key role in both disease resistance and pollen development, and represents a new type of plant disease resistance. The dominant allele, Xa13, is required for both bacterial growth and pollen development. Promoter mutations in Xa13 cause down-regulation of expression during hostpathogen interaction, resulting in the fully recessive xa13 that confers race-specific resistance (Chu et al. 2006b). Also five other genes (Xa4, Xa2, Xa-7, Xa-23 and Xa-25) with resistance to bacterial blight have been mapped or delimited to a narrow physical interval (Wang et al. 1996; Sun et al. 2004b; Gao et al. 2005; He et al. 2006b; Fan et al. 2006b). Further studies found that most of the blast-resistance genes are mapped on chromosomes 11 and 4, and some are closely linked. This kind of clustering distribution is especially obvious during the genetic research of the blast-resistant genes (for more details, see Figure 2). Chen et al. (2005) first mapped the Pi37 (t) on chromosome 1, and ultimately the Pi37 (t) was defined to a 374-kb interval where only four candidate genes with the resistance gene conserved structure (NBS-LRR) were further identified to a DNA fragment of 60 kb in length. The Pi36 (t) locus, which was

preliminarily mapped on chromosome 8, was then physically delimited to an interval of about 17.0 kb (Liu et al. 2005d). Chen et al. (2006c) isolated Pi-d2 by a map-based cloning strategy. Pi-d2 encodes a receptor-like kinase protein with a predicted extracellular domain of a bulb-type mannose-specific binding lectin (B-lectin) and an intracellular serine-threonine kinase domain. Pigm (t) was finely mapped to an approximately 70-kb interval between markers C5483 and C0428 on chromosome 6, which contains five candidate NBS–LRR disease resistance genes. Another blast-resistant gene, Pi26 (t), might also be located at the same region (Deng et al. 2006). There is still much progress being made in the genetic research of blast-resistant genes (Tang et al. 2000; Zhang et al. 2003; Chen et al. 2004b; Zhou et al. 2004; Zhang et al. 2006a), however, due to the limited length of this paper we will not discuss them all in detail. Chinese scientists overseas have also made much progress in the studies of disease resistance. Liu et al. (2002) reported that Pi2 (t) is closed linked with Pi9 (t). Qu et al. (2006) cloned the Pi9 gene, which encodes a nucleotide-binding site LRR protein. Insect-resistance studies are mainly carried out on brown planthopper (BPH) and white brown planthopper (wbph). Chen et al. (2006a) fine-mapped a resistance gene, which was designated tentatively as bph19 (t), against BPH on chromosome 3. Yang et al. (2004b) delimited bph15 to a region of 47 kb on chromosome 4. Another three BPH-resistant genes, Bph12 (t), bph2, bph9 and a WBPH-resistant gene wbph6 (t) were located on chromosomes 4, 12, 12 and 11, respectively (Ma et al. 2002; Yang et al. 2002a; Sun et al. 2006; Su et al. 2006). Hybrid sterility and wide compatibility Cultivated rice can be classified into two distinct subspecies: indica and japonica. The hybrids between indica and japonica rice varieties show the higher yield potential compared with indica/indica or japonica/japonica hybrids due to greater genetic divergence. However, use of intersubspecific heterosis has encountered many obstacles, and the primary one is the partial to complete fertility of the indica/japonica F1 hybrids. A large number of loci conferring the male or female sterility of the hybrids have been identified. Towards the genetic basis of the hybrid sterility, several genetic models are proposed. The “one-locus sporo-gametophytic interaction” proposed by Ikehashi and Araki (1985) is the most popular one; the genetic behavior of most of the identified loci can be explained by this model. For example, at the S5 locus causing hybrid female sterility, three alleles, S5i, S5j and S5n, are present in indica, japonica, and wide compatible varieties (WCVs), respectively. The S5n allele is considered to be the major contributor to the full fertility of indica/japonica hybrids. Because of its important role in restoring panicle fertility, many studies have been


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conducted to determine the location of the S5n gene. A fine mapping of the S5n gene to an interval of 40 kb on chromosome 6 was reported independently (Ji et al. 2005; Qiu et al. 2005). Also, a number of loci causing hybrid male sterility, such as, Sa, S-b, S-c, S-d, S-e and S-f, f5-Du were detected, and some of them (S-a, S-b, S-c, f5-Du) have been mapped (Zhuang et al. 1999; Yang et al. 2004a; Li et al. 2006b, Wang et al. 2006a). Genetic map and QTL mapping Most rice agronomic traits are quantitative in nature and are controlled by polygenes or minor genes or quantitative traits loci (QTL). QTL also show Mendelian inheritance, but are greatly influenced by environments. The availability of comprehensive molecular maps in rice has opened new avenues to map such QTL with molecular markers. In China, several research groups constructed rice genetic maps to detect QTL using different mapping populations, such as Zaiyeqing8/Jingxi17 DH lines,

Zhenshan97/Minghui63 RI lines and Zhenshan97/Mingyang46 RI lines (Zhu et al. 1993; and Xing et al. 2002; Zhuang et al. 2002). Some QTLs have been mapped with molecular markers including yield, quality and resistance QTLs, and two of them, SKC1 and GS3, have been cloned. SKC1 is the first QTL cloned by Chinese scientist Dr Hongxuan Lin, which is involved in regulating K+/Na+ homeostasis under salt-stress (Ren et al. 2005). SKC1 encodes a member of the high affinity K+ transporter (HKT)-type transporters and functions as a Na+-selective transporter. This gene has the potential for improving salt-tolerance in crops. Fan et al. (2006a) cloned the GS3 gene located in the pericentromeric region of rice chromosome 3, which has been frequently identified as a major QTL for both grain weight (a yield trait) and grain length (a quality trait). GS3 consists of five exons and encodes 232 amino acids with a putative PEBP (phosphatidylethanolamine-binding protein)-like domain, a transmembrane region, a putative TNFR (tumor necrosis factor

Figure 2. The genomic position of genes mentioned in this review. Gene symbols can be found in the references. The schematic chromosomes in the background are from the International Rice Genome Sequencing Project (2005).


receptor)/NGFR (nerve growth factor receptor) family cysteinerich domain and a von Willebrand factor type C (VWFC) module. Three other QTLs, a yield-improving QTL qGY2-1, a grain length QTL Lk-4 (t) and two rolled leaf QTLs, rl(t) and rl8 were fine-mapped (Shao et al. 2005a; Shao et al. 2005b; He et al. 2006a; Zhou et al. 2006). All of these results have led to major advances in markerassisted selection and pyramiding of useful genes. Molecular breeding Molecular breeding can be classified into two types: transformation and marker-assisted selection (MAS) Particle bombardment and Agrobacterium-mediated transformation have greatly facilitated the production of transgenic rice. In China, the first rice transgenic plant was produced by Baojian Li in 1990. Since then, transgenic rice plants have been produced in many laboratories by transferring genes for herbicide, salt, drought-tolerance, and Bt. The first transgenic hybrid rice with a herbicide-tolerance gene was developed and applied in the China National Rice Research Institute (CNRRI). Dr Yaoguang Liu’s laboratory developed a multi-gene assembly and transformation vector system, and used this system to introduce as many as 10 transgenes into the rice genome (Lin et al. 2003). Molecular markers have facilitated the use of MAS in rice breeding. In MAS, individuals carrying target genes are selected in a segregating population based on linked markers rather than on their phenotype. Thus, the population can be screened at any stage of growth and in various environments. MAS, protocols of which were first developed by Zheng et al. (1995), increases the efficiency of a breeding program by selecting for markers linked to target traits or QTLs. As mentioned, several QTLs/genes for resistance to diseases, insects, and high-yielding have been mapped with molecular markers. Cheng et al. (2004a) bred a hybrid rice restorer line R9308 from a three-cross combination: C57 (japonica)/300 Hao (japonica)/IR26 (indica) by MAS with indica/japonica-specific molecular markers, and developed a super hybrid rice variety, Xieyou9308. Many other hybrid rice restorer lines such as R218, R8006, Q611, RB207, 1826, and Minghui63-Xa21 with blight-resistance and high-yielding have also been developed. The Guangdong Provincial Academic of Agricultural Sciences pyramided the Pi-1, Pi-2 and Xa23 genes into the rice varieties GD-7S or W889 by using MAS, and produced the three-gene pyramiding lines. Sichuan University developed multi-gene hybrid rice restorer lines and fertility lines (2301S, 2305S, Paiei64S, Zhuguang612S and Wanghui7058) with the BT, SCK, SBK and GNA genes by using MAS. New gene screening and genetic analysis using

mutants Detailed developmental analyses of mutant phenotypes and spatiotemporal expression patterns of the relative genes contribute greatly to a better understanding of plant architecture (Itoh et al. 2005). To efficiently discover genes essential for rice genetic improvement, scientists in China have focused on developing functional genomics tools and genetic resources (i. e. genome-wide mutant generation, transcript profiling and data mining) in rice. Since the 1980s, more than 100 000 accessions of radiation- and chemical-induced or insertional-caused mutagenesis have been generated (Chen et al. 2003; Zhang et al. 2006b), and much progress has been made on rice molecular genetics. So far at least 16 variant/mutant genes including MOC1, BC1 and GH2 genes have been isolated and characterized (Xue et al. 2003; Guo et al. 2006). These mutants and genes, together with those already available, will serve as an indispensable resource for genetic discovery in rice. In this section, we highlight recent progress made in new gene screenings and their genetic analysis in China. Most of the cloned and finely mapped genes by Chinese scientists are shown in Table 1 and Figure 2. Tillering Tillering in rice is an important agronomic trait for grain production and genetic study. A rice spontaneous mutant monoculm1 (moc1) was discovered by Dr Qian Qian of CNRRI in 1991. The MOC1 gene was cloned by Dr Jiayang Li’s research group in cooperation with our laboratory (Li et al. 2003d). The moc1 mutant plants have only a main culm without any tillers due to a defect in the formation of tiller buds. MOC1 encodes a putative GRAS (GAI, RGA, SCR) family nuclear protein, which is mainly expressed in the axillary buds and functions to initiate axillary buds and to promote their outgrowth. Tang et al. (2001) mapped a FEW-TILLING 1 (FT1) mutant gene on chromosome 2. Jiang et al. (2006a) reported two REDUCED CLUM NUMBER (RCN) genes and mapped the genes RCN8 and RCN9 respectively on the chromosome 1 (119.6 cM) and the chromosome 6 (63.6 cM). Among all tillering mutants, research on dwarf tillering is of great interest. For more details, please check the review written by Wang et al. (2006b). Shi (2006) reported a new gene MT1, on chromosome 1, which is orthologous to MAX4 (MORE AXILLARY GROWTH4)/CCD8. A rice htd-1 mutant, related to tillering and dwarfing, was cloned by Zou et al. (2006). HTD-1 is an orthologous gene of AtMAX3/CCD7. Sui et al. (2006) finely mapped sdt3 on chromosome 11. Jiang et al. (2006b) obtained an excessive tillering mutant and mapped the caused gene ext-M1B (t) on chromosome 6. Mutants and genes of reproductive organs The studies on molecular genetics of floral development have become of great significance since the 1990s. The acquisition


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Table 1. Rice genes cloned or finely mapped by Chinese scientists Gene symbol

Character Gene name

of inheritance

Chrom-

Candidate

osome

region a

Candidate gene/enco ded protein

Putative function b

Reference

sd-g

SEMI-DWARF-G

Recessive

5

85 kb

sd-t (t)

SEMI-DWARF-T

Recessive

4

147 kb

Jiang et al. 2002

sdt2

SEMI-DWARF TILLERING

Recessive

4

0.05 cM

Zhao et al. 2005

sdt3

SEMI DWARF TILLERING

Recessive

11

93 kb

HTD1

HIGH TILLERING AND

Recessive

4

30 kb

DWARF1

Liang et al. 2004

Sui et al. 2006 Orthologous

Negative

of AtMAX3/

regulation of

CCD7

the outgrowth

Zou et al. 2006

of axillary buds MT1

MULTIPLE TILLERS 1

Recessive

1

30 kb

Orthologous

Shi et al. 2006

of AtMAX4/ CCD8 EUI1

ELONGATED UPPERMOST Recessive

5

30 kb

INTERNODE 1 EUI2

ELONGATED UPPERMOST Recessive

10

41.7 kb

INTERNODE 2 S5n

HYBRID STERILITY/C

Cytochrome

Has an important

P450 mono-

role in gibberellin Zhu et al. 2006

Luo et al. 2006a;

oxygenase

biosynthesis

Epoxide

Peng 2005; Zhu 2005;

hydrolase

Wei 2006b

6

40 kb

Qiu et al. 2005; Ji et al. 2005

5

27 kb

Li et al. 2006

3

46 kb

Yang et al. 2004a

10

110 kb

OMPATIBILITY S-b

HYBRID STERILITY/ COMPATIBILITY

S-c

HYBRID STERILITY/ COMPATIBILITY

Rf1 c

FERTILITY RESTORING 1

Dominant

PPR proteins mRNA silencing RF1A and

by cleavage and

RF1B

degradation,

Wang et al. 2006d

respectively Rf-6 (t)

FERTILITY RESTORING-6 (T) Dominant

10

105 kb

Liu et al. 2004b

f5-Du

HYBRID STERILITY/

Dominant

5

70 kb

Wang et al. 2006a

PMS1

PHOTOPERIOD-SENSTITIVE Recessive

7

85 kb

Liu et al. 2001

12

28.4 kb

Lu et al. 2005

2

19 kb

COMPATIBILITY MALE STERILITY 1 PMS3

PHOTOPERIOD-SENSTITIVE Recessive MALE STERILITY 3

TMS5

THERMOSENSITIVE GENIC Recessive MALE STERILE

NAC (NAMATAF-

Yang et al. 2006

CUC-related) gene family

TDR

TAPETUM DEGENERATION Recessive

2

113 kb

RETARDATION

Encodes a

Required for

Li et al. 2006a

putative basic tapetum helix-loophelix degradation protein

and anther development

xa13

RESISTANCE OF xanthomo Recessive

8

9.2 kb

nus oryzae pv. oryzae 13

Involved in

Chu et al. 2006b

rice bacterial blight disease resistance and pollen development

Xa2

RESISTANCE OF xanthomonus Dominant oryzae pv. oryzae 2

4

190 kb

He et al. 2006b


Table 1. (continued) Gene symbol Xa26

Character Gene name

of inheri-

Chrom-

Candidate

osome

region a

tance RESISTANCE OF

Dominant

11

20 kb

xanthomonus oryzae pv. oryzae 26 Xa4

RESISTANCE OF


Putative function b

LRR receptor Involved in rice kinase-like

bacterial blight

protein

disease resistance

Reference Sun et al. 2004a

Dominant

11

47 kb

Sun et al. 2004a

Dominant

8

17.0 kb

Liu et al. 2005d

Dominant

1

60 kb

Chen et al. 2005

Dominant

6

180 kb

xanthomonus oryzae pv. oryzae 4 Pi-36 (t)

RESISTANCE OF pyricularia oryzae-36(t)

Pi-37 (t)

RESISTANCE OF pyricularia oryzae-37(t)

Pi-d2

RESISTANCE OF pyricularia oryzae-d2

Pigm (t)

RESISTANCE OF

B-lectin rece

The gene for rice

ptor kinase

blast resistance

Chen et al. 2006c

Dominant

6

70 kb

Deng et al. 2006

BROWN PLANTHOPPER 15 Recessive

4

47.0 kb

Yang et al. 2004b

BPH19 (t) BROWN PLANTHOPPER 19 (t) Recessive

3

60 kb

1

7.4 kb

pyricularia oryzae gm (t) BPH15 SKC

SHOOT K+ CONCENT 1

Chen et al. 2006a A member of

Maintain K + hom-

HKT-type

eostasis in the salt-

transporter

tolerant variety

Ren et al. 2005

under salt stress GS3

GRAIN SIZE 3

3

7.9 kb

Transmebrane Control grain size

Fan et al. 2006a

protein q-GY2-1 RL (t)

ROLLING LEAF (t)

RL8

ROLLING LEAF 8

Incomplete

2

102.9 kb

He et al. 2006

2

137 kb

Shao et al. 2005b

5

542 kb

Shao et al. 2005a

6

20 kb

recessive Incomplete recessive MOC1

MONO CULM 1

Recessive

A putative

Functions to initiate Li et al. 2003d

GRAS family axillary buds and to

ALK

ALKALI DEGENERATION

Recessive

6

9.1kb

GENE

nuclear

promote their

protein

outgrowth

Soluble starch Controls the synthase II

Gao et al. 2003

gelatinization temperature

FGR

FRAGRANCE

Recessive

8

69 kb

Chen et al. 2006b

CL

CLUSTERED SPIKELETS

Dominant

6

196 kb

Zheng et al. 2003

FON4

FLORAL ORGAN NUMBER Recessive

11

600 kb

Ortholog of the Involved in Arabidopsis

Chu et al. 2006a

flower

clavata3 gene development (clv3) PS

PISTILLOID-STAMEN

Recessive

1

20 kb

Single C2H2

Luo et al. 2006b

zinc-finger domain containing protein PS-4

PURPLE STIGMA-4

Recessive

6

0.88 cM

Han et al. 2006

PSE (T)

PREMATURE

Recessive

7

220 kb

Li et al. 2005

SENECENCE (t)


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Table 1. (continued) Gene symbol RL9 (t)

Character Gene name

of inheritance

Rolling leaf 9 (t)

Recessive

Chrom-

Candidate

osome

region a

9

42 kb


Putative function b

MYB domain

Reference Yan et al. 2006

containing protein OsALB23 Oryza sativa ALBINO 23

Recessive

2

280 kb

Kong et al. 2006

LA

LAZY RICE

Recessive

11

0.4 cM

Li et al. 2003b

LLA

LARGE LEAF ANGER

ARL1

ADVENTITIOUS

1 Recessive

3

Oswrky11 10 kb

ROOTLESS

Wang et al. 2005

Lob-domain

Related in adven- Liu et al. 2005a

protein

titious root

Encodes a

Synthesize coniferyl Zhang et al. 2006c

cinnamyl-

and sinapyl alcohol

alcohol

precursors in rice

fromation GH2

GOLD HULL AND

Recessive

2

30 kb

INTERNODE 2

dehydrogenase lignin biosynthesis BEL

BENTAZON SENSITIVE

Recessive

3

92 kb

LETHALITY

Cytochrome

Confer rice bentazon Pan 2006

P450 hydrox- resistance ylase gene

BC1 a

BRITTLE CULM 1

Recessive

3

3.3 kb

COBRA-like

Related in the biosyn- Li et al. 2003e

protein

thesis of the cell walls

The candidate region refers to the reported minimum interval of the cloned or fine-mapped gene. bOnly the cloned genes have descriptions

in this row. cRf1 refers to two separated loci. For details please see Wang et al. (2006). GRAS (GAI, RGA, SCR); HKT, high affinity K + transporter; LRR, leucine-rich repest; MYB, myeloblastosis; NAC, NAM-ATAFCUC-related; PPR, pentatricopeptide repeat.

and research on the rice mutants related to reproductive development play an important role in uncovering the function and interaction of genes in reproductive processes, and their application in rice breeding. A rice floral organ mutant, termed pistilloid-stamen (ps) with degenerated lemma and palea was isolated (Luo et al. 2006b). The PS gene encodes a protein with a single C2H2 zinc-finger domain. Chu et al. (2006a) cloned a FLORAL-ORGAN-NUMBER 4 (FON4) mutant gene, encoding a small putative secreted protein, a putative ortholog of the Arabidopsis CLAVATA3 (CLV3) gene. Other six flower-organ mutant genes (PS-4, OsLH, SRS-1, NPA1, CL and WP [t]) have been fine-mapped (Bai et al. 2000; Luo et al. 2002; Zheng et al. 2003; Li et al. 2003a; Chu et al. 2005; Han et al. 2006) Genes related to rice quality Until now, only one gene related to rice quality has been cloned by Chinese scientists. Besides amylose content (AC), gelatinization temperature (GT) is another important parameter for evaluating the cooking and eating quality of rice. The inheritance of the genes affecting GT has been widely studied and is considered to be controlled by the major gene ALK, encoding the soluble starch synthase II (SSSII). This gene was finally mapped on chromosome 6 and delimited to a 9.1-kb DNA

fragment (Gao et al. 2003). Comparison between the DNA sequences from different rice varieties, together with the results obtained with digestion of the rice seeds in alkali solution, indicated that the base substitutions in the coding sequence of ALK may cause the alteration in GT. Chen et al. (2006b) reported that a single recessive gene (FGR) on chromosome 8 is responsible for the production of 2acetyl-1-pyrroline (2AP), which stands out as the main compound among a total of 114 different volatile compounds detected in rice fragrance. Leaf morphology A total of five leaf mutant genes have been fine-mapped in China. Yan et al. (2006) isolated a recessive rolling leaf gene (RL9 (t)) on chromosome 9, encoding a MYB-domain containing protein. A rice T-DNA-inserted mutant, pse (t) (premature senescence, tentatively), was isolated on chromosome 7 by Li et al. (2005). A rice initiation-type lesion mimic mutant (lmi) was identified (Liu et al. 2003), which was isolated from an indica rice Zhongxian 3037 through γ radiation mutagenesis. The LMI locus is mapped to the short arm of chromosome 8, near the centromere. Kong et al. (2006) reported that rice albino mutant Osalb23 without thylakoid inside the chloroplast was finemapped on chromosome 2.


Plant architecture Tiller angle of rice is an important agronomic trait that contributes to breeding new varieties with ideal architectures. Li et al. (2003b) reported mapping and characterization of a rice mutant defective in tiller angle (la). The LA gene was controlled by a single gene and located within a 0.4 cM interval on chromosome 11. Wang et al. (2005a) isolated a large leaf angle (lla) mutant T429 from T1 transgenic lines. The flanking sequence was used in a BLAST (Basic Local Alignment Search Tool) search of the National Center for Biotechnology Information (NCBI) database. The results showed that the flanking sequence was highly homologous to two overlapping PAC clones, AC002744 and AP002839, in rice chromosome 1. This locus has three putative mRNAs: WRKY16, WRKY11and WRKY2, designated lla mutant gene OsWRKY11. Other mutants A completely dominant gene temporarily named Mi3 (t) exhibiting a phenotype of minute grain, was located between RM282 (5.1 cM) and RM6283 (0.9 cM) on the short arm of chromosome 3 (Liu et al. 2005c). Lignin content and composition are two important agronomic traits for the use of agricultural residues. Rice gold hull and internode phenotype is a classical morphological marker trait that has long been applied to breeding and genetics studies. Zhang et al. (2006c) cloned the GOLD HULL AND INTERNODE 2 (GH2) gene in rice using a lignin-deficient mutant, and GH2 encodes a cinnamyl-alcohol dehydrogenase (CAD). Liu et al. (2005a) isolated a novel gene controlling the initiation of adventitious root primordia in rice. The gene, designated ADVENTITIOUS ROOTLESS1 (ARL1), encodes a protein with a LATERAL ORGAN BOUNDARIES (LOB) domain. The BEL gene, which is sensitive to bentazon was located on chromosome 3 within the region of 92 kb between two SNP makers (SNP158 and SNP138) and is a cytochrome P450 hydroxylase gene (Pan 2006). Plant mechanical strength is another important agronomic trait. A classic rice mutant, brittle culm1 (bc1), was isolated using a map-based cloning approach (Li et al. 2003e). BC1, encoding a COBRA-like protein, is expressed mainly in developing sclerenchyma cells and in vascular bundles of rice. The mutations in BC1 cause not only a reduction in cell wall thickness and cellulose content, but also an increase at lignin levels, suggesting that BC1, a gene that controls the mechanical strength of monocots, plays an important role in the biosynthesis of the cell walls of mechanical tissues.

Prospect The complete sequencing of the rice genome has greatly facilitated the isolation and characterization of genes for agronomic

significance, and the discovery of elite rice resources and functional genes will further enhance rice genetic improvement. The research should focus on integration of the genetic resources, functional genomics and molecular design breeding for the future. Integration of genetic resources Since the 1980s, radiation and chemical mutagens have been used to generate artificial rice mutants, and with the breakthrough in molecular technology, scientists have gradually shifted their attention to the identification of genes that regulate rice morphogenesis or physiological traits, and the dissection of molecular mechanisms of related genes from different rice mutants/germplasms. Morphological mutants play an indispensable role in the study of rice development. Up to now, about 1 698 kinds of rice mutants have been reported (Kurata et al. 2005; Guo et al. 2006). Nowadays there are four major mutant libraries supported by a website in China. These are: RiceData created by CNRRI (http://www.ricedata.cn); RMD (Rice Mutant Database) maintained by Huazhong Agricultural University (Zhang et al. 2006b) (http://rmd.ncpgr.cn); SHIP (Shanghai TDNA Insertion Population) established at SIPPE (Shanghai Institute of Plant Physiology and Ecology) (http://ship.plantsignal. cn/index.do); and TRIM (Taiwan of Ching Rice Insertional Mutants Database) by ASPGC (Academia Sinica Plant Genome Center) (http://trim.sinica.edu.tw). These rice mutants are greatly beneficial to the identification of functional genes of key agronomic traits, and rice molecular breeding. With such a large increasing number of rice mutants, systemically classifying, exchanging and sharing them to better serve studies on functional genomics has become a challenging problem. The integration of rice genetic recourses/mutants is essential, so it is necessary to establish an organization for the integration of all kinds of rice mutants in China, which will further promote the efficient use of rice mutants and genetics development. Construction of a website for rice genetics To facilitate communication and scientific research, we need a website for rice genetics of our own just like the “Oryzabase” created by the National Institute of Genetics of Japan. With the development of bioinformatics, many studies of genetics should be carried out with the assistance of websites. To date, there are a large number of bioinformatics-related websites; however, many of them are too complex to be conveniently used by Chinese scientists. A website is also a platform to release all kinds of relevant information systematically classified and reorganized about rice genetics and functional genomics (and provide information associated with germplasms) to be facilitated by researchers. There are many available


Vol. 49 No. 6 2007

bioinformatics resources (Shen et al. 2004; Zhao et al. 2004; Gao et al. 2006; Ye et al. 2006; Zeng et al. 2006) and mutant libraries in which the websites listed above could be collected or integrated. In addition, this professional website should also include all of the relevant information about the development, physiology and breeding of rice. Of course, it will not be easy to construct a website that can provide all kinds of specialized knowledge; however, with the assistance of all institutes involved in rice research in China, it would be worth starting now.

lar design breeding will be the most effective and prospective breeding method in rice. This is the beginning of a new era, an era of molecular genetics, and an era of functional genomics. And we stand here, in the shoulder of the giant, we can expect more and we should expect more. In years past, especially in the recent 5 years, with the development of the modern technology of molecular biology, Chinese scientists are gradually catching up. We can expect a brighter future, not only for rice genetics, but also for plant genetics.

Functional genomics

Update

As shown in this review, many genes revealed by mutants have been accumulated. To date, there exist 16 genes that have been cloned by Chinese scientists, and many genes have been fine-mapped (Table 1). It is expected that in the next decade, the number of rice functional genes to be isolated and characterized will increase greatly. However, most of these reports have so far only focused on gene isolation. The studies on gene function and physiological pathways are still less involved; therefore, this will be a major task in the coming era of functional genomics. From the viewpoint of functional genomics, individual gene characterization is not enough to achieve such kinds of studies, but systematic work using genomic and bioinformatics approaches is required. The collection and positioning of many pieces of relevant genes will decipher the multi-gene networks and thus, determine the morphological and developmental regulations for those gene networks. As a model species, progress in rice functional genomics will ultimately attribute to the better understanding of plant development of monocotyledons.

Recent work demonstrated that GW2, a QTL for rice grain width and weight, encodes a previously unknown RING-type E3 ubiquitin ligase which negatively regulates cell division by targeting its substrate (s) to proteasomes for regulated proteolysis (Song et al. 2007).

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(Handling editor: Yong-Biao Xue)