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Update on Rice Mutant Resources

Mutant Resources in Rice for Functional Genomics of the Grasses^[W]

Virginia Bioinformatics Institute, Virginia Tech, Blacksburg, Virginia 24061 (A.K., A.P.); Centre de Cooperation Internationale en Recherche Agronomique pour le Développement, 34398 Montpellier cedex 5, France (E.G.); Department of Life Science and National Research Laboratory of Plant Functional Genomics, Pohang University of Science and Technology, Pohang 790–784, South Korea (G.A.); Institute of Plant and Microbial Biology (Y.-i.C.H.) and Institute of Molecular Biology (S.-M.Y.), Academia Sinica, Nankang, Taipei 11529, Taiwan; Division of Applied Life Sciences (BK21), Plant Molecular Biology and Biotechnology Research Center, Gyeongsang National University, Jinju 660–701, South Korea (C.-d.H.); Rice Functional Genomics, National Institute of Agricultural Biotechnology, Rural Development Administration, Suwon 441–707, South Korea (M.C.L.); CSIRO Plant Industry, Canberra, Australian Capital Territory 2601, Australia (N.U.); Temasek Life Sciences Laboratory, National University of Singapore, Singapore 117604, Singapore (S.R.); National Key Laboratory of Crop Genetic Improvement, Huazhong Agricultural University, Wuhan 430070, China (Q.Z.); Plant Biology and Agronomy, University of California, Davis, California 95616 (V.S.); Division of Genome and Biodiversity Research, Genetics Department, National Institute of Agrobiological Sciences, Tsukuba City, Ibaraki 305–8602, Japan (H.H.); and International Rice Research Institute, Metro Manila, Philippines (H.L.)

Rice (Oryza sativa) is the reference genome for the grasses, including cereals. The complete genome sequence lays the foundation for comparative genomics to the other grasses based on genome structure and individual gene function (Devos, 2005; International Rice Genome Sequencing Project, 2005). The basic complement of monocot genes in rice can be examined by functional genomics studies because of the many advantages of rice as a system for genetic analysis, as well as the worldwide development of resources.

The analysis of mutants by forward and reverse genetics approaches is an effective way to study gene function. Knockout (KO) mutations, which abolish gene expression and display a phenotype, provide a direct causal relationship between the gene sequence and its biological function. However, not all gene mutations display a KO mutant phenotype, primarily due to gene redundancy, because plant genomes have been shown to have large segmental genomic duplications, as well as tandem duplications of gene families (Yu et al., 2005; Sterck et al., 2007). In many cases, the redundancy is partial or unequal, due to overlap in expression of duplicated genes (Briggs et al., 2006), or the gene activity is required only under some specific conditions, such as biotic/abiotic stresses where the mutant phenotype can be observed.

The use of molecular tags or DNA insertions, such as transposons or T-DNA, is favored for mutations because their genome positions can be easily monitored to determine the correlations between tagged genes and phenotypes. The limitations in identifying gene functions by KO mutations alone are resolved by employing heterologous DNA insertions with engineered properties to monitor the expression of tagged genes using entrapment vectors or to alter the expression of tagged genes using activation tagging (Pereira, 2000).

The International Rice Functional Genomics Consortium, combined with many national programs, set a goal to generate mutant resources toward discovering the function of all rice genes, primarily through reverse genetics approaches (Hirochika et al., 2004). This resource update describes the generation of over 200,000 insertion flanking sequence tags (FSTs), which tag two-thirds of the predicted protein-coding genes, with one-half of the protein-coding genes estimated to have knockout mutations. The insertion sequences comprise the endogenous Tos17 retrotransposon showing the highest insertion rate in exons, as well as engineered maize (Zea mays) Ds/dSpm transposons and Agrobacterium T-DNA, which function as enhancer trap (ET), gene trap (GT), or activation tags (ATs). In addition, chemical and physical mutagen-derived mutant populations have been developed that are available for TILLING and other high-throughput screens. The extensive number and variety of mutant resources described here for rice are very amenable for dissecting the functions of genes of interest in other grasses.

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Insertion Mutants

With the sequencing of plant genomes, it was recognized that insertion mutants indexed by their position in the genome would be very suitable for systematic analysis of annotated genes by reverse genetics (Parinov and Sundaresan, 2000). Arabidopsis (Arabidopsis thaliana) genome sequence-indexed mutants can now be found in databases (http://signal.salk.edu/Source/AtTOME_Data_Source.html), which comprise a total of 379,674 inserts tagging 30,280 of the predicted 33,003 genes.

In rice, the two-component maize transposon Ac-Ds (Chin et al., 1999; Upadhyaya et al., 2002; Greco et al., 2003; Kolesnik et al., 2004) and En/Spm-dSpm (Greco et al., 2004; Kumar et al., 2008) systems have been well characterized, and good genetic selection schemes have been developed to select for transpositional activity useful for large-scale mutagenesis (Hirochika et al., 2004; Zhu et al., 2007). In addition, the endogenous rice Tos17 retrotransposon is active in specific genotypes and conditions and is an effective insertion mutagen in the rice genome (Miyao et al., 2003). The development of efficient protocols for rice transformation has helped in the generation of a large number of transgenic rice plants bearing low-copy T-DNA insertions (Jeon et al., 2000; Sallaud et al., 2003).

In addition to KO or loss-of-function mutagenesis, the engineering of transposon and T-DNA constructs offers immense flexibility in fashioning the insertion sequences to detect adjacent gene expression or activate the expression of adjacent genes by activation tagging, resulting in gain-of-function mutations. These modified insertions can contribute to gene function discovery of redundant genes and those having lethal mutant effects.

Gene Entrapment
To facilitate the analysis of genes based on their expression patterns, GT and ET constructs have been designed that carry a reporter gene and can display the expression pattern of an adjacent trapped gene (Sundaresan et al., 1995). The reporter gene pattern in ET inserts reflects the adjacent plant gene enhancer activity, and in GT inserts the adjacent gene promoter activity. ET and GT constructs have been used in both T-DNA and Ac-Ds transposons in rice, yielding interesting gene expression patterns and entrapped genes, which support their widespread generation and use for complementing KO mutagenesis (Hirochika et al., 2004; An et al., 2005).

Activation Tagging
T-DNA AT populations have been developed using vectors with cauliflower mosaic virus 35S enhancer multimers, the inserts characterized by FSTs and phenomic data for forward and reverse genetics screens (Jeong et al., 2002; Chern et al., 2007; Hsing et al., 2007; Wan et al., 2009). Recently, an Ac-Ds AT system has also been developed (Qu et al., 2008) using convenient markers for selection of multiple transposants from a few starter transformed lines. In both these AT systems, activation of adjacent genes is observed, albeit 52.7% of the T-DNA lines and 20.8% of the Ds tags activate adjacent genes, which can be as far away as 10 kb from the AT enhancer.

Chemical and Physical Mutagenesis

Chemical agents, such as ethyl methanesulfonate (EMS), methyl nitrosourea, and diepoxybutane, or physical methods like fast-neutron, -rays, and ion beam irradiation can cause a high density of mutations that can saturate the genome (Hirochika et al., 2004). Mutant populations have been generated in rice in which the point mutations can be screened by TILLING and larger deletions by PCR-based screens (Wu et al., 2005; Till et al., 2007). The IR64 (Wu et al., 2005) and the Nipponbare (Till et al., 2007) populations, as well as other unpublished populations also shown in Table I , offer different backgrounds and mutation spectrum. The IR64 mutant collection comprises a total of 66,891 mutant lines in the M4 generation. Of these, about 15,000 are -ray-induced mutants, each carrying 30 to 40 deletions per genome, thus contributing to a conservative estimate of over 500,000 mutations in the collection (H. Leung, unpublished data). Screening for mutations in such populations can be done using genome-wide chips or other high-throughput genotyping technologies. These populations and/or the DNA pools are presently available to screen for specific genes on a small scale.

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The first rice genes identified by insertional mutagenesis were with Tos17 in a forward genetics screen for viviparous mutants (Agrawal et al., 2001), and simultaneously in a reverse genetics screen for inserts in phytochrome A genes (Takano et al., 2001). With T-DNA, genes were identified by forward screens (Jung et al., 2003), by reverse genetics PCR-based screens for mutations in specific genes (Lee et al., 2003), as well as expression-based GT screens (Kang et al., 2005). Likewise, the maize Ac-Ds transposon system also yielded tagged genes (Zhu et al., 2003, 2004).

Because the complete genome sequence became available, the generation of FST information of mutant populations has made the mutants more accessible to address biological questions. Table I shows the different mutant populations available and the FSTs that can be screened for inserts in genes of interest. Such queries can be made in silico, thus providing a convenient way to assess mutant populations around the world. The Ds and dSpm insertions are generated by transposition from a few starter transformed lines that can be scaled up for genome saturation and do not directly result from a regeneration process (Kolesnik et al., 2004; van Enckevort et al., 2005; Upadhyaya et al., 2006; He et al., 2007; Park et al., 2007; Qu et al., 2008). The FST resource of the endogenous Tos17 retrotransposon are generated by regeneration process in Nipponbare (Miyao et al., 2003), which also accompanies Agrobacterium transformation of T-DNA yielding additional Tos17 insertions (Piffanelli et al., 2007). The T-DNA insertions with FSTs in various genetic backgrounds comprise an extensive diverse resource (Chen et al., 2003; Sallaud et al., 2004; Jeong et al., 2006; Zhang et al., 2006; Hsing et al., 2007).

The generation of insertions accompanied by a regeneration phase, such as for T-DNA and Tos17, can result in a high frequency of untagged mutations in the background that can complicate genetic analysis of the mutants (H. Leung and E. Guiderdoni, unpublished data). To alleviate this problem, genetic segregation analysis and the use of multiple mutants of the gene are useful. Transposon inserts have a much lower frequency of background mutations, leading to many genes identified by forward screens (Zhu et al., 2007), and the use of reversions that restore the wild-type phenotype is a convenient approach to prove gene-phenotype relationships.

Resources and Databases for Reverse Genetics

To facilitate the identification of insertion mutations in genes using available FST information, a number of project database Web sites are available as shown in Table I. In addition, functional genomics databases are available, such as RiceGE/SIGnAL (http://signal.salk.edu/cgi-bin/RiceGE), OryGenesDB (http://orygenesdb.cirad.fr), and Gramene (http://www.gramene.org), where the FST information has been collated and mutants can found for inserts in genes of interest. These databases link rice genes to other grass genes and thus direct functional queries to the rice mutant resources.

Properties of Insertion Mutants

We compiled 206,668 insertion FSTs from our contributing groups, which comprise 180,639 unique hits in the genome (Supplemental Table S1). The different insertion types (Tos17, T-DNA, Ds, dSpm) show differences in their specificity, with Tos17 showing the highest proportion of insertions in exons (Fig. 1 ). A remarkably large proportion of all the inserts (62.5%) are in genic regions, including 5' and 3' regions, as described in Figure 1. However, many genes have multiple different insertions, with a total of 32,459 genes containing inserts out of the total 56,985 (56.9%) nuclear genes with assigned locus IDs. Among the 41,753 predicted protein-coding (see Supplemental Materials and Methods S1) rice genes, 28,545 (68.4%) have inserts in the genic region. Assuming that the most probable insertions to produce KO mutations would be those in exons, introns, and the 5'-untranslated region, the insertions were recalculated to be 21,239 (50.8%) in the protein-coding genes (Supplemental Table S1). One of the major reasons for a low frequency of insertions in genes is the actual target size, with around 13,000 genes of 1-kb size showing only around 35% bearing insertions (Supplemental Fig. S1). The insertion mutants found for the rice annotated genes, defined by the GO-slim biological process (10,232 total) and molecular function (12,765) categories (Supplemental Figs. S2 and S3), reveal an even distribution of >90% in total genic region and around 80% in the critical KO mutation target region. This reveals that a high proportion of mutations in annotated genes would most probably cause KO mutants, while the frequencies in the unannotated genes is relatively lower. However, some genes annotated to be involved in pollen-pistil interaction and pollination biological processes have a lower than expected number of mutations in the coding regions (Supplemental Fig. S3).

View larger version (16K): [in this window] [in a new window] [as a PowerPoint slide]   Figure 1. Distribution of insertion positions within genic regions in rice. The three classes of insertion mutagens: endogenous Tos17 retrotransposon, Agrobacterium T-DNA, and maize cut-and-paste transposons (Ds and dSpm), shown with their insertion positions in different parts of genes with color code shown alongside. The numbers of individual insertion types in genes in relation to the total number of insertions are entered below the insertion name. Datasets from the following resources (Table I) were used: Ds, CSIRO, KRDD/GNU, OSTID, UCD; dSpm, UCD; T-DNA, CIRAD, POSTECH, RMD, SHIP, TRIM, ZJU; Tos17, CIRAD and NIAS. 500-bp upstream and downstream regions correspond to sequences upstream and downstream of the transcription unit (start site to site of termination). See Supplemental Table S1 for more information.

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Supplemental Data

The following materials are available in the online version of this article.

Supplemental Figure S1. Gene size and distribution of insertion mutations.

Supplemental Figure S2. GO-slim molecular function categories of all tagged genes.

Supplemental Figure S3. GO-slim biological process categories of all tagged genes.

Supplemental Table S1. Genomic distribution and statistics of rice inserts.

Supplemental Materials and Methods S1. Datasets and analysis.

Received September 1, 2008; accepted November 4, 2008; published January 7, 2009.

	FOOTNOTES

 
The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantphysiol.org) is: Andy Pereira (pereiraa{at}vbi.vt.edu).

^[W] The online version of this article contains Web-only data.

www.plantphysiol.org/cgi/doi/10.1104/pp.108.128918

^* Corresponding author; e-mail pereiraa{at}vbi.vt.edu.

	LITERATURE CITED

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Agrawal GK, Yamazaki M, Kobayashi M, Hirochika R, Miyao A, Hirochika H (2001) Screening of the rice viviparous mutants generated by endogenous retrotransposon Tos17 insertion. Tagging of a zeaxanthin epoxidase gene and a novel OsTATC gene. Plant Physiol 125: 1248–1257[Abstract/Free Full Text]

An G, Jeong DH, Jung KH, Lee S (2005) Reverse genetic approaches for functional genomics of rice. Plant Mol Biol 59: 111–123[CrossRef][Web of Science][Medline]

Briggs GC, Osmont KS, Shindo C, Sibout R, Hardtke CS (2006) Unequal genetic redundancies in Arabidopsis—a neglected phenomenon? Trends Plant Sci 11: 492–498[CrossRef][Web of Science][Medline]

Chen S, Jin W, Wang M, Zhang F, Zhou J, Jia Q, Wu Y, Liu F, Wu P (2003) Distribution and characterization of over 1000 T-DNA tags in rice genome. Plant J 36: 105–113[CrossRef][Web of Science][Medline]

Chern CG, Fan MJ, Yu SM, Hour AL, Lu PC, Lin YC, Wei FJ, Huang SC, Chen S, Lai MH, et al (2007) A rice phenomics study—phenotype scoring and seed propagation of a T-DNA insertion-induced rice mutant population. Plant Mol Biol 65: 427–438[CrossRef][Web of Science][Medline]

Chin HG, Choe MS, Lee SH, Park SH, Koo JC, Kim NY, Lee JJ, Oh BG, Yi GH, Kim SC, et al (1999) Molecular analysis of rice plants harboring an Ac/Ds transposable element-mediated gene trapping system. Plant J 19: 615–623[CrossRef][Web of Science][Medline]

Devos KM (2005) Updating the ‘crop circle’. Curr Opin Plant Biol 8: 155–162[CrossRef][Web of Science][Medline]

Greco R, Ouwerkerk PB, De Kam RJ, Sallaud C, Favalli C, Colombo L, Guiderdoni E, Meijer AH, Hoge JH, Pereira A (2003) Transpositional behaviour of an Ac/Ds system for reverse genetics in rice. Theor Appl Genet 108: 10–24[CrossRef][Web of Science][Medline]

Greco R, Ouwerkerk PB, Taal AJ, Sallaud C, Guiderdoni E, Meijer AH, Hoge JH, Pereira A (2004) Transcription and somatic transposition of the maize En/Spm transposon system in rice. Mol Genet Genomics 270: 514–523[CrossRef][Web of Science][Medline]

He C, Dey M, Lin Z, Duan F, Li F, Wu R (2007) An efficient method for producing an indexed, insertional-mutant library in rice. Genomics 89: 532–540[CrossRef][Web of Science][Medline]

Hsing YI, Chern CG, Fan MJ, Lu PC, Chen KT, Lo SF, Sun PK, Ho SL, Lee KW, Wang YC, et al (2007) A rice gene activation/knockout mutant resource for high throughput functional genomics. Plant Mol Biol 63: 351–364[CrossRef][Web of Science][Medline]

Hirochika H, Guiderdoni E, An G, Hsing YI, Eun MY, Han CD, Upadhyaya N, Ramachandran S, Zhang Q, Pereira A, et al (2004) Rice mutant resources for gene discovery. Plant Mol Biol 54: 325–334[CrossRef][Web of Science][Medline]

International Rice Genome Sequencing Project (2005) The map-based sequence of the rice genome. Nature 436: 793–800[CrossRef][Medline]

Jeon JS, Lee S, Jung KH, Jun SH, Jeong DH, Lee J, Kim C, Jang S, Yang K, Nam J, et al (2000) T-DNA insertional mutagenesis for functional genomics in rice. Plant J 22: 561–570[CrossRef][Web of Science][Medline]

Jeong DH, An S, Kang HG, Moon S, Han JJ, Park S, Lee HS, An K, An G (2002) T-DNA insertional mutagenesis for activation tagging in rice. Plant Physiol 130: 1636–1644[Abstract/Free Full Text]

Jeong DH, An S, Park S, Kang HG, Park GG, Kim SR, Sim J, Kim YO, Kim MK, Kim SR (2006) Generation of a flanking sequence-tag database for activation-tagging lines in japonica rice. Plant J 45: 123–132[CrossRef][Web of Science][Medline]

Jung KH, Hur J, Ryu CH, Choi Y, Chung YY, Miyao A, Hirochika H, An G (2003) Characterization of a rice chlorophyll-deficient mutant using the T-DNA gene-trap system. Plant Cell Physiol 44: 463–472[Abstract/Free Full Text]

Kang HG, Park S, Matsuoka M, An G (2005) White-core endosperm floury endosperm-4 in rice is generated by knockout mutations in the C-type pyruvate orthophosphate dikinase gene (OsPPDKB). Plant J 42: 901–911[CrossRef][Web of Science][Medline]

Kolesnik T, Szeverenyi I, Bachmann D, Kumar CS, Jiang S, Ramamoorthy R, Cai M, Ma ZG, Sundaresan V, Ramachandran S (2004) Establishing an efficient Ac/Ds tagging system in rice: large-scale analysis of Ds flanking sequences. Plant J 37: 301–314[Web of Science][Medline]

Kumar CS, Wing RA, Sundaresan V (2008) Efficient insertional mutagenesis in rice using the maize En/Spm elements. Plant J 44: 879–892[CrossRef]

Lee S, Kim J, Son JS, Nam J, Jeong DH, Lee K, Jang S, Yoo J, Lee J, Lee DY, et al (2003) Systematic reverse genetic screening of T-DNA tagged genes in rice for functional genomic analyses: MADS-box genes as a test case. Plant Cell Physiol 44: 1403–1411[Abstract/Free Full Text]

Miyao A, Tanaka K, Murata K, Sawaki H, Takeda S, Abe K, Shinozuka Y, Onosato K, Hirochika H (2003) Target site specificity of the Tos17 retrotransposon shows a preference for insertion within genes and against insertion in retrotransposon-rich regions of the genome. Plant Cell 15: 1771–1780[Abstract/Free Full Text]

Parinov S, Sundaresan V (2000) Functional genomics in Arabidopsis: large-scale insertional mutagenesis complements the genome sequencing project. Curr Opin Biotechnol 11: 157–161[CrossRef][Web of Science][Medline]

Park SH, Jun NS, Kim CM, Oh TY, Huang J, Xuan YH, Park SJ, Je BI, Piao HL, Park SH, et al (2007) Analysis of gene-trap Ds rice populations in Korea. Plant Mol Biol 65: 373–384[Medline]

Pereira A (2000) A transgenic perspective on plant functional genomics. Transgenic Res 9: 245–260[CrossRef][Web of Science][Medline]

Piffanelli P, Droc G, Mieulet D, Lanau N, Bès M, Bourgeois E, Rouvière C, Gavory F, Cruaud C, Ghesquière A, et al (2007) Large-scale characterization of Tos17 insertion sites in a rice T-DNA mutant library. Plant Mol Biol 65: 587–601[CrossRef][Web of Science][Medline]

Qu S, Desai A, Wing R, Sundaresan V (2008) A versatile transposon-based activation tag vector system for functional genomics in cereals and other monocot plants. Plant Physiol 146: 189–199[Abstract/Free Full Text]

Sallaud C, Meynard D, van Boxtel J, Gay C, Bès M, Brizard JP, Larmande P, Ortega D, Raynal M, Portefaix M, et al (2003) Highly efficient production and characterization of T-DNA plants for rice (Oryza sativa L.) functional genomics. Theor Appl Genet 106: 1396–1408[Medline]

Sallaud C, Gay C, Larmande P, Bès M, Piffanelli P, Piégu B, Droc G, Regad F, Bourgeois E, Meynard D, et al (2004) High throughput T-DNA insertion mutagenesis in rice: a first step towards in silico reverse genetics. Plant J 39: 450–464[CrossRef][Web of Science][Medline]

Sterck L, Rombauts S, Vandepoele K, Rouzé P, Van de Peer Y (2007) How many genes are there in plants (... and why are they there)? Curr Opin Plant Biol 10: 199–203[CrossRef][Web of Science][Medline]

Sundaresan V, Springer P, Volpe T, Haward S, Jones JD, Dean C, Ma H, Martienssen R (1995) Patterns of gene action in plant development revealed by enhancer trap and gene trap transposable elements. Genes Dev 9: 1797–1810[Abstract/Free Full Text]

Takano M, Kanegae H, Shinomura T, Miyao A, Hirochika H, Furuya M (2001) Isolation and characterization of rice phytochrome A mutants. Plant Cell 13: 521–34[Abstract/Free Full Text]

Till BJ, Cooper J, Tai TH, Colowit P, Greene EA, Henikoff S, Comai L (2007) Discovery of chemically induced mutations in rice by TILLING. BMC Plant Biol 7: 19[CrossRef][Medline]

Upadhyaya NM, Zhou XR, Ramm K, Zhu QH, Wu L, Eamens A, Sivakumar R, Kato T, Yun DW, Kumar S, et al (2002) An iAc/Ds gene and enhancer trapping system for insertional mutagenesis in rice. Funct Plant Biol 29: 547–559[CrossRef][Web of Science]

Upadhyaya NM, Zhu QH, Zhou XR, Eamens AL, Hoque MS, Ramm K, Shivakkumar R, Smith KF, Pan ST, Li S, et al (2006) Dissociation (Ds) constructs, mapped Ds launch pads and a transiently expressed transposase system suitable for localized insertional mutagenesis in rice. Theor Appl Genet 112: 1326–1341[CrossRef][Web of Science][Medline]

van Enckevort LJ, Droc G, Piffanelli P, Greco R, Gagneur C, Weber C, González VM, Cabot P, Fornara F, Berri S (2005) EU-OSTID: a collection of transposon insertional mutants for functional genomics in rice. Plant Mol Biol 59: 99–110[CrossRef][Web of Science][Medline]

Wan S, Wu J, Zhang Z, Sun X, Lv Y, Gao C, Ning Y, Ma J, Guo Y, Zhang Q, et al (2009) Activation tagging, an efficient tool for functional analysis of the rice genome. Plant Mol Biol 69: 69–80[CrossRef][Web of Science][Medline]

Wu JL, Wu C, Lei C, Baraoidan M, Bordeos A, Madamba MR, Ramos-Pamplona M, Mauleon R, Portugal A, Ulat VJ, et al (2005) Chemical- and irradiation-induced mutants of indica rice IR64 for forward and reverse genetics. Plant Mol Biol 59: 85–97[CrossRef][Web of Science][Medline]

Yu J, Wang J, Lin W, Li S, Li H, Zhou J, Ni P, Dong W, Hu S, Zeng C, et al (2005) The genomes of Oryza sativa: a history of duplications. PLoS Biol 3: e38[CrossRef][Medline]

Zhang J, Li C, Wu C, Xiong L, Chen G, Zhang Q, Wang S (2006) RMD: a rice mutant database for functional analysis of the rice genome. Nucleic Acids Res 34: D745–748[Abstract/Free Full Text]

Zhu QH, Hoque MS, Dennis ES, Upadhyaya NM (2003) Ds tagging of BRANCHED FLORETLESS 1 (BFL1) that mediates the transition from spikelet to floret meristem in rice (Oryza sativa L). BMC Plant Biol 3: 6[CrossRef][Medline]

Zhu QH, Ramm K, Shivakkumar R, Dennis ES, Upadhyaya NM (2004) The ANTHER INDEHISCENCE1 gene encoding a single MYB domain protein is involved in anther development in rice (Oryza sativa L.). Plant Physiol 135: 1514–1525[Abstract/Free Full Text]

Zhu QH, Eun MY, Han CD, Kumar CS, Pereira A, Ramachandran S, Sundaresan V, Eamens AL, Upadhyaya NM, Wu R (2007) Transposon insertional mutants: a resource for rice functional genomics. In NM Upadhyaya. ed, Rice Functional Genomics—Challenges, Progress and Prospects. Springer, New York, pp 223–271

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