Expression dynamics of metabolic and regulatory components across stages of panicle and seed development in indica rice
Carefully analyzed expression profiles can serve as a valuable reference for deciphering gene functions. We exploited the potential of whole genome microarrays to measure the spatial and temporal expression profiles of rice genes in 19 stages of vegetative and reproductive development. We could verify expression of 22,980 genes in at least one of the tissues. Differential expression analysis with respect to five vegetative tissues and preceding stages of development revealed reproductive stage-preferential/-specific genes. By using subtractive logic, we identified 354 and 456 genes expressing specifically during panicle and seed development, respectively. The metabolic/hormonal pathways and transcription factor families playing key role in reproductive development were elucidated after overlaying the expression data on the public databases and manually curated list of transcription factors, respectively. During floral meristem differentiation (P1) and male meiosis (P3), the genes involved in jasmonic acid and phenylpropanoid biosynthesis were significantly upregulated. P6 stage of panicle, containing mature gametophytes, exhibited enrichment of transcripts involved in homogalacturonon degradation. Genes regulating auxin biosynthesis were induced during early seed development. We validated the stage-specificity of regulatory regions of three panicle-specific genes, OsAGO3, OsSub42, and RTS, and an early seed-specific gene, XYH, in transgenic rice. The data generated here provides a snapshot of the underlying complexity of the gene networks regulating rice reproductive development.
KeywordsDevelopment Expression Meta-analysis Metabolic pathways Panicle Promoter Seed Transcription factors
This work was supported by Department of Biotechnology, Ministry of Science & Technology, Government of India (Project No. BT/AB/FG-I(PH-II)(4)/2009). We acknowledge Dr. Ramesh Hariharan and his team at Strand LS Bengaluru, India for their help in microarray data analysis and Ms. Manupriya for providing the list of transcription factor family genes in rice. Senior Research fellowship by the Council for Scientific and Industrial Research (CSIR) to R.S., S.R., P.D, M.J., A.N., and P.S. and University Grants Commissions (UGC) fellowship to P.A. are acknowledged.
Microarray data used in this study have been deposited in the Gene Expression Omnibus database at the National Center for Biotechnology Information under the accession nos. GSE6893 and GSE6901. All the datasets shortlisted in this manuscript including list of panicle or seed-specific genes, differentially expressed genes during panicle or seed development with respect to all four vegetative stages and unique genes upregulated with respect to preceding stage of development are given in Supplementary Table S3.
- Adams (2008) Transcriptome: connecting the genome to gene function. Nature Education 1Google Scholar
- Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate-a practical and powerful approach to multiple testing. J R Stat Soc Ser B 57:289–300Google Scholar
- Endo M, Matsubara H, Kokubun T, Masuko H, Takahata Y, Tsuchiya T, Fukuda H, Demura T, Watanabe M (2002) The advantages of cDNA microarray as an effective tool for identification of reproductive organ-specific genes in a model legume, Lotus japonicus. FEBS Lett 514:229–237PubMedCrossRefGoogle Scholar
- Endo M, Tsuchiya T, Saito H, Matsubara H, Hakozaki H, Masuko H, Kamada M, Higashitani A, Takahashi H, Fukuda H, Demura T, Watanabe M (2004) Identification and molecular characterization of novel anther-specific genes in Oryza sativa L. by using cDNA microarray. Genes Genet Syst 79:213–226PubMedCrossRefGoogle Scholar
- Hobo T, Suwabe K, Aya K, Suzuki G, Yano K, Ishimizu T, Fujita M, Kikuchi S, Hamada K, Miyano M, Fujioka T, Kaneko F, Kazama T, Mizuta Y, Takahashi H, Shiono K, Nakazono M, Tsutsumi N, Nagamura Y, Kurata N, Watanabe M, Matsuoka M (2008) Various spatiotemporal expression profiles of anther-expressed genes in rice. Plant Cell Physiol 49:1417–1428PubMedCrossRefGoogle Scholar
- Howell KA, Narsai R, Carroll A, Ivanova A, Lohse M, Usadel B, Millar AH, Whelan J (2009) Mapping metabolic and transcript temporal switches during germination in rice highlights specific transcription factors and the role of RNA instability in the germination process. Plant Physiol 149:961–980PubMedCrossRefGoogle Scholar
- Jain M, Nijhawan A, Arora R, Agarwal P, Ray S, Sharma P, Kapoor S, Tyagi AK, Khurana JP (2007) F-box proteins in rice. Genome-wide analysis, classification, temporal and spatial gene expression during panicle and seed development, and regulation by light and abiotic stress. Plant Physiol 143:1467–1483PubMedCrossRefGoogle Scholar
- Jaiswal P, Ni J, Yap I, Ware D, Spooner W, Youens-Clark K, Ren L, Liang C, Zhao W, Ratnapu K, Faga B, Canaran P, Fogleman M, Hebbard C, Avraham S, Schmidt S, Casstevens TM, Buckler ES, Stein L, McCouch S (2006) Gramene: a bird’s eye view of cereal genomes. Nucleic Acids Res 34:D717–D723PubMedCrossRefGoogle Scholar
- Laitinen RA, Immanen J, Auvinen P, Rudd S, Alatalo E, Paulin L, Ainasoja M, Kotilainen M, Koskela S, Teeri TH, Elomaa P (2005) Analysis of the floral transcriptome uncovers new regulators of organ determination and gene families related to flower organ differentiation in Gerbera hybrida (Asteraceae). Genome Res 15:475–486PubMedCrossRefGoogle Scholar
- Lan L, Chen W, Lai Y, Suo J, Kong Z, Li C, Lu Y, Zhang Y, Zhao X, Zhang X, Han B, Cheng J, Xue Y (2004) Monitoring of gene expression profiles and isolation of candidate genes involved in pollination and fertilization in rice (Oryza sativa L.) with a 10 K cDNA microarray. Plant Mol Biol 54:471–487PubMedCrossRefGoogle Scholar
- Luo H, Lee JY, Hu Q, Nelson-Vasilchik K, Eitas TK, Lickwar C, Kausch AP, Chandlee JM, Hodges TK (2006) RTS, a rice anther-specific gene is required for male fertility and its promoter sequence directs tissue-specific gene expression in different plant species. Plant Mol Biol 62:397–408PubMedCrossRefGoogle Scholar
- Sato Y, Antonio B, Namiki N, Motoyama R, Sugimoto K, Takehisa H, Minami H, Kamatsuki K, Kusaba M, Hirochika H, Nagamura Y (2011) Field transcriptome revealed critical developmental and physiological transitions involved in the expression of growth potential in japonica rice. BMC Plant Biol 11:10PubMedCrossRefGoogle Scholar
- Sharma R, Kapoor M, Tyagi AK, Kapoor S (2010) Comparative transcript profiling of TCP family genes provide insight into gene functions and diversification in rice and Arabidopsis. J Plant Mol Biol Biotechnol 1:24–38Google Scholar
- Suwabe K, Suzuki G, Takahashi H, Shiono K, Endo M, Yano K, Fujita M, Masuko H, Saito H, Fujioka T, Kaneko F, Kazama T, Mizuta Y, Kawagishi-Kobayashi M, Tsutsumi N, Kurata N, Nakazono M, Watanabe M (2008) Separated transcriptomes of male gametophyte and tapetum in rice: validity of a laser microdissection (LM) microarray. Plant Cell Physiol 49:1407–1416PubMedCrossRefGoogle Scholar
- Wu Z, Irizarry RA, Gentleman R, Murillo FM, Spencer F (2003) A model based background adjustment for oligonucleotide expression arrays. Technical Report, Department of Biostatistics. Working Papers, Baltimore, MD.Google Scholar