Skip to main content
Log in

Expression dynamics of metabolic and regulatory components across stages of panicle and seed development in indica rice

  • Original Paper
  • Published:
Functional & Integrative Genomics Aims and scope Submit manuscript

Abstract

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Adams (2008) Transcriptome: connecting the genome to gene function. Nature Education 1

  • Agarwal P, Arora R, Ray S, Singh AK, Singh VP, Takatsuji H, Kapoor S, Tyagi AK (2007) Genome-wide identification of C2H2 zinc-finger gene family in rice and their phylogeny and expression analysis. Plant Mol Biol 65:467–485

    Article  PubMed  CAS  Google Scholar 

  • Agarwal P, Kapoor S, Tyagi AK (2011) Transcription factors regulating the progression of monocot and dicot seed development. Bioessays 33:189–202

    Article  PubMed  CAS  Google Scholar 

  • Agrawal GK, Abe K, Yamazaki M, Miyao A, Hirochika H (2005) Conservation of the E-function for floral organ identity in rice revealed by the analysis of tissue culture-induced loss-of-function mutants of the OsMADS1 gene. Plant Mol Biol 59:125–135

    Article  PubMed  CAS  Google Scholar 

  • Aluru M, Xu Y, Guo R, Wang Z, Li S, White W, Wang K, Rodermel S (2008) Generation of transgenic maize with enhanced provitamin A content. J Exp Bot 59:3551–3562

    Article  PubMed  CAS  Google Scholar 

  • Alves-Ferreira M, Wellmer F, Banhara A, Kumar V, Riechmann JL, Meyerowitz EM (2007) Global expression profiling applied to the analysis of Arabidopsis stamen development. Plant Physiol 145:747–762

    Article  PubMed  CAS  Google Scholar 

  • An H, Roussot C, Suarez-Lopez P, Corbesier L, Vincent C, Pineiro M, Hepworth S, Mouradov A, Justin S, Turnbull C, Coupland G (2004) CONSTANS acts in the phloem to regulate a systemic signal that induces photoperiodic flowering of Arabidopsis. Development 131:3615–3626

    Article  PubMed  CAS  Google Scholar 

  • Arora R, Agarwal P, Ray S, Singh AK, Singh VP, Tyagi AK, Kapoor S (2007) MADS-box gene family in rice: genome-wide identification, organization and expression profiling during reproductive development and stress. BMC Genomics 8:242

    Article  PubMed  CAS  Google Scholar 

  • Baltz R, Domon C, Pillay DT, Steinmetz A (1992) Characterization of a pollen-specific cDNA from sunflower encoding a zinc finger protein. Plant J 2:713–721

    PubMed  CAS  Google Scholar 

  • Becerra C, Puigdomenech P, Vicient CM (2006) Computational and experimental analysis identifies Arabidopsis genes specifically expressed during early seed development. BMC Genomics 7:38

    Article  PubMed  CAS  Google Scholar 

  • Becker JD, Feijo JA (2007) How many genes are needed to make a pollen tube? Lessons from transcriptomics. Ann Bot (Lond) 100:1117–1123

    Article  CAS  Google 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 57:289–300

    Google Scholar 

  • Bhalla PL, Swoboda I, Singh MB (2001) Reduction in allergenicity of grass pollen by genetic engineering. Int Arch Allergy Immunol 124:51–54

    Article  PubMed  CAS  Google Scholar 

  • Cao PJ, Bartley LE, Jung KH, Ronald PC (2008) Construction of a rice glycosyltransferase phylogenomic database and identification of rice-diverged glycosyltransferases. Mol Plant 1:858–877

    Article  PubMed  CAS  Google Scholar 

  • Carninci P (2008) Non-coding RNA transcription: turning on neighbours. Nat Cell Biol 10:1023–1024

    Article  PubMed  CAS  Google Scholar 

  • Chardon F, Damerval C (2005) Phylogenomic analysis of the PEBP gene family in cereals. J Mol Evol 61:579–590

    Article  PubMed  CAS  Google Scholar 

  • Cheng JC, Seeley KA, Goupil P, Sung ZR (1996) Expression of DC8 is associated with, but not dependent on embryogenesis. Plant Mol Biol 31:127–141

    Article  PubMed  CAS  Google Scholar 

  • Chung YY, Kim SR, Finkel D, Yanofsky MF, An G (1994) Early flowering and reduced apical dominance result from ectopic expression of a rice MADS box gene. Plant Mol Biol 26:657–665

    Article  PubMed  CAS  Google Scholar 

  • Chung YY, Kim SR, Kang HG, Noh YS, Park MC, Finkel D, An G (1995) Characterization of two MADS box genes homologous to GLOBOSA. Plant Sci 109:45–56

    Article  CAS  Google Scholar 

  • Clark SE, Williams RW, Meyerowitz EM (1997) The CLAVATA1 gene encodes a putative receptor kinase that controls shoot and floral meristem size in Arabidopsis. Cell 89:575–585

    Article  PubMed  CAS  Google Scholar 

  • Clouse SD, Sasse JM (1998) Brassinosteroids: essential regulators of plant growth and development. Annu Rev Plant Physiol Plant Mol Biol 49:427–451

    Article  PubMed  CAS  Google Scholar 

  • Curtis MD, Grossniklaus U (2003) A gateway cloning vector set for high-throughput functional analysis of genes in planta. Plant Physiol 133:462–469

    Article  PubMed  CAS  Google Scholar 

  • Danilevskaya ON, Hermon P, Hantke S, Muszynski MG, Kollipara K, Ananiev EV (2003) Duplicated fie genes in maize: expression pattern and imprinting suggest distinct functions. Plant Cell 15:425–438

    Article  PubMed  CAS  Google Scholar 

  • Davidson SE, Elliott RC, Helliwell CA, Poole AT, Reid JB (2003) The pea gene NA encodes ent-kaurenoic acid oxidase. Plant Physiol 131:335–344

    Article  PubMed  CAS  Google Scholar 

  • Day RC, Herridge RP, Ambrose BA, Macknight RC (2008) Transcriptome analysis of proliferating Arabidopsis endosperm reveals biological implications for the control of syncytial division, cytokinin signaling, and gene expression regulation. Plant Physiol 148:1964–1984

    Article  PubMed  CAS  Google Scholar 

  • DeLong A, Calderon-Urrea A, Dellaporta SL (1993) Sex determination gene TASSELSEED2 of maize encodes a short-chain alcohol dehydrogenase required for stage-specific floral organ abortion. Cell 74:757–768

    Article  PubMed  CAS  Google Scholar 

  • Deveshwar P, Bovill WD, Sharma R, Able JA, Kapoor S (2011) Analysis of anther transcriptomes to identify genes contributing to meiosis and male gametophyte development in rice. BMC Plant Biol 11:78

    Article  PubMed  CAS  Google Scholar 

  • Ding Z, Doyle MR, Amasino RM, Davis SJ (2007) A complex genetic interaction between Arabidopsis thaliana TOC1 and CCA1/LHY in driving the circadian clock and in output regulation. Genetics 176:1501–1510

    Article  PubMed  CAS  Google Scholar 

  • Drea S, Leader DJ, Arnold BC, Shaw P, Dolan L, Doonan JH (2005) Systematic spatial analysis of gene expression during wheat caryopsis development. Plant Cell 17:2172–2185

    Article  PubMed  CAS  Google Scholar 

  • Ebisuya M, Yamamoto T, Nakajima M, Nishida E (2008) Ripples from neighbouring transcription. Nat Cell Biol 10:1106–1113

    Article  PubMed  CAS  Google 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 514:229–237

    Article  PubMed  CAS  Google 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 79:213–226

    Article  PubMed  CAS  Google Scholar 

  • Fait A, Angelovici R, Less H, Ohad I, Urbanczyk-Wochniak E, Fernie AR, Galili G (2006) Arabidopsis seed development and germination is associated with temporally distinct metabolic switches. Plant Physiol 142:839–854

    Article  PubMed  CAS  Google Scholar 

  • Fischer-Iglesias C, Sundberg B, Neuhaus G, Jones AM (2001) Auxin distribution and transport during embryonic pattern formation in wheat. Plant J 26:115–129

    Article  PubMed  CAS  Google Scholar 

  • Fujita M, Horiuchi Y, Ueda Y, Mizuta Y, Kubo T, Yano K, Yamaki S, Tsuda K, Nagata T, Niihama M, Kato H, Kikuchi S, Hamada K, Mochizuki T, Ishimizu T, Iwai H, Tsutsumi N, Kurata N (2010) Rice expression atlas in reproductive development. Plant Cell Physiol 51:2060–2081

    Article  PubMed  CAS  Google Scholar 

  • Furtado A, Henry RJ (2005) The wheat Em promoter drives reporter gene expression in embryo and aleurone tissue of transgenic barley and rice. Plant Biotechnol J 3:421–434

    Article  PubMed  CAS  Google Scholar 

  • Furtado A, Henry RJ, Takaiwa F (2008) Comparison of promoters in transgenic rice. Plant Biotechnol J 6:679–693

    Article  PubMed  CAS  Google Scholar 

  • Furutani I, Sukegawa S, Kyozuka J (2006) Genome-wide analysis of spatial and temporal gene expression in rice panicle development. Plant J 46:503–511

    Article  PubMed  CAS  Google Scholar 

  • Galego L, Almeida J (2002) Role of DIVARICATA in the control of dorsoventral asymmetry in Antirrhinum flowers. Genes Dev 16:880–891

    Article  PubMed  CAS  Google Scholar 

  • Greco R, Stagi L, Colombo L, Angenent GC, Sari-Gorla M, Pe ME (1997) MADS box genes expressed in developing inflorescences of rice and sorghum. Mol Gen Genet 253:615–623

    Article  PubMed  CAS  Google Scholar 

  • Grimanelli D, Perotti E, Ramirez J, Leblanc O (2005) Timing of the maternal-to-zygotic transition during early seed development in maize. Plant Cell 17:1061–1072

    Article  PubMed  CAS  Google Scholar 

  • Gupta V, Khurana R, Tyagi AK (2007) Promoters of two anther-specific genes confer organ-specific gene expression in a stage-specific manner in transgenic systems. Plant Cell Rep 26:1919–1931

    Article  PubMed  CAS  Google Scholar 

  • Hansen M, Friis C, Bowra S, Holm PB, Vincze E (2009) A pathway-specific microarray analysis highlights the complex and co-ordinated transcriptional networks of the developing grain of field-grown barley. J Exp Bot 60:153–167

    Article  PubMed  CAS  Google Scholar 

  • Hennig L, Gruissem W, Grossniklaus U, Kohler C (2004) Transcriptional programs of early reproductive stages in Arabidopsis. Plant Physiol 135:1765–1775

    Article  PubMed  CAS  Google Scholar 

  • Hirano K, Aya K, Hobo T, Sakakibara H, Kojima M, Shim RA, Hasegawa Y, Ueguchi-Tanaka M, Matsuoka M (2008) Comprehensive transcriptome analysis of phytohormone biosynthesis and signaling genes in microspore/pollen and tapetum of rice. Plant Cell Physiol 49:1429–1450

    Article  PubMed  CAS  Google 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 49:1417–1428

    Article  PubMed  CAS  Google 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 149:961–980

    Article  PubMed  CAS  Google Scholar 

  • Hu J, Mitchum MG, Barnaby N, Ayele BT, Ogawa M, Nam E, Lai WC, Hanada A, Alonso JM, Ecker JR, Swain SM, Yamaguchi S, Kamiya Y, Sun TP (2008) Potential sites of bioactive gibberellin production during reproductive growth in Arabidopsis. Plant Cell 20:320–336

    Article  PubMed  CAS  Google Scholar 

  • Hundertmark M, Hincha DK (2008) LEA (late embryogenesis abundant) proteins and their encoding genes in Arabidopsis thaliana. BMC Genomics 9:118

    Article  PubMed  CAS  Google Scholar 

  • Ikeda K, Sunohara H, Nagato Y (2004) Developmental course of inflorescence and spikelet in rice. Breed Sci 54:147–156

    Article  Google Scholar 

  • Ingram GC, Boisnard-Lorig C, Dumas C, Rogowsky PM (2000) Expression patterns of genes encoding HD-ZipIV homeo domain proteins define specific domains in maize embryos and meristems. Plant J 22:401–414

    Article  PubMed  CAS  Google Scholar 

  • Itoh J, Nonomura K, Ikeda K, Yamaki S, Inukai Y, Yamagishi H, Kitano H, Nagato Y (2005) Rice plant development: from zygote to spikelet. Plant Cell Physiol 46:23–47

    Article  PubMed  CAS  Google Scholar 

  • Iwasaki M, Nitasaka E (2006) The FEATHERED gene is required for polarity establishment in lateral organs especially flowers of the Japanese morning glory (Ipomoea nil). Plant Mol Biol 62:913–925

    Article  PubMed  CAS  Google Scholar 

  • Jain M, Khurana JP (2009) Transcript profiling reveals diverse roles of auxin-responsive genes during reproductive development and abiotic stress in rice. FEBS J 276:3148–3162

    Article  PubMed  CAS  Google Scholar 

  • Jain M, Kaur N, Garg R, Thakur JK, Tyagi AK, Khurana JP (2006) Structure and expression analysis of early auxin-responsive Aux/IAA gene family in rice (Oryza sativa). Funct Integr Genomics 6:47–59

    Article  PubMed  CAS  Google 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 143:1467–1483

    Article  PubMed  CAS  Google Scholar 

  • Jain M, Tyagi AK, Khurana JP (2008) Genome-wide identification, classification, evolutionary expansion and expression analyses of homeobox genes in rice. FEBS J 275:2845–2861

    Article  PubMed  CAS  Google 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–D723

    Article  PubMed  CAS  Google Scholar 

  • Jefferson RA, Kavanagh TA, Bevan MW (1987) GUS fusions: beta-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J 6:3901–3907

    PubMed  CAS  Google Scholar 

  • Jeon JS, Lee S, Jung KH, Yang WS, Yi GH, Oh BG, An G (2000) Production of transgenic rice plants showing reduced heading date and plant height by ectopic expression of rice MADS-box genes. Mol Breed 6:581–592

    Article  CAS  Google Scholar 

  • Jeon JS, Lee S, An G (2008) Intragenic control of expression of a rice MADS box gene OsMADS1. Mol Cells 26:474–480

    PubMed  CAS  Google Scholar 

  • Jia H, Chen R, Cong B, Cao K, Sun C, Luo D (2000) Characterization and transcriptional profiles of two rice MADS-box genes. Plant Sci 155:115–122

    Article  PubMed  CAS  Google Scholar 

  • Jiang SY, Christoffels A, Ramamoorthy R, Ramachandran S (2009) Expansion mechanisms and functional annotations of hypothetical genes in the rice genome. Plant Physiol 150:1997–2008

    Article  PubMed  CAS  Google Scholar 

  • Jiao Y, Tausta SL, Gandotra N, Sun N, Liu T, Clay NK, Ceserani T, Chen M, Ma L, Holford M, Zhang HY, Zhao H, Deng XW, Nelson T (2009) A transcriptome atlas of rice cell types uncovers cellular, functional and developmental hierarchies. Nat Genet 41:258–263

    Article  PubMed  CAS  Google Scholar 

  • Kang HG, An G (1997) Isolation and characterization of a rice MADS box gene belonging to the AGL2 gene family. Mol Cells 7:45–51

    PubMed  CAS  Google Scholar 

  • Kang HG, Jang S, Chung JE, Cho YG, An G (1997) Characterization of two rice MADS box genes that control flowering time. Mol Cells 7:559–566

    PubMed  CAS  Google Scholar 

  • Kania T, Russenberger D, Peng S, Apel K, Melzer S (1997) FPF1 promotes flowering in Arabidopsis. Plant Cell 9:1327–1338

    Article  PubMed  CAS  Google Scholar 

  • Komatsu M, Maekawa M, Shimamoto K, Kyozuka J (2001) The LAX1 and FRIZZY PANICLE 2 genes determine the inflorescence architecture of rice by controlling rachis-branch and spikelet development. Dev Biol 231:364–373

    Article  PubMed  CAS  Google Scholar 

  • Komatsu K, Maekawa M, Ujiie S, Satake Y, Furutani I, Okamoto H, Shimamoto K, Kyozuka J (2003) LAX and SPA: major regulators of shoot branching in rice. Proc Natl Acad Sci USA 100:11765–11770

    Article  PubMed  CAS  Google Scholar 

  • Komiya R, Ikegami A, Tamaki S, Yokoi S, Shimamoto K (2008) Hd3a and RFT1 are essential for flowering in rice. Development 135:767–774

    Article  PubMed  CAS  Google Scholar 

  • Kondou H, Ooka H, Yamada H, Satoh K, Kikuchi S, Takahara Y, Yamamoto K (2006) Microarray analysis of gene expression at initial stages of rice seed development. Breed Sci 56:235–242

    Article  CAS  Google Scholar 

  • Kyozuka J, Konishi S, Nemoto K, Izawa T, Shimamoto K (1998) Down-regulation of RFL, the FLO/LFY homolog of rice, accompanied with panicle branch initiation. Proc Natl Acad Sci USA 95:1979–1982

    Article  PubMed  CAS  Google 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 15:475–486

    Article  PubMed  Google Scholar 

  • Lamacchia C, Shewry PR, Di Fonzo N, Forsyth JL, Harris N, Lazzeri PA, Napier JA, Halford NG, Barcelo P (2001) Endosperm-specific activity of a storage protein gene promoter in transgenic wheat seed. J Exp Bot 52:243–250

    Article  PubMed  CAS  Google 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 54:471–487

    Article  PubMed  CAS  Google Scholar 

  • Lee JM, Williams ME, Tingey SV, Rafalski JA (2002) DNA array profiling of gene expression changes during maize embryo development. Funct Integr Genomics 2:13–27

    Article  PubMed  CAS  Google Scholar 

  • Lee S, Kim J, Son JS, Nam J, Jeong DH, Lee K, Jang S, Yoo J, Lee J, Lee DY, Kang HG, An G (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

    Article  PubMed  CAS  Google Scholar 

  • Li L, Wang X, Sasidharan R, Stolc V, Deng W, He H, Korbel J, Chen X, Tongprasit W, Ronald P, Chen R, Gerstein M, Deng XW (2007a) Global identification and characterization of transcriptionally active regions in the rice genome. PLoS One 2:e294

    Article  PubMed  CAS  Google Scholar 

  • Li M, Xu W, Yang W, Kong Z, Xue Y (2007b) Genome-wide gene expression profiling reveals conserved and novel molecular functions of the stigma in rice. Plant Physiol 144:1797–1812

    Article  PubMed  CAS  Google Scholar 

  • Li Z, Zhang H, Ge S, Gu X, Gao G, Luo J (2009) Expression pattern divergence of duplicated genes in rice. BMC Bioinforma 10(Suppl 6):S8

    Article  CAS  Google Scholar 

  • Liu XL, Covington MF, Fankhauser C, Chory J, Wagner DR (2001) ELF3 encodes a circadian clock-regulated nuclear protein that functions in an Arabidopsis PHYB signal transduction pathway. Plant Cell 13:1293–1304

    Article  PubMed  CAS  Google Scholar 

  • Liu X, Fu J, Gu D, Liu W, Liu T, Peng Y, Wang J, Wang G (2008) Genome-wide analysis of gene expression profiles during the kernel development of maize (Zea mays L.). Genomics 91:378–387

    Article  PubMed  CAS  Google 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 62:397–408

    Article  PubMed  CAS  Google Scholar 

  • Lynn K, Fernandez A, Aida M, Sedbrook J, Tasaka M, Masson P, Barton MK (1999) The PINHEAD/ZWILLE gene acts pleiotropically in Arabidopsis development and has overlapping functions with the ARGONAUTE1 gene. Development 126:469–481

    PubMed  CAS  Google Scholar 

  • Ma H (2005) Molecular genetic analyses of microsporogenesis and microgametogenesis in flowering plants. Annu Rev Plant Biol 56:393–434

    Article  PubMed  CAS  Google Scholar 

  • Ma H, Zhao J (2010) Genome-wide identification, classification, and expression analysis of the arabinogalactan protein gene family in rice (Oryza sativa L.). J Exp Bot 61:2647–2668

    Article  PubMed  CAS  Google Scholar 

  • Ma L, Chen C, Liu X, Jiao Y, Su N, Li L, Wang X, Cao M, Sun N, Zhang X, Bao J, Li J, Pedersen S, Bolund L, Zhao H, Yuan L, Wong GK, Wang J, Deng XW (2005) A microarray analysis of the rice transcriptome and its comparison to Arabidopsis. Genome Res 15:1274–1283

    Article  PubMed  CAS  Google Scholar 

  • Madera M, Gough J (2002) A comparison of profile hidden Markov model procedures for remote homology detection. Nuc Acids Res 30:4321–4328

    Article  CAS  Google Scholar 

  • Michalak P (2008) Coexpression, coregulation, and cofunctionality of neighboring genes in eukaryotic genomes. Genomics 91:243–248

    Article  PubMed  CAS  Google Scholar 

  • Millar AA, Clemens S, Zachgo S, Giblin EM, Taylor DC, Kunst L (1999) CUT1, an Arabidopsis gene required for cuticular wax biosynthesis and pollen fertility, encodes a very-long-chain fatty acid condensing enzyme. Plant Cell 11:825–838

    Article  PubMed  CAS  Google Scholar 

  • Mohanty A, Sarma NP, Tyagi AK (1999) Agrobacterium-mediated high frequency transformation of an elite indica rice variety Pusa Basmati 1 and transmission of the transgene to R2 progeny. Plant Sci 147:125–135

    Article  Google Scholar 

  • Moon YH, Kang HG, Jung JY, Jeon JS, Sung SK, An G (1999) Determination of the motif responsible for interaction between the rice APETALA1/AGAMOUS-LIKE9 family proteins using a yeast two-hybrid system. Plant Physiol 120:1193–1204

    Article  PubMed  CAS  Google Scholar 

  • Muller J, Wang Y, Franzen R, Santi L, Salamini F, Rohde W (2001) In vitro interactions between barley TALE homeodomain proteins suggest a role for protein-protein associations in the regulation of Knox gene function. Plant J 27:13–23

    Article  PubMed  CAS  Google Scholar 

  • Nijhawan A, Jain M, Tyagi AK, Khurana JP (2008) Genomic survey and gene expression analysis of the basic leucine zipper transcription factor family in rice. Plant Physiol 146:333–350

    Article  PubMed  CAS  Google Scholar 

  • Okazaki N, Okazaki K, Watanabe Y, Kato-Hayashi M, Yamamoto M, Okayama H (1998) Novel factor highly conserved among eukaryotes controls sexual development in fission yeast. Mol Cell Biol 18:887–895

    PubMed  CAS  Google Scholar 

  • Perez-Prat E, van Lookeren Campagne MM (2002) Hybrid seed production and the challenge of propagating male-sterile plants. Trends Plant Sci 7:199–203

    Article  PubMed  CAS  Google Scholar 

  • Prasad K, Vijayraghavan U (2003) Double-stranded RNA interference of a rice PI/GLO paralog, OsMADS2, uncovers its second-whorl-specific function in floral organ patterning. Genetics 165:2301–2305

    PubMed  CAS  Google Scholar 

  • Prasad K, Sriram P, Kumar CS, Kushalappa K, Vijayraghavan U (2001) Ectopic expression of rice OsMADS1 reveals a role in specifying the lemma and palea, grass floral organs analogous to sepals. Dev Genes Evol 211:281–290

    Article  PubMed  CAS  Google Scholar 

  • Prasad K, Parameswaran S, Vijayraghavan U (2005) OsMADS1, a rice MADS-box factor, controls differentiation of specific cell types in the lemma and palea and is an early-acting regulator of inner floral organs. Plant J 43:915–928

    Article  PubMed  CAS  Google Scholar 

  • Qu le Q, Takaiwa F (2004) Evaluation of tissue specificity and expression strength of rice seed component gene promoters in transgenic rice. Plant Biotechnol J 2:113–125

    Article  PubMed  Google Scholar 

  • Raghavan V (1988) Anther and pollen development in rice (Oryza sativa). Amer J Bot 75:183–196

    Article  Google Scholar 

  • Ray S, Dansana PK, Giri J, Deveshwar P, Arora R, Agarwal P, Khurana JP, Kapoor S, Tyagi AK (2011) Modulation of transcription factor and metabolic pathway genes in response to water-deficit stress in rice. Funct Integr Genomics 11:157–178

    Article  PubMed  CAS  Google Scholar 

  • Ren XY, Fiers MW, Stiekema WJ, Nap JP (2005) Local coexpression domains of two to four genes in the genome of Arabidopsis. Plant Physiol 138:923–934

    Article  PubMed  CAS  Google Scholar 

  • Ren XY, Stiekema WJ, Nap JP (2007) Local coexpression domains in the genome of rice show no microsynteny with Arabidopsis domains. Plant Mol Biol 65:205–217

    Article  PubMed  CAS  Google Scholar 

  • Riano-Pachon DM, Ruzicic S, Dreyer I, Mueller-Roeber B (2007) PlnTFDB: an integrative plant transcription factor database. BMC Bioinforma 8:42

    Article  CAS  Google Scholar 

  • Roque E, Gomez MD, Ellul P, Wallbraun M, Madueno F, Beltran JP, Canas LA (2007) The PsEND1 promoter: a novel tool to produce genetically engineered male-sterile plants by early anther ablation. Plant Cell Rep 26:313–325

    Article  PubMed  CAS  Google Scholar 

  • Russell DA, Fromm ME (1997) Tissue-specific expression in transgenic maize of four endosperm promoters from maize and rice. Transgenic Res 6:157–168

    Article  PubMed  CAS  Google 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 11:10

    Article  PubMed  CAS  Google Scholar 

  • Sentoku N, Sato Y, Kurata N, Ito Y, Kitano H, Matsuoka M (1999) Regional expression of the rice KN1-type homeobox gene family during embryo, shoot, and flower development. Plant Cell 11:1651–1664

    Article  PubMed  CAS  Google Scholar 

  • Sharma R, Mohan Singh RK, Malik G, Deveshwar P, Tyagi AK, Kapoor S, Kapoor M (2009) Rice cytosine DNA methyltransferases—gene expression profiling during reproductive development and abiotic stress. FEBS J 276:6301–6311

    Article  PubMed  CAS  Google 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 1:24–38

    CAS  Google Scholar 

  • Simkin AJ, Qian T, Caillet V, Michoux F, Ben Amor M, Lin C, Tanksley S, McCarthy J (2006) Oleosin gene family of Coffea canephora: quantitative expression analysis of five oleosin genes in developing and germinating coffee grain. J Plant Physiol 163:691–708

    Article  PubMed  CAS  Google Scholar 

  • Singh A, Giri J, Kapoor S, Tyagi AK, Pandey GK (2010) Protein phosphatase complement in rice: genome-wide identification and transcriptional analysis under abiotic stress conditions and reproductive development. BMC Genomics 11:435

    Article  PubMed  CAS  Google Scholar 

  • Smyth DR, Bowman JL, Meyerowitz EM (1990) Early flower development in Arabidopsis. Plant Cell 2:755–767

    Article  PubMed  CAS  Google Scholar 

  • Song JY, Leung T, Ehler LK, Wang C, Liu Z (2000) Regulation of meristem organization and cell division by TSO1, an Arabidopsis gene with cysteine-rich repeats. Development 127:2207–2217

    PubMed  CAS  Google Scholar 

  • Sunilkumar G, Connell JP, Smith CW, Reddy AS, Rathore KS (2002) Cotton alpha-globulin promoter: isolation and functional characterization in transgenic cotton, Arabidopsis, and tobacco. Transgenic Res 11:347–359

    Article  PubMed  CAS  Google 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 49:1407–1416

    Article  PubMed  CAS  Google Scholar 

  • Takeda T, Suwa Y, Suzuki M, Kitano H, Ueguchi-Tanaka M, Ashikari M, Matsuoka M, Ueguchi C (2003) The OsTB1 gene negatively regulates lateral branching in rice. Plant J 33:513–520

    Article  PubMed  CAS  Google Scholar 

  • Tebbji F, Nantel A, Matton DP (2010) Transcription profiling of fertilization and early seed development events in a solanaceous species using a 7.7 K cDNA microarray from Solanum chacoense ovules. BMC Plant Biol 10:174

    Article  PubMed  CAS  Google Scholar 

  • Toki S, Hara N, Ono K, Onodera H, Tagiri A, Oka S, Tanaka H (2006) Early infection of scutellum tissue with Agrobacterium allows high-speed transformation of rice. Plant J 47:969–976

    Article  PubMed  CAS  Google Scholar 

  • Twell D, Yamaguchi J, McCormick S (1990) Pollen-specific gene expression in transgenic plants: coordinate regulation of two different tomato gene promoters during microsporogenesis. Development 109:705–713

    PubMed  CAS  Google Scholar 

  • Wang Z, Liang Y, Li C, Xu Y, Lan L, Zhao D, Chen C, Xu Z, Xue Y, Chong K (2005) Microarray analysis of gene expression involved in anther development in rice (Oryza sativa L.). Plant Mol Biol 58:721–737

    Article  PubMed  CAS  Google Scholar 

  • Wang L, Xie W, Chen Y, Tang W, Yang J, Ye R, Liu L, Lin Y, Xu C, Xiao J, Zhang Q (2010) A dynamic gene expression atlas covering the entire life cycle of rice. Plant J 61:752–766

    Article  PubMed  CAS  Google Scholar 

  • Wellmer F, Riechmann JL, Alves-Ferreira M, Meyerowitz EM (2004) Genome-wide analysis of spatial gene expression in Arabidopsis flowers. Plant Cell 16:1314–1326

    Article  PubMed  CAS  Google Scholar 

  • Wellmer F, Alves-Ferreira M, Dubois A, Riechmann JL, Meyerowitz EM (2006) Genome-wide analysis of gene expression during early Arabidopsis flower development. PLoS Genet 2:e117

    Article  PubMed  CAS  Google Scholar 

  • Wilson ZA, Zhang DB (2009) From Arabidopsis to rice: pathways in pollen development. J Exp Bot 60:1479–1492

    Article  PubMed  CAS  Google Scholar 

  • Wilson ID, Barker GL, Lu C, Coghill JA, Beswick RW, Lenton JR, Edwards KJ (2005a) Alteration of the embryo transcriptome of hexaploid winter wheat (Triticum aestivum cv. Mercia) during maturation and germination. Funct Integr Genomics 5:144–154

    Article  PubMed  Google Scholar 

  • Wilson IW, Kennedy GC, Peacock JW, Dennis ES (2005b) Microarray analysis reveals vegetative molecular phenotypes of Arabidopsis flowering-time mutants. Plant Cell Physiol 46:1190–1201

    Article  PubMed  CAS  Google 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.

  • Xu BY, Liu G, Jin ZQ (2006) Isolation, sequencing analysis and characterization of the promoter of banana lectin gene. Sheng Wu Gong Cheng Xue Bao 22:945–949

    PubMed  CAS  Google Scholar 

  • Yamaguchi T, Hirano HY (2006) Function and diversification of MADS-box genes in rice. Scientific World J 6:1923–1932

    Article  Google Scholar 

  • Yamaguchi T, Lee DY, Miyao A, Hirochika H, An G, Hirano HY (2006) Functional diversification of the two C-class MADS box genes OsMADS3 and OsMADS58 in Oryza sativa. Plant Cell 18:15–28

    Article  PubMed  CAS  Google Scholar 

  • Yang SL, Xie LF, Mao HZ, Puah CS, Yang WC, Jiang L, Sundaresan V, Ye D (2003) Tapetum determinant1 is required for cell specialization in the Arabidopsis anther. Plant Cell 15:2792–2804

    Article  PubMed  CAS  Google Scholar 

  • Yang C, Vizcay-Barrena G, Conner K, Wilson ZA (2007) MALE STERILITY1 is required for tapetal development and pollen wall biosynthesis. Plant Cell 19:3530–3548

    Article  PubMed  CAS  Google Scholar 

  • Yi Y, Mirosevich J, Shyr Y, Matusik R, George AL Jr (2005) Coupled analysis of gene expression and chromosomal location. Genomics 85:401–412

    Article  PubMed  CAS  Google Scholar 

  • Yin Y, Vafeados D, Tao Y, Yoshida S, Asami T, Chory J (2005) A new class of transcription factors mediates brassinosteroid-regulated gene expression in Arabidopsis. Cell 120:249–259

    Article  PubMed  CAS  Google Scholar 

  • Zhan S, Horrocks J, Lukens LN (2006) Islands of co-expressed neighbouring genes in Arabidopsis thaliana suggest higher-order chromosome domains. Plant J 45:347–357

    Article  PubMed  CAS  Google Scholar 

  • Zhang X, Feng B, Zhang Q, Zhang D, Altman N, Ma H (2005) Genome-wide expression profiling and identification of gene activities during early flower development in Arabidopsis. Plant Mol Biol 58:401–419

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

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.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Sanjay Kapoor.

Additional information

The authors Rita Sharma and Pinky Agarwal contributed equally to this work.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Table S1

(XLS 12 kb)

Table S2

(XLS 24 kb)

Table S3

(XLS 1198 kb)

Table S4

(XLS 57 kb)

Table S5

(XLS 33 kb)

Table S6

(XLS 557 kb)

Table S7

(XLS 19 kb)

Table S8

(XLS 20 kb)

Supplementary Figures (DOC 3903 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Sharma, R., Agarwal, P., Ray, S. et al. Expression dynamics of metabolic and regulatory components across stages of panicle and seed development in indica rice. Funct Integr Genomics 12, 229–248 (2012). https://doi.org/10.1007/s10142-012-0274-3

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10142-012-0274-3

Keywords

Navigation