Functional & Integrative Genomics

, Volume 12, Issue 2, pp 229–248 | Cite as

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

  • Rita Sharma
  • Pinky Agarwal
  • Swatismita Ray
  • Priyanka Deveshwar
  • Pooja Sharma
  • Niharika Sharma
  • Aashima Nijhawan
  • Mukesh Jain
  • Ashok Kumar Singh
  • Vijay Pal Singh
  • Jitendra Paul Khurana
  • Akhilesh Kumar Tyagi
  • Sanjay Kapoor
Original Paper


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.


Development 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.

Supplementary material

10142_2012_274_MOESM1_ESM.xls (12 kb)
Table S1 (XLS 12 kb)
10142_2012_274_MOESM2_ESM.xls (24 kb)
Table S2 (XLS 24 kb)
10142_2012_274_MOESM3_ESM.xls (1.2 mb)
Table S3 (XLS 1198 kb)
10142_2012_274_MOESM4_ESM.xls (57 kb)
Table S4 (XLS 57 kb)
10142_2012_274_MOESM5_ESM.xls (33 kb)
Table S5 (XLS 33 kb)
10142_2012_274_MOESM6_ESM.xls (557 kb)
Table S6 (XLS 557 kb)
10142_2012_274_MOESM7_ESM.xls (20 kb)
Table S7 (XLS 19 kb)
10142_2012_274_MOESM8_ESM.xls (20 kb)
Table S8 (XLS 20 kb)
10142_2012_274_MOESM9_ESM.doc (3.8 mb)
Supplementary Figures (DOC 3903 kb)


  1. Adams (2008) Transcriptome: connecting the genome to gene function. Nature Education 1Google Scholar
  2. 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 65:467–485PubMedCrossRefGoogle Scholar
  3. Agarwal P, Kapoor S, Tyagi AK (2011) Transcription factors regulating the progression of monocot and dicot seed development. Bioessays 33:189–202PubMedCrossRefGoogle Scholar
  4. 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 59:125–135PubMedCrossRefGoogle Scholar
  5. 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 59:3551–3562PubMedCrossRefGoogle Scholar
  6. 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 145:747–762PubMedCrossRefGoogle Scholar
  7. 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 131:3615–3626PubMedCrossRefGoogle Scholar
  8. 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 8:242PubMedCrossRefGoogle Scholar
  9. Baltz R, Domon C, Pillay DT, Steinmetz A (1992) Characterization of a pollen-specific cDNA from sunflower encoding a zinc finger protein. Plant J 2:713–721PubMedGoogle Scholar
  10. Becerra C, Puigdomenech P, Vicient CM (2006) Computational and experimental analysis identifies Arabidopsis genes specifically expressed during early seed development. BMC Genomics 7:38PubMedCrossRefGoogle Scholar
  11. Becker JD, Feijo JA (2007) How many genes are needed to make a pollen tube? Lessons from transcriptomics. Ann Bot (Lond) 100:1117–1123CrossRefGoogle Scholar
  12. 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
  13. Bhalla PL, Swoboda I, Singh MB (2001) Reduction in allergenicity of grass pollen by genetic engineering. Int Arch Allergy Immunol 124:51–54PubMedCrossRefGoogle Scholar
  14. Cao PJ, Bartley LE, Jung KH, Ronald PC (2008) Construction of a rice glycosyltransferase phylogenomic database and identification of rice-diverged glycosyltransferases. Mol Plant 1:858–877PubMedCrossRefGoogle Scholar
  15. Carninci P (2008) Non-coding RNA transcription: turning on neighbours. Nat Cell Biol 10:1023–1024PubMedCrossRefGoogle Scholar
  16. Chardon F, Damerval C (2005) Phylogenomic analysis of the PEBP gene family in cereals. J Mol Evol 61:579–590PubMedCrossRefGoogle Scholar
  17. Cheng JC, Seeley KA, Goupil P, Sung ZR (1996) Expression of DC8 is associated with, but not dependent on embryogenesis. Plant Mol Biol 31:127–141PubMedCrossRefGoogle Scholar
  18. 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 26:657–665PubMedCrossRefGoogle Scholar
  19. 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 109:45–56CrossRefGoogle Scholar
  20. 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 89:575–585PubMedCrossRefGoogle Scholar
  21. Clouse SD, Sasse JM (1998) Brassinosteroids: essential regulators of plant growth and development. Annu Rev Plant Physiol Plant Mol Biol 49:427–451PubMedCrossRefGoogle Scholar
  22. Curtis MD, Grossniklaus U (2003) A gateway cloning vector set for high-throughput functional analysis of genes in planta. Plant Physiol 133:462–469PubMedCrossRefGoogle Scholar
  23. 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 15:425–438PubMedCrossRefGoogle Scholar
  24. Davidson SE, Elliott RC, Helliwell CA, Poole AT, Reid JB (2003) The pea gene NA encodes ent-kaurenoic acid oxidase. Plant Physiol 131:335–344PubMedCrossRefGoogle Scholar
  25. 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 148:1964–1984PubMedCrossRefGoogle Scholar
  26. 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 74:757–768PubMedCrossRefGoogle Scholar
  27. 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 11:78PubMedCrossRefGoogle Scholar
  28. 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 176:1501–1510PubMedCrossRefGoogle Scholar
  29. 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 17:2172–2185PubMedCrossRefGoogle Scholar
  30. Ebisuya M, Yamamoto T, Nakajima M, Nishida E (2008) Ripples from neighbouring transcription. Nat Cell Biol 10:1106–1113PubMedCrossRefGoogle Scholar
  31. 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
  32. 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
  33. 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 142:839–854PubMedCrossRefGoogle Scholar
  34. Fischer-Iglesias C, Sundberg B, Neuhaus G, Jones AM (2001) Auxin distribution and transport during embryonic pattern formation in wheat. Plant J 26:115–129PubMedCrossRefGoogle Scholar
  35. 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 51:2060–2081PubMedCrossRefGoogle Scholar
  36. 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 3:421–434PubMedCrossRefGoogle Scholar
  37. Furtado A, Henry RJ, Takaiwa F (2008) Comparison of promoters in transgenic rice. Plant Biotechnol J 6:679–693PubMedCrossRefGoogle Scholar
  38. Furutani I, Sukegawa S, Kyozuka J (2006) Genome-wide analysis of spatial and temporal gene expression in rice panicle development. Plant J 46:503–511PubMedCrossRefGoogle Scholar
  39. Galego L, Almeida J (2002) Role of DIVARICATA in the control of dorsoventral asymmetry in Antirrhinum flowers. Genes Dev 16:880–891PubMedCrossRefGoogle Scholar
  40. 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 253:615–623PubMedCrossRefGoogle Scholar
  41. Grimanelli D, Perotti E, Ramirez J, Leblanc O (2005) Timing of the maternal-to-zygotic transition during early seed development in maize. Plant Cell 17:1061–1072PubMedCrossRefGoogle Scholar
  42. 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 26:1919–1931PubMedCrossRefGoogle Scholar
  43. 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 60:153–167PubMedCrossRefGoogle Scholar
  44. Hennig L, Gruissem W, Grossniklaus U, Kohler C (2004) Transcriptional programs of early reproductive stages in Arabidopsis. Plant Physiol 135:1765–1775PubMedCrossRefGoogle Scholar
  45. 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 49:1429–1450PubMedCrossRefGoogle Scholar
  46. 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
  47. 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
  48. 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 20:320–336PubMedCrossRefGoogle Scholar
  49. Hundertmark M, Hincha DK (2008) LEA (late embryogenesis abundant) proteins and their encoding genes in Arabidopsis thaliana. BMC Genomics 9:118PubMedCrossRefGoogle Scholar
  50. Ikeda K, Sunohara H, Nagato Y (2004) Developmental course of inflorescence and spikelet in rice. Breed Sci 54:147–156CrossRefGoogle Scholar
  51. 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 22:401–414PubMedCrossRefGoogle Scholar
  52. 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 46:23–47PubMedCrossRefGoogle Scholar
  53. 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 62:913–925PubMedCrossRefGoogle Scholar
  54. Jain M, Khurana JP (2009) Transcript profiling reveals diverse roles of auxin-responsive genes during reproductive development and abiotic stress in rice. FEBS J 276:3148–3162PubMedCrossRefGoogle Scholar
  55. 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 6:47–59PubMedCrossRefGoogle Scholar
  56. 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
  57. Jain M, Tyagi AK, Khurana JP (2008) Genome-wide identification, classification, evolutionary expansion and expression analyses of homeobox genes in rice. FEBS J 275:2845–2861PubMedCrossRefGoogle Scholar
  58. 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
  59. Jefferson RA, Kavanagh TA, Bevan MW (1987) GUS fusions: beta-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J 6:3901–3907PubMedGoogle Scholar
  60. 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 6:581–592CrossRefGoogle Scholar
  61. Jeon JS, Lee S, An G (2008) Intragenic control of expression of a rice MADS box gene OsMADS1. Mol Cells 26:474–480PubMedGoogle Scholar
  62. 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 155:115–122PubMedCrossRefGoogle Scholar
  63. Jiang SY, Christoffels A, Ramamoorthy R, Ramachandran S (2009) Expansion mechanisms and functional annotations of hypothetical genes in the rice genome. Plant Physiol 150:1997–2008PubMedCrossRefGoogle Scholar
  64. 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 41:258–263PubMedCrossRefGoogle Scholar
  65. Kang HG, An G (1997) Isolation and characterization of a rice MADS box gene belonging to the AGL2 gene family. Mol Cells 7:45–51PubMedGoogle Scholar
  66. Kang HG, Jang S, Chung JE, Cho YG, An G (1997) Characterization of two rice MADS box genes that control flowering time. Mol Cells 7:559–566PubMedGoogle Scholar
  67. Kania T, Russenberger D, Peng S, Apel K, Melzer S (1997) FPF1 promotes flowering in Arabidopsis. Plant Cell 9:1327–1338PubMedCrossRefGoogle Scholar
  68. 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 231:364–373PubMedCrossRefGoogle Scholar
  69. 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 100:11765–11770PubMedCrossRefGoogle Scholar
  70. Komiya R, Ikegami A, Tamaki S, Yokoi S, Shimamoto K (2008) Hd3a and RFT1 are essential for flowering in rice. Development 135:767–774PubMedCrossRefGoogle Scholar
  71. 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 56:235–242CrossRefGoogle Scholar
  72. 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 95:1979–1982PubMedCrossRefGoogle Scholar
  73. 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
  74. 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 52:243–250PubMedCrossRefGoogle Scholar
  75. 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
  76. Lee JM, Williams ME, Tingey SV, Rafalski JA (2002) DNA array profiling of gene expression changes during maize embryo development. Funct Integr Genomics 2:13–27PubMedCrossRefGoogle Scholar
  77. 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 44:1403–1411PubMedCrossRefGoogle Scholar
  78. 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:e294PubMedCrossRefGoogle Scholar
  79. 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 144:1797–1812PubMedCrossRefGoogle Scholar
  80. 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):S8CrossRefGoogle Scholar
  81. 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 13:1293–1304PubMedCrossRefGoogle Scholar
  82. 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 91:378–387PubMedCrossRefGoogle Scholar
  83. 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
  84. 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 126:469–481PubMedGoogle Scholar
  85. Ma H (2005) Molecular genetic analyses of microsporogenesis and microgametogenesis in flowering plants. Annu Rev Plant Biol 56:393–434PubMedCrossRefGoogle Scholar
  86. 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 61:2647–2668PubMedCrossRefGoogle Scholar
  87. 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 15:1274–1283PubMedCrossRefGoogle Scholar
  88. Madera M, Gough J (2002) A comparison of profile hidden Markov model procedures for remote homology detection. Nuc Acids Res 30:4321–4328CrossRefGoogle Scholar
  89. Michalak P (2008) Coexpression, coregulation, and cofunctionality of neighboring genes in eukaryotic genomes. Genomics 91:243–248PubMedCrossRefGoogle Scholar
  90. 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 11:825–838PubMedCrossRefGoogle Scholar
  91. 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 147:125–135CrossRefGoogle Scholar
  92. 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 120:1193–1204PubMedCrossRefGoogle Scholar
  93. 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 27:13–23PubMedCrossRefGoogle Scholar
  94. 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 146:333–350PubMedCrossRefGoogle Scholar
  95. 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 18:887–895PubMedGoogle Scholar
  96. Perez-Prat E, van Lookeren Campagne MM (2002) Hybrid seed production and the challenge of propagating male-sterile plants. Trends Plant Sci 7:199–203PubMedCrossRefGoogle Scholar
  97. 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 165:2301–2305PubMedGoogle Scholar
  98. 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 211:281–290PubMedCrossRefGoogle Scholar
  99. 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 43:915–928PubMedCrossRefGoogle Scholar
  100. 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 2:113–125PubMedCrossRefGoogle Scholar
  101. Raghavan V (1988) Anther and pollen development in rice (Oryza sativa). Amer J Bot 75:183–196CrossRefGoogle Scholar
  102. 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 11:157–178PubMedCrossRefGoogle Scholar
  103. Ren XY, Fiers MW, Stiekema WJ, Nap JP (2005) Local coexpression domains of two to four genes in the genome of Arabidopsis. Plant Physiol 138:923–934PubMedCrossRefGoogle Scholar
  104. Ren XY, Stiekema WJ, Nap JP (2007) Local coexpression domains in the genome of rice show no microsynteny with Arabidopsis domains. Plant Mol Biol 65:205–217PubMedCrossRefGoogle Scholar
  105. Riano-Pachon DM, Ruzicic S, Dreyer I, Mueller-Roeber B (2007) PlnTFDB: an integrative plant transcription factor database. BMC Bioinforma 8:42CrossRefGoogle Scholar
  106. 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 26:313–325PubMedCrossRefGoogle Scholar
  107. Russell DA, Fromm ME (1997) Tissue-specific expression in transgenic maize of four endosperm promoters from maize and rice. Transgenic Res 6:157–168PubMedCrossRefGoogle Scholar
  108. 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
  109. 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 11:1651–1664PubMedCrossRefGoogle Scholar
  110. 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 276:6301–6311PubMedCrossRefGoogle Scholar
  111. 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
  112. 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 163:691–708PubMedCrossRefGoogle Scholar
  113. 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 11:435PubMedCrossRefGoogle Scholar
  114. Smyth DR, Bowman JL, Meyerowitz EM (1990) Early flower development in Arabidopsis. Plant Cell 2:755–767PubMedCrossRefGoogle Scholar
  115. 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 127:2207–2217PubMedGoogle Scholar
  116. 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 11:347–359PubMedCrossRefGoogle Scholar
  117. 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
  118. 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 33:513–520PubMedCrossRefGoogle Scholar
  119. 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 10:174PubMedCrossRefGoogle Scholar
  120. 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 47:969–976PubMedCrossRefGoogle Scholar
  121. 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 109:705–713PubMedGoogle Scholar
  122. 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 58:721–737PubMedCrossRefGoogle Scholar
  123. 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 61:752–766PubMedCrossRefGoogle Scholar
  124. Wellmer F, Riechmann JL, Alves-Ferreira M, Meyerowitz EM (2004) Genome-wide analysis of spatial gene expression in Arabidopsis flowers. Plant Cell 16:1314–1326PubMedCrossRefGoogle Scholar
  125. 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:e117PubMedCrossRefGoogle Scholar
  126. Wilson ZA, Zhang DB (2009) From Arabidopsis to rice: pathways in pollen development. J Exp Bot 60:1479–1492PubMedCrossRefGoogle Scholar
  127. 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 5:144–154PubMedCrossRefGoogle Scholar
  128. Wilson IW, Kennedy GC, Peacock JW, Dennis ES (2005b) Microarray analysis reveals vegetative molecular phenotypes of Arabidopsis flowering-time mutants. Plant Cell Physiol 46:1190–1201PubMedCrossRefGoogle Scholar
  129. 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
  130. 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 22:945–949PubMedGoogle Scholar
  131. Yamaguchi T, Hirano HY (2006) Function and diversification of MADS-box genes in rice. Scientific World J 6:1923–1932CrossRefGoogle Scholar
  132. 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 18:15–28PubMedCrossRefGoogle Scholar
  133. 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 15:2792–2804PubMedCrossRefGoogle Scholar
  134. Yang C, Vizcay-Barrena G, Conner K, Wilson ZA (2007) MALE STERILITY1 is required for tapetal development and pollen wall biosynthesis. Plant Cell 19:3530–3548PubMedCrossRefGoogle Scholar
  135. Yi Y, Mirosevich J, Shyr Y, Matusik R, George AL Jr (2005) Coupled analysis of gene expression and chromosomal location. Genomics 85:401–412PubMedCrossRefGoogle Scholar
  136. 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 120:249–259PubMedCrossRefGoogle Scholar
  137. Zhan S, Horrocks J, Lukens LN (2006) Islands of co-expressed neighbouring genes in Arabidopsis thaliana suggest higher-order chromosome domains. Plant J 45:347–357PubMedCrossRefGoogle Scholar
  138. 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 58:401–419PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2012

Authors and Affiliations

  • Rita Sharma
    • 1
    • 3
  • Pinky Agarwal
    • 1
    • 4
  • Swatismita Ray
    • 1
    • 5
  • Priyanka Deveshwar
    • 1
  • Pooja Sharma
    • 1
  • Niharika Sharma
    • 1
    • 6
  • Aashima Nijhawan
    • 1
  • Mukesh Jain
    • 1
    • 4
  • Ashok Kumar Singh
    • 2
  • Vijay Pal Singh
    • 2
  • Jitendra Paul Khurana
    • 1
  • Akhilesh Kumar Tyagi
    • 1
    • 4
  • Sanjay Kapoor
    • 1
  1. 1.Interdisciplinary Centre for Plant Genomics and Department of Plant Molecular BiologyUniversity of Delhi South CampusNew DelhiIndia
  2. 2.Division of GeneticsIndian Agriculture Research InstituteNew DelhiIndia
  3. 3.Department of Plant PathologyUniversity of CaliforniaDavisUSA
  4. 4.National Institute for Plant Genome ResearchNew DelhiIndia
  5. 5.Biotechnology and Bioresources Management DivisionTata Energy Research InstituteNew DelhiIndia
  6. 6.Plant Molecular Biology and Biotechnology Group, Melbourne School of Land and EnvironmentUniversity of MelbourneParkvilleAustralia

Personalised recommendations