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Molecular analysis of early rice stamen development using organ-specific gene expression profiling

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Abstract

Elucidating the regulatory mechanisms of plant organ formation is an important component of plant developmental biology and will be useful for crop improvement applications. Plant organ formation, or organogenesis, occurs when a group of primordial cells differentiates into an organ, through a well-orchestrated series of events, with a given shape, structure and function. Research over the past two decades has elucidated the molecular mechanisms of organ identity and dorsalventral axis determinations. However, little is known about the molecular mechanisms underlying the successive processes. To develop an effective approach for studying organ formation at the molecular level, we generated organ-specific gene expression profiles (GEPs) reflecting early development in rice stamen. In this study, we demonstrated that the GEPs are highly correlated with early stamen development, suggesting that this analysis is useful for dissecting stamen development regulation. Based on the molecular and morphological correlation, we found that over 26 genes, that were preferentially up-regulated during early stamen development, may participate in stamen development regulation. In addition, we found that differentially expressed genes during early stamen development are clustered into two clades, suggesting that stamen development may comprise of two distinct phases of pattern formation and cellular differentiation. Moreover, the organ-specific quantitative changes in gene expression levels may play a critical role for regulating plant organ formation.

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Abbreviations

aRNA:

antisense RNA

cDNA:

complementary DNA

DEPC:

diethyl pyrocarbonate

dUTP:

deoxyuridine triphosphate

EMS:

EXCESS MICROSPOROCYTES

ESTs:

expression sequence tags

EXS:

EXTRA SPOROGENOUS CELLS

FIL:

FILAMENTOUS FLOWER

LLS:

LETHAL LEAF SPOT

LPA:

linear polyacrylamide

msca1 :

male sterile converted anther1

NZZ:

NOZZLE

OsMADS7:

rice MADS-box protein 7

PCR:

polymerase chain reaction

PHD:

plant homeodomain

RNA:

ribosome nucleic acid

RT:

reverse transcription

SPL:

SPOROCYTELESS

TPD:

TAPETUM DETERMINANT

References

  • Bai SL, Peng YB, Cui JX, Gu HT, Xu LY, Li YQ, Xu ZH, Bai SN (2004) Developmental analyses reveal early arrests of the spore-bearing parts of reproductive organs in unisexual flowers of cucumber (Cucumis sativus L). Planta 220:230–240

    Article  PubMed  CAS  Google Scholar 

  • Baugh LR, Hill AA, Brown EL, Hunter CP (2001) Quantitative analysis of mRNA amplification by in vitro transcription. Nucleic Acids Res 29:E29

    Article  PubMed  CAS  Google Scholar 

  • Bey M, Stuber K, Fellenberg K, Schwarz-Sommer Z, Sommer H, Saedler H, Zachgo S (2004) Characterization of antirrhinum petal development and identification of target genes of the class BMADS box gene DEFICIENS. Plant Cell 16:3197–3215

    Article  PubMed  Google Scholar 

  • Canales C, Bhatt AM, Scott R, Dickinson H (2002) EXS, a putative LRR receptor kinase, regulates male germline cell number and tapetal identity and promotes seed development in Arabidopsis. Curr Biol 12:1718–1727

    Article  PubMed  CAS  Google Scholar 

  • Chaubal R, Anderson JR, Trimnell MR, Fox TW, Albertsen MC, Bedinger P (2003) The transformation of anthers in the msca1 mutant of maize. Planta 216:778–788

    PubMed  CAS  Google Scholar 

  • Coen ES, Meyerowitz EM (1991) The war of the whorls: genetic interactions controlling flower development. Nature 353:31–37

    Article  PubMed  CAS  Google Scholar 

  • Coen E, Rolland-Lagan AG, Matthews M, Bangham JA, Prusinkiewicz P (2004) The genetics of geometry. Proc Natl Acad Sci USA 101:4728–4735

    Article  PubMed  CAS  Google Scholar 

  • Coen ES, Carpenter R (1993) The metamorphosis of flowers. Plant Cell 5:1175–1181

    Article  PubMed  Google Scholar 

  • Freeling M (1992) A conceptual framework for maize leaf development. Dev Biol 153:44–58

    Article  PubMed  CAS  Google Scholar 

  • Goldberg RB, Beals TP, Sanders PM (1993) Anther development: basic principles and practical applications. Plant Cell 5:1217–1229

    Article  PubMed  CAS  Google Scholar 

  • Kang HG, Seonghoe J, 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 

  • Kerr MK, Churchill GA (2001) Experimental design for gene expression microarrays. Biostatistics 2:183–201

    Article  PubMed  Google Scholar 

  • Koltunow AM, Truettner J, Cox KH, Wallroth M, Goldberg RB (1990) Different temporal and spatial gene expression patterns occur during anther development. Plant Cell 2:1201–1224

    Article  PubMed  CAS  Google Scholar 

  • Liang YK, Wang Y, Zhang Y, Li SG, Lu XC, Li H, Zou C, Xu ZH, Bai SN (2003) OsSET1, a novel SET-domain containing gene from rice. J Exp Bot 54:1995–1996

    Article  PubMed  CAS  Google Scholar 

  • Mao X, Cai T, Olyarchuk JG, Wei L (2005) Automated genome annotation and pathway identification using the KEGG Orthology (KO) as a controlled vocabulary. Bioinformatics 21:3787–3793

    Article  PubMed  CAS  Google Scholar 

  • McConnell JR, Barton MK (1998) Leaf polarity and meristem formation in Arabidopsis. Development 125:2935–2942

    PubMed  CAS  Google Scholar 

  • Nonomura K, Miyoshi K, Eiguchi M, Suzuki T, Miyao A, Hirochika H, Kurata N (2003) The MSP1 gene is necessary to restrict the number of cells entering into male and female sporogenesis and to initiate anther wall formation in rice. Plant Cell 15:1728–1739

    Article  PubMed  CAS  Google Scholar 

  • Poethig RS (1997) Leaf morphogenesis in flowering plants. Plant Cell 9:1077–1087

    Article  PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Sablowski RW, Meyerowitz EM (1998) A homolog of NO APICAL MERISTEM is an immediate target of the floral homeotic genes APETALA3/PISTILLATA. Cell 92:93–103

    Article  PubMed  CAS  Google Scholar 

  • Sachs T (1969) Regeneration experiments on the determination of the form of leaves. Israel J Bot 18:21–30

    Google Scholar 

  • Sanders PM, Bui AQ, Weterings K, McIntire KN, Hsu Y-C, Lee PY, Truong MT, Beals TP, Goldberg RB (1999) Anther developmental defects in Arabidopsis thaliana male-sterile mutants. Sex Plant Reprod 11:297–322

    Article  CAS  Google Scholar 

  • Sawa S, Watanabe K, Goto K, Liu YG, Shibata D, Kanaya E, Morita EH, Okada K (1999) FILAMENTOUS FLOWER, a meristem and organ identity gene of Arabidopsis, encodes a protein with a zinc finger and HMG-related domains. Genes Dev 13:1079–1088

    PubMed  CAS  Google Scholar 

  • Schiefthaler U, Balasubramanian S, Sieber P, Chevalier D, Wisman E, Schneitz K (1999) Molecular analysis of NOZZLE, a gene involved in pattern formation and early sporogenesis during sex organ development in Arabidopsis thaliana. Proc Natl Acad Sci USA 96:11664–11669

    Article  PubMed  CAS  Google Scholar 

  • Sorensen A, Guerineau F, Canales-Holzeis C, Dickinson HG, Scott RJ (2002) A novel extinction screen in Arabidopsis thaliana identifies mutant plants defective in early microsporangial development. Plant J 29:581–594

    Article  PubMed  CAS  Google Scholar 

  • Sussex IM (1955b) Morphogenesis in Solanum tuberosem L: experimental investigation of leaf dorsiventrality and orientation in the juvenile shoot. Phytomorphology 5:286–300

    Google Scholar 

  • Sussex IM (1955a) Morphogenesis in Solanum tuberosum L: apical structure and developmental pattern of the juvenile shoot. Phytomorphology 5:253–273

    Google Scholar 

  • Tsukaya H (2003) Organ shape and size: a lesson from studies of leaf morphogenesis. Curr Opin Plant Biol 6:57–62

    Article  PubMed  Google Scholar 

  • Waites R, Hudson A (1995) phantastica: a gene required for dorsoventrality of leaves in Antirrhinum majus. Development 121:2143–2153

    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 

  • Yang M, Wardzala E, Johal GS, Gray J (2004) The wound-inducible Lls1 gene from maize is an orthologue of the Arabidopsis Acd1 gene, and the LLS1 protein is present in non-photosynthetic tissues. Plant Mol Biol 54:175–91

    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 WC, Ye D, Xu J, Sundaresan V (1999) The SPOROCYTELESS gene of Arabidopsis is required for initiation of sporogenesis and encodes a novel nuclear protein. Genes Dev 13:2108–2117

    PubMed  CAS  Google Scholar 

  • Zhao DZ, Wang GF, Speal B, Ma H (2002) The excess microsporocytes1 gene encodes a putative leucine-rich repeat receptor protein kinase that controls somatic and reproductive cell fates in the Arabidopsis anther. Genes Dev 16:2021–2031

    Article  PubMed  CAS  Google Scholar 

  • Zik M, Irish VF (2003) Global identification of target genes regulated by APETALA3 and PISTILLATA floral homeotic gene action. Plant Cell 15:207–222

    Article  PubMed  CAS  Google Scholar 

  • Zimmermann P, Hirsch-Hoffmann M, Hennig L, Gruissem W (2004) GENEVESTIGATOR Arabidopsis microarray database and analysis toolbox. Plant Physiol 136:2621–2632

    Article  PubMed  CAS  Google Scholar 

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Correspondence to Shu-Nong Bai.

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Xiao-Chun Lu, Hua-Qin Gong contributed equally to this work.

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Lu, XC., Gong, HQ., Huang, ML. et al. Molecular analysis of early rice stamen development using organ-specific gene expression profiling. Plant Mol Biol 61, 845–861 (2006). https://doi.org/10.1007/s11103-006-0054-3

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