Putative cis-regulatory elements in genes highly expressed in rice sperm cells

BMC Research Notes

Mohan B Singh²  Prem L Bhalla²  Scott D Russell¹  Niharika Sharma² 

[1] Department of Botany and Microbiology, University of Oklahoma, Norman, OK 73019, USA;Plant Molecular Biology and Biotechnology Laboratory, Australian Research Council Centre of Excellence for Integrative Legume Research, Melbourne School of Land and Environment, University of Melbourne, Parkville, Victoria 3010, Australia

关键词: Oryza sativa;    gene expression;    male gamete;    plant reproduction;    cis-regulatory elements;   

Others  :  1167245
DOI  :  10.1186/1756-0500-4-319

 received in 2011-03-08, accepted in 2011-09-05,  发布年份 2011

【 摘 要 】

Background

The male germ line in flowering plants is initiated within developing pollen grains via asymmetric division. The smaller cell then becomes totally encased within a much larger vegetative cell, forming a unique "cell within a cell structure". The generative cell subsequently divides to give rise to two non-motile diminutive sperm cells, which take part in double fertilization and lead to the seed set. Sperm cells are difficult to investigate because of their presence within the confines of the larger vegetative cell. However, recently developed techniques for the isolation of rice sperm cells and the fully annotated rice genome sequence have allowed for the characterization of the transcriptional repertoire of sperm cells. Microarray gene expression data has identified a subset of rice genes that show unique or highly preferential expression in sperm cells. This information has led to the identification of cis-regulatory elements (CREs), which are conserved in sperm-expressed genes and are putatively associated with the control of cell-specific expression.

Findings

We aimed to identify the CREs associated with rice sperm cell-specific gene expression data using in silico prediction tools. We analyzed 1-kb upstream regions of the top 40 sperm cell co-expressed genes for over-represented conserved and novel motifs. Analysis of upstream regions with the SIGNALSCAN program with the PLACE database, MEME and the Mclip tool helped to find combinatorial sets of known transcriptional factor-binding sites along with two novel motifs putatively associated with the co-expression of sperm cell-specific genes.

Conclusions

Our data shows the occurrence of novel motifs, which are putative CREs and are likely targets of transcriptional factors regulating sperm cell gene expression. These motifs can be used to design the experimental verification of regulatory elements and the identification of transcriptional factors that regulate sperm cell-specific gene expression.

【 授权许可】

   
2011 Singh et al; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

Figure 3.

【 参考文献 】

• [1]Gou XP, Xu Y, Tang L, Yan F, Chen F: Representative cDNA library from isolated rice sperm cells. Act Bot Sin 2001, 43(10):1093-1096.
• [2]Borges F, Gomes G, Gardner R, Moreno N, McCormick S, Feijó JA, Becker JD: Comparative transcriptomics of Arabidopsis sperm cells. Plant Physiol 2008, 148(2):1168-1181.
• [3]Engel ML, Chaboud A, Dumas C, McCormick S: Sperm cells of Zea mays have a complex complement of mRNAs. Plant J 2003, 34(5):697-707.
• [4]Okada T, Bhalla PL, Singh MB: Expressed sequence tag analysis of Lilium longiflorum generative cells. Plant Cell Physiol 2006, 47(6):698-705.
• [5]Engel ML, Holmes-Davis R, McCormick S: Green sperm. Identification of male gamete promoters in Arabidopsis. Plant Physiol 2005, 138(4):2124-2133.
• [6]Riechmann JL, Heard J, Martin G, Reuber L, Jiang C, Keddie J, Adam L, Pineda O, Ratcliffe OJ, Samaha RR, Creelman R, Pilgrim M, Broun P, Zhang JZ, Ghandehari D, Sherman BK, Yu G: Arabidopsis transcription factors: genome-wide comparative analysis among eukaryotes. Science 2000, 290(5499):2105-2110.
• [7]Higo K, Ugawa Y, Iwamoto M, Korenaga T: Plant cis-acting regulatory DNA elements (PLACE) database. Nucleic Acids Res 1999, 27(1):297-300.
• [8]Prestridge DS: SIGNAL SCAN: A computer program that scans DNA sequences for eukaryotic transcriptional elements. Comput Appl Biosci 1991, 7(2):203-206.
• [9]Bailey TL, Williams N, Misleh C, Li WW: MEME: discovering and analyzing DNA and protein sequence motifs. Nucleic Acids Res 2006, (34 Web server):W369-W373.
• [10]Gou X, Yuan T, Wei X, Russell SD: Gene expression in the dimorphic sperm cells of Plumbago zeylanica: transcript profiling, diversity, and relationship to cell type. Plant J 2009, 60(1):33-47.
• [11]Mori T, Kuroiwa H, Higashiyama T, Kuroiwa T: GENERATIVE CELL SPECIFIC 1 is essential for angiosperm fertilization. Nat Cell Biol 2006, 8(1):64-71.
• [12]Borges F, Pereira PA, Slotkin RK, Martienssen RA, Becker JD: MicroRNA activity in Arabidopsis male germline. J Exp Bot 2011, 62(5):1611-1620.
• [13]Gowik U, Burscheidt J, Akyildiz M, Schlue U, Koczor M, Streubel M, Westhoff P: cis-Regulatory elements for mesophyll-specific gene expression in the C4 plant Flaveria trinervia the promoter of the C4 phosphoenolpyruvate carboxylase gene. Plant Cell 2004, 16(5):1077-1090.
• [14]Yanagisawa S, Schmidt RJ: Diversity and similarity among recognition sequences of Dof transcription factors. Plant J 1999, 17(2):209-214.
• [15]Yanagisawa S: Dof1 and Dof2 transcription factors are associated with expression of multiple genes involved in carbon metabolism in maize. Plant J 2000, 21(3):281-288.
• [16]Sakai H, Aoyama T, Oka A: Arabidopsis ARR1 and ARR2 response regulators operate as transcriptional activators. Plant J 2000, 24(6):703-711.
• [17]Ross EJ, Stone JM, Elowsky CG, Arredondo-Peter R, Klucas RV, Sarath G: Activation of the Oryza sativa non-symbiotic haemoglobin-2 promoter by the cytokinin-regulated transcription factor, ARR1. J Exp Bot 2004, 55(403):1721-1731.
• [18]Shirsat A, Wilford N, Croy R, Boulter D: Sequences responsible for the tissue specific promoter activity of a pea legumin gene in tobacco. Mol Gen Genet 1989, 215(2):326-331.
• [19]Reyes JC, Muro-Pastor MI, Florencio FJ: The GATA family of transcription factors in Arabidopsis and rice. Plant Physiol 2004, 134(4):1718-1732.
• [20]Priest HD, Filichkin SA, Mockler TC: Cis-regulatory elements in plant cell signalling. Curr Opin Plant Biol 2009, 12(5):643-649.
• [21]Lam E, Chua NH: ASF-2: a factor that binds to the cauliflower mosaic virus 35S promoter and a conserved GATA motif in Cab promoters. Plant Cell 1989, 1(12):1147-1156.
• [22]Villain P, Mache R, Zhou DX: The mechanism of GT element-mediated cell type-specific transcriptional control. J Biol Chem 1996, 271(51):32593-32598.
• [23]Le Gourrierec J, Li YF, Zhou DX: Transcriptional activation by Arabidopsis GT-1 may be through interaction with TFIIA-TBP-TATA complex. Plant J 1999, 18(6):663-668.
• [24]Zhou DX: Regulatory mechanism of plant gene transcription by GT-elements and GT-factors. Trends Plant Sci 1999, 4(6):210-214.
• [25]Rogers HJ, Bate N, Combe J, Sullivan J, Sweetman J, Swan C, Lonsdale DM, Twell D: Functional analysis of cis-regulatory elements within the promoter of the tobacco late pollen gene g10. Plant Mol Biol 2001, 45(5):577-585.
• [26]Elmayan T, Tepfer M: Evaluation in tobacco of the organ specificity and strength of the rolD promoter, domain A of the 35S promoter and the 35S2 promoter. Transgenic Res 1995, 4(6):388-3896.
• [27]Zhang ZL, Xie Z, Zou X, Casaretto J, Ho TH, Shen QJ: A rice WRKY gene encodes a transcriptional repressor of the gibberellin signaling pathway in aleurone cells. Plant Physiol 2004, 134(4):1500-1513.
• [28]Eulgem T, Rushton PJ, Schmelzer E, Hahlbrock K, Somssich IE: Early nuclear events in plant defence signalling: rapid gene activation by WRKY transcription factors. The EMBO J 1999, 18(17):4689-4699.
• [29]Eulgem T, Rushton PJ, Robatzek S, Somssich IE: The WRKY superfamily of plant transcription factors. Trends Plant Sci 2000, 5(5):199-206.
• [30]Xie Z, Zhang ZL, Zou X, Huang J, Ruas P, Thompson D, Shen QJ: Annotations and functional analyses of the rice WRKY gene superfamily reveal positive and negative regulators of abscisic acid signaling in aleurone cells. Plant Physiol 2005, 137(1):176-189.
• [31]Stålberg K, Ellerstöm M, Ezcurra I, Ablov S, Rask L: Disruption of an overlapping E-box/ABRE motif abolished high transcription of the napA storage-protein promoter in transgenic Brassica napus seeds. Planta 1996, 199(4):515-519.
• [32]Hartmann U, Sagasser M, Mehrtens F, Stracke R, Weisshaar B: Differential combinatorial interactions of cis-acting elements recognized by R2R3-MYB, BZIP, and BHLH factors control light-responsive and tissue-specific activation of phenylpropanoid biosynthesis genes. Plant Mol Biol 2005, 57(2):155-171.
• [33]Abe H, Urao T, Ito T, Seki M, Shinozaki K, Yamaguchi-Shinozaki K: Arabidopsis AtMYC2 (bHLH) and AtMYB2 (MYB) function as transcriptional activators in abscisic acid signalling. Plant Cell 2003, 15(1):63-78.
• [34]Chinnusamy V, Ohta M, Kanrar S, Lee BH, Hong X, Agarwal M, Zhu JK: ICE1: a regulator of cold-induced transcriptome and freezing tolerance in Arabidopsis. Genes Dev 2003, 17(8):1043-1054.
• [35]Quinn JM, Barraco P, Eriksson M, Merchant S: Coordinate copper- and oxygen-responsive Cyc6 and Cpx1 expression in Chlamydomonas is mediated by the same element. J Biol Chem 2000, 275(9):6080-6089.
• [36]Filichkin SA, Leonard JM, Monteros A, Liu PP, Nonogaki H: A novel endo-beta-mannanase gene in tomato LeMAN5 is associated with anther and pollen development. Plant Physiol 2004, 134(3):1080-1087.
• [37]Urao T, Yamaguchi-Shinozaki K, Urao S, Shinozaki K: An Arabidopsis myb homolog is induced by dehydration stress and its gene product binds to the conserved MYB recognition sequence. Plant Cell 1993, 5(11):1529-1539.
• [38]Lüscher B, Eisenman RN: New light on Myc and Myb. Part II. Myb. Genes Dev 1990, 4(12):2235-2241.
• [39]Luo H, Song F, Goodman RM, Zheng Z: Up-regulation of OsBIHD1, a rice gene encoding BELL homeodomain transcriptional factor, in disease resistance responses. Plant Biol 2005, 7(5):459-468.
• [40]Wenkel S, Turck F, Singer K, Gissot L, Le Gourrierec J, Samach A, Coupland G: CONSTANS and the CCAAT box binding complex share a functionally important domain and interact to regulate flowering of Arabidopsis. Plant Cell 2006, 18(11):2971-2984.
• [41]Haralampidis K, Milioni D, Rigas S, Hatzopoulos P: Combinatorial interaction of cis elements specifies the expression of the Arabidopsis AtHsp90-1 gene. Plant Physiol 2002, 129(3):1138-1149.
• [42]Kagaya Y, Ohmiya K, Hattori T: RAV1, a novel DNA-binding protein, binds to bipartite recognition sequence through two distinct DNA-binding domains uniquely found in higher plants. Nucleic Acids Res 1999, 27(2):470-478.
• [43]Riechmann JL, Meyerowitz EM: The AP2/EREBP family of plant transcription factors. Biol Chem 1998, 379(6):633-646.
• [44]Hatorangan MR, Sentausa E, Wijaya GY: In silico identification of cis-regulatory elements of phosphate transporter genes in rice (Oryza sativa L.). J Crop Sci Biotechnol 2009, 12(1):25-30.
• [45]Cohn B, Manque P, Lara AM, Serrano M, Sheth N, Buck G: Putative cis-regulatory elements associated with heat shock genes activated during excystation of Cryptosporidium parvum. PLoS One 2010, 5(3):e9512.
• [46]Frickey T, Weiller G: Mclip: motif detection based on cliques of gapped local profile-to-profile alignments. Bioinformatics 2007, 23(4):502-503.