IN SILICO ANALYSIS OF TRANSCRIPTION FACTOR BINDING SITES IN PROMOTERS OF GERMIN-LIKE PROTEIN GENES IN RICE
Abstract
Germins (GERs) and germin-like proteins (GLPs) play important roles in responses to various stresses; however, their function is still not fully understood. Significant insight into their function can be obtained by analyzing their promoters. In the present study, the 5' upstream promoters (1000 bp) of 43 Asian rice (Oryza sativa var. Japonica) GLP genes were retrieved from the Plant Ensemble, based on the Rice Annotation Project database (RAP-DB). Phylogenetic analysis via MEGA6 showed a narrow genetic background (0.2%) with a Tajima neutrality value (π) of 0.69. Overall, 4234 transcription factor (TF) binding sites (TFBSs) were found on chromosomes 1, 2, 3, 4, 5, 8, 9, 11 and 12 via “MatInspector” from 90 different TF families using a total of 444. Common TFs and DiAlign analyses showed that Arabidopsis homeobox protein (AHBP), MYB-like proteins (MYBL) and vertebrate TATA-box-binding protein (VTBP) were the most abundant, common and evolutionarily conserved elements in the upstream region from 0 to -800. Finding their mutual interaction via Farmworker analysis uncovered three new cis-regulatory modules (VTBP_VTBP, MYBS_MYBS, and AHBP_VTBP), which appear to be decisive for OsGLPs regulation. In silico functional analysis via ModelInspector revealed 77 cis-regulatory modules, each comprised of two elements, among which DOFF_OPAQ_03 and GTBX_MYCL_01 were the most frequent and mostly found on chromosome 8 and 12, indicating that the combinatorial interaction of these elements has a fundamental role in various biological processes. The study revealed the importance of these elements in regulating the expression of OsGLPs that will help in predicting the role of these genes in various stresses and can have application in biotechnology.
Key words: TFBS; in silico; rice; germin-like proteins (GLPs); promoter
Received: November 16, 2015; Revised: January 12, 2016; Accepted: January 19, 2016; Published online: September 20, 2016
How to cite this article: Ilyas M, Naqvi SMS, Mahmood T. In silico analysis of transcription factor binding sites in promoters of germin-like protein genes in rice. Arch Biol Sci. 2016;68(4):863-76.
Downloads
References
Thompson E, Lane B. Relation of protein synthesis in imbibing wheat embryos to the cell-free translational capacities of bulk mRNA from dry and imbibing embryos. J Biol Chem. 1980;255(12):5965-70.
Banerjee J, Maiti MK. Functional role of rice germin-like protein1 in regulation of plant height and disease resistance. Biochem Bioph Res Co. 2010;394(1):178-83.
Barman AR, Banerjee J. Versatility of germin-like proteins in their sequences, expressions, and functions. Funct Integr Genomic. 2015;15(5):533-48.
Segarra CI, Casalongue CA, Pinedo ML, Ronchi VP, Conde RD. A germin-like protein of wheat leaf apoplast inhibits serine proteases. J Exp Bot. 2003;54(386):1335-41.
Davidson RM, Reeves PA, Manosalva PM, Leach JE. Germins: A diverse protein family important for crop improvement. Plant Sci. 2009;177(6):499-510.
Dunwell JM, Gibbings JG, Mahmood T, Saqlan Naqvi S. Germin and germin-like proteins: evolution, structure, and function. Crit Rev Plant Sci. 2008;27(5):342-75.
Park SH, Yi N, Kim YS, Jeong MH, Bang SW, Choi YD, Kim JK. Analysis of five novel putative constitutive gene promoters in transgenic rice plants. J Exp Bot. 2010;61(9):2459-67.
Cartharius K, Frech K, Grote K, Klocke B, Haltmeier M, Klingenhoff A, Frisch M, Bayerlein M, Werner T. MatInspector and beyond: Promoter analysis based on transcription factor binding sites. Bioinformatics. 2005;21(13):2933-42.
Zhao J, Wang J, An L, Doerge R, Chen ZJ, Grau CR, Meng J, Osborn TC. Analysis of gene expression profiles in response to Sclerotinia sclerotiorum in Brassica napus. Planta. 2007;227(1):13-24.
Chawade A, Bräutigam M, Lindlöf A, Olsson O, Olsson B. Putative cold acclimation pathways in Arabidopsis thaliana identified by a combined analysis of mRNA co-expression patterns, promoter motifs and transcription factors. BMC Genomics. 2007;8(1):304.
Yi J, Derynck MR, Chen L, Dhaubhadel S. Differential expression of CHS7 and CHS8 genes in soybean. Planta. 2010;231(3):741-53.
Ibraheem O, Botha CEJ, Bradley G. In silico analysis of cis-acting regulatory elements in 5′ regulatory regions of sucrose transporter gene families in rice (Oryza sativa Japonica) and Arabidopsis thaliana. Comput Biol Chem. 2010;34(5–6):268-83.
Yadav DK, Shukla D, Tuteja N. Rice heterotrimeric G-protein alpha subunit (RGA1): In silico analysis of the gene and promoter and its upregulation under abiotic stress. Plant Physiol Biochem. 2013;63:262-71.
Federico ML, Iñiguez-Luy FL, Skadsen RW, Kaeppler HF. Spatial and temporal divergence of expression in duplicated barley germin-like protein-encoding genes. Genetics. 2006;174(1):179-90.
Fan Z, Gu H, Chen X, Song H, Wang Q, Liu M, Qu LJ, Chen Z. Cloning and expression analysis of Zmglp1, a new germin-like protein gene in maize. Biochem Biophys Res Commun. 2005;331(4):1257-63.
Sassaki FT, Bravo JP, González ER, Maia IG. Expression pattern and promoter analysis of a Eucalyptus grandis germin-like gene. Plant Mol Biol Rep. 2014;33(1):12-21.
Mathieu M, Neutelings G, Hawkins S, Grenier E, David H. Cloning of a pine germin-like protein (GLP) gene promoter and analysis of its activity in transgenic tobacco Bright Yellow-2 cells. Physiol Plant. 2003;117(3):425-34.
Chen J-Y, Wen F-X, Chen X-J, Cheng X-Y, Xu H-X. Nucleotide Sequence of Promoter of Triticum aestivum Germin-like Protein 3. Mol Plant Breeding. 2005;3(6):901-2.
Himmelbach A, Liu L, Zierold U, Altschmied L, Maucher H, Beier F, Müller D, Hensel G, Heise A, Schützendübel A, Kumlehn J, Schweizer P. Promoters of the barley germin-like GER4 gene cluster enable strong transgene expression in response to pathogen attack. Plant Cell. 2010;22(3):937-52.
Yang L, Li T, Zhang S, Gao G, Yang C. Characterization of the GLP13 gene promoter in Arabidopsis thaliana. Biol Plantarum. 2013;57(2):231-7.
Ruiz-López N, Haslam RP, Venegas-Calerón M, Li T, Bauer J, Napier JA, Sayanova O. Enhancing the accumulation of omega-3 long chain polyunsaturated fatty acids in transgenic Arabidopsis thaliana via iterative metabolic engineering and genetic crossing. Transgenic Res. 2012;21(6):1233-43.
Yasmin T, Mahmood T, Hyder MZ, Akbar S, Naqvi SS. Cloning, sequencing and in silico analysis of germin-like protein gene 1 promoter from Oryza sativa L. ssp. indica. Pakistan J Bot. 2008;40(4):1627-34.
Mahmood T, Zeeshan Hyder M, Saqlan Naqvi S. Cloning and sequence analysis of germin-like protein gene 2 promoter from Oryza sativa L. ssp. indica. Mitochondrial DNA. 2007;18(1):26-32.
Mahmood T, Nazar N, Yasmin T, Abbasi BH, Ahmad M, Naqvi SMS. Comparative analysis of regulatory elements in different germin-like protein gene promoters. Afri J Biotechnol. 2010;9(13):1871-80.
Ali I, Mahmood T. Identification and analysis of regulatory elements in the germin and germin-like proteins family promoters in rice. Turk J Bot. 2015;39:389-400.
Mahmood T, Yasmin T, Haque MI, Naqvi SMS. Characterization of a rice germin-like protein gene promoter. Genet Mol Res. 2013;12(1):360-9.
Munir F, Hayashi S, Batley J, Naqvi SMS, Mahmood T. Germin-like protein 2 gene promoter from rice is responsive to fungal pathogens in transgenic potato plants. Funct Integr Genomics. 2016:16(1):19-27.
Yasmin T, Mahmood T, Hyder MZ, Akbar S, Naqvi SS. Cloning, sequencing and in silico analysis of germin-like protein gene-promoter from Oryza sativa L. ssp. indica. Pakistan J Bot. 2008;40(4):1627-34.
Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol. 2013;30(12):2725-9.
Frech K, Danescu-Mayer J, Werner T. A novel method to develop highly specific models for regulatory units detects a new LTR in GenBank which contains a functional promoter. J Mol Biol. 1997;270(5):674-87.
Kafri R, Levy M, Pilpel Y. The regulatory utilization of genetic redundancy through responsive backup circuits. National Acad Sciences. 2006;103(31):11653-8.
Ober D. Seeing double: Gene duplication and diversification in plant secondary metabolism. Trends Plant Sci. 2005;10(9):444-9.
Druka A, Kudrna D, Kannangara CG, von Wettstein D, Kleinhofs A. Physical and genetic mapping of barley (Hordeum vulgare) germin-like cDNAs. National Acad Sciences. 2002;99(2):850-5.
Manosalva PM, Davidson RM, Liu B, Zhu X, Hulbert SH, Leung H, Leach JE. A germin-like protein gene family functions as a complex quantitative trait locus conferring broad-spectrum disease resistance in rice. Plant Physiol. 2009;149(1):286-96.
Hsam S, Lapochkina I, Zeller F. Chromosomal location of genes for resistance to powdery mildew in common wheat (Triticum aestivum L. em Thell.). 8. Gene Pm32 in a wheat-Aegilops speltoides translocation line. Euphytica. 2003;133(3):367-70.
Zimmermann G, Bäumlein H, Mock H-P, Himmelbach A, Schweizer P. The multigene family encoding germin-like proteins of barley. Regulation and function in basal host resistance. Plant Physiol. 2006;142(1):181-92.
Lohmann JU, Hong RL, Hobe M, Busch MA, Parcy F, Simon R, Weigel D. A molecular link between stem cell regulation and floral patterning in Arabidopsis. Cell. 2001;105(6):793-803.
Gubler F, Jacobsen JV. Gibberellin-responsive elements in the promoter of a barley high-pI alpha-amylase gene. Plant Cell. 1992;4(11):1435-41.
Wang R, Guan P, Chen M, Xing X, Zhang Y, Crawford NM. Multiple regulatory elements in the Arabidopsis NIA1 promoter act synergistically to form a nitrate enhancer. Plant Physiol. 2010;154(1):423-32.
Diaz I, Vicente-Carbajosa J, Abraham Z, Martinez M, Isabel-La Moneda I, Carbonero P. The GAMYB protein from barley interacts with the DOF transcription factor BPBF and activates endosperm-specific genes during seed development. Plant J. 2002;29(4):453-64.
Guo M, Thomas J, Collins G, Timmermans MC. Direct repression of KNOX loci by the Asymmetric Leaves1 complex of Arabidopsis. Plant Cell. 2008;20(1):48-58.
Zhu Y, Cai XL, Wang ZY, Hong MM. An interaction between a MYC protein and an EREBP protein is involved in transcriptional regulation of the rice Wx gene. J Biol Chem. 2003;278(48):47803-11.
Rubio-Somoza I, Martinez M, Diaz I, Carbonero P. HvMCB1,a R1MYB transcription factor from barley with antagonistic regulatory functions during seed development and germination. Plant J. 2006;45(1):17-30.
Li L, Yu X, Thompson A, Guo M, Yoshida S, Asami T, Chory J, Yin Y. Arabidopsis MYB30 is a direct target of BES1 and cooperates with BES1 to regulate brassinosteroid-induced gene expression. Plant J. 2009;58(2):275-86.
Sriraman V, Eichenlaub-Ritter U, Bartsch JW, Rittger A, Mulders SM, Richards JS. Regulated expression of ADAM8 (a disintegrin and metalloprotease domain 8) in the mouse ovary: evidence for a regulatory role of luteinizing hormone, progesterone receptor, and epidermal growth factor-like growth factors. Bio Rep. 2008;78(6):1038-48.
Papp B, Pál C, Hurst LD. Evolution of cis-regulatory elements in duplicated genes of yeast. Trends in Genet. 2003;19(8):417-22.
Davidson R, Manosalva P, Snelling J, Bruce M, Leung H, Leach J. Rice germin-Like proteins: Allelic diversity and relationships to early stress responses. Rice. 2010;3(1):43-55.
Staiger D, Apel K, Trepp G. The Atger3 promoter confers circadian clock-regulated transcription with peak expression at the beginning of the night. Plant Mol Biol. 1999;40(5):873-82.
Gao MJ, Lydiate DJ, Li X, Lui H, Gjetvaj B, Hegedus DD, Rozwadowski K. Repression of seed maturation genes by a trihelix transcriptional repressor in Arabidopsis seedlings. Plant Cell. 2009;21(1):54-71.
Yoo CY, Pence HE, Jin JB, Miura K, Gosney MJ, Hasegawa PM, Mickelbart MV. The Arabidopsis GTL1 transcription factor regulates water use efficiency and drought tolerance by modulating stomatal density via transrepression of SDD1. Plant Cell. 2010;22(12):4128-41.
Xi J, Qiu Y, Du L, Poovaiah BW. Plant-specific trihelix transcription factor AtGT2L interacts with calcium/calmodulin and responds to cold and salt stresses. Plant Sci. 2012;186:274-80.
Ogo Y, Kobayashi T, Nakanishi Itai R, Nakanishi H, Kakei Y, Takahashi M, Toki S, Mori S, Nishizawa NK. A novel NAC transcription factor, IDEF2, that recognizes the iron deficiency-responsive element 2 regulates the genes involved in iron homeostasis in plants. J Biol Chem. 2008;283(19):13407-17.
Balazadeh S, Kwasniewski M, Caldana C, Mehrnia M, Zanor MI, Xue GP, Mueller-Roeber B. ORS1, an H2O2-responsive NAC transcription factor, controls senescence in Arabidopsis thaliana. Moleculer Plant. 2011;4(2):346-60.
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):155-71.
Girin T, Paicu T, Stephenson P, Fuentes S, Korner E, O'Brien M, Sorefan K, Wood TA, Balanzá V, Ferrándiz C, Smyth DR, Østergaard L. Indehiscent and Spatula interact to specify carpel and valve margin tissue and thus promote seed dispersal in Arabidopsis. Plant Cell. 2011;23(10):3641-53.
Walcher CL, Nemhauser JL. Bipartite promoter element required for auxin response. Plant Physiol. 2012;158(1):273-82.
Petit JM, van Wuytswinkel O, Briat JF, Lobreaux S. Characterization of an iron-dependent regulatory sequence involved in the transcriptional control of AtFer1 and ZmFer1 plant ferritin genes by iron. J Biol Chem. 2001;276(8):5584-90.
Nole-Wilson S, Krizek BA. DNA binding properties of the Arabidopsis floral development protein Aintegumenta. Nucleic Acids Res. 2000;28(21):4076-82.
McDonald WH, Ohi R, Smelkova N, Frendewey D, Gould KL. Myb-related fission yeast cdc5p is a component of a 40S snRNP-containing complex and is essential for pre-mRNA splicing. Mol Cell Biol. 1999;19(8):5352-62.
Chen A, Gu M, Sun S, Zhu L, Hong S, Xu G. Identification of two conserved cis-acting elements, MYCS and P1BS, involved in the regulation of mycorrhiza-activated phosphate transporters in eudicot species. New Phytol. 2011;189(4):1157-69.
Schneidereit A, Imlau A, Sauer N. Conserved cis-regulatory elements for DNA-binding-with-one-finger and homeo-domain-leucine-zipper transcription factors regulate companion cell-specific expression of the Arabidopsis thaliana Sucrose transporter 2 gene. Planta. 2008;228(4):651-62.
Kawakatsu T, Yamamoto MP, Hirose S, Yano M, Takaiwa F. Characterization of a new rice glutelin gene GluD-1 expressed in the starchy endosperm. J Exp Bot. 2008;59(15):4233-45.
Simpson SD, Nakashima K, Narusaka Y, Seki M, Shinozaki K, Yamaguchi-Shinozaki K. Two different novel cis-acting elements of erd1, a clpA homologous Arabidopsis gene function in induction by dehydration stress and dark-induced senescence. Plant J. 2003;33(2):259-70.
Zou X, Neuman D, Shen QJ. Interactions of two transcriptional repressors and two transcriptional activators in modulating gibberellin signaling in aleurone cells. Plant Physiol. 2008;148(1):176-86.
Ramireddy E, Brenner WG, Pfeifer A, Heyl A, Schmulling T. In planta analysis of a cis-regulatory cytokinin response motif in Arabidopsis and identification of a novel enhancer sequence. Plant Cell Physiol. 2013;54(7):1079-92.
Kawagoe Y, Campbell BR, Murai N. Synergism between CACGTG (G-box) and CACCTG cis-elements is required for activation of the bean seed storage protein beta-phaseolin gene. Plant J. 1994;5(6):885-90.
Gilmartin PM, Chua NH. Spacing between GT-1 binding sites within a light-responsive element is critical for transcriptional activity. Plant Cell. 1990;2(5):447-55.
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 signaling. Plant Cell. 2003;15(1):63-78.
Chen W, Chao G, Singh KB. The promoter of a H2O2-inducible, Arabidopsis glutathione S-transferase gene contains closely linked OBF- and OBP1-binding sites. Plant J. 1996;10(6):955-66.
Yamamoto MP, Onodera Y, Touno SM, Takaiwa F. Synergism between RPBF Dof and RISBZ1 bZIP activators in the regulation of rice seed expression genes. Plant Physiol. 2006;141(4):1694-707.
Lin T, Sharma P, Gonzalez DH, Viola IL, Hannapel DJ. The impact of the long-distance transport of a BEL1-like messenger RNA on development. Plant Physiol. 2013;161(2):760-72.
Downloads
Published
How to Cite
Issue
Section
License
Authors grant the journal right of first publication with the work simultaneously licensed under a Creative Commons Attribution 4.0 International License that allows others to share the work with an acknowledgment of the work’s authorship and initial publication in this journal.