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Acta Agron Sin ›› 2012, Vol. 38 ›› Issue (09): 1570-1582.doi: 10.3724/SP.J.1006.2012.01570

• CROP GENETICS & BREEDING · GERMPLASM RESOURCES · MOLECULAR GENETICS • Previous Articles     Next Articles

Genome-Wide Identification, Classification, and Expression of NF-YB Gene Family in Soybean

ZHENG Wei-Jun1,2,XU Zhao-Shi2,*,FENG Zhi-Juan2,LI Lian-Cheng2,CHEN Ming2,CHAI Shou-Cheng1,MA You-Zhi2   

  1. 1 College of Agronomy, Northwest A & F University, Yangling 712100, China; 2 Institute of Crop Sciences, Chinese Academy of Agricultural Sciences / National Key Facility for Crop Gene Resources and Genetic Improvement, Key Laboratory of Crop Genetics and Breeding of Ministry of Agriculture, Beijing 100081, China
  • Received:2012-02-17 Revised:2012-04-16 Online:2012-09-12 Published:2012-07-03
  • Contact: 徐兆师, E-mail: xuzhaoshi@yahoo.com.cn, Tel: 010-82106773; 柴守诚, E-mail: chaishoucheng@126.com, Tel: 029-87082205

Abstract: Based on soybean genome database and bioinformatics method, we obtained soybean NF-YB family genes and their positions on chromosome and duplication information. NF-YB proteins were classified according to their phylogenetic relationship. The soybean RNA-sequencing data from the SoyBase database and EST data from NCBI UniGene were used to analyze the expression pattern of these genes at different development stages. A total of 28 NF-YB genes were systematically identified from soybean and classified into three types. They were located on 14 chromosomes and most of them had stress related cis-acting elements in their promoter regions. Ten differentially expressed genes were found at each developmental stage, and four of them were highly expressed in different tissues other than root nodules and root. Among other six genes, two were highly expressed in root nodule, two were specifically expressed in root nodules and two were specifically expressed in root. The results facilitate functional analysis and utilization of NF-YB genes in crop genetic improvement.

Key words: NF-YB, Genome-wide identification, Phylogeny, Differential expression, Promoter

[1]Gelinas R, Endlich B, Pfeiffer C, Yagi M, Stamatoyannopoulos G. G to A substitution in the distal CCAAT box of the A gamma-globin gene in Greek hereditary persistence of fetal haemoglobin. Nature, 1985, 313: 323-325

[2]Mantovani R. A survey of 178 NF-Y binding CCAAT boxes. Nucl Acids Res, 1998, 26: 1135-1143

[3]Bucher P. Weight matrix descriptions of four eukaryotic RNA polymerase II promoter elements derived from 502 unrelated promoter sequences. J Mol Biol, 1990, 212: 563-578

[4]Forsburg S L, Guarente L. Mutational analysis of upstream activation sequence 2 of the CYC1 gene of Saccharomyces cerevisiae: a HAP2-HAP3-responsive site. Mol Cell Biol, 1988, 8: 647-654

[5]Maity S N, de Crombrugghe B. Role of the CCAAT-binding protein CBF/NF-Y in transcription. Trends Biochem Sci, 1998, 23: 174-178

[6]Mantovani R. The molecular biology of the CCAAT-binding factor NF-Y. Gene, 1999, 239: 15-27

[7]Mazon M J, Gancedo J M, Gancedo C. Phosphorylation and inactivation of yeast fructose-bisphosphatase in vivo by glucose and by proton ionophores. A possible role for cAMP. Eur J Biochem, 1982, 127: 605-608

[8]Pinkham J L, Guarente L. Cloning and molecular analysis of the HAP2 locus: a global regulator of respiratory genes in Saccharomyces cerevisiae. Mol Cell Biol, 1985, 5: 3410-3416

[9]Dang V D, Bohn C, Bolotin-Fukuhara M, Daignan-Fornier B. The CCAAT box-binding factor stimulates ammonium assimilation in Saccharomyces cerevisiae, defining a new cross-pathway regulation between nitrogen and carbon metabolisms. J Bacteriol, 1996, 178: 1842-1849

[10]Gancedo J M. Yeast carbon catabolite repression. Microbiol Mol Biol Rev, 1998, 62: 334-361

[11]Gusmaroli G, Tonelli C, Mantovani R. Regulation of the CCAAT-Binding NF-Y subunits in Arabidopsis thaliana. Gene, 2001, 264: 173-185

[12]Gusmaroli G, Tonelli C, Mantovani R. Regulation of novel members of the Arabidopsis thaliana CCAAT-binding nuclear factor Y subunits. Gene, 2002, 283: 41-48

[13]Meinke D. A homeotic mutant of Arabidopsis thaliana with leafy cotyledons. Science, 1992, 258: 1647-1650

[14]Meinke D W, Franzmann L H, Nickle T C, Yeung E C. Leafy cotyledon mutants of Arabidopsis. Plant Cell, 1994, 6: 1049-1064

[15]Lotan T, Ohto M, Yee K M, West M A, Lo R, Kwong R W, Yamagishi K, Fischer R L, Goldberg R B, Harada J J. Arabidopsis LEAFY COTYLEDON1 is sufficient to induce embryo development in vegetative cells. Cell, 1998, 93: 1195-1205

[16]Vicient C M, Bies-Etheve N, Delseny M. Changes in gene expression in the leafy cotyledon1 (lec1) and fusca3 (fus3) mutants of Arabidopsis thaliana. J Exp Bot, 2000, 51: 995-1003

[17]Kwong R W, Bui A Q, Lee H, Kwong L W, Fischer R L, Goldberg R B, Harada J J. LEAFY COTYLEDON1-LIKE defines a class of regulators essential for embryo development. Plant Cell, 2003, 15: 5-18

[18]Cai X, Ballif J, Endo S, Davis E, Liang M, Chen D, De Wald D, Kreps J, Zhu T, Wu Y. A putative CCAAT-binding transcription factor is a regulator of flowering timing in Arabidopsis. Plant Physiol, 2007, 145: 98-105

[19]Chen N Z, Zhang X Q, Wei P C, Chen Q J, Ren F, Chen J, Wang X C. AtHAP3b plays a crucial role in the regulation of flowering time in Arabidopsis during osmotic stress. J Biochem Mol Biol , 2007, 40: 1083-1089

[20]Li W X, Oono Y K, Zhu J H, He X J, Wu J M, Iida K, Lu X Y, Cui X P, Jin H L, Zhu J K. The Arabidopsis NFYA5 transcription factor is regulated transcriptionally and posttranscriptionally to promote drought resistance. Plant Cell, 2008, 20: 2238-2251

[21]Nelson D E, Repetti P P, Adams T R, Creelman R A, Wu J, Warner D C, Anstrom D C, Bensen R J, Castiglioni P P, Donnarummo M G, Hinchey B S, Kumimoto R W, Maszle D R, Canales R D, Krolikowski K A, Dotson S B, Gutterson N, Ratcliffe O J, Heard J E. Plant nuclear factor Y (NF-Y) B subunits confer drought tolerance and lead to improved corn yields on water-limited acres. Proc Natl Acad Sci USA, 2007, 104: 16450-16455

[22]Hu H, Dai M, Yao J, Xiao B, Li X, Zhang Q, Xiong L. Overexpressing a NAM, ATAF, and CUC (NAC) transcription factor enhances drought resistance and salt tolerance in rice. Proc Natl Acad Sci USA, 2006, 103: 12987-12992

[23]Xiao B Z, Chen X, Xiang C B, Tang N, Zhang Q F, Xiong L Z. Evaluation of seven function-known candidate genes for their effects on improving drought resistance of transgenic rice under field conditions. Mol Plant, 2009, 2: 73-83

[24]Schmutz J, Cannon S B, Schlueter J, Ma J, Mitros T, Nelson W, Hyten DL, Song Q, Thelen J J, Cheng J, Xu D, Hellsten U, May G D, Yu Y, Sakurai T, Umezawa T, Bhattacharyya M K, Sandhu D, Valliyodan B, Lindquist E, Peto M, Grant D, Shu S, Goodstein D, Barry K, Futrell-Griggs M, Abernathy B, Du J, Tian Z, Zhu L, Gill N, Joshi T, Libault M, Sethuraman A, Zhang X C, Shinozaki K, Nguyen H T, Wing R A, Cregan P, Specht J, Grimwood J, Rokhsar D, Stacey G, Shoemaker R C, Jackson S A. Genome sequence of the palaeopolyploid soybean. Nature, 2010, 463: 178-183

[25]Siefers N, Dang K K, Kumimoto R W, Bynum W E, Tayrose G, Holt B F. Tissue-specific expression patterns of Arabidopsis NF-Y transcription factors suggest potential for extensive combinatorial complexity. Plant Physiol, 2009, 149: 625-641

[26]Huala E, Dickerman A W, Garcia-Hernandez M, Weems D, Reiser L, LaFond F, Hanley D, Kiphart D, Zhuang M, Huang W, Mueller L A, Bhattacharyya D, Bhaya D, Sobral B W, Beavis W, Meinke D W, Town C D, Somerville C, Rhee S Y. The Arabidopsis information resource (TAIR): a comprehensive database and web-based information retrieval, analysis, and visualization system for a model plant. Nucl Acids Res , 2001, 29: 102-105

[27]Ouyang S, Zhu W, Hamilton J, Lin H, Campbell M, Childs K, Thibaud-Nissen F, Malek R L, Lee Y, Zheng L, Orvis J, Haas B, Wortman J, Buell C R. The TIGR rice genome annotation resource: improvements and new features. Nucl Acids Res, 2007, 35(database issue): D883-D887

[28]Zhang H, Jin J P, Tang L, Zhao Y, Gu X C, Gao G, Luo J C. PlantTFDB 2.0: update and improvement of the comprehensive plant transcription factor database. Nucl Acids Res, 2011, 39: D1114-D1117

[29]Finn R D, Mistry J, Schuster-Bockler B, Griffiths-Jones S, Hollich V, Lassmann T, Moxon S, Marshall M, Khanna A, Durbin R, Eddy S R, Sonnhammer E L L, Bateman A. Pfam: clans, web tools and services. Nucl Acids Res, 2006, 34(database issue): D247-D251

[30]Guo A-Y(郭安源), Zhu Q-H(朱其惠), Chen X(陈新), Luo J-C(罗静初). GSDS: A gene structure display server. Hereditas (Beijing) (遗传), 2007, 29(8): 1023-1026 (in Chinese with Enlish abstract)

[31]Tamura K, Dudley J, Nei M, Kumar S. MEGA4: Molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol and Evol, 2007, 24: 1596-1599

[32]MapInspect software. [2012-03-12] http://www.plantbreeding.wur.nl/UK/software_mapinspect.html

[33]Yang S, Zhang X, Yue J X, Tian D, Chen J Q: Recent duplications dominate NBS-encoding gene expansion in two woody species. Mol Genet Genom, 2008, 280: 187-198

[34]Jain M, Nijhawan A, Arora R, Agarwal P, Ray S, Sharma P, Kapoor S, Tyagi A K, Khurana J P. 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, 2007, 143: 1467-1483

[35]Thirumurugan T, Ito Y, Kubo T, Serizawa A, Kurata N. Identification, characterization and interaction of HAP family genes in rice. Mol Genet Genom, 2008, 279: 279-289

[36]Heikoff S, Greene E A, Pietrokovski S, Bork P, Attwood T K, Hood L. Gene families: the taxonomy of protein paralogs and chimeras. Science,1997, 278: 609-614

[37]Schlueter J A, Dixon P, Granger C, Grant D, Clark L, Doyle J J, Shoemaker R C. Mining EST databases to resolve evolutionary events in major crop species. Genome, 2004, 47: 868-876

[38]Blanc G, Barakat A, Guyot R, Cooke R, Delseny M. Extensive duplication and reshuffling in the Arabidopsis genome. Plant Cell, 2000, 12: 1093-1101

[39]Wang X, Shi X, Hao B, Ge S, Luo J. Duplication and DNA segmental loss in the rice genome: implications for diploidization. New Phytol, 2005, 165: 937-946

[40]Blanc G, Wolfe K H. Wide spread palepolyploidy in model plant species inferred from age distributions of duplicate genes. Plant Cell, 2004, 16: 1667-1678

[41]Zhaxybayeva O, Gogarten J P. Spliceosomal introns: new insights into their evolution. Curr Biol, 2003, 13: R764-R766

[42]Romier C, Cocchiarella F, Mantovani R, Moras D. The NF-YB/NF-YC structure gives insight into DNA binding and transcription regulation by CCAAT factor NF-Y. J Biol Chem, 2003, 10, 278: 1336-1345

[43]Lynch M, Conery J S. The evolutionary fate and consequences of duplicate genes. Science, 2000, 290: 1151-1155

[44]Le D T, Nishiyama R, Watanabe Y, Mochida K, Yamaguchi-Shinozaki K, Shinozaki K, Tran L S. Genome-wide survey and expression analysis of the plant-specific NAC transcription factor family in soybean during development dand dehydration stress DNA Res, 2011, 18: 263-276

[45]Riechmann J L, Heard J, Martin G, Reuber L, Jiang C, Keddie J, Adam L, Pineda O, Ratcliffe O J, Samaha R R, Creelman R, Pilgrim M, Broun P, Zhang J Z, Ghandehari D, Sherman B K, Yu G. Arabidopsis transcription factors: genome-wide comparative analysis among eukaryotes. Science, 2000, 290: 2105-2110

[46]Kim S, Na J G, Hampsey M, Reinberg D. The Dr1/DRAP1 heterodimer is a global repressor of transcription in vivo. Proc Natl Acad Sci USA, 1997, 94(3): 820-825

[47]Kang J Y, Choi H I, Im M Y, Kim S Y. Arabidopsis basic leucine zipper proteins that mediate stress-responsive abscisic acid signaling. Plant Cell, 2002, 14: 343-357

[48]Gong W, He K, Covington M, Dinesh-Kumar S P, Snyder M, Harmer S L, Zhu Y X, Deng X W. The development of protein microarrays and their applications in DNA-protein and protein-protein interaction analyses of Arabidopsis transcription factors. Mol Plant, 2008, 1: 27-41

[49]Hughes M A, Dunn M A. The molecular biology of plant acclimation to low temperature. J Exp Bot, 1996, 47: 291-305

[50]Yamamoto A, Mizukami Y, Sakurai H. Identification of a novel class of target genes and a novel type of binding sequence of heat shock transcription factor in Saccharomyces cerevisiae. J Biol Chem, 2005, 280: 11911-11919

[51]Marta R, Christiane V, Francesca F, Giraudat J, Jeffrey L. The genetics of adaptive responses to drought stress: abscisic acid dependent and abscisic acid-independent signaling component. Physiol Plant, 2005, 123: 111-119

[52]Shen Q, Zhang P, Ho T H. Modular nature of abscisic acid (ABA) response complexes: composite promoter units that are necessary and sufficient for ABA induction of gene expression in barley. Plant Cell, 1996, 8: 1107-1119

[53]Narusaka Y, Nakashima K, Shinwari Z K, Sakuma Y, Furihata T, Abe H, Narusaka M, Shinozaki K, Yamaguchi-Shinozaki K. Interaction between two cis-acting elements, ABRE and DRE, in ABA-dependent expression of Arabidopsis rd29A gene in response to dehydration and high-salinity stresses. Plant J, 2003, 34: 137-148

[54]Shinozaki K, Yamaguchi-Shinozaki K. Molecular responses to dehydration and low temperature: differences and cross-talk between two stress signaling pathways. Curr Opin Plant Biol, 2000, 3: 217-223

[55]Jeong J S, Kim Y S, Baek K H, Jung H, Ha S H, Do Choi Y, Kim M, Reuzeau C, Kim J K. Root-specific expression of OsNAC10 improves drought tolerance and grain yield in rice under field drought conditions. Plant Physiol, 2010, 153: 185-197

[56]Takeuchi K, Gyohda A, Tominaga M, Kawakatsu M, Hatakeyama A, Ishii N, Shimaya K, Nishimura T, Riemann M, Nick P, Hashimoto M, Komano T, Endo A, Okamoto T, Jikumaru Y, Kamiya Y, Terakawa T, Koshiba T. RSOsPR10 expression in response to environmental stresses is regulated antagonistically by jasmonate/ethylene and salicylic acid signaling pathways in rice roots. Plant Cell Physiol, 2011, 52: 1686-1696

[57]Stephenson T J, McIntyre C L, Collet C, Xue G P. Genome-wide identification and expression analysis of the NF-Y family of transcription factors in Triticum aestivum. Plant Mol Biol, 2007, 65: 77-92
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