Identification and expression analyses of calmodulin-binding transcription activator genes in soybean

Plant and Soil

Volumn 386, Issue 1-2, 2014, Pages 205-221

  Wang, Guoping ^a   Zeng, Houqing ^a   Hu, Xiaoyan ^a   Zhu, Yiyong ^b   Chen, Yang ^a   Shen, Chenjia ^a   Wang, Huizhong ^a   Poovaiah, B W ^c   Du, Liqun ^a,c  

^a HANGZHOU NORMAL UNIVERSITY   (China)

^b NANJING AGRICULTURAL UNIVERSITY   (China)

^c WASHINGTON STATE UNIVERSITY   (United States)

Author keywords

Biotic and abiotic stress; Ca2+ Calmodulin; Calmodulin binding transcription activator (CAMTA); cis element; Soybean (Glycine max); Transcriptional regulation

Indexed keywords

CALCIUM; ENVIRONMENTAL STRESS; GENE EXPRESSION; ION; PHOSPHORUS; PROTEIN; SOIL NITROGEN; SOYBEAN;

ANIMALIA; ARABIDOPSIS; FUNGI; GLYCINE MAX; HEXAPODA;

EID: 84919643602     PISSN: 0032079X     EISSN: 15735036     Source Type: Journal    
DOI: 10.1007/s11104-014-2267-6     Document Type: Article

References (70)

1. Bari R, Jones JD (2009) Role of plant hormones in plant defence responses. Plant Mol Biol 69:473–488
2. Batistič O, Kudla J (2012) Analysis of calcium signaling pathways in plants. BBA-Gen Subj 1820:1283–1293
3. Bouche N, Scharlat A, Snedden W, Bouchez D, Fromm H (2002) A novel family of calmodulin-binding transcription activators in multicellular organisms. J Biol Chem 277:21851–21861
4. Bouche N, Yellin A, Snedden WA, Fromm H (2005) Plant-specific calmodulin-binding proteins. Annu Rev Plant Biol 56:435–466
5. Chen L, Song Y, Li S, Zhang L, Zou C, Yu D (2012) The role of WRKY transcription factors in plant abiotic stresses. BBA-Gene Regul Mech 1819:120–128
6. Choi MS, Kim MC, Yoo JH, Moon BC, Koo SC, Park BO, Lee JH, Koo YD, Han HJ, Lee SY, Chung WS, Lim CO, Cho MJ (2005) Isolation of a calmodulin-binding transcription factor from rice (Oryza sativa L.). J Biol Chem 280:40820–40831
7. 2+ sensors in plant signalling. Biochem J 425:27–40
8. Dodd AN, Kudla J, Sanders D (2010) The language of calcium signaling. Annu Rev Plant Biol 61:593–620
9. Doherty CJ, Van Buskirk HA, Myers SJ, Thomashow MF (2009) Roles for Arabidopsis CAMTA transcription factors in cold-regulated gene expression and freezing tolerance. Plant Cell 21:972–984
10. 2+/calmodulin-binding proteins involved in transcriptional regulation: interaction with fsh/Ring3 class transcription activators. Plant Mol Biol 54:549–569
11. 2+/calmodulin is critical for brassinosteroid biosynthesis and plant growth. Nature 437:741–745
12. 2+/calmodulin regulates salicylic-acid-mediated plant immunity. Nature 457:1154–1158
13. Du L, Yang T, Puthanveettil SV, Poovaiah BW (2011) Decoding of calcium signal through calmodulin: calmodulin-binding proteins in plants. In: Luan S (ed) Coding and decoding of calcium signals in plants. Springer, Berlin, pp 177–233
14. Fan XD, Wang JQ, Yang N, Dong YY, Liu L, Wang FW, Wang N, Chen H, Liu WC, Sun YP, Wu JY, Li HY (2013) Gene expression profiling of soybean leaves and roots under salt, saline-alkali and drought stress by high-throughput Illumina sequencing. Gene 512:392–402
15. Finkler A, Ashery-Padan R, Fromm H (2007) CAMTAs: calmodulin-binding transcription activators from plants to human. Febs Lett 581:3893–3898
16. Galon Y, Nave R, Boyce JM, Nachmias D, Knight MR, Fromm H (2008) Calmodulin-binding transcription activator (CAMTA) 3 mediates biotic defense responses in Arabidopsis. Febs Lett 582:943–948
17. Galon Y, Aloni R, Nachmias D, Snir O, Feldmesser E, Scrase-Field S, Boyce JM, Bouche N, Knight MR, Fromm H (2010a) Calmodulin-binding transcription activator 1 mediates auxin signaling and responds to stresses in Arabidopsis. Planta 232:165–178
18. Galon Y, Finkler A, Fromm H (2010b) Calcium-regulated transcription in plants. Mol Plant 3:653–669
19. Guo AY, Zhu QH, Chen X, Luo JC (2007) GSDS: a gene structure display server. Yi Chuan 29:1023–1026
20. Han J, Gong P, Reddig K, Mitra M, Guo P, Li HS (2006) The fly CAMTA transcription factor potentiates deactivation of rhodopsin, a G protein-coupled light receptor. Cell 127:847–858
21. Hobo T, Asada M, Kowyama Y, Hattori T (1999) ACGT-containing abscisic acid response element (ABRE) and coupling element 3 (CE3) are functionally equivalent. Plant J 19:679–689
22. Hoth S, Morgante M, Sanchez JP, Hanafey MK, Tingey SV, Chua NH (2002) Genome-wide gene expression profiling in Arabidopsis thaliana reveals new targets of abscisic acid and largely impaired gene regulation in the abi1-1 mutant. J Cell Sci 115:4891–4900
23. Iwasaki T, Yamaguchi-Shinozaki K, Shinozaki K (1995) Identification of a cis-regulatory region of a gene in Arabidopsis thaliana whose induction by dehydration is mediated by abscisic acid and requires protein synthesis. Mol Gen Genet 247:391–398
24. Jian B, Liu B, Bi Y, Hou W, Wu C, Han T (2008) Validation of internal control for gene expression study in soybean by quantitative real-time PCR. BMC Mol Biol 9:59
25. 2+-responsive cis elements in Arabidopsis. Plant Cell 18:2733–2748
26. Kim MC, Chung WS, Yun DJ, Cho MJ (2009) Calcium and calmodulin-mediated regulation of gene expression in plants. Mol Plant 2:13–21
27. Kim Y, Park S, Gilmour SJ, Thomashow MF (2013) Roles of CAMTA transcription factors and salicylic acid in configuring the low-temperature transcriptome and freezing tolerance of Arabidopsis. Plant J 75:364–376
28. Koo SC, Choi MS, Chun HJ, Shin DB, Park BS, Kim YH, Kim MC (2009) The calmodulin-binding transcription factor OsCBT suppresses defense responses to pathogens in rice. Mol Cells 27:563–570
29. Kudla J, Batistic O, Hashimoto K (2010) Calcium signals: the lead currency of plant information processing. Plant Cell 22:541–63
30. Kulcheski FR, de Oliveira LF, Molina LG, Almerao MP, Rodrigues FA, Marcolino J, Barbosa JF, Stolf-Moreira R, Nepomuceno AL, Marcelino-Guimaraes FC, Abdelnoor RV, Nascimento LC, Carazzolle MF, Pereira GA, Margis R (2011) Identification of novel soybean microRNAs involved in abiotic and biotic stresses. BMC Genomics 12:307
31. Laluk K, Prasad KV, Savchenko T, Celesnik H, Dehesh K, Levy M, Mitchell-Olds T, Reddy AS (2012) The calmodulin-binding transcription factor SIGNAL RESPONSIVE1 is a novel regulator of glucosinolate metabolism and herbivory tolerance in Arabidopsis. Plant Cell Physiol 53:2008–2015
32. +-PPase AVP1 regulates auxin-mediated organ development. Science 310:121–125
33. Liu JH, Peng T, Dai W (2013) Critical cis-acting elements and interacting transcription factors: key players associated with abiotic stress responses in plants. Plant Mol Biol Rep 32:303–317
34. Ludwig AA, Romeis T, Jones JD (2004) CDPK-mediated signalling pathways: specificity and cross-talk. J Exp Bot 55:181–188
35. Manavalan LP, Guttikonda SK, Tran LSP, Nguyen HT (2009) Physiological and molecular approaches to improve drought resistance in soybean. Plant Cell Physiol 50:1260–1276
36. Maruyama-Nakashita A, Nakamura Y, Watanabe-Takahashi A, Inoue E, Yamaya T, Takahashi H (2005) Identification of a novel cis-acting element conferring sulfur deficiency response in Arabidopsis roots. Plant J 42:305–314
37. McAinsh MR, Pittman JK (2009) New Phytol 181:275–294
38. Mitsuda N, Isono T, Sato MH (2003) Arabidopsis CAMTA family proteins enhance V-PPase expression in pollen. Plant Cell Physiol 44:975–981
39. Nakashima K, Yamaguchi-Shinozaki K (2006) Regulons involved in osmotic stress-responsive and cold stress-responsive gene expression in plants. Physiol Plant 126:62–71
40. Nie H, Zhao C, Wu G, Wu Y, Chen Y, Tang D (2012) SR1, a calmodulin-binding transcription factor, modulates plant defense and ethylene-induced senescence by directly regulating NDR1 and EIN 3. Plant Physiol 158:1847–1859
41. Oldroyd GE, Dixon R (2014) Biotechnological solutions to the nitrogen problem. Curr Opin Biotechnol 26:19–24
42. Osakabe Y, Yamaguchi-Shinozaki K, Shinozaki K, Tran LSP (2013) ABA control of plant macroelement membrane transport systems in response to water deficit and high salinity. New Phytol 202:35–49
43. Pandey N, Ranjan A, Pant P, Tripathi RK, Ateek F, Pandey HP, Patre UV, Sawant SV (2013) CAMTA 1 regulates drought responses in Arabidopsis thaliana. BMC Genomics 14:216
44. Pieterse CM, Van Loon LC (2004) NPR1: the spider in the web of induced resistance signaling pathways. Curr Opin Plant Biol 7:456–464
45. Poovaiah BW, Du L, Wang H, Yang T (2013) Recent advances in calcium/calmodulin-mediated signaling with an emphasis on plant-microbe interactions. Plant Physiol 163:531–542
46. Popescu SC, Popescu GV, Bachan S, Zhang Z, Seay M, Gerstein M, Snyder M, Dinesh-Kumar SP (2007) Differential binding of calmodulin-related proteins to their targets revealed through high-density Arabidopsis protein microarrays. Proc Natl Acad Sci U S A 104:4730–35
47. Punta M, Coggill PC, Eberhardt RY, Mistry J, Tate J, Boursnell C, Pang N, Forslund K, Ceric G, Clements J, Heger A, Holm L, Sonnhammer ELL, Eddy SR, Bateman A, Finn RD (2012) The Pfam protein families database. Nucleic Acids Res 40:D290–D301
48. Qiu YJ, Xi J, Du LQ, Suttle JC, Poovaiah BW (2012) Coupling calcium/calmodulin-mediated signaling and herbivore-induced plant response through calmodulin-binding transcription factor AtSR1/CAMTA3. Plant Mol Biol 79:89–99
49. Reddy ASN (2001) Calcium: silver bullet in signaling. Plant Sci 160:381–404
50. Reddy ASN, Reddy VS, Golovkin M (2000) A calmodulin binding protein from Arabidopsis is induced by ethylene and contains a DNA-binding motif. Biochem Biophys Res Commun 279:762–69
51. Reddy AS, Ali GS, Celesnik H, Day IS (2011) Coping with stresses: roles of calcium- and calcium/calmodulin-regulated gene expression. Plant Cell 23:2010–2032
52. Ren J, Wen L, Gao X, Jin C, Xue Y, Yao X (2009) DOG 1.0: illustrator of protein domain structures. Cell Res 19:271–273
53. Rubio V, Linhares F, Solano R, Martín AC, Iglesias J, Leyva A, Paz-Ares J (2001) A conserved MYB transcription factor involved in phosphate starvation signaling both in vascular plants and in unicellular algae. Gene Dev 15:2122–2133
54. Sakuma Y, Liu Q, Dubouzet JG, Abe H, Shinozaki K, Yamaguchi-Shinozaki K (2002) DNA-binding specificity of the ERF/AP2 domain of Arabidopsis DREBs, transcription factors involved in dehydration-and cold-inducible gene expression. Biochem Biophys Res Commun 290:998–1009
55. Schmutz J, Cannon SB, Schlueter J, Ma J, Mitros T, Nelson W, Hyten DL, Song Q, Thelen JJ, Cheng J, Xu D, Hellsten U, May GD, Yu Y, Sakurai T, Umezawa T, Bhattacharyya MK, 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 XC, Shinozaki K, Nguyen HT, Wing RA, Cregan P, Specht J, Grimwood J, Rokhsar D, Stacey G, Shoemaker RC, Jackson SA (2010) Genome sequence of the palaeopolyploid soybean. Nature 463:178–183
56. Song K, Backs J, McAnally J, Qi X, Gerard RD, Richardson JA, Hill JA, Bassel-Duby R, Olson EN (2006) The transcriptional coactivator CAMTA2 stimulates cardiac growth by opposing class II histone deacetylases. Cell 125:453–466
57. Tran LSP, Mochida K (2010) Functional genomics of soybean for improvement of productivity in adverse conditions. Func Integr Genomic 10:447–462
58. Ulmasov T, Hagen G, Guilfoyle TJ (1997) ARF1, a transcription factor that binds to auxin response elements. Science 276:1865–1868
59. Valdes-Lopez O, Thibivilliers S, Qiu J, Xu WW, Nguyen TH, Libault M, Le BH, Goldberg RB, Hill CB, Hartman GL, Diers B, Stacey G (2011) Identification of quantitative trait loci controlling gene expression during the innate immunity response of soybean. Plant Physiol 157:1975–1986
60. Williams ME, Foster R, Chua NH (1992) Sequences flanking the hexameric G-box core CACGTG affect the specificity of protein binding. Plant Cell 4:485–496
61. Xiong L, Schumaker KS, Zhu JK (2002) Cell signaling during cold, drought, and salt stress. Plant Cell 14:S165–S183
62. Yamaguchi-Shinozaki K, Shinozaki K (2006) Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Annu Rev Plant Biol 57:781–803
63. Yang T, Poovaiah BW (2000) An early ethylene up-regulated gene encoding a calmodulin-binding protein involved in plant senescence and death. J Biol Chem 275:38467–38473
64. Yang T, Poovaiah BW (2002) A calmodulin-binding/CGCG box DNA-binding protein family involved in multiple signaling pathways in plants. J Biol Chem 277:45049–45058
65. Yang T, Poovaiah BW (2003) Calcium/calmodulin-mediated signal network in plants. Trends Plant Sci 8:505–512
66. Yang T, Peng H, Whitaker BD, Conway WS (2012) Characterization of a calcium/calmodulin-regulated SR/CAMTA gene family during tomato fruit development and ripening. BMC Plant Biol 12:19
67. Yang T, Peng H, Whitaker BD, Jurick WM (2013) Differential expression of calcium/calmodulin-regulated SlSRs in response to abiotic and biotic stresses in tomato fruit. Physiol Plant 148:445–455
68. Zeng HQ, Zhu YY, Huang SQ, Yang ZM (2010) Analysis of phosphorus-deficient responsive miRNAs and cis-elements from soybean (Glycine max L.). J Plant Physiol 167:1289–1297
69. + ATPase in rice roots. Plant Soil 357:205–214
70. +-ATPase activity and coupled with potassium efflux from cluster roots of phosphorus-deficient white lupin. Plant Soil 366:389–400