Common bean (Phaseolus vulgaris L.) PvTIFY orchestrates global changes in transcript profile response to jasmonate and phosphorus deficiency

BMC Plant Biology

Volumn 13, Issue 1, 2013, Pages

  Aparicio Fabre, Rosaura ^a   Guillén, Gabriel ^a   Loredo, Montserrat ^a   Arellano, Jesús ^a   Valdés López, Oswaldo ^a   Ramírez, Mario ^a   Íñiguez, Luis P ^a   Panzeri, Dario ^b   Castiglioni, Bianca ^b   Cremonesi, Paola ^b   Strozzi, Francesco ^b   Stella, Alessandra ^b   Girard, Lourdes ^a   Sparvoli, Francesca ^b   Hernández, Georgina ^a  

^a UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

^b CNR Consiglio Nazionale delle Ricerche   (Italy)

Author keywords

JA signaling; P starvation response; Phaseolus vulgaris PvTIFY genes; TIFY gene family; Transcription factors; Transcriptome analysis

Indexed keywords

ARABIDOPSIS; PHASEOLUS VULGARIS;

CYCLOPENTANE DERIVATIVE; JASMONIC ACID; OXYLIPIN; PHOSPHORUS; TRANSCRIPTION FACTOR;

ARTICLE; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PHASEOLUS; PHYSIOLOGY; SIGNAL TRANSDUCTION;

CYCLOPENTANES; GENE EXPRESSION REGULATION, PLANT; OXYLIPINS; PHASEOLUS; PHOSPHORUS; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS;

MLCS; MLOWN;

EID: 84876069144     PISSN: None     EISSN: 14712229     Source Type: Journal    
DOI: 10.1186/1471-2229-13-26     Document Type: Article

References (74)

1. Libault M, Joshi T, Benedito VA, Xu D, Udvardi MK, Stacey G. Legume transcription factor genes: what makes legume so special?. Plant Physiol 2009, 151:991-1001. 10.1104/pp.109.144105, 2773095, 19726573.
2. Broughton WJ, Hernández G, Blair M, Beebe S, Gepts P, Vanderleyden J. Beans (Phaseolus spp.) - model food legumes. Plant Soil 2003, 252:55-128.
3. Goodstein DM, Shu S, Howson R, Neupane R, Hayes RD, Fazo J, Mitros T, Dirks W, Hellsten U, Putnam N, Rokhsar DS. Phytozome: a comparative platform for green plant genomics. Nucleic Acids Res 2012, 40:D1178-D1186. 10.1093/nar/gkr944, 3245001, 22110026.
4. Phaseolus vulgaris v1.0 DOE-JGI and USDA-NIFA, http://www.phytozome.net/commonbean.
5. Hernández G, Ramírez M, Valdés-López O, Tesfaye M, Graham MA, Czechowski T, Schlereth A, Wandrey M, Erban A, Cheung F, Wu HC, Lara M, Town CD, Kopka J, Udvardi MK, Vance CP. Phosphorus stress in common bean: root transcript and metabolic responses. Plant Physiol 2007, 144:752-767. 10.1104/pp.107.096958, 1914166, 17449651.
6. Hernández G, Valdés-López O, Ramírez M, Goffard N, Weiller G, Aparicio-Fabre R, Fuentes SI, Erban A, Kopka J, Udvardi MK, Vance CP. Global changes in the transcript and metabolic profiles during symbiotic nitrogen fixation in phosphorus-stressed common bean plants. Plant Phsyiol 2009, 151:1221-1238.
7. Nishii A, Takemura M, Fujita H, Shikata M, Yokota A, Kohchi T. Characterization of a novel gene encoding a putative single zinc-finger protein, ZIM, expressed during the reproductive phase in Arabidopsis thaliana. Biosci Biotechnol Biochem 2000, 64:1402-1409. 10.1271/bbb.64.1402, 10945256.
8. Vanholme B, Grunewald W, Bateman A, Kohchi T, Gheysen G. The tify family previously known as ZIM. Trends Plant Sci 2007, 12:239-244. 10.1016/j.tplants.2007.04.004, 17499004.
9. Ye H, Du H, Tang N, Li X, Xiong L. Identification and expression profiling analysis of TIFY family genes involved in stress and phytohormone responses in rice. Plant Mol Biol 2009, 71:291-305. 10.1007/s11103-009-9524-8, 19618278.
10. Zhu D, Bai X, Luo X, Chen Q, Cai H, Ji W, Zhu Y. Identification of wild soybean (Glycine soja) TIFY family genes and their expresión profile analysis under bicarbonate stress. Plant Cell Rep 2013, 32:263-272. 10.1007/s00299-012-1360-7, 23090726.
11. Browse J. Jasmonate passes muster: a receptor and targets for the defense hormone. Annu Rev Plant Biol 2009, 60:183-205. 10.1146/annurev.arplant.043008.092007, 19025383.
12. Chico JM, Chini A, Fonseca S, Solano R. JAZ repressors set the rhythm in nuclear dynamics and signaling. Curr Opin Plant Biol 2008, 11:503-508. 10.1016/j.pbi.2008.06.012, 18691930.
13. Chung HS, Niu Y, Browse J, Howe GA. Top hits in contemporary JAZ: an update on jasmonate signaling. Phytochemistry 2009, 70:1547-1559. 10.1016/j.phytochem.2009.08.022, 3271379, 19800644.
14. Katsir L, Chung SH, Koo AJK, Howe GA. Jasmonate signaling: a conserved mechanism of hormone sensing. Curr Opin Plant Biol 2008, 11:428-435. 10.1016/j.pbi.2008.05.004, 2560989, 18583180.
15. Staswick PE. JAZing up jasmonate signaling. Trends Plant Sci 2008, 13:66-71.
16. Staswick PE, Tiryaki I. The oxilipin signal jasmonic acid is activated by an enzyme that conjugates it to isoleucine in Arabidopsis. Plant Cell 2004, 16:2117-2127. 10.1105/tpc.104.023549, 519202, 15258265.
17. Thines B, Katsir L, Melotto M, Niu Y, Mandaokar A, Liu G, Nomura K, He SY, Howe GA, Browse J. JAZ repressor proteins are targets of the SCFCOI1 complex during jamonate signalling. Nature 2007, 448:661-665. 10.1038/nature05960, 17637677.
18. Chini A, Fonseca S, Fernández G, Adie B, Chico JM, Lorenzo O, García-Casado G, López-Vidriero I, Lozano FM, Ponce MR, Micol JL, Solano R. The JAZ family of repressors is the missing link in jasmonate signalling. Nature 2007, 448:666-671. 10.1038/nature06006, 17637675.
19. Yan Y, Stolz S, Chetelat A, Reymond P, Pagni M, Dubugnon L, Farmer EE. A downstream mediator in the growth repression limb of the jasmonate pathway. Plant Cell 2007, 19:2470-2483. 10.1105/tpc.107.050708, 2002611, 17675405.
20. Pauwels L, Fernández Barbero G, Geerinck J, Tilleman S, Grunewald W, Cuéllar Pérez A, Chico JM, Vanden Bossche R, Sewell J, Gil E, García-Casado G, Witters E, Inzé D, Long JA, Jaeger GD, Solano R. NINJA connects the co-repressor TOPLESS to jasmonate signalling. Nature 2010, 464:788-791. 10.1038/nature08854, 2849182, 20360743.
21. Melotto M, Mecey C, Niu Y, Chung HS, Katsir L, Yao J, Zeng W, Thines B, Staswick PE, Browse J, Howe GA, He SY. A critical role of two positively charged amino acids in the Jas motif of Arabidopsis JAZ proteins in mediating coronatine - and jasmonoyl isoleucine-dependent interactions with the COI1 F-box protein. Plant J 2008, 55:979-988. 10.1111/j.1365-313X.2008.03566.x, 2653208, 18547396.
22. Katsir L, Schilmiller AL, Satswick PE, He SY, Howe GA. COI1 is a critical component of a receptor for jasmonate and the bacterial virulence factor coronatine. Proc Natl Acad Sci USA 2008, 105:7100-7105. 10.1073/pnas.0802332105, 2383947, 18458331.
23. Yan J, Zhang C, Gu M, Bai Z, Zhang W, Qi T, Cheng Z, Peng W, Luo H, Nan F, Wang Z, Xie D. The Arabidopsis CORONATINE INSENSITIVE 1 protein is a jasmonate receptor. Plant Cell 2009, 21:2220-2236. 10.1105/tpc.109.065730, 2751961, 19717617.
24. Seo JS, Joo J, Kim MJ, Kim YK, Nahm BH, Song SI, Cheong JJ, Lee JS, Kim JK, Choi YD. OsbHLH148, a basic helix-loop-helix protein, interacts with OsJAZ proteins in a jasmonate signaling pathway leading to drought tolerance in rice. Plant J 2011, 65:907-921. 10.1111/j.1365-313X.2010.04477.x, 21332845.
25. Armengaud P, Breitling R, Amtmann A. The potassium-dependent transcriptome of Arabidopsis reveals a prominent role of jasmonic acid in nutrient signaling. Plant Physiol 2004, 136:2556-2576. 10.1104/pp.104.046482, 523322, 15347784.
26. Chacón-López A, Ibarra-Laclette E, Sánchez-Calderón L, Gutiérrez-Alanís D, Herrera-Estrella L. Global expression pattern comparison between low phosphorus insensitive 4 and WT Arabidopsis reveals an important role of reactive oxygen species and jasmonic acid in the root tip response to phosphate starvation. Plant Signal Behav 2011, 6:382-392. 10.4161/psb.6.3.14160, 3142420, 21368582.
27. Graham PH, Rosas JC, Estevez de Jensen C, Peralta E, Tlusty B, Acosta-Gallegos J, Arraes Pereira PA. Addressing edaphic constraints to bean production: the bean/cowpea CRSP project in perspective. Field Crops Res 2003, 82:179-192.
28. Raghothama KG. Phosphate acquisition. Annu Rev Plant Physiol Plant Mol Biol 1999, 50:665-693. 10.1146/annurev.arplant.50.1.665, 15012223.
29. Vance CP, Udhe-Stone C, Allan DL. Phosphorus acquisition and use: critical adaptations by plants for securing a nonrenewable resource. New Phytol 2003, 157:423-447.
30. Williamson L, Ribrioux S, Fitter A, Leyser O. Phosphate availability regulates root system architecture in Arabidopsis. Plant Physiol 2001, 126:1-8.
31. López-Bucio J, Hernández-Abreu E, Sánchez-Calderón L, Nieto-Jacobo ME, Simpson J, Herrera-Estrella L. Phosphate availability alters architecture and causes changes in hormone sensitivity in the Arabidopsis root system. Plant Physiol 2002, 129:244-256. 10.1104/pp.010934, 155888, 12011355.
32. Sánchez-Calderón L, López-Bucio J, Chacón-López A, Nieto-Jacobo F, Dubrovsky JG, Herrera-Estrella L. Phosphate starvation induces a determinate developmental program in the roots of Arabidopsis thaliana. Plant Cell Physiol 2005, 46:174-184. 10.1093/pcp/pci011, 15659445.
33. Sánchez-Calderón L, López-Bucio J, Chacón-López A, Gutierrez-Ortega A, Hernández-Abreu E, Herrera-Estrella L. Characterization of low phosphorus insensitive mutants reveal a cross-talk between low-phosphorus induced determinate root development and the activation of genes involved in the adaptation of Arabidopsis to phosphorus deficiency. Plant Physiol 2006, 140:879-889. 10.1104/pp.105.073825, 1400555, 16443695.
34. Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, Davis AP, Dolinski K, Dwight SS, Eppig JT, Harris MA, Hill DP, Issel-Tarver L, Kasarskis A, Lewis S, Matese JC, Richardson JE, Ringwald M, Rubin GM, Sherlock G, The Gene Ontology Consortium Gene ontology: tool for the unification of biology. Nature Genet 2000, 25:25-29. 10.1038/75556, 3037419, 10802651, The Gene Ontology Consortium.
35. Thimm O, Bläsing O, Gibon Y, Nagel A, Meyer S, Krüger P, Selbig J, Müller LA, Rhee SY, Stitt M. MAPMAN: a user-driven tool to display genomic data sets onto diagrams of metabolic pathways and other biological processes. Plant J 2004, 37:914-939. 10.1111/j.1365-313X.2004.02016.x, 14996223.
36. Eddy SR. Profile hidden Markov models. Bioinformatics 1998, 14:755-763. 10.1093/bioinformatics/14.9.755, 9918945.
37. Finn RD, Mistry J, Tate J, Coggill P, Heger A, Pollington JE, Gavin OL, Gunesekaran P, Ceric G, Forslund K, Holm L, Sonnhammer EL, Eddy SR, Bateman A. The Pfam protein families database. Nucl Acids Res 2010, 38(Suppl 1):D211-D222. 2808889, 19920124.
38. Crooks GE, Hon G, Chandonia JM, Brenner SE. WebLogo: a sequence logo generator. Genome Res 2004, 14:1188-1190. 10.1101/gr.849004, 419797, 15173120.
39. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 1997, 25:4876-4882. 10.1093/nar/25.24.4876, 147148, 9396791.
40. Lim A, Zhang L. WebPHYLIP: a web interface to PHYLIP. Bioinformatics 1999, 15:1068-1069. 10.1093/bioinformatics/15.12.1068, 10746002.
41. Huson DH, Bryant D. Application of phylogenetic networks in evolutionary studies. Mol Biol Evol 2006, 23:254-267.
42. Valdés-López O, Yang SS, Aparicio-Fabre R, Graham PH, Reyes JL, Vance CP, Hernández G. MicroRNAs expression profile in common bean (Phaseolus vulgaris) during nutrient deficiency stresses and manganese toxicity. New Phytol 2010, 187:805-818. 10.1111/j.1469-8137.2010.03320.x, 20553393.
43. Franco AA, Munns DN. Nodulation and growth of Phaseolus vulgaris solution culture. Plant Soil 1982, 66:149-160.
44. Estrada-Navarrete G, Alvarado-Affantrager X, Olivares JE, Gillén G, Díaz-Camino C, Campos F, Quinto C, Gresshoff PM, Sánchez F. Fast, efficient and reproducible genetic transformation of Phaseolus spp. by Agrobacterium rhizogenes. Nat Protoc 2007, 2:1819-1824. 10.1038/nprot.2007.259, 17641650.
45. Valdés-López O, Arenas-Huertero C, Ramírez M, Girard L, Sánchez F, Vance CP, Reyes JL, Hernández G. Essential role of MYB transcription factor: PvPHR1 and microRNA: PvmiR399 in the phosphorus deficiency signaling in common bean roots. Plant Cell Environ 2008, 31:1834-1843. 10.1111/j.1365-3040.2008.01883.x, 18771575.
46. The Gene Index Project http://compbio.dfci.harvard.edu/tgi/plant.html.
47. Curtis M, Grossniklaus U. A Gateway TM cloning vector set for high-throughput functional analysis of genes in plants. Plant Physiol 2003, 133:462-469. 10.1104/pp.103.027979, 523872, 14555774.
48. Martínez-Salazar J, Romero D. Role of the ruvB gene in homologous and homeologous recombination in Rhizobium etli. Gene 2000, 243:125-131. 10.1016/S0378-1119(99)00548-X, 10675620.
49. Shaner NC, Campbell RE, Steinbach PA, Giepmans BNG, Palmer AE, Tsien RY. Improved monomeric red, orange, and yellow fluorescent proteins derived from Discosoma sp. red fluorescence protein. Nat Biotechnol 2004, 22:1567-1572. 10.1038/nbt1037, 15558047.
50. Edgar R, Domrachev M, Lash AE. Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res 2002, 30:207-210. 10.1093/nar/30.1.207, 99122, 11752295.
51. Smyth GK. Linear models and empirical Bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol 2004, 3(Article 3):1-26.
52. Routledge R. Fisher's exact test. Encyclopedia of biostatistics Volume 2 1998, 1519-1523. New York: John Wiley, Armitage P, Colton T.
53. Smale ST, Kadonaga JT. The RNA polymerase II core promoter. Annu Rev Biochem 2003, 72:449-479. 10.1146/annurev.biochem.72.121801.161520, 12651739.
54. Vandepoele K, Quimabya M, Casneuf T, De Veylder L, Van de Peer Y. Unraveling transcription control in Arabidopsis using cis-regulatory elements and coexpression networks. Plant Physiol 2009, 150:535-546. 10.1104/pp.109.136028, 2689962, 19357200.
55. Menkens AE, Schindler U, Cashmore AR. The G-box: a ubiquitous regulatory DNA element in plants bound by the GBF family of bZIP proteins. Trends Biochem Sci 1995, 20:506-510. 10.1016/S0968-0004(00)89118-5, 8571452.
56. Seitz AB, Voytsekh O, Mohan KM, Mittag M. The role of an E-box element. Multiple fuctions and interacting partners. Plant Signal Behav 2010, 5:1077-1080. 10.4161/psb.5.9.12564, 3115072, 20818183.
57. Walcher CL, Nemhauser JL. Bipartite promoter element required for auxin response. Plant Signal Behav 2012, 158:273-282.
58. Grunewald W, Vanholme B, Pauwels L, Inzé D, Gheysen G, Goosens A. Expression of the Arabidopsis jasmonate signalling repressor JAZ1/TIFY10A is stimulated by auxin. EMBO Rep 2009, 10:923-928. 10.1038/embor.2009.103, 2726675, 19575013.
59. Geiss-Friedlander R, Melchior F. Concepts in sumoylation: a decade on. Nature Rev Mol Cell Biol 2007, 8:947-956.
60. Chung HS, Koo AJK, Gao X, Jayanty S, Thines B, Jones AD, Howe GA. Regulation and function of Arabidipsis JASMONATE ZIM-domain genes in response to wounding and herbivory. Plant Physiol 2008, 146:952-964. 10.1104/pp.107.115691, 2259048, 18223147.
61. Rubio V, Linhares F, Solano R, Martín AC, Iglesias J, Leyva A, Paz-Ares J. A conserved MYB transcription factor involved in phosphate starvation signaling both in vascular plant and unicellular algae. Genes Dev 2001, 15:2122-2133. 10.1101/gad.204401, 312755, 11511543.
62. Chen ZH, Nimmo GA, Jenkins G, Nimmo HG. BHLH32 modulates several biochemical and morphological process that respond to Pi starvation in Arabidopsis. Biochem J 2007, 405:191-198. 1925254, 17376028.
63. Devaiah B, Karthikeyan AS, Raghothama KG. WRKY75 transcription factor is a modulator of phosphate acquisition and root development in Arabidopsis. Plant Physiol 2007, 143:1789-1801. 10.1104/pp.106.093971, 1851818, 17322336.
64. Devaiah B, Nagarajna VK, Raghothama KG. Phosphate homeostasis and root development in Arabidopsis are synchronized by the zing finger transcription factor ZAT6. Plant Physiol 2007, 145:147-159. 10.1104/pp.107.101691, 1976576, 17631527.
65. Devaiah B, Madhuvanthi R, Karthikeyan AS, Raghothama KG. Phosphate starvation responses and giberellic acid biosynthesis are regulated by the MYB62 transcription factor in Arabidopsis. Mol Plant 2009, 2:43-58. 10.1093/mp/ssn081, 2639739, 19529828.
66. Hammond JP, Bennett MJ, Bowen HC, Briadley MR, Eastwood DC, May ST, Rahn C, Swaruo R, Woolaway KE, White PJ. Changes in gene expression in Arabidopsis shoots during phosphate starvation and the potential for developing smart plants. Plant Physiol 2003, 132:578-596. 10.1104/pp.103.020941, 166999, 12805589.
67. Misson J, Raghothama KG, Jain A, Jouhet J, Block MA, Bligny R, Ortet P, Creff A, Somerville S, Rolland N, Doumas P, Nacry P, Herrera-Estrella L, Nussaume L, Thibaud MC. A genome-wide transcriptional analysis using Arabidopsis thaliana Affymetrix gene chips determined plant responses to phosphate deprivation. Proc Natl Acad Sci USA 2005, 102:11934-11939. 10.1073/pnas.0505266102, 1188001, 16085708.
68. Morcuende R, Bari R, Gibon Y, Zheng WM, Pant BD, Blasing O, Usadel B, Czechowski T, Udvardi MK, Stitt M, Scheible WR. Genomic-wide reprogramming of metabolism and regulatory networks of Arabidopsis in response to phosphorus. Plant Cell Environ 2007, 30:85-112. 10.1111/j.1365-3040.2006.01608.x, 17177879.
69. Wu P, Ligeng M, Hou X, Wang M, Wu Y, Liu F, Deng XW. Phosphate starvation triggers distinct alterations of genome expression in Arabidopsis roots and leaves. Plant Physiol 2003, 132:1260-1271. 10.1104/pp.103.021022, 167066, 12857808.
70. Müller R, Morant M, Jarmer H, Nilsson L, Nielsen TH. Genome-wide analysis of the Arabidopsis leaf transcriptome reveals interaction of phosphate and sugar metabolism. Plant Physiol 2007, 143:156-171. 1761981, 17085508.
71. Uhde-Stone C, Zinn KE, Ramírez-Yañez M, Li A, Vance CP, Allan DL. Nylon filter arrays reveal differential gene expression in proteoid roots of white lupin in response to phosphorus deficiency. Plant Physiol 2003, 131:1064-1079. 10.1104/pp.102.016881, 166872, 12644659.
72. Wasaki J, Yonetani R, Kuroda S, Shinano T, Yasaki J, Fujii F, Shimbo K, Yamamoto K, Sakata K, Sasaki T, Kishimoto N, Kikuchi S, Yamagishi M, Osaki M. Transcriptomic analysis of metabolic changes by phosphorus stress in rice plant roots. Plant Cell Environ 2003, 26:1515-1523.
73. Neumann G, Römheld V. Root excretion of carboxylic acids and protons in phosphorus-deficient plants. Plant Soil 1999, 211:121-130.
74. Shen H, Yan X, Zhao M, Zheng S, Wang X. Exudation of organic acids in common bean as related to mobilization of aluminum- and iron-bound phosphates. Environ Exp Bot 2002, 48:1-9.