MicroRNA expression profile in common bean (Phaseolus vulgaris) under nutrient deficiency stresses and manganese toxicity

New Phytologist

Volumn 187, Issue 3, 2010, Pages 805-818

  Valdés López, Oswaldo ^a,c   Yang, S Samuel ^d   Aparicio Fabre, Rosaura ^a   Graham, Peter H ^c   Reyes, José Luis ^b   Vance, Carroll P ^c,d   Hernández, Georgina ^a  

^a INSTITUTO DE CIENCIAS FÍSICAS   (Mexico)

^b INSTITUTO DE BIOTECNOLOGÍA   (Mexico)

^c UNIVERSITY OF MINNESOTA   (United States)

^d AGRICULTURAL RESEARCH SERVICE   (United States)

Author keywords

Common bean (Phaseolus vulgaris); Common bean microRNAs; Manganese toxicity; Nutrient deficiency stress; Nutrient stress responsive microRNAs

Indexed keywords

MANGANESE; MICRORNA; PLANT RNA;

GENE EXPRESSION; GENETIC ANALYSIS; IRON; LEGUME; MANGANESE; MULTIVARIATE ANALYSIS; NITROGEN; NUTRIENT LIMITATION; PH; PHOSPHORUS; POLYMERASE CHAIN REACTION; RNA; TOXICITY;

ARTICLE; ATOMIC ABSORPTION SPECTROMETRY; BEAN; BIOMASS; CLUSTER ANALYSIS; DNA MICROARRAY; DRUG EFFECT; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; NORTHERN BLOTTING; PHENOTYPE; PHYSIOLOGICAL STRESS; PRINCIPAL COMPONENT ANALYSIS; DRUG EFFECTS; PHASEOLUS; TOXICITY;

BIOMASS; BLOTTING, NORTHERN; CLUSTER ANALYSIS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, PLANT; MANGANESE; MICRORNAS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PHASEOLUS; PHENOTYPE; PRINCIPAL COMPONENT ANALYSIS; RNA, PLANT; SPECTROPHOTOMETRY, ATOMIC; STRESS, PHYSIOLOGICAL;

PHASEOLUS VULGARIS;

EID: 77955159749     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/j.1469-8137.2010.03320.x     Document Type: Article

References (68)

1. Abdel-Ghany SE, Pilon M. MicroRNA-mediated systemic down-regulation of cooper protein expression in response to low copper availability in Arabidopsis. The Journal of Biological Chemistry 2008, 283:15932-15945.
2. Allen E, Xie Z, Gustafson AM, Carrington JC. MicroRNA-directed phasing during trans-acting siRNA biogenesis in plants. Cell 2005, 121:207-221.
3. Arenas-Huertero C, Pérez B, Rabanal F, Blanco-Melo D, De la Rosa C, Estrada-Navarrete G, Sanchez F, Covarrubias AA, Reyes JL. Conserved and novel miRNAs in the legume Phaseolus vulgaris in response to stress. Plant Molecular Biology 2009, 70:385-401.
4. Aukerman MJ, Sakai H. Regulation of flowering time and floral organ identity by a microRNA and its APETALA2-like target gene. The Plant Cell 2003, 15:2730-2741.
5. Bari R, Pant BD, Stitt M, Scheible WR. PHO2, microRNA399 and PHRI define a phosphate signaling pathway in plants. Plant Physiology 2006, 141:988-999.
6. Bonnet E, Van de Peer Y, Rouzé P. The small RNA world in plants. New Phytologist 2006, 171:451-468.
7. Boualem A, Laporte P, Jovanovic M, Laffont C, Plet J, Combier JP, Niebel A, Crespi M, Frugier F. MicroRNA166 controls root and nodule development in Medicago truncatula. Plant Journal 2008, 54:876-887.
8. Broughton WJ, Hernández G, Blair M, Beebe S, Gepts P, Vanderleyden J. Beans (Phaseolus spp.) - model food legume. Plant and Soil 2003, 252:55-128.
9. Buhtz A, Springer F, Chapell L, Baulcome D, Kehr J. Identification and characterization of small RNAs from the phloem of Brassica napus. Plant Journal 2008, 53:739-749.
10. Chen X. A microRNA as a translational repressor of APETALA2 in Arabidopsis flower development. Science 2004, 303:2022-2025.
11. Chiou TJ, Aung K, Lin SI, Wu CC, Chiang SF, Su CI. Regulation to phosphate homeostasis by MicroRNA in Arabidopsis. The Plant Cell 2006, 18:412-421.
12. Chuck G, Candela H, Hake S. Big impacts by small RNAs in plant development. Current Opinion in Plant Biology 2008a, 12:1-6.
13. Chuck G, Meeley R, Hake S. Floral meristem initiation and meristem cell fate are regulated by maize AP2 genes ids1 and sid1. Development 2008b, 135:3013-3019.
14. Colebatch G, Desbrosses G, Ott T, Krusell L, Montanari O, Kloska S, Kopka J, Udvardi MK. Global changes in transcription orchestrate metabolic differentiation during symbiotic nitrogen fixation in Lotus japonicus. Plant Journal 2004, 39:487-512.
15. Combier JP, Frugier F, de Billy F, Boualem A, El-Yahyaoui F, Moreau S, Vernié T, Ott T, Gamas P, Crespi M. MtHAP2-1 is a key transcriptional regulator of symbiotic nodule development regulated by miR169 in Medicago truncatula. Genes and Development 2006, 20:3084-3088.
16. Covarrubias AA, Reyes JL. Post-transcriptional gene regulation of salinity and drought responses by plant microRNAs. Plant, Cell & Environment 2009, 33:481-489.
17. Doyle JJ, Luckow MA. The rest of the iceberg. Legume diversity and evolution in a phylogenetic context. Plant Physiology 2003, 131:900-910.
18. Eisen MB, Spellman PT, Brown PO, Botstein D. Cluster analysis and display of genome-wide expression patterns. Proceeding of the National Academy of Sciences, USA 1998, 95:14863-14868.
19. Franco AA, Munns DN. Nodulation and growth of Phaseolus vulgaris solution culture. Plant and Soil 1982, 66:149-160.
20. Gifford ML, Dean A, Gutierrez RA, Coruzzi GM, Birnbaum KD. Cell-specific nitrogen responses mediate developmental plasticity. Proceeding of the National Academy of Sciences, USA 2008, 195:803-808.
21. 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 Crop Research 2003, 82:179-192.
22. Graham PH, Vance CP. Legumes: importance and constraints for greater use. Plant Physiology 2003, 131:872-877.
23. Grotz N, Guerinot ML. Molecular aspects of Cu, Fe and Zn homeostasis in plants. Biochimica el Biophysica Acta-Molecular Cell Research 2006, 1763:595-608.
24. Gutiérrez RA, Lejay L, Dean A, Chiaromonte F, Shasha DE, Coruzzi GM. Qualitative network models and genome-wide expression data define carbon/nitrogen-responsive molecular machines in Arabidopsis. Genome Biology 2007, 8:R7.
25. Haydon MJ, Cobbett CS. Transporters of ligands for essential metal ions in plants. New Phytologist 2007, 174:499-506.
26. Hernández G, Ramírez M, Valdés-López O, Tesfaye M, Graham MA, Czechowski T, Schlereth A, Wandrey M, Erban A, Cheung F. Phosphorus stress in common bean: root transcript and metabolic responses. Plant Physiology 2007, 144:752-767.
27. Hernández G, Valdés-López O, Ramírez M, Goffard N, Weiller G, Aparicio-Fabre R, Fuentes SI, Erban A, Kopka J, Udvardi MK. Global changes in the transcript and metabolic profiles during symbiotic nitrogen fixation in phosphorus-stressed common bean plants. Plant Physiology 2009, 151:1221-1238.
28. Hobert O. Gene regulation by transcription factors and microRNAs. Science 2008, 319:1785-1786.
29. Horst WJ, Fecht M, Naumann A, Wissemeier AH, Maier P. Physiology of manganese toxicity and tolerance in Vigna unguiculata (L.) Walp. Journal of Plant Nutrition and Soil Science 1999, 162:263-274.
30. Hsieh LC, Lin SI, Shih ACC, Chen JW, Lin WY, Tseng CY, Li WH, Chiou TJ. Uncovering small RNA-mediated responses to phosphate deficiency in Arabidopsis by deep sequencing. Plant Physiology 2009, 151:2120-2132.
31. Izaguirre-Mayoral ML, Sinclair TR. Soybean genotypic difference in growth, nutrient accumulation and ultrastructure in response to manganese and iron supply in solution culture. Annals of Botany 2005, 96:149-158.
32. Jagadeeswaran G, Zheng Y, Li YF, Shukla LI, Matts J, Hoyt P, Macmil SL, Wiley GB, Roe BA, Zhang W. Cloning and characterization of small RNAs from Medicago truncatula reveals four novel legume-specific microRNA families. New Phytologist 2009, 184:85-98.
33. Jain A, Poling MD, Smith AP, Nagarajan VK, Lahner B, Meagher RB, Raghothama KG. Variations in the composition of gelling agents affect morphological and molecular responses to deficiencies of phosphate and other nutrients. Plant Physiology 2009, 150:1033-1049.
34. Jeong DH, German MA, Rymarquis LA, Thatcher SR, Green PJ. Abiotic stree-associated miRNAs: detection and functional analysis. Plant MicroRNAs, Methods in Molecular Biology 2009, 203-230. Meyers BC, Green PJ, eds, Vol. 592, New York, NY, USA, Humana Press
35. Jones-Rhoades MW, Bartel DP, Bartel B. MicroRNAs and their regulatory roles in plants. Annual Review of Plant Biology 2006, 57:19-53.
36. Jorgensen RA. RNA traffics information systemically in plants. Proceeding of the National Academy of Sciences, USA 2002, 99:11561-11563.
37. Joshi T, Yan Z, Libault M, Jeong DH, Park S, Green PJ, Sherrier DJ, Farmer A, May G, Meyers BC. Prediction of novel miRNAs and associated target genes in Glycine max. BMC Bioinformatics 2010, 11(Suppl. 1):S14. http://dx.doi.org/10.1186/1471-2105-11-S1-S14, doi:
38. Jung JH, Seo YH, Seo PJ, Reyes JL, Yun J, Chua NH, Park CM. The GIGANTEA-regulated microRNA172 mediates photoperiodic flowering independent of CONSTANS in Arabidopsis. The Plant Cell 2007, 19:2736-2748.
39. Kawashima CG, Yoshimoto N, Maruyama-Nakashita A, Tsuchiya YN, Saito K, Takahashi H, Dalmay T. Sulphur starvation induces the expression of microRNA-395 and one of its target genes but in different cell types. Plant Journal 2009, 57:313-321.
40. Korshunova YO, Eide D, Clark WG, Guerinot ML, Pakrasi HB. The IRT1 protein from Arabidopsis is a metal transporter with broad substrate range. Plant Molecular Biology 1999, 40:37-44.
41. Krouk G, Tranchina D, Lejay L, Cruikshank AA, Shasha DE, Coruzzi GM, Gutiérrez RA. A systems approach uncovers restrictions for signal interactions regulating genome-wide responses to nutritional cues in Arabidopsis. PLoS Computational Biology 2009, 5:e1000326.
42. Lelandais-Briere C, Naya L, Sallet E, Calenge F, Frugier F, Hartmann C, Gouzy J, Crespi M. Genome-wide Medicago truncatula small RNA analysis revealed novel microRNAs and isoforms differentially regulated in roots and nodules. The Plant Cell 2009, 21:2780-2796.
43. Lough TJ, Lucas WJ. Integrative plant biology: role of phloem long-distance macromolecular trafficking. Annual Review of Plant Biology 2006, 129:203-232.
44. Mallory AC, Vaucheret H. Functions of microRNAs and related small RNAs in plants. Nature Genetics 2006, 38:S31-S36.
45. Mendoza A, Leija A, Martínez-Romero E, Hernández G, Mora J. The enhancement of ammonium assimilation in Rhizobium etli prevents nodulation in Phaseolus vulgaris. Molecular Plant-Microbe Interaction 1995, 4:584-592.
46. Mora ML, Rosas A, Ribera A, Rengel Z. Differential tolerance to Mn toxicity in perennial ryegrass genotypes: involvement of antioxidative enzymes and root exudation of carboxylates. Plant and Soil 2009, 320:79-89.
47. Oldroyd GE, Downie JA. Calcium, kinases and nodulation signaling in legumes. Nature Reviews Molecular Cell Biology 2004, 5:566-576.
48. Pant BD, Buhtz A, Kehr J, Scheible WR. MicroRNA399 is a long-distance signal for the regulation of plant phosphate homeostasis. Plant Journal 2008, 53:731-738.
49. Pant BD, Musialak-Lange M, Nuc P, May P, Buhtz A, Kehr J, Walther D, Scheinle WR. Identification of nutrient-responsive Arabidopsis and rapeseed micorRNAs by comprehensive real-time polymerase chain reaction profiling and small RNA sequencing. Plant Physiology 2009, 150:1541-1555.
50. Pearson K. On lines and planes of closest fit to systems of points in space. Philosophical Magazine 1901, 2:559-572.
51. Peltzer-Meschini A, Blanco FA, Zanetti ME, Beker MP, Küster H, Pühler A, Aguilar OM. Host genes involved in nodulation preference in common bean (Phaseolus vulgaris) -Rhizobium etli symbiosis revealed by suppressive substractive hybridization. Molecular Plant-Microbe Interaction 2008, 21:456-468.
52. Simon SA, Meyers BC, Sherrier DJ. MicroRNAs in the rhizobial legume symbiosis. Plant Physiology 2009, 151:1002-1008.
53. Subramanian S, Fu Y, Sunkar R, Barbazuk WB, Zhu JK, Yu O. Novel and nodulation-regulated microRNAs in soybean roots. BMC Genomic 2008, 9:160. http://dx.doi.org/10.1186/1471-2164-9-160, doi:
54. Sunkar R, Chinnusamy V, Zhu J, Zhu J-K. Small RNAs as big players in plant abiotic stress responses and nutrient deprivation. Trends in Plant Sciences 2007, 12:301-309.
55. Sunkar R, Jagadeeswaran G. In silico identification of conserved microRNAs in large number of diverse plant species. BMC Plant Biology 2008, 8:37. http://dx.doi.org/10.1186/1471-2229-8-37, doi:
56. Szittya G, Moxon S, Santos DS, Jing R, Fevereiro MPS, Moulton V, Dalmay T. High-throughput sequencing of Medicago truncatula short RNAs identifies eight new miRNA families. BMC Genomics 2008, 9:593. http://dx.doi.org/10.1186/1471-2164-9-593, doi:
57. Tesfaye M, Samac DA, Vance CP. Insights into symbiotic nitrogen fixation in Medicago truncatula. Molecular Plant-Microbe Interaction 2006, 19:330-341.
58. 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 phosphorus-deficiency signaling in common bean roots. Plant, Cell & Environment 2008, 31:1834-1843.
59. Voinnet O. Origin, biogenesis, and activity of plant microRNAs. Cell 2009, 136:669-687.
60. Wang Y, Li P, Cao X, Wang X, Zhang A, Li X. Identification and expression analysis of miRNAs from nitrogen-fixing soybean nodules. Biochemical and Biophysical Research Communications 2009, 378:799-803.
61. Yamasaki H, Abdel-Ghany S, Cohu C, Kobyashi Y, Shikanai T, Pilon M. Regulation of cooper homeostasis by micro-RNA in Arabidopsis. The Journal of Biological Chemistry 2008, 282:16369-16378.
62. Yamasaki H, Hayashi M, Fukazawa M, Kobayashi Y, Shikanai T. SQUAMOSA promoter binding protein-like7 is a central regulator for copper homeostasis in Arabidopsis. The Plant Cell 2009, 21:347-361.
63. Yoo BC, Kragler F, Varkonyi-Gasic E, Haywood V, Archer-Evans S, Lee YM, Lough TJ, Lucas WJ. A systemic small RNA signaling system in plants. The Plant Cell 2004, 16:1979-2000.
64. Zhang B, Pan X, Cannon CH, Cobb GP, Anderson TA. Conservation and divergence of plant microRNA genes. Plant Journal 2006, 46:243-259.
65. Zhang B, Pan X, Stellwag EJ. Identification of soybean microRNAs and their targets. Planta 2008, 229:161-182.
66. Zhao L, Kim YJ, Dinh T, Chen X. MiR172 regulates stem cell fate and defines the inner boundary of APETALA3 and PISTILLATA expression domain in Arabidopsis floral meristems. Plant Journal 2007, 51:840-849.
67. Zhou ZS, Huang SQ, Yang ZM. Bioinformatic identification and expression analysis of new microRNAs from Medicago truncatula. Biochemical and Biophysical Research Communications 2008, 374:538-542.
68. Zhu QH, Upadhyaya NM, Gubler F, Helliwell CA. Overexpression of miR172 causes lost of spikelet determinacy and floral organ abnormalities in rice (Orzya sativa). BMC Plant Biology 2009, 9:149. http://dx.doi.org/10.1186/1471-2229-9-149, doi: