Effects of drought on the microtranscriptome of field-grown sugarcane plants

Planta

Volumn 237, Issue 3, 2013, Pages 783-798

  Gentile, Agustina ^a   Ferreira, Thaís H ^a   Mattos, Raphael S ^a   Dias, Lara I ^a   Hoshino, Andrea A ^a   Carneiro, Monalisa S ^b   Souza, Glaucia M ^c   Calsa Jr , Tercílio ^d   Nogueira, Rejane M ^e   Endres, Laurício ^f   Menossi, Marcelo ^a  

^a UNIVERSITY OF CAMPINAS   (Brazil)

^b FEDERAL UNIVERSITY OF SÃO CARLOS   (Brazil)

^c UNIVERSITY OF SÃO PAULO   (Brazil)

^d DEPARTAMENTO DE MICOLOGIA   (Brazil)

^e UNIVERSIDADE FEDERAL RURAL DE PERNAMBUCO   (Brazil)

^f FEDERAL UNIVERSITY OF ALAGOAS   (Brazil)

Author keywords

Bioenergy; Drought stress; Field conditions; MicroRNAs; Solexa sequencing; Sugarcane

Indexed keywords

SACCHARUM;

EID: 84874308411     PISSN: 00320935     EISSN: 14322048     Source Type: Journal    
DOI: 10.1007/s00425-012-1795-7     Document Type: Article

References (83)

1. Agarwal PK, Agarwal P, Reddy MK, Sopory SK (2006) Role of DREB transcription factors in abiotic and biotic stress tolerance in plants. Plant Cell Rep 25: 1263-1274.
2. Audic S, Claverie JM (1997) The significance of digital gene expression profiles. Genome Res 7: 986-995.
3. Axtell MJ (2008) Evolution of microRNAs and their targets: are all microRNAs biologically relevant? BBA Gene Regul Mech 1779: 725-734.
4. Axtell MJ, Bartel DP (2005) Antiquity of microRNAs and their targets in land plants. Plant Cell 17: 1658-1673.
5. Bartel DP (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116: 281-297.
6. Bentley DR (2006) Whole-genome re-sequencing. Curr Opin Genet Dev 16: 545-552.
7. Boyer RS (1982) Plant productivity and environment. Science 218: 443-448.
8. Carrington JC, Ambros V (2003) Role of microRNAs in plant and animal development. Science 301: 336-338.
9. Chapman EJ, Carrington JC (2007) Specialization and evolution of endogenous small RNA pathways. Nat Rev Genet 8: 884-896.
10. Chaves MM, Pereira JS, Maroco J, Rodrigues ML, Ricardo CP, Osorio ML, Carvalho I, Faria T, Pinheiro C (2002) How plants cope with water stress in the field. Photosynthesis and growth. Ann Bot 89: 907-916.
11. Chaves MM, Flexas J, Pinheiro C (2009) Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell. Ann Bot 103: 551-560.
12. Chen CF, Ridzon DA, Broomer AJ, Zhou ZH, Lee DH, Nguyen JT, Barbisin M, Xu NL, Mahuvakar VR, Andersen MR, Lao KQ, Livak KJ, Guegler KJ (2005) Real-time quantification of microRNAs by stem-loop RT-PCR. Nucleic Acids Res 33: e179.
13. Combier JP, Frugier F, de Billy F, Boualem A, El-Yahyaoui F, Moreau S, Vernie T, Ott T, Gamas P, Crespi M, Niebel A (2006) MtHAP2-1 is a key transcriptional regulator of symbiotic nodule development regulated by microRNA169 in Medicago truncatula. Genes Dev 20: 3084-3088.
14. Dai X, Zhao PX (2011) psRNATarget: a plant small RNA target analysis server. Nucleic Acids Res 39: W155-W159.
15. Dezar CA, Gago GM, Gonzalez DH, Chan RL (2005) Hahb-4, a sunflower homeobox-leucine zipper gene, is a developmental regulator and confers drought tolerance to Arabidopsis thaliana plants. Transgenic Res 14: 429-440.
16. Dharmasiri N, Dharmasiri S, Estelle M (2005) The F-box protein TIR1 is an auxin receptor. Nature 435: 441-445.
17. Ditt RF, Gentile A, Tavares RG, Camargo SR, Fernandez JH, da Silva MJ, Menossi M (2011) Analysis of the stress-inducible transcription factor SsNAC23 in sugarcane plants. Sci Agr 68: 454-461.
18. Eckardt NA (2004) Small RNA on the move. Plant Cell 16: 1951-1954.
19. Fahlgren N, Carrington JC (2010) miRNA target prediction in plants. Methods Mol Biol 592: 51-57.
20. Ferreira TH, Gentile A, Vilela RD, Costa GGL, Dias LI, Endres L, Menossi M (2012) microRNAs associated with drought response in the bioenergy crop sugarcane (Saccharum spp.). PLoS One 7: e46703.
21. Flexas J, Bota J, Galmes J, Medrano H, Ribas-Carbo M (2006) Keeping a positive carbon balance under adverse conditions: responses of photosynthesis and respiration to water stress. Physiol Plantarum 127: 343-352.
22. Floyd SK, Bowman JL (2004) Gene regulation: ancient microRNA target sequences in plants. Nature 428: 485-486.
23. Golldack D, Luking I, Yang O (2011) Plant tolerance to drought and salinity: stress regulating transcription factors and their functional significance in the cellular transcriptional network. Plant Cell Rep 30: 1383-1391.
24. Gustafson AM, Allen E, Givan S, Smith D, Carrington JC, Kasschau KD (2005) ASRP: the Arabidopsis small RNA project database. Nucleic Acids Res 33: D637-D640.
25. Gutowski JA, Lienhard GE (1976) Transition-state analogs for thiamin pyrophosphate-dependent enzymes. J Biol Chem 251: 2863-2866.
26. Hegedus D, Yu M, Baldwin D, Gruber M, Sharpe A, Parkin I, Whitwill S, Lydiate D (2003) Molecular characterization of Brassica napus NAC domain transcriptional activators induced in response to biotic and abiotic stress. Plant Mol Biol 53: 383-397.
27. Hoen PA, Ariyurek Y, Thygesen HH, Vreugdenhil E, Vossen RH, De Menezes RX, Boer JM, van Ommen GJ, Den Dunnen JT (2008) Deep sequencing-based expression analysis shows major advances in robustness, resolution and inter-lab portability over five microarray platforms. Nucleic Acids Res 36: e141.
28. Hofacker IL (2003) Vienna RNA secondary structure server. Nucleic Acids Res 31: 3429-3431.
29. Hynes LW, Peng J, Richards DE, Harberd NP (2003) Transgenic expression of the Arabidopsis DELLA proteins GAI and gai confers altered gibberellin response in tobacco. Transgenic Res 12: 707-714.
30. Inman-Bamber NG, Smith DM (2005) Water relations in sugarcane and response to water deficits. Field Crop Res 92: 185-202.
31. Jian XY, Zhang L, Li GL, Zhang L, Wang XJ, Cao XF, Fang XH, Chen F (2010) Identification of novel stress-regulated microRNAs from Oryza sativa L. Genomics 95: 47-55.
32. Jones-Rhoades MW, Bartel DP (2004) Computational identification of plant microRNAs and their targets, including a stress-induced miRNA. Mol Cell 14: 787-799.
33. Jones-Rhoades MW, Bartel DP, Bartel B (2006) MicroRNAS and their regulatory roles in plants. Annu Rev Plant Biol 57: 19-53.
34. Kidner C, Timmermans M (2006) In situ hybridization as a tool to study the role of microRNAs in plant development. Methods Mol Biol 342: 159-179.
35. Krishnaswamy S, Verma S, Rahman MH, Kav NN (2011) Functional characterization of four APETALA2-family genes (RAP2. 6, RAP2. 6L, DREB19 and DREB26) in Arabidopsis. Plant Mol Biol 75: 107-127.
36. Li WX, Oono Y, Zhu J, He XJ, Wu JM, Iida K, Lu XY, Cui X, Jin H, Zhu JK (2008) The Arabidopsis NFYA5 transcription factor is regulated transcriptionally and posttranscriptionally to promote drought resistance. Plant Cell 20: 2238-2251.
37. Llave C, Kasschau KD, Rector MA, Carrington JC (2002) Endogenous and silencing-associated small RNAs in plants. Plant Cell 14: 1605-1619.
38. Lu S, Sun YH, Shi R, Clark C, Li L, Chiang VL (2005) Novel and mechanical stress-responsive MicroRNAs in Populus trichocarpa that are absent from Arabidopsis. Plant Cell 17: 2186-2203.
39. Ma HS, Liang D, Shuai P, Xia XL, Yin WL (2010) The salt- and drought-inducible poplar GRAS protein SCL7 confers salt and drought tolerance in Arabidopsis thaliana. J Exp Bot 61: 4011-4019.
40. Matts J, Jagadeeswaran G, Roe BA, Sunkar R (2010) Identification of microRNAs and their targets in switchgrass, a model biofuel plant species. J Plant Physiol 167: 896-904.
41. Maybank J, Bonsal BR, Jones K, Lawford RG, O'Brien EG et al (1995) Drought as a natural disaster. Atmos Ocean 33: 195-222.
42. Meyers BC, Axtell MJ, Bartel B, Bartel DP, Baulcombe D, Bowman JL, Cao X, Carrington JC, Chen X, Green PJ, Griffiths-Jones S, Jacobsen SE, Mallory AC, Martienssen RA, Poethig RS, Qi Y, Vaucheret H, Voinnet O, Watanabe Y, Weigel D, Zhu JK (2008) Criteria for annotation of plant MicroRNAs. Plant Cell 20: 3186-3190.
43. Molnar A, Schwach F, Studholme DJ, Thuenemann EC, Baulcombe DC (2007) miRNAs control gene expression in the single-cell alga Chlamydomonas reinhardtii. Nature 447: 1126-1129.
44. Nelson DE, Repetti PP, Adams TR, Creelman RA, Wu J, Warner DC, Anstrom DC, Bensen RJ, Castiglioni PP, Donnarummo MG, Hinchey BS, Kumimoto RW, Maszle DR, Canales RD, Krolikowski KA, Dotson SB, Gutterson N, Ratcliffe OJ, Heard JE (2007) 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 104: 16450-16455.
45. Nemeria N, Yan Y, Zhang Z, Brown AM, Arjunan P, Furey W, Guest JR, Jordan F (2001) Inhibition of the Escherichia coli pyruvate dehydrogenase complex E1 subunit and its tyrosine 177 variants by thiamin 2-thiazolone and thiamin 2-thiothiazolone diphosphates-evidence for reversible tight-binding inhibition. J Biol Chem 276: 45969-45978.
46. Pabinger S, Thallinger GG, Snajder R, Eichhorn H, Rader R, Trajanoski Z (2009) QPCR: application for real-time PCR data management and analysis. BMC Bioinform 10: 268.
47. Pantaleo V, Szittya G, Moxon S, Miozzi L, Moulton V, Dalmay T, Burgyan J (2010) Identification of grapevine microRNAs and their targets using high-throughput sequencing and degradome analysis. Plant J 62: 960-976.
48. Papini-Terzi FS, Rocha FR, Vencio RZN, Oliveira KC, Felix JD, Vicentini R, Rocha CD, Simoes ACQ, Ulian EC, Di Mauro SMZ, Da Silva AM, Pereira CAD, Menossi M, Souza GM (2005) Transcription profiling of signal transduction-related genes in sugarcane tissues. DNA Res 12: 27-38.
49. Perez-Torres CA, Lopez-Bucio J, Cruz-Ramirez A, Ibarra-Laclette E, Dharmasiri S, Estelle M, Herrera-Estrella L (2008) Phosphate availability alters lateral root development in Arabidopsis by modulating auxin sensitivity via a mechanism involving the TIR1 auxin receptor. Plant Cell 20: 3258-3272.
50. Pysh LD, Wysocka-Diller JW, Camilleri C, Bouchez D, Benfey PN (1999) The GRAS gene family in Arabidopsis: sequence characterization and basic expression analysis of the Scarecrow-like genes. Plant J 18: 111-119.
51. Reinhart BJ, Weinstein EG, Rhoades MW, Bartel B, Bartel DP (2002) MicroRNAs in plants. Genes Dev 16: 1616-1626.
52. Rhoades MW, Reinhart BJ, Lim LP, Burge CB, Bartel B, Bartel DP (2002) Prediction of plant microRNA targets. Cell 110: 513-520.
53. Rivero RM, Gimeno J, van Deynze A, Walia H, Blumwald E (2010) Enhanced cytokinin synthesis in tobacco plants expressing PSARK: IPT prevents the degradation of photosynthetic protein complexes during drought. Plant Cell Physiol 51: 1929-1941.
54. Rocha FR, Papini-Terzi FS, Nishiyama MY, Vencio RZN, Vicentini R, Duarte RDC, de Rosa VE, Vinagre F, Barsalobres C, Medeiros AH, Rodrigues FA, Ulian EC, Zingaretti SM, Galbiatti JA, Almeida RS, Figueira AVO, Hemerly AS, Silva-Filho MC, Menossi M, Souza GM (2007) Signal transduction-related responses to phytohormones and environmental challenges in sugarcane. BMC Genomics 8: 71.
55. Ruan MB, Zhao YT, Meng ZH, Wang XJ, Yang WC (2009) Conserved miRNA analysis in Gossypium hirsutum through small RNA sequencing. Genomics 94: 263-268.
56. Ruby JG, Jan C, Player C, Axtell MJ, Lee W, Nusbaum C, Ge H, Bartel DP (2006) Large-scale sequencing reveals 21U-RNAs and additional microRNAs and endogenous siRNAs in C. elegans. Cell 127: 1193-1207.
57. 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.
58. Santos D (2010) Distribuição do sistema radicular e produtividade de cana-de-açúcar (Saccharum ssp.) fertirrigada por gotejamento subsuperficial. Dissertation, Universidade Estadual Paulista "Júlio de Mesquita Filho".
59. Santos AA, Lopes KV, Apfata JA, Fontes EP (2010) NSP-interacting kinase, NIK: a transducer of plant defence signalling. J Exp Bot 61: 3839-3845.
60. Shendure J, Porreca GJ, Reppas NB, Lin X, McCutcheon JP, Rosenbaum AM, Wang MD, Zhang K, Mitra RD, Church GM (2005) Accurate multiplex polony sequencing of an evolved bacterial genome. Science 309: 1728-1732.
61. Stephenson TJ, McIntyre CL, Collet C, Xue GP (2007) Genome-wide identification and expression analysis of the NF-Y family of transcription factors in Triticum aestivum. Plant Mol Biol 65: 77-92.
62. Sun H, Huang X, Xu X, Lan H, Huang J, Zhang H-S (2011) ENAC1, a NAC transcription factor, is an early and transient response regulator induced by abiotic stress in rice (Oryza sativa L.). Mol Biotechnol 52: 1-10.
63. Sunkar R, Zhu JK (2004) Novel and stress-regulated microRNAs and other small RNAs from Arabidopsis. Plant Cell 16: 2001-2019.
64. Thiebaut F, Grativol C, Carnavale-Bottino M, Rojas CA, Tanurdzic M, Farinelli L, Martienssen RA, Hemerly AS, Ferreira PC (2012) Computational identification and analysis of novel sugarcane microRNAs. BMC Genomics 13: 290.
65. Unver T, Budak H (2009) Conserved microRNAs and their targets in model grass species Brachypodium distachyon. Planta 230: 659-669.
66. Varkonyi-Gasic E, Wu RM, Wood M, Walton EF, Hellens RP (2007) Protocol: a highly sensitive RT-PCR method for detection and quantification of microRNAs. Plant Methods 3: 12.
67. Vasconcelos ACM, Casagrande AA, Perecin D, Jorge LAC, Landell MGA (2003) Avaliação do sistema radicular da cana-de-açúcar por diferentes métodos. R Bras Ci Solo 27: 849-858.
68. Vettore AL, da Silva FR, Kemper EL, Arruda P (2001) The libraries that made SUCEST. Genet Mol Biol 24: 1-7.
69. Voinnet O (2009) Origin, biogenesis, and activity of plant microRNAs. Cell 136: 669-687.
70. Wei B, Cai T, Zhang RZ, Li AL, Huo NX, Li S, Gu YQ, Vogel J, Jia JZ, Qi YJ, Mao L (2009) Novel microRNAs uncovered by deep sequencing of small RNA transcriptomes in bread wheat (Triticum aestivum L.) and Brachypodium distachyon (L.) Beauv. Funct Integr Genomic 9: 499-511.
71. Wu L, Zhang QQ, Zhou HY, Ni FR, Wu XY, Qi YJ (2009) Rice microRNA effector complexes and targets. Plant Cell 21: 3421-3435.
72. Xin M, Wang Y, Yao Y, Xie C, Peng H, Ni Z, Sun Q (2010) Diverse set of microRNAs are responsive to powdery mildew infection and heat stress in wheat (Triticum aestivum L.). BMC Plant Biol 10: 123.
73. Yang XZ, Li L (2011) miRDeep-P: a computational tool for analyzing the microRNA transcriptome in plants. Bioinformatics 27: 2614-2615.
74. Yang XZ, Zhang HY, Li L (2011) Global analysis of gene-level microRNA expression in Arabidopsis using deep sequencing data. Genomics 98: 40-46.
75. Zanca AS, Vicentini R, Ortiz-Morea FA, Del Bem LEV, da Silva MJ, Vincentz M, Nogueira FTS (2010) Identification and expression analysis of microRNAs and targets in the biofuel crop sugarcane. BMC Plant Biol 10: 260.
76. Zhang J, Xu Y, Huan Q, Chong K (2009a) Deep sequencing of Brachypodium small RNAs at the global genome level identifies microRNAs involved in cold stress response. BMC Genomics 10: 449.
77. Zhang LF, Chia JM, Kumari S, Stein JC, Liu ZJ, Narechania A, Maher CA, Guill K, McMullen MD, Ware D (2009b) A genome-wide characterization of microRNA genes in maize. Plos Genet 5: e1000716.
78. Zhao B, Liang R, Ge L, Li W, Xiao H, Lin H, Ruan K, Jin Y (2007a) Identification of drought-induced microRNAs in rice. Biochem Biophys Res Commun 354: 585-590.
79. Zhao BT, Liang RQ, Ge LF, Li W, Xiao HS, Lin HX, Ruan KC, Jin YX (2007b) Identification of drought-induced microRNAs in rice. Biochem Biophy Res Comm 354: 585-590.
80. Zhao T, Li G, Mi S, Li S, Hannon GJ, Wang XJ, Qi Y (2007c) A complex system of small RNAs in the unicellular green alga Chlamydomonas reinhardtii. Genes Dev 21: 1190-1203.
81. Zhao B, Ge L, Liang R, Li W, Ruan K, Lin H, Jin Y (2009) Members of miR-169 family are induced by high salinity and transiently inhibit the NF-YA transcription factor. BMC Mol Biol 10: 29.
82. Zhao CZ, Xia H, Frazier TP, Yao YY, Bi YP, Li AQ, Li MJ, Li CS, Zhang BH, Wang XJ (2010) Deep sequencing identifies novel and conserved microRNAs in peanuts (Arachis hypogaea L.). BMC Plant Biol 10: 3.
83. Zhou L, Liu Y, Liu Z, Kong D, Duan M, Luo L (2010) Genome-wide identification and analysis of drought-responsive microRNAs in Oryza sativa. J Exp Bot 61: 4157-4168.