Identification of conserved and novel microRNAs that are responsive to heat stress in Brassica rapa

Journal of Experimental Botany

Volumn 63, Issue 2, 2012, Pages 1025-1038

  Yu, Xiang ^a   Wang, Han ^a   Lu, Yizhen ^b   De Ruiter, Marjo ^c   Cariaso, Mike ^c   Prins, Marcel ^c   Van Tunen, Arjen ^c   He, Yuke ^a  

^a INSTITUTE OF PLANT PHYSIOLOGY AND ECOLOGY   (China)

^b ZHEJIANG UNIVERSITY   (China)

^c KEYGENE N V   (Netherlands)

Author keywords

Brassica rapa; heat response; miRNA; small RNA

Indexed keywords

MICRORNA; PLANT RNA;

ARTICLE; BRASSICA RAPA; DOWN REGULATION; GENE EXPRESSION REGULATION; GENETICS; HEAT; HIGH THROUGHPUT SEQUENCING; METABOLISM; MOLECULAR EVOLUTION; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHYSIOLOGICAL STRESS; PHYSIOLOGY; PLANT GENOME; REAL TIME POLYMERASE CHAIN REACTION; SEQUENCE ANALYSIS;

BASE SEQUENCE; BRASSICA RAPA; DOWN-REGULATION; EVOLUTION, MOLECULAR; GENE EXPRESSION REGULATION, PLANT; GENOME, PLANT; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HOT TEMPERATURE; MICRORNAS; MOLECULAR SEQUENCE DATA; REAL-TIME POLYMERASE CHAIN REACTION; RNA, PLANT; SEQUENCE ANALYSIS, RNA; STRESS, PHYSIOLOGICAL;

ARABIDOPSIS; ARABIDOPSIS THALIANA; BRASSICA RAPA; BRASSICA RAPA SUBSP. PEKINENSIS;

EID: 84862907762     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/err337     Document Type: Article

References (58)

1. Addo-Quaye C, Eshoo TW, Bartel DP, Axtell MJ. 2008. Endogenous siRNA and miRNA targets identified by sequencing of the Arabidopsis degradome. Current Biology 18, 758-762.
2. Axtell MJ, Jan C, Rajagopalan R, Bartel DP. 2006. A two-hit trigger for siRNA biogenesis in plants. Cell 127, 565-577. (Pubitemid 44647429)
3. Babiarz JE, Ruby JG, Wang Y, Bartel DP, Blelloch R. 2008. Mouse ES cells express endogenous shRNAs, siRNAs, and other Microprocessor-independent, Dicer-dependent small RNAs. Genes and Development 22, 2773-2785.
4. Brodersen P, Sakvarelidze-Achard L, Bruun-Rasmussen M, Dunoyer P, Yamamoto YY, Sieburth L, Voinnet O. 2008. Widespread translational inhibition by plant miRNAs and siRNAs. Science 320, 1185-1190. (Pubitemid 351929501)
5. Chellappan P, Xia J, Zhou X, Gao S, Zhang X, Coutino G, Vazquez F, Zhang W, Jin H. 2010. SiRNAs from miRNA sites mediate DNA methylation of target genes. Nucleic Acids Research 38, 6883-6894.
6. Chen HM, Chen LT, Patel K, Li YH, Baulcombe DC, Wu SH. 2010. 22-Nucleotide RNAs trigger secondary siRNA biogenesis in plants. Proceedings of the National Academy of Sciences, USA 107, 15269-15274.
7. Chen K, Rajewsky N. 2007. The evolution of gene regulation by transcription factors and microRNAs. Nature Reviews Genetics 8, 93-103. (Pubitemid 46122839)
8. Chen X. 2004. A MicroRNA as a translational repressor of APETALA2 in Arabidopsis flower developmenT. Science 303, 2022-2024.
9. Chen X. 2009. Small RNAs and their roles in plant development. Annual Review of Cell and Developmental Biology 25, 21-44.
10. Cuperus JT, Carbonell A, Fahlgren N, Garcia-Ruiz H, Burke RT, Takeda A, Sullivan CM, Gilbert SD, Montgomery TA, Carrington JC. 2010. Unique functionality of 22-nt miRNAs in triggering RDR6-dependent siRNA biogenesis from target transcripts in Arabidopsis. Nature Structural and Molecular Biology 17, 997-1003.
11. de Felippes FF, Schneeberger K, Dezulian T, Huson DH, Weigel D. 2008. Evolution of Arabidopsis thaliana microRNAs from random sequences. RNA 14, 2455-2459.
12. Devor EJ, Peek AS, Lanier W, Samollow PB. 2009. Marsupial-specific microRNAs evolved from marsupial-specific transposable elements. Gene 448, 187-191.
13. Fahlgren N, Jogdeo S, Kasschau KD, Sullivan CM, Chapman EJ, Laubinger S, Smith LM, Dasenko M, Givan SA, Weigel D, Carrington JC. 2010. MicroRNA gene evolution in Arabidopsis lyrata and Arabidopsis thaliana. The Plant Cell 22, 1074-1089.
14. Fujii H, Chiou TJ, Lin SI, Aung K, Zhu JK. 2005. A miRNA involved in phosphate-starvation response in Arabidopsis. Current Biology 15, 2038-2043. (Pubitemid 41654628)
15. German MA, Pillay M, Jeong DH, et al. 2008. Global identification of microRNA-target RNA pairs by parallel analysis of RNA ends. Nat Biotechnol 26, 941-946.
16. He XF, Fang YY, Feng L, Guo HS. 2008. Characterization of conserved and novel microRNAs and their targets, including a TuMV-induced TIR-NBS-LRR class R gene-derived novel miRNA in Brassica. FEBS Letters 582, 2445-2452.
17. Hsieh LC, Lin SI, Shih AC, Chen JW, Lin WY, Tseng CY, Li WH, Chiou TJ. 2009. Uncovering small RNA-mediated responses to phosphate deficiency in Arabidopsis by deep sequencing. Plant Physiology 151, 2120-2132.
18. Jamalkandi SA, Masoudi-Nejad A. 2009. Reconstruction of Arabidopsis thaliana fully integrated small RNA pathway. Functional and Integrated Genomics 9, 419-432.
19. Jones-Rhoades MW, Bartel DP, Bartel B. 2006. MicroRNAs and their regulatory roles in plants. Annual Review of Plant Biology 57, 19-53. (Pubitemid 44061017)
20. Kotak S, Larkindale J, Lee U, von Koskull-Doring P, Vierling E, Scharf KD. 2007. Complexity of the heat stress response in plants. Current Opinion in Plant Biology 10, 310-316. (Pubitemid 46710484)
21. Kurihara Y, Takashi Y, Watanabe Y. 2006. The interaction between DCL1 and HYL1 is important for efficient and precise processing of pri-miRNA in plant microRNA biogenesis. RNA 12, 206-212. (Pubitemid 43121925)
22. Kutter C, Schob H, Stadler M, Meins F, Jr., Si-Ammour A. 2007. MicroRNA-mediated regulation of stomatal development in Arabidopsis. The Plant Cell 19, 2417-2429. (Pubitemid 47583834)
23. Kwon Y, Kim SH, Jung MS, Kim MS, Oh JE, Ju HW, Kim KI, Vierling E, Lee H, Hong SW. 2007. Arabidopsis hot2 encodes an endochitinase-like protein that is essential for tolerance to heat, salt and drought stresses. The Plant Journal 49, 184-193. (Pubitemid 46058945)
24. Lanet E, Delannoy E, Sormani R, Floris M, Brodersen P, Crete P, Voinnet O, Robaglia C. 2009. Biochemical evidence for translational repression by Arabidopsis microRNAs. The Plant Cell 21, 1762-1768.
25. Larkindale J, Hall JD, Knight MR, Vierling E. 2005. Heat stress phenotypes of Arabidopsis mutants implicate multiple signaling pathways in the acquisition of thermotolerance. Plant Physiology 138, 882-897. (Pubitemid 43793166)
26. Lelandais-Briere C, Naya L, Sallet E, Calenge F, Frugier F, Hartmann C, Gouzy J, Crespi M. 2009. Genome-wide Medicago truncatula small RNA analysis revealed novel microRNAs and isoforms differentially regulated in roots and nodules. The Plant Cell 21, 2780-2796.
27. Li T, Li H, Zhang YX, Liu JY. 2010a. Identification and analysis of seven H2O2-responsive miRNAs and 32 new miRNAs in the seedlings of rice (Oryza sativa L. ssp. indica). Nucleic Acids Research 39, 2821-2833.
28. 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. The Plant Cell 20, 2238-2251. (Pubitemid 352844522)
29. Li YF, Zheng Y, Addo-Quaye C, Zhang L, Saini A, Jagadeeswaran G, Axtell MJ, Zhang W, Sunkar R. 2010b. Transcriptome-wide identification of microRNA targets in rice. The Plant Journal 62, 742-759.
30. Liu HT, Gao F, Cui SJ, Han JL, Sun DY, Zhou RG. 2006. Primary evidence for involvement of IP3 in heat-shock signal transduction in Arabidopsis. Cell Res 16, 394-400.
31. Liu Z, Jia L, Mao Y, He Y. 2010. Classification and quantification of leaf curvature. Journal of Experimental Botany 61, 2757-2767.
32. Liu Z, Jia L, Wang H, He Y. 2011. HYL1 regulates the balance between adaxial and abaxial identity for leaf flattening via miRNA-mediated pathways. Journal of Experimental Botany 62, 4367-4381.
33. Mallory AC, Bartel DP, Bartel B. 2005. MicroRNA-directed regulation of Arabidopsis AUXIN RESPONSE FACTOR17 is essential for proper development and modulates expression of early auxin response genes. The Plant Cell 17, 1360-1375. (Pubitemid 43138190)
34. Meyers BC, Axtell MJ, Bartel B, et al. 2008. Criteria for annotation of plant MicroRNAs. The Plant Cell 20, 3186-3190.
35. Mittler R. 2006. Abiotic stress, the field environment and stress combination. Trends Plant Sci 11, 15-19. (Pubitemid 43053973)
36. Miyoshi K, Miyoshi T, Siomi H. 2010. Many ways to generate microRNA-like small RNAs: non-canonical pathways for microRNA production. Molecular Genetics and Genomics 284, 95-103.
37. Mun JH, Kwon SJ, Yang TJ, et al. 2009. Genome-wide comparative analysis of the Brassica rapa gene space reveals genome shrinkage and differential loss of duplicated genes after whole genome triplication. Genome Biology 10, R111.
38. 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. The Plant Journal 62, 960-976.
39. Piriyapongsa J, Jordan IK. 2008. Dual coding of siRNAs and miRNAs by plant transposable elements. RNA 14, 814-821. (Pubitemid 351574902)
40. Reyes JL, Chua NH. 2007. ABA induction of miR159 controls transcript levels of two MYB factors during Arabidopsis seed germination. The Plant Journal 49, 592-606. (Pubitemid 46233079)
41. Sakuma Y, Maruyama K, Qin F, Osakabe Y, Shinozaki K, Yamaguchi-Shinozaki K. 2006. Dual function of an Arabidopsis transcription factor DREB2A in water-stress-responsive and heat-stress-responsive gene expression. Proceedings of the National Academy of Sciences, USA 103, 18822-18827. (Pubitemid 44913494)
42. Shukla LI, Chinnusamy V, Sunkar R. 2008. The role of microRNAs and other endogenous small RNAs in plant stress responses. Biochimica Biophysica Acta 1779, 743-748.
43. Sieber P, Wellmer F, Gheyselinck J, Riechmann JL, Meyerowitz EM. 2007. Redundancy and specialization among plant microRNAs: role of the MIR164 family in developmental robustness. Development 134, 1051-1060. (Pubitemid 46630073)
44. Snowdon RJ. 2007. Cytogenetics and genome analysis in Brassica crops. Chromosome Research 15, 85-95. (Pubitemid 46295260)
45. Sunkar R, Kapoor A, Zhu JK. 2006. Posttranscriptional induction of two Cu/Zn superoxide dismutase genes in Arabidopsis is mediated by downregulation of miR398 and important for oxidative stress tolerance. The Plant Cell 18, 2051-2065. (Pubitemid 44260196)
46. Suzuki N, Rizhsky L, Liang H, Shuman J, Shulaev V, Mittler R. 2005. Enhanced tolerance to environmental stress in transgenic plants expressing the transcriptional coactivator multiprotein bridging factor 1c. Plant Physiology 139, 1313-1322. (Pubitemid 43786833)
47. Town CD, Cheung F, Maiti R, et al. 2006. Comparative genomics of Brassica oleracea and Arabidopsis thaliana reveal gene loss, fragmentation, and dispersal after polyploidy. The Plant Cell 18, 1348-1359. (Pubitemid 43956101)
48. Vazquez F, Blevins T, Ailhas J, Boller T, Meins F. Jr 2008. Evolution of Arabidopsis MIR genes generates novel microRNA classes. Nucleic Acids Research 36, 6429-6438.
49. Wang JW, Czech B, Weigel D. 2009. MiR156-regulated SPL transcription factors define an endogenous flowering pathway in Arabidopsis thaliana. Cell 138, 738-749.
50. Wang L, Yu X, Wang H, Lu YZ, de Ruiter M, Prins M, He YK. 2011. A novel class of heat-responsive small RNAs derived from the chloroplast genome of Chinese cabbage (Brassica rapa). BMC Genomics 12, 289.
51. Wang P, Duan W, Takabayashi A, Endo T, Shikanai T, Ye JY, Mi H. 2006. Chloroplastic NAD(P)H dehydrogenase in tobacco leaves functions in alleviation of oxidative damage caused by temperature stress. Plant Physiology 141, 465-474. (Pubitemid 43974541)
52. Wu G, Park MY, Conway SR, Wang JW, Weigel D, Poethig RS. 2009. The sequential action of miR156 and miR172 regulates developmental timing in Arabidopsis. Cell 138, 750-759.
53. Wu L, Zhou H, Zhang Q, Zhang J, Ni F, Liu C, Qi Y. 2010. DNA methylation mediated by a microRNA pathway. Molecular Cell 38, 465-475.
54. 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 Biology 10, 123.
55. Yang X, Wen X, Gong H, Lu Q, Yang Z, Tang Y, Liang Z, Lu C. 2007. Genetic engineering of the biosynthesis of glycinebetaine enhances thermotolerance of photosystem II in tobacco plants. Planta 225, 719-733. (Pubitemid 46204237)
56. Zhang W, Gao S, Zhou X, Xia J, Chellappan P, Zhang X, Jin H. 2010. Multiple distinct small RNAs originate from the same microRNA precursors. Genome Biology 11, R81.
57. Zhou GK, Kubo M, Zhong R, Demura T, Ye ZH. 2007. Overexpression of miR165 affects apical meristem formation, organ polarity establishment and vascular development in Arabidopsis. The Plant Cell Physiol 48, 391-404. (Pubitemid 47355538)
58. Zhu QH, Spriggs A, Matthew L, Fan L, Kennedy G, Gubler F, Helliwell C. 2008. A diverse set of microRNAs and microRNA-like small RNAs in developing rice grains. Genome Research 18, 1456-1465.