The miR156-SPL9-DFR pathway coordinates the relationship between development and abiotic stress tolerance in plants

Plant Journal

Volumn 80, Issue 6, 2014, Pages 1108-1117

  Cui, Long Gang ^a   Shan, Jun Xiang ^a   Shi, Min ^a   Gao, Ji Ping ^a   Lin, Hong Xuan ^a  

^a INSTITUTE OF GEOLOGY AND GEOPHYSICS   (China)

Author keywords

anthocyanin; Arabidopsis thaliana; development; miRNA; rice; stress tolerance

Indexed keywords

ANTHOCYANINS; RNA;

ARABIDOPSIS THALIANA; DEVELOPMENT; MIRNA; RICE; STRESS TOLERANCE;

PLANTS (BOTANY);

ARABIDOPSIS THALIANA;

ALCOHOL DEHYDROGENASE; ANTHOCYANIN; ARABIDOPSIS PROTEIN; DIHYDROFLAVANOL 4-REDUCTASE; MICRORNA; MIRN156 MICRORNA, ARABIDOPSIS; SPL9 PROTEIN, ARABIDOPSIS; TRANSACTIVATOR PROTEIN;

ADAPTATION; ARABIDOPSIS; FLOWER; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PHYSIOLOGICAL STRESS; PHYSIOLOGY; PLANT LEAF; PROMOTER REGION; SIGNAL TRANSDUCTION; TRANSGENIC PLANT;

ADAPTATION, PHYSIOLOGICAL; ALCOHOL OXIDOREDUCTASES; ANTHOCYANINS; ARABIDOPSIS; ARABIDOPSIS PROTEINS; FLOWERS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE EXPRESSION REGULATION, PLANT; MICRORNAS; PLANT LEAVES; PLANTS, GENETICALLY MODIFIED; PROMOTER REGIONS, GENETIC; SIGNAL TRANSDUCTION; STRESS, PHYSIOLOGICAL; TRANS-ACTIVATORS;

EID: 84916603302     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/tpj.12712     Document Type: Article

References (47)

1. Ambros, V., (2001) microRNAs: Tiny regulators with great potential. Cell, 107, 823-826.
2. Ambros, V., (2011) MicroRNAs and developmental timing. Curr. Opin. Genet. Dev. 21, 511-517.
3. Azuma, K., Ohyama, A., Ippoushi, K., Ichiyanagi, T., Takeuchi, A., Saito, T., and, Fukuoka, H., (2008) Structures and antioxidant activity of anthocyanins in many accessions of eggplant and its related species. J. Agric. Food Chem. 56, 10154-10159.
4. Balasubramanian, S., Sureshkumar, S., Lempe, J., and, Weigel, D., (2006) Potent induction of Arabidopsis thaliana flowering by elevated growth temperature. PLoS Genet. 2, 980-989.
5. Bergonzi, S., Albani, M.C., Ver Loren, van Themaat, E., Nordstrom, K.J., Wang, R., Schneeberger, K., Moerland, P.D., and, Coupland, G., (2013) Mechanisms of age-dependent response to winter temperature in perennial flowering of Arabis alpina. Science, 340, 1094-1097.
6. Carrington, J.C., and, Ambros, V., (2003) Role of microRNAs in plant and animal development. Science, 301, 336-338.
7. Chalker-Scott, L., (1999) Environmental significance of anthocyanins in plant stress responses. Photochem. Photobiol. 70, 1-9.
8. Franco-Zorrilla, J.M., Valli, A., Todesco, M., Mateos, I., Puga, M.I., Rubio-Somoza, I., Leyva, A., Weigel, D., Garcia, J.A., and, Paz-Ares, J., (2007) Target mimicry provides a new mechanism for regulation of microRNA activity. Nat. Genet. 39, 1033-1037.
9. Gou, J.Y., Felippes, F.F., Liu, C.J., Weigel, D., and, Wang, J.W., (2011) Negative regulation of anthocyanin biosynthesis in Arabidopsis by a miR156-targeted SPL transcription factor. Plant Cell, 23, 1512-1522.
10. Halfter, U., Ishitani, M., and, Zhu, J.K., (2000) The Arabidopsis SOS2 protein kinase physically interacts with and is activated by the calcium-binding protein SOS3. Proc. Natl Acad. Sci. USA, 97, 3735-3740.
11. Harb, A., Krishnan, A., Ambavaram, M.M.R., and, Pereira, A., (2010) Molecular and physiological analysis of drought stress in Arabidopsis reveals early responses leading to acclimation in plant growth. Plant Physiol. 154, 1254-1271.
12. Hellens, R.P., Allan, A.C., Friel, E.N., Bolitho, K., Grafton, K., Templeton, M.D., Karunairetnam, S., Gleave, A.P., and, Laing, W.A., (2005) Transient expression vectors for functional genomics, quantification of promoter activity and RNA silencing in plants. Plant Methods, 1, 13.
13. Henderson, I.R., and, Dean, C., (2004) Control of Arabidopsis flowering: the chill before the bloom. Development, 131, 3829-3838.
14. Huijser, P., and, Schmid, M., (2011) The control of developmental phase transitions in plants. Development, 138, 4117-4129.
15. Ishitani, M., Liu, J.P., Halfter, U., Kim, C.S., Shi, W.M., and, Zhu, J.K., (2000) SOS3 function in plant salt tolerance requires N-myristoylation and calcium binding. Plant Cell, 12, 1667-1677.
16. Kim, J.J., Lee, J.H., Kim, W., Jung, H.S., Huijser, P., and, Ahn, J.H., (2012) The microRNA156-SQUAMOSA PROMOTER BINDING PROTEIN-LIKE3 module regulates ambient temperature-responsive flowering via FLOWERING LOCUS T in Arabidopsis. Plant Physiol. 159, 461-478.
17. Lee, H., Yoo, S.J., Lee, J.H., Kim, W., Yoo, S.K., Fitzgerald, H., Carrington, J.C., and, Ahn, J.H., (2010) Genetic framework for flowering-time regulation by ambient temperature-responsive miRNAs in Arabidopsis. Nucleic Acids Res. 38, 3081-3093.
18. Lee, J.H., Ryu, H.S., Chung, K.S., Pose, D., Kim, S., Schmid, M., and, Ahn, J.H., (2013) Regulation of temperature-responsive flowering by MADS-box transcription factor repressors. Science, 342, 628-632.
19. Li, K.X., Wang, Y.N., Han, C.Y., Zhang, W.S., Jia, H.Z., and, Li, X., (2007) GA signaling and CO/FT regulatory module mediate salt-induced late flowering in Arabidopsis thaliana. Plant Growth Regul. 53, 195-206.
20. Liu, J.P., and, Zhu, J.K., (1998) A calcium sensor homolog required for plant salt tolerance. Science, 280, 1943-1945.
21. Liu, J., Ishitani, M., Halfter, U., Kim, C.S., and, Zhu, J.K., (2000) The Arabidopsis thaliana SOS2 gene encodes a protein kinase that is required for salt tolerance. Proc. Natl Acad. Sci. USA, 97, 3730-3734.
22. Liu, H.H., Tian, X., Li, Y.J., Wu, C.A., and, Zheng, C.C., (2008) Microarray-based analysis of stress-regulated microRNAs in Arabidopsis thaliana. RNA, 14, 836-843.
23. May, P., Liao, W., Wu, Y.J., Shuai, B., McCombie, W.R., Zhang, M.Q., and, Liu, Q.A., (2013) The effects of carbon dioxide and temperature on microRNA expression in Arabidopsis development. Nat. Commun., 4, 2145.
24. Oh, J.E., Kim, Y.H., Kim, J.H., Kwon, Y.R., and, Lee, H., (2011) Enhanced level of anthocyanin leads to increased salt tolerance in Arabidopsis PAP1-D plants upon sucrose treatment. J. Korean Soc. Appl. Biol. Chem. 54, 79-88.
25. Pasquinelli, A.E., and, Ruvkun, G., (2002) Control of developmental timing by microRNAs and their targets. Annu. Rev. Cell Dev. Biol. 18, 495-513.
26. Poethig, R.S., (2010) The past, present, and future of vegetative phase change. Plant Physiol. 154, 541-544.
27. Qi, T., Song, S., Ren, Q., Wu, D., Huang, H., Chen, Y., Fan, M., Peng, W., Ren, C., and, Xie, D., (2011) The Jasmonate-ZIM-domain proteins interact with the WD-Repeat/bHLH/MYB complexes to regulate Jasmonate-mediated anthocyanin accumulation and trichome initiation in Arabidopsis thaliana. Plant Cell, 23, 1795-1814.
28. + exchanger in Arabidopsis thaliana, by SOS2 and SOS3. Proc. Natl Acad. Sci. USA, 99, 8436-8441.
29. Rogers, K., and, Chen, X.M., (2013) Biogenesis, turnover, and mode of action of plant microRNAs. Plant Cell, 25, 2383-2399.
30. Schwab, R., Palatnik, J.F., Riester, M., Schommer, C., Schmid, M., and, Weigel, D., (2005) Specific effects of microRNAs on the plant transcriptome. Dev. Cell, 8, 517-527.
31. Shinozaki, K., and, YamaguchiShinozaki, K., (1997) Gene expression and signal transduction in water-stress response. Plant Physiol. 115, 327-334.
32. Shinozaki, K., and, Yamaguchi-Shinozaki, K., (2007) Gene networks involved in drought stress response and tolerance. J. Exp. Bot. 58, 221-227.
33. Srikanth, A., and, Schmid, M., (2011) Regulation of flowering time: all roads lead to Rome. Cell. Mol. Life Sci. 68, 2013-2037.
34. Stief, A., Altmann, S., Hoffmann, K., Pant, B.D., Scheible, W.R., and, Baurle, I., (2014) Arabidopsis miR156 regulates tolerance to recurring environmental stress through SPL transcription factors. Plant Cell, 26, 1792-1807.
35. Sunkar, R., and, Zhu, J.K., (2004) Novel and stress-regulated microRNAs and other small RNAs from Arabidopsis. Plant Cell, 16, 2001-2019.
36. Varkonyi-Gasic, E., Wu, R.M., Wood, M., Walton, E.F., and, Hellens, R.P., (2007) Protocol: a highly sensitive RT-PCR method for detection and quantification of microRNAs. Plant Methods, 3, 12.
37. Voinnet, O., (2009) Origin, biogenesis, and activity of plant microRNAs. Cell, 136, 669-687.
38. Wang, J.W., Czech, B., and, Weigel, D., (2009) miR156-regulated SPL transcription factors define an endogenous flowering pathway in Arabidopsis thaliana. Cell, 138, 738-749.
39. Wang, H., Fan, W., Li, H., Yang, J., Huang, J., and, Zhang, P., (2013) Functional characterization of dihydroflavonol-4-reductase in anthocyanin biosynthesis of purple sweet potato underlies the direct evidence of anthocyanins function against abiotic stresses. PLoS ONE, 8, e78484.
40. Wu, G., and, Poethig, R.S., (2006) Temporal regulation of shoot development in Arabidopsis thaliana by miR156 and its target SPL3. Development, 133, 3539-3547.
41. Wu, G., Park, M.Y., Conway, S.R., Wang, J.W., Weigel, D., and, Poethig, R.S., (2009) The sequential action of miR156 and miR172 regulates developmental timing in Arabidopsis. Cell, 138, 750-759.
42. Xie, K.B., Wu, C.Q., and, Xiong, L.Z., (2006) Genomic organization, differential expression, and interaction of SQUAMOSA promoter-binding-like transcription factors and microRNA156 in rice. Plant Physiol. 142, 280-293.
43. Xu, M.Y., Zhang, L., Li, W.W., Hu, X.L., Wang, M.B., Fan, Y.L., Zhang, C.Y., and, Wang, L., (2014) Stress-induced early flowering is mediated by miR169 in Arabidopsis thaliana. J. Exp. Bot. 65, 89-101.
44. Yang, L., Xu, M.L., Koo, Y., He, J., and, Poethig, R.S., (2013) Sugar promotes vegetative phase change in Arabidopsis thaliana by repressing the expression of MIR156A and MIR156C. Elife, 2, e00260.
45. Yu, S., Cao, L., Zhou, C.M., Zhang, T.Q., Lian, H., Sun, Y., Wu, J.Q., Huang, J.R., Wang, G.D., and, Wang, J.W., (2013) Sugar is an endogenous cue for juvenile-to-adult phase transition in plants. Elife, 2, e00269.
46. Zhou, X.F., Wang, G.D., Sutoh, K., Zhu, J.K., and, Zhang, W.X., (2008) Identification of cold-inducible microRNAs in plants by transcriptome analysis. Biochim. Biophys. Acta, 1779, 780-788.
47. Zhou, C.M., Zhang, T.Q., Wang, X., Yu, S., Lian, H., Tang, H., Feng, Z.Y., Zozomova-Lihova, J., and, Wang, J.W., (2013) Molecular basis of age-dependent vernalization in Cardamine flexuosa. Science, 340, 1097-1100.