MiR408 is involved in abiotic stress responses in Arabidopsis

Plant Journal

Volumn 84, Issue 1, 2015, Pages 169-187

  Ma, Chao ^a,b   Burd, Shaul ^b   Lers, Amnon ^b  

^a SHANGHAI JIAO TONG UNIVERSITY   (China)

^b VOLCANI CENTER   (Israel)

Author keywords

abiotic stress; Arabidopsis thaliana; copper; miR408; miRNA; oxidative stress

Indexed keywords

ANTIOXIDANTS; COPPER; COPPER COMPOUNDS; DROUGHT; GENE EXPRESSION; OSMOSIS; OXIDATIVE STRESS; PLANTS (BOTANY);

ABIOTIC STRESS; ABIOTIC STRESS TOLERANCES; ARABIDOPSIS THALIANA; ENVIRONMENTAL CONDITIONS; GLUTATHIONE S-TRANSFERASES; MIR408; MIRNA; PLANT MICRORNAS (MIRNAS);

RNA;

ARABIDOPSIS PROTEIN; MICRORNA; MIRN408 MICRORNA, ARABIDOPSIS;

ARABIDOPSIS; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MOLECULAR GENETICS; PHYSIOLOGICAL STRESS; PHYSIOLOGY; TRANSGENIC PLANT;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; GENE EXPRESSION REGULATION, PLANT; MICRORNAS; MOLECULAR SEQUENCE DATA; PLANTS, GENETICALLY MODIFIED; STRESS, PHYSIOLOGICAL;

EID: 84942750488     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/tpj.12999     Document Type: Article

References (130)

1. Abdel-Ghany, S.E., and, Pilon, M., (2008) MicroRNA-mediated systemic down-regulation of copper protein expression in response to low copper availability in Arabidopsis. J. Biol. Chem. 283, 15932-15945.
2. Abdel-Ghany, S.E., Burkhead, J.L., Gogolin, K.A., Andres-Colas, N., Bodecker, J.R., Puig, S., Penarrubia, L., and, Pilon, M., (2005) AtCCS is a functional homolog of the yeast copper chaperone Ccs1/Lys7. FEBS Lett. 579, 2307-2312.
3. Adrees, M., Ali, S., Rizwan, M., Ibrahim, M., Abbas, F., Farid, M., Zia-ur-Rehman, M., Irshad, M.K., and, Bharwana, S.A., (2015) The effect of excess copper on growth and physiology of important food crops: a review. Environ. Sci. Pollut. Res. 22, 8148-8162.
4. Alscher, R.G., Erturk, N., and, Heath, L.S., (2002) Role of superoxide dismutases (SODs) in controlling oxidative stress in plants. J. Exp. Bot. 53, 1331-1341.
5. Axtell, M.J., and, Bowman, J.L., (2008) Evolution of plant microRNAs and their targets. Trends Plant Sci. 13, 343-349.
6. Balazadeh, S., Riano-Pachon, D.M., and, Mueller-Roeber, B., (2008) Transcription factors regulating leaf senescence in Arabidopsis thaliana. Plant Biol. 10, 63-75.
7. Balazadeh, S., Siddiqui, H., Allu, A.D., Matallana-Ramirez, L.P., Caldana, C., Mehrnia, M., Zanor, M.I., Kohler, B., and, Mueller-Roeber, B., (2010) A gene regulatory network controlled by the NAC transcription factor ANAC092/AtNAC2/ORE1 during salt-promoted senescence. Plant J. 62, 250-264.
8. Bartel, D.P., (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell, 116, 281-297.
9. Bartel, D.P., (2009) MicroRNAs: target recognition and regulatory functions. Cell, 136, 215-233.
10. Bartel, D.P., and, Chen, C.Z., (2004) Micromanagers of gene expression: the potentially widespread influence of metazoan microRNAs. Nat. Rev. Genet. 5, 396-400.
11. Bernal, M., Casero, D., Singh, V., et al. (2012) Transcriptome sequencing identifies SPL7-regulated copper acquisition genes FRO4/FRO5 and the copper dependence of iron homeostasis in Arabidopsis. Plant Cell, 24, 738-761.
12. Billard, V., Ourry, A., Maillard, A., Garnica, M., Coquet, L., Jouenne, T., Cruz, F., Garcia-Mina, J.-M., Yvin, J.-C., and, Etienne, P., (2014) Copper-Deficiency in Brassica napus Induces Copper Remobilization, Molybdenum Accumulation and Modification of the Expression of Chloroplastic Proteins. PloS one, 9, e109889.
13. Birtic, S., Ksas, B., Genty, B., Mueller, M.J., Triantaphylides, C., and, Havaux, M., (2011) Using spontaneous photon emission to image lipid oxidation patterns in plant tissues. Plant J. 67, 1103-1115.
14. Boutigny, S., Sautron, E., Finazzi, G., Rivasseau, C., Frelet-Barrand, A., Pilon, M., Rolland, N., and, Seigneurin-Berny, D., (2014) HMA1 and PAA1, two chloroplast-envelope P-IB-ATPases, play distinct roles in chloroplast copper homeostasis. J. Exp. Bot. 65, 1529-1540.
15. Buchanan-Wollaston, V., Page, T., Harrison, E., et al. (2005) Comparative transcriptome analysis reveals significant differences in gene expression and signalling pathways between developmental and dark/starvation-induced senescence in Arabidopsis. Plant J. 42, 567-585.
16. Burkhead, J.L., Reynolds, K.A.G., Abdel-Ghany, S.E., Cohu, C.M., and, Pilon, M., (2009) Copper homeostasis. New Phytol. 182, 799-816.
17. Carrington, J.C., and, Ambros, V., (2003) Role of microRNAs in plant and animal development. Science, 301, 336-338.
18. Carrio-Segui, A., Garcia-Molina, A., Sanz, A., and, Penarrubia, L., (2015) Defective copper transport in the copt5 mutant affects cadmium tolerance. Plant Cell Physiol. 56, 442-454.
19. Chen, X.M., (2009) Small RNAs and their roles in plant development. Annu. Rev. Cell Dev. Biol. 25, 21-44.
20. Chen, X.M., (2012) Small RNAs in development-insights from plants. Curr. Opin. Genet. Dev. 22, 361-367.
21. Chen, C., Ridzon, D.A., Broomer, A.J., et al. (2005) Real-time quantification of microRNAs by stem-loop RT-PCR. Nucleic Acids Res. 33, e179.
22. Chen, X.P., Zhong, Z.F., Xu, Z.T., Chen, L.D., and, Wang, Y.T., (2010) 2 ',7'-Dichlorodihydrofluorescein as a fluorescent probe for reactive oxygen species measurement: forty years of application and controversy. Free Radic. Res. 44, 587-604.
23. Chen, L.J., Wuriyanghan, H., Zhang, Y.Q., et al. (2013) An S-domain receptor-like kinase, OsSIK2, confers abiotic stress tolerance and delays dark-induced leaf senescence in rice. Plant Physiol. 163, 1752-1765.
24. Choi, M., and, Davidson, V.L., (2011) Cupredoxins-A study of how proteins may evolve to use metals for bioenergetic processes. Metallomics, 3, 140-151.
25. Chu, C.C., Lee, W.C., Guo, W.Y., Pan, S.M., Chen, L.J., Li, H.M., and, Jinn, T.L., (2005) A copper chaperone for superoxide dismutase that confers three types of copper/zinc superoxide dismutase activity in Arabidopsis. Plant Physiol. 139, 425-436.
26. Clough, S.J., and, Bent, A.F., (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16, 735-743.
27. Cohu, C.M., and, Pilon, M., (2007) Regulation of superoxide dismutase expression by copper availability. Physiol. Plant. 129, 747-755.
28. DalCorso, G., Manara, A., Piasentin, S., and, Furini, A., (2014) Nutrient metal elements in plants. Metallomics, 6, 1770-1788.
29. Dat, J., Vandenabeele, S., Vranova, E., Van Montagu, M., Inze, D., and, Van Breusegem, F., (2000) Dual action of the active oxygen species during plant stress responses. Cell. Mol. Life Sci. 57, 779-795.
30. Ding, Y.F., Tao, Y.L., and, Zhu, C., (2013) Emerging roles of microRNAs in the mediation of drought stress response in plants. J. Exp. Bot. 64, 3077-3086.
31. Distelfeld, A., Avni, R., and, Fischer, A.M., (2014) Senescence, nutrient remobilization, and yield in wheat and barley. J. Exp. Bot. 65, 3783-3798.
32. Dolferus, R., (2014) To grow or not to grow: a stressful decision for plants. Plant Sci. 229, 247-261.
33. Duan, Y., Zhang, W., Li, B., Wang, Y., Li, K., Sodmergen Han, C., Zhang, Y., and, Li, X., (2010) An endoplasmic reticulum response pathway mediates programmed cell death of root tip induced by water stress in Arabidopsis. New Phytol. 186, 681-695.
34. Edwards, R., Dixon, D.P., and, Walbot, V., (2000) Plant glutathione S-transferases: enzymes with multiple functions in sickness and in health. Trends Plant Sci. 5, 193-198.
35. Farage-Barhom, S., Burd, S., Sonego, L., Perl-Treves, R., and, Lers, A., (2008) Expression analysis of the BFN1 nuclease gene promoter during senescence, abscission, and programmed cell death-related processes. J. Exp. Bot. 59, 3247-3258.
36. Feng, H., Zhang, Q., Wang, Q., Wang, X., Liu, J., Li, M., Huang, L., and, Kang, Z., (2013) Target of tae-miR408, a chemocyanin-like protein gene (TaCLP1), plays positive roles in wheat response to high-salinity, heavy cupric stress and stripe rust. Plant Mol. Biol. 83, 433-443.
37. Flynt, A.S., and, Lai, E.C., (2008) Biological principles of microRNA-mediated regulation: shared themes amid diversity. Nat. Rev. Genet. 9, 831-842.
38. Gadjev, I., Vanderauwera, S., Gechev, T.S., Laloi, C., Minkov, I.N., Shulaev, V., Apel, K., Inze, D., Mittler, R., and, Van Breusegem, F., (2006) Transcriptomic footprints disclose specificity of reactive oxygen species signaling in Arabidopsis. Plant Physiol. 141, 436-445.
39. Gan, S., and, Amasino, R.M., (1997) Making sense of senescence. Plant Physiol. 113, 313-319.
40. Gayomba, S.R., Jung, H.I., Yan, J.P., Danku, J., Rutzke, M.A., Bernal, M., Kramer, U., Kochian, L.V., Salt, D.E., and, Vatamaniuk, O.K., (2013) The CTR/COPT-dependent copper uptake and SPL7-dependent copper deficiency responses are required for basal cadmium tolerance in A-thaliana. Metallomics, 5, 1262-1275.
41. Gepstein, S., and, Glick, B.R., (2013) Strategies to ameliorate abiotic stress-induced plant senescence. Plant Mol. Biol. 82, 623-633.
42. Gill, S.S., and, Tuteja, N., (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol. Biochem. 48, 909-930.
43. Gill, S.S., Anjum, N.A., Gill, R., Yadav, S., Hasanuzzaman, M., Fujita, M., Mishra, P., Sabat, S.C., and, Tuteja, N., (2015) Superoxide dismutase-mentor of abiotic stress tolerance in crop plants. Environ. Sci. Pollut. Res. 22, 10375-10394.
44. Giri, J., Dansana, P.K., Kothari, K.S., Sharma, G., Vij, S., and, Tyagi, A.K., (2013) SAPs as novel regulators of abiotic stress response in plants. BioEssays, 35, 639-648.
45. Guan, Q., Lu, X., Zeng, H., Zhang, Y., and, Zhu, J., (2013) Heat stress induction of miR398 triggers a regulatory loop that is critical for thermotolerance in Arabidopsis. Plant J. 74, 840-851.
46. Guerra, D., Crosatti, C., Khoshro, H.H., Mastrangelo, A.M., Mica, E., and, Mazzucotelli, E., (2015) Post-transcriptional and post-translational regulations of drought and heat response in plants: a spider's web of mechanisms. Front. Plant Sci. 6, 57. doi: 10.3389/fpls.2015.00057.
47. Guiboileau, A., Sormani, R., Meyer, C., and, Masclaux-Daubresse, C., (2010) Senescence and death of plant organs: nutrient recycling and developmental regulation. C. R. Biol. 333, 382-391.
48. Gupta, A.S., Heinen, J.L., Holaday, A.S., Burke, J.J., and, Allen, R.D., (1993) Increased resistance to oxidative stress in transgenic plants that overexpress chloroplastic cu/zn superoxide-dismutase. Proc. Natl Acad. Sci. USA, 90, 1629-1633.
49. Hajiboland, R., (2012) Effect of micronutrient deficiencies on plants stress responses. In Abiotic Stress Responses in Plants: Metabolism, Productivity and Sustainability (, Ahmad, P., and, Prasad, M.N.V., eds). Springer: New York, pp. 283-329.
50. Hartel, H., Haseloff, R.F., Ebert, B., and, Rank, B., (1992) Free-radical formation in chloroplasts-methyl viologen action. J. Photochem. Photobiol. B, 12, 375-387.
51. Havaux, M., (2003) Spontaneous and thermoinduced photon emission: new methods to detect and quantify oxidative stress in plants. Trends Plant Sci. 8, 409-413.
52. Himelblau, E., and, Amasino, R.M., (2001) Nutrients mobilized from leaves of Arabidopsis thaliana during leaf senescence. J. Plant Physiol. 158, 1317-1323.
53. Hodges, D.M., DeLong, J.M., Forney, C.F., and, Prange, R.K., (1999) Improving the thiobarbituric acid-reactive-substances assay for estimating lipid peroxidation in plant tissues containing anthocyanin and other interfering compounds. Planta, 207, 604-611.
54. Huang, C.H., Kuo, W.Y., Weiss, C., and, Jinn, T.L., (2012) Copper chaperone-dependent and -independent activation of three copper-zinc superoxide dismutase homologs localized in different cellular compartments in Arabidopsis. Plant Physiol. 158, 737-746.
55. Huijser, P., and, Schmid, M., (2011) The control of developmental phase transitions in plants. Development, 138, 4117-4129.
56. Jaspers, P., and, Kangasjarvi, J., (2010) Reactive oxygen species in abiotic stress signaling. Physiol. Plant. 138, 405-413.
57. Jeong, D.H., and, Green, P.J., (2013) The role of rice microRNAs in abiotic stress responses. J. Plant Biol. 56, 187-197.
58. Jeong, D.H., Park, S., Zhai, J.X., Gurazada, S.G.R., De Paoli, E., Meyers, B.C., and, Green, P.J., (2011) Massive analysis of rice small RNAs: mechanistic implications of regulated MicroRNAs and variants for differential target RNA cleavage. Plant Cell, 23, 4185-4207.
59. Jibran, R., Hunter, D.A., and, Dijkwel, P.P., (2013) Hormonal regulation of leaf senescence through integration of developmental and stress signals. Plant Mol. Biol. 82, 547-561.
60. Jing, X.S., Hou, P.C., Lu, Y.J., et al. (2015) Overexpression of copper/zinc superoxide dismutase from mangrove Kandelia candel in tobacco enhances salinity tolerance by the reduction of reactive oxygen species in chloroplast. Front. Plant Sci. 6, 23. doi: 10.3389/fpls.2015.00023.
61. Jones-Rhoades, M.W., Bartel, D.P., and, Bartel, B., (2006) MicroRNAS and their regulatory roles in plants. Annu. Rev. Plant Biol. 57, 19-53.
62. Jovanovic, Z., Stanisavljevic, N., Mikic, A., Radovic, S., and, Maksimovic, V., (2014) Water deficit down-regulates miR398 and miR408 in pea (Pisum sativum L.). Plant Physiol. Biochem. 83C, 26-31.
63. Kant, S., Peng, M., and, Rothstein, S.J., (2011) Genetic regulation by NLA and microRNA827 for maintaining nitrate-dependent phosphate homeostasis in Arabidopsis. PLoS Genet. 7, e1002021.
64. Khraiwesh, B., Zhu, J.K., and, Zhu, J., (2012) Role of miRNAs and siRNAs in biotic and abiotic stress responses of plants. Biochim. Biophys. Acta, 1819, 137-148.
65. Kim, J.H., Woo, H.R., Kim, J., Lim, P.O., Lee, I.C., Choi, S.H., Hwang, D., and, Nam, H.G., (2009) Trifurcate feed-forward regulation of age-dependent cell death involving miR164 in Arabidopsis. Science, 323, 1053-1057.
66. Kim, M.D., Kim, Y.H., Kwon, S.Y., Yun, D.J., Kwak, S.S., and, Lee, H.S., (2010) Enhanced tolerance to methyl viologen-induced oxidative stress and high temperature in transgenic potato plants overexpressing the CuZnSOD, APX and NDPK2 genes. Physiol. Plant. 140, 153-162.
67. Kliebenstein, D.J., Monde, R.A., and, Last, R.L., (1998) Superoxide dismutase in Arabidopsis: an eclectic enzyme family with disparate regulation and protein localization. Plant Physiol. 118, 637-650.
68. Koffler, B.E., Luschin-Ebengreuth, N., Stabentheiner, E., Müller, M., and, Zechmann, B., (2014) Compartment specific response of antioxidants to drought stress in Arabidopsis. Plant Sci. 227, 133-144.
69. Kozomara, A., and, Griffiths-Jones, S., (2011) miRBase: integrating microRNA annotation and deep-sequencing data. Nucleic Acids Res. 39, D152-D157.
70. Kwon, S.Y., Jeong, Y.J., Lee, H.S., Kim, J.S., Cho, K.Y., Allen, R.D., and, Kwak, S.S., (2002) Enhanced tolerances of transgenic tobacco plants expressing both superoxide dismutase and ascorbate peroxidase in chloroplasts against methyl viologen-mediated oxidative stress. Plant, Cell Environ. 25, 873-882.
71. Lers, A., (2007) Environmental regulation of leaf senescence. In Senescence Processes in Plants (, Gan, S., ed.). Blackwell: Oxford, pp. 108-144.
72. Li, Y.F., Zheng, Y., Addo-Quaye, C., Zhang, L., Saini, A., Jagadeeswaran, G., Axtell, M.J., Zhang, W.X., and, Sunkar, R., (2010) Transcriptome-wide identification of microRNA targets in rice. Plant J. 62, 742-759.
73. Li, S., Liu, L., Zhuang, X., et al. (2013) MicroRNAs inhibit the translation of target mRNAs on the endoplasmic reticulum in Arabidopsis. Cell, 153, 562-574.
74. de Lima, J.C., Loss-Morais, G., and, Margis, R., (2012) MicroRNAs play critical roles during plant development and in response to abiotic stresses. Genet. Mol. Biol. 35, 1069-1077.
75. 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.
76. Liu, Z., Kumari, S., Zhang, L., Zheng, Y., and, Ware, D., (2012) Characterization of miRNAs in response to short-term waterlogging in three inbred lines of Zea mays. PLoS One, 7, e39786.
77. Liu, T.Y., Lin, W.Y., Huang, T.K., and, Chiou, T.J., (2014) MicroRNA-mediated surveillance of phosphate transporters on the move. Trends Plant Sci. 19, 647-655.
78. Mahanty, S., Kaul, T., Pandey, P., Reddy, R.A., Mallikarjuna, G., Reddy, C.S., Sopory, S., and, Reddy, M.K., (2012) Biochemical and molecular analyses of copper-zinc superoxide dismutase from a C-4 plant Pennisetum glaucum reveals an adaptive role in response to oxidative stress. Gene, 505, 309-317.
79. McKersie, B.D., Chen, Y.R., Debeus, M., Bowley, S.R., Bowler, C., Inze, D., Dhalluin, K., and, Botterman, J., (1993) Superoxide-dismutase enhances tolerance of freezing stress in transgenic alfalfa (Medicago-sativa L). Plant Physiol. 103, 1155-1163.
80. Mishra, A., Heyer, A.G., and, Mishra, K.B., (2014) Chlorophyll fluorescence emission can screen cold tolerance of cold acclimated Arabidopsis thaliana accessions. Plant Methods, 10, 38.
81. Mittler, R., Vanderauwera, S., Gollery, M., and, Van Breusegem, F., (2004) Reactive oxygen gene network of plants. Trends Plant Sci. 9, 490-498.
82. Mutum, R.D., Balyan, S.C., Kansal, S., Agarwal, P., Kumar, S., Kumar, M., and, Raghuvanshi, S., (2013) Evolution of variety-specific regulatory schema for expression of osa-miR408 in indica rice varieties under drought stress. FEBS J. 280, 1717-1730.
83. Nersissian, A.M., Immoos, C., Hill, M.G., Hart, P.J., Williams, G., Herrmann, R.G., and, Valentine, J.S., (1998) Uclacyanins, stellacyanins, and plantacyanins ape distinct subfamilies of phytocyanins: plant-specific mononuclear blue copper proteins. Protein Sci. 7, 1915-1929.
84. Pant, B.D., Buhtz, A., Kehr, J., and, Scheible, W.R., (2008) MicroRNA399 is a long-distance signal for the regulation of plant phosphate homeostasis. Plant J. 53, 731-738.
85. Penarrubia, L., Andres-Colas, N., Moreno, J., and, Puig, S., (2010) Regulation of copper transport in Arabidopsis thaliana: a biochemical oscillator? J. Biol. Inorg. Chem. 15, 29-36.
86. Penarrubia, L., Romero, P., Carrio-Segui, A., Andres-Borderia, A., Moreno, J., and, Sanz, A., (2015) Temporal aspects of copper homeostasis and its crosstalk with hormones. Front. Plant Sci. 6, 255.
87. Penfold, C.A., and, Buchanan-Wollaston, V., (2014) Modelling transcriptional networks in leaf senescence. J. Exp. Bot. 65, 3859-3873.
88. Petrov, V., Hille, J., Mueller-Roeber, B., and, Gechev, T.S., (2015) ROS-mediated abiotic stress-induced programmed cell death in plants. Front. Plant Sci. 6, 69. doi: 10.3389/fpls.2015.00069.
89. Prashanth, S.R., Sadhasivam, V., and, Parida, A., (2008) Over expression of cytosolic copper/zinc superoxide dismutase from a mangrove plant Avicennia mayina in indica Rice var Pusa Basmati-1 confers abiotic stress tolerance. Transgenic Res. 17, 281-291.
90. Rajwanshi, R., Chakraborty, S., Jayanandi, K., Deb, B., and, Lightfoot, D.A., (2014) Orthologous plant microRNAs: microregulators with great potential for improving stress tolerance in plants. Theor. Appl. Genet. 127, 2525-2543.
91. Ramachandran, V., and, Chen, X.M., (2008) Small RNA metabolism in Arabidopsis. Trends Plant Sci. 13, 368-374.
92. Ravet, K., and, Pilon, M., (2013) Copper and iron homeostasis in plants: the challenges of oxidative stress. Antioxid. Redox Signal. 19, 919-932.
93. Reinhart, B.J., Weinstein, E.G., Rhoades, M.W., Bartel, B., and, Bartel, D.P., (2002) MicroRNAs in plants. Genes Dev. 16, 1616-1626.
94. Rosenwasser, S., Belausov, E., Riov, J., Holdengreber, V., and, Friedman, H., (2010) Gibberellic acid (GA3) inhibits ROS increase in chloroplasts during dark-induced senescence of pelargonium cuttings. J. Plant Growth Regul. 29, 375-384.
95. Rubio-Somoza, I., and, Weigel, D., (2011) MicroRNA networks and developmental plasticity in plants. Trends Plant Sci. 16, 258-264.
96. Schommer, C., Palatnik, J.F., Aggarwal, P., Chetelat, A., Cubas, P., Farmer, E.E., Nath, U., and, Weigel, D., (2008) Control of jasmonate biosynthesis and senescence by miR319 targets. PLoS Biol. 6, 1991-2001.
97. Schuetz, M., Benske, A., Smith, R.A., Watanabe, Y., Tobimatsu, Y., Ralph, J., Demura, T., Ellis, B., and, Samuels, A.L., (2014) Laccases direct lignification in the discrete secondary cell wall domains of protoxylem. Plant Physiol. 166, 798-807.
98. 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.
99. Shen, J., Xie, K., and, Xiong, L., (2010) Global expression profiling of rice microRNAs by one-tube stem-loop reverse transcription quantitative PCR revealed important roles of microRNAs in abiotic stress responses. Mol. Genet. Genomics, 284, 477-488.
100. Smillie, R.M., and, Hetherington, S.E., (1983) Stress tolerance and stress-induced injury in crop plants measured by chlorophyll fluorescence in vivo. Chilling, freezing, ice cover, heat, and high light. Plant Physiol. 72, 1043-1050.
101. Spanudakis, E., and, Jackson, S., (2014) The role of microRNAs in the control of flowering time. J. Exp. Bot. 65, 365-380.
102. Stroher, E., Wang, X.J., Roloff, N., Klein, P., Husemann, A., and, Dietz, K.J., (2009) Redox-dependent regulation of the stress-induced zinc-finger protein SAP12 in Arabidopsis thaliana. Mol. Plant, 2, 357-367.
103. Sunkar, R., (2010) MicroRNAs with macro-effects on plant stress responses. Semin. Cell Dev. Biol. 21, 805-811.
104. Sunkar, R., and, Zhu, J.K., (2004) Novel and stress-regulated microRNAs and other small RNAs from Arabidopsis. Plant Cell, 16, 2001-2019.
105. Sunkar, R., Kapoor, A., and, Zhu, J.K., (2006) Posttranscriptional induction of two Cu/Zn superoxide dismutase genes in Arabidopsis is mediated by downregulation of miR398 and important for oxidative stress tolerance. Plant Cell, 18, 2051-2065.
106. Sunkar, R., Li, Y.F., and, Jagadeeswaran, G., (2012) Functions of microRNAs in plant stress responses. Trends Plant Sci. 17, 196-203.
107. Suzuki, N., Koussevitzky, S., Mittler, R., and, Miller, G., (2012) ROS and redox signalling in the response of plants to abiotic stress. Plant, Cell Environ. 35, 259-270.
108. Tang, L., Kwon, S.Y., Kim, S.H., Kim, J.S., Choi, J.S., Cho, K.Y., Sung, C.K., Kwak, S.S., and, Lee, H.S., (2006) Enhanced tolerance of transgenic potato plants expressing both superoxide dismutase and ascorbate peroxidase in chloroplasts against oxidative stress and high temperature. Plant Cell Rep. 25, 1380-1386.
109. Taulavuori, E., Hellstrom, E.K., Taulavuori, K., and, Laine, K., (2001) Comparison of two methods used to analyse lipid peroxidation from Vaccinium myrtillus (L.) during snow removal, reacclimation and cold acclimation. J. Exp. Bot. 52, 2375-2380.
110. Thatcher, S.R., Burd, S., Wright, C., Lers, A., and, Green, P.J., (2015) Differential expression of miRNAs and their target genes in senescing leaves and siliques: insights from deep sequencing of small RNAs and cleaved target RNAs. Plant, Cell Environ. 38, 188-200.
111. Thomas, H., (2013) Senescence, ageing and death of the whole plant. New Phytol. 197, 696-711.
112. Trevisan, S., Nonis, A., Begheldo, M., Manoli, A., Palme, K., Caporale, G., Ruperti, B., and, Quaggiotti, S., (2012) Expression and tissue-specific localization of nitrate-responsive miRNAs in roots of maize seedlings. Plant, Cell Environ. 35, 1137-1155.
113. Trindade, I., Capitao, C., Dalmay, T., Fevereiro, M.P., and, dos Santos, D.M., (2010) miR398 and miR408 are up-regulated in response to water deficit in Medicago truncatula. Planta, 231, 705-716.
114. Verslues, P.E., Agarwal, M., Katiyar-Agarwal, S., Zhu, J.H., and, Zhu, J.K., (2006) Methods and concepts in quantifying resistance to drought, salt and freezing, abiotic stresses that affect plant water status. Plant J. 45, 523-539.
115. Voinnet, O., (2009) Origin, biogenesis, and activity of plant microRNAs. Cell, 136, 669-687.
116. Xu, J., Duan, X.G., Yang, J., Beeching, J.R., and, Zhang, P., (2013) Enhanced reactive oxygen species scavenging by overproduction of superoxide dismutase and catalase delays postharvest physiological deterioration of cassava storage roots. Plant Physiol. 161, 1517-1528.
117. Xu, X.B., Bai, H.Q., Liu, C.P., Chen, E.Y., Chen, Q.G., Zhuang, J.Y., and, Shen, B., (2014) Genome-wide analysis of micrornas and their target genes related to leaf senescence of rice. PLoS One, 9, e114313.
118. Yamasaki, H., Abdel-Ghany, S.E., Cohu, C.M., Kobayashi, Y., Shikanai, T., and, Pilon, M., (2007) Regulation of copper homeostasis by micro-RNA in Arabidopsis. J. Biol. Chem. 282, 16369-16378.
119. Yamasaki, H., Pilon, M., and, Shikanai, T., (2008) How do plants respond to copper deficiency?. Plant Signal. Behav. 3, 231-232.
120. Yamasaki, H., Hayashi, M., Fukazawa, M., Kobayashi, Y., and, Shikanai, T., (2009) SQUAMOSA promoter binding Protein-Like7 is a central regulator for copper homeostasis in Arabidopsis. Plant Cell, 21, 347-361.
121. Yang, C.H., Li, D.Y., Mao, D.H., Liu, X., Ji, C.J., Li, X.B., Zhao, X.F., Cheng, Z.K., Chen, C.Y., and, Zhu, L.H., (2013) Overexpression of microRNA319 impacts leaf morphogenesis and leads to enhanced cold tolerance in rice (Oryza sativa L.). Plant Cell Environ. 36, 2207-2218.
122. Yruela, I., (2013) Transition metals in plant photosynthesis. Metallomics, 5, 1090-1109.
123. Zeng, H.Q., Wang, G.P., Hu, X.Y., Wang, H.Z., Du, L.Q., and, Zhu, Y.Y., (2014) Role of microRNAs in plant responses to nutrient stress. Plant Soil, 374, 1005-1021.
124. Zhang, H.Y., and, Li, L., (2013) SQUAMOSA promoter binding protein-like7 regulated microRNA408 is required for vegetative development in Arabidopsis. Plant J. 74, 98-109.
125. Zhang, H.Y., Zhao, X., Li, J.G., Cai, H.Q., Deng, X.W., and, Li, L., (2014a) MicroRNA408 is critical for the HY5-SPL7 gene network that mediates the coordinated response to light and copper. Plant Cell, 26, 4933-4953.
126. Zhang, X.N., Li, X., and, Liu, J.H., (2014b) Identification of conserved and novel cold-responsive microRNAs in trifoliate orange (Poncirus trifoliata (L.) Raf.) using high-throughput sequencing. Plant Mol. Biol. Rep. 32, 328-341.
127. Zhao, Q., Nakashima, J., Chen, F., Yin, Y.B., Fu, C.X., Yun, J.F., Shao, H., Wang, X.Q., Wang, Z.Y., and, Dixon, R.A., (2013) LACCASE is necessary and nonredundant with PEROXIDASE for lignin polymerization during vascular development in Arabidopsis. Plant Cell, 25, 3976-3987.
128. Zhou, L., Liu, Y., Liu, Z., Kong, D., Duan, M., and, Luo, L., (2010a) Genome-wide identification and analysis of drought-responsive microRNAs in Oryza sativa. J. Exp. Bot. 61, 4157-4168.
129. Zhou, M., Gu, L., Li, P., Song, X., Wei, L., Chen, Z., and, Cao, X., (2010b) Degradome sequencing reveals endogenous small RNA targets in rice (Oryza sativa L. ssp. indica). Front. Biol. 5, 67-90.
130. Zhou, M., Li, D.Y., Li, Z.G., Hu, Q., Yang, C.H., Zhu, L.H., and, Luo, H., (2013) Constitutive expression of a miR319 gene alters plant development and enhances salt and drought tolerance in transgenic creeping bentgrass. Plant Physiol. 161, 1375-1391.