RNA-seq analysis reveals MAPKKK family members related to drought tolerance in maize

PLoS ONE

Volumn 10, Issue 11, 2015, Pages

  Liu, Ya ^a   Zhou, Miaoyi ^a   Gao, Zhaoxu ^b   Ren, Wen ^a   Yang, Fengling ^a   He, Hang ^b   Zhao, Jiuran ^a  

^a INSTITUTE OF PLANT AND ENVIRONMENT PROTECTION   (China)

^b PEKING UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ETHYLENE; MITOGEN ACTIVATED PROTEIN KINASE KINASE KINASE; PROLINE; SALICYLIC ACID; STARCH; TRANSCRIPTOME;

ABIOTIC STRESS; ARTICLE; CONTROLLED STUDY; DROUGHT STRESS; DROUGHT TOLERANCE; GENE EXPRESSION; GENE LOCATION; GENETIC ASSOCIATION; GENETIC VARIABILITY; MAIZE; MITOGEN ACTIVATED PROTEIN KINASE KINASE KINASE GENE; NONHUMAN; OXIDATION REDUCTION REACTION; PHOTOSYNTHESIS; PHYLOGENETIC TREE; PLANT GENOME; PLANT LEAF; PLANT METABOLISM; PLANT ROOT; PLANT STEM; REAL TIME POLYMERASE CHAIN REACTION; RNA SEQUENCE; SEQUENCE ANALYSIS; ADAPTATION; ANTIBODY SPECIFICITY; BIOLOGY; BIOMASS; CHROMOSOMAL MAPPING; CLASSIFICATION; CLUSTER ANALYSIS; DROUGHT; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MOLECULAR GENETICS; MULTIGENE FAMILY; PHYLOGENY; PHYSIOLOGICAL STRESS; PROCEDURES;

ADAPTATION, BIOLOGICAL; BIOMASS; CHROMOSOME MAPPING; CLUSTER ANALYSIS; COMPUTATIONAL BIOLOGY; DROUGHTS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, PLANT; MAP KINASE KINASE KINASES; MOLECULAR SEQUENCE ANNOTATION; MULTIGENE FAMILY; ORGAN SPECIFICITY; PHYLOGENY; SEQUENCE ANALYSIS, RNA; STRESS, PHYSIOLOGICAL; TRANSCRIPTOME; ZEA MAYS;

EID: 84957544727     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0143128     Document Type: Article

References (74)

1. Chaves MM, Flexas J, Pinheiro C. Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell. Annals of Botany. 2009; 103(4):551-60. doi: 10.1093/aob/mcn125 PMID: WOS:000263162300002.
2. Krugman T, Peleg Z, Quansah L, Chague V, Korol AB, Nevo E, et al. Alteration in expression of hormone-related genes in wild emmer wheat roots associated with drought adaptation mechanisms. Functional & Integrative Genomics. 2011; 11(4):565-83. doi: 10.1007/s10142-011-0231-6 PMID: WOS:000300093500005.
3. Kakumanu A, Ambavaram MMR, Klumas C, Krishnan A, Batlang U, Myers E, et al. Effects of Drought on Gene Expression in Maize Reproductive and Leaf Meristem Tissue Revealed by RNA-Seq. Plant Physiology. 2012; 160(2):846-67. doi: 10.1104/pp.112.200444 PMID: WOS:000309523800022.
4. Xu J, Yuan Y, Xu Y, Zhang G, Guo X, Wu F, et al. Identification of candidate genes for drought tolerance by whole-genome resequencing in maize. Bmc Plant Biology. 2014; 14: 83. doi: 10.1186/1471-2229-14-83 PMID: WOS:000335345900001.
5. de Ronde JA, van der Mescht A, Steyn HSF. Proline accumulation in response to drought and heat stress in cotton. African crop science journal. 2000; 8(1):85-91.
6. Roosens NH, Al Bitar F, Loenders K, Angenon G, Jacobs M. Overexpression of ornithine-d-aminotransferase increases proline biosynthesis and confers osmotolerance in transgenic plants. Molecular Breeding. 2002; 9(2):73-80. doi: 10.1023/a:1026791932238 PMID: WOS:000176815600002.
7. Frye CA, Tang D, Innes RW. Negative regulation of defense responses in plants by a conserved MAPKK kinase. Proceedings of the National Academy of Sciences of the United States of America. 2001; 98(1):373-8. PMID: 11114160
8. Morris PC. MAP kinase signal transduction pathways in plants. New Phytologist. 2001; 151(1):67-89.
9. Mizoguchi T, Irie K, Hirayama T, Hayashida N, Yamaguchi-Shinozaki K, Matsumoto K, et al. A gene encoding a mitogen-activated protein kinase kinase kinase is induced simultaneously with genes for a mitogen-activated protein kinase and an S6 ribosomal protein kinase by touch, cold, and water stress in Arabidopsis thaliana. Plant Biology. 1996; 93:765-9.
10. Agrawal GK, Rakwal R, Iwahashi H. Isolation of novel rice (Oryza sativa L.) multiple stress responsive MAP kinase gene, OsMSRMK2, whose mRNA accumulates rapidly in response to environmental cues. Biochemical and Biophysical Research Communications. 2002; 294(5):1009-16. http://dx.doi.org/10. 1016/S0006-291X(02)00571-5. PMID: 12074577
11. Jeong MJ, Lee SK, Kim BG, Kwon TR, Cho WS, Park YT, et al. A rice (Oryza sativa L.) MAP kinase gene, OsMAPK44, is involved in response to abiotic stresses. Plant Cell Tissue and Organ Culture. 2006; 85(2):151-60. doi: 10.1007/s11240-005-9064-0 PMID: WOS:000237361300004.
12. Xiong LZ, Yang YN. Disease resistance and abiotic stress tolerance in rice are inversely modulated by an abscisic acid-inducible mitogen-activated protein kinase. Plant Cell. 2003; 15(3):745-59. doi: 10.1105/tpc.008714 PMID: WOS:000185078000015.
13. Kumar K, Rao KP, Sharma P, Sinha AK. Differential regulation of rice mitogen activated protein kinase kinase (MKK) by abiotic stress. Plant Physiology and Biochemistry. 2008; 46(10):891-7. http://dx.doi. org/10.1016/j.plaphy.2008.05.014. doi: 10.1016/j.plaphy.2008.05.014 PMID: 18619847
14. Wang J, Ding H, Zhang A, Ma F, Cao J, Jiang M. A Novel Mitogen-Activated Protein Kinase Gene in Maize (Zea mays), ZmMPK3, is Involved in Response to Diverse Environmental Cues. Journal of Integrative Plant Biology. 2010; 52(5):442-52. doi: 10.1111/j.1744-7909.2010.00906.x PMID: WOS:000277004100002.
15. Jonak C, Kiegerl S, LigterinkW, Barker PJ, Huskisson NS, Hirt H. Stress signaling in plants: a mitogenactivated protein kinase pathway is activated by cold and drought. Proceedings of the National Academy of Sciences of the United States of America. 1996; 93(20):11274-9. PMID: 8855346
16. Virk N, Liu B, Zhang H, Li X, Zhang Y, Li D, et al. Tomato SlMPK4 is required for resistance against Botrytis cinerea and tolerance to drought stress. Acta Physiologiae Plantarum. 2013; 35(4):1211-21. doi: 10.1007/s11738-012-1160-2 PMID: WOS:000316339400021.
17. Ichimura K, Mizoguchi T, Yoshida R, Yuasa T, Shinozaki K. Various abiotic stresses rapidly activate Arabidopsis MAP kinases ATMPK4 and ATMPK6. The Plant Journal. 2000; 24(5):655-65. PMID: 11123804
18. Banno H, Hirano K, Nakamura T, Irie K, Nomoto S, Matsumoto K, et al. NPK1, a tobacco gene that encodes a protein with a domain homologous to yeast BCK1, STE11, and Byr2 protein kinases. Molecular and cellular biology. 1993; 13(8):4745-52. PMID: 8336712
19. Shou HX, Bordallo P, Wang K. Expression of the Nicotiana protein kinase (NPK1) enhanced drought tolerance in transgenic maize. Journal of Experimental Botany. 2004; 55(399):1013-9. doi: 10.1093/jxb/erb129 PMID: WOS:000221142000006.
20. Muoma JVO, Ombori O. Agrobacterium-Mediated Transformation of Selected Kenyan Maize (Zea mays L.) Genotypes by Introgression of Nicotiana Protein Kinase (npk1) to Enhance Drought Tolerance. American Journal of Plant Sciences. 2014; 5.
21. Xiao B-Z, Chen X, Xiang C-B, Tang N, Zhang Q-F, Xiong L-Z. Evaluation of Seven Function-Known Candidate Genes for their Effects on Improving Drought Resistance of Transgenic Rice under Field Conditions. Molecular Plant. 2009; 2(1):73-83. doi: 10.1093/mp/ssn068 PMID: WOS:000264188800008.
22. Widmann C, Gibson S, Jarpe MB, Johnson GL. Mitogen-Activated Protein Kinase: Conservation of a Three-Kinase Module From Yeast to Human. Physiological Society. 1999; 79(1):143-80.
23. Agrawal GK, Agrawal SK, Shibato J, Iwahashi H, Rakwal R. Novel rice MAP kinases OsMSRMK3 and OsWJUMK1 involved in encountering diverse environmental stresses and developmental regulation. Biochemical and Biophysical Research Communications. 2003; 300(3):775-83. http://dx.doi.org/10. 1016/S0006-291X(02)02868-1. PMID: 12507518
24. Andreasson E, Ellis B. Convergence and specificity in the Arabidopsis MAPK nexus. Trends in Plant Science. 2010; 15(2):106-13. http://dx.doi.org/10.1016/j.tplants.2009.12.001. doi: 10.1016/j.tplants. 2009.12.001 PMID: 20047850
25. Jonak C, Ökrész L, Bögre L, Hirt H. Complexity, Cross Talk and Integration of Plant MAP Kinase Signalling. Current Opinion in Plant Biology. 2002; 5(5):415-24. http://dx.doi.org/10.1016/S1369-5266(02) 00285-6. PMID: 12183180
26. Lewis TS, Shapiro PS, Ahn NG. Signal Transduction through MAP Kinase Cascades. In: George FVW, George K, editors. Advances in Cancer Research. Volume 74: Academic Press; 1998. p. 49-139. PMID: 9561267
27. Madhani HD, Fink GR. The riddle of MAP kinase signaling specificity. Trends in Genetics. 1998; 14 (4):151-5. http://dx.doi.org/10.1016/S0168-9525(98)01425-5. PMID: 9594663
28. Teige M, Scheikl E, Eulgem T, Dóczi R, Ichimura K, Shinozaki K, et al. The MKK2 Pathway Mediates Cold and Salt Stress Signaling in Arabidopsis. Molecular Cell. 2004; 15(1):141-52. http://dx.doi.org/10. 1016/j.molcel.2004.06.023. PMID: 15225555
29. Tena G, Asai T, Chiu W-L, Sheen J. Plant mitogen-activated protein kinase signaling cascades. Current Opinion in Plant Biology. 2001; 4(5):392-400. http://dx.doi.org/10.1016/S1369-5266(00)00191-6. PMID: 11597496
30. Wrzaczek M, Hirt H. Plant MAP kinase pathways: how many and what for? Biology of the Cell. 2001; 93 (1-2):81-7. http://dx.doi.org/10.1016/S0248-4900(01)01121-2. PMID: 11730326
31. Huang HJ, Fu SF, Tai YH, Chou WC, Huang DD. Expression of Oryza sativa MAP kinase gene is developmentally regulated and stress-responsive. Physiologia Plantarum. 2002; 114(4):572-80. doi: 10.1034/j.1399-3054.2002.1140410.x PMID: WOS:000175376200010.
32. Matsuoka D, Nanmori T, Sato K, Fukami Y, Kikkawa U, Yasuda T. Activation of AtMEK1, an Arabidopsis mitogen-activated protein kinase kinase, in vitro and in vivo: analysis of active mutants expressed in E. coli and generation of the active form in stress response in seedlings. Plant Journal. 2002; 29 (5):637-47. doi: 10.1046/j.0960-7412.2001.01246.x PMID: WOS:000174709800010.
33. Schaeffer HJ, Weber MJ. Mitogen-activated protein kinases: specific messages from ubiquitous messengers. Molecular and cellular biology. 1999; 19(4):2435-44. PMID: 10082509
34. Mizoguchi T, Ichimura K, Yoshida R, Shinozaki K. MAP kinase cascades in Arabidopsis: their roles in stress and hormone responses. MAP Kinases in Plant Signal Transduction. 2000; 27:29-38.
35. Group M, Ichimura K, Shinozaki K, Tena G, Sheen J, Henry Y, et al. Mitogen-activated protein kinase cascades in plants: a new nomenclature. Trends in Plant Science. 2002; 7(7):301-8. http://dx.doi.org/10.1016/S1360-1385(02)02302-6. PMID: 12119167
36. Hamel L-P, Nicole M-C, Sritubtim S, Morency M-J, Ellis M, Ehlting J, et al. Ancient signals: comparative genomics of plant MAPK and MAPKK gene families. Trends in Plant Science. 2006; 11(4):192-8. http://dx.doi.org/10.1016/j.tplants.2006.02.007. PMID: 16537113
37. Rao KP, Richa T, Kumar K, Raghuram B, Sinha AK. In Silico Analysis Reveals 75 Members of Mitogen-Activated Protein Kinase Kinase Kinase Gene Family in Rice. DNA Research. 2010; 17(3):139-53. doi: 10.1093/dnares/dsq011 PMID: WOS:000279411300002.
38. Zhang M, Pan J, Kong X, Zhou Y, Liu Y, Sun L, et al. ZmMKK3, a novel maize group B mitogen-activated protein kinase kinase gene, mediates osmotic stress and ABA signal responses. Journal of Plant Physiology. 2012; 169(15):1501-10. http://dx.doi.org/10.1016/j.jplph.2012.06.008. doi: 10.1016/j.jplph. 2012.06.008 PMID: 22835533
39. Kong X, Pan J, Zhang M, Xing X, Zhou Y, Liu Y, et al. ZmMKK4, a novel group C mitogen-activated protein kinase kinase in maize (Zea mays), confers salt and cold tolerance in transgenic Arabidopsis. Plant Cell and Environment. 2011; 34(8):1291-303. doi: 10.1111/j.1365-3040.2011.02329.x PMID: WOS:000292698900007.
40. Wu T, Kong X-P, Zong X-J, Li D-P, Li D-Q. Expression analysis of five maize MAP kinase genes in response to various abiotic stresses and signal molecules. Molecular Biology Reports. 2011; 38 (6):3967-75. doi: 10.1007/s11033-010-0514-3 PMID: WOS:000291656800043.
41. Liu Y, Zhou Y, Liu L, Sun L, Zhang M, Liu Y, et al. Maize ZmMEK1 is a single-copy gene. Molecular Biology Reports. 2012; 39(3):2957-66. doi: 10.1007/s11033-011-1057-y PMID: WOS:000301107800103.
42. Pan J, Zhang M, Kong X, Xing X, Liu Y, Zhou Y, et al. ZmMPK17, a novel maize group D MAP kinase gene, is involved in multiple stress responses. Planta. 2012; 235(4):661-76. doi: 10.1007/s00425-011-1510-0 PMID: WOS:000302253900001.
43. Berberich T, Sano H, Kusano T. Involvement of a MAP kinase, ZmMPK5, in senescence and recovery from low-temperature stress in maize. Molecular and General Genetics MGG. 1999; 262(3):534-42. PMID: 10589842
44. Liu Y, Zhang D, Wang L, Li D. Genome-Wide Analysis of Mitogen-Activated Protein Kinase Gene Family in Maize. Plant Molecular Biology Reporter. 2013; 31(6):1446-60. doi: 10.1007/s11105-013-0623-y PMID: WOS:000326804400025.
45. Kong X, Pan J, Zhang D, Jiang S, Cai G, Wang L, et al. Identification of mitogen-activated protein kinase kinase gene family and MKK-MAPK interaction network in maize. Biochemical and Biophysical Research Communications. 2013; 441(4):964-9. http://dx.doi.org/10.1016/j.bbrc.2013.11.008. doi: 10.1016/j.bbrc.2013.11.008 PMID: 24220337
46. Jouannic S, Hamal A, Leprince AS, Tregear JW, Kreis M, Henry Y. Plant MAP kinase kinase kinases structure, classification and evolution. Gene. 1999; 233(1-2):1-11. http://dx.doi.org/10.1016/S0378-1119(99)00152-3. PMID: 10375615
47. Jouannic S, Hamal A, Leprince A-S, Tregear JW, Kreis M, Henry Y. Characterisation of novel plant genes encoding MEKK/STE11 and RAF-related protein kinases. Gene. 1999; 229(1-2):171-81. http://dx.doi.org/10.1016/S0378-1119(99)00012-8. PMID: 10095117
48. Ligterink W, Hirt H. Mitogen-activated protein (MAP) kinase pathways in plants: Versatile signaling tools. International Review of Cytology. Volume 201: Academic Press; 2001. p. 209-75. PMID: 11057833
49. Champion A, Picaud A, Henry Y. Reassessing the MAP3K and MAP4K relationships. Trends in Plant Science. 2004; 9(3):123-9. http://dx.doi.org/10.1016/j.tplants.2004.01.005. PMID: 15003235
50. Rodriguez MC, Petersen M, Mundy J. Mitogen-activated protein kinase signaling in plants. Annual review of plant biology. 2010; 61:621-49. doi: 10.1146/annurev-arplant-042809-112252 PMID: 20441529
51. Ning J, Li X, Hicks LM, Xiong L. A Raf-Like MAPKKK Gene DSM1 Mediates Drought Resistance through Reactive Oxygen Species Scavenging in Rice. Plant Physiology. 2010; 152(2):876-90. doi: 10.1104/pp.109.149856 PMID: WOS:000274246600041.
52. Kovtun Y, Chiu WL, Zeng W, Sheen J. Suppression of auxin signal transduction by a MAPK cascade in higher plants. Nature. 1998; 395(6703):716-20. PMID: 9790195
53. Kovtun Y, Chiu WL, Tena G, Sheen J. Functional analysis of oxidative stress-activated mitogen-activated protein kinase cascade in plants. Proceedings of the National Academy of Sciences of the United States of America. 2000; 97(6):2940-5. PMID: 10717008
54. Cai G, Wang G, Wang L, Liu Y, Pan J, Li D. A maize mitogen-activated protein kinase kinase, ZmMKK1, positively regulated the salt and drought tolerance in transgenic Arabidopsis. Journal of Plant Physiology. 2014; 171(12):1003-16. http://dx.doi.org/10.1016/j.jplph.2014.02.012. doi: 10.1016/j. jplph.2014.02.012 PMID: 24974327
55. Lin F, Ding H, Wang J, Zhang H, Zhang A, Zhang Y, et al. Positive feedback regulation of maize NADPH oxidase by mitogen-activated protein kinase cascade in abscisic acid signalling. Journal of Experimental Botany. 2009; 60(11):3221-38. doi: 10.1093/jxb/erp157 PMID: WOS:000268588300024.
56. Kong X, Sun L, Zhou Y, Zhang M, Liu Y, Pan J, et al. ZmMKK4 regulates osmotic stress through reactive oxygen species scavenging in transgenic tobacco. Plant Cell Reports. 2011; 30(11):2097-104. doi: 10.1007/s00299-011-1116-9 PMID: WOS:000297200800010.
57. Kong X, Lv W, Zhang D, Jiang S, Zhang S, Li D. Genome-Wide Identification and Analysis of Expression Profiles of Maize Mitogen-Activated Protein Kinase Kinase Kinase. Plos One. 2013; 8(2). e57714 doi: 10.1371/journal.pone.0057714 PMID: WOS:000315519000153.
58. Trapnell C, Roberts A, Goff L, Pertea G, Kim D, Kelley DR, et al. Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nature Protocols. 2012; 7(3):562-78. doi: 10.1038/nprot.2012.016 PMID: WOS:000300948500013.
59. Ding Y, Virlouvet L, Liu N, Riethoven JJ, Fromm M, Avramova Z. Dehydration stress memory genes of Zea mays; comparison with Arabidopsis thaliana. Bmc Plant Biology. 2014; 14. 141 doi: 10.1186/1471-2229-14-141 PMID: WOS:000338155200001.
60. Salvo SA, Hirsch CN, Buell CR, Kaeppler SM, Kaeppler HF. Whole Transcriptome Profiling of Maize during Early Somatic Embryogenesis Reveals Altered Expression of Stress Factors and Embryogenesis-Related Genes. Plos One. 2014; 9(10).
61. Dolezal AL, Shu X, Obrian GR, Nielsen DM, Woloshuk CP, Boston RS, et al. Aspergillus flavus infection induces transcriptional and physical changes in developing maize kernels. Frontiers in Microbiology. 2014; 5. 384 doi: 10.3389/fmicb.2014.00384 PMID: WOS:000340037900001.
62. Yue X, Zhao X, Fei Y, Zhang X. Correlation of Aquaporins and Transmembrane Solute Transporters Revealed by Genome-Wide Analysis in Developing Maize Leaf. Comparative and Functional Genomics. 2012. 546930 doi: 10.1155/2012/546930 PMID: WOS:000309548400001.
63. Bosch M, Mayer CD, Cookson A, Donnison IS. Identification of genes involved in cell wall biogenesis in grasses by differential gene expression profiling of elongating and non-elongating maize internodes. Journal of Experimental Botany. 2011; 62(10):3545-61. doi: 10.1093/jxb/err045 PMID: WOS:000292557000023.
64. Ouaked F, Rozhon W, Lecourieux D, Hirt H. A MAPK pathway mediates ethylene signaling in plants. Embo Journal. 2003; 22(6):1282-8. doi: 10.1093/emboj/cdg131 PMID: WOS:000181546000006.
65. Senaratna T, Touchell D, Bunn E, Dixon K. Acetyl salicylic acid (Aspirin) and salicylic acid induce multiple stress toleranca in bean and tomato plants. Plant Growth Regulation. 2000; 30(2):157-61.
66. Wu L, Zhang Z, Zhang H, Wang X-C, Huang R. Transcriptional Modulation of Ethylene Response Factor Protein JERF3 in the Oxidative Stress Response Enhances Tolerance of Tobacco Seedlings to Salt, Drought, and Freezing. Plant Physiology. 2008; 148(4):1953-63. doi: 10.1104/pp.108.126813 PMID: WOS:000261501500018.
67. Collins CN, Tardieu F, Tuberosa R. Quantitative trait loci and crop performance under abiotic stress: where do we stand? Plant Physiology. 2008; 147:469-86. doi: 10.1104/pp.108.118117 PMID: 18524878
68. Zhang H, Liu W, Wan L, Li F, Dai L, Li D, et al. Functional analyses of ethylene response factor JERF3 with the aim of improving tolerance to drought and osmotic stress in transgenic rice. Transgenic Research. 2010; 19(5):809-18. doi: 10.1007/s11248-009-9357-x PMID: WOS:000281702600007.
69. Zhang Z, Li F, Li D, Zhang H, Huang R. Expression of ethylene response factor JERF1 in rice improves tolerance to drought. Planta. 2010; 232(3):765-74. doi: 10.1007/s00425-010-1208-8 PMID: WOS:000280081800017.
70. Barkosky RR, Einhellig FA. Effects of salicylic acid on plant-water relationships. Journal of Chemical Ecology. 1993; 19(2):237-47. doi: 10.1007/BF00993692 PMID: 24248871
71. He Q, Zhao S, Ma Q, Zhang Y, Huang L, Li G, et al. Endogenous salicylic acid levels and signaling positively regulate Arabidopsis response to polyethylene glycol-simulated drought stress. Journal of Plant Growth Regulation. 2014.
72. Overmyer K, Brosché M, Kangasjärvi J. Reactive oxygen species and hormonal control of cell death. Trends in Plant Science. 2003; 8(7):335-42. http://dx.doi.org/10.1016/S1360-1385(03)00135-3. PMID: 12878018
73. Kim S-H, Woo D-H, Kim J-M, Lee S-Y, Chung WS, Moon Y-H. Arabidopsis MKK4 mediates osmoticstress response via its regulation of MPK3 activity. Biochemical and Biophysical Research Communications. 2011; 412(1):150-4. http://dx.doi.org/10.1016/j.bbrc.2011.07.064. doi: 10.1016/j.bbrc.2011. 07.064 PMID: 21806969
74. Long L, Gao W, Xu L, Liu M, Luo X, He X, et al. GbMPK3, a mitogen-activated protein kinase from cotton, enhances drought and oxidative stress tolerance in tobacco. Plant Cell Tissue and Organ Culture. 2014; 116(2):153-62. doi: 10.1007/s11240-013-0392-1 PMID: WOS:000330386700003.