The role of MAPK in plant response to abiotic stress

doi:10.11686/cyxb2023090

Abstract

Abstract:

Mitogen-activated protein kinase （MAPK） is a highly conserved serine/threonine （Ser/Thr） protein kinase， occurring widely in eukaryotic intermediate reaction pathways. Plant MAPK has 11 relatively conserved sub-domains， which are all essential elements for Ser/Thr protein kinase to play its catalytic role， and its expression is regulated by reactive oxygen species， nitric oxide and hormones. MAPK phosphorylates a variety of substrates including transcription factors， protein kinases and cytoskeleton related proteins， and plays an important role in regulating plant response to abiotic stresses （salt， drought， extreme temperature， and heavy metals）. In this review， we summarize the results of research on the discovery of plant MAPK family members， their structure and classification， regulatory mechanisms， and their roles in response to various abiotic stresses. We also propose directions for future research. The information in this review provides a theoretical basis and identifies genetic resources for the genetic improvement of crops to produce new， stress-resistant varieties.

Key words: mitogen-activated protein kinase, regulatory mechanism, abiotic stress, MAPK cascade pathway, phosphorylation

Xin-miao ZHANG, Guo-qiang WU, Ming WEI. The role of MAPK in plant response to abiotic stress[J]. Acta Prataculturae Sinica, 2024, 33(1): 182-197.

Figures/Tables 3

References 133

1	Bai Y， Kissoudis C， Yan Z， et al. Plant behaviour under combined stress： Tomato responses to combined salinity and pathogen stress. The Plant Journal， 2018， 93（4）： 781-793.
2	Chen X X， Ding Y L， Yang Y Q， et al. Protein kinases in plant responses to drought， salt， and cold stress. Journal of Integrative Plant Biology， 2021， 63（1）： 53-78.
3	Molle V， Kremer L. Division and cell envelope regulation by Ser/Thr phosphorylation： Mycobacterium shows the way. Molecular Microbiology， 2010， 75（5）： 1064-1077.
4	Zhang M M， Su J B， Zhang Y， et al. Conveying endogenous and exogenous signals： MAPK cascades in plant growth and defense. Current Opinion in Plant Biology， 2018， 45： 1-10.
5	Shao Y M， Yu X X， Xu X W， et al. The YDA-MKK4/MKK5-MPK3/MPK6 cascade functions downstream of the RGF1-RGI ligand-receptor pair in regulating mitotic activity in root apical meristem. Molecular Plant， 2020， 13（11）： 1608-1623.
6	Bai F W， Matton D P. The Arabidopsis mitogen-activated protein kinase kinase kinase 20 （MKKK20） C-terminal domain interacts with MKK3 and harbors a typical DEF mammalian MAP kinase docking site. Plant Signaling & Behavior， 2018， 13（8）： e1503498.
7	Zhang M M， Zhang S Q. Mitogen-activated protein kinase cascades in plant signaling. Journal of Integrative Plant Biology， 2022， 64（2）： 301-341.
8	Xie C， Yang L， Gai Y P. MAPKKKs in plants： Multidimensional regulators of plant growth and stress responses. International Journal of Molecular Sciences， 2023， 24（4）： 4117.
9	Stafstrom J P， Altschuler M， Anderson D H. Molecular cloning and expression of a MAP kinase homologue from pea. Plant Molecular Biology， 1993， 22（1）： 83-90.
10	Ichimura K， Shinozaki K， Tena G， et al. Mitogen-activated protein kinase cascades in plants： A new nomenclature. Trends in Plant Science， 2002， 7（7）： 301-308.
11	Wang T Z， Liu M J， Wu Y， et al. Genome-wide identification and expression analysis of MAPK gene family in lettuce （Lactuca sativa L.） and functional analysis of LsMAPK4 in high- temperature-induced bolting. International Journal of Molecular Sciences， 2022， 23（19）： 11129.
12	Xie K B， Chen J P， Wang Q， et al. Direct phosphorylation and activation of a mitogen-activated protein kinase by a calcium-dependent protein kinase in rice. The Plant Cell， 2014， 26（7）： 3077-3089.
13	Teige M， Scheikl E， Eulgem T， et al. The MKK2 pathway mediates cold and salt stress signaling in Arabidopsis. Molecular Cell， 2004， 15（1）： 141-152.
14	Mao X X， Zhang J J， Liu W G， et al. The MKKK62-MKK3-MAPK7/14 module negatively regulates seed dormancy in rice. Rice， 2019， 12（1）： 2.
15	Zhou H Y， Ren S Y， Han Y F， et al. Identification and analysis of mitogen-activated protein kinase （MAPK） cascades in Fragaria vesca. International Journal of Molecular Sciences， 2017， 18（8）： 1766.
16	Zhang D， Jiang S， Pan J， et al. The overexpression of a maize mitogen-activated protein kinase gene （ZmMPK5） confers salt stress tolerance and induces defence responses in tobacco. Plant Biology， 2014， 16（3）： 558-570.
17	Pan J W， Zhang M Y， Kong X P， et al. ZmMPK17， a novel maize group D MAP kinase gene， is involved in multiple stress responses. Planta， 2012， 235（4）： 661-676.
18	Long L L， Gao W， Xu L， 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）： 153-162.
19	Wang C， Lu W J， He X W， et al. The cotton mitogen-activated protein kinase kinase 3 functions in drought tolerance by regulating stomatal responses and root growth. Plant and Cell Physiology， 2016， 57（8）： 1629-1642.
20	Zhang J， Zou D， Li Y， et al. GhMPK17， a cotton mitogen-activated protein kinase， is involved in plant response to high salinity and osmotic stresses and ABA signaling. PLoS One， 2014， 9（4）： e95642.
21	Liu X， Zhao M， Gu C， et al. Genome-wide identification of MAPK family genes and their response to abiotic stresses in tea plant （Camellia sinensi）. Open Life Sciences， 2022， 17（1）： 1064-1074.
22	Ergen N Z， Thimmapuram J， Bohnert H J， et al. Transcriptome pathways unique to dehydration tolerant relatives of modern wheat. Functional & Integrative Genomics， 2009， 9（3）： 377-396.
23	Liu X， Wei R， Tian M Y， et al. Combined transcriptome and metabolome profiling provide insights into cold responses in rapeseed （Brassica napus L.） genotypes with contrasting cold-stress sensitivity. International Journal of Molecular Sciences， 2022， 23（21）： 13546.
24	Zhang X， Li Y P， Xing Q J， et al. Genome-wide identification of mitogen-activated protein kinase （MAPK） cascade and expression profiling of CmMAPKs in melon （Cucumis melo L.）. PLoS One， 2020， 15（5）： e0232756.
25	Wu J， Liang X Y， Lin M， et al. Comprehensive analysis of MAPK gene family in Populus trichocarpa and physiological characterization of PtMAPK3‐1 in response to MeJA induction. Physiologia Plantarum， 2023， 175（1）： e13869.
26	Majeed Y， Zhu X， Zhang N， et al. Harnessing the role of mitogen-activated protein kinases against abiotic stresses in plants. Frontiers in Plant Science， 2023， 14： 932923.
27	Shang Y T， Luo X B， Zhang H， et al. Genome-wide identification and analysis of the MAPK and MAPKK gene families in potato （Solanum tuberosum L.）. Agronomy， 2022， 13（1）： 93.
28	Chatterjee A， Paul A， Unnati G M， et al. MAPK cascade gene family in Camellia sinensis： In-silico identification， expression profiles and regulatory network analysis. BMC Genomics， 2020， 21（1）： 613.
29	Jiao J. Bioinformatics analysis of pear MAPKs family and functional study of PbrMAPK15. Nanjing： Nanjing Agricultural University， 2017.
	焦瑾. 梨MAPK家族基因生物信息分析及PbrMAPK15的功能验证. 南京：南京农业大学， 2017.
30	Li X C. Identification and expression profile analysis of MAPK and MKK gene family in Arabidopsis pumila. Shihezi： Shihezi University， 2020.
	李晓翠. 新疆小拟南芥MAPK和MKK基因家族的鉴定及表达特征分析. 石河子：石河子大学， 2020.
31	Sachdev S， Ansari S A， Ansari M I， et al. Abiotic stress and reactive oxygen species： Generation， signaling， and defense mechanisms. Antioxidants， 2021， 10（2）： 277.
32	Sies H， Belousov V V， Chandel N S， et al. Defining roles of specific reactive oxygen species （ROS） in cell biology and physiology. Nature Reviews Molecular Cell Biology， 2022， 23（7）： 499-515.
33	Duan H， Ma Y C， Liu R， et al. Effect of combined waterlogging and salinity stresses on euhalophyte Suaeda glauca. Plant Physiology and Biochemistry， 2018， 127： 231-237.
34	Baxter A， Mittler R， Suzuki N. ROS as key players in plant stress signalling. Journal of Experimental Botany， 2014， 65（5）： 1229-1240.
35	Jalmi S K， Sinha A K. ROS mediated MAPK signaling in abiotic and biotic stress- striking similarities and differences. Frontiers in Plant Science， 2015， 6： 769.
36	Liu Y K， Liu L X， Qi J P， et al. Cadmium activates ZmMPK3-1 and ZmMPK6-1 via induction of reactive oxygen species in maize roots. Biochemical and Biophysical Research Communications， 2019， 516（3）： 747-752.
37	Moon H， Lee B， Choi G， et al. NDP kinase 2 interacts with two oxidative stress-activated MAPKs to regulate cellular redox state and enhances multiple stress tolerance in transgenic plants. Proceedings of the National Academy of Sciences， 2003， 100（1）： 358-363.
38	Samuel M A， Miles G P， Ellis B E. Ozone treatment rapidly activates MAP kinase signalling in plants. The Plant Journal， 2000， 22（4）： 367-376.
39	Shi B， Ni L， Liu Y P， et al. OsDMI3-mediated activation of OsMPK1 regulates the activities of antioxidant enzymes in abscisic acid signalling in rice： OsDMI3 and OsMPK1 in ABA signaling. Plant， Cell & Environment， 2014， 37（2）： 341-352.
40	Xie G S， Sasaki K， Imai R， et al. A redox-sensitive cysteine residue regulates the kinase activities of OsMPK3 and OsMPK6 in vitro. Plant Science， 2014， 227： 69-75.
41	Zhang T， Zhu M M， Song W Y， et al. Oxidation and phosphorylation of MAP kinase 4 cause protein aggregation. Biochimicaet Biophysica Acta-Proteins and Proteomics， 2015， 1854（2）： 156-165.
42	Wang J X， Ding H D， Zhang A， et al. 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）： 442-452.
43	Zhou J， Xia X J， Zhou Y H， et al. RBOH1-dependent H₂O₂ production and subsequent activation of MPK1/2 play an important role in acclimation-induced cross-tolerance in tomato. Journal of Experimental Botany， 2014， 65（2）： 595-607.
44	Rezayian M， Niknam V， Ebrahimzadeh H. Oxidative damage and antioxidative system in algae. Toxicology Reports， 2019， 6： 1309-1313.
45	Bot P， Mun B G， Imran Q M， et al. Differential expression of AtWAKL10 in response to nitric oxide suggests a putative role in biotic and abiotic stress responses. PeerJ， 2019， 7： e7383.
46	Nabi R B S， Tayade R， Hussain A， et al. Nitric oxide regulates plant responses to drought， salinity， and heavy metal stress. Environmental and Experimental Botany， 2019， 161： 120-133.
47	Shi H T， Ye T T， Zhu J K， et al. Constitutive production of nitric oxide leads to enhanced drought stress resistance and extensive transcriptional reprogramming in Arabidopsis. Journal of Experimental Botany， 2014， 65（15）： 4119-4131.
48	Hasanuzzaman M， Oku H， Nahar K， et al. Nitric oxide-induced salt stress tolerance in plants： ROS metabolism， signaling， and molecular interactions. Plant Biotechnology Reports， 2018， 12（2）： 77-92.
49	Fancy N N， Bahlmann A K， Loake G J. Nitric oxide function in plant abiotic stress. Plant， Cell & Environment， 2017， 40（4）： 462-472.
50	Xiong J， Fu G F， Tao L X， et al. Roles of nitric oxide in alleviating heavy metal toxicity in plants. Archives of Biochemistry and Biophysics， 2010， 497（1/2）： 13-20.
51	Soares C， Carvalho M E A， Azevedo R A， et al. Plants facing oxidative challenges-a little help from the antioxidant networks. Environmental and Experimental Botany， 2019， 161： 4-25.
52	Shahzad B， Tanveer M， Che Z， et al. Role of 24-epibrassinolide （EBL） in mediating heavy metal and pesticide induced oxidative stress in plants： A review. Ecotoxicology and Environmental Safety， 2018， 147： 935-944.
53	Thao N P， Khan M I R， Thu N B A， et al. Role of ethylene and its cross talk with other signaling molecules in plant responses to heavy metal stress. Plant Physiology， 2015， 169（1）： 73-84.
54	Ye Y， Li Z， Xing D. Nitric oxide promotes MPK6-mediated caspase-3-like activation in cadmium-induced Arabidopsis thaliana programmed cell death： NO and MPK6 regulate Cd²⁺-induced PCD. Plant， Cell & Environment， 2013， 36（1）： 1-15.
55	Lv X Z， Ge S B， Jalal A G， et al. Crosstalk between nitric oxide and MPK1/2 mediates cold acclimation-induced chilling tolerance in tomato. Plant and Cell Physiology， 2017， 58（11）： 1963-1975.
56	He H Y， He L F. Crosstalk between melatonin and nitric oxide in plant development and stress responses. Physiologia Plantarum， 2020， 170（2）： 218-226.
57	Zhang A， Jiang M Y， Zhang J H， et al. Nitric oxide induced by hydrogen peroxide mediates abscisic acid-induced activation of the mitogen-activated protein kinase cascade involved in antioxidant defense in maize leaves. New Phytologist， 2007， 175（1）： 36-50.
58	Wei L J， Zhang J， Wei S H， et al. Nitric oxide alleviates salt stress through protein S-nitrosylation and transcriptional regulation in tomato seedlings. Planta， 2022， 256（6）： 101.
59	Hong Y B， Wang H， Gao Y Z， et al. ERF transcription factor OsBIERF3 positively contributes to immunity against fungal and bacterial diseases but negatively regulates cold tolerance in rice. International Journal of Molecular Sciences， 2022， 23（2）： 606.
60	Lin L， Wu J， Jiang M Y， et al. Plant mitogen-activated protein kinase cascades in environmental stresses. International Journal of Molecular Sciences， 2021， 22（4）： 1543.
61	Chen J， Wang L， Yuan M. Update on the roles of rice MAPK cascades. International Journal of Molecular Sciences， 2021， 22（4）： 1679.
62	Sun T J， Zhang Y L. MAP kinase cascades in plant development and immune signaling. EMBO Reports， 2022， 23（2）： e53817.
63	Novikova G V， Moshkov I E， Smith A R， et al. The effect of ethylene on MAP kinase-like activity in Arabidopsis thaliana. FEBS Letters， 2000， 474（1）： 29-32.
64	Shu P， Li Y J， Li Z Y， et al. SlMAPK3 enhances tolerance to salt stress in tomato plants by scavenging ROS accumulation and up-regulating the expression of ethylene signaling related genes. Environmental and Experimental Botany， 2022， 193： 104698.
65	Liao L， Li S C， Li Y J， et al. Pre- or post-harvest treatment with MeJA improves post-harvest storage of lemon fruit by stimulating the antioxidant system and alleviating chilling injury. Plants， 2022， 11（21）： 2840.
66	Ali A， Chu N， Ma P P， et al. Genome-wide analysis of mitogen-activated protein （MAP） kinase gene family expression in response to biotic and abiotic stresses in sugarcane. Physiologia Plantarum， 2021， 171（1）： 86-107.
67	Xie Y F， Ding M L， Yin X C， et al. MAPKK2/4/5/7-MAPK3-JAZs modulate phenolic acid biosynthesis in Salvia miltiorrhiza. Phytochemistry， 2022， 199： 113177.
68	Wang K， He J J， Gao Y， et al. Exogenous melatonin improved the growth and development of naked oat seedlings under cadmium stress. Environmental Science and Pollution Research， 2022， 58（29）： 88109-88118.
69	Zhang T G， Shi Z F， Zhang X H， et al. Alleviating effects of exogenous melatonin on salt stress in cucumber. Scientia Horticulturae， 2020， 262： 109070.
70	Sun T T， Zhang J K， Zhang Q， et al. Exogenous application of acetic acid enhances drought tolerance by influencing the MAPK signaling pathway induced by ABA and JA in apple plants. Tree Physiology， 2022， 42（9）： 1827-1840.
71	Yang X F， Kim M Y， Ha J M， et al. Overexpression of the soybean NAC gene GmNAC109 increases lateral root formation and abiotic stress tolerance in transgenic Arabidopsis plants. Frontiers in Plant Science， 2019， 10： 1036.
72	Tolosa L N， Zhang Z B. The role of major transcription factors in solanaceous food crops under different stress conditions： Current and future perspectives. Plants， 2020， 9（1）： 56.
73	Baillo E H， Kimotho R N， Zhang Z B， et al. Transcription factors associated with abiotic and biotic stress tolerance and their potential for crops improvement. Genes， 2019， 10（10）： 771.
74	Khan S A， Li M Z， Wang S M， et al. Revisiting the role of plant transcription factors in the battle against abiotic stress. International Journal of Molecular Sciences， 2018， 19（6）： 1634.
75	Schmidt R， Mieulet D， Hubberten H M， et al. Salt-responsive erf1 regulates reactive oxygen species-dependent signaling during the initial response to salt stress in rice. The Plant Cell， 2013， 25（6）： 2115-2131.
76	Cai J J， Liu T， Li Y Q， et al. A C-terminal fragment of Arabidopsis oxidative stress 2 can play a positive role in salt tolerance. Biochemical and Biophysical Research Communications， 2021， 556： 23-30.
77	Verma D， Jalmi S K， Bhagat P K， et al. A bHLH transcription factor， MYC2， imparts salt intolerance by regulating proline biosynthesis in Arabidopsis. The FEBS Journal， 2020， 287（12）： 2560-2576.
78	Li H， Ding Y L， Shi Y T， et al. MPK3- and MPK6-mediated ICE1 phosphorylation negatively regulates ICE1 stability and freezing tolerance in Arabidopsis. Developmental Cell， 2017， 43（5）： 630-642.
79	Wang P C， Du Y Y， Zhao X L， et al. The MPK6-ERF6-ROS-responsive cis-acting element7/GCC Box complex modulates oxidative gene transcription and the oxidative response in Arabidopsis. Plant Physiology， 2013， 161（3）： 1392-1408.
80	Wang N N， Zhao L L， Lu R， et al. Cotton mitogen-activated protein kinase4 （GhMPK4） confers the transgenic Arabidopsis hypersensitivity to salt and osmotic stresses. Plant Cell， Tissue and Organ Culture， 2015， 123（3）： 619-632.
81	Li F J， Li M Y， Wang P， et al. Regulation of cotton （Gossypium hirsutum） drought responses by mitogen‐activated protein （MAP） kinase cascade-mediated phosphorylation of GhWRKY59. New Phytologist， 2017， 215（4）： 1462-1475.
82	Chen L， Zhang B， Xia L J， et al. The GhMAP3K62-GhMKK16-GhMPK32 kinase cascade regulates drought tolerance by activating GhEDT1-mediated ABA accumulation in cotton. Journal of Advanced Research， 2022， 11： 2.
83	Zhao L I， Yan J W， Xiang Y， et al. ZmWRKY104 transcription factor phosphorylated by ZmMPK6 functioning in ABA-induced antioxidant defense and enhance drought tolerance in maize. Biology， 2021， 10（9）： 893.
84	Li D Y， Sun Q R， Zhang G F， et al. MxMPK6-2-bHLH104 interaction is involved in reactive oxygen species signaling in response to iron deficiency in apple rootstock. Journal of Experimental Botany， 2021， 72（5）： 1919-1932.
85	Ichimaru K， Yamaguchi K， Harada K， et al. Cooperative regulation of PBI1 and MAPKs controls WRKY45 transcription factor in rice immunity. Nature Communications， 2022， 13（1）： 2397.
86	Prakash V， Singh V P， Tripathi D K， et al. Nitric oxide （NO） and salicylic acid （SA）： A framework for their relationship in plant development under abiotic stress. Plant Biology， 2021， 23（S1）： 39-49.
87	Ahmad I， Zhu G L， Zhou G S， et al. Pivotal role of phytohormones and their responsive genes in plant growth and their signaling and transduction pathway under salt stress in cotton. International Journal of Molecular Sciences， 2022， 23（13）： 7339.
88	Abulfaraj A A. Stepwise signal transduction cascades under salt stress in leaves of wild barley （Hordeum spontaneum）. Biotechnology & Biotechnological Equipment， 2020， 34（1）： 860-872.
89	Sun Y P， Ma C， Kang X， et al. Hydrogen sulfide and nitric oxide are involved in melatonin-induced salt tolerance in cucumber. Plant Physiology and Biochemistry， 2021， 167： 101-112.
90	Shen L K， Zhuang B C， Wu Q， et al. Phosphatidic acid promotes the activation and plasma membrane localization of MKK7 and MKK9 in response to salt stress. Plant Science， 2019， 287： 110190.
91	Sun S Y， Wang Y P， Wang J W， et al. Transcriptome responses to salt stress in roots and leaves of Lilium pumilum. Scientia Horticulturae， 2023， 309： 111622.
92	Yan Z W， Wang J X， Wang F X， et al. MPK3/6-induced degradation of ARR1/10/12 promotes salt tolerance in Arabidopsis. EMBO Reports， 2021， 22（10）： e52457.
93	Zhou H P， Xiao F， Zheng Y， et al. Pamp-induced secreted peptide 3 modulates salt tolerance through receptor-like kinase 7 in plants. The Plant Cell， 2022， 34（2）： 927-944.
94	Liu J， Wang X M， Yang L， et al. Involvement of active MKK9-MAPK3/MAPK6 in increasing respiration in salt-treated Arabidopsis callus. Protoplasma， 2020， 257（3）： 965-977.
95	Jia M， Luo N， Meng X B， et al. OsMPK4 promotes phosphorylation and degradation of IPA1 in response to salt stress to confer salt tolerance in rice. Journal of Genetics and Genomics， 2022， 49（8）： 766-775.
96	Na Y J， Choi H K， Park M Y， et al. OsMAPKKK63 is involved in salt stress response and seed dormancy control. Plant Signaling & Behavior， 2019， 14（3）： e1578633.
97	Zhu Z G， Zhang Q T， Li X J， et al. Cloning， subcellular localization， and expression analysis of MAPK genes from Vitis yeshanesis. Journal of Agricultural Biotechnology， 2020， 28（3）： 429-440.
	朱自果，张庆田，李秀杰，等. 燕山葡萄MAPK基因的克隆、亚细胞定位及表达分析. 农业生物技术学报， 2020， 28（3）： 429-440.
98	Liang D， Zhang C X， Wang M， et al. Cloning and expression analysis of a mitogen-activated protein kinase 13 gene in peanut. Journal of Peanut Science， 2019， 48（2）： 10-18.
	梁丹，张朝昕，王冕，等. 花生MAPK13基因的克隆及表达分析研究. 花生学报， 2019， 48（2）： 10-18.
99	Sharma D， Verma N， Pandey C， et al. MAP kinase as regulators for stress responses in plants： An overview//Pandey G K.. Protein kinases and stress signaling in plants. New Jersey： Wiley-Blackwell， 2020： 369-392.
100	Chen L， Sun H， Wang F J， et al. Genome-wide identification of MAPK cascade genes reveals the GhMAP3K14-GhMKK11-GhMPK31 pathway is involved in the drought response in cotton. Plant Molecular Biology， 2020， 103（1/2）： 211-223.
101	Sadau S B， Ahmad A， Tajo S M， et al. Overexpression of GhMPK3 from cotton enhances cold， drought， and salt stress in Arabidopsis. Agronomy， 2021， 11（6）： 1049.
102	Kumar K， Raina S K， Sultan S M. Arabidopsis MAPK signaling pathways and their cross talks in abiotic stress response. Journal of Plant Biochemistry and Biotechnology， 2020， 29（4）： 700-714.
103	Shan D Q， Wang C， Song H D， et al. The MdMEK2-MdMPK6-MdWRKY17 pathway stabilizes chlorophyll levels by directly regulating MdSUFB in apple under drought stress. The Plant Journal， 2021， 108（3）： 814-828.
104	Ma J J， Lan J P， Zhang T， et al. Overexpression of OsMPK17 protein enhances drought tolerance of rice. Acta Agronomica Sinica， 2020， 46（1）： 20-30.
	马金姣，兰金苹，张彤，等. 过表达OsMPK17激酶蛋白质增强了水稻的耐旱性. 作物学报， 2020， 46（1）： 20-30.
105	Zhu X， Zhang N， Liu X， et al. Mitogen-activated protein kinase 11 （MAPK11） maintains growth and photosynthesis of potato plant under drought condition. Plant Cell Reports， 2021， 40（3）： 491-506.
106	Zhou M， Zhao B B， Li H S， et al. Comprehensive analysis of MAPK cascade genes in sorghum （Sorghum bicolor L.） reveals SbMPK14 as a potential target for drought sensitivity regulation. Genomics， 2022， 114（2）： 110311.
107	Zhu D， Chang Y， Pei T， et al. MAPK-like protein 1 positively regulates maize seedling drought sensitivity by suppressing ABA biosynthesis. The Plant Journal， 2020， 102（4）： 747-760.
108	Wei X S， Liu S， Sun C， et al. Convergence and divergence： Signal perception and transduction mechanisms of cold stress in Arabidopsis and rice. Plants， 2021， 10（9）： 1864.
109	Chen L， Song H Y， Xin J， et al. Comprehensive genome-wide identification and functional characterization of MAPK cascade gene families in Nelumbo. International Journal of Biological Macromolecules， 2023， 233： 123543.
110	Ding Y L， Lv J， Shi Y T， et al. EGR 2 phosphatase regulates OST1 kinase activity and freezing tolerance in Arabidopsis. The EMBO Journal， 2019， 38（1）： e99819.
111	Ponce-Pineda I G， Carmona-Salazar L， Saucedo-García M， et al. MPK6 kinase regulates plasma membrane H⁺-ATPase activity in cold acclimation. International Journal of Molecular Sciences， 2021， 22（12）： 6338.
112	Xia C X， Gong Y S， Chong K， et al. Phosphatase OSPP2C27 directly dephosphorylates OSMAPK3 and OSBHLH002 to negatively regulate cold tolerance in rice. Plant， Cell & Environment， 2021， 44（2）： 491-505.
113	Tak H， Negi S， Rajpurohit Y S， et al. MusaMPK5， a mitogen activated protein kinase is involved in regulation of cold tolerance in banana. Plant Physiology and Biochemistry， 2020， 146： 112-123.
114	Yin Z J， Zhu W P， Zhang X G， et al. Molecular characterization， expression and interaction of MAPK， MAPKK and MAPKKK genes in upland cotton. Genomics， 2021， 113（1）： 1071-1086.
115	Du X Z， Jin Z P， Liu Z Q， et al. H₂S persulfidated and increased kinase activity of MPK4 to response cold stress in Arabidopsis. Frontiers in Molecular Biosciences， 2021， 8： 635470.
116	Song A P， Hu Y C， Ding L， et al. Comprehensive analysis of mitogen-activated protein kinase cascades in Chrysanthemum. PeerJ， 2018， 6： e5037.
117	Majeed Y， Zhu X， Zhang N， et al. Functional analysis of mitogen-activated protein kinases （MAPKs） in potato under biotic and abiotic stress. Molecular Breeding， 2022， 42（6）： 31.
118	Wang Z， Yan S， Ren W C， et al. Genome-wide identification of MAPK， MAPKK， and MAPKKK gene families in Fagopyrum tataricum and analysis of their expression patterns under abiotic stress. Frontiers in Genetics， 2022， 13： 894048.
119	He X W， Wang C Z， Wang H B， et al. The function of MAPK cascades in response to various stresses in horticultural plants. Frontiers in Plant Science， 2020， 11： 952.
120	Kumar R R， Arora K， Goswami S， et al. MAPK enzymes： A ROS activated signaling sensors involved in modulating heat stress response， tolerance and grain stability of wheat under heat stress. Biotech， 2020， 10（9）： 380.
121	Opdenakker K， Remans T， Keunen E， et al. Exposure of Arabidopsis thaliana to Cd or Cu excess leads to oxidative stress mediated alterations in MAPKinase transcript levels. Environmental and Experimental Botany， 2012， 83： 53-61.
122	Liu J X， Wang J X， Lee S C， et al. Copper-caused oxidative stress triggers the activation of antioxidant enzymes via ZmMPK3 in maize leaves. PLoS One， 2018， 13（9）： e0203612.
123	Mumtaz M A， Hao Y， Mehmood S， et al. Physiological and transcriptomic analysis provide molecular insight into 24-epibrassinolide mediated Cr （Ⅵ）-toxicity tolerance in pepper plants. Environmental Pollution， 2022， 306： 119375.
124	Guo Z H， Zeng P， Xiao X Y， et al. Physiological， anatomical， and transcriptional responses of mulberry （Morus alba L.） to Cd stress in contaminated soil. Environmental Pollution， 2021， 284： 117387.
125	Zhou L Y， Lv C G， Kang C Z， et al. Mitogen-activated protein kinase genes of Artemisia annua and their expression analysis under cadmium stress. China Journal of Chinese Materia Medica， 2016， 41（6）： 1016-1020.
	周良云，吕朝耕，康传志，等. 黄花蒿促分裂原活化蛋白激酶基因及其在重金属镉胁迫下表达分析. 中国中药杂志， 2016， 41（6）： 1016-1020.
126	Su T T， Fu L B， Kuang L H， et al. Transcriptome-wide m6A methylation profile reveals regulatory networks in roots of barley under cadmium stress. Journal of Hazardous Materials， 2022， 423： 127140.
127	Zhao F Y， Hu F， Zhang S Y， et al. MAPKs regulate root growth by influencing auxin signaling and cell cycle-related gene expression in cadmium-stressed rice. Environmental Science and Pollution Research， 2013， 20（8）： 5449-5460.
128	Xu Z G， Dong M， Peng X Y， et al. New insight into the molecular basis of cadmium stress responses of wild paper mulberry plant by transcriptome analysis. Ecotoxicology and Environmental Safety， 2019， 171： 301-312.
129	Zhang W W， Song J F， Yue S Q， et al. MhMAPK4 from Malus hupehensis Rehd. decreases cell death in tobacco roots by controlling Cd²⁺ uptake. Ecotoxicology and Environmental Safety， 2019， 168： 230-240.
130	Muhammad T， Zhang J， Ma Y， et al. Overexpression of a mitogen-activated protein kinase SlMAPK3 positively regulates tomato tolerance to cadmium and drought stress. Molecules， 2019， 24（3）： 556.
131	Jin C W， Mao Q Q， Luo B F， et al. Mutation of mpk6 enhances cadmium tolerance in Arabidopsis plants by alleviating oxidative stress. Plant and Soil， 2013， 371（1/2）： 387-396.
132	Huang T L， Huang L Y， Fu S F， et al. Genomic profiling of rice roots with short- and long-term chromium stress. Plant Molecular Biology， 2014， 86（1/2）： 157-170.
133	Pandey C， Banerjee G， Sinha A K. Differential expression of mitogen activated protein kinase （MAPK） and stress-related genes in rice overexpressing MPK3 and MPK6 under abiotic stress. International Journal of Plant and Environment， 2020， 6（4）： 264-269.

物种 Species	基因名称 Gene name	基因ID Gene ID	氨基酸数量 Number of amino acids （aa）	分子量 Molecular weight （kDa）	等电点 Isoelectric point （KJ）	胁迫类型 Stress types	参考文献 Reference
拟南芥 A. thaliana	AtMPK3	At3g45640	370	42.72	5.87	低温、高盐、低渗透、铜、镉Low temperature， high-salt， low permeability， cuprum， cadmium	［10］
	AtMPK6	At2g43790	496	45.06	5.17	低渗透、干旱、低温、镉、铜Low permeability， drought， low temperature， cadmium， cuprum	［13］
	AtMPK4	At4g01370	376	42.85	6.01	高盐High-salt	［13］
莴苣L. sativa	LsMAPK3-2	Lsat_1_v5_gn_9_20480	372	42.88	5.38	高温High temperature	［11］
	LsMAPK4	Lsat_1_v5_gn_3_137680	378	43.46	6.32	高温High temperature
	LsMAPK6	Lsat_1_v5_gn_1_74260	382	58.42	6.57	高温High temperature
水稻O. sativa	OsMAPK3	LOC_Os03g17700	369	43.00	5.48	低温、干旱、高盐、镉、铜、砷Low temperature， drought， high-salt， cadmium， cuprum， arsenic	［12］
	OsMAPK4	LOC_Os10g38950	376	42.77	5.96	高盐、砷High-salt， arsenic	［14］
	OsMAPK14	LOC_Os02g05480	370	42.47	6.70	干旱Drought	［14］
	OsMAPK6	Os06g06090	399	44.96	5.45	镉、铜Cadmium， cuprum	［10］
野草莓Fragaria vesca	FvMAPK5	LOC101297368	391	44.71	5.65	低温、干旱Low temperature， drought	［15］
野草莓Fragaria vesca	FvMAPK8	LOC101306313	371	42.71	5.62	低温、干旱Low temperature， drought	［15］
玉米Zea mays	ZmMAPK5	LOC100272353	376	43.49	5.47	高盐、低温High-salt， low temperature	［16］
玉米Zea mays	ZmMAPK17	LOC103637414	456	46.26	5.05	高盐High-salt	［17］
海岛棉Gossypium barbadense	GbMAPK3	A03G043800.1	375	43.02	5.50	干旱Drought	［18］
陆地棉Gossypium hirsutum	GhMAPK7	LOC107936554	368	42.51	8.06	干旱Drought	［19］
陆地棉Gossypium hirsutum	GhMAPK17	LOC107921990	498	56.95	6.99	高盐High-salt	［20］
山茶树Camellia sinensis	CsMPK3-1	TEA026040	372	42.76	5.25	低温Low temperature	［21］
	CsMPK3-2	TEA020852	365	41.68	5.89	低温、高温、干旱Low temperature， high temperature， drought
	CsMPK4-2	TEA021759	330	38.21	5.41	高温、干旱High temperature， drought
	CsMPK4-3	TEA006436	367	42.24	6.28	低温、高温、干旱Low temperature， high temperature， drought
	CsMPK15	TEA012905	587	66.87	6.99	低温、高温、干旱Low temperature， high temperature， drought
	CsMPK19-1	TEA018880	599	67.28	9.22	低温、高温、干旱Low temperature， high temperature， drought
	CsMPK19-2	TEA022253	792	90.12	9.25	高温、干旱High temperature， drought
小麦Triticum aestivum	TaMAPK8	LOC543037	470	54.61	9.09	干旱Drought	［22］
甘蓝型油菜Brassica napus	BnMAPK4	LOC106438618	373	42.51	5.85	低温Low temperature	［23］
甜瓜Cucumis melo	CmMAPK1	MELO3C010966	386	44.71	6.44	干旱Drought	［24］
	CmMAPK3	MELO3C020718	370	42.75	5.46	高盐、干旱High-salt， drought
	CmMAPK4-1	MELO3C005705	383	43.98	6.09	干旱Drought
	CmMAPK4-2	MELO3C021187	370	42.89	5.97	干旱Drought
	CmMAPK6-1	MELO3C011444	405	46.34	5.44	干旱Drought
	CmMAPK7	MELO3C016399	371	42.74	6.57	高盐、干旱High-salt， drought
	CmMAPK9-1	MELO3C017350	645	73.12	7.34	干旱Drought
	CmMAPK9-2	MELO3C018306	469	54.01	6.82	干旱Drought
	CmMAPK9-4	MELO3C002124	479	54.82	8.56	干旱Drought
	CmMAPK13	MELO3C026848	370	42.61	5.01	干旱Drought
	CmMAPK16	MELO3C021394	565	64.47	8.81	干旱Drought
	CmMAPK20-1	MELO3C014472	606	68.31	9.10	高盐High-salt
	CmMAPK20-2	MELO3C019687	620	70.32	9.28	高盐High-salt
烟草Nicotiana tabacum	NtMPK3	AB052964	393	45.17	4.93	低渗透Low permeability	［10］
烟草Nicotiana tabacum	NtMPK6-1	AF165186	357	39.58	5.41	高渗透、低渗透High permeability， low permeability	［10］

物种 Species	基因名称 Gene name	基因ID Gene ID	氨基酸数量 Number of amino acids （aa）	分子量 Molecular weight （kDa）	等电点 Isoelectric point （KJ）	胁迫类型 Stress types	参考文献 Reference
拟南芥 A. thaliana	AtMPK3	At3g45640	370	42.72	5.87	低温、高盐、低渗透、铜、镉Low temperature， high-salt， low permeability， cuprum， cadmium	［10］
	AtMPK6	At2g43790	496	45.06	5.17	低渗透、干旱、低温、镉、铜Low permeability， drought， low temperature， cadmium， cuprum	［13］
	AtMPK4	At4g01370	376	42.85	6.01	高盐High-salt	［13］
莴苣L. sativa	LsMAPK3-2	Lsat_1_v5_gn_9_20480	372	42.88	5.38	高温High temperature	［11］
	LsMAPK4	Lsat_1_v5_gn_3_137680	378	43.46	6.32	高温High temperature
	LsMAPK6	Lsat_1_v5_gn_1_74260	382	58.42	6.57	高温High temperature
水稻O. sativa	OsMAPK3	LOC_Os03g17700	369	43.00	5.48	低温、干旱、高盐、镉、铜、砷Low temperature， drought， high-salt， cadmium， cuprum， arsenic	［12］
	OsMAPK4	LOC_Os10g38950	376	42.77	5.96	高盐、砷High-salt， arsenic	［14］
	OsMAPK14	LOC_Os02g05480	370	42.47	6.70	干旱Drought	［14］
	OsMAPK6	Os06g06090	399	44.96	5.45	镉、铜Cadmium， cuprum	［10］
野草莓Fragaria vesca	FvMAPK5	LOC101297368	391	44.71	5.65	低温、干旱Low temperature， drought	［15］
野草莓Fragaria vesca	FvMAPK8	LOC101306313	371	42.71	5.62	低温、干旱Low temperature， drought	［15］
玉米Zea mays	ZmMAPK5	LOC100272353	376	43.49	5.47	高盐、低温High-salt， low temperature	［16］
玉米Zea mays	ZmMAPK17	LOC103637414	456	46.26	5.05	高盐High-salt	［17］
海岛棉Gossypium barbadense	GbMAPK3	A03G043800.1	375	43.02	5.50	干旱Drought	［18］
陆地棉Gossypium hirsutum	GhMAPK7	LOC107936554	368	42.51	8.06	干旱Drought	［19］
陆地棉Gossypium hirsutum	GhMAPK17	LOC107921990	498	56.95	6.99	高盐High-salt	［20］
山茶树Camellia sinensis	CsMPK3-1	TEA026040	372	42.76	5.25	低温Low temperature	［21］
	CsMPK3-2	TEA020852	365	41.68	5.89	低温、高温、干旱Low temperature， high temperature， drought
	CsMPK4-2	TEA021759	330	38.21	5.41	高温、干旱High temperature， drought
	CsMPK4-3	TEA006436	367	42.24	6.28	低温、高温、干旱Low temperature， high temperature， drought
	CsMPK15	TEA012905	587	66.87	6.99	低温、高温、干旱Low temperature， high temperature， drought
	CsMPK19-1	TEA018880	599	67.28	9.22	低温、高温、干旱Low temperature， high temperature， drought
	CsMPK19-2	TEA022253	792	90.12	9.25	高温、干旱High temperature， drought
小麦Triticum aestivum	TaMAPK8	LOC543037	470	54.61	9.09	干旱Drought	［22］
甘蓝型油菜Brassica napus	BnMAPK4	LOC106438618	373	42.51	5.85	低温Low temperature	［23］
甜瓜Cucumis melo	CmMAPK1	MELO3C010966	386	44.71	6.44	干旱Drought	［24］
	CmMAPK3	MELO3C020718	370	42.75	5.46	高盐、干旱High-salt， drought
	CmMAPK4-1	MELO3C005705	383	43.98	6.09	干旱Drought
	CmMAPK4-2	MELO3C021187	370	42.89	5.97	干旱Drought
	CmMAPK6-1	MELO3C011444	405	46.34	5.44	干旱Drought
	CmMAPK7	MELO3C016399	371	42.74	6.57	高盐、干旱High-salt， drought
	CmMAPK9-1	MELO3C017350	645	73.12	7.34	干旱Drought
	CmMAPK9-2	MELO3C018306	469	54.01	6.82	干旱Drought
	CmMAPK9-4	MELO3C002124	479	54.82	8.56	干旱Drought
	CmMAPK13	MELO3C026848	370	42.61	5.01	干旱Drought
	CmMAPK16	MELO3C021394	565	64.47	8.81	干旱Drought
	CmMAPK20-1	MELO3C014472	606	68.31	9.10	高盐High-salt
	CmMAPK20-2	MELO3C019687	620	70.32	9.28	高盐High-salt
烟草Nicotiana tabacum	NtMPK3	AB052964	393	45.17	4.93	低渗透Low permeability	［10］
烟草Nicotiana tabacum	NtMPK6-1	AF165186	357	39.58	5.41	高渗透、低渗透High permeability， low permeability	［10］

[1]	Xian-fei SHI, Yu GAO, Xu-sheng HUANG, Ya-li ZHOU, Gui-ping CAI, Xin-ru LI, Run-zhi LI, Jin-ai XUE. Functional characterization of Cyperus esculentus CeWRKY transcription factors in response to abiotic stress [J]. Acta Prataculturae Sinica, 2023, 32(8): 186-201.
[2]	Jie ZHANG, Kai CHENG, Ying-chun WANG. Analysis of the calcium-dependent protein kinase RtCDPK16 response to abiotic stress in Reaumuria trigyna [J]. Acta Prataculturae Sinica, 2023, 32(2): 97-109.
[3]	Jiao-yang TIAN, Qiu-xia WANG, Shu-wen ZHENG, Wen-xian LIU. Genome-wide identification and expression profile analysis of the CPP gene family in Medicago truncatula [J]. Acta Prataculturae Sinica, 2022, 31(7): 111-121.
[4]	Chun-jie LI, Ming-xiao LANG, Zhen-jiang CHEN, Tai-xiang CHEN, Jing LIU, Yuan-yuan JIN, Xue-kai WEI. Effects of Epichloë endophytic fungi on the germination of grass seeds [J]. Acta Prataculturae Sinica, 2022, 31(3): 192-206.
[5]	Guo-xiang ZHANG, Wei-leng GUO, Ming-yu BI, Li-shuang ZHANG, Dan WANG, Chang-hong GUO. Identification of CAX gene family and expression profile analysis of response to abiotic stress in alfalfa [J]. Acta Prataculturae Sinica, 2022, 31(12): 106-117.
[6]	Jia-ju ZHANG, Jie YU, Ming-na LI, Jun-mei KANG, Qing-chuan YANG, Rui-cai LONG. Identification and functional analysis of lncRNA167 and its cleavage product miR167c in Medicago truncatula [J]. Acta Prataculturae Sinica, 2022, 31(1): 164-180.
[7]	HOU Jie-ru, DUAN Xiao-yue, LI Zhou, PENG Yan. Cloning and expression analysis of TrSAMDC1 in white clover [J]. Acta Prataculturae Sinica, 2020, 29(8): 170-178.
[8]	YANG Liu-hui, YIN Hang, HUANG Qin-mei, ZHANG Yan-ni, HE Miao, ZHOU Yun-wei. An analysis of the response of the LpWRKY20 gene to abiotic stress and its role in drought resistance [J]. Acta Prataculturae Sinica, 2020, 29(1): 193-202.
[9]	GAO Hui-juan, LÜ Xin-pei, WANG Run-juan, REN Wei, CHENG Ji-nan, WANG Yong-ping, SHAO Kun-zhong, ZHANG Jin-lin. Application of RNA-seq technology in research on herb, shrub and tree stress resistance [J]. Acta Prataculturae Sinica, 2019, 28(12): 184-196.
[10]	LI Meng-zhan, YIN Hong-ju, LI Ding-ding, LIU Ya-qi, WANG Suo-min. Knock out of two splice variants of MYB 40 using the gene-editing technique CRISPR/Cas9 [J]. Acta Prataculturae Sinica, 2019, 28(1): 120-127.
[11]	XIE Zhi-jian, ZHOU Chun-huo, HE Ya-qin, SONG Tao, YU Yang, WU Jia. A review of Astragalus sinicus in paddy fields in south China since 2000s [J]. Acta Prataculturae Sinica, 2018, 27(8): 185-196.
[12]	SUO Ya-fei, DU Chao, LI Ning-ning, WANG Yan, WANG Ying-chun. Cloning and function analysis of RtSOD gene in the rare recretohalophyte Reaumuria trigyna [J]. Acta Prataculturae Sinica, 2018, 27(4): 98-110.
[13]	WU Zhi-gang, WU Shu-jia, WANG Ying-chun, ZHENG Lin-lin. Advances in studies of calcium-dependent protein kinase (CDPK) in plants [J]. Acta Prataculturae Sinica, 2018, 27(1): 204-214.
[14]	ZHANG Xue, SUN Xin-Bo, FAN Bo, ZHANG Yin-Bing, HAN Lie-Bao, XU Li-Xin. Molecular cloning and expression analysis of ZjCSD from Zoysia japonica [J]. Acta Prataculturae Sinica, 2017, 26(2): 102-110.
[15]	CHAO Zhao-Xia, REN Yan-Ping, QIAN Jin, YAO Zheng-Pei, XU Lei, ZHANG Hua. Functional analysis of two stress-related promoters in Medicago varia cultivar Xinmu No.1 [J]. Acta Prataculturae Sinica, 2017, 26(1): 131-141.