[an error occurred while processing this directive]
Research Article

Genome-wide identification, phylogenetic and expression of MAPKKK gene family in Arabidopsis pumila

Expand
  • 1. College of Life Sciences, Shihezi University, Shihezi 832003, China
    2. Center for Crop Biotechnology, College of Agriculture, Anhui Science and Technology University, Fengyang 233100, China

Received date: 2022-08-03

  Revised date: 2022-09-18

  Online published: 2022-09-30

Supported by

the National Natural Science Foundation of China(32270385);the National Natural Science Foundation of China(U1303302);the National Natural Science Foundation of China(31060149);the Talent Introduction Start-up Fund Project of Anhui Science and Technology University(NXYJ202001)

Abstract

Mitogen-activated protein kinase kinase kinases (MAPKKKs) are important components of the MAPK cascade and play crucial roles in development and stress responses. Arabidopsis pumila is an ephemeral Brassicaceae plant growing in Xinjiang desert regions, which possesses salt tolerance. To explore the evolution and function of the MAPKKK gene family in A. pumila, 143 ApMAPKKK genes were identified from A. pumila genome by genome-wide analysis, which were categorized into three subfamilies: ZIK (20), MEKK (36) and RAF (87). There existed 74 and 72 colinear genes between A. thaliana, A. lyrata and A. pumila, respectively, indicating that this gene family expanded obviously in A. pumila genome. Evolutionary analysis revealed that there were 64 duplicated gene pairs with Ka/Ks less than 1, and purifying selection was dominant. RNA-seq data were used to analyze the expression characteristics of ApMAPKKK genes in response to salt stress and in different tissues. The results showed that most ApMAPKKK genes were up-regulated under 250 mmol/L NaCl stress. For example, ApMAPKKK18-1/2 and ApMAPKKK17-1/2 were substantially up-regulated. Tissue expression profiles showed that ApMAPKKK mainly presented six expression patterns. Some duplicated genes were differentially expressed in response to salt stress and in different tissues. These results lay a foundation for further understanding the complex mechanism of MAPKKK gene family transduction pathway in response to abiotic stresses in A. pumila.

Cite this article

Qianbin Zhu, Zhicheng Gan, Xiaocui Li, Yingjie Zhang, Heming Zhao, Xianzhong Huang . Genome-wide identification, phylogenetic and expression of MAPKKK gene family in Arabidopsis pumila[J]. Hereditas(Beijing), 2022 , 44(11) : 1044 -1055 . DOI: 10.16288/j.yczz.22-261

References

[1] Zhu JK. Abiotic stress signaling and responses in plants. Cell, 2016, 167(2): 313-324.
[2] Zhang MM, Zhang SQ. Mitogen-activated protein kinase cascades in plant signaling. J Integr Plant Biol, 2022, 64(2): 301-341.
[3] Ichimura K, Shinozaki K, Tena G, Sheen J, Henry Y, Champion A, Kreis M, Zhang SQ, Hirt H, Wilson C, Heberle-Bors E, Ellis BE, Morris PC, Innes RW, Ecker JR, Scheel D, Klessig DF, Machida Y, Mundy J, Ohashi Y, Walker JC. Mitogen-activated protein kinase cascades in plants: a new nomenclature. Trends Plant Sci, 2002, 7(7): 301-308.
[4] Zhang MM, Su JB, Zhang Y, Xu J, Zhang SQ. Conveying endogenous and exogenous signals: MAPK cascades in plant growth and defense. Curr Opin Plant Biol, 2018, 45(Pt A):1-10.
[5] Wang W, Feng BM, Zhou JM, Tang DZ. Plant immune signaling: advancing on two frontiers. J Integr Plant Biol, 2020, 62(1): 2-24.
[6] Jonak C, Okrész L, B?gre L, Hirt H. Complexity, cross talk and integration of plant MAP kinase signalling. Curr Opin Plant Biol, 2002, 5(5): 415-424.
[7] 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 Res, 2010, 17(3): 139-153.
[8] Wu P, Wang WL, Li Y, Hou XL. Divergent evolutionary patterns of the MAPK cascade genes in Brassica rapa and plant phylogenetics. Hortic Res, 2017, 4: 17079.
[9] Rodriguez MCS, Petersen M, Mundy J. Mitogen-activated protein kinase signaling in plants. Annu Rev Plant Biol, 2010, 61: 621-649.
[10] Asai T, Tena G, Plotnikova J, Willmann MR, Chiu WL, Gomez-Gomez L, Boller T, Ausubel FM, Sheen J. MAP kinase signalling cascade in Arabidopsis innate immunity. Nature, 2002, 415(6875): 977-983.
[11] Matsuoka D, Yasufuku T, Furuya T, Nanmori T. An abscisic acid inducible Arabidopsis MAPKKK, MAPKKK18 regulates leaf senescence via its kinase activity. Plant Mol Biol, 2015, 87(6): 565-575.
[12] Li YY, Cai HX, Liu P, Wang CY, Gao HY, Wu CA, Yan K, Zhang SZ, Huang JG, Zheng CC. Arabidopsis MAPKKK 18 positively regulates drought stress resistance via downstream MAPKK3. Biochem Biophys Res Commun, 2017, 484(2): 292-297.
[13] Shao YM, Yu XX, Xu XW, Li Y, Yuan WX, Xu Y, Mao CZ, Zhang SQ, Xu J. The YDA-MKK4/MKK5-MPK3/MPK6 cascade functions downstream of the RGF1-RGI ligand- receptor pair in regulating mitotic activity in root apical meristem. Mol Plant, 2020, 13(11): 1608-1623.
[14] Soyano T, Nishihama R, Morikiyo K, Ishikawa M, Machida Y. NQK1/NtMEK1 is a MAPKK that acts in the NPK1 MAPKKK-mediated MAPK cascade and is required for plant cytokinesis. Genes Dev, 2003, 17(8): 1055-1067.
[15] Liu YL, Schiff M, Dinesh-Kumar SP. Involvement of MEK1 MAPKK, NTF6 MAPK, WRKY/MYB transcription factors, COI1 and CTR1 in N-mediated resistance to tobacco mosaic virus. Plant J, 2004, 38(5): 800-809.
[16] Li FJ, Li MY, Wang P, Cox KL, Duan LS, Dever JK, Shan LB, Li ZH, He P. Regulation of cotton (Gossypium hirsutum) drought responses by mitogen-activated protein (MAP) kinase cascade-mediated phosphorylation of GhWRKY59. New Phytol, 2017, 215(4): 1462-1475.
[17] Xu R, Duan PG, Yu HY, Zhou ZK, Zhang BL, Wang RC, Li J, Zhang GZ, Zhuang SS, Lyu J, Li N, Chai TY, Tian ZX, Yao SG, Li YH. Control of grain size and weight by the OsMKKK10-OsMKK4-OsMAPK6 signaling pathway in rice. Mol Plant, 2018, 11(6): 860-873.
[18] Guo T, Chen K, Dong NQ, Shi CL, Ye WW, Gao JP, Shan JX, Lin HX. GRAIN SIZE AND NUMBER1 negatively regulates the OsMKKK10-OsMKK4-OsMPK6 cascade to coordinate the trade-off between grain number per panicle and grain size in rice. Plant Cell, 2018, 30(4): 871-888.
[19] Liu ZQ, Mei EY, Tian XJ, He ML, Tang JQ, Xu M, Liu JL, Song L, Li XF, Wang ZY, Guan QJ, Xu QJ, Bu QY. OsMKKK 70 regulates grain size and leaf angle in rice through the OsMKK4-OsMAPK6-OsWRKY53 signaling pathway. J Integr Plant Biol, 2021, 63(12): 2043-2057.
[20] Wang M, Yue H, Feng KW, Deng PC, Song WN, Nie XJ. Genome-wide identification, phylogeny and expressional profiles of mitogen activated protein kinase kinase kinase (MAPKKK) gene family in bread wheat (Triticum aestivum L.). BMC Genomics, 2016, 17(1): 668.
[21] Kong XP, Lv W, Zhang D, Jiang SS, Zhang SZ, Li DQ. Genome-wide identification and analysis of expression profiles of maize mitogen-activated protein kinase kinase kinase. PLoS One, 2013, 8(2): e57714.
[22] Zhang JB, Wang XP, Wang YC, Chen YH, Luo JW, Li DD, Li XB. Genome-wide identification and functional characterization of cotton (Gossypium hirsutum) MAPKKK gene family in response to drought stress. BMC Plant Biol, 2020, 20(1): 217.
[23] Huang XZ, Yang LF, Jin YH, Lin J, Liu F. Generation, annotation, and analysis of a large-scale expressed sequence tag library from Arabidopsis pumila to explore salt-responsive genes. Front Plant Sci, 2017, 8: 955.
[24] Yang LF, Jin YH, Huang W, Sun Q, Liu F, Huang XZ. Full-length transcriptome sequences of ephemeral plant Arabidopsis pumila provides insight into gene expression dynamics during continuous salt stress. BMC Genomics, 2018, 19(1): 717.
[25] Li XC, Kang KC, Huang XZ, Fan YB, Song MM, Huang YJ, Ding JJ. Genome-wide identification, phylogenetic analysis and expression profiling of the MKK gene family in Arabidopsis pumila. Hereditas(Beijing), 2020, 42(4): 403-421.
[25] 李晓翠, 康凯程, 黄先忠, 范永斌, 宋苗苗, 黄韵杰, 丁佳佳. 小拟南芥MKK基因家族全基因组鉴定及进化和表达分析. 遗传, 2020, 42(4): 403-421.
[26] Thompson JD, Gibson TJ, Higgins DG. Multiple sequence alignment using ClustalW and ClustalX. Curr Protoc Bioinformatics, 2002, Chapter 2: Unit 2.3.
[27] Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol, 2013, 30(12): 2725-2729.
[28] Wang YP, Tang HB, Debarry JD, Tan X, Li JP, Wang XY, Lee TH, Jin HZ, Marler B, Guo H, Kissinger JC, Paterson AH. MCScanX: a toolkit for detection and evolutionary analysis of gene synteny and collinearity. Nucleic Acids Res, 2012, 40(7): e49.
[29] Chen CJ, Chen H, Zhang Y, Thomas HR, Frank MH, He YH, Xia R. TBtools: an integrative toolkit developed for interactive analyses of big biological data. Mol Plant, 2020, 13(8): 1194-1202.
[30] Tang K, Dong CJ, Liu JY. Genome-wide comparative analysis of the phospholipase D gene families among allotetraploid cotton and its diploid progenitors. PLoS One, 2016, 11(5): e0156281.
[31] Rozas J, Ferrer-Mata A, Sánchez-DelBarrio JC, Guirao- Rico S, Librado P, Ramos-Onsins SE, Sánchez-Gracia A. DnaSP 6: DNA sequence polymorphism analysis of large data sets. Mol Biol Evol, 2017, 34(12), 3299-3302.
[32] Yadav CB, Bonthala VS, Muthamilarasan M, Pandey G, Khan Y, Prasad M. Genome-wide development of transposable elements-based markers in foxtail millet and construction of an integrated database. DNA Res, 2015, 22(1): 79-90.
[33] Niu XQ, Luo XY, Kang KC, Huang XZ, Hu NB, Sui YH, Ai H. Genome-wide identification, comparative evolution and expression analysis of PEBP gene family from Capsicum annuum. Acta Hortic Sin, 2021, 48(5), 947-959.
[33] 牛西强, 罗潇云, 康凯程, 黄先忠, 胡能兵, 隋益虎, 艾昊. 辣椒PEBP基因家族的全基因组鉴定、比较进化与组织表达分析. 园艺学报, 2021, 48(5), 947-959.
[34] Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2 (-Delta Delta C(T)) method. Methods, 2001, 25(4): 402- 408.
[35] Altenhoff AM, Studer RA, Robinson-Rechavi M, Dessimoz C. Resolving the ortholog conjecture: orthologs tend to be weakly, but significantly, more similar in function than paralogs. PLoS Comput Biol, 2012, 8(5): e1002514.
[36] Mattick JS. Introns: evolution and function. Curr Opin Genet Dev, 1994, 4(6): 823-831.
[37] Ye JQ, Yang H, Shi HT, Wei YX, Tie WW, Ding ZH, Yan Y, Luo Y, Xia ZQ, Wang WQ, Peng M, Li KM, Zhang H, Hu W. The MAPKKK gene family in cassava: genome-wide identification and expression analysis against drought stress. Sci Rep, 2017, 7(1): 14939.
[38] Zhang TC, Qiao Q, Novikova PY, Wang Q, Yue JP, Guan YL, Ming SP, Liu TM, De J, Liu YX, Al-Shehbaz IA, Sun H, Van Montagu M, Huang JL, Van de Peer Y, Qiong L. Genome of Crucihimalaya himalaica, a close relative of Arabidopsis, shows ecological adaptation to high altitude. Proc Natl Acad Sci USA, 2019, 116(14): 7137-7146.
[39] Mao ZM, An ZX, Zhou GL, Yang CY, Han YL, Li XY, Zhang YF. Flora of Xinjiang (vol. 2, part 2). Urumqi: Xinjiang Science and Technology Health Press, 1995, 145-146.
[39] 毛祖美, 安争夕, 周桂玲, 杨昌友, 韩英兰, 李学禹, 张彦福. 《新疆植物志》(第二卷第二分册). 乌鲁木齐: 新疆科技卫生出版社, 1995, 145-146.
[40] Teige M, Scheikl E, Eulgem T, Dóczi R, Ichimura K, Shinozaki K, Dangl JL, Hirt H. The MKK2 pathway mediates cold and salt stress signaling in Arabidopsis. Mol Cell, 2004, 15(1): 141-152.
[41] Julkowska MM, Testerink C. Tuning plant signaling and growth to survive salt. Trends Plant Sci, 2015, 20(9): 586-594.
[42] Hong CY, Chao YY, Yang MY, Cheng SY, Cho SC, Kao CH. NaCl-induced expression of glutathione reductase in roots of rice (Oryza sativa L.) seedlings is mediated through hydrogen peroxide but not abscisic acid. Plant Soil, 2009, 320: 103-115.
[43] Bienert GP, Schjoerring JK, Jahn TP. Membrane transport of hydrogen peroxide. Biochim Biophys Acta, 2006, 1758(8): 994-1003.
[44] Choi SW, Lee SB, Na YJ, Jeung SG, Kim SY. Arabidopsis MAP3K16 and other salt-inducible MAP3Ks regulate ABA response redundantly. Mol Cells, 2017, 40(3): 230-242.
[45] Matsuoka D, Soga K, Yasufuku T, Nanmori T.Control of plant growth and development by overexpressing MAP3K17, an ABA-inducible MAP3K, in Arabidopsis. Plant Biotechnol (Tokyo), 2018, 35(2): 171-176.
[46] Virk N, Li DY, Tian LM, Huang L, Hong YB, Li XH, Zhang YF, Liu B, Zhang HJ, Song FM. Arabidopsis Raf-Like mitogen-activated protein kinase kinase kinase gene Raf43 is required for tolerance to multiple abiotic stresses. PLoS One, 2015, 10(7): e0133975.
[47] Kim JM, Woo DH, Kim SH, Lee SY, Park HY, Seok HY, Chung WS, Moon YH. Arabidopsis MKKK 20 is involved in osmotic stress response via regulation of MPK6 activity. Plant Cell Rep, 2012, 31(1): 217-224.
[48] Schmidt R, Mieulet D, Hubberten HM, Obata T, Hoefgen R, Fernie AR, Fisahn J, San Segundo B, Guiderdoni E, Schippers JHM, Mueller-Roeber B. Salt-responsive ERF1 regulates reactive oxygen species-dependent signaling during the initial response to salt stress in rice. Plant Cell, 2013, 25(6): 2115-2131.
[49] Kondrashov FA. Gene duplication as a mechanism of genomic adaptation to a changing environment. Proc Biol Sci, 2012, 279(1749): 5048-5057.
[50] Zhao CZ, Wang PC, Si T, Hsu CC, Wang L, Zayed O, Yu ZP, Zhu YF, Dong J, Tao WA, Zhu JK. MAP kinase cascades regulate the cold response by modulating ICE1 protein stability. Dev Cell, 2017, 43(5): 618-629.e5.
[51] Qiu JL, Zhou L, Yun BW, Nielsen HB, Fiil BK, Petersen K, Mackinlay J, Loake GJ, Mundy J, Morris PC.Arabidopsis mitogen-activated protein kinase kinases MKK1 and MKK2 have overlapping functions in defense signaling mediated by MEKK1, MPK4, and MKS1. Plant Physiol, 2008, 148(1): 212-222.
[52] Kong Q, Qu N, Gao MH, Zhang ZB, Ding XJ, Yang F, Li YZ, Dong OX, Chen S, Li X, Zhang YL. The MEKK1-MKK1/MKK2-MPK4 kinase cascade negatively regulates immunity mediated by a mitogen-activated protein kinase kinase kinase in Arabidopsis. Plant Cell, 2012, 24(5): 2225-2236.
[53] Xu HY, Zhang C, Li ZC, Wang ZR, Jiang XX, Shi YF, Tian SN, Braun E, Mei Y, Qiu WL, Li S, Wang B, Xu J, Navarre D, Ren DT, Cheng NH, Nakata PA, Graham MA, Whitham SA, Liu JZ. The MAPK kinase kinase GmMEKK1 regulates cell death and defense responses. Plant Physiol, 2018, 178(2): 907-922.
Outlines

/