Stk2, a Mitogen-Activated Protein Kinase from Setosphaeria turcica, Specifically Complements the Functions of the Fus3 and Kss1 of Saccharomyces cerevisiae in Filamentation, Invasive Growth, and Mating Behavior

doi:10.1016/S2095-3119(13)60296-8

Journal of Integrative Agriculture ›› 2013, Vol. 12 ›› Issue (12): 2209-2216.DOI: 10.1016/S2095-3119(13)60296-8

Stk2, a Mitogen-Activated Protein Kinase from Setosphaeria turcica, Specifically Complements the Functions of the Fus3 and Kss1 of Saccharomyces cerevisiae in Filamentation, Invasive Growth, and Mating Behavior

GU Shou-qin, YANG Yang, LI Po, ZHANG Chang-zhi, FAN Yu, ZHANG Xiao-yu, TIAN Lan

1.Mycotoxin and Molecular Plant Pathology Laboratory, Agricultural University of Hebei, Baoding 071000, P.R.China
2.Institute of Plant Protection, Hebei Academy of Agriculture and Forestry Sciences, Baoding 071000, P.R.China
3.Tangshan Normal University, Tangshan 063000, P.R.China

收稿日期:2012-12-10 出版日期:2013-12-01 发布日期:2013-12-17
通讯作者: DONG Jin-gao, Tel: +86-312-7528266, E-mail: shmdjg@hebau.edu.cn
作者简介:GU Shou-qin, Tel: +86-312-7528142, E-mail: gushouqin@126.com; YANG Yang, Mobiel: 15932183899, E-mail: yang0619yang88@126.com;
基金资助:
This study was supported by the National Natural Science Foundation of China (30471126 and 31171805). We thank Stefan Hohmann’s Laboratory at Göteborg University in Sweden for providing the S. cerevisiae strains and Prof. Malcolm Whiteway from the National Research Council of Canada for providing the yeast expression vector.

Stk2, a Mitogen-Activated Protein Kinase from Setosphaeria turcica, Specifically Complements the Functions of the Fus3 and Kss1 of Saccharomyces cerevisiae in Filamentation, Invasive Growth, and Mating Behavior

GU Shou-qin, YANG Yang, LI Po, ZHANG Chang-zhi, FAN Yu, ZHANG Xiao-yu, TIAN Lan

1.Mycotoxin and Molecular Plant Pathology Laboratory, Agricultural University of Hebei, Baoding 071000, P.R.China
2.Institute of Plant Protection, Hebei Academy of Agriculture and Forestry Sciences, Baoding 071000, P.R.China
3.Tangshan Normal University, Tangshan 063000, P.R.China

Received:2012-12-10 Online:2013-12-01 Published:2013-12-17
Contact: DONG Jin-gao, Tel: +86-312-7528266, E-mail: shmdjg@hebau.edu.cn
About author:GU Shou-qin, Tel: +86-312-7528142, E-mail: gushouqin@126.com; YANG Yang, Mobiel: 15932183899, E-mail: yang0619yang88@126.com;
Supported by:
This study was supported by the National Natural Science Foundation of China (30471126 and 31171805). We thank Stefan Hohmann’s Laboratory at Göteborg University in Sweden for providing the S. cerevisiae strains and Prof. Malcolm Whiteway from the National Research Council of Canada for providing the yeast expression vector.

摘要/Abstract

摘要： Setosphaeria turcica, an essential phytopathogenic fungus, is the primary cause of serious yield losses in corn; however, its pathogenic mechanism is poorly understood. We cloned STK2, a newly discovered mitogen-activated protein kinase gene with a deduced amino acid sequence that is 96% identical to MAK2 from Phaeosphaeria nodorum, 56% identical to KSS1 and 57% identical to FUS3 from Saccharomyces cerevisiae. To deduce Stk2 function in S. turcica and to identify the genetic relationship between STK2 and KSS1/FUS3 from S. cerevisiae, a restructured vector containing the open reading frame of STK2 was transformed into a fus3/kss1 double deletion mutant of S. cerevisiae. The results show that the STK2 complementary strain clearly formed pseudohyphae and ascospores, and the strain grew on the surface of the medium after rinsing with sterile water and the characteristics of the complementary strain was the same as the wild-type strain. Moreover, STK2 complemented the function of KSS1 in filamentation and invasive growth, as well as the mating behavior of FUS3 in S. cerevisiae, however, its exact functions in S. turcica will be studied in the future research.

关键词: Setosphaeria turcica , MAPK , filamentation , invasive growth , mating behavior

Abstract: Setosphaeria turcica, an essential phytopathogenic fungus, is the primary cause of serious yield losses in corn; however,
its pathogenic mechanism is poorly understood. We cloned STK2, a newly discovered mitogen-activated protein kinase gene with a deduced amino acid sequence that is 96% identical to MAK2 from Phaeosphaeria nodorum, 56% identical to
KSS1 and 57% identical to FUS3 from Saccharomyces cerevisiae. To deduce Stk2 function in S. turcica and to identify the
genetic relationship between STK2 and KSS1/FUS3 from S. cerevisiae, a restructured vector containing the open reading
frame of STK2 was transformed into a fus3/kss1 double deletion mutant of S. cerevisiae. The results show that the STK2
complementary strain clearly formed pseudohyphae and ascospores, and the strain grew on the surface of the medium after
rinsing with sterile water and the characteristics of the complementary strain was the same as the wild-type strain. Moreover,
STK2 complemented the function of KSS1 in filamentation and invasive growth, as well as the mating behavior of FUS3 in
S. cerevisiae, however, its exact functions in S. turcica will be studied in the future research.

Key words: Setosphaeria turcica , MAPK , filamentation , invasive growth , mating behavior

GU Shou-qin, YANG Yang, LI Po, ZHANG Chang-zhi, FAN Yu, ZHANG Xiao-yu, TIAN Lan. Stk2, a Mitogen-Activated Protein Kinase from Setosphaeria turcica, Specifically Complements the Functions of the Fus3 and Kss1 of Saccharomyces cerevisiae in Filamentation, Invasive Growth, and Mating Behavior[J]. Journal of Integrative Agriculture, 2013, 12(12): 2209-2216.

参考文献

[1]Borchardt D S, Welz H G, Geiger H H. 1998. Genetic structure of setosphaeria turcica populations in tropical and temperate climates. Phytopathology, 88, 322-329

[2]Breitkreutz A, Boucher L, Tyers M. 2001. MAPK specificity in the yeast pheromone response independent of transcriptional activation. Current Biology, 11, 1266-1271

[3]Cheetham J, Smith D A, da Silva Dantas A, Doris K S,Patterson M J, Bruce C R, Quinn J. 2007. A single MAPKKK regulates the Hog1 MAPK pathway in the pathogenic fungus Candida albicans. Molecular Biologyof the Cell, 18, 4603-4614

[4]Chen J, Wang Q, Chen J Y. 2000. CEK2, a novel MAPK from Candida albicans complement the mating defect offus3/kss1 mutant. Acta Biochimica et Biophysica Sinica,32, 299-304 (in Chinese)

[5]Chen R E, Thorner J. 2007. Function and regulation inMAPK signaling pathways: lessons learned from the yeast Saccharomyces cerevisiae. Biochimica et Biophysica Acta, 1773, 1311-1340

[6]Cook J G, Bardwell L, Thorner J. 1997. Inhibitory and activating functions for MAPK Kss1 in the S. cerevisiae filamentous-growth signalling pathway. Nature, 390, 85-88

[7]Eliahu N, Igbaria A, Rose M S, Horwitz B A, Lev S.2007. Melanin biosynthesis in the maize pathogenCochliobolus heterostrophus depends on two mitogen-activated protein kinases, Chk1 and Mps1, and the transcription factor Cmr1. Eukaryot Cell, 6, 421-429

[8]Flandez M, Cosano I C, Nombela C, Martin H, Molina M.2004. Reciprocal regulation between Slt2 MAPK andisoforms of Msg5 dual-specificity protein phosphatase modulates the yeast cell integrity pathway. Journal of Biological Chemistry, 279, 11027-11034

[9]Garrido E, Voss U, Muller P, Castillo-Lluva S, KahmannR, Perez-Martin J. 2004. The induction of sexual development and virulence in the smut fungus Ustilagomaydis depends on Crk1, a novel MAPK protein. Genes& Development, 18, 3117-3130

[10]Gartner A, Nasmyth K, Ammerer G. 1992. Signal transduction in Saccharomyces cerevisiae requires tyrosine and threonine phosphorylation of FUS3 andKSS1. Genes & Development, 6, 1280-1292

[11]Gietz R D, Woods R A. 2002. Transformation of yeast bylithium acetate/single-stranded carrier DNA/polyethylene glycol method. Methods in Enzymology, 350, 87-96

[12]Guo J, Dai X, Xu J R, Wang Y, Bai P, Liu F, Duan Y, Zhang H,Huang L, Kang Z. 2011. Molecular characterization of aFus3/Kss1 type MAPK from Puccinia striiformis f. sp. tritici, PsMAPK1. PLoS One, 6, e21895.

[13]Hamel L P, Nicole M C, Duplessis S, Ellis B E. 2012. Mitogen-activated protein kinase signaling in plant- interacting fungi: distinct messages from conserved messengers. The Plant Cell, 24, 1327-1351

[14]Hu G, Kamp A, Linning R, Naik S, Bakkeren G. 2007. Complementation of Ustilago maydis MAPK mutants by a wheat leaf rust, Puccinia triticina homolog: potential for functional analyses of rust genes. Molecular Plant- Microbe Interactions, 20, 637-647

[15]J imenez-Sanchez M, Cid V J, Molina M. 2007. Retrophosphorylation of Mkk1 and Mkk2 MAPKKs by the Slt2 MAPK in the yeast cell integrity pathway. Journal of Biological Chemistry, 282, 31174-31185

[16]Jin Q, Li C, Li Y, Shang J, Li D, Chen B, Dong H. 2013. Complexity of roles and regulation of the PMK1-MAPK pathway in mycelium development, conidiation and appressorium formation in Magnaporthe oryzae. Gene Expression Patterns, 13, 133-141

[17]Jonak C, Heberle-Bors E, Hirt H. 1994. MAP kinases: universal multi-purpose signaling tools. Plant Molecular Biology, 24, 407-416

[18]Kaffarnik F, Muller P, Leibundgut M, Kahmann R, Feldbrugge M. 2003. PKA and MAPK phosphorylation of Prf1 allows promoter discrimination in Ustilago maydis. EMBO Journal, 22, 5817-5826

[19]Kronstad J, de Maria A D, Funnell D, Laidlaw R D, Lee N, de Sa M M, Ramesh M. 1998. Signaling via cAMP in fungi: interconnections with mitogen-activated protein kinase pathways. Archives of Microbiology, 170, 395-404

[20]Lev S, Sharon A, Hadar R, Ma H, Horwitz B A. 1999. A mitogen-activated protein kinase of the corn leaf pathogen Cochliobolus heterostrophus is involved in conidiation, appressorium formation, and pathogenicity: diverse roles for mitogen-activated protein kinase homologs in foliar pathogens. Proceedings of the National Academy of Sciences of the United States of America, 96, 13542-13547

[21]Lew R R, Levina N N, Shabala L, Anderca M I, Shabala S N. 2006. Role of a mitogen-activated protein kinase cascade in ion flux-mediated turgor regulation in fungi. Eukaryotic Cell, 5, 480-487

[22]Liu W, Soulie M C, Perrino C, Fillinger S. 2011. The osmosensing signal transduction pathway from Botrytis cinerea regulates cell wall integrity and MAP kinase pathways control melanin biosynthesis with influence of light. Fungal Genetics and Biology, 48, 377-387

[23]Ma D, Cook J G, Thorner J. 1995. Phosphorylation and localization of Kss1, a MAP kinase of the Saccharomyces cerevisiae pheromone response pathway. Molecular Biology of the Cell, 6, 889-909

[24]Ma D, Li R. 2013. Current understanding of HOG-MAPK path-way in Aspergillus fumigatus. Mycopathologia, 175, 13-23

[25]Madhani H D, Styles C A, Fink G R. 1997. MAP kinases with distinct inhibitory functions impart signaling specificity during yeast differentiation. Cell, 91, 673-684

[26]Mahanty S K, Wang Y, Farley F W, Elion E A. 1999. Nuclear shuttling of yeast scaffold Ste5 is required for its recruitment to the plasma membrane and activation of the mating MAPK cascade. Cell, 98, 501-512

[27]Mao K, Wang K, Zhao M, Xu T, Klionsky D J. 2011. Two MAPK-signaling pathways are required for mitophagy in Saccharomyces cerevisiae. Journal of Cell Biology, 193, 755-767

[28]Mazor Y, Kupiec M. 2009. Developmentally regulated MAPK pathways modulate heterochromatin in Saccharomyces cerevisiae. Nucleic Acids Research, 37, 4839-4849

[29]Moriwaki A, Kihara J, Mori C, Arase S. 2007. A MAP kinase gene, BMK1, is required for conidiation and pathogenicity in the rice leaf spot pathogen Bipolaris oryzae. African Journal of Microbiology Research, 162, 108-114

[30]Muller P, Aichinger C, Feldbrugge M, Kahmann R. 1999. The MAP kinase kpp2 regulates mating and pathogenic development in Ustilago maydis. Molecular Microbiology, 34, 1007-1017

[31]Puri S, Kumar R, Chadha S, Tati S, Conti H R, Hube B, Cullen P J, Edgerton M. 2012. Secreted aspartic protease cleavage of Candida albicans Msb2 activates Cek1 MAPK signaling affecting biofilm formation and oropharyngeal candidiasis. PLoS One, 7, e46020.

[32]Richards E, Reichardt M, Rogers S. 2001. Preparation of genomic DNA from plant tissue. Current Protocols in Molecular Biology, 27, 2.3.1-23.7.

[33]Rispail N, Di Pietro A. 2009. Fusarium oxysporum Ste12 controls invasive growth and virulence downstream of the Fmk1 MAPK cascade. Molecular Plant-Microbe Interactions, 22, 830-839

[34]Ruiz-Roldan M C, Maier F J, Schafer W. 2001. PTK1, a mitogen-activated-protein kinase gene, is required for conidiation, appressorium formation, and pathogenicity of Pyrenophora teres on barley. Molecular Plant- Microbe Interactions, 14, 116-125

[35]Schamber A, Leroch M, Diwo J, Mendgen K, Hahn M. 2010. The role of mitogen-activated protein (MAP) kinase signalling components and the Ste12 transcription factor in germination and pathogenicity of Botrytis cinerea. Molecular Plant Pathology, 11, 105-119

[36]Serrano R, Martin H, Casamayor A, Arino J. 2006. Signaling alkaline pH stress in the yeast Saccharomyces cerevisiae through the Wsc1 cell surface sensor and the Slt2 MAPK pathway. The Journal of Biological Chemistry, 281, 39785-39795

[37]Solomon P S, Waters O D, Simmonds J, Cooper R M, Oliver R P. 2005. The Mak2 MAP kinase signal transduction pathway is required for pathogenicity in Stagonospora nodorum. Current Genetics, 48, 60-68

[38]Zhan X L, Deschenes R J, Guan K L. 1997. Differential regulation of FUS3 MAP kinase by tyrosine-specific phosphatases PTP2/PTP3 and dual-specificity phosphatase MSG5 in Saccharomyces cerevisiae. Genes & Development, 11, 1690-1702

[39]Zhang H, Xue C, Kong L, Li G, Xu J R. 2011. A Pmk1- interacting gene is involved in appressorium differentiation and plant infection in Magnaporthe oryzae. Eukaryotic Cell, 10, 1062-1070

[40]Zhao X, Xu J R. 2007. A highly conserved MAPK-docking site in Mst7 is essential for Pmk1 activation in Magnaporthe grisea. Molecular Microbiology, 63, 881-894.

Stk2, a Mitogen-Activated Protein Kinase from Setosphaeria turcica, Specifically Complements the Functions of the Fus3 and Kss1 of Saccharomyces cerevisiae in Filamentation, Invasive Growth, and Mating Behavior

Stk2, a Mitogen-Activated Protein Kinase from Setosphaeria turcica, Specifically Complements the Functions of the Fus3 and Kss1 of Saccharomyces cerevisiae in Filamentation, Invasive Growth, and Mating Behavior

PDF

可视化

摘要/Abstract

引用本文

使用本文

参考文献

相关文章 5

编辑推荐

Metrics

[1]	ZHANG Xiao-li, SI Bing-wen, FAN Cheng-ming, LI Hong-jie , WANG Xiao-ming. Proteomics Identification of Differentially Expressed Leaf Proteins in Response to Setosphaeria turcica Infection in Resistant Maize[J]. Journal of Integrative Agriculture, 2014, 13(4): 789-803.
[2]	WENG Chang-mei, LU Jun-xing, WAN Hua-fang, WANG Shu-wen, WANG Zhen, LU Kun, LIANG Ying. Over-Expression of BnMAPK1 in Brassica napus Enhances Tolerance to Drought Stress[J]. Journal of Integrative Agriculture, 2014, 13(11): 2407-2415.
[3]	LIAN Wei-wei, TANG Yi-miao, GAO Shi-qing, ZHANG Zhao, ZHAO Xin, ZHAO Chang-ping. Phylogenetic Analysis and Expression Patterns of the MAPK Gene Family in Wheat (Triticum aestivum L.)[J]. Journal of Integrative Agriculture, 2012, 12(8): 1227-1235.
[4]	LIU Shu-sheng, John Colvin , Paul J De Barro. Species Concepts as Applied to the Whitefly Bemisia tabaci Systematics: How Many Species Are There?[J]. Journal of Integrative Agriculture, 2012, 11(2): 176-186.
[5]	LI Fang-fang, XIA Jun, LI Jun-min, LIU Shu-sheng , WANG Xiao-wei. p38 MAPK is a Component of the Signal Transduction Pathway Triggering Cold Stress Response in the MED Cryptic Species of Bemisia tabaci[J]. Journal of Integrative Agriculture, 2012, 11(2): 303-311.