Mycobiology

The Korean Society of Mycology (한국균학회)
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The Cell Wall Integrity MAP Kinase Signaling Pathway Is Required for Development, Pathogenicity, and Stress Adaption of the Pepper Anthracnose Fungus Colletotrichum scovillei

  • Teng Fu (Division of Bio-Resource Sciences and Interdisciplinary Program in Smart Agriculture, Kangwon National University) ;
  • Sung Wook Kang (Division of Bio-Resource Sciences and Interdisciplinary Program in Smart Agriculture, Kangwon National University) ;
  • Yong-Won Song (Division of Bio-Resource Sciences and Interdisciplinary Program in Smart Agriculture, Kangwon National University) ;
  • Kyoung Su Kim (Division of Bio-Resource Sciences and Interdisciplinary Program in Smart Agriculture, Kangwon National University)
  • Received : 2023.02.08
  • Accepted : 2023.05.18
  • Published : 2023.06.30
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Abstract

The cell wall integrity (CWI) signaling pathway plays important roles in the dissemination and infection of several plant pathogenic fungi. However, its roles in the pepper fruit anthracnose fungus Colletotrichum scovillei remain uninvestigated. In this study, the major components of the CWI signaling pathway-CsMCK1 (MAPKKK), CsMKK1 (MAPKK), and CsMPS1 (MAPK)-were functionally characterized in C. scovillei via homology-dependent gene replacement. The ΔCsmck1, DCsmkk1, and ΔCsmps1 mutants showed impairments in fungal growth, conidiation, and tolerance to CWI and salt stresses. Moreover, ΔCsmck1, ΔCsmkk1, and ΔCsmps1 failed to develop anthracnose disease on pepper fruits due to defects in appressorium formation and invasive hyphae growth. These results suggest that CsMCK1, CsMKK1, and CsMPS1 play important roles in mycelial growth, conidiation, appressorium formation, plant infection, and stress adaption of C. scovillei. These findings will contribute to a better understanding of the roles of the CWI signaling pathway in the development of pepper fruit anthracnose disease.

Keywords

Acknowledgement

This study was supported by the Basic Science Research Program through the National Research Foundation of Korea grant (NRF-2020R1A2C100550700) funded by the Ministry of Education, Science and Technology, Republic of Korea. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

References

  1. Dichtl K, Samantaray S, Wagener J. Cell wall integrity signalling in human pathogenic fungi. Cell Microbiol. 2016;18(9):1228-1238. https://doi.org/10.1111/cmi.12612
  2. Bowman SM, Free SJ. The structure and synthesis of the fungal cell wall. Bioessays. 2006;28(8):799-808. https://doi.org/10.1002/bies.20441
  3. Garcia-Rubio R, De Oliveira HC, Rivera J, et al. The fungal cell wall: Candida, Cryptococcus, and Aspergillus species. Front Microbiol. 2019;10:2993.
  4. Valiante V. The cell wall integrity signaling pathway and its involvement in secondary metabolite production. J Fungi. 2017;3(4):68.
  5. Levin DE. Cell wall integrity signaling in Saccharomyces cerevisiae. Microbiol Mol Biol Rev. 2005;69(2):262-291. https://doi.org/10.1128/MMBR.69.2.262-291.2005
  6. Rui O, Hahn M. The Slt2-type MAP kinase Bmp3 of Botrytis cinerea is required for normal saprotrophic growth, conidiation, plant surface sensing and host tissue colonization. Mol Plant Pathol. 2007;8(2):173-184. https://doi.org/10.1111/j.1364-3703.2007.00383.x
  7. Xu J-R, Staiger CJ, Hamer JE. Inactivation of the mitogen-activated protein kinase Mps1 from the rice blast fungus prevents penetration of host cells but allows activation of plant defense responses. Proc Natl Acad Sci USA. 1998;95(21):12713-12718. https://doi.org/10.1073/pnas.95.21.12713
  8. Segorbe D, Di Pietro A, P erez-Nadales E, et al. Three Fusarium oxysporum mitogen-activated protein kinases (MAPKs) have distinct and complementary roles in stress adaptation and cross-kingdom pathogenicity. Mol Plant Pathol. 2017;18(7):912-924. https://doi.org/10.1111/mpp.12446
  9. Jeon J, Goh J, Yoo S, et al. A putative MAP kinase kinase kinase, MCK1, is required for cell wall integrity and pathogenicity of the rice blast fungus, Magnaporthe oryzae. Mol Plant Microbe Interact. 2008;21(5):525-534. https://doi.org/10.1094/MPMI-21-5-0525
  10. Yin Z, Tang W, Wang J, et al. Phosphodiesterase MoPdeH targets MoMck1 of the conserved mitogen-activated protein (MAP) kinase signalling pathway to regulate cell wall integrity in rice blast fungus Magnaporthe oryzae. Mol Plant Pathol. 2016;17(5):654-668. https://doi.org/10.1111/mpp.12317
  11. Fu T, Han J-H, Shin J-H, et al. Homeobox transcription factors are required for fungal development and the suppression of host defense mechanisms in the Colletotrichum scovillei-pepper pathosystem. mBio. 2021;12(4):e01620-01621. https://doi.org/10.1128/mBio.01620-21
  12. Gao Y, He L, Li X, et al. Toxicity and biochemical action of the antibiotic fungicide tetramycin on Colletotrichum scovillei. Pestic Biochem Physiol. 2018;147:51-58. https://doi.org/10.1016/j.pestbp.2018.02.012
  13. Fu T, Shin J, Lee N, et al. Mitogen-activated protein kinase CsPMK1 is essential for pepper fruit anthracnose by Colletotrichum scovillei. Front Microbiol. 2022;13:770119.
  14. Fu T, Park H-H, Kim KS. Role of the cAMP signaling pathway in the dissemination and development on pepper fruit anthracnose disease caused by Colletotrichum scovillei. Front Cell Infect Microbiol. 2022;12:1003195.
  15. Liao CY, Chen MY, Chen YK, et al. Formation of highly branched hyphae by Colletotrichum acutatum within the fruit cuticles of Capsicum spp. Plant Pathol. 2012;61(2):262-270. https://doi.org/10.1111/j.1365-3059.2011.02523.x
  16. Fu T, Lee NH, Shin JH, et al. NADPH oxidases are required for appressorium-mediated penetration in Colletotrichum scovillei-pepper fruit pathosystem. Plant Pathol J. 2022;38(4):345-354. https://doi.org/10.5423/PPJ.OA.05.2022.0066
  17. Fu T, Park G-C, Han JH, et al. MoRBP9 encoding a ran-binding protein microtubule-organizing center is required for asexual reproduction and infection in the rice blast pathogen Magnaporthe oryzae. Plant Pathol J. 2019;35(6):564-574. https://doi.org/10.5423/PPJ.OA.07.2019.0204
  18. Shin J-H, Han J-H, Park H-H, et al. Optimization of polyethylene glycol-mediated transformation of the pepper anthracnose pathogen Colletotrichum scovillei to develop an applied genomics approach. Plant Pathol J. 2019;35(6):575-584. https://doi.org/10.5423/PPJ.OA.06.2019.0171
  19. Han J-H, Shin J-H, Fu T, et al. A new record and characterization of asparagus purple spot caused by Stemphylium vesicarium in Korea. Mycobiology. 2019;47(1):120-125. https://doi.org/10.1080/12298093.2018.1561238
  20. Fang Y-L, Xia L-M, Wang P, et al. The MAPKKK CgMck1 is required for cell wall integrity, appressorium development, and pathogenicity in Colletotrichum gloeosporioides. Genes. 2018;9(11):543.
  21. Xie M, Yang J, Jiang K, et al. AoBck1 and AoMkk1 are necessary to maintain cell wall integrity, vegetative growth, conidiation, stress resistance, and pathogenicity in the nematode-trapping fungus Arthrobotrys oligospora. Front Microbiol. 2021;12:649582.
  22. Su YY, Qi YL, Cai L. Induction of sporulation in plant pathogenic fungi. Mycology. 2012;3:195-200. https://doi.org/10.1080/21501203.2012.719042
  23. Rocha MC, Fabri JHTM, Sim~oes IT, et al. The cell wall integrity pathway contributes to the early stages of Aspergillus fumigatus asexual development. Appl Environ Microbiol. 2020;86(7):e02347-19.
  24. Zheng W, Zhao X, Xie Q, et al. A conserved homeobox transcription factor Htf1 is required for phialide development and conidiogenesis in Fusarium species. PLoS One. 2012;7(9):e45432.
  25. Gonz alez-Rubio G, Sastre-Vergara L, Molina M, et al. Substrates of the MAPK Slt2: shaping yeast cell integrity. J Fungi. 2022;8(4):368.
  26. Levin DE. Regulation of cell wall biogenesis in Saccharomyces cerevisiae: the cell wall integrity signaling pathway. Genetics. 2011;189(4):1145-1175. https://doi.org/10.1534/genetics.111.128264