Browse > Article
http://dx.doi.org/10.1080/12298093.2022.2148393

The Autophagy Protein CsATG8 is Involved in Asexual Development and Virulence in the Pepper Anthracnose Fungus Colletotrichum scovillei  

Kwang Ho Lee (Division of Bio-Resource Sciences and Interdisciplinary Program in Smart Agriculture, Kangwon National University)
Adiyantara Gumilang (Division of Bio-Resource Sciences and Interdisciplinary Program in Smart Agriculture, Kangwon National University)
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)
Kyoung Su Kim (Division of Bio-Resource Sciences and Interdisciplinary Program in Smart Agriculture, Kangwon National University)
Publication Information
Mycobiology / v.50, no.6, 2022 , pp. 467-474 More about this Journal
Abstract
Autophagy serves as a survival mechanism and plays important role in nutrient recycling under conditions of starvation, nutrient storage, ad differentiation of plant pathogenic fungi. However, autophagy-related genes have not been investigated in Colletotrichum scovillei, a causal agent of pepper fruit anthracnose disease. ATG8 is involved in autophagosome formation and is considered a marker of autophagy. Therefore, we generated an ATG8 deletion mutant, ΔCsatg8, via homologous recombination to determine the functional roles of CsATG8 in the development and virulence of C. scovillei. Compared with the wild-type, the deletion mutant ΔCsatg8 exhibited a severe reduction in conidiation. Conidia produced by ΔCsatg8 were defective in survival, conidial germination, and appressorium formation. Moreover, conidia of ΔCsatg8 showed reduced lipid amount and PTS1 selectivity. A virulence assay showed that anthracnose development on pepper fruits was reduced in ΔCsatg8. Taken together, our results suggest that CsATG8 plays various roles in conidium production and associated development, and virulence in C. scovillei.
Keywords
Colletotrichum scovillei; pepper anthracnose; autophagy; CsATG8;
Citations & Related Records
Times Cited By KSCI : 7  (Citation Analysis)
연도 인용수 순위
1 Asakura M, Ninomiya S, Sugimoto M, et al. Atg26-mediated pexophagy is required for host invasion by the plant pathogenic fungus Colletotrichum orbiculare. Plant Cell. 2009;21(4):1291-1304.   DOI
2 Deng Y, Qu Z, Naqvi NI. Role of macroautophagy in nutrient homeostasis during fungal development and pathogenesis. Cells. 2012;1(3):449-463.   DOI
3 Kershaw MJ, Talbot NJ. Genome-wide functional analysis reveals that infection-associated fungal autophagy is necessary for rice blast disease. Proc Natl Acad Sci USA. 2009;106(37):15967-15972.   DOI
4 Hirata E, Ohya Y, Suzuki K. Atg4 plays an important role in efficient expansion of autophagic isolation membranes by cleaving lipidated Atg8 in Saccharomyces cerevisiae. PLoS One. 2017;12(7):e0181047.
5 Nakatogawa H, Suzuki K, Kamada Y, et al. Dynamics and diversity in autophagy mechanisms: lessons from yeast. Nat Rev Mol Cell Biol. 2009;10(7):458-467.   DOI
6 Deng YZ, Ramos-Pamplona M, Naqvi NI. Autophagy-assisted glycogen catabolism regulates asexual differentiation in Magnaporthe oryzae. Autophagy. 2009;5(1):33-43.   DOI
7 Yu JH, Hamari Z, Han KH, et al. Double-joint PCR: a PCR-based molecular tool for gene manipulations in filamentous fungi. Fungal Genet Biol. 2004;41(11):973-981.   DOI
8 Choi J, Kim Y, Kim S, et al. MoCRZ1, a gene encoding a calcineurin-responsive transcription factor, regulates fungal growth and pathogenicity of Magnaporthe oryzae. Fungal Genet Biol. 2009;46(3):243-254.   DOI
9 Kim S, Park SY, Kim KS, et al. Homeobox transcription factors are required for conidiation and appressorium development in the rice blast fungus Magnaporthe oryzae. PLOS Genet. 2009;5(12):e1000757.
10 Sweigard JA, Chumley FG, Valent B. Cloning and analysis of CUT1, a cutinase gene from Magnaporthe grisea. Mol Gen Genet. 1992;232(2):174-182.   DOI
11 Shin JH, Han JH, Park HH, 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.   DOI
12 Wang JY, Wu XY, Zhang Z, et al. Fluorescent co-localization of PTS1 and PTS2 and its application in analysis of the gene function and the peroxisomal dynamic in Magnaporthe oryzae. J Zhejiang Univ Sci B. 2008;9(10):802-810.   DOI
13 Kim JO, Choi KY, Han JH, et al. The complete mitochondrial genome sequence of the ascomycete plant pathogen Colletotrichum acutatum. Mitochondrial DNA A DNA Mapp Seq Anal. 2016;27(6):4547-4548.
14 Chi MH, Park SY, Lee YH. A quick and safe method for fungal DNA extraction. Plant Pathol J. 2009;25(1):108-111.   DOI
15 Sambrook J, Russell DW. 2001. Molecular cloning: a laboratory manual. 3rd ed. Cold Spring Harbor (NY): Cold Spring Harbor Laboratory Press.
16 Han JH, Chon JK, Ahn JH, et al. Whole genome sequence and genome annotation of Colletotrichum acutatum, causal agent of anthracnose in pepper plants in South Korea. Genom Data. 2016;8:45-46.
17 Bianchi DE, Turian G. Lipid content of conidia of Neurospora crassa. Nature. 1967;214(5095):1344-1345.   DOI
18 Daryaei A. Conidium "fitness" in Trichoderma [dissertation]. Oxford (PA): Lincoln University; 2014.
19 Fu T, Shin JH, Lee NH, et al. Mitogen-activated protein kinase CsPMK1 is essential for pepper fruit anthracnose by Colletotrichum scovillei. Front Microbiol. 2022;13:770119.
20 Jeon J, Rho H, Kim S, et al. Role of MoAND1-mediated nuclear positioning in morphogenesis and pathogenicity in the rice blast fungus, Magnaporthe oryzae. Fungal Genet Biol. 2014;69:43-51.   DOI
21 Park J, Kong S, Kim S, et al. Roles of forkhead-box transcription factors in controlling development, pathogenicity, and stress response in Magnaporthe oryzae. Plant Pathol J. 2014;30(2):136-150.   DOI
22 Sun CB, Suresh A, Deng YZ, et al. A multidrug resistance transporter in magnaporthe is required for host penetration and for survival during oxidative stress. Plant Cell. 2006;18(12):3686-3705.
23 Otera H, Okumoto K, Tateishi K, et al. Peroxisome targeting signal type 1 (PTS1) receptor is involved in import of both PTS1 and PTS2: studies with PEX5-defective CHO cell mutants. Mol Cell Biol. 1998;18(1):388-399.   DOI
24 Liu XH, Lu JP, Zhang L, et al. Involvement of a Magnaporthe grisea serine/threonine kinase gene, MgATG1, in appressorium turgor and pathogenesis. Eukaryot Cell. 2007;6(6):997-1005.   DOI
25 Shin JH, Fu T, Kim KS. Pex7 selectively imports PTS2 target proteins to peroxisomes and is required for anthracnose disease development in Colletotrichum scovillei. Fungal Genet Biol. 2021;157:103636.
26 Fujiki Y, Matsuzono Y, Matsuzaki T, et al. Import of peroxisomal membrane proteins: the interplay of Pex3p-and Pex19p-mediated interactions. Biochim Biophys Acta. 2006;1763(12):1639-1646.   DOI
27 Food and Agriculture Organization of the United Nations [Internet]. Rome (Italy): FAOSTAT; 2021 [cited 2021 November 3]. Available from: http://www.fao.org/faostat/en/#data/QC/
28 Lee NH, Fu T, Shin JH, et al. The small GTPase CsRAC1 is important for fungal development and pepper anthracnose in Colletotrichum scovillei. Plant Pathol J. 2021;37(6):607-618.   DOI
29 Forster H, Adaskaveg JE. Identification of subpopulations of Colletotrichum acutatum and epidemiology of almond anthracnose in California. Phytopathology. 1999;89(11):1056-1065.   DOI
30 Giacomin RM, de Fatima Ruas C, Moreira AFP, et al. Inheritance of anthracnose resistance (Colletotrichum scovillei) in ripe and unripe Capsicum annuum fruits. J Phytopathol. 2020;168(3):184-192.   DOI
31 Saxena A, Raghuwanshi R, Gupta VK, et al. Chilli anthracnose: the epidemiology and management. Front Microbiol. 2016;7:1527.
32 Klionsky DJ, Cuervo AM, Seglen PO. Methods for monitoring autophagy from yeast to human. Autophagy. 2007;3(3):181-206.   DOI
33 Fu T, Han JH, Shin JH, 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.
34 Yorimitsu T, Klionsky DJ. Autophagy: molecular machinery for self-eating. Cell Death Differ. 2005;12(S2):1542-1552.   DOI
35 Pollack JK, Harris SD, Marten MR. Autophagy in filamentous fungi. Fungal Genet Biol. 2009;46(1):1-8.   DOI
36 Pinan-Lucarre B, Balguerie A, Clave C. Accelerated cell death in Podospora autophagy mutants. Eukaryot Cell. 2005;4(11):1765-1774.   DOI
37 Pollack JK, Li ZJ, Marten MR. Fungal mycelia show lag time before re-growth on endogenous carbon. Biotechnol Bioeng. 2008;100(3):458-465.   DOI
38 Reggiori F, Klionsky DJ. Autophagy in the eukaryotic cell. Eukaryot Cell. 2002;1(1):11-21.   DOI