The G Protein Subunit α1, CaGα1, Mediates Ethylene Sensing of Mango Anthracnose Pathogen to Regulate Fungal Development and Virulence and Mediates Surface Sensing for Spore Germination

Overview

Journal Front Microbiol

Specialty Microbiology

Date 2022 Dec 12

PMID 36504764

Authors

Chao-Yang Kao

Chun-Ta Wu

Hsien-Che Lin

Dai-Keng Hsieh

Huey-Ling Lin

Miin-Huey Lee

Affiliations

Soon will be listed here.

Abstract

Mango is an important tropic fruit, but its production is highly restricted by anthracnose diseases. Mango anthracnose development is related to the fruit-ripening hormone ethylene, but how the pathogen senses ethylene and affects the infection remains largely unknown. In this study, mango pathogen strain TYC-2 was shown to sense ethylene to enhance spore germination, appressorium formation and virulence. Upon further analysis of ethylene sensing signaling, three histidine kinase genes () and a G-protein gene () were functionally characterized. Ethylene upregulated the expression of the three but had no influence on expression. No function in ethylene sensing was identified for the three . Ethylene enhanced spore germination and multiple appressorium formation of the wild-type TYC-2 but not CaGα1 mutants. TYC-2 has extremely low germination in water, where self-inhibition may play a role in ethylene sensing CaGα1 signaling. Self-inhibitors extracted from TYC-2 inhibited spore germination of TYC-2 and CaGα1 mutants, but ethylene could not rescue the inhibition, indicating that the self-inhibition was not mediated by CaGα1 and had no interactions with ethylene. Interestingly, spore germination of CaGα1 mutants was significantly enhanced in water on hydrophobic but not hydrophilic surfaces, suggesting that CaGα1 is involved in surface sensing. In the pathogenicity assay, CaGα1 mutants showed less virulence with delayed germination and little appressorium formation at early infection on mango leaves and fruit. Transcriptome and qRT-PCR analyses identified several pathogenicity-related genes regulated by ethylene, indicating that ethylene may regulate TYC-2 virulence partially by regulating the expression of these genes.

References

Barhoom S, Sharon A . cAMP regulation of "pathogenic" and "saprophytic" fungal spore germination. Fungal Genet Biol. 2004; 41(3):317-26. DOI: 10.1016/j.fgb.2003.11.011. View

Miyara I, Shafran H, Kramer Haimovich H, Rollins J, Sherman A, Prusky D . Multi-factor regulation of pectate lyase secretion by Colletotrichum gloeosporioides pathogenic on avocado fruits. Mol Plant Pathol. 2008; 9(3):281-91. PMC: 6640356. DOI: 10.1111/j.1364-3703.2007.00462.x. View

Wang W, Esch J, Shiu S, Agula H, Binder B, Chang C . Identification of important regions for ethylene binding and signaling in the transmembrane domain of the ETR1 ethylene receptor of Arabidopsis. Plant Cell. 2006; 18(12):3429-42. PMC: 1785413. DOI: 10.1105/tpc.106.044537. View

Tzima A, Paplomatas E, Tsitsigiannis D, Kang S . The G protein β subunit controls virulence and multiple growth- and development-related traits in Verticillium dahliae. Fungal Genet Biol. 2012; 49(4):271-83. DOI: 10.1016/j.fgb.2012.02.005. View

Kou Y, Naqvi N . Surface sensing and signaling networks in plant pathogenic fungi. Semin Cell Dev Biol. 2016; 57:84-92. DOI: 10.1016/j.semcdb.2016.04.019. View

Fernandez J, Orth K . Rise of a Cereal Killer: The Biology of Magnaporthe oryzae Biotrophic Growth. Trends Microbiol. 2018; 26(7):582-597. PMC: 6003838. DOI: 10.1016/j.tim.2017.12.007. View

Liang X, Shang S, Dong Q, Wang B, Zhang R, Gleason M . Transcriptomic analysis reveals candidate genes regulating development and host interactions of Colletotrichum fructicola. BMC Genomics. 2018; 19(1):557. PMC: 6064131. DOI: 10.1186/s12864-018-4934-0. View

Warwar V, Dickman M . Effects of Calcium and Calmodulin on Spore Germination and Appressorium Development in Colletotrichum trifolii. Appl Environ Microbiol. 1996; 62(1):74-9. PMC: 1388743. DOI: 10.1128/aem.62.1.74-79.1996. View

Li X, Ke Z, Xu S, Tang W, Liu Z . The G-protein alpha subunit CgGa1 mediates growth, sporulation, penetration and pathogenicity in Colletotrichum gloeosporioides. Microb Pathog. 2021; 161(Pt A):105254. DOI: 10.1016/j.micpath.2021.105254. View

10.

Lee M, Chiu C, Roubtsova T, Chou C, Bostock R . Overexpression of a redox-regulated cutinase gene, MfCUT1, increases virulence of the brown rot pathogen Monilinia fructicola on Prunus spp. Mol Plant Microbe Interact. 2010; 23(2):176-86. DOI: 10.1094/MPMI-23-2-0176. View

11.

Defosse T, Sharma A, Mondal A, Duge de Bernonville T, Latge J, Calderone R . Hybrid histidine kinases in pathogenic fungi. Mol Microbiol. 2015; 95(6):914-24. DOI: 10.1111/mmi.12911. View

12.

Papon N, Binder B . An Evolutionary Perspective on Ethylene Sensing in Microorganisms. Trends Microbiol. 2019; 27(3):193-196. DOI: 10.1016/j.tim.2018.12.002. View

13.

Podila G, Rogers L, Kolattukudy P . Chemical Signals from Avocado Surface Wax Trigger Germination and Appressorium Formation in Colletotrichum gloeosporioides. Plant Physiol. 1993; 103(1):267-272. PMC: 158972. DOI: 10.1104/pp.103.1.267. View

14.

Beckerman J, Ebbole D . MPG1, a gene encoding a fungal hydrophobin of Magnaporthe grisea, is involved in surface recognition. Mol Plant Microbe Interact. 1996; 9(6):450-6. DOI: 10.1094/mpmi-9-0450. View

15.

Herivaux A, So Y, Gastebois A, Latge J, Bouchara J, Bahn Y . Major Sensing Proteins in Pathogenic Fungi: The Hybrid Histidine Kinase Family. PLoS Pathog. 2016; 12(7):e1005683. PMC: 4965123. DOI: 10.1371/journal.ppat.1005683. View

16.

Liu X, Li B, Cai J, Zheng X, Feng Y, Huang G . Colletotrichum Species Causing Anthracnose of Rubber Trees in China. Sci Rep. 2018; 8(1):10435. PMC: 6041288. DOI: 10.1038/s41598-018-28166-7. View

17.

Chaky J, Anderson K, Moss M, Vaillancourt L . Surface Hydrophobicity and Surface Rigidity Induce Spore Germination in Colletotrichum graminicola. Phytopathology. 2008; 91(6):558-64. DOI: 10.1094/PHYTO.2001.91.6.558. View

18.

Lengeler K, Davidson R, DSouza C, Harashima T, Shen W, Wang P . Signal transduction cascades regulating fungal development and virulence. Microbiol Mol Biol Rev. 2000; 64(4):746-85. PMC: 99013. DOI: 10.1128/MMBR.64.4.746-785.2000. View

19.

Kim Y, Li D, Kolattukudy P . Induction of Ca2+-calmodulin signaling by hard-surface contact primes Colletotrichum gloeosporioides conidia to germinate and form appressoria. J Bacteriol. 1998; 180(19):5144-50. PMC: 107551. DOI: 10.1128/JB.180.19.5144-5150.1998. View

20.

Yu P, Wang C, Chen P, Lee M . YAP1 homologue-mediated redox sensing is crucial for a successful infection by Monilinia fructicola. Mol Plant Pathol. 2016; 18(6):783-797. PMC: 6638302. DOI: 10.1111/mpp.12438. View