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Distinct Roles of Ena ATP Family Proteins in Sodium Accumulation, Invasive Growth, and Full Virulence in Colletotrichum gloeosporioides.

ABSTRACT: Colletotrichum gloeosporioides, a significant fungal pathogen of crops and trees, causes large economic losses worldwide. However, its pathogenic mechanism remains totally unclear. In this study, four Ena ATPases (Exitus natru-type adenosine triphosphatases), homology of yeast Ena proteins, were identified in C. gloeosporioides. Gene deletion mutants of ΔCgena1, ΔCgena2, ΔCgena3, and ΔCgena4 were obtained through the method of gene replacement. First, a subcellular localization pattern indicated that CgEna1 and CgEna4 were localized in the plasma membrane, while the CgEna2 and CgEna3 were distributed in the endoparasitic reticulum. Next, it was found that CgEna1 and CgEna4 were required for sodium accumulation in C. gloeosporioides. CgEna3 was required for extracellular ion stress of sodium and potassium. CgEna1 and CgEna3 were involved in conidial germination, appressorium formation, invasive hyphal development, and full virulence. The mutant of ΔCgena4 was more sensitive to the conditions of high concentrations of ion and the alkaline. Together, these results indicated that CgEna ATPase proteins have distinct roles in sodium accumulation, stress resistance, and full virulence in C. gloeosporioides.

SUBMITTER: Deng TC

PROVIDER: S-EPMC10219246 | biostudies-literature | 2023 May

REPOSITORIES: biostudies-literature

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Distinct Roles of Ena ATP Family Proteins in Sodium Accumulation, Invasive Growth, and Full Virulence in Colletotrichum gloeosporioides.

Deng Tian-Ci TC Yang Ji-Yun JY Sun Mei-Ling ML Zhang Yun-Zhao YZ Pan Yun-Ting YT Huang Lin L

Journal of fungi (Basel, Switzerland) 20230513 5

Colletotrichum gloeosporioides, a significant fungal pathogen of crops and trees, causes large economic losses worldwide. However, its pathogenic mechanism remains totally unclear. In this study, four Ena ATPases (Exitus natru-type adenosine triphosphatases), homology of yeast Ena proteins, were identified in C. gloeosporioides. Gene deletion mutants of ΔCgena1, ΔCgena2, ΔCgena3, and ΔCgena4 were obtained through the method of gene replacement. Fi ...[more]

PMID: 37233277

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Project description:The limit of the Colletotrichum gloeosporioides species complex is defined genetically, based on a strongly supported clade within the Colletotrichum ITS gene tree. All taxa accepted within this clade are morphologically more or less typical of the broadly defined C. gloeosporioides, as it has been applied in the literature for the past 50 years. We accept 22 species plus one subspecies within the C. gloeosporioides complex. These include C. asianum, C. cordylinicola, C. fructicola, C. gloeosporioides, C. horii, C. kahawae subsp. kahawae, C. musae, C. nupharicola, C. psidii, C. siamense, C. theobromicola, C. tropicale, and C. xanthorrhoeae, along with the taxa described here as new, C. aenigma, C. aeschynomenes, C. alatae, C. alienum, C. aotearoa, C. clidemiae, C. kahawae subsp. ciggaro, C. salsolae, and C. ti, plus the nom. nov. C. queenslandicum (for C. gloeosporioides var. minus). All of the taxa are defined genetically on the basis of multi-gene phylogenies. Brief morphological descriptions are provided for species where no modern description is available. Many of the species are unable to be reliably distinguished using ITS, the official barcoding gene for fungi. Particularly problematic are a set of species genetically close to C. musae and another set of species genetically close to C. kahawae, referred to here as the Musae clade and the Kahawae clade, respectively. Each clade contains several species that are phylogenetically well supported in multi-gene analyses, but within the clades branch lengths are short because of the small number of phylogenetically informative characters, and in a few cases individual gene trees are incongruent. Some single genes or combinations of genes, such as glyceraldehyde-3-phosphate dehydrogenase and glutamine synthetase, can be used to reliably distinguish most taxa and will need to be developed as secondary barcodes for species level identification, which is important because many of these fungi are of biosecurity significance. In addition to the accepted species, notes are provided for names where a possible close relationship with C. gloeosporioides sensu lato has been suggested in the recent literature, along with all subspecific taxa and formae speciales within C. gloeosporioides and its putative teleomorph Glomerella cingulata.Taxonomic noveltiesName replacement - C. queenslandicum B. Weir & P.R. Johnst. New species - C. aenigma B. Weir & P.R. Johnst., C. aeschynomenes B. Weir & P.R. Johnst., C. alatae B. Weir & P.R. Johnst., C. alienum B. Weir & P.R. Johnst, C. aotearoa B. Weir & P.R. Johnst., C. clidemiae B. Weir & P.R. Johnst., C. salsolae B. Weir & P.R. Johnst., C. ti B. Weir & P.R. Johnst. New subspecies - C. kahawae subsp. ciggaro B. Weir & P.R. Johnst. Typification: Epitypification - C. queenslandicum B. Weir & P.R. Johnst.

Project description:BackgroundIpomoea cairica (L.) Sweet is a destructive invasive weed in South China but rarely infected with pathogens in nature. Its pathogen resistance mechanism is largely unknown at present. Some non-pathogenic isolates of Fusarium oxysporum and Fusarium fujikuroi are prevalent on many plant species and function as pathogen resistance inducers of host plants. The objective of the present research is to investigate whether the symbiosis between the both fungi and I. cairica is present, and thereby induces pathogen resistance of I. cairica.MethodsThrough field investigation, we explored the occurrence rates of F. oxysporum and F. fujikuroi on leaf surfaces of I. cairica plants in natural habitats and compared their abundance between healthy leaves and leaves infected with Colletotrichum gloeosporioides, a natural pathogen. With artificial inoculation, we assessed their pathogenicity to I. cairica and studied their contribution of pathogen resistance to I. cairica against C. gloeosporioides.ResultsWe found that F. oxysporum and F. fujikuroi were widely epiphytic on healthy leaf surfaces of I. cairica in sunny non-saline, shady non-saline and sunny saline habitats. Their occurrence rates reached up to 100%. Moreover, we found that the abundance of F. oxysporum and F. fujikuroi on leaves infected with C. gloeosporioides were significantly lower than that of healthy leaves. With artificial inoculation, we empirically confirmed that F. oxysporum and F. fujikuroi were non-pathogenic to I. cairica. It was interesting that colonization by F. fujikuroi, F. oxysporum alone and a mixture of both fungi resulted in a reduction of C. gloeosporioides infection to I. cairica accompanied by lower lesion area to leaf surface area ratio, increased hydrogen peroxide (H2O2) concentration and salicylic acid (SA) level relative to the control. However, NPR1 expression, chitinase and β-1,3-glucanase activities as well as stem length and biomass of I. cairica plant only could be significantly improved by F. oxysporum and a mixture of both fungi but not by F. fujikuroi. In addition, as compared to colonization by F. oxysporum and a mixture of both fungi, F. fujikuroi induced significantly higher jasmonic acid (JA) level but significantly lower β-1,3-glucanase activity in leaves of I. cairica plants. Thus, our findings indicated the symbiosis of epiphytic fungi F. fujikuroi and F. oxysporum induced systemic resistance of I. cairica against C. gloeosporioides. F. oxysporum played a dominant role in inducing pathogen resistance of I. cairica. Its presence alleviated the antagonism of the JA signaling on SA-dependent β-1,3-glucanase activity and enabled I. cairica plants to maintain relatively higher level of resistance against C. gloeosporioides.

Dataset Information

Distinct Roles of Ena ATP Family Proteins in Sodium Accumulation, Invasive Growth, and Full Virulence in Colletotrichum gloeosporioides.

Publications

Distinct Roles of Ena ATP Family Proteins in Sodium Accumulation, Invasive Growth, and Full Virulence in <i>Colletotrichum gloeosporioides</i>.

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