Confocal microscopy study to understand<i>Clonostachys rosea</i>and<i>Botrytis cinerea</i>interactions in tomato plants

Saraiva, Rodrigo Moreira; Czymmek, Kirk; Borges, Álefe Vitorino; Caires, Nilmara Pereira; Maffia, Luiz A.

doi:10.1080/09583157.2014.948382

Cited by 11 publications

(10 citation statements)

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“…Deletion of lysm1 or lysm2 does not influence this ability; however, the failure of the lysm1 lysm2 double deletion strains to suppress expression of PR1 and PR4 to the same extent as the WT strain provides an indication that both LYSM proteins jointly influence this ability. The increased ratio between C. rosea and wheat DNA during root surface colonization and reduced ability of internal root colonization of the lysm2 strain, shows that LYSM2 also influences the interaction of C. rosea with plants; although, the exact mechanism will require extensive microscopic investigations of the root colonization process (Saraiva et al, 2015). The role of the LYSM2 protein in internal root colonization is in line with several examples from plant pathogenic fungi where deletion of LysM effector genes reduces their ability to infect the host plant (de Jonge and Thomma, 2009;de Jonge et al, 2010;Marshall et al, 2011;Mentlak et al, 2012;Kombrink and Thomma, 2013;Takahara et al, 2016).…”

Section: Discussionmentioning

confidence: 99%

LysM Proteins Regulate Fungal Development and Contribute to Hyphal Protection and Biocontrol Traits in Clonostachys rosea

et al. 2020

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Lysin motif (LysM) modules are approximately 50 amino acids long and bind to peptidoglycan, chitin and its derivatives. Certain LysM proteins in plant pathogenic and entomopathogenic fungi are shown to scavenge chitin oligosaccharides and thereby dampen host defense reactions. Other LysM proteins can protect the fungal cell wall against hydrolytic enzymes. In this study, we investigated the biological function of LysM proteins in the mycoparasitic fungus Clonostachys rosea. The C. rosea genome contained three genes coding for LysM-containing proteins and gene expression analysis revealed that lysm1 and lysm2 were induced during mycoparasitic interaction with Fusarium graminearum and during colonization of wheat roots. Lysm1 was suppressed in germinating conidia, while lysm2 was induced during growth in chitin or peptidoglycan-containing medium. Deletion of lysm1 and lysm2 resulted in mutants with increased levels of conidiation and conidial germination, but reduced ability to control plant diseases caused by F. graminearum and Botrytis cinerea. The lysm2 strain showed a distinct, accelerated mycelial disintegration phenotype accompanied by reduced biomass production and hyphal protection against hydrolytic enzymes including chitinases, suggesting a role of LYSM2 in hyphal protection against chitinases. The lysm2 and lysm1 lysm2 strains displayed reduced ability to colonize wheat roots, while only lysm1 lysm2 failed to suppress expression of the wheat defense response genes PR1 and PR4. Based on our data, we propose a role of LYSM1 as a regulator of fungal development and of LYSM2 in cell wall protection against endogenous hydrolytic enzymes, while both are required to suppress plant defense responses. Our findings expand the understanding of the role of LysM proteins in fungal-fungal interactions and biocontrol.

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Section: Discussionmentioning

confidence: 99%

LysM Proteins Regulate Fungal Development and Contribute to Hyphal Protection and Biocontrol Traits in Clonostachys rosea

et al. 2020

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“…However, C. rosea is not a plant pathogenic fungus and hence the selective advantages for high numbers of PL1 genes in this species should be different from plant pathogenic fungi. C. rosea is reported to intimately interact with plants through root surface colonization [ 24 , 42 ] and by penetrating epidermal cells [ 43 ]. This intimate interaction with plants can result in plant growth promotion [ 44 ] and induction of defense reactions in both wheat and tomato [ 44 , 45 ], but it is difficult to argue how this superficial level of plant interaction can justify the existence of 17 PL1 genes in C. rosea .…”

Section: Discussionmentioning

confidence: 99%

Evolution and functional characterization of pectate lyase PEL12, a member of a highly expanded Clonostachys rosea polysaccharide lyase 1 family

et al. 2018

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BackgroundPectin is one of the major and most complex plant cell wall components that needs to be overcome by microorganisms as part of their strategies for plant invasion or nutrition. Microbial pectinolytic enzymes therefore play a significant role for plant-associated microorganisms and for the decomposition and recycling of plant organic matter. Recently, comparative studies revealed significant gene copy number expansion of the polysaccharide lyase 1 (PL1) pectin/pectate lyase gene family in the Clonostachys rosea genome, while only low numbers were found in Trichoderma species. Both of these fungal genera are widely known for their ability to parasitize and kill other fungi (mycoparasitism) and certain species are thus used for biocontrol of plant pathogenic fungi.ResultsIn order to understand the role of the high number of pectin degrading enzymes in Clonostachys, we studied diversity and evolution of the PL1 gene family in C. rosea compared with other Sordariomycetes with varying nutritional life styles. Out of 17 members of C. rosea PL1, we could only detect two to be secreted at acidic pH. One of them, the pectate lyase pel12 gene was found to be strongly induced by pectin and, to a lower degree, by polygalacturonic acid. Heterologous expression of the PEL12 in a PL1-free background of T. reesei revealed direct enzymatic involvement of this protein in utilization of pectin at pH 5 without a requirement for Ca2+. The mutants showed increased utilization of pectin compounds, but did not increase biocontrol ability in detached leaf assay against the plant pathogen Botrytis cinerea compared to the wild type.ConclusionsIn this study, we aimed to gain insight into diversity and evolution of the PL1 gene family in C. rosea and other Sordariomycete species in relation to their nutritional modes. We show that C. rosea PL1 expansion does not correlate with its mycoparasitic nutritional mode and resembles those of strong plant pathogenic fungi. We further investigated regulation, specificity and function of the C. rosea PEL12 and show that this enzyme is directly involved in degradation of pectin and pectin-related compounds, but not in C. rosea biocontrol.Electronic supplementary materialThe online version of this article (10.1186/s12866-018-1310-9) contains supplementary material, which is available to authorized users.

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“…These fungi can be found as saprotrophs in various ecological niches including soil and dead organic matter ( Moreira et al, 2016 ; Jensen et al, 2021 ). Certain species can thrive in rhizospheres where they can colonize the plant root surfaces and establish a beneficial relationship with the plant host as endophytes ( Sutton et al, 2002 ; Karlsson et al, 2015 ; Saraiva et al, 2015 ; Maillard et al, 2020 ; Jensen et al, 2021 ). In addition, these species can live as necrotrophic mycoparasites by killing and feeding on their mycohosts ( Alvindia and Natsuaki, 2008 ; Dugan et al, 2012 ; Sun et al, 2018 ; Jensen et al, 2021 ).…”

Section: Introductionmentioning

confidence: 99%

“…To succeed in these distinct ecological niches, Clonostachys spp. have evolved capabilities for decomposition of organic materials, competition with other microorganisms for nutrients and space in soil and rhizosphere, and interference competition through antibiosis and mycoparasitism ( Morandi et al, 2000 ; Li et al, 2002 ; Saraiva et al, 2015 ; Sun et al, 2017 ; Fatema et al, 2018 ). Due to these properties, certain Clonostachys strains are used as efficient biological control agents against fungal plant diseases in agricultural and horticultural production systems ( Jensen et al, 2000 ; Sutton et al, 2002 ; Xue et al, 2008 ; Cota et al, 2009 ; Salamone et al, 2018 ).…”

Section: Introductionmentioning

confidence: 99%

Insights into the ecological generalist lifestyle of Clonostachys fungi through analysis of their predicted secretomes

Piombo

Guaschino²,

Jensen³

et al. 2023

Front. Microbiol.

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IntroductionThe fungal secretome comprise diverse proteins that are involved in various aspects of fungal lifestyles, including adaptation to ecological niches and environmental interactions. The aim of this study was to investigate the composition and activity of fungal secretomes in mycoparasitic and beneficial fungal-plant interactions.MethodsWe used six Clonostachys spp. that exhibit saprotrophic, mycotrophic and plant endophytic lifestyles. Genome-wide analyses was performed to investigate the composition, diversity, evolution and gene expression of Clonostachys secretomes in relation to their potential role in mycoparasitic and endophytic lifestyles.Results and discussionOur analyses showed that the predicted secretomes of the analyzed species comprised between 7 and 8% of the respective proteomes. Mining of transcriptome data collected during previous studies showed that 18% of the genes encoding predicted secreted proteins were upregulated during the interactions with the mycohosts Fusarium graminearum and Helminthosporium solani. Functional annotation of the predicted secretomes revealed that the most represented protease family was subclass S8A (11–14% of the total), which include members that are shown to be involved in the response to nematodes and mycohosts. Conversely, the most numerous lipases and carbohydrate-active enzyme (CAZyme) groups appeared to be potentially involved in eliciting defense responses in the plants. For example, analysis of gene family evolution identified nine CAZyme orthogroups evolving for gene gains (p ≤ 0.05), predicted to be involved in hemicellulose degradation, potentially producing plant defense-inducing oligomers. Moreover, 8–10% of the secretomes was composed of cysteine-enriched proteins, including hydrophobins, important for root colonization. Effectors were more numerous, comprising 35–37% of the secretomes, where certain members belonged to seven orthogroups evolving for gene gains and were induced during the C. rosea response to F. graminearum or H. solani. Furthermore, the considered Clonostachys spp. possessed high numbers of proteins containing Common in Fungal Extracellular Membranes (CFEM) modules, known for their role in fungal virulence. Overall, this study improves our understanding of Clonostachys spp. adaptation to diverse ecological niches and establishes a basis for future investigation aiming at sustainable biocontrol of plant diseases.

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Confocal microscopy study to understandClonostachys roseaandBotrytis cinereainteractions in tomato plants

Cited by 11 publications

References 31 publications

LysM Proteins Regulate Fungal Development and Contribute to Hyphal Protection and Biocontrol Traits in Clonostachys rosea

LysM Proteins Regulate Fungal Development and Contribute to Hyphal Protection and Biocontrol Traits in Clonostachys rosea

Evolution and functional characterization of pectate lyase PEL12, a member of a highly expanded Clonostachys rosea polysaccharide lyase 1 family

Insights into the ecological generalist lifestyle of Clonostachys fungi through analysis of their predicted secretomes

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