Transcriptome analysis and functional validation reveal a novel gene, <i>BcCGF1</i>, that enhances fungal virulence by promoting infection‐related development and host penetration

Zhang, Mingzhe; Sun, Chenhao; Liu, Yue; Feng, Hui-Qiang; Chang, Haowu; Cao, Shengnan; Li, Guihua; Song, Yang; Hou, Jie; Zhu‐Salzman, Keyan; Zhang, Hao; Qin, Qing‐Ming

doi:10.1111/mpp.12934

Cited by 30 publications

(30 citation statements)

References 60 publications

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“…ROS might assist in host invasion by providing substrates for oxidases that can modify the cuticle [ 9 ]. Moreover, endogenous ROS play crucial roles in B. cinerea conidial germination and host penetration [ 55 , 56 ]. Here, we show that oxidoreductase activities are enriched in upregulated fungal genes during early P. patens infection (4 hpi), including genes encoding BcniaD and BcniiA, that are further upregulated during the entire time course of infection analyzed.…”

Section: Discussionmentioning

confidence: 99%

Botrytis cinerea Transcriptome during the Infection Process of the Bryophyte Physcomitrium patens and Angiosperms

Reboledo

Agorio

Vignale

et al. 2020

JoF

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Botrytis cinerea is a necrotrophic pathogen that causes grey mold in many plant species, including crops and model plants of angiosperms. B. cinerea also infects and colonizes the bryophyte Physcomitrium patens (previously Physcomitrella patens), which perceives the pathogen and activates defense mechanisms. However, these defenses are not sufficient to stop fungal invasion, leading finally to plant decay. To gain more insights into B. cinerea infection and virulence strategies displayed during moss colonization, we performed genome wide transcriptional profiling of B. cinerea during different infection stages. We show that, in total, 1015 B. cinerea genes were differentially expressed in moss tissues. Expression patterns of upregulated genes and gene ontology enrichment analysis revealed that infection of P. patens tissues by B. cinerea depends on reactive oxygen species generation and detoxification, transporter activities, plant cell wall degradation and modification, toxin production and probable plant defense evasion by effector proteins. Moreover, a comparison with available RNAseq data during angiosperm infection, including Arabidopsis thaliana, Solanum lycopersicum and Lactuca sativa, suggests that B. cinerea has virulence and infection functions used in all hosts, while others are more specific to P. patens or angiosperms.

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Section: Discussionmentioning

confidence: 99%

Botrytis cinerea Transcriptome during the Infection Process of the Bryophyte Physcomitrium patens and Angiosperms

Reboledo

Agorio

Vignale

et al. 2020

JoF

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“…To investigate the roles of BcCYP2 in the pathogen growth and virulence, we generated B. cinerea BcCYP2 knockout (KO) mutant ∆ Bccyp2 with the illustrated strategy ( Figure S1b ) and its complemented strain ∆ Bccyp2 -C as previously described [ 6 , 35 , 36 ]. The deletion of BcCYP2 in the mutant strains was confirmed by PCR detection and quantitative reverse transcription PCR (qRT-PCR) analysis ( Figure S1c ).…”

Section: Resultsmentioning

confidence: 99%

“…The vector pSULPH, resistant to chlorimuron ethyl, was used to generate the complemented strain Δ Bccyp2 -C [ 6 , 35 , 36 ]. The fragment containing 1156 bp upstream and 1070 bp downstream of BcCYP2 coding region was amplified by PCR and cloned into pSULPH to generate the complementary vector.…”

Section: Methodsmentioning

confidence: 99%

Cyclophilin BcCyp2 Regulates Infection-Related Development to Facilitate Virulence of the Gray Mold Fungus Botrytis cinerea

Sun

Chang

et al. 2021

IJMS

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Cyclophilin (Cyp) and Ca2+/calcineurin proteins are cellular components related to fungal morphogenesis and virulence; however, their roles in mediating the pathogenesis of Botrytis cinerea, the causative agent of gray mold on over 1000 plant species, remain largely unexplored. Here, we show that disruption of cyclophilin gene BcCYP2 did not impair the pathogen mycelial growth, osmotic and oxidative stress adaptation as well as cell wall integrity, but delayed conidial germination and germling development, altered conidial and sclerotial morphology, reduced infection cushion (IC) formation, sclerotial production and virulence. Exogenous cyclic adenosine monophosphate (cAMP) rescued the deficiency of IC formation of the ∆Bccyp2 mutants, and exogenous cyclosporine A (CsA), an inhibitor targeting cyclophilins, altered hyphal morphology and prevented host-cell penetration in the BcCYP2 harboring strains. Moreover, calcineurin-dependent (CND) genes are differentially expressed in strains losing BcCYP2 in the presence of CsA, suggesting that BcCyp2 functions in the upstream of cAMP- and Ca2+/calcineurin-dependent signaling pathways. Interestingly, during IC formation, expression of BcCYP2 is downregulated in a mutant losing BcJAR1, a gene encoding histone 3 lysine 4 (H3K4) demethylase that regulates fungal development and pathogenesis, in B. cinerea, implying that BcCyp2 functions under the control of BcJar1. Collectively, our findings provide new insights into cyclophilins mediating the pathogenesis of B. cinerea and potential targets for drug intervention for fungal diseases.

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“…Indeed, one region identified in the G1 population contains the gene encoding the Pectin Methyl Esterase BcPme1 required for full virulence of B. cinerea on several host including grapevine (Valette-Collet et al . 2003), and another region contains the gene encoding BcCgf1, a small secreted protein that is essential for infection structure development (Zhang et al . 2020).…”

Section: Resultsmentioning

confidence: 99%

Population Genomics Reveals Molecular Determinants of Specialization to Tomato in the Polyphagous Fungal PathogenBotrytis cinereain France

Mercier

Simon

Lapalu

et al. 2020

Preprint

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Many fungal plant pathogens encompass multiple populations specialized on different plant species. Understanding the factors underlying pathogen adaptation to their hosts is a major challenge of evolutionary microbiology, and it should help preventing the emergence of new specialized pathogens on novel hosts. Previous studies have shown that French populations of the grey mould pathogen Botrytis cinerea parasitizing tomato and grapevine are differentiated from each other, and have higher aggressiveness on their host-of-origin than on other hosts, indicating some degree of host specialization in this polyphagous pathogen. Here, we aimed at identifying the genomic features underlying the specialization of B. cinerea populations to tomato and grapevine. Based on whole genome sequences of 32 isolates, we confirmed the subdivision of B. cinerea pathogens into two genetic clusters on grapevine and another, single cluster on tomato. Levels of genetic variation in the different clusters were similar, suggesting that the tomato-specific cluster has not recently emerged following a bottleneck. Using genome scans for selective sweeps and divergent selection, tests of positive selection based on polymorphism and divergence at synonymous and non-synonymous sites and analyses of presence/absence variation, we identified several candidate genes that represent possible determinants of host specialization in the tomato-associated population. This work deepens our understanding of the genomic changes underlying the specialization of fungal pathogen populations.

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Transcriptome analysis and functional validation reveal a novel gene, BcCGF1, that enhances fungal virulence by promoting infection‐related development and host penetration

Abstract: This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

Cited by 30 publications

References 60 publications

Botrytis cinerea Transcriptome during the Infection Process of the Bryophyte Physcomitrium patens and Angiosperms

Botrytis cinerea Transcriptome during the Infection Process of the Bryophyte Physcomitrium patens and Angiosperms

Cyclophilin BcCyp2 Regulates Infection-Related Development to Facilitate Virulence of the Gray Mold Fungus Botrytis cinerea

Population Genomics Reveals Molecular Determinants of Specialization to Tomato in the Polyphagous Fungal PathogenBotrytis cinereain France

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