Involvement of <scp>BcS</scp>tr2 in methionine biosynthesis, vegetative differentiation, multiple stress tolerance and virulence in <scp>B</scp>otrytis cinerea

Shao, Wenyong; Yang, Yalan; Lv, Chao; Ren, Weichao; Chen, Changjun

doi:10.1111/mpp.12292

Cited by 15 publications

(13 citation statements)

References 49 publications

(64 reference statements)

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“…LGI2-1, found exclusively in this clonal complex and also harboring a putative cystathionine ␥-synthase gene. The extent to which this gene mediates unique stress-related adaptations in these strains, such as those shown with cystathionine ␥-synthase of the fungal agent Botrytis cinerea in relation to resistance to osmotic, oxidative, and thermal stresses (21), remains to be determined. WGS-based analysis of LGI2 revealed sequence divergence in two other strains, J3422 (serotype 4b; CC1) and 2008-911 (serotype 1/2c; CC9) ( Fig.…”

Section: Listeria Arsenic Resistance Genomic Islandmentioning

confidence: 99%

The Arsenic Resistance-Associated Listeria Genomic Island LGI2 Exhibits Sequence and Integration Site Diversity and a Propensity for Three Listeria monocytogenes Clones with Enhanced Virulence

Lee

Ward

Jima

et al. 2017

Appl Environ Microbiol

108

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In the foodborne pathogen , arsenic resistance is encountered primarily in serotype 4b clones considered to have enhanced virulence and is associated with an arsenic resistance gene cluster within a 35-kb chromosomal region, genomic island 2 (LGI2). LGI2 was first identified in strain Scott A and includes genes putatively involved in arsenic and cadmium resistance, DNA integration, conjugation, and pathogenicity. However, the genomic localization and sequence content of LGI2 remain poorly characterized. Here we investigated 85 arsenic-resistant strains, mostly of serotype 4b. All but one of the 70 serotype 4b strains belonged to clonal complex 1 (CC1), CC2, and CC4, three major clones associated with enhanced virulence. PCR analysis suggested that 53 strains (62.4%) harbored an island highly similar to LGI2 of Scott A, frequently (42/53) in the same location as Scott A ( homolog). Random-primed PCR and whole-genome sequencing revealed seven novel insertion sites, mostly internal to chromosomal coding sequences, among strains harboring LGI2 outside the homolog. Interestingly, many CC1 strains harbored a noticeably diversified LGI2 (LGI2-1) in a unique location ( homolog) and with a novel additional gene. With few exceptions, the tested LGI2 genes were not detected in arsenic-resistant strains of serogroup 1/2, which instead often harbored a Tn-associated arsenic resistance determinant not encountered in serotype 4b. These findings indicate that in , LGI2 has a propensity for certain serotype 4b clones, exhibits content diversity, and is highly promiscuous, suggesting an ability to mobilize various accessory genes into diverse chromosomal loci. is widely distributed in the environment and causes listeriosis, a foodborne disease with high mortality and morbidity. Arsenic and other heavy metals can powerfully shape the populations of human pathogens with pronounced environmental lifestyles such as Arsenic resistance is encountered primarily in certain serotype 4b clones considered to have enhanced virulence and is associated with a large chromosomal island, genomic island 2 (LGI2). LGI2 also harbors a cadmium resistance cassette and genes putatively involved in DNA integration, conjugation, and pathogenicity. Our findings indicate that LGI2 exhibits pronounced content plasticity and is capable of transferring various accessory genes into diverse chromosomal locations. LGI2 may serve as a paradigm on how exposure to a potent environmental toxicant such as arsenic may have dynamically selected for arsenic-resistant subpopulations in certain clones of which also contribute significantly to disease.

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Section: Listeria Arsenic Resistance Genomic Islandmentioning

confidence: 99%

The Arsenic Resistance-Associated Listeria Genomic Island LGI2 Exhibits Sequence and Integration Site Diversity and a Propensity for Three Listeria monocytogenes Clones with Enhanced Virulence

Lee

Ward

Jima

et al. 2017

Appl Environ Microbiol

108

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Section: Inactivation Of Aametr Affects Several Critical Genes Relatementioning

confidence: 75%

“…In F. graminearum , fungal mutants lacking FgMetB exhibited decreased virulence to wheat, which is consistent with low levels of deoxynivalenol (DON) production in wheat kernels ( 20 ). In Botrytis cinerea , mutants lacking BcMetB exhibited significantly decreased virulence on host plant tissues ( 30 ). Consistent with our previous findings, this study demonstrated the important role of AaMetB , AaMetC , and AaMetX in the full pathogenicity of A. alternata , indicating that AaMetB , AaMetC , and AaMetX , involved in methionine biosynthesis, are critical factors related to the virulence of fungal pathogens.…”

Section: Discussionmentioning

confidence: 99%

“…In Aspergillus fumigatus , selenite sensitivity of the laeA mutant can be restored by overexpression of MetR ( 29 ). In Botrytis cinerea , BcStr2 is involved in methionine biosynthesis, and the BcStr2 deletion mutant exhibited reduced conidiation and virulence and increased sensitivity to osmotic and oxidative stress ( 30 ). In addition, the biosynthesis of methionine is also critical to the virulence of Magnaporthe oryzae and Fusarium graminearum ( 20 , 31 ).…”

Section: Introductionmentioning

confidence: 99%

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Critical Role of MetR/MetB/MetC/MetX in Cysteine and Methionine Metabolism, Fungal Development, and Virulence of Alternaria alternata

Gai

et al. 2021

Appl Environ Microbiol

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Methionine is a unique sulfur-containing amino acid which plays an important role in biological protein synthesis and various cellular processes. Here, we characterized the biological functions of AaMetB, AaMetC, and AaMetX in the tangerine pathotype of Alternaria alternata. Morphological analysis showed that the mutants lacking AaMetB, AaMetC, or AaMetX resulted in less aerial hyphae and fewer conidia in artificial media. Pathogenicity analysis showed that AaMetB, AaMetC, and AaMetX are required for full virulence. The defects in vegetative growth, conidiation, and virulence of MetB, MetC, and MetX deletion mutants (hereafter called ΔMetB, ΔMetC, and ΔMetX) can be restored by exogenous methionine and homocysteine, indicating that AaMetB, AaMetC, and AaMetX are required for methionine biosynthesis. However, exogenous cysteine restored the growth and virulence defects of ΔMetR but not ΔMetB, ΔMetC, and ΔMetX, suggesting that AaMetR is essential for cysteine biosynthesis. Oxidant sensitivity assay showed that only ΔMetR is sensitive to H2O2 and many reactive oxygen species (ROS)-generating compounds, indicating that AaMetR is essential for oxidative tolerance. Interestingly, fungicide indoor bioassays showed that only the ΔMetR mutant is susceptive to chlorothalonil, a fungicide that could bind to the cysteine of glyceraldehyde-3-phosphate dehydrogenase. Comparative transcriptome analysis showed that the inactivation of MetB, MetC, MetX, and MetR significantly affected the expression of methionine metabolism-related genes. Moreover, the inactivation of AaMetR significantly affected the expression of many genes related to glutathione metabolism, which is essential for ROS tolerance. Taken together, our study provides genetic evidence to define the critical roles of AaMetB, AaMetC, AaMetX, and AaMetR in cysteine and methionine metabolism, fungal development, and virulence of Alternaria alternata. IMPORTANCE The transcription factor MetR, regulating methionine metabolism, is essential for ROS tolerance and virulence in many phytopathogenic fungi. However, the underlying regulatory mechanism of MetR involved in this process is still unclear. In the present study, we generated AaMetB, AaMetC, and AaMetX deletion mutants and compared these mutants with AaMetR-disrupted mutants. Interestingly, we found that AaMetB, AaMetC, and AaMetX are required for vegetative growth, conidiation, and pathogenicity in Alternaria alternata but not for ROS tolerance and cysteine metabolism. Furthermore, we found that MetR is involved in the biosynthesis of cysteine, which is an essential substrate for the biosynthesis of methionine and glutathione. This study emphasizes the critical roles of MetR, MetB, MetC, and MetX in the regulation of cysteine and methionine metabolism, as well as the cross-link with glutathione-mediated ROS tolerance in phytopathogenic fungi, which provides a foundation for future investigations.

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“…The primers for the construction of gene deletion plasmids and other primers used in this study are presented in Table S2. Fungal protoplast preparation and transformations were performed as previously described with some modifications (Shao et al ., 2016). More details of the construction of the gene deletion mutants and complement strains are shown in Methods S1.…”

Section: Methodsmentioning

confidence: 99%

Plant volatile organic compound (E)‐2‐hexenal facilitates Botrytis cinerea infection of fruits by inducing sulfate assimilation

Tong

Zhang

et al. 2021

New Phytologist

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Investigation into plant-fungal pathogen interactions is one of the most interesting fields in plant sciences. However, the roles of plant volatile organic compounds in the arms race are still largely unknown.Based on precise quantification of plant volatiles, we discovered that the plant volatile organic compound (E)-2-hexenal, at concentrations that were similar to or lower than those in tissues of strawberry and tomato fruits, upregulates sulfate assimilation in spores and hyphae of the phytopathogenic fungus Botrytis cinerea. This upregulation is independent of the types of sulfur sources in the plant and can be achieved in the presence of inorganic sulfate and organic sulfur sources.Using the fungal deletion mutants, we further found that sulfate assimilation is involved in the infection of tomato and strawberry fruits by B. cinerea, and that the severity of the disease is proportional to the sulfate content in the fruits. Both before and during the infection, (E)-2hexenal induced utilisation of plant sulfate by B. cinerea facilitates its pathogenesis through enhancing its tolerance to oxidative stress.This work provides novel insights into the role of plant volatiles in plant-fungal pathogen interaction and highlights the importance of sulfur levels in the host in the prevention of grey mould disease.

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Involvement of BcStr2 in methionine biosynthesis, vegetative differentiation, multiple stress tolerance and virulence in Botrytis cinerea

Cited by 15 publications

References 49 publications

The Arsenic Resistance-Associated Listeria Genomic Island LGI2 Exhibits Sequence and Integration Site Diversity and a Propensity for Three Listeria monocytogenes Clones with Enhanced Virulence

The Arsenic Resistance-Associated Listeria Genomic Island LGI2 Exhibits Sequence and Integration Site Diversity and a Propensity for Three Listeria monocytogenes Clones with Enhanced Virulence

Critical Role of MetR/MetB/MetC/MetX in Cysteine and Methionine Metabolism, Fungal Development, and Virulence of Alternaria alternata

Plant volatile organic compound (E)‐2‐hexenal facilitates Botrytis cinerea infection of fruits by inducing sulfate assimilation

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