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Genomic and transcriptomic analyses of the tangerine pathotype of Alternaria alternata in response to oxidative stress.

ABSTRACT: The tangerine pathotype of Alternaria alternata produces the A. citri toxin (ACT) and is the causal agent of citrus brown spot that results in significant yield losses worldwide. Both the production of ACT and the ability to detoxify reactive oxygen species (ROS) are required for A. alternata pathogenicity in citrus. In this study, we report the 34.41?Mb genome sequence of strain Z7 of the tangerine pathotype of A. alternata. The host selective ACT gene cluster in strain Z7 was identified, which included 25 genes with 19 of them not reported previously. Of these, 10 genes were present only in the tangerine pathotype, representing the most likely candidate genes for this pathotype specialization. A transcriptome analysis of the global effects of H2O2 on gene expression revealed 1108 up-regulated and 498 down-regulated genes. Expressions of those genes encoding catalase, peroxiredoxin, thioredoxin and glutathione were highly induced. Genes encoding several protein families including kinases, transcription factors, transporters, cytochrome P450, ubiquitin and heat shock proteins were found associated with adaptation to oxidative stress. Our data not only revealed the molecular basis of ACT biosynthesis but also provided new insights into the potential pathways that the phytopathogen A. alternata copes with oxidative stress.

SUBMITTER: Wang M

PROVIDER: S-EPMC5007530 | biostudies-literature | 2016 Sep

REPOSITORIES: biostudies-literature

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Genomic and transcriptomic analyses of the tangerine pathotype of Alternaria alternata in response to oxidative stress.

Wang Mingshuang M Sun Xuepeng X Yu Dongliang D Xu Jianping J Chung Kuangren K Li Hongye H

Scientific reports 20160901

The tangerine pathotype of Alternaria alternata produces the A. citri toxin (ACT) and is the causal agent of citrus brown spot that results in significant yield losses worldwide. Both the production of ACT and the ability to detoxify reactive oxygen species (ROS) are required for A. alternata pathogenicity in citrus. In this study, we report the 34.41 Mb genome sequence of strain Z7 of the tangerine pathotype of A. alternata. The host selective ACT gene cluster in strain Z7 was identified, which ...[more]

PMID: 27582273

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Project description:The COP9 signalosome (CSN) is a highly conserved protein complex involved in the ubiquitin-proteasome system. Its metalloisopeptidase activity resides in subunit 5 (CSN5). Functions of csn5 in phytopathogenic fungi are poorly understood. Here, we knocked out the csn5 ortholog (Aacsn5) in the tangerine pathotype of Alternaria alternata. The ?Aacsn5 mutant showed a moderately reduced growth rate compared to the wildtype strain and was unable to produce conidia. The growth of ?Aacsn5 mutant was not affected in response to oxidative and osmotic stresses. Virulence assays revealed that ?Aacsn5 induced no or significantly reduced necrotic lesions on detached citrus leaves. The defects in hyphal growth, conidial sporulation, and pathogenicity of ?Aacsn5 were restored by genetic complementation of the mutant with wildtype Aacsn5. To explore the molecular mechanisms of conidiation and pathogenesis underlying Aacsn5 regulation, we systematically examined the transcriptomes of both ?Aacsn5 and the wildtype. Generally, 881 genes were overexpressed and 777 were underexpressed in the ?Aacsn5 mutant during conidiation while 694 overexpressed and 993 underexpressed during infection. During asexual development, genes related to the transport processes and nitrogen metabolism were significantly downregulated; the expression of csn1-4 and csn7 in ?Aacsn5 was significantly elevated; secondary metabolism gene clusters were broadly affected; especially, the transcript level of the whole of cluster 28 and 30 was strongly induced. During infection, the expression of the host-specific ACT toxin gene cluster which controls the biosynthesis of the citrus specific toxin was significantly repressed; many other SM clusters with unknown products were also regulated; 86 out of 373 carbohydrate-active enzymes responsible for breaking down the plant dead tissues showed uniquely decreased expression. Taken together, our results expand our understanding of the roles of csn5 on conidiation and pathogenicity in plant pathogenic fungi and provide a foundation for future investigations.

Project description:The fungal nicotinamide adenine dinucleotide phosphate (NADPH) oxidase (Nox) complex, which has been implicated in the production of low-level reactive oxygen species (ROS), contains mainly NoxA, NoxB (gp91(phox) homologues) and NoxR (p67(phox) homologue). Here, we report the developmental and pathological functions of NoxB and NoxR in the tangerine pathotype of Alternaria alternata. Loss-of-function genetics revealed that all three Nox components are required for the accumulation of cellular hydrogen peroxide (H₂O₂). Alternaria alternata strains lacking NoxA, NoxB or NoxR also displayed an increased sensitivity to H₂O₂ and many ROS-generating oxidants. These phenotypes are highly similar to those previously seen for the Δyap1 mutant lacking a YAP1 transcriptional regulator and for the Δhog1 mutant lacking a HOG1 mitogen-activated protein (MAP) kinase, implicating a possible link among them. A fungal strain carrying a NoxA NoxB or NoxA NoxR double mutation was more sensitive to the test compounds than the strain mutated at a single gene, implicating a synergistic function among Nox components. The ΔnoxB mutant strain failed to produce any conidia; both ΔnoxA and ΔnoxR mutant strains showed a severe reduction in sporulation. Mutant strains carrying defective NoxB had higher chitin content than the wild-type and were insensitive to calcofluor white, Congo red and the fungicides vinclozolin and fludioxonil. Virulence assays revealed that all three Nox components are required for the elaboration of the penetration process. The inability to penetrate the citrus host, observed for Δnox mutants, could be overcome by wounding and by reacquiring a dominant Nox gene. The A. alternata NoxR did not influence the expression of NoxB, but negatively regulated NoxA. Importantly, the expression of both YAP1 and HOG1 genes, whose products are involved in resistance to ROS, was down-regulated in fungi carrying defective NoxA, NoxB or NoxR. Our results highlight the requirement of Nox in ROS resistance and provide insights into its critical role in regulating both YAP1 and HOG1 in A. alternata.

Project description:Alternaria blotch disease of apple (Malus × domestica Borkh.), caused by the apple pathotype of Alternaria alternata, is one of the most serious fungal diseases to affect apples. To develop an understanding of how apples respond to A. alternata apple pathotype (AAAP) infection, we examined the host transcript accumulation over the period between 0 and 72 h post AAAP inoculation. Large-scale gene expression analysis was conducted of the compatible interaction between "Starking Delicious" apple cultivar and AAAP using RNA-Seq and digital gene expression (DGE) profiling methods. Our results show that a total of 9080 differentially expressed genes (DEGs) were detected (>two-fold and FDR < 0.001) by RNA-Seq. During the early phase of infection, 12 h post inoculation (HPI), AAAP exhibited limited fungal development and little change in the transcript accumulation status (950 DEGs). During the intermediate phase of infection, the period between 18 and 36 HPI, increased fungal development, active infection, and increased transcript accumulation were detected (4111 and 3838 DEGs detected at each time point, respectively). The majority of DEGs were detected by 72 HPI, suggesting that this is an important time point in the response of apples' AAAP infection. Subsequent gene ontology (GO) and pathway enrichment analyses showed that DEGs are predominately involved in biological processes and metabolic pathways; results showed that almost gene associated with photosynthesis, oxidation-reduction were down-regulated, while transcription factors (i.e., WRKY, MYB, NAC, and Hsf) and DEGs involved in cell wall modification, defense signaling, the synthesis of defense-related metabolites, including pathogenesis-related (PRs) genes and phenylpropanoid/cyanoamino acid /flavonoid biosynthesis, were activated during this process. Our study also suggested that the cell wall defensive vulnerability and the down-regulation of most PRs and HSP70s in "Starking Delicious" following AAAP infection might interpret its susceptible to AAAP.

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Genomic and transcriptomic analyses of the tangerine pathotype of Alternaria alternata in response to oxidative stress.

Publications

Genomic and transcriptomic analyses of the tangerine pathotype of Alternaria alternata in response to oxidative stress.

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