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Comparative expression analysis of potential pathogenicity-associated genes of high- and low-virulent Sporisorium scitamineum isolates during interaction with sugarcane.

ABSTRACT: Sporisorium scitamineum is a teleomorphic, biotrophic fungus causing the globally prevalent sugarcane smut disease in sugarcane. The severity of the disease depends on two major factors, viz. degree of resistance in the host genotype and virulence level of the pathogen. Hence, in this study, temporal transcriptomic expression of potential pathogenicity-associated genes of two distinctly virulent S. scitamineum isolates, viz. SsV89101 (low virulent) and Ss97009 (high virulent) were analyzed during interaction with a smut susceptible sugarcane cv. Co 97009 at six different time intervals. The pathogenicity-associated genes profiled in this study comprises 14 plant cell wall degrading enzymes (PCWDEs) and ten candidates secreted effector protein-coding (CSEPs) genes. Absolute quantification of pathogen biomass and comparative expression profiling analyses of these pathogenicity-associated genes during host-pathogen interaction indicated that there was a significant variation between low and high virulent isolates. More precisely, the higher and early expression (24 hpi) of certain PCWDEs, viz. Chitinase-1 and Laccase, and the CSEPs, viz. SUC2, SRT1 and CMU1 during the colonization of high virulent isolate suggested that they might possibly play a major role in facilitating faster and successful pathogen ingress, and tissue colonization than the less-virulent isolate. Transcript expression profiling of Chitinase and Laccases were also in correlation with their corresponding enzyme activity assays. Comprehensively, this quantitative temporal expression analysis has provided critical insights into the early expression of pathogenicity-associated genes and their putative role in attributing to higher virulence. Moreover, this study provides valuable clues for the screening of candidate virulence determinants for further functional characterization of the test pathogen isolates used for the evaluation of smut resistance in breeding clones.

Supplementary information

The online version contains supplementary material available at 10.1007/s13205-021-02893-7.

SUBMITTER: Nalayeni K

PROVIDER: S-EPMC8222464 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Sugarcane smut caused by the basidiomycetous fungus Sporisorium scitamineum is one of the most devastating diseases that affect sugarcane production, globally. At present, the most practical and effective management strategy for the disease is the cultivation of resistant cultivars. In this connection, a detailed understanding of the host's defense mechanism in response to smut isolates with varying degrees of virulence at the molecular level would facilitate the development of reliable and durable smut-resistant sugarcane varieties. Hence, in this study, a comparative whole transcriptome analysis was performed employing Illumina RNA-seq in the smut susceptible cultivar Co 97009 inoculated with two distinct S. scitamineum isolates, Ss97009 (high-virulent) and SsV89101 (low-virulent) during the early phases of infection (2 dpi and 5 dpi) and at the phase of sporogenesis (whip emergence) (60 dpi). Though the differential gene expression profiling identified significant transcriptional changes during the early phase of infection in response to both the isolates, the number of differentially expressed genes (DEGs) were more abundant at 60 dpi during interaction with the high virulent isolate Ss97009, as compared to the low virulent isolate SsV89101. Functional analysis of these DEGs revealed that a majority of them were associated with hormone signaling and the synthesis of defense-related metabolites, suggesting a complex network of defense mechanisms is being operated in response to specific isolates of the smut pathogen. For instance, up-regulation of hormone-related genes, transcription factors, and flavonoid biosynthesis pathway genes was observed in response to both the isolates in the early phase of interaction. In comparison to early phases of infection, only a few pathogenesis-related proteins were up-regulated at 60 dpi in response to Ss97009, which might have rendered the host susceptible to infection. Strikingly, few other carbohydrate metabolism-associated genes like invertases were up-regulated in Ss97009 inoculated plants during the whip emergence stage, representing a shift from sucrose storage to smut symptoms. Altogether, this study established the major switching of defense signaling pathways in response to S. scitamineum isolates with different virulence attributes and provided novel insights into the molecular mechanisms of sugarcane-smut interaction.

Project description:BackgroundSugarcane smut, which is caused by Sporisorium scitamineum, has been threatening global sugarcane production. Breeding smut resistant sugarcane varieties has been proven to be the most effective method of controlling this particular disease. However, a lack of genome information of sugarcane has hindered the development of genome-assisted resistance breeding programs. Furthermore, the molecular basis of sugarcane response to S. scitamineum infection at the proteome level was incomplete and combining proteomic and transcriptional analysis has not yet been conducted.ResultsWe identified 273 and 341 differentially expressed proteins in sugarcane smut-resistant (Yacheng05-179) and susceptible (ROC22) genotypes at 48 h after inoculation with S. scitamineum by employing an isobaric tag for relative and absolute quantification (iTRAQ). The proteome quantitative data were then validated by multiple reaction monitoring (MRM). The integrative analysis showed that the correlations between the quantitative proteins and the corresponding genes that was obtained in our previous transcriptome study were poor, which were 0.1502 and 0.2466 in Yacheng05-179 and ROC22, respectively, thereby revealing a post-transcriptional event during Yacheng05-179-S. scitamineum incompatible interaction and ROC22-S. scitamineum compatible interaction. Most differentially expressed proteins were closely related to sugarcane smut resistance such as beta-1,3-glucanase, peroxidase, pathogenesis-related protein 1 (PR1), endo-1,4-beta-xylanase, heat shock protein, and lectin. Ethylene and gibberellic acid pathways, phenylpropanoid metabolism and PRs, such as PR1, PR2, PR5 and PR14, were more active in Yacheng05-179, which suggested of their possible roles in sugarcane smut resistance. However, calcium signaling, reactive oxygen species, nitric oxide, and abscisic acid pathways in Yacheng05-179 were repressed by S. scitamineum and might not be crucial for defense against this particular pathogen.ConclusionsThese results indicated complex resistance-related events in sugarcane-S. scitamineum interaction, and provided novel insights into the molecular mechanism underlying the response of sugarcane to S. scitamineum infection.

Project description:Sporisorium scitamineum is the fungal pathogen causing severe sugarcane smut disease that leads to massive economic losses globally. S. scitamineum invades host cane by dikaryotic hyphae, formed after sexual mating of two haploid sporidia of opposite mating type. Therefore, mating/filamentation is critical for S. scitamineum pathogenicity, while its molecular mechanisms remain largely unknown. The AGC (cyclic AMP [cAMP]-dependent protein kinase 1 [protein kinase A {PKA}], cGMP-dependent protein kinase [PKG], and protein kinase C [PKC]) kinase family is a group of serine/threonine (Ser/Thr) protein kinases conserved among eukaryotic genomes, serving a variety of physiological functions, including cell growth, metabolism, differentiation, and cell death. In this study, we identified an AGC kinase, named SsAgc1 (for S. scitamineum Agc1), and characterized its function by reverse genetics. Our results showed that SsAgc1 is critical for S. scitamineum mating/filamentation and pathogenicity, and oxidative stress tolerance under some circumstances. Transcriptional profiling revealed that the SsAgc1 signaling pathway may control expression of the genes governing fungal mating/filamentation and tryptophan metabolism, especially for tryptophol production. We showed that tryptophan and tryptophol could at least partially restore ssagc1Δ mating/filamentation. Overall, our work revealed a signaling pathway mediated by AGC protein kinases to regulate fungal mating/filamentation, possibly through sensing and responding to tryptophol as signal molecules.IMPORTANCE The AGC signaling pathway represents a conserved distinct signaling pathway in regulation of fungal differentiation and virulence, while it has not been identified or characterized in the sugarcane smut fungus Sporisorium scitamineum In this study, we identified a PAS domain-containing AGC kinase, SsAgc1, in S. scitamineum Functional analysis revealed that SsAgc1 plays a regulatory role on the fungal dimorphic switch.

Project description:BackgroundSugarcane smut can cause losses in cane yield and sugar content that range from 30% to total crop failure. Losses tend to increase with the passage of years. Sporisorium scitamineum is the fungus that causes sugarcane smut. This fungus has the potential to infect all sugarcane species unless a species is resistant to biotrophic fungal pathogens. However, it remains unclear how the fungus breaks through the cell walls of sugarcane and causes the formation of black or gray whip-like structures on the sugarcane plants.ResultsHere, we report the first high-quality genome sequence of S. scitamineum assembled de novo with a contig N50 of 41 kb, a scaffold N50 of 884 kb and genome size 19.8 Mb, containing an estimated 6,636 genes. This phytopathogen can utilize a wide range of carbon and nitrogen sources. A reduced set of genes encoding plant cell wall hydrolytic enzymes leads to its biotrophic lifestyle, in which damage to the host should be minimized. As a bipolar mating fungus, a and b loci are linked and the mating-type locus segregates as a single locus. The S. scitamineum genome has only 6 G protein-coupled receptors (GPCRs) grouped into five classes, which are responsible for transducing extracellular signals into intracellular responses, however, the genome is without any PTH11-like GPCR. There are 192 virulence associated genes in the genome of S. scitamineum, among which 31 expressed in all the stages, which mainly encode for energy metabolism and redox of short-chain compound related enzymes. Sixty-eight candidates for secreted effector proteins (CSEPs) were found in the genome of S. scitamineum, and 32 of them expressed in the different stages of sugarcane infection, which are probably involved in infection and/or triggering defense responses. There are two non-ribosomal peptide synthetase (NRPS) gene clusters that are involved in the generation of ferrichrome and ferrichrome A, while the terpenes gene cluster is composed of three unknown function genes and seven biosynthesis related genes.ConclusionsAs a destructive pathogen to sugar industry, the S. scitamineum genome will facilitate future research on the genomic basis and the pathogenic mechanisms of sugarcane smut.

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Comparative expression analysis of potential pathogenicity-associated genes of high- and low-virulent Sporisorium scitamineum isolates during interaction with sugarcane.

Supplementary information

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