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Comparative proteomics reveals that central metabolism changes are associated with resistance against Sporisorium scitamineum in sugarcane.

ABSTRACT: Sugarcane 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.We 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.These 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.

SUBMITTER: Su Y

PROVIDER: S-EPMC5062822 | biostudies-literature | 2016 Oct

REPOSITORIES: biostudies-literature

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Comparative proteomics reveals that central metabolism changes are associated with resistance against Sporisorium scitamineum in sugarcane.

Su Yachun Y Xu Liping L Wang Zhuqing Z Peng Qiong Q Yang Yuting Y Chen Yun Y Que Youxiong Y

BMC genomics 20161012 1

<h4>Background</h4>Sugarcane 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 i ...[more]

PMID: 27733120

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Project description:Smut caused by biotrophic fungus Sporisorium scitamineum is a major disease of cultivated sugarcane that can cause considerable yield losses. It has been suggested in literature that there are at least two types of resistance mechanisms in sugarcane plants: an external resistance, due to chemical or physical barriers in the sugarcane bud, and an internal resistance governed by the interaction of plant and fungus within the plant tissue. Detailed molecular studies interrogating these two different resistance mechanisms in sugarcane are scarce. Here, we use light microscopy and global expression profiling with RNA-seq to investigate these mechanisms in sugarcane cultivar CP74-2005, a cultivar that possibly possesses both internal and external defence mechanisms. A total of 861 differentially expressed genes (DEGs) were identified in a comparison between infected and non-infected buds at 48 hours post-inoculation (hpi), with 457 (53%) genes successfully annotated using BLAST2GO software. This includes genes involved in the phenylpropanoid pathway, cell wall biosynthesis, plant hormone signal transduction and disease resistance genes. Finally, the expression of 13 DEGs with putative roles in S. scitamineum resistance were confirmed by quantitative real-time reverse transcription PCR (qRT-PCR) analysis, and the results were consistent with the RNA-seq data. These results highlight that the early sugarcane response to S. scitamineum infection is complex and many of the disease response genes are attenuated in sugarcane cultivar CP74-2005, while others, like genes involved in the phenylpropanoid pathway, are induced. This may point to the role of the different disease resistance mechanisms that operate in cultivars such as CP74-2005, whereby the early response is dominated by external mechanisms and then as the infection progresses, the internal mechanisms are switched on. Identification of genes underlying resistance in sugarcane will increase our knowledge of the sugarcane-S. scitamineum interaction and facilitate the introgression of new resistance genes into commercial sugarcane cultivars.

Project description:BACKGROUND: Sugarcane 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. RESULTS: Here, 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. CONCLUSIONS: As 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.

Project description:Sugarcane smut caused by Sporisorium scitamineum is a critical fungal disease in the sugarcane industry. However, molecular mechanistic studies of pathological response of sugarcane to S. scitamineum are scarce and preliminary. Here, transcriptome analysis of sugarcane disease induced by S. scitamineum at 24, 48 and 120 h was conducted, using an S. scitamineum-resistant and -susceptible genotype (Yacheng05-179 and "ROC"22). The reliability of Illumina data was confirmed by real-time quantitative PCR. In total, transcriptome sequencing of eight samples revealed gene annotations of 65,852 unigenes. Correlation analysis of differentially expressed genes indicated that after S. scitamineum infection, most differentially expressed genes and related metabolic pathways in both sugarcane genotypes were common, covering most biological activities. However, expression of resistance-associated genes in Yacheng05-179 (24-48 h) occurred earlier than those in "ROC"22 (48-120 h), and more transcript expressions were observed in the former, suggesting resistance specificity and early timing of these genes in non-affinity sugarcane and S. scitamineum interactions. Obtained unigenes were related to cellular components, molecular functions and biological processes. From these data, functional annotations associated with resistance were obtained, including signal transduction mechanisms, energy production and conversion, inorganic ion transport and metabolism, and defense mechanisms. Pathway enrichment analysis revealed that differentially expressed genes are involved in plant hormone signal transduction, flavonoid biosynthesis, plant-pathogen interaction, cell wall fortification pathway and other resistance-associated metabolic pathways. Disease inoculation experiments and the validation of in vitro antibacterial activity of the chitinase gene ScChi show that this sugarcane chitinase gene identified through RNA-Seq analysis is relevant to plant-pathogen interactions. In conclusion, expression data here represent the most comprehensive dataset available for sugarcane smut induced by S. scitamineum and will serve as a resource for finally unraveling the molecular mechanisms of sugarcane responses to S. scitamineum.

Project description:Dimorphic fungi have the ability to change morphology during their lifecycle, a crucial feature for the establishment of infection and fungal growth and development in planta. Life cycle of the dimorphic sugarcane smut fungi, Sporisorium scitamineum, involves recognition and mating of compatible saprophytic yeast-like haploid sporidia (MAT-1 and MAT-2) that upon fusion, develop into infective dikaryotic mycelia. Although the dimorphic transition is intrinsically linked with the pathogenicity and virulence of S. scitamineum, it has never been studied using a proteomics approach. In the present study, an iTRAQ-based comparative proteomic analysis of three distinct stages covering the dimorphic transition period - haploid sporidial stage (MAT-1 and MAT-2) to the transition phase (24 hours post co-culturing (hpc)) and dikaryotic mycelial stage (48 hpc) was carried out. Functional categorization showed that the most altered biological processes were energy production, primary metabolism especially carbohydrate, amino acid, fatty acid, followed by translation, post-translation and protein turnover. The identified proteins could be grouped into 8 distinct clusters with different trends in abundance. Enrichment analysis of the clusters showed that biological processes related to energy production through oxidative phosphorylation, citrate cycle, and β-oxidation, transcription, translation and redox homeostasis were specifically altered. In addition, an overall downregulation of carbohydrate metabolism and reprogrammed amino acid metabolism were observed. Several differentially abundant proteins (DAPs), especially in the dikaryotic mycelial stage were predicted as effectors. Taken together, key molecular mechanisms underpinning the dimorphic transition in S. scitamineum at the proteome level were highlighted. A catalogue of stage-specific and dimorphic transition-associated -proteins and potential effectors identified herein are potential candidates for defective mutant screening to elucidate their functional role in the dimorphic transition and pathogenicity in S. scitamineum.

Project description: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 informationThe online version contains supplementary material available at 10.1007/s13205-021-02893-7.

Dataset Information

Comparative proteomics reveals that central metabolism changes are associated with resistance against Sporisorium scitamineum in sugarcane.

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Comparative proteomics reveals that central metabolism changes are associated with resistance against Sporisorium scitamineum in sugarcane.

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