Sugarcane Cell Wall-Associated Defense Responses to Infection by Sporisorium scitamineum.
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ABSTRACT:
SUBMITTER: Marques JPR
PROVIDER: S-EPMC5974332 | biostudies-literature | 2018
REPOSITORIES: biostudies-literature
Publications
Sugarcane Cell Wall-Associated Defense Responses to Infection by <i>Sporisorium scitamineum</i>.
Marques João P R JPR Hoy Jeffrey W JW Appezzato-da-Glória Beatriz B Viveros Andrés F G AFG Vieira Maria L C MLC Baisakh Niranjan N
Frontiers in plant science 20180523
The plant cell wall is known to be the first barrier against plant pathogens. Detailed information about sugarcane cell wall-associated defense responses to infection by the causal agent of smut, <i>Sporisorium scitamineum</i>, is scarce. Herein, (immuno)histochemical analysis of two smut resistant and two susceptible sugarcane cultivars was conducted to understand host cell wall structural and compositional modifications in response to fungal infection. Results showed that the fungus grew on th ...[more]
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Project description:Smut disease is caused by Sporisorium scitamineum, an important sugarcane fungal pathogen causing an extensive loss in yield and sugar quality. The available literature suggests that there are two types of smut resistance mechanisms: external resistance by physical or chemical barriers and intrinsic internal resistance mechanisms operating at host⁻pathogen interaction at cellular and molecular levels. The nature of smut resistance mechanisms, however, remains largely unknown. The present study investigated the changes in proteome occurring in two sugarcane varieties with contrasting susceptibility to smut-F134 and NCo310-at whip development stage after S. scitamineum infection. Total proteins from pathogen inoculated and uninoculated (control) leaves were separated by two-dimensional gel electrophoresis (2D-PAGE). Protein identification was performed using BLASTp and tBLASTn against NCBI nonredundant protein databases and EST databases, respectively. A total of thirty proteins spots representing differentially expressed proteins (DEPs), 16 from F134 and 14 from NCo310, were identified and analyzed by MALDI-TOF/TOF MS. In F134, 4 DEPs were upregulated and nine were downregulated, while, nine were upregulated and three were downregulated in NCo310. The DEPs were associated with DNA binding, metabolic processes, defense, stress response, photorespiration, protein refolding, chloroplast, nucleus and plasma membrane. Finally, the expression of CAT, SOD, and PAL with recognized roles in S. scitamineum infection in both sugarcane verities were analyzed by real-time quantitative PCR (RT-qPCR) technique. Identification of genes critical for smut resistance in sugarcane will increase our knowledge of S. scitamineum-sugarcane interaction and help to develop molecular and conventional breeding strategies for variety improvement.
| S-EPMC6387155 | biostudies-other
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.
| S-EPMC5993111 | biostudies-literature
Project description:Sporisorium scitamineum is a biotrophic fungus responsible for the sugarcane smut, a worldwide spread disease. This study provides the complete sequence of individual chromosomes of S. scitamineum from telomere to telomere achieved by a combination of PacBio long reads and Illumina short reads sequence data, as well as a draft sequence of a second fungal strain. Comparative analysis to previous available sequences of another strain detected few polymorphisms among the three genomes. The novel complete sequence described herein allowed us to identify and annotate extended subtelomeric regions, repetitive elements and the mitochondrial DNA sequence. The genome comprises 19,979,571 bases, 6,677 genes encoding proteins, 111 tRNAs and 3 assembled copies of rDNA, out of our estimated number of copies as 130. Chromosomal reorganizations were detected when comparing to sequences of S. reilianum, the closest smut relative, potentially influenced by repeats of transposable elements. Repetitive elements may have also directed the linkage of the two mating-type loci. The fungal transcriptome profiling from in vitro and from interaction with sugarcane at two time points (early infection and whip emergence) revealed that 13.5% of the genes were differentially expressed in planta and particular to each developmental stage. Among them are plant cell wall degrading enzymes, proteases, lipases, chitin modification and lignin degradation enzymes, sugar transporters and transcriptional factors. The fungus also modulates transcription of genes related to surviving against reactive oxygen species and other toxic metabolites produced by the plant. Previously described effectors in smut/plant interactions were detected but some new candidates are proposed. Ten genomic islands harboring some of the candidate genes unique to S. scitamineum were expressed only in planta. RNAseq data was also used to reassure gene predictions.
| S-EPMC4466345 | biostudies-literature
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.
| S-EPMC5062822 | biostudies-literature
Project description:BackgroundSugarcane smut caused by Sporisorium scitamineum leads to a significant reduction in cane yield and sucrose content. MicroRNAs (miRNAs) play an important role in regulating plant responses to biotic stress. The present study was the first to use two sugarcane genotypes, YA05-179 (smut-resistant) and ROC22 (smut-susceptible), to identify differentially expressed miRNAs in sugarcane challenged with S. scitamineum by using high-throughput sequencing.ResultsThe predicted target gene number corresponding to known differentially expressed miRNAs in YA05-179 was less than that in ROC22, however most of them were in common. Expression of differential miRNAs under S. scitamineum challenge was mostly downregulated, with similar trends in the two varieties. Gene ontology (GO) analysis showed that the target gene classification of known miRNAs was similar to that of the newly identified miRNAs. These were mainly associated with cellular processes and metabolic processes in the biological process category, as well as combination and catalytic activity in the molecular function category. Kyoto Encyclopedia of Genes and Genomes (KEGG) pathway enrichment analysis revealed that these predicted target genes involved in a series of physiological and biochemical pathways or disease resistance-related physiological metabolism and signal transduction pathways, suggesting that the molecular interaction mechanism between sugarcane and S. scitamineum was a complex network system. These findings also showed certain predicted target genes of miR5671, miR5054, miR5783, miR5221, and miR6478 play roles in the mitogen-activated protein kinase (MAPK) signaling pathway, plant hormone signal transduction, and plant-pathogen interaction. Quantitative real-time PCR (qRT-PCR) analysis showed that majority of the known miRNAs and its predicted target genes followed a negatively regulated mode. Seven out of eight predicted target genes showed identical expression after 12 h treatment and reached the highest degree of matching at 48 h, indicating that the regulatory role of miRNAs on the target genes in sugarcane was maximized at 48 h after S. scitamineum challenge.ConclusionsTaken together, our findings serve as evidence for the association of miRNA expression with the molecular mechanism underlying the pathogenesis of sugarcane smut, particularly on the significance of miRNA levels in relation to the cultivation of smut-resistant sugarcane varieties.
| S-EPMC5404671 | biostudies-literature
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.
| S-EPMC4246466 | biostudies-literature
Project description:The basidiomycetous fungus Sporisorium scitamineum causes a serious sugarcane smut disease in major sugarcane growing areas. Sexual mating is essential for infection to the host; however, its underlying molecular mechanism has not been fully studied. In this study, we identified a conserved farnesyltransferase (FTase) β subunit Ram1 in S. scitamineum. The ram1Δ mutant displayed significantly reduced mating/filamentation, thus of weak pathogenicity to the host cane. The ram1Δ mutant sporidia showed more tolerant toward cell wall stressor Congo red compared to that of the wild-type. Transcriptional profiling showed that Congo red treatment resulted in notable up-regulation of the core genes involving in cell wall integrity pathway in ram1Δ sporidia compared with that of WT, indicating that Ram1 may be involved in cell wall integrity regulation. In yeast the heterodimeric FTase is responsible for post-translational modification of Ras (small G protein) and a-factor (pheromone). We also identified and characterized two conserved Ras proteins, Ras1 and Ras2, respectively, and a MAT-1 pheromone precursor Mfa1. The ras1Δ, ras2Δ and mfa1Δ mutants all displayed reduced mating/filamentation similar as the ram1Δ mutant. However, both ras1Δ and ras2Δ mutants were hypersensitive to Congo red while the mfa1Δ mutant was the same as wild-type. Overall our study displayed that RAM1 plays an essential role in S. scitamineum mating/filamentation, pathogenicity, and cell wall stability.
| S-EPMC6517510 | biostudies-literature
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.
| S-EPMC4149577 | biostudies-literature
Project description:Sporisorium scitamineum is a fungal smut pathogen epidemic in sugarcane producing areas. Early detection and proper identification of the smut are an essential requirement in its management practice. In this study, we developed a TaqMan real-time PCR assay using specific primers (bEQ-F/bEQ-R) and a TaqMan probe (bEQ-P) which were designed based on the bE (b East mating type) gene (Genbank Accession no. U61290.1). This method was more sensitive (a detection limit of 10 ag pbE DNA and 0.8 ng sugarcane genomic DNA) than that of conventional PCR (10 fg and 100 ng, resp.). Reliability was demonstrated through the positive detection of samples collected from artificially inoculated sugarcane plantlets (FN40). This assay was capable of detecting the smut pathogen at the initial stage (12 h) of infection and suitable for inspection of sugarcane pathogen-free seed cane and seedlings. Furthermore, quantification of pathogen was verified in pathogen-challenged buds in different sugarcane genotypes, which suggested its feasibility for evaluation of smut resistance in different sugarcane genotypes. Taken together, this novel assay can be used as a diagnostic tool for sensitive, accurate, fast, and quantitative detection of the smut pathogen especially for asymptomatic seed cane or plants and evaluation of smut resistance of sugarcane genotypes.
| S-EPMC3819024 | biostudies-literature
Project description:Sugarcane smut is the most damaging disease that is present almost across the globe, causing mild to severe yield losses depending upon the cultivar types, pathogen races and climatic conditions. Cultivation of smut-resistant cultivars is the most feasible and economical option to mitigate its damages. Previous investigations revealed that there is a scarcity of information on early detection and effective strategies to suppress etiological agents of smut disease due to the characteristics overlapping within species complexes. In this study, 104 sugarcane cultivars were screened by artificial inoculation with homogenate of all possible pathogen races of Sporisorium scitamineum during two consecutive growing seasons. The logistic smut growth pattern and the disease intrinsic rate were recorded by disease growth curve. Variable levels of disease incidence i.e., ranging from 0 to 54.10% were observed among these sugarcane cultivars. Besides, pathogen DNA in plant shoots of all the cultivars was successfully amplified by PCR method using smut-specific primers except 26 cultivars which showed an immune reaction in the field trial. Furthermore, the plant germination and tillering of susceptible sugarcane cultivars were greatly influenced by pathogen inoculation. In susceptible cultivars, S. scitamineum caused a significant reduction in setts germination, coupled with profuse tillering, resulting in fewer millable canes. Correlation analysis demonstrated that there was a positive relationship between reduction in setts germination and increase in the number of tillers. The present study would be helpful for the evaluation of smut resistance in a wide range of sugarcane germplasm, especially from the aspects of setts germination and tillers formation, and it also screened out several excellent germplasm for potential application in sugarcane breeding.
| S-EPMC11199591 | biostudies-literature