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Sugarcane smut: shedding light on the development of the whip-shaped sorus.

ABSTRACT: Sugarcane smut is caused by the fungus Sporisorium scitamineum (Ustilaginales/Ustilaginomycotina/Basidiomycota), which is responsible for losses in sugarcane production worldwide. Infected plants show a profound metabolic modification resulting in the development of a whip-shaped structure (sorus) composed of a mixture of plant tissues and fungal hyphae. Within this structure, ustilospores develop and disseminate the disease. Despite the importance of this disease, a detailed histopathological analysis of the plant-pathogen interaction is lacking.The whip-shaped sorus was investigated using light microscopy, scanning and transmission electron microscopy, histochemical tests and epifluorescence microscopy coupled with deconvolution.Sorus growth is mediated by intercalary meristem activity at the base of the sorus, where the fungus causes partial host cell wall degradation and formation of intercellular spaces. Sporogenesis in S. scitamineum is thallic, with ustilospore initials in intercalary or terminal positions, and mostly restricted to the base of the sorus. Ustilospore maturation is centrifugal in relation to the ground parenchyma and occurs throughout the sorus median region. At the apex of the sorus, the fungus produces sterile cells and promotes host cell detachment. Hyphae are present throughout the central axis of the sorus (columella). The plant cell produces callose around the intracellular hyphae as well as inside the papillae at the infection site.The ontogeny of the whip-shaped sorus suggests that the fungus can cause the acropetal growth in the intercalary meristem. The sporogenesis of S. scitamineum was described in detail, demonstrating that the spores are formed exclusively at the base of the whip. Light was also shed on the nature of the sterile cells. The presence of the fungus alters the host cell wall composition, promotes its degradation and causes the release of some peripheral cells of the sorus. Finally, callose was observed around fungal hyphae in infected cells, suggesting that deposition of callose by the host may act as a structural response to fungal infection.

SUBMITTER: Marques JPR

PROVIDER: S-EPMC5378185 | biostudies-literature | 2017 Mar

REPOSITORIES: biostudies-literature

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Sugarcane smut: shedding light on the development of the whip-shaped sorus.

Marques João Paulo R JPR Appezzato-da-Glória Beatriz B Piepenbring Meike M Massola Nelson S NS Monteiro-Vitorello Claudia B CB Vieira Maria Lucia Carneiro MLC

Annals of botany 20170301 5

<h4>Background and aims</h4>Sugarcane smut is caused by the fungus Sporisorium scitamineum (Ustilaginales/Ustilaginomycotina/Basidiomycota), which is responsible for losses in sugarcane production worldwide. Infected plants show a profound metabolic modification resulting in the development of a whip-shaped structure (sorus) composed of a mixture of plant tissues and fungal hyphae. Within this structure, ustilospores develop and disseminate the disease. Despite the importance of this disease, a ...[more]

PMID: 27568298

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Project description:Sugarcane smut caused by Sporisorium scitamineum is a severe, global sugarcane disease with severe economic losses and is difficult to prevent. To explore more effective control techniques for smut, the effects and physiological mechanism of silicon (Si) on smut resistance in two smut-susceptible cultivars, ROC22 and Badila, were investigated. The results show that Si application significantly enhances smut resistance in ROC22 and Badila, and the incidence of sugarcane smut decreased by 11.57-22.58% (ROC22) and 27.75-46.67% (Badila). The incidence of smut is negatively correlated with the amount of Si applied and the Si content in sugarcane leaves, stems, and roots (highly significantly negatively correlated with stem Si content). Under S. scitamineum stress, the activities of pathogenesis-related enzymes, chitinase and β-1,3-glucanase, secondary metabolism-related enzymes such as polyphenoloxidase (PPO) and phenylalanine-ammonia-lyase (PAL), and the contents of secondary metabolites, total soluble phenol, and lignin in sugarcane leaves treated with Si were significantly higher than those without Si (CK). The results also demonstrated that the content of malondialdehyde (MDA) and hydrogen peroxide (H2O2), the superoxide dismutase (SOD) activity of sugarcane leaves treated with Si increased in the seedling and tillering stages, and the peroxidase (POD) activity decreased in the seedling stage, which caused the accumulation of reactive oxygen species (ROS) that in turn triggered defense responses. Moreover, MDA and H2O2 levels decreased, and the activities of SOD and POD increased at the jointing stage, which was beneficial to the removal of excessive ROS. Collectively, these results suggest that Si modulates pathogenesis-related protein activity, secondary metabolism, and active oxygen metabolism of sugarcane that positively regulate resistance to smut. This study is the first to reveal the physiological mechanism of Si in improving smut resistance in sugarcane, and the results provide a theoretical basis for the development of Si fertilizers to control sugarcane smut.

Project description:BackgroundSugarcane smut caused by Sporisorium scitamineum is one of the most severe fungal diseases in the sugarcane industry. Using a molecular biological technique to mine sugarcane resistance genes can provide gene resources for further genetic engineering of sugarcane disease-resistant breeding. Jasmonate ZIM (zinc-finger inflorescence meristem) domain (JAZ) proteins, which involved in the responses to plant pathogens and abiotic stresses, are important signaling molecules of the jasmonic acid (JA) pathway.ResultsSeven differentially expressed sugarcane JAZ genes, ScJAZ1-ScJAZ7, were mined from the transcriptome of sugarcane after inoculation with S. scitamineum. Bioinformatic analyses revealed that these seven ScJAZ genes encoded basic proteins that contain the TIFY and CCT_2 domains. Quantitative reverse transcription polymerase chain reaction (qRT-PCR) analysis demonstrated that the ScJAZ1-ScJAZ7 genes were tissue specific and differentially expressed under adverse stress. During S. scitamineum infection, the transcripts of ScJAZ4 and ScJAZ5 were both upregulated in the susceptible genotype ROC22 and the resistant genotype Yacheng05-179; ScJAZ1, ScJAZ2, ScJAZ3, and ScJAZ7 were downregulated in Yacheng05-179 and upregulated in ROC22; and the expression of ScJAZ6 did not change in ROC22, but was upregulated in Yacheng05-179. The transcripts of the seven ScJAZ genes were increased by the stimuli of salicylic acid and abscisic acid, particularly methyl jasmonate. The expression of the genes ScJAZ1-ScJAZ7 was immediately upregulated by the stressors hydrogen peroxide, sodium chloride, and copper chloride, whereas slightly induced after treatment with calcium chloride and polyethylene glycol. In addition, the expression of ScJAZ6, as well as seven tobacco immunity-associated marker genes were upregulated, and antimicrobial activity against Pseudomonas solanacearum and Fusarium solani var. coeruleum was observed during the transient overexpression of ScJAZ6 in Nicotiana benthamiana, suggesting that the ScJAZ6 gene is associated with plant immunity.ConclusionsThe different expression profiles of the ScJAZ1-ScJAZ7 genes during S. scitamineum infection, the positive response of ScJAZ1-ScJAZ7 to hormones and abiotic treatments, and the function analysis of the ScJAZ6 gene revealed their involvement in the defense against biotic and abiotic stresses. The findings of the present study facilitate further research on the ScJAZ gene family especially their regulatory mechanism in sugarcane.

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.

Dataset Information

Sugarcane smut: shedding light on the development of the whip-shaped sorus.

Publications

Sugarcane smut: shedding light on the development of the whip-shaped sorus.

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