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Genome analysis of the foxtail millet pathogen Sclerospora graminicola reveals the complex effector repertoire of graminicolous downy mildews.

ABSTRACT: Downy mildew, caused by the oomycete pathogen Sclerospora graminicola, is an economically important disease of Gramineae crops including foxtail millet (Setaria italica). Plants infected with S. graminicola are generally stunted and often undergo a transformation of flower organs into leaves (phyllody or witches' broom), resulting in serious yield loss. To establish the molecular basis of downy mildew disease in foxtail millet, we carried out whole-genome sequencing and an RNA-seq analysis of S. graminicola.Sequence reads were generated from S. graminicola using an Illumina sequencing platform and assembled de novo into a draft genome sequence comprising approximately 360 Mbp. Of this sequence, 73% comprised repetitive elements, and a total of 16,736 genes were predicted from the RNA-seq data. The predicted genes included those encoding effector-like proteins with high sequence similarity to those previously identified in other oomycete pathogens. Genes encoding jacalin-like lectin-domain-containing secreted proteins were enriched in S. graminicola compared to other oomycetes. Of a total of 1220 genes encoding putative secreted proteins, 91 significantly changed their expression levels during the infection of plant tissues compared to the sporangia and zoospore stages of the S. graminicola lifecycle.We established the draft genome sequence of a downy mildew pathogen that infects Gramineae plants. Based on this sequence and our transcriptome analysis, we generated a catalog of in planta-induced candidate effector genes, providing a solid foundation from which to identify the effectors causing phyllody.

SUBMITTER: Kobayashi M

PROVIDER: S-EPMC5700566 | biostudies-literature | 2017 Nov

REPOSITORIES: biostudies-literature

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Genome analysis of the foxtail millet pathogen Sclerospora graminicola reveals the complex effector repertoire of graminicolous downy mildews.

Kobayashi Michie M Hiraka Yukie Y Abe Akira A Yaegashi Hiroki H Natsume Satoshi S Kikuchi Hideko H Takagi Hiroki H Saitoh Hiromasa H Win Joe J Kamoun Sophien S Terauchi Ryohei R

BMC genomics 20171122 1

<h4>Background</h4>Downy mildew, caused by the oomycete pathogen Sclerospora graminicola, is an economically important disease of Gramineae crops including foxtail millet (Setaria italica). Plants infected with S. graminicola are generally stunted and often undergo a transformation of flower organs into leaves (phyllody or witches' broom), resulting in serious yield loss. To establish the molecular basis of downy mildew disease in foxtail millet, we carried out whole-genome sequencing and an RNA ...[more]

PMID: 29166857

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Project description:Downy mildew of foxtail millet is an important oomycete disease caused by Sclerospora graminicola, affecting the yield and quality of the crop. Foxtail millet infected with S. graminicola exhibit symptoms of leaf yellowing and leaf cracking. To uncover the pathogenic mechanism of this disease, we explored the effects on chlorophyll synthesis and photosynthesis of foxtail millet leaves infected by S. graminicola. An elite foxtail millet variety, JG21, susceptible to S. graminicola, was used as for this study. S. graminicola inhibited chlorophyll synthesis and caused loose mesophyll cell arrangement. In addition, some cells were severely vacuolated in S. graminicola-infected foxtail millet leaves at the early stages of infection. S. graminicola could invade the mesophyll cells through haustoria which destroyed the chloroplast structure at the middle stages of infection causing significant accumulation of osmiophilic particles (OPs) and disintegrated chloroplast grana lamellae. Furthermore, foxtail millet leaves split longitudinally at the later stages of infection. Chlorophyll and carotenoid contents in infected leaves decreased significantly compared with those in the control. Net photosynthetic rate (Pn) of leaves and stomatal conductance showed a downward trend, and intercellular carbon dioxide concentrations increased significantly following the infection with S. graminicola. A total of 1,618 differentially expressed genes (DEGs) were detected between the control group and the treatment groups using RNA sequencing (RNA-Seq) among S1-S5 stages. DEGs associated with "photosynthesis" and "light reaction" were enriched. Gene expression patterns showed that 91.3% of 23 genes related to chlorophyll synthesis and photosynthesis, were significantly down-regulated than the control during S1-S5 stages. Based on the gene expression dataset, weighed gene co-expression network analysis (WGCNA) with 19 gene co-expression modules related to photosynthesis revealed six hub genes related to chlorophyll synthesis, which were suppressed during infection. The results suggest that infection of S. graminicola led to weak chlorophyll synthesis and rapid chloroplasts disappearance in foxtail millet. The defense responses and resistance of foxtail millet to S. graminicola were inhibited because chloroplast structure and function were destroyed in leaves, and the sexual reproduction in S. graminicola could be completed rapidly.

Dataset Information

Genome analysis of the foxtail millet pathogen Sclerospora graminicola reveals the complex effector repertoire of graminicolous downy mildews.

Publications

Genome analysis of the foxtail millet pathogen Sclerospora graminicola reveals the complex effector repertoire of graminicolous downy mildews.

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