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Transcriptional Changes in Potato Sprouts upon Interaction with Rhizoctonia solani Indicate Pathogen-Induced Interference in the Defence Pathways of Potato

ABSTRACT: Rhizoctonia solani is the causer of black scurf disease on potatoes and is responsible for high economical losses in global agriculture. In order to increase the limited knowledge of the plants’ molecular response to this pathogen, we inoculated potatoes with R. solani AG3-PT isolate Ben3 and carried out RNA sequencing with total RNA extracted from potato sprouts at three and eight days post inoculation (dpi). In this dual RNA-sequencing experiment, the necrotrophic lifestyle of R. solani AG3-PT during early phases of interaction with its host has already been characterised. Here the potato plants’ comprehensive transcriptional response to inoculation with R. solani AG3 was evaluated for the first time based on significantly different expressed plant genes extracted with DESeq analysis. Overall, 1640 genes were differentially expressed, comparing control (−Rs) and with R. solani AG3-PT isolate Ben3 inoculated plants (+Rs). Genes involved in the production of anti-fungal proteins and secondary metabolites with antifungal properties were significantly up regulated upon inoculation with R. solani. Gene ontology (GO) terms involved in the regulation of hormone levels (i.e., ethylene (ET) and jasmonic acid (JA) at 3 dpi and salicylic acid (SA) and JA response pathways at 8 dpi) were significantly enriched. Contrastingly, the GO term “response to abiotic stimulus” was down regulated at both time points analysed. These results may support future breeding efforts toward the development of cultivars with higher resistance level to black scurf disease or the development of new control strategies.

SUBMITTER: Zrenner R

PROVIDER: S-EPMC8002989 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Rhizoctonia solani is a soil-borne basidiomycete fungus with a necrotrophic lifestyle which is classified into fourteen reproductively incompatible anastomosis groups (AGs). One of these, AG8, is a devastating pathogen causing bare patch of cereals, brassicas and legumes. R. solani is a multinucleate heterokaryon containing significant heterozygosity within a single cell. This complexity posed significant challenges for the assembly of its genome. We present a high quality genome assembly of R. solani AG8 and a manually curated set of 13,964 genes supported by RNA-seq. The AG8 genome assembly used novel methods to produce a haploid representation of its heterokaryotic state. The whole-genomes of AG8, the rice pathogen AG1-IA and the potato pathogen AG3 were observed to be syntenic and co-linear. Genes and functions putatively relevant to pathogenicity were highlighted by comparing AG8 to known pathogenicity genes, orthology databases spanning 197 phytopathogenic taxa and AG1-IA. We also observed SNP-level "hypermutation" of CpG dinucleotides to TpG between AG8 nuclei, with similarities to repeat-induced point mutation (RIP). Interestingly, gene-coding regions were widely affected along with repetitive DNA, which has not been previously observed for RIP in mononuclear fungi of the Pezizomycotina. The rate of heterozygous SNP mutations within this single isolate of AG8 was observed to be higher than SNP mutation rates observed across populations of most fungal species compared. Comparative analyses were combined to predict biological processes relevant to AG8 and 308 proteins with effector-like characteristics, forming a valuable resource for further study of this pathosystem. Predicted effector-like proteins had elevated levels of non-synonymous point mutations relative to synonymous mutations (dN/dS), suggesting that they may be under diversifying selection pressures. In addition, the distant relationship to sequenced necrotrophs of the Ascomycota suggests the R. solani genome sequence may prove to be a useful resource in future comparative analysis of plant pathogens.

Project description:Background: Sugar beet is an important root crop, accounting for 30 % of the sugar production worldwide. The long growing season make sugar beets exposed to a range of plant pathogens for longer periods than most other crops. Here, contrasting sugar beet genotypes were used for transcriptome analysis to reveal differential responses and new defense genes to Rhizoctonia solani, a soilborn fungal pathogen. Results: After curation of primary RNA-sequencing reads, 16,768 genes deriving from 36 samples composed of two susceptible and two resistant sugar beet genotypes, three time-points (0, two and five days post inoculation), each in three replicates were subjected for analysis. Among the elevated 217 transcripts at 2 dpi, three resistance-like genes (Bv4_088600_cumk, Bv8u_204980_frqg, and Bv_44840_iifo) were activated. By employing edgeR package statistics, 660 genes were significantly different (false discovery rate < 0.05) between resistant and susceptible genotypes in their response to R. solani inoculation. A combination of eukaryotic orthologous group assignments and gene ontology enrichment analyses, revealed three Bet v I/Major latex protein homologous genes (Bv7_162510_pymu, Bv7_162520_etow, Bv_27270_xeas) in the resistant genotypes after five days of fungal challenge. Co-expression network analysis of differentially expressed sugar beet genes further identified a MYB46 transcription factor, a plant disease resistance response protein (DRR206) and a flavonoid o-methyltransferase protein. MYB46 has a key function in secondary cell wall formation and exist as a singleton in the sugar beet genome. The genome of R. solani is enriched in cell wall degrading enzyme encoding genes and it is anticipated that they represent important virulence factors. Compared to Arabidopsis thaliana, sugar beet has 2.4-fold more carbohydrate esterases and particularly large numbers (26-fold) of auxiliary activity encoding genes whose function in cell wall biosynthesis is largely unknown. Conclusions: Based on components identified in this sugar beet transcript data set we conclude that defense responses to R. solani are attributed to a wide range of gene categories but functional information is missing to a large extent. This calls for careful integration to avoid negative side effects to obtain optimal combinations of these traits in order to reach the long-term goal of improved resistance in sugar beet.

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Transcriptional Changes in Potato Sprouts upon Interaction with Rhizoctonia solani Indicate Pathogen-Induced Interference in the Defence Pathways of Potato

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