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Leaf rust (Puccinia recondita f. sp. secalis) triggers substantial changes in rye (Secale cereale L.) at the transcriptome and metabolome levels

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dc.abstract.enBackground Rye (Secale cereale L.) is a cereal crop highly tolerant to environmental stresses, including abiotic and biotic stresses (e.g., fungal diseases). Among these fungal diseases, leaf rust (LR) is a major threat to rye produc tion. Despite extensive research, the genetic basis of the rye immune response to LR remains unclear. Results An RNA seq analysis was conducted to examine the immune response of three unrelated rye inbred lines (D33, D39, and L318) infected with compatible and incompatible Puccinia recondita f. sp. secalis (Prs) isolates. In total, 877 unique differentially expressed genes (DEGs) were identified at 20 and 36 h post treatment (hpt). Most of the DEGs were up regulated. Two lines (D39 and L318) had more up regulated genes than down regulated genes, whereas the opposite trend was observed for line D33. The functional classification of the DEGs helped identify the largest gene groups regulated by LR. Notably, these groups included several DEGs encoding cytochrome P450, receptor like kinases, methylesterases, pathogenesis related protein 1, xyloglucan endotransglucosylases/hydrolases, and peroxidases. The metabolomic response was highly conserved among the genotypes, with line D33 displaying the most gen otype specific changes in secondary metabolites. The effect of pathogen compatibility on metabolomic changes was less than the effects of the time points and genotypes. Accordingly, the secondary metabolome of rye is altered by the recognition of the pathogen rather than by a successful infection. The results of the enrichment analysis of the DEGs and differentially accumulated metabolites (DAMs) reflected the involvement of phenylpropanoid and diterpenoid biosynthesis as well as thiamine metabolism in the rye immune response. Conclusion Our work provides novel insights into the genetic and metabolic responses of rye to LR. Numerous immune response related DEGs and DAMs were identified, thereby clarifying the mechanisms underlying the rye response to compatible and incompatible Prs isolates during the early stages of LR development. The integration of transcriptomic and metabolomic analyses elucidated the contributions of phenylpropanoid biosynthesis and fla vonoid pathways to the rye immune response to Prs. This combined analysis of omics data provides valuable insights relevant for future research conducted to enhance rye resistance to LR.
dc.affiliationWydział Rolnictwa, Ogrodnictwa i Biotechnologii
dc.affiliation.instituteKatedra Metod Matematycznych i Statystycznych
dc.contributor.authorKrępski, T.
dc.contributor.authorPiasecka, A.
dc.contributor.authorŚwięcicka, M.
dc.contributor.authorKańczurzewska, M.
dc.contributor.authorSawikowska, Aneta
dc.contributor.authorDmochowska-Boguta, M.
dc.contributor.authorRakoczy-Trojanowska, M.
dc.contributor.authorMatuszkiewicz, M.
dc.date.access2024-12-09
dc.date.accessioned2024-12-09T07:30:04Z
dc.date.available2024-12-09T07:30:04Z
dc.date.copyright2024-02-13
dc.date.issued2024
dc.description.abstract<jats:title>Abstract</jats:title><jats:sec> <jats:title>Background</jats:title> <jats:p>Rye (<jats:italic>Secale cereale</jats:italic> L.) is a cereal crop highly tolerant to environmental stresses, including abiotic and biotic stresses (e.g., fungal diseases). Among these fungal diseases, leaf rust (LR) is a major threat to rye production. Despite extensive research, the genetic basis of the rye immune response to LR remains unclear. </jats:p> </jats:sec><jats:sec> <jats:title>Results</jats:title> <jats:p>An RNA-seq analysis was conducted to examine the immune response of three unrelated rye inbred lines (D33, D39, and L318) infected with compatible and incompatible <jats:italic>Puccinia recondita</jats:italic> f. sp. <jats:italic>secalis</jats:italic> (<jats:italic>Prs</jats:italic>) isolates. In total, 877 unique differentially expressed genes (DEGs) were identified at 20 and 36 h post-treatment (hpt). Most of the DEGs were up-regulated. Two lines (D39 and L318) had more up-regulated genes than down-regulated genes, whereas the opposite trend was observed for line D33. The functional classification of the DEGs helped identify the largest gene groups regulated by LR. Notably, these groups included several DEGs encoding cytochrome P450, receptor-like kinases, methylesterases, pathogenesis-related protein-1, xyloglucan endotransglucosylases/hydrolases, and peroxidases. </jats:p> <jats:p>The metabolomic response was highly conserved among the genotypes, with line D33 displaying the most genotype-specific changes in secondary metabolites. The effect of pathogen compatibility on metabolomic changes was less than the effects of the time-points and genotypes. Accordingly, the secondary metabolome of rye is altered by the recognition of the pathogen rather than by a successful infection. The results of the enrichment analysis of the DEGs and differentially accumulated metabolites (DAMs) reflected the involvement of phenylpropanoid and diterpenoid biosynthesis as well as thiamine metabolism in the rye immune response. </jats:p> </jats:sec><jats:sec> <jats:title>Conclusion</jats:title> <jats:p>Our work provides novel insights into the genetic and metabolic responses of rye to LR. Numerous immune response-related DEGs and DAMs were identified, thereby clarifying the mechanisms underlying the rye response to compatible and incompatible <jats:italic>Prs</jats:italic> isolates during the early stages of LR development. The integration of transcriptomic and metabolomic analyses elucidated the contributions of phenylpropanoid biosynthesis and flavonoid pathways to the rye immune response to <jats:italic>Prs</jats:italic>. This combined analysis of omics data provides valuable insights relevant for future research conducted to enhance rye resistance to LR.</jats:p> </jats:sec>
dc.description.accesstimeat_publication
dc.description.bibliographyil., bibliogr.
dc.description.financepublication_nocost
dc.description.financecost0,00
dc.description.if4,3
dc.description.points140
dc.description.versionfinal_published
dc.description.volume24
dc.identifier.doi10.1186/s12870-024-04726-0
dc.identifier.issn1471-2229
dc.identifier.urihttps://sciencerep.up.poznan.pl/handle/item/2177
dc.identifier.weblinkhttps://bmcplantbiol.biomedcentral.com/articles/10.1186/s12870-024-04726-0
dc.languageen
dc.relation.ispartofBMC Plant Biology
dc.relation.pagesart. 107
dc.rightsCC-BY
dc.sciencecloudsend
dc.share.typeOPEN_JOURNAL
dc.subject.enbiotic stress
dc.subject.enfungal disease
dc.subject.enplant immune response
dc.subject.enRNA‑seq
dc.subject.endifferentially accumulated metabolites
dc.titleLeaf rust (Puccinia recondita f. sp. secalis) triggers substantial changes in rye (Secale cereale L.) at the transcriptome and metabolome levels
dc.typeJournalArticle
dspace.entity.typePublication
oaire.citation.issue1
oaire.citation.volume24