Unknown,Transcriptomics,Genomics,Proteomics

Dataset Information

Transcriptome and Metabolite Profiling of the Infection Cycle of Zymoseptoria tritici on Wheat Reveals a Biphasic Interaction with Plant Immunity Involving Differential Pathogen Chromosomal Contributions and a Variation on the Hemibiotrophic Lifestyle Definition.

ABSTRACT: The hemibiotrophic fungus Zymoseptoria tritici causes Septoria tritici blotch disease of wheat (Triticum aestivum). Pathogen reproduction on wheat occurs without cell penetration, suggesting that dynamic and intimate intercellular communication occurs between fungus and plant throughout the disease cycle. We used deep RNA sequencing and metabolomics to investigate the physiology of plant and pathogen throughout an asexual reproductive cycle of Z. tritici on wheat leaves. Over 3,000 pathogen genes, more than 7,000 wheat genes, and more than 300 metabolites were differentially regulated. Intriguingly, individual fungal chromosomes contributed unequally to the overall gene expression changes. Early transcriptional down-regulation of putative host defense genes was detected in inoculated leaves. There was little evidence for fungal nutrient acquisition from the plant throughout symptomless colonization by Z. tritici, which may instead be utilizing lipid and fatty acid stores for growth. However, the fungus then subsequently manipulated specific plant carbohydrates, including fructan metabolites, during the switch to necrotrophic growth and reproduction. This switch coincided with increased expression of jasmonic acid biosynthesis genes and large-scale activation of other plant defense responses. Fungal genes encoding putative secondary metabolite clusters and secreted effector proteins were identified with distinct infection phase-specific expression patterns, although functional analysis suggested that many have overlapping/redundant functions in virulence. The pathogenic lifestyle of Z. tritici on wheat revealed through this study, involving initial defense suppression by a slow-growing extracellular and nutritionally limited pathogen followed by defense (hyper) activation during reproduction, reveals a subtle modification of the conceptual definition of hemibiotrophic plant infection.

INSTRUMENT(S): Illumina HiSeq 2000

ORGANISM(S): Triticum aestivum

SUBMITTER: Keywan Hassani-Pak

PROVIDER: E-MTAB-4116 | biostudies-arrayexpress |

REPOSITORIES: biostudies-arrayexpress

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Publications

Transcriptome and metabolite profiling of the infection cycle of Zymoseptoria tritici on wheat reveals a biphasic interaction with plant immunity involving differential pathogen chromosomal contributions and a variation on the hemibiotrophic lifestyle definition.

Rudd Jason J JJ Kanyuka Kostya K Hassani-Pak Keywan K Derbyshire Mark M Andongabo Ambrose A Devonshire Jean J Lysenko Artem A Saqi Mansoor M Desai Nalini M NM Powers Stephen J SJ Hooper Juliet J Ambroso Linda L Bharti Arvind A Farmer Andrew A Hammond-Kosack Kim E KE Dietrich Robert A RA Courbot Mikael M

Plant physiology 20150116 3

The hemibiotrophic fungus Zymoseptoria tritici causes Septoria tritici blotch disease of wheat (Triticum aestivum). Pathogen reproduction on wheat occurs without cell penetration, suggesting that dynamic and intimate intercellular communication occurs between fungus and plant throughout the disease cycle. We used deep RNA sequencing and metabolomics to investigate the physiology of plant and pathogen throughout an asexual reproductive cycle of Z. tritici on wheat leaves. Over 3,000 pathogen gene ...[more]

PMID: 25596183

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Project description:Rhamnolipids (RLs), glycolipids biosynthesized by the Pseudomonas and Burkholderia genera, are known to display various activities against a wide range of pathogens. Most previous studies on RLs focused on their direct antimicrobial activity, while only a few reports described the mechanisms by which RLs induce resistance against phytopathogens and the related fitness cost on plant physiology. Here, we combined transcriptomic and metabolomic approaches to unravel the mechanisms underlying RL-induced resistance in wheat against the hemibiotrophic fungus Zymoseptoria tritici, a major pathogen of this crop. Investigations were carried out by treating wheat plants with a bioinspired synthetic mono-RL with a 12-carbon fatty acid tail, dodecanoyl α/β-L-rhamnopyranoside (Rh-Est-C12), under both infectious and non-infectious conditions to examine its potential wheat defense-eliciting and priming bioactivities. Whereas, Rh-Est-C12 conferred to wheat a significant protection against Z. tritici (41% disease severity reduction), only a slight effect of this RL on wheat leaf gene expression and metabolite accumulation was observed. A subset of 24 differentially expressed genes (DEGs) and 11 differentially accumulated metabolites (DAMs) was scored in elicitation modalities 2, 5 and 15 days post-treatment (dpt), and 25 DEGs and 17 DAMs were recorded in priming modalities 5 and 15 dpt. Most changes were down-regulations, and only a few DEGs and DAMs associated with resistance to pathogens were identified. Nevertheless, a transient early regulation in gene expression was highlighted at 2 dpt (e.g., genes involved in signaling, transcription, translation, cell-wall structure and function), suggesting a perception of the RL by the plant upon treatment. Further in vitro and in planta bioassays showed that Rh-Est-C12 displays a significant direct antimicrobial activity toward Z. tritici. Taken together, our results suggest that Rh-Est-C12 confers protection to wheat against Z. tritici through direct antifungal activity and, to a lesser extent, by induction of plant defenses without causing major alterations in plant metabolism. This study provides new insights into the modes of action of RLs on the wheat-Z. tritici pathosystem and highlights the potential interest in Rh-Est-C12, a low-fitness cost molecule, to control this pathogen.

Dataset Information

Transcriptome and Metabolite Profiling of the Infection Cycle of Zymoseptoria tritici on Wheat Reveals a Biphasic Interaction with Plant Immunity Involving Differential Pathogen Chromosomal Contributions and a Variation on the Hemibiotrophic Lifestyle Definition.

Publications

Transcriptome and metabolite profiling of the infection cycle of Zymoseptoria tritici on wheat reveals a biphasic interaction with plant immunity involving differential pathogen chromosomal contributions and a variation on the hemibiotrophic lifestyle definition.

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