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Phoma medicaginis stimulates the induction of the octadecanoid and phenylpropanoid pathways in Medicago truncatula.

ABSTRACT: Gene expression changes and metabolite abundances were measured during the interaction of Medicago truncatula with the fungal necrotrophic pathogen Phoma medicaginis in leaf tissue of susceptible and resistant accessions. Over 330 genes were differentially expressed in plants infected with P. medicaginis relative to mock-inoculated plants at 12 h post-inoculation. Of these, 191 were induced in either the resistant or the susceptible accession, with 143 genes repressed. Expression changes were observed in genes involved in the oxidative burst, cell wall strengthening and lipid metabolism, as well as several transcription factors. Genes related to salicylic acid, jasmonate and ethylene responses were up-regulated, as well as genes leading to the production of jasmonic acid. Significant induction of genes in the phenylpropanoid pathway leading to lignin and isoflavonoid biosynthesis occurred. High-pressure liquid chromatography with UV detection (HPLC-UV) identified several phenolic compounds induced by P. medicaginis, as well as constitutively higher levels of phenolic compounds, in the resistant M. truncatula accession. Differentially regulated genes induced in both the resistant and susceptible accessions, but with different kinetics, and constitutively more highly expressed and induced phenolic compounds provide candidates for functional analysis. Taken together, these results highlight the importance of the octadecanoid and phenylpropanoid pathways in defence against this necrotrophic pathogen.

SUBMITTER: Kamphuis LG

PROVIDER: S-EPMC6638703 | biostudies-literature | 2012 Aug

REPOSITORIES: biostudies-literature

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Phoma medicaginis stimulates the induction of the octadecanoid and phenylpropanoid pathways in Medicago truncatula.

Kamphuis Lars G LG Williams Angela H AH Küster Helge H Trengove Robert D RD Singh Karam B KB Oliver Richard P RP Ellwood Simon R SR

Molecular plant pathology 20120103 6

Gene expression changes and metabolite abundances were measured during the interaction of Medicago truncatula with the fungal necrotrophic pathogen Phoma medicaginis in leaf tissue of susceptible and resistant accessions. Over 330 genes were differentially expressed in plants infected with P. medicaginis relative to mock-inoculated plants at 12 h post-inoculation. Of these, 191 were induced in either the resistant or the susceptible accession, with 143 genes repressed. Expression changes were ob ...[more]

PMID: 22212347

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Project description:Information on disease process and pathogenicity mechanisms is important for understanding plant disease. Spring black stem and leaf spot caused by the necrotrophic pathogen Phoma medicaginis var. medicaginis Malbr. & Roum causes large losses to alfalfa. However, till now, little is known about alfalfa-P. medicagnis interactions and the pathogenicity mechanisms of the pathogen. Here, alfalfa inoculated with P. medicaginis was subjected to GC-MS based metabolic profiling. The metabolic response in P. medicaginis-inoculated and mock-inoculated alfalfa leaves was assessed at 2, 4, 6, 8, 12, 16, 20, 24, 26 and 28 days post inoculation. In total, 101 peaks were detected in the control and inoculated groups, from which 70 metabolites were tentatively identified. Using multivariate analysis, 16 significantly regulated compounds, including amino acids, nitrogen-containing compounds and organic acids, polyols, fatty acids, and sugars were tentatively identified (Variable importance values, VIP>1.0 and p <0.05). Among these metabolites, the levels of malate, 5-oxoproline, palmitic acid and stearic acid were increased significantly in P. medicaginis-infected alfalfa leaves compared to the controls. In contrast, the levels ofγ-aminobutyric acid and 2-pyrrolidinone were significantly decreased in infected leaves compared to the controls. Further metabolic pathway analysis of the 16 significantly regulated compounds demonstrated that glycolysis, the tricarboxylic acid cycle, and β-oxidation of fatty acids were significantly induced in the alfalfa leaves at later stages of P. medicaginis infection. The strong induction of tricarboxylic acid cycle pathways at later infection stages caused by the pathogen may induce senescence in the alfalfa leaves, leading to plant death. However, intermediate metabolites of these metabolic pathways, and inositol phosphate, glutathione, the metabolic pathways of some amino acids accumulated rapidly and strongly at early stages of infection, which may enhance the ability of alfalfa to resist necrotrophic P. medicaginis disease. Understanding metabolic pathways is essential for understanding pathogenesis.

Project description:BackgroundPathogenic members of the Fusarium oxysporum species complex are responsible for vascular wilt disease on many important crops including legumes, where they can be one of the most destructive disease causing necrotrophic fungi. We previously developed a model legume-infecting pathosystem based on the reference legume Medicago truncatula and a pathogenic F. oxysporum forma specialis (f. sp.) medicaginis (Fom). To dissect the molecular pathogenicity arsenal used by this root-infecting pathogen, we sequenced its transcriptome during infection of a susceptible and resistant host accession.ResultsHigh coverage RNA-Seq of Fom infected root samples harvested from susceptible (DZA315) or resistant (A17) M. truncatula seedlings at early or later stages of infection (2 or 7 days post infection (dpi)) and from vegetative (in vitro) samples facilitated the identification of unique and overlapping sets of in planta differentially expressed genes. This included enrichment, particularly in DZA315 in planta up-regulated datasets, for proteins associated with sugar, protein and plant cell wall metabolism, membrane transport, nutrient uptake and oxidative processes. Genes encoding effector-like proteins were identified, including homologues of the F. oxysporum f. sp. lycopersici Secreted In Xylem (SIX) proteins, and several novel candidate effectors based on predicted secretion, small protein size and high in-planta induced expression. The majority of the effector candidates contain no known protein domains but do share high similarity to predicted proteins predominantly from other F. oxysporum ff. spp. as well as other Fusaria (F. solani, F. fujikori, F. verticilloides, F. graminearum and F. pseudograminearum), and from another wilt pathogen of the same class, a Verticillium species. Overall, this suggests these novel effector candidates may play important roles in Fusaria and wilt pathogen virulence.ConclusionCombining high coverage in planta RNA-Seq with knowledge of fungal pathogenicity protein features facilitated the identification of differentially expressed pathogenicity associated genes and novel effector candidates expressed during infection of a resistant or susceptible M. truncatula host. The knowledge from this first in depth in planta transcriptome sequencing of any F. oxysporum ff. spp. pathogenic on legumes will facilitate the dissection of Fusarium wilt pathogenicity mechanisms on many important legume crops.

Project description:BACKGROUND: Small RNAs (sRNAs) are 20-24 nucleotide (nt) RNAs and are involved in plant development and response to abiotic stresses. Plants have several sRNA pathways implicated in the transcriptional and post-transcriptional silencing of gene expression. Two key enzyme families common to all pathways are the Dicer-like (DCL) proteins involved in sRNAs maturation and the Argonautes (AGOs) involved in the targeting and functional action of sRNAs. Post-transcriptional silencing mediated by AGOs may occur by cleavage or translational repression of target mRNA's, while transcriptional silencing may be controlled by DNA methylation and chromatin remodeling. Thus far, these gene families have not been characterized in legumes, nor has their involvement in adaptation to water deficit been studied. RESULTS: A bioinformatic search in Medicago truncatula genome databases, using Arabidopsis thaliana AGO and DCL cDNA and protein sequences, identified three sequences encoding for putative Dicer-like genes and twelve sequences encoding for putative Argonaute genes. Under water deficit conditions and mainly in roots, MtDCL1 and MtAGO1, two enzymes probably involved in the processing and activation of microRNAs (miRNAs), increased their transcript levels. mir162 which target DCL1 mRNA and mir168 which target AGO1 mRNA reduced their expression in the roots of plants subjected to water deficit. Three putative genes, MtDCL3, MtAGO4b and MtAGO4c probably involved in DNA methylation mechanisms, increased their mRNA levels. However, the mRNA levels of MtAGO6 reduced, which probably encodes a protein with functions similar to MtAGO4. MtAGO7 mRNA levels increased and possibly encodes a protein involved in the production of trans-acting small interfering RNAs. The transcript abundance of MtAGO12a, MtAGO12b and MtAGO12c reduced under water deprivation. Plants recovered from water deprivation reacquire the mRNA levels of the controls. CONCLUSIONS: Our work demonstrates that in M. truncatula the transcript accumulation of the components of small RNA pathways is being modulated under water deficit. This shows that the transcriptional and post-transcriptional control of gene expression mediated by sRNAs is probably involved in plant adaptation to abiotic environmental changes. In the future this will allow the manipulation of these pathways providing a more efficient response of legumes towards water shortage.

Dataset Information

Phoma medicaginis stimulates the induction of the octadecanoid and phenylpropanoid pathways in Medicago truncatula.

Publications

Phoma medicaginis stimulates the induction of the octadecanoid and phenylpropanoid pathways in Medicago truncatula.

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