Dataset Information

Conserved secreted effectors contribute to endophytic growth and multihost plant compatibility in a vascular wilt fungus

ABSTRACT: Fungal interactions with plant roots, either beneficial or detrimental, have a major impact on agriculture and ecosystems1. The soil inhabiting ascomycete Fusarium oxysporum (Fo) constitutes a species complex of worldwide distribution causing vascular wilt in more than a hundred different crops2,3. Individual isolates of the fungus exhibit host-specific pathogenicity, determined by proteinaceous effectors termed secreted in xylem (SIX)4,5. However, such isolates can also colonize roots of non-host plants asymptomatically as endophytes, or even protect the plant against pathogenic isolates6,7. The molecular determinants of multi-host plant colonization are currently unknown. Here, we identified a set of fungal effectors termed ERCs (Early Root Compatibility effectors), which are secreted during early biotrophic growth of Fo on both host and non-host plants. In contrast to SIX effectors, which are encoded on lineage specific (LS) genomic regions5,8, ERCs are encoded on core genomic regions and broadly conserved across the Fo species complex. Targeted deletion of ERC genes in pathogenic Fo isolate resulted in reduced virulence on the host plant and rapid activation of plant immune responses, while in a non-pathogenic isolate it led to impaired root colonization and loss of biocontrol ability. Strikingly, some ERCs also contribute to Fo infection on the non-vascular land plant Marchantia polymorpha. Our results reveal an evolutionarily conserved mechanism for multi-host colonization by root infecting fungi.

INSTRUMENT(S): LTQ Orbitrap Elite

ORGANISM(S): Fusarium Oxysporum F. Sp. Lycopersici 4287

TISSUE(S): Plant Cell, Root

SUBMITTER: Amey Redkar

LAB HEAD: Antonio Di Pietro

PROVIDER: PXD026400 | Pride | 2022-09-12

REPOSITORIES: Pride

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Dataset's files

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			Action	DRS
	Experiment_MS18-239_Amey_AFI_from_OT_181218_102_MS18-239_AFI.mzid_Experiment_MS18-239_Amey_AFI_from_OT_181218_102_MS18-239_AFI.MGF	Mzid
	Experiment_MS19-185_Amey_CFM_from_OT_190801_112_MS19-185_CFM.mzid_Experiment_MS19-185_Amey_CFM_from_OT_190801_112_MS19-185_CFM.MGF	Mzid
	Experiment_MS19-185_Amey_CFP_from_OT_190801_112_MS19-185_CFP.mzid_Experiment_MS19-185_Amey_CFP_from_OT_190801_112_MS19-185_CFP.MGF	Mzid
	Experiment__5_AFI_72_Rep2_from_OT_190208_112_MS19-023_48-AFI_5.mzid_Experiment__5_AFI_72_Rep2_from_OT_190208_112_MS19-023_48-AFI_5.MGF	Mzid
	Experiment__6_AFI_72_Rep3_from_OT_190208_112_MS19-023_48-AFI_6.mzid_Experiment__6_AFI_72_Rep3_from_OT_190208_112_MS19-023_48-AFI_6.MGF	Mzid

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Publications

Conserved secreted effectors contribute to endophytic growth and multihost plant compatibility in a vascular wilt fungus.

Redkar Amey A Sabale Mugdha M Schudoma Christian C Zechmann Bernd B Gupta Yogesh K YK López-Berges Manuel S MS Venturini Giovanni G Gimenez-Ibanez Selena S Turrà David D Solano Roberto R Di Pietro Antonio A

The Plant cell 20220801 9

Fungal interactions with plant roots, either beneficial or detrimental, have a crucial impact on agriculture and ecosystems. The cosmopolitan plant pathogen Fusarium oxysporum (Fo) provokes vascular wilts in more than a hundred different crops. Isolates of this fungus exhibit host-specific pathogenicity, which is conferred by lineage-specific Secreted In Xylem (SIX) effectors encoded on accessory genomic regions. However, such isolates also can colonize the roots of other plants asymptomatically ...[more]

PMID: 35689625

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Project description:Fusarium oxysporum is one of the most common species causing soybean root rot and seedling blight in the U.S. In a recent study, significant variation in aggressiveness was observed among isolates of F. oxysporum collected from roots in Iowa, ranging from highly pathogenic to weakly or non-pathogenic isolates. In the present work, a RNA-seq-based analysis was used for the first time to investigate the molecular aspect of the interaction of a partially resistant soybean genotype with non-pathogenic/pathogenic isolates of F. oxysporum at 72 and 96 hours post inoculation (hpi). Markedly different gene expression profiles were observed in compatible and incompatible host-pathogen combinations. A peak of differentially expressed genes (DEGs) was observed at 72 hpi in soybean roots in response to both isolates, although the number of DEGs was about eight times higher for the pathogenic isolate compared to the non-pathogenic one (1,659 vs. 203 DEGs, respectively). Furthermore, not only the number of genes, but also the magnitude of induction was much greater in response to the pathogenic isolate. This response included a stronger activation of many well-known defense-related genes, and several genes involved in ethylene biosynthesis and signalling, transcription factors, secondary and sugar metabolism. In addition, 1130 fungal genes were differentially expressed between the F. oxysporum isolates in planta during the infection process. Interestingly, 10% of these genes encode plant cell-wall degrading enzymes, reactive oxygen species-related enzymes and fungal proteins involved in primary metabolic pathways. Such information may be useful in the development of new methods of broadening resistance of soybean to F. oxysporum, including the silencing of important fungal genes, and also to understand the molecular basis of soybean-F. oxysporum interactions. Soybean seedlings mRNA profiles inoculated with a non-pathogenic and pathogenic isolates of F. oxysporum and collected at 72 and 96 hpi, were generated using Illumina HiSeq 2500. Control seedlings were also included for each time of inoculation. Three biological replicates were considered for each condition, 18 samples in total.

Project description:Background: Cell walls (CWs) are protein-rich polysaccharide matrices essential for plant growth and environmental acclimationadaptation. The CW constitutes the first physical barrier as well as a primary source of sugars for plant microbes, such as the vascular pathogen Fusarium oxysporum (Fo). Fo colonizes roots, advancing through the plant primary CWs towards the vasculature, where it grows causing devastation in many crops. The pathogenicity of Fo and other vascular microbes relies on their capacity to reach and colonize the xylem. However, little is known about the root-microbe interaction before the pathogen reaches the vasculature and the role of the plant CW during this process. Results: Using the pathosystem Arabidopsis-Fo5176, we show dynamic transcriptional changes in both fungus and root during their interaction. One of the earliest plant responses to Fo5176 was the downregulation of primary CW synthesis genes. We observed enhanced resistance to Fo5176 in Arabidopsis mutants impaired in primary CW cellulose synthesis. Previous studies showed an induction of ectopic lignification, accumulation of defense-related phytohormones, and dwarfism in primary CW cellulose synthesis deficient plants, potentially explaining their resistance to Fo5176. We confirmed that Arabidopsis roots deposit lignin in response to Fo5176 infection but we show that lignin-deficient mutants were as susceptible as wildtype plants to Fo5176. Genetic impairment of jasmonic acid biosynthesis and signaling did not alter Arabidopsis response to Fo5176, whereas impairment of ethylene signaling did increase vasculature colonization by Fo5176. AbolishingThis ethylene signaling interruption attenuated the observed resistance while maintaining the dwarfism observed in primary CW cellulose-deficient mutants. Conclusions: Our study provides significant insights on the dynamic root-vascular pathogen interaction at the transcriptome level and the vital role of primary CW cellulose during defense response to these pathogens. These findings represent an essential resource for the generation of plant resistance to Fo that can be transferred to other vascular pathosystems.