Gall-Inducing Parasites: Convergent and Conserved Strategies of Plant Manipulation by Insects and Nematodes

Favery, Bruno; Dubreuil, Géraldine; Chen, Ming‐Shun; Giron, David; Abad, Pierre

doi:10.1146/annurev-phyto-010820-012722

Cited by 51 publications

(42 citation statements)

References 147 publications

(191 reference statements)

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“…Similarly, Heterodera schachtii has been shown to activate the NADPH oxidases RbohD and RbohF to produce ROS, restricting infected plant cell death and promoting feeding cell formation in Arabidopsis (Siddique et al ., 2014). Ontogenesis of the RKN‐induced feeding site implies manipulation of multiple host signalling pathways to allow root to differentiate into highly metabolic, hypertrophied, and polynucleate feeding GCs, the proliferation of neighbouring cells, and de novo formation of a network of vascular tissues around the GCs (Bartlem et al ., 2014; Rodiuc et al ., 2014; Favery et al ., 2020). In addition to its function in the plant responses to biotic and abiotic stress, H 2 O 2 is indeed an important molecule transducing internal signals required for plant growth and development, in particular by interfering with hormonal signalling pathways and with the activity of target proteins such as receptor kinases and transcription factors (Černý et al ., 2018; Smirnoff & Arnaud, 2019).…”

Section: Discussionmentioning

confidence: 99%

A Meloidogyne incognita C‐type lectin effector targets plant catalases to promote parasitism

et al. 2021

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Summary Root‐knot nematodes, Meloidogyne spp., secrete effectors to modulate plant immune responses and establish a parasitic relationship with host plants. However, the functions and plant targets of C‐type lectin (CTL)‐like effectors of Meloidogyne incognita remain unknown. Here, we characterized a CTL‐like effector of M. incognita, MiCTL1a, and identified its target and role in nematode parasitism. In situ hybridization demonstrated the expression of MiCTL1 in the subventral glands; and in planta, immunolocalization showed its secretion during M. incognita parasitism. Virus‐induced gene silencing of the MiCTL1 reduced the infection ability of M. incognita in Nicotiana benthamiana. The ectopic expression in Arabidopsis not only increased susceptibility to M. incognita but also promoted root growth. Yeast two‐hybrid and co‐immunoprecipitation assays revealed that MiCTL1a interacts with Arabidopsis catalases, which play essential roles in hydrogen peroxide homeostasis. Knockout or overexpression of catalases showed either increased or reduced susceptibility to M. incognita, respectively. Moreover, MiCTL1a not only reduced catalase activity in vitro and in planta but also modulated stress‐related gene expressions in Arabidopsis. Our data suggest that MiCTL1a interacts with plant catalases and interferes with catalase activity, allowing M. incognita to establish a parasitic relationship with its host by fine‐tuning responses mediated by reactive oxygen species.

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Section: Discussionmentioning

confidence: 99%

A Meloidogyne incognita C‐type lectin effector targets plant catalases to promote parasitism

et al. 2021

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“…RFS caused by Ustilaginoidea virens (teleomorph: Villosiclava virens ), is a devastating grain disease in main rice planting areas worldwide, especially in China, India and Southeast Asia [ 1 , 2 ]. The occurrence of RFS can cause both serious yield loss and grain contamination by cyclopeptide mycotoxins [ 3 , 4 ].…”

Section: Introductionmentioning

confidence: 99%

A novel transcription factor UvCGBP1 regulates development and virulence of rice false smut fungus Ustilaginoidea virens

Líu

Chen

et al. 2021

Virulence

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Ustilaginoidea virens , causing rice false smut (RFS) is an economically important ascomycetous fungal pathogen distributed in rice-growing regions worldwide. Here, we identified a novel transcription factor UvCGBP1 ( C utinase G -box b inding p rotein) from this fungus, which is unique to ascomycetes. Deletion of UvCGBP1 affected development and virulence of U. virens . A total of 865 downstream target genes of UvCGBP1 was identified using ChIP-seq and the most significant KEGG enriched functional pathway was the MAPK signaling pathway. Approximately 36% of target genes contain the AGGGG (G-box) motif in their promoter. Among the targets, deletion of UvCGBP1 affected transcriptional and translational levels of UvPmk1 and UvSlt2 , both of which were important in virulence. ChIP-qPCR, yeast one-hybrid and EMSA confirmed that UvCGBP1 can bind the promoter of UvPmk1 or UvSlt2 . Overexpression of UvPmk1 in the ∆UvCGBP1-33 mutant restored partially its virulence and hyphae growth, indicating that UvCGBP1 could function via the MAPK pathway to regulate fungal virulence. Taken together, this study uncovered a novel regulatory mechanism of fungal virulence linking the MAPK pathway mediated by a G-box binding transcription factor, UvCGBP1.

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“…The effectors involved in giant cells neo-organogenesis and functioning may target different subcellular compartments and cellular host functions. Indeed, transcriptomic studies of the plant response to RKN infection have revealed that RKN can hijack several key host cellular processes, such as the cell cycle, phytohormone signaling, intercellular transport, and metabolism to favor parasitism (Caillaud et al, 2008;Gheysen and Mitchum, 2019;Favery et al, 2020).…”

Section: Introductionmentioning

confidence: 99%

The Meloidogyne incognita Nuclear Effector MiEFF1 Interacts With Arabidopsis Cytosolic Glyceraldehyde-3-Phosphate Dehydrogenases to Promote Parasitism

et al. 2021

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Root-knot nematodes are obligate endoparasites that maintain a biotrophic relationship with their hosts over a period of several weeks. They induce the differentiation of root cells into specialized multinucleate hypertrophied feeding cells known as giant cells. Nematode effectors synthesized in the esophageal glands and injected into the plant tissue through the syringe-like stylet play a key role in giant cell ontogenesis. The Meloidogyne incognita MiEFF1 is one of the rare effectors of phytopathogenic nematodes to have been located in vivo in feeding cells. This effector specifically targets the giant cell nuclei. We investigated the Arabidopsis functions modulated by this effector, by using a yeast two-hybrid approach to identify its host targets. We characterized a universal stress protein (USP) and cytosolic glyceraldehyde-3-phosphate dehydrogenases (GAPCs) as the targets of MiEFF1. We validated the interaction of MiEFF1 with these host targets in the plant cell nucleus, by bimolecular fluorescence complementation (BiFC). A functional analysis with Arabidopsis GUS reporter lines and knockout mutant lines showed that GAPCs were induced in giant cells and that their non-metabolic functions were required for root-knot nematode infection. These susceptibility factors are potentially interesting targets for the development of new root-knot nematode control strategies.

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Gall-Inducing Parasites: Convergent and Conserved Strategies of Plant Manipulation by Insects and Nematodes

Cited by 51 publications

References 147 publications

A Meloidogyne incognita C‐type lectin effector targets plant catalases to promote parasitism

A Meloidogyne incognita C‐type lectin effector targets plant catalases to promote parasitism

A novel transcription factor UvCGBP1 regulates development and virulence of rice false smut fungus Ustilaginoidea virens

The Meloidogyne incognita Nuclear Effector MiEFF1 Interacts With Arabidopsis Cytosolic Glyceraldehyde-3-Phosphate Dehydrogenases to Promote Parasitism

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