The root-knot nematode effector Mi2G02 hijacks a host plant trihelix transcription factor to promote nematode parasitism

Zhao, Jianlong; Huang, Kaiwei; Liu, Rui; Lai, Yuqing; Abad, Pierre; Favery, Bruno; Jian, Heng; Ling, Jian; Li, Yan; Yang, Yuhong; Xie, Bingyan; Quentin, Michaël; Mao, Zhenchuan

doi:10.1016/j.xplc.2023.100723

Cited by 4 publications

(2 citation statements)

References 75 publications

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“…Co‐IPs were performed with BeyoMag anti‐HA Magnetic Beads (Beyotime), and the eluted proteins were identified by western blotting with anti‐GFP (Beyotime) and anti‐HA (Beyotime) antibodies as described by Zhao et al. ( 2023 ).…”

Section: Methodsmentioning

confidence: 99%

The root‐knot nematode effector MiEFF12 targets the host ER quality control system to suppress immune responses and allow parasitism

Soulé,

Huang,

Mulet

et al. 2024

Molecular Plant Pathology

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Root‐knot nematodes (RKNs) are microscopic parasitic worms able to infest the roots of thousands of plant species, causing massive crop yield losses worldwide. They evade the plant's immune system and manipulate plant cell physiology and metabolism to transform a few root cells into giant cells, which serve as feeding sites for the nematode. RKN parasitism is facilitated by the secretion in planta of effector molecules, mostly proteins that hijack host cellular processes. We describe here a conserved RKN‐specific effector, effector 12 (EFF12), that is synthesized exclusively in the oesophageal glands of the nematode, and we demonstrate its function in parasitism. In the plant, MiEFF12 localizes to the endoplasmic reticulum (ER). A combination of RNA‐sequencing analysis and immunity‐suppression bioassays revealed the contribution of MiEFF12 to the modulation of host immunity. Yeast two‐hybrid, split luciferase and co‐immunoprecipitation approaches identified an essential component of the ER quality control system, the Solanum lycopersicum plant bap‐like (PBL), and basic leucine zipper 60 (BZIP60) proteins as host targets of MiEFF12. Finally, silencing the PBL genes in Nicotiana benthamiana decreased susceptibility to Meloidogyne incognita infection. Our results suggest that EFF12 manipulates PBL function to modify plant immune responses to allow parasitism.

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Section: Methodsmentioning

confidence: 99%

The root‐knot nematode effector MiEFF12 targets the host ER quality control system to suppress immune responses and allow parasitism

Soulé,

Huang,

Mulet

et al. 2024

Molecular Plant Pathology

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“…Total RNA was extracted each time, and RT-qPCR was performed on a Bio-Rad CFX96 (Bio-Rad, Hercules, CA, USA) real-time PCR system (all primers are shown in Supplementary Table S4) using the following amplification program: 95 • C for 5 min and 40 cycles of 95 • C for 30 s and 60 • C for 30 s. Data were processed using the 2 −∆∆CT method [31]. The gene encoding glyceraldehyde-3-phosphate dehydrogenase (GAPDH) of M. incognita (Minc12412) was used as an internal control for the normalization of RT-qPCR data, as previously described [32]. At least three biological experiments with three technical replicates for each reaction were performed.…”

Section: Reverse Transcription Quantitative Real-time Pcr (Rt-qpcr)mentioning

confidence: 99%

NRPS-like ATRR in Plant-Parasitic Nematodes Involved in Glycine Betaine Metabolism to Promote Parasitism

Zhang,

Li,

Ling

et al. 2024

IJMS

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Plant-parasitic nematodes (PPNs) are among the most serious phytopathogens and cause widespread and serious damage in major crops. In this study, using a genome mining method, we identified nonribosomal peptide synthetase (NRPS)-like enzymes in genomes of plant-parasitic nematodes, which are conserved with two consecutive reducing domains at the N-terminus (A-T-R1-R2) and homologous to fungal NRPS-like ATRR. We experimentally investigated the roles of the NRPS-like enzyme (MiATRR) in nematode (Meloidogyne incognita) parasitism. Heterologous expression of Miatrr in Saccharomyces cerevisiae can overcome the growth inhibition caused by high concentrations of glycine betaine. RT-qPCR detection shows that Miatrr is significantly upregulated at the early parasitic life stage (J2s in plants) of M. incognita. Host-derived Miatrr RNA interference (RNAi) in Arabidopsis thaliana can significantly decrease the number of galls and egg masses of M. incognita, as well as retard development and reduce the body size of the nematode. Although exogenous glycine betaine and choline have no obvious impact on the survival of free-living M. incognita J2s (pre-parasitic J2s), they impact the performance of the nematode in planta, especially in Miatrr-RNAi plants. Following application of exogenous glycine betaine and choline in the rhizosphere soil of A. thaliana, the numbers of galls and egg masses were obviously reduced by glycine betaine but increased by choline. Based on the knowledge about the function of fungal NRPS-like ATRR and the roles of glycine betaine in host plants and nematodes, we suggest that MiATRR is involved in nematode–plant interaction by acting as a glycine betaine reductase, converting glycine betaine to choline. This may be a universal strategy in plant-parasitic nematodes utilizing NRPS-like ATRR to promote their parasitism on host plants.

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Silencing CsMAP65-2 and CsMAP65-3 in cucumber reduces susceptibility to Meloidogyne incognita

Liang,

Ji,

et al. 2025

Plant Physiology and Biochemistry

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The root-knot nematode effector Mi2G02 hijacks a host plant trihelix transcription factor to promote nematode parasitism

Cited by 4 publications

References 75 publications

The root‐knot nematode effector MiEFF12 targets the host ER quality control system to suppress immune responses and allow parasitism

The root‐knot nematode effector MiEFF12 targets the host ER quality control system to suppress immune responses and allow parasitism

NRPS-like ATRR in Plant-Parasitic Nematodes Involved in Glycine Betaine Metabolism to Promote Parasitism

Silencing CsMAP65-2 and CsMAP65-3 in cucumber reduces susceptibility to Meloidogyne incognita

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