Local auxin synthesis mediated by YUCCA4 induced during root-knot nematode infection positively regulates gall growth and nematode development

Abstract

Parasites and pathogens are known to manipulate the host’s endogenous signaling pathways to facilitate the infection process. In particular, plant-parasitic root-knot nematodes (RKN) are known to elicit auxin response at the infection sites, to aid the development of root galls as feeding sites for the parasites. Here we describe the role of local auxin synthesis induced during RKN infection. Exogenous application of auxin synthesis inhibitors decreased RKN gall formation rates, gall size and auxin response in galls, while auxin and auxin analogues produced the opposite effects, re-enforcing the notion that auxin positively regulates RKN gall formation. Among the auxin biosynthesis enzymes, YUCCA4 (YUC4) was found to be dramatically up-regulated during RKN infection, suggesting it may be a major contributor to the auxin accumulation during gall formation. However, yuc4-1 showed only very transient decrease in gall auxin levels and did not show significant changes in RKN infection rates, implying the loss of YUC4 is likely compensated by other auxin sources. Nevertheless, yuc4-1 plants produced significantly smaller galls with fewer mature females and egg masses, confirming that auxin synthesized by YUC4 is required for proper gall formation and RKN development within. Interestingly, YUC4 promoter was also activated during cyst nematode infection. These lines of evidence imply auxin biosynthesis from multiple sources, one of them being YUC4, is induced upon plant endoparasitic nematode invasion and likely contribute to their infections. The coordination of these different auxins adds another layer of complexity of hormonal regulations during plant parasitic nematode interaction.

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

“…The de novo formation of new organs, such as lateral roots, rhizobium-induced nodules, or nematode-induced galls, from one or a few root cells requires the recruitment of similar developmental programs ( Yamaguchi et al., 2017 ; Soyano et al., 2019 ; Olmo et al., 2020 ). Several genes, including ABERRANT LATERAL ROOT FORMATION 4 ( ALF4 ), a RIBULOSE-PHOSPHATE 3-EPIMERASE ( RPE ), and YUCCA4 ( YUC4 ), have been reported to have functions associated with lateral root initiation and/or development, and their expression is regulated in nematode-induced galls; they have also been shown to be required for normal feeding-site formation and nematode development ( Favery et al., 1998 ; Olmo et al., 2019 ; Suzuki et al., 2022 ). These genes include cell-cycle genes and TF genes, such as LBD16 and PUCHI , that play key roles in controlling lateral root initiation and morphogenesis ( Torres-Martínez et al., 2019 ); they are induced following nematode infection and are required for feeding-site development and successful RKN parasitism ( Cabrera et al, 2014b ; Suzuki et al., 2021 ).…”

A Major Role of Class III HD-ZIPs in Promoting Sugar Beet Cyst Nematode Syncytium Formation inArabidopsis

“…At the early stage of infection, perturbations to auxin homeostasis are key to syncytium establishment. A local accumulation of auxin is pivotal for syncytium initiation and is associated with changes in auxin biosynthesis, polar transport, and signaling (Grunewald et al, 2009; Lee et al, 2011; Habash et al, 2017; Oosterbeek et al, 2021; Suzuki et al, 2022). Several CN effectors have been identified to directly modulate auxin accumulation and signaling at the infection site.…”

“…Host genes related to auxin biosynthesis, distribution, and signaling are also modulated by CN at the infection site. YUCCA4 ( YUC4 ), encoding a member of YUCCA family enzymes that mediates a speed limiting step in the main auxin biosynthesis pathway, is up-regulated at the CN infection site, along with a few other auxin biosynthesis enzymes (Guarneri et al, 2022; Suzuki et al, 2022). Auxin efflux PIN1 and PIN7 genes are down-regulated at the early feeding site to prevent out flow of auxin from the initial syncytial cell, while PIN3 and PIN4 proteins are re-localized to the lateral membranes of the expanding syncytium to re-distribute auxin for lateral expansion of the syncytium (Grunewald et al, 2009).…”

The regeneration conferring transcription factor complex ERF115‐PAT1 coordinates a wound‐induced response in root‐knot nematode induced galls

“…Wound sensing also involves local auxin signalling, coordinating downstream transcriptional responses at the wound vicinity (Hoermayer et al ., 2020). Auxin has as well been shown to positively regulate RKN gall onset (Suzuki et al ., 2022).…”