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

Abstract

Summary The establishment of root‐knot nematode (RKN; Meloidogyne spp.) induced galls in the plant host roots likely involves a wound‐induced regeneration response. Confocal imaging demonstrates physical stress or injury caused by RKN infection during parasitism in the model host Arabidopsis thaliana. The ERF115‐PAT1 heterodimeric transcription factor complex plays a recognized role in wound‐induced regeneration. ERF115 and PAT1 expression flanks injured gall cells likely driving mechanisms of wound healing, implying a local reactivation of cell division which is also hypothetically involved in gall genesis. Herein, functional investigation revealed that ectopic ERF115 expression resulted in premature induction of galls, and callus formation adjacent to the expanding female RKN was seen upon PAT1 upregulation. Smaller galls and less reproduction were observed in ERF115 and PAT1 knockouts. Investigation of components in the ERF115 network upon overexpression and knockdown by qRT‐PCR suggests it contributes to steer gall wound‐sensing and subsequent competence for tissue regeneration. High expression of CYCD6;1 was detected in galls, and WIND1 overexpression resulted in similar ERF115OE gall phenotypes, also showing faster gall induction. Along these lines, we show that the ERF115‐PAT1 complex likely coordinates stress signalling with tissue healing, keeping the gall functional until maturation and nematode reproduction.

Functional studies of plant transcription factors and their relevance in the plant root-knot nematode interaction

“…Furthermore, overexpression of ERF115 ( ERF115OE ), ERF114 , and PAT1 resulted in accelerated gall induction and downstream activation of key players in the regenerative pathway, possibly related to the high cell division rates observed, particularly in the ERF115OE line, following mechanical stress induced by RKNs. In conclusion, the ERF115-PAT1 complex contributes to the regenerative potential of nematode-induced galls by facilitating tissue healing, thereby maintaining the gall’s functionality until maturation and nematode reproduction ( Ribeiro et al., 2024 ; Table 1 ; Figure 2 ).…”

Multi‐scale mechanisms driving root regeneration: From regeneration competence to tissue repatterning

“…Indeed, while low cuts have the highest regeneration potential, they do not regenerate if there is extended damage and cell death in the stump(Durgaprasad et al, 2019). Similarly, penetration by parasitic nematodes causes extensive meristem damage triggering ERF115 expression necessary for the development of galls needed for nematode reproduction, yet does not induce regeneration(Ribeiro et al, 2023).Ó 2024 The Author(s). The Plant Journal published by Society for Experimental Biology and John Wiley & Sons Ltd., The Plant Journal, (2024), 119, 1183-1196…”