A role for ALF4 during gall and giant cell development in the biotic interaction between Arabidopsis and Meloidogyne spp.

Abstract

Root-knot nematodes (RKNs; Meloidogyne spp.) are a major pest for the agriculture worldwide. RKNs induce specialized feeding cells (giant cells, GCs) inside galls which are de novo formed pseudo-organs in the roots that share similarities with other developmental processes as lateral root (LR) and callus formation or grafting involving new vascular development or pericycle proliferation. Hence, it is pertinent to study the molecular mechanisms directing the plant-nematode interaction. In this respect, ALF4 is a key gene during LR formation, vascular vessels reconnection in grafting, hormone-induced callus formation or de novo root organogenesis from leaf explants. Our results show that ALF4 is also induced in galls at early infection stages in an auxin-independent way. Furthermore, ALF4 activity is necessary for the formation of proper galls and GCs, as the mutant alf4-1 presents aberrant galls and GCs with severe structural abnormalities leading to a dramatic reduction in the nematode egg production. However, a low-reproduction rate is maintained, that might be explained by the local auxin maximum build by the nematodes in galls, partially rescuing alf4-1 phenotype. This would be similar to the partial rescue described for LR formation with exogenous auxins and also agrees with the LR emergence from alf4-1 galls but not from uninfected roots. In addition, ALF4 is also induced in syncytia formed by cyst nematodes. All these data support a pivotal role for ALF4 during de novo organogenesis processes induced by endoparasitic nematodes, in addition to its role in LR formation, callus development or vessel reconnection during grafting.

Root‐knot nematodes induce gall formation by recruiting developmental pathways of post‐embryonic organogenesis and regeneration to promote transient pluripotency

“…How the nematode achieves these massive structural changes in the roots remains unclear. We have recently reported the formation of nematode feeding‐sites in Arabidopsis leaves, consisting of callus‐like structures containing GCs (Olmo et al , 2017a), the induction of ALF4 and also the formation of aberrant small GCs in the alf4‐1 mutant in root galls (Olmo et al , 2019). Activation of ALF4 is also necessary during LR development (DiDonato et al , 2004), for CIM‐C formation or during grafting (Sugimoto et al , 2010; Melnyk et al , 2015).…”

“…Moreover, those genes coregulated with LBD16 in GCs and galls showed a similar expression profile in those pluripotent cells of the CIM‐C (Cabrera et al , 2015). Some regenerative capacity of galls has also been described; for example, LRs/ARs develop from the galls in Col‐0 and also from mutants severely impaired in LR formation ( arf7/arf19 , slr or alf4 ), but only from the gall zone (Olmo et al , 2017a, 2019). Infected poplar roots also developed new suckers from galls (Baldacci‐Cresp et al , 2016).…”

“…Genes are characteristic of adventitious roots (in orange), root regeneration (in purple), callus‐induced media callus (CIM‐C; in red), wounding‐induced callus (WI‐C; in green) and lateral root formation (LR; in blue). Genes altered during root‐knot nematode (RKN) infection are in black bold (this paper; Cabrera et al , 2014, 2016; Kyndt et al , 2016; Yamaguchi et al , 2017; Olmo et al , 2019). In grey are those genes not yet studied or have been described as differentially expressed after RKN infection.…”

“…, 2015), is also necessary for correct gall development (Olmo et al . , 2019). These results suggested a link between RKN development, LR and callus formation.…”

Parasitic worms hijack key plant protein to build their nest

“…Researchers have been working for decades to identify the factors from both the nematodes and the host plants that contribute to this process (Sandstedt and Schuster , Bird and Saurer ). From their previous work, Olmo et al () found that the gene expression pattern during giant cell formation matches closely to the reprogramming that occurs during callus formation. The giant cells also grow an extensive network of vasculature around them to ensure the supply of nutrients; a process that resembles vasculature development following grafting.…”