Developmental Pathways Mediated by Hormones in Nematode Feeding Sites

Abstract

Abstract Sedentary plant endoparasitic (root-knot and cyst) nematodes induce the formation of their feeding sites by directing the transdifferentiation of normal plant root cells into nematode feeding cells, namely giant cells (GCs) and syncytia. In the past years, transcriptomic analyses combined with molecular cell biology have revealed dramatic and specific changes in gene expression in syncytia and GCs. Among the genes whose expression is modified to establish feeding sites are those involved in hormone-regulated developmental pathways in the roots, particularly those related to auxins and cytokinins. The high concentrations of auxins and cytokinins in galls and syncytia have been described in detail by the use of reporter genes driven by specific promoters as ‘sensors’ of both phytohormones, such as DR5 , ARR5 or TCS . Moreover, several molecular evidences link the formation of nematode feeding sites (NFSs) to developmental processes such as maintenance of the root apical meristem, lateral root initiation or vascular tissue development, in which the two hormones are involved. The mechanisms that nematodes use to interfere with plant developmental pathways are unclear, but some seem to involve nematode secreted molecules, such as the CLE -like and the CEP peptides. Only in a few cases, plant hormone transduction and developmental circuits hijacked by nematodes to induce and maintain feeding sites have been studied in detail. Analysis combining hormone genetic sensors, mutants and comparative transcriptomics lead to the identification of relevant plant regulators that are exploited for NFS differentiation. We present the current knowledge connecting the hormonal-controlled developmental processes of the root with the development of the NFS, which seem to be different for GCs and syncytia. For instance, LBD16 and WRKY23, two key transcription factors in the signal transduction leading to lateral root formation mediated by auxins, play distinctive roles during gall/GC and syncytia formation, respectively. However, the expression of either gene in the feeding site is not strictly plant auxin-dependent, indicating that their regulation by nematodes differs in some aspects from the endogenous pathways operating in normal root development. We also highlight the evidences linking gall and GC ontogeny to the pericycle and discuss the transfer cell-like identity of feeding cells.