Directing Trophic Divergence in Plant-Pathogen Interactions: Antagonistic Phytohormones With NO Doubt?

Abstract

A fundamental process culminating in the mechanisms of plant-pathogen interactions is the regulation of trophic divergence into biotrophic, hemibiotrophic, and necrotrophic interactions. Plant hormones, of almost all types, play significant roles in this regulatory apparatus. In plant-pathogen interactions, two classical mechanisms underlying hormone-dependent trophic divergence are long recognized. While salicylic acid dominates in the execution of host defense response against biotrophic and early-stage hemibiotrophic pathogens, jasmonic acid, and ethylene are key players facilitating host defense response against necrotrophic and later-stage hemibiotrophic pathogens. Evidence increasingly suggests that trophic divergence appears to be modulated by more complex signaling networks. Acting antagonistically or agonistically, other hormones such as auxins, cytokinins, abscisic acid, gibberellins, brassinosteroids, and strigolactones, as well as nitric oxide, are emerging candidates in the regulation of trophic divergence. In this review, the latest advances in the dynamic regulation of trophic divergence are summarized, emphasizing common and contrasting hormonal and nitric oxide signaling strategies deployed in plant-pathogen interactions.

Keywords: biotrophs; hemibiotrophs; hormones; necrotrophs; nitric oxide; plant-pathogen interactions; trophic divergence.

FIGURE 1

Hormone crosstalk in directing biotrophic, hemibiotrophic, and necrotrophic interactions. During trophic divergence, SA orchestrates both biotrophic and hemibiotrophic interactions, while JA/ET orchestrates both necrotrophic and hemibiotrophic interactions. By interacting with SA, JA/ET, and other hormones, auxin, CK, ABA, GA, BR, and SL as well as their important biosynthesis, transport and response genes, receptors, regulatory components, and transcription factors are all involved in directing trophic divergence, and their crosstalk are widely diversified across these three trophic interactions. Red upward triangle arrows are used to indicate positive regulators for host immunity, and blue downward triangle arrows for negative regulators for host immunity in each specific trophic interaction. Black triangle arrows are denoted for positive regulations in the pathway, while black round arrows for negative regulations in the pathway. Question marks designate potential regulations that require further investigations. Trophic divergence by different hormones are separated by horizontal dotted lines, while different regulatory modules within a trophic interaction are separated by vertical dotted lines.