Phylogeny and Expression of NADPH Oxidases during Symbiotic Nodule Formation

Jesús Montiel,Carmen Quinto,Citlali Fonseca-García

doi:10.3390/agriculture8110179

Abstract

The mutualistic interaction between gram-negative soil bacteria and the roots of legumes leads to the establishment of nodules, where atmospheric nitrogen is fixed. Nodulation is a multistep process with numerous essential players. Among these are reactive oxygen species (ROS), which are mainly generated by Nicotinamide Adenine Dinucleotide Phosphate (NADPH) oxidases. In plants, these enzymes are known as respiratory burst oxidase homologs (RBOHs). In legumes, these proteins are encoded by a multigene family with members that are differentially expressed in various tissues and organs at distinct developmental stages. RBOHs have critical roles at several stages of nodulation: in the early signaling pathway triggered by nodulation factors in the root hairs, during both the progression of infection threads and nodule ontogeny, and in nitrogen fixation and senescence. Data from the literature along with the analysis conducted here imply that legumes use different RBOHs for different stages of nodulation; these RBOHs belong to the same phylogenetic subgroup, even though they are not strictly orthologous. Accordingly, the regulation of activity of a given RBOH during the nodulation process probably varies among legumes.

Highlights

The symbiotic association of legumes with gram-negative soil bacteria results in the formation of nodules, unique structures in which the bacteria fix atmospheric nitrogen
respiratory burst oxidase homologs (RBOHs) have been shown to function throughout the nodulation process in several legumes that
RBOHs have been shown to function throughout the nodulation process in several legumes that develop indeterminate and determinate nodules

Summary

Introduction

The symbiotic association of legumes with gram-negative soil bacteria results in the formation of nodules, unique structures in which the bacteria fix atmospheric nitrogen. The Rboh genes encompass a large family, the members of which are differentially expressed in different tissues and organs at distinct developmental phases [5,9,10,11]. These enzymes have important roles at various stages of nodulation, such as in the signaling pathway triggered by Nod factors in the root hairs, in the advancement of the infection thread, in nodule ontogeny, in nitrogen fixation, and in senescence of the nodules. We analyzed the role of Rboh genes in nodulation, focusing on their patterns of expression and their phylogenetic relationships in legumes, based on available genome sequences

ROS in the Early Signaling Pathway

RBOHs Modulate Infection Thread Growth and Nodule Organogenesis

Phylogenetic Distribution and Expression of Rboh Genes of Legumes in Nodules

Conclusions