Evolution of NIN and NIN-like Genes in Relation to Nodule Symbiosis.

Jieyu Liu,Ton Bisseling

doi:10.3390/genes11070777

Abstract

Legumes and actinorhizal plants are capable of forming root nodules symbiosis with rhizobia and Frankia bacteria. All these nodulating species belong to the nitrogen fixation clade. Most likely, nodulation evolved once in the last common ancestor of this clade. NIN (NODULE INCEPTION) is a transcription factor that is essential for nodulation in all studied species. Therefore, it seems probable that it was recruited at the start when nodulation evolved. NIN is the founding member of the NIN-like protein (NLP) family. It arose by duplication, and this occurred before nodulation evolved. Therefore, several plant species outside the nitrogen fixation clade have NLP(s), which is orthologous to NIN. In this review, we discuss how NIN has diverged from the ancestral NLP, what minimal changes would have been essential for it to become a key transcription controlling nodulation, and which adaptations might have evolved later.

Highlights

Nitrogen-fixing root nodule-formation is a special property of some plant species
We hypothesize that, in legumes and these actinorhizal plants, a conserved module, involved in communication between the epidermis and pericycle, is active, and this was already present in the common ancestor of the nitrogen fixation clade (NFC): Nod factor signaling induces NIN expression in the epidermis; NIN activates the production of a mobile signal; this mobile signal induces NIN expression and cell division in the pericycle
In Medicago root hairs, cell wall modification genes are induced upon rhizobial infection, and the expression of many of them depends on NIN [74]

Summary

Introduction

Nitrogen-fixing root nodule-formation is a special property of some plant species. All these species belong to the nitrogen fixation clade (NFC), which is composed of four orders: Fabales, Rosales, Cucurbitales and Fagales [1]. NIN most likely plays a role in infection of the actinorhizal plant, as it has been shown to be required for Frankia-induced root hair deformation in Casuarina glauca (Casuarina) [11]. This suggests that the role of NIN in infection thread formation is conserved in both legumes and actinorhizal plants. In Medicago, it has been shown that a mutation in NOOT1 causes a homeotic switch in the formation of the nodule vasculature, as it becomes actinorhizal-like since it is formed from pericycle cells that remain mitotically active [7,21]. We will discuss possible evolutionary events underlying the recruitment of NIN in nodule symbiosis, based on comparing the NIN and NLPs of legumes, actinorhizal-like plants and non-nodulating species

Phylogenetic Analysis of NIN

Evolutionary Adaptations in the NIN Promoter to Serve in Nodule Formation

Function of NIN

Are NIN and NLPs Functionally Equivalent?

Concluding Remarks