Cross-Regulation between N Metabolism and Nitric Oxide (NO) Signaling during Plant Immunity.

Elise Thalineau,Hoai-Nam Truong,Carine Fournier,Alexandre Boscari,David Wendehenne,Sylvain Jeandroz,Antoine Berger

doi:10.3389/fpls.2016.00472

Abstract

Plants are sessile organisms that have evolved a complex immune system which helps them cope with pathogen attacks. However, the capacity of a plant to mobilize different defense responses is strongly affected by its physiological status. Nitrogen (N) is a major nutrient that can play an important role in plant immunity by increasing or decreasing plant resistance to pathogens. Although no general rule can be drawn about the effect of N availability and quality on the fate of plant/pathogen interactions, plants’ capacity to acquire, assimilate, allocate N, and maintain amino acid homeostasis appears to partly mediate the effects of N on plant defense. Nitric oxide (NO), one of the products of N metabolism, plays an important role in plant immunity signaling. NO is generated in part through Nitrate Reductase (NR), a key enzyme involved in nitrate assimilation, and its production depends on levels of nitrate/nitrite, NR substrate/product, as well as on L-arginine and polyamine levels. Cross-regulation between NO signaling and N supply/metabolism has been evidenced. NO production can be affected by N supply, and conversely NO appears to regulate nitrate transport and assimilation. Based on this knowledge, we hypothesized that N availability partly controls plant resistance to pathogens by controlling NO homeostasis. Using the Medicago truncatula/Aphanomyces euteiches pathosystem, we showed that NO homeostasis is important for resistance to this oomycete and that N availability impacts NO homeostasis by affecting S-nitrosothiol (SNO) levels and S-nitrosoglutathione reductase activity in roots. These results could therefore explain the increased resistance we noted in N-deprived as compared to N-replete M. truncatula seedlings. They open onto new perspectives for the studies of N/plant defense interactions.

Highlights

Plants are sessile organisms that have evolved a complex immune system which helps them cope with pathogen attacks
Using the Medicago truncatula/Aphanomyces euteiches pathosystem, we showed that Nitric oxide (NO) homeostasis is important for resistance to this oomycete and that N availability impacts NO homeostasis by affecting S-nitrosothiol (SNO) levels and S-nitrosoglutathione reductase activity in roots
We found a higher NO3− content in 35S::GSNO reductase (GSNOR)-infected roots than in control infected roots, the amplitude of the pathogen-induced decrease in NO3− level was not impacted in 35S::GSNOR roots, suggesting that this process is independent of glutathione to produce S-nitrosoglutathione (GSNO) homeostasis

Summary

Introduction

Plants are sessile organisms that have evolved a complex immune system which helps them cope with pathogen attacks. In response to these attacks, plants activate multiple defense reactions both at the site of infection and systemically, which in many cases lead to resistance These reactions include massive transcriptional reprogramming, cell wall reinforcement, synthesis of NO/N Metabolism Interaction in Immunity antimicrobial metabolites, and production of pathogenesisrelated (PR) proteins. Pathogen attacks are correlated with modulation of the expression of genes or of the activity of enzymes involved in N assimilation such as NR or GS2, in N remobilization such as GS1, and in amino acid metabolism [reviewed by Fagard et al (2014)]. NO rapidly reacts with superoxide (O·2−) to form peroxynitrite (ONOO−), an oxidizing and nitrating RNS produced for instance in plant cells during immune responses (Vandelle and Delledonne, 2011) These molecules associated with NO turnover play a role in the plant immune response. GSNO plays a key role in mediating the structural and functional changes of NPR1, a key transcription coactivator of plant immunity (Tada et al, 2008)

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Conclusion