Abstract

The symbiotic relationship between legumes and nitrogen-fixing rhizobia induces local and systemic responses, which ultimately lead to nodule formation. The autoregulation of nodulation (AON) is a systemic mechanism related to innate immunity that controls nodule development and involves different components ranging from hormones, peptides, receptors to small RNAs. Here, we characterized a rapid systemic redox changes induced during soybean–Bradyrhizobium japonicum symbiotic interaction. A transient peak of reactive oxygen species (ROS) generation was found in soybean leaves after 30 min of root inoculation with B. japonicum. The ROS response was accompanied by changes in the redox state of glutathione and by activation of antioxidant enzymes. Moreover, the ROS peak and antioxidant enzyme activation were abolished in leaves by the addition, in either root or leaf, of DPI, an NADPH oxidase inhibitor. Likewise, these systemic redox changes primed the plant increasing its tolerance to photooxidative stress. With the use of non-nodulating nfr5-mutant and hyper-nodulating nark-mutant soybean plants, we subsequently studied the systemic redox changes. The nfr5-mutant lacked the systemic redox changes after inoculation, whereas the nark-mutant showed a similar redox systemic signaling than the wild type plants. However, neither nfr5- nor nark-mutant exhibited tolerance to photooxidative stress condition. Altogether, these results demonstrated that (i) the early redox systemic signaling during symbiotic interaction depends on a Nod factor receptor, and that (ii) the induced tolerance response depends on the AON mechanisms.

Highlights

  • The symbiotic interaction between legume plants and nitrogenfixing soil bacteria has great importance at a basic, ecological and economic level and, the legume–rhizobium symbiosis interaction is the most important in terms of the biological nitrogen fixation (Graham and Vance, 2003)

  • The participation of local reactive oxygen species (ROS) signaling in roots after symbiont perception has been widely studied (Cárdenas et al, 2008; Muñoz et al, 2012, 2014a; Damiani et al, 2016), much less is known about the ROS systemic production during the legume–rhizobium interaction

  • Plants recognize different signal molecules from microorganisms, like microorganism associated molecular patterns (MAMPs) and other pathogenic and symbiotic signals that modulate the immune system of plants (Limpens et al, 2015; Couto and Zipfel, 2016)

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Summary

Introduction

The symbiotic interaction between legume plants and nitrogenfixing soil bacteria has great importance at a basic, ecological and economic level and, the legume–rhizobium symbiosis interaction is the most important in terms of the biological nitrogen fixation (Graham and Vance, 2003). The legume–rhizobium interaction could induce PGPR like-responses, improving host plant growth and tolerance/resistance to abiotic/biotic stress conditions. Rhizobia have acquired the ability to evade the initial microbeassociated molecular pattern (MAMP) triggered immunity (Boller and Felix, 2009) by modulating the host immune response to avoid being recognized as a pathogen (Zamioudis and Pieterse, 2012). In this regard, many biochemical, molecular and hormonal changes occur at local and systemic levels during the legume–rhizobium interaction so that rhizobia coordinate the organogenesis of the nodule with infection (Nadzieja et al, 2018). Nod factors are formed by a chitin backbone with an N-linked fatty acid moiety attached to the non-reducing terminal sugar and other modifications (Oldroyd and Downie, 2008; Oldroyd et al, 2011)

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