Chapter Two - Hormonal interactions in the regulation of the nitrogen-fixing legume-Rhizobium symbiosis

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Abstract

Plant hormones have long been associated with the ability of legumes to form nitrogen-fixing symbioses. During the nodulation program, two events are required: The formation of a new root organ, the nodule, and the successful infection of rhizobia into the root, and later the nodule. Cell-type specific hormone synthesis, perception and downstream responses are required in the epidermis, the root cortex and in vascular tissues to coordinate infection and nodule development. Recent progress in this area has demonstrated the crucial role of plant hormones in feedback regulation of nodule development and infection. Hormonal communication between shoot and root has also been linked to the systemic autoregulation of nodule numbers. Future studies will need to focus on how legumes regulate nodule development separately from other organogenesis processes like lateral root formation, even though the same hormones are involved in both. Similarly, balancing nodulation with restraints of abiotic and biotic stresses will require integration of hormone studies in plants facing several simultaneous challenges. While most studies have focused on the effects of single hormones, it will also be necessary to develop new tools for single cell hormone analyses and concurrent analysis of multiple hormones.

Introduction

The interaction between rhizobia and their legume hosts results in the formation of nitrogen-fixing root nodules. The symbiosis starts with the recognition of plant flavonoids, which activates Nod factor synthesis by rhizobia. Nod factor recognition by the host controls activation/repression of defense responses, the formation of an infection thread (or crack-entry infection in some legumes) and initiation of nodule development (Oldroyd, 2013). This involves signaling between the infected root hair and the inner layers of the root where nodule development starts. Typically, in temperate legumes forming indeterminate nodules, like Medicago truncatula or pea, nodule development starts in the pericycle, endodermis and inner cortex (Xiao et al. 2014), while in legumes forming determinate nodules, like Lotus japonicus and soybean, cell divisions start in the outer/middle cortex and the pericycle (Hirsch, 1992). Because nitrogen fixation and nodule formation require continuous input of carbon, the symbiosis is autoregulated to optimize nodule numbers. This involves a systemic signaling circuit between root and shoot (autoregulation of nodulation, AON), in which rhizobia induce signaling peptides that move to the shoot, where they are perceived by a receptor kinase. This triggers the movement of a shoot-to-root signal preventing the formation of further nodules (reviewed by Mortier et al., 2012b, Reid et al., 2011). At later stages of the symbiosis, in ineffective symbioses or under stressful conditions, the plant induces nodule senescence and loss of nitrogen fixation (Van de Velde et al., 2006).

While rhizobia synthesize some plant hormones, there is so far no strong evidence that these are essential for nodule initiation or infection and this topic is not covered in this review. However, hormones synthesized by rhizobia might play a role in enhancing the efficiency of the symbiosis. In contrast, spatiotemporal control of hormone synthesis, transport and perception by the host were shown to be essential for successful infection and nodule development. This review focusses on the role of the phytohormones abscisic acid, auxin, cytokinin, ethylene, gibberellic acid, jasmonic acid and strigolactones. Due to space constraints, not all studies could be mentioned here. For a broader review on the role of phytohormones and related signals in legume-rhizobia interactions, including other hormones and signals and the influence of hormone synthesis by rhizobia, please refer to Ferguson and Mathesius, 2014, Bensmihen, 2015, and Liu, Zhang, Yang, Yu, and Wang (2018).

Section snippets

Abscisic acid

Abscisic acid (ABA) is well known for its roles in drought responses and seed ripening, but also plays roles in the root development and biotic interactions. ABA has emerged as an important regulator of both rhizobial infection and nodule development. In several legumes, external addition of ABA in the low micro-molar range negatively influences nodule numbers and infections (e.g. Ding et al., 2008, Liang et al., 2007, Suzuki et al., 2004), while an ABA inhibitor was shown to increase nodule

Auxin

The plant hormone auxin represents a group of related hormones, of which indole-3-acetic acid (IAA) is the most studied and likely the most abundant one. However, other forms of auxin are present in plants and may play specific functions, although these remain largely unexplored. Auxin is generally known for its role in the control of cell division, differentiation, and elongation; these functions are essential for organ initiation and differentiation throughout the plant (Benková et al., 2003)

Cytokinin

Similar to auxins, cytokinins generally have roles in plant development and cell cycle control. While cytokinins are represented by a group of related adenine-derived hormones, most studies have not differentiated between different cytokinin functions and these forms will therefore be referred to as ‘cytokinin’. Cytokinin signaling via specific cytokinin receptors is essential for nodule initiation in legumes forming both determinate and indeterminate nodules, but the role of cytokinin differs

Ethylene

The gaseous, diffusible hormone ethylene plays important roles in plants, most notably in biotic and abiotic stress responses, fruit ripening and senescence. Application of ethylene to legume roots inhibits nodulation, while ethylene synthesis inhibitors consistently increase nodule numbers in most legumes, with soybean and Sesbania rostrata being notable exceptions (D'Haeze et al., 2003, Guinel, 2015). This suggests that ethylene is generally a negative regulator of nodulation, by affecting

Gibberellins

Gibberellins (GAs) were first identified as a class of plant hormones with stimulating effects on plant growth. GAs have been reported to have both positive and negative effects on nodulation in different legumes and at different stages of nodulation. For example, GA application was shown to inhibit nodulation and infection in L. japonicus, where GA inhibited early Nod factor signaling through NSP2 and NIN (Maekawa et al., 2009). Similarly, exogenous addition of active GA to M. truncatula

Jasmonic acid

Jasmonic acid (JA) is a small lipid that acts as a plant hormone in many biotic and abiotic stress responses. In particular, JA is required for the induction of wound responses and systemic resistance to herbivores but also plays roles in plant development. During nodulation, JA acts during early infection events, where JA inhibits infection, possibly through affecting calcium spiking signaling and nodulin gene expression (RIP1 [Rhizobium Indiced Peroxidase1]; ENOD11 and NIN) in M. truncatula

Strigolactones

Strigolactones (SLs) are multifaceted hormones that were first identified as root exudates stimulating spore germination and hyphal growth of mycorrhizal fungal symbioses and controlling parasitic weed germination, but they also have roles in shoot branching and root development (reviewed by De Cuyper & Goormachtig, 2017).

In general, SLs appear to have a positive role in nodulation, at least at low concentrations. In several legumes, nodule numbers were found to be slightly increased after the

Summary and outlook

Hormone pathways evolved long before the relatively recent evolution of nodulation in legumes. The role of plant hormones in development and in the response to environmental stresses had to be adapted to the regulation of nodulation. While our picture of the hormonal regulation of nodulation is steadily growing (summarized in Fig. 1), we still only have a sketchy understanding of the specific role of hormones in nodulation as opposed to other developmental processes, for example through the

Acknowledgments

UM was supported by the Australian Research Council (DP150102002), by the Hermon Slade Foundation (HSF 16-02) and by the Australian Research Council and The Grains Research and Development Corporation (IC170100005).

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