Legumes Regulate Symbiosis with Rhizobia via Their Innate Immune System

Abstract

Plant roots are constantly exposed to a diverse microbiota of pathogens and mutualistic partners. The host's immune system is an essential component for its survival, enabling it to monitor nearby microbes for potential threats and respond with a defence response when required. Current research suggests that the plant immune system has also been employed in the legume-rhizobia symbiosis as a means of monitoring different rhizobia strains and that successful rhizobia have evolved to overcome this system to infect the roots and initiate nodulation. With clear implications for host-specificity, the immune system has the potential to be an important target for engineering versatile crops for effective nodulation in the field. However, current knowledge of the interacting components governing this pathway is limited, and further research is required to build on what is currently known to improve our understanding. This review provides a general overview of the plant immune system's role in nodulation. With a focus on the cycles of microbe-associated molecular pattern-triggered immunity (MTI) and effector-triggered immunity (ETI), we highlight key molecular players and recent findings while addressing the current knowledge gaps in this area.

Keywords: legumes; nodulation; pathogen; plant immune system; rhizobia; symbiosis.

Figure 1

A general model for the interplay of nodulation and defence signalling mechanisms induced by rhizobial infection at the root hair cell. To attract rhizobial partners, legume roots exude flavonoids into the rhizosphere, which then bind to the rhizobial transcriptional activator NodD. In response, rhizobia produce Nod factors (NFs) via NodABC gene transcription. Secreted NFs are recognised by their cognate plant Nod factor receptors, activating symbiotic signalling to promote nodulation. However, NFs have also been shown to induce a small defence response upon recognition, including the production of reactive oxygen species (ROS) and the upregulation of defence genes. NFs also attenuate defences in the nonlegume Arabidopsis via LYSIN MOTIF-CONTAINING RECEPTOR-LIKE KINASE 3 (AtLYK3). Chitinases are implicated in this host-specific recognition via NF degradation activity. Additionally, host plants also contain pattern recognition receptor (PRR) membrane proteins to perceive bacterial microbial-associated molecular patterns (MAMPs), triggering a mitogen-activated protein kinase (MAPK) signalling cascade that leads to an associated defence response and MAMP-triggered immunity (MTI). These include FLAGELLINSENSITIVE2 (FLS2) and exopolysaccharide receptor 3 (Epr3), which function to perceive flagellin and exopolysaccharides (EPS), respectively. However, certain rhizobial flagellins, such as that of Sinorhizobium meliloti, lack the flagellin 22 (flg22) epitope for perception [27,28]. NodD also induces the TtsI transcriptional activator, which initiates type III secretion system (T3SS) transcription. Certain rhizobia secrete nodulation outer protein (Nop) proteins via secretion systems (T3SS, type IV secretion system, and type VI secretion system) to attenuate plant defences and promote infection and establishment. Resistant plants have evolved to produce nucleotide binding site-leucine-rich repeat receptor (NLR) proteins to recognise these Nops. Recognition activates defence signalling once again, leading to the inhibition of infection and effector-triggered immunity (ETI). Plant-pathogen NLRs form calcium-permeable channels that induce ROS and cell death but have not yet been identified in nodulation. MAP2K—MAPK kinase; MAP3K—MAP2K kinase; TNL—Toll/interleukin 1 (TIR) NLR; CNL—coiled-coil (CC)-NLR; hNLRs—helper NLRs; Ca²⁺—calcium ions; Cyt—cytosolic and P—phosphate group. Created with BioRender.com.

Figure 2

A comparison of the proposed roles of chitinases targeting the glycosidic linkages in either chitin or NFs for degradation. In response to a phytopathogenic fungi, the plant releases chitinases, which function to degrade the chitin backbone and/or release elicitors to further upregulate defences. In response to NFs, chitinase NOD FACTOR HYDROLASE1 (NFH1) degrades NFs to regulate NF levels and optimise root hair infection. In the absence of NFH1, NF levels are unregulated, which results in delayed root-hair infection and abnormal nodule development. NF—Nod Factor and NFH1—NOD FACTOR HYDROLASE1. Created with BioRender.com.