An extracellular network of Arabidopsis leucine-rich repeat receptor kinases

Abstract

The cells of multicellular organisms receive extracellular signals using surface receptors. The extracellular domains (ECDs) of cell surface receptors function as interaction platforms, and as regulatory modules of receptor activation. Understanding how interactions between ECDs produce signal-competent receptor complexes is challenging because of their low biochemical tractability. In plants, the discovery of ECD interactions is complicated by the massive expansion of receptor families, which creates tremendous potential for changeover in receptor interactions. The largest of these families in Arabidopsis thaliana consists of 225 evolutionarily related leucine-rich repeat receptor kinases (LRR-RKs), which function in the sensing of microorganisms, cell expansion, stomata development and stem-cell maintenance. Although the principles that govern LRR-RK signalling activation are emerging, the systems-level organization of this family of proteins is unknown. Here, to address this, we investigated 40,000 potential ECD interactions using a sensitized high-throughput interaction assay, and produced an LRR-based cell surface interaction network (CSI) that consists of 567 interactions. To demonstrate the power of CSI for detecting biologically relevant interactions, we predicted and validated the functions of uncharacterized LRR-RKs in plant growth and immunity. In addition, we show that CSI operates as a unified regulatory network in which the LRR-RKs most crucial for its overall structure are required to prevent the aberrant signalling of receptors that are several network-steps away. Thus, plants have evolved LRR-RK networks to process extracellular signals into carefully balanced responses.

Inorganic nitrogen availability alters Eucalyptus grandis receptivity to the ectomycorrhizal fungus Pisolithus albus but not symbiotic nitrogen transfer

“…Disease resistance proteins, including those containing leucinerich repeat receptor-like protein kinase (LRR-RLK) domains, make up a large family and are found extensively in the genomes of most plants (Wu et al, 2016). Their function is not well understood but they are thought to act as early detector networks of microbial presence and/or effectors and alter signal transduction accordingly to activate plant defence pathways (McHale et al, 2006;Smakowska-Luzan et al, 2018). Similarly, membrane-bound receptor proteins such as lectin receptor kinases are able to sense the presence of microbial elicitors and trigger downstream defence pathways (Singh & Zimmerli, 2013;Tang et al, 2017).…”

Molecular dialogues between viruses and receptor‐like kinases in plants

“…The ECDs of plant RLKs are considerably diverse, and may include extensin‐like, lectin‐like, epidermal‐growth‐factor‐like (including cysteine‐rich), lysine motif, and leucine‐rich repeat (LRR) domains, among others (Gish and Clark, ). RLK ECDs may homo‐ or hetero‐multimerize in order to perceive endogenous or exogenous ligands, including peptides, steroids, oligosaccharides, polysaccharides, and lipopolisaccharides, and transduce these signals to the cell interior (Breiden and Simon, ; Ye et al , ; He et al , ; Smakowska‐Luzan et al , ), which often results in the initiation of specific intracellular signalling events.…”

“…These molecular patterns are usually recognized as danger signals by plant cells, leading to the activation of immune responses (Macho and Zipfel, ) and the subsequent development of pattern‐triggered immunity (PTI). Other RLKs have been found to interact with PRRs, providing a scaffold for their association with other proteins or regulating the activation of signalling (Tang et al , ; Smakowska‐Luzan et al , ). Additionally, non‐PRR RLKs may also contribute to the plant response to pathogen perception by regulating molecular cross‐talks or developmental rearrangements associated with immunity (Tang et al , ).…”

“…Still to be elucidated are the mechanisms employed by monopartite geminiviruses, which lack an NSP, as well as viruses belonging to other families, to interfere with this signalling cascade. Of note, AtNIK1 interacts with AtBAK1 (Smakowska‐Luzan et al , ), raising the possibility that the previously observed contribution of AtBAK1 to antiviral immunity relies on this pathway and not PTI. However, considering that both AtNIK1 and AtBAK1 belong to the same subfamily of LRR‐RLKs (subfamily II) in Arabidopsis, and share a similar structural organization (Shiu and Bleecker, ), a role for NIK1 as a co‐receptor or signalling partner for other RLK(s) should not be ruled out.…”

“…1). This is further supported by the observation that viral infections often result in the induction of PTI-related genes (Whitham et al, 2003;Love et al, 2005;Carr et al, 2010;Hanssen et al, 2011;Nicaise and Candresse, 2017), and by the discovery of at least two viral proteins, the capsid protein (CP) from Plum pox virus (PPV) (genus Potyvirus) and the movement protein (MP) of Cucumber mosaic virus (CMV) (genus Cucumovirus), with PTI-suppressing activity (Nicaise and Candresse, 2017;Kong et al, 2018). That suppressing PTI could be beneficial for an invading virus is not inconceivable, since the activation of PTI results in multiple outputs associated with plant defence, some of which may have a negative effect on the viral infection: at least in some cases, accumulation of reactive oxygen species (ROS) can have a deleterious effect on the viral invasion (Wu et al, 2017), and the activation of salicylic acid (SA) signalling has proven effective against a plethora of different plant viruses (reviewed in Alazem and Lin (2015)).…”