The RLK/Pelle family of kinases

The RLK/Pelle class of proteins kinases is composed of over 600 members in Arabidopsis. Many of the proteins in this family are receptor-like kinases (RLK), while others have lost their extracellular domains and are found as cytoplasmic kinases. Proteins in this family that are RLKs have a variety of extracellular domains that drive function in a large number of processes, from cell wall interactions to disease resistance to developmental control. This review will briefly cover the major subclasses of RLK/Pelle proteins and their roles. In addition, two specific groups on RLKs will be discussed in detail, relating recent findings in Arabidopsis and how well these conclusions have been able to be translated to agronomically important species. Finally, some details on kinase activity and signal transduction will be addressed, along with the mystery of RLK/Pelle members lacking kinase enzymatic activity.     

An autophosphorylation site database for leucine‐rich repeat receptor‐like kinases in Arabidopsis thaliana

Leucine‐rich repeat receptor‐like kinases (LRR RLKs) form a large family of plant signaling proteins consisting of an extracellular domain connected by a single‐pass transmembrane sequence to a cytoplasmic kinase domain. Autophosphorylation on specific Ser and/or Thr residues in the cytoplasmic domain is often critical for the activation of several LRR RLK family members with proven functional roles in plant growth regulation, morphogenesis, disease resistance, and stress responses. While identification and functional characterization of in vivo phosphorylation sites is ultimately required for a full understanding of LRR RLK biology and function, bacterial expression of recombinant LRR RLK cytoplasmic catalytic domains for identification of in vitro autophosphorylation sites provides a useful resource for further targeted identification and functional analysis of in vivo sites. In this study we employed high‐throughput cloning and a variety of mass spectrometry approaches to generate an autophosphorylation site database representative of more than 30% of the approximately 223 LRR RLKs in Arabidopsis thaliana. We used His‐tagged constructs of complete cytoplasmic domains to identify a total of 592 phosphorylation events across 73 LRR RLKs, with 497 sites uniquely assigned to specific Ser (268 sites) or Thr (229 sites) residues in 68 LRR RLKs. Multiple autophosphorylation sites per LRR RLK were the norm, with an average of seven sites per cytoplasmic domain, while some proteins showed more than 20 unique autophosphorylation sites. The database was used to analyze trends in the localization of phosphorylation sites across cytoplasmic kinase subdomains and to derive a statistically significant sequence motif for phospho‐Ser autophosphorylation.     

The multifunctional leucine-rich repeat receptor kinase BAK1 is implicated in Arabidopsis development and immunity

Plant receptor-like kinases (RLKs) are transmembrane proteins with putative N-terminal extracellular ligand-binding domains and C-terminal intracellular protein kinase domains. RLKs have been implicated in multiple physiological programs including plant development and immunity to microbial infection. Arabidopsis thaliana gene expression patterns support an important role of this class of proteins in biotic stress adaptation. Here, we provide a comprehensive survey of plant immunity-related RLK gene expression. We further document the role of the Arabidopsis Brassinosteroid Insensitive 1 (BRI1)-associated receptor kinase 1 (BAK1) in seemingly unrelated biological processes, such as plant development and immunity, and propose a role of this protein as an adaptor molecule that is required for proper functionality of numerous RLKs. This view is supported by the identification of an additional RLK, PEPR1, and its closest homolog, PEPR2 as BAK1-interacting RLKs.     

小麦受体样蛋白激酶及其衍生蛋白的研究进展

受体样蛋白激酶及其衍生蛋白(受体样胞内激酶和受体样蛋白)在调控植物生长、发育和不良环境反应等过程中发挥重要作用。该文简要介绍了近年来获得的对植物受体样蛋白激酶及其衍生蛋白的主要认识, 着重总结了小麦(Triticum aestivum)受体样蛋白激酶及其衍生蛋白的研究进展与不足, 并展望了该领域的发展趋势, 对在小麦中进一步有效开展受体样蛋白激酶及其衍生蛋白的结构和功能研究具参考意义。     

Transcriptional regulation of the CRK/DUF26 group of Receptor-like protein kinases by ozone and plant hormones in Arabidopsis

Background  

Plant Receptor-like/Pelle kinases (RLK) are a group of conserved signalling components that regulate developmental programs and responses to biotic and abiotic stresses. One of the largest RLK groups is formed by the Domain of Unknown Function 26 (DUF26) RLKs, also called Cysteine-rich Receptor-like Kinases (CRKs), which have been suggested to play important roles in the regulation of pathogen defence and programmed cell death. Despite the vast number of RLKs present in plants, however, only a few of them have been functionally characterized.     

Signalling through kinase-defective domains: the prevalence of atypical receptor-like kinases in plants

The structure of plant receptor-like kinases (RLKs) is similar to that of animal receptor tyrosine kinases (RTKs), and consists of an extracellular domain, a transmembrane span, and a cytoplasmic domain containing the conserved kinase domain. The mechanism by which animal RTKs, and probably plant RLKs, signal includes the dimerization of the receptor, their intermolecular phosphorylation, and the phosphorylation of downstream signalling proteins. However, atypical RTKs with a kinase-dead domain that signal through phosphorylation-independent mechanisms have also been described in animals. In the last few years, some atypical RLKs have also been reported in plants. Here these examples and their possible signalling mechanisms are reviewed. Plant genomes contain a much larger number of genes coding for receptor kinases than other organisms. The prevalence of atypical RLKs in plants is analysed here. A sequence analysis of the Arabidopsis kinome revealed that 13% of the kinase genes do not retain some of the residues that are considered as invariant within kinase catalytic domains, and are thus putatively kinase-defective. This percentage rises to close to 20% when analysing RLKs, suggesting that phosphorylation-independent mechanisms mediated by atypical RLKs are particularly important for signal transduction in plants.     

Challenges in understanding RLK function

Plants use receptor-like kinases (RLKs) to transduce extracellular signals into the cell. Recent advancements in RLK research include the cloning of the BRASSINOSTEROID INSENSITIVE 1 and CLAVATA 1 genes, revealing RLK roles in development. Our understanding of RLK function has also been broadened by transgenic approaches in the study of the RLKs pollen receptor kinase 1, and wall associated kinase 1. These results extend the observations that RLKs function in developmental processes and plant defense responses. Additionally, expression based studies suggest roles for other newly reported RLKs in development and light responses. Taken together, the studies confirm the importance of RLKs in diverse plant processes, yet major challenges remain. These include identifying ligands that activate RLKs and characterizing downstream pathways. These challenges can be conquered by coordinated efforts from investigators using molecular, genetic, and biochemical approaches.     

RLKs orchestrate the signaling in plant male-female interaction

Different from animals, sessile plants are equipped with a large receptor-like kinase (RLK) superfamily. RLKs are a family of single trans-membrane proteins with divergent N-terminal extracellular domains capped by a signal peptide and C-terminal intracellular kinase. Researches in the last two decades have uncovered an increasing number of RLKs that regulate plant development, stress response and sexual reproduction, highlighting a dominant role of RLK signaling in cell-to-cell communications. Sexual reproduction in flowering plants is featured by interactions between the male gametophyte and the female tissues to facilitate sperm delivery and fertilization. Emerging evidences suggest that RLKs regulate almost every aspect of plant reproductive process, especially during pollination. Therefore, in this review we will focus mainly on the function and signaling of RLKs in plant male-female interaction and discuss the future prospects on these topics.     

Multi-tasking of somatic embryogenesis receptor-like protein kinases

Receptor-like protein kinases (RLKs) are transmembrane proteins crucial for cell-to-cell and cell-to-environment communications. The extracellular domain of a RLK is responsible for perception of a specific extracellular ligand to trigger a unique intercellular signaling cascade, often via phosphorylation of cellular proteins. The signal is then transduced to the nucleus of a cell where it alters gene expression. There are more than 610 RLKs in Arabidopsis thaliana, only a handful of them have been functionally characterized. This review focuses on recent advances in our understanding of a small group of RLKs named somatic embryogenesis receptor-like protein kinases (SERKs). SERKs act as coreceptors in multiple signaling pathways via their physical interactions with distinct ligand-binding RLKs.     

Self/nonself perception and recognition mechanisms in plants: a comparison of self-incompatibility and innate immunity

Analyses of emerging concepts indicate that parallels exist between self-incompatibility and pathogen recognition. In the case of surveillance of 'nonself', plant immune responses are triggered either by pattern recognition receptors (PRRs) that detect conserved pathogen-associated molecular patterns (PAMPs) or by resistance (R) proteins recognizing isolate-specific pathogen effectors. PAMP detection is an important component of innate immunity in plants and serves as an early warning system for the presence of potential pathogens and activation of plant defense mechanisms. In the Brassicaceae, the recognition of 'self' and self-incompatibility are components of a receptor-ligand based mechanism that utilizes an S receptor kinase (SRK) to perceive and reject 'self'-pollen. SRK is an S-domain receptor-like kinase (RLK), which in turn is part of the RLK family, some members of which represent PRRs involved in the detection of PAMPs. S-domain RLKs also occur in species that do not exhibit self-incompatibility and are up-regulated in response to wounding, PAMPs and pathogen recognition. Although evolution may have driven expansion of certain RLK families to serve roles in particular physiological processes, this may not exclude these receptor types from functioning in different programs. Recent findings on self/nonself recognition are reviewed and conceptual and mechanistic links between microbial recognition and self-incompatibility are discussed.     

Plant pattern-recognition receptors controlling innate immunity

Plants are exposed to numerous potential pathogenic microbes. To counter the threat, plants have evolved diverse patternrecognition receptors(PRRs), which are receptor kinases(RKs) and receptor proteins(RPs) specialized to detect conserved pathogen/microbe-associated molecular patterns(PAMPs/MAMPs). Although only a handful of RKs and RPs are known PRRs,they belong to the receptor-like kinase(RLK) and receptor-like protein(RLP) superfamilies that undergo lineage-specific expansion, suggesting that many of these RLKs and RLPs are potential PRRs. Analyses of existing PRRs have uncovered ligand-induced RLK-RK or RLK-RP oligomerization as a common mechanism for immune activation. PRRs can recruit additional components to form dynamic receptor complexes, which mediate specific cellular responses. Detailed analyses of these components are shedding light on molecular mechanisms underlying the regulation of PRR activity and downstream signaling.     

Erratum to: Plant pattern-recognition receptors controlling innate immunity

Plants are exposed to numerous potential pathogenic microbes. To counter the threat, plants have evolved diverse patternrecognition receptors(PRRs), which are receptor kinases(RKs) and receptor proteins(RPs) specialized to detect conserved pathogen/microbe-associated molecular patterns(PAMPs/MAMPs). Although only a handful of RKs and RPs are known PRRs, they belong to the receptor-like kinase(RLK) and receptor-like protein(RLP) superfamilies that undergo lineage- specific expansion, suggesting that many of these RLKs and RLPs are potential PRRs. Analyses of existing PRRs have uncovered ligand-induced RLK-RK or RLK-RP oligomerization as a common mechanism for immune activation. PRRs can recruit additional components to form dynamic receptor complexes, which mediate specific cellular responses. Detailed analyses of these components are shedding light on molecular mechanisms underlying the regulation of PRR activity and downstream signaling.     

Functional immobilization of plant receptor-like kinase onto microbeads towards receptor array construction and receptor-based ligand fishing

Despite the large number of receptor-like kinases (RLKs) in plants, few of their specific ligands are known. Ligand fishing is one of the most challenging post-genomic technologies. Here, we report a strategy for functional immobilization of plant RLKs on microbeads via covalent linkage. Because of the high density of immobilized RLKs, ligand-receptor interaction can be visualized at high sensitivity using fluorescent-labeled ligands under the confocal laser scanning microscope. Moreover, using a receptor-based affinity chromatography system with RLK microbeads, the ligand of the receptor was directly retrieved at high purity from complex natural samples. Our RLK microbeads and receptor-based ligand fishing approach is a feasible alternative to conventional forward genetics and bioassay-based biochemical purification for identification of novel ligand-receptor pairs in plants.     

Plasmodesmal receptor-like kinases identified through analysis of rice cell wall extracted proteins

In plants, plasmodesmata (PD) are intercellular channels that function in both metabolite exchange and the transport of proteins and RNAs. Currently, many of the PD structural and regulatory components remain to be elucidated. Receptor-like kinases (RLKs) belonging to a notably expanded protein family in plants compared to the animal kingdom have been shown to play important roles in plant growth, development, pathogen resistance, and cell death. In this study, cell biological approaches were used to identify potential PD-associated RLK proteins among proteins contained within cell walls isolated from rice callus cultured cells. A total of 15 rice RLKs were investigated to determine their subcellular localization, using an Agrobacterium-mediated transient expression system. Of these six PD-associated RLKs were identified based on their co-localization with a viral movement protein that served as a PD marker, plasmolysis experiments, and subcellular localization at points of wall contact between spongy mesophyll cells. These findings suggest potential PD functions in apoplasmic signaling in response to environmental stimuli and developmental inputs.     

Structure and function of the receptor-like protein kinases of higher plants

Cell surface receptors located in the plasma membrane have a prominent role in the initiation of cellular signalling. Recent evidence strongly suggests that plant cells carry cell surface receptors with intrinsic protein kinase activity. The plant receptor-like protein kinases (RLKs) are structurally related to the polypeptide growth factor receptors of animals which consist of a large extracytoplasmic domain, a single membrane spanning segment and a cytoplasmic domain of the protein kinase gene family. Most of the animal growth factor receptor protein kinases are tyrosine kinases; however, the plant RLKs all appear to be serine/threonine protein kinases. Based on structural similarities in their extracellular domains the RLKs fall into three categories: the S-domain class, related to the self-incompatibility locus glycoproteins of Brassica; the leucine-rich repeat class, containing a tandemly repeated motif that has been found in numerous proteins from a variety of eukaryotes; and a third class that has epidermal growth factor-like repeats. Distinct members of these putative receptors have been found in both monocytyledonous plants such as maize and in members of the dicotyledonous Brassicaceae. The diversity among plant RLKs, reflected in their structural and functional properties, has opened up a broad new area of investigation into cellular signalling in plants with far-reaching implications for the mechanisms by which plant cells perceive and respond to extracellular signals.     

Analysis of Phosphorylation of the Receptor-Like Protein Kinase HAESA during Arabidopsis Floral Abscission

Receptor-like protein kinases (RLKs) are the largest family of plant transmembrane signaling proteins. Here we present functional analysis of HAESA, an RLK that regulates floral organ abscission in Arabidopsis. Through in vitro and in vivo analysis of HAE phosphorylation, we provide evidence that a conserved phosphorylation site on a region of the HAE protein kinase domain known as the activation segment positively regulates HAE activity. Additional analysis has identified another putative activation segment phosphorylation site common to multiple RLKs that potentially modulates HAE activity. Comparative analysis suggests that phosphorylation of this second activation segment residue is an RLK specific adaptation that may regulate protein kinase activity and substrate specificity. A growing number of RLKs have been shown to exhibit biologically relevant dual specificity toward serine/threonine and tyrosine residues, but the mechanisms underlying dual specificity of RLKs are not well understood. We show that a phospho-mimetic mutant of both HAE activation segment residues exhibits enhanced tyrosine auto-phosphorylation in vitro, indicating phosphorylation of this residue may contribute to dual specificity of HAE. These results add to an emerging framework for understanding the mechanisms and evolution of regulation of RLK activity and substrate specificity.     

Probing the roles of LRR RLK genes in Arabidopsis thaliana roots using a custom T-DNA insertion set

Leucine-rich repeat receptor-like protein kinases (LRR RLKs) represent the largest group of Arabidopsis RLKs with approximately 235 members. A minority of these LRR RLKs have been assigned to diverse roles in development, pathogen resistance and hormone perception. Using a reverse genetics approach, a collection of homozygous T-DNA insertion lines for 69 root expressed LRR RLK genes was screened for root developmental defects and altered response after exposure to environmental, hormonal/chemical and abiotic stress. The obtained data demonstrate that LRR RLKs play a role in a wide variety of signal transduction pathways related to hormone and abiotic stress responses. The described collection of T-DNA insertion mutants provides a valuable tool for future research into the function of LRR RLK genes.     

Expansion of the receptor-like kinase/Pelle gene family and receptor-like proteins in Arabidopsis

Receptor-like kinases (RLKs) are a family of transmembrane proteins with versatile N-terminal extracellular domains and C-terminal intracellular kinases. They control a wide range of physiological responses in plants and belong to one of the largest gene families in the Arabidopsis genome with more than 600 members. Interestingly, this gene family constitutes 60% of all kinases in Arabidopsis and accounts for nearly all transmembrane kinases in Arabidopsis. Analysis of four fungal, six metazoan, and two Plasmodium sp. genomes indicates that the family was represented in all but fungal genomes, indicating an ancient origin for the family with a more recent expansion only in the plant lineages. The RLK/Pelle family can be divided into several subfamilies based on three independent criteria: the phylogeny based on kinase domain sequences, the extracellular domain identities, and intron locations and phases. A large number of receptor-like proteins (RLPs) resembling the extracellular domains of RLKs are also found in the Arabidopsis genome. However, not all RLK subfamilies have corresponding RLPs. Several RLK/Pelle subfamilies have undergone differential expansions. More than 33% of the RLK/Pelle members are found in tandem clusters, substantially higher than the genome average. In addition, 470 of the RLK/Pelle family members are located within the segmentally duplicated regions in the Arabidopsis genome and 268 of them have a close relative in the corresponding regions. Therefore, tandem duplications and segmental/whole-genome duplications represent two of the major mechanisms for the expansion of the RLK/Pelle family in Arabidopsis.     

植物M/MLD类受体蛋白激酶及其生物学功能的研究进展北大核心CSCD

植物受体蛋白激酶通过与胞外信号结合感知和接收外部信号传递,在植物各个生理过程及生物代谢中发挥着重大的作用。其中M/MLD类受体蛋白激酶是一类植物特有的具有Malectin-like结构域的受体蛋白激酶。研究表明,M/MLD-RLKs亚家族参与植物发育过程及生物/非生物胁迫调控。该研究对近年来国内外有关植物M/MLD-RLKs的发现、结构特点以及生物学功能等方面的研究进展进行综述,并重点阐述其在调控植物根系、叶片、花发育及响应多种胁迫过程中的作用,为深入研究M/MLD-RLKs在植物生长发育过程中的生理功能提供参考。     

Multiple receptor-like kinase cDNAs from liverwort Marchantia polymorpha and two charophycean green algae, Closterium ehrenbergii and Nitella axillaris: Extensive gene duplications and gene shufflings in the early evolution of streptophytes

Plant receptor-like kinases (RLKs) comprise a large family with more than several hundred members in vascular plants. The RLK family is thought to have diverged specifically in the plant kingdom, and no family member has been identified in other lineages except for animals and Plasmodium, both of which have RLK related families of small size. To know the time of divergence of RLK family members by gene duplications and domain shufflings, comprehensive isolations of RLK cDNAs were performed from a nonvascular plant, liverwort Marchantia polymorpha and two charophycean green algae, Closterium ehrenbergii, and Nitella axillaris, thought to be the closest relatives to land plants. We obtained twenty-nine, fourteen, and thirteen RLK related cDNAs from M. polymorpha, C. ehrenbergii, and N. axillaris, respectively. The amino acid sequences of these RLKs were compared with those of vascular plants, and phylogenetic trees were inferred by GAMT, a genetic algorithm-based maximum likelihood (ML) method that outputs multiple trees, together with best one. The inferred ML trees revealed ancient gene duplications generating subfamilies with different domain organizations, which occurred extensively at least before the divergence of vascular and nonvascular plants. Rather it remains possible that the extensive gene duplications occurred during the early evolution of streptophytes. Multicellular-specific somatic embryogenesis receptor kinase (SERK) involved in somatic embryogenesis was found in a unicellular alga C. ehrenbergii, suggesting the evolution of SERK by gene recruitment of a unicellular gene.