Receptor‐Like Kinases: Key Regulators of Plant Development and Defense (2013)

Plants are multi-cellular organisms that live in diverse and fluctuating environments. Cell-cell and cell-environment communication are therefore critical to plant growth and development. In animals, transmembrane receptor protein tyrosine kinases play significant roles in cell-cell signaling. There was a great deal of surprise in the plant community, however, when the first receptor-like protein kinase (RLK) was isolated from maize by John C. Walker and Ren Zhang (1990) over twenty years ago, because plant cells contain cell walls which were thought to be more rigid and less dynamic than the extracellular matrix of animal cells. Researchers were also initially skeptical that small signaling molecules (ligands) could freely move through cell walls to deliver signals. The identification of RLKs from plants suggested that plants utilize mechanisms similar to animals in cell-cell communication. Genome sequencing revealed that plant genomes encode a great number of RLKs, much more than in animals. For example, the Arabidopsis genome possesses around 610 RLK coding sequences (Shiu and Bleecker 2001a, 2001b), whereas the rice genome contains almost twice the number found in Arabidopsis (Shiu et al. 2004). A typical RLK contains an extracellular domain, a single-pass transmembrane domain, and a cytoplasmic kinase domain. Usually the extracellular domain of a ligand-binding RLK physically interacts with a small ligand molecule, one either secreted from surrounding cells or presented as a conserved pathogen associated molecular pattern (PAMP), which triggers or secures the homo- or hetero-dimerization of two RLK molecules, leading to mutual phosphorylation of both RLKs. The activated RLKs then transduce the signal to downstream networks and eventually alter gene transcription patterns, establishing a cellular response to the specific ligand. Based on their characterized biological roles thus far, most RLKs can be categorized functionally into two groups, those that have roles in development or those that function in defense. Some RLKs, however, play dual roles in both development and defense. In this special issue, up-to-date mechanistic details of several RLKs in regulating plant development and defense are discussed (He et al. 2013; Jiang et al. 2013; Lin et al. 2013; Niederhuth et al. 2013; Shpak 2013; Wierzba and Tax 2013; Wu and Zhou 2013; Zhang and Thomma 2013). Although hundreds of RLKs have been identified in many plant species, so far only around fifty of them have been functionally characterized. Most of the characterized RLKs belong to the largest subfamily of RLKs, named leucine-rich repeat receptor-like protein kinases (LRR-RLKs) based on their extracellular domains (Shiu and Bleecker 2001a, 2001b, 2003). RLKs mediate a wide range of physiological processes during normal growth and development, from zygotic embryogenesis to flowering. For instance, BAM1/2, EMS1, FER, SERK1/2, and RPK2/TOAD2 are involved in anther development and fertilization (Zhao et al. 2002; Albrecht et al. 2005; Colcombet et al. 2005; Hord et al. 2006; Escobar-Restrepo et al. 2007; Mizuno et al. 2007); PXY/TDR controls xylem differentiation (Fisher and Turner 2007; Hirakawa et al. 2010); BAM1/2, CLV1, RPK2, and CRN regulate shoot apical meristem maintenance and development (Clark et al. 1997; DeYoung et al. 2006; Müller et al. 2008; Kinoshita et al. 2010); ERECTA, ERL1, ERL2, and PSKR mediate plant architecture, cell proliferation and organ growth (Torii et al. 1996; Matsubayashi et al. 2002; Shpak et al. 2003); BRI1, BRL1, BRL3, BAK1, SERK1, and BKK1 are the receptors and co-receptors for brassinosteroids (BRs), regulating BR perception and signal initiation (Li et al. 2002; Nam and Li 2002; Karlova et al. 2006; He et al. 2007; Gou et al. 2012; Santiago et al. 2013; Sun et al. 2013); ERECTA, ERL1, and ERL2 also control stomatal development (Shpak et al. 2005; Lee et al. 2012). SERK1, SERK2, BAK1, and BKK1 not only regulate BR signaling but also regulate BR-independent cell-death and root developmental pathways (He et al. 2007; Li 2010; Du et al. 2012); RPK1/TOAD2, ACR4/ALE2, GSO1/GSO2 are involved in zygotic embryogenesis (Tanaka et al. 2002; Nodine et al. 2007; Tsuwamoto et al. 2008). There are also still many secreted proteins that could be ligands for RLKs. For example, polypeptides called LUREs were found to be secreted from synergid cells for pollen tube guidance (Okuda et al. 2009), and it was proposed that their cognate RLKs are located on the tips of pollen tubes to control fertilization. However the responsible RLKs still need to be identified. Several receptor-like kinases have been found to be involved in pathogen recognition. Typically, plants detect invading pathogens by recognizing conserved signatures called Pathogen Associated Molecular Patterns, or PAMPs. RLKs directly perceiving PAMPs are called pattern recognition receptors (PRRs). FLS2 and EFR are the two best characterized PRRs, binding to the PAMPs flg22 and EF-Tu, respectively (Gómez-Gómez and Boller 2000; Zipfel et al. 2006). When the extracellular domain of a PRR binds a PAMP, a downstream innate immune response is triggered. In addition to PRRs, recent studies have also revealed that some RLKs such as BAK1 and BKK1 can act as co-receptors of FLS2 and EFR to mediate their corresponding signaling pathways (Chinchilla et al. 2007; Heese et al. 2007; Boller and Felix 2009). Other recent studies have also uncovered that some RLKs are involved in abiotic stress responses. For example, the expression of RPK1 is induced by drought, ABA, high salt and low temperature. Loss-of-function genetic analyses indicated that RPK1 is involved in ABA-related stress responses (Osakabe et al. 2005). GHR1 is another RLK which responds to ABA and H2O2 mediated stomatal movement (Hua et al. 2012). There are still numerous RLKs whose expression is induced by either biotic or abiotic stress, but their specific roles in regulating defense responses need to be characterized in the future. Genetic analyses have revealed the roles of a small fraction of RLKs. Most are yet to be functionally defined. For those whose functions are already known, the detailed molecular mechanisms are still not completely understood. One of the greatest challenges regarding RLK-mediated signaling pathways is the identification of ligands. In addition, due to functional redundancy, it is difficult to uncover the functions of many RLKs. Furthermore, some RLKs are involved in multiple signaling pathways. For example, BAK1 regulates the BR signaling pathway to promote growth (Li et al. 2002; Nam and Li 2002). BAK1 also acts as a co-receptor in FLS2- and EFR-mediated signaling pathways to induce defense responses (Chinchilla et al. 2007; Heese et al. 2007). This makes biological sense as switching on defense responses causes the reduction of growth. In fact, BAK1 may be involved in multiple pathways distinct from the ones already uncovered. An outstanding question is how BAK1 and its other co-receptors are able to regulate multiple signaling pathways, especially those leading to opposite biological consequences. Genetics, proteomics, and other novel technologies will be useful to ultimately elucidate these questions in the near future. The knowledge obtained from these studies will contribute significantly to our better understanding of the big picture of plant growth and development, and to future genetic engineering-based crop improvements for higher productivity, including better adaptations to various biotic and abiotic stresses. Jia Li Special Issue Editor Ministry of Education Key Laboratory of Cell Activities and Stress Adaptations, School of Life Sciences, Lanzhou University Lanzhou 730000, China Frans E. Tax Special Issue Editor Department of Molecular and Cellular Biology, University of Arizona, Tucson AZ 85721-0036, USA