receptor-like cytoplasmic kinases: central players in plant …biologia.ucr.ac.cr/profesores/garcia...

PP69CH10_Zhou ARI 3 April 2018 9:24

Annual Review of Plant Biology

Receptor-Like CytoplasmicKinases: Central Playersin Plant ReceptorKinase–Mediated SignalingXiangxiu Liang and Jian-Min ZhouState Key Laboratory of Plant Genomics, Institute of Genetics and Developmental Biology,Chinese Academy of Sciences, Chaoyang District, 100101 Beijing, China;email: [email protected]

Annu. Rev. Plant Biol. 2018. 69:267–99

The Annual Review of Plant Biology is online atplant.annualreviews.org

https://doi.org/10.1146/annurev-arplant-042817-040540

Copyright c© 2018 by Annual Reviews.All rights reserved

Keywords

receptor-like cytoplasmic kinases, ROS, reactive oxygen species, MAPkinases, mitogen-activated protein kinases, plant immunity, growth,development, abiotic stresses

Abstract

Receptor kinases (RKs) are of paramount importance in transmembrane sig-naling that governs plant reproduction, growth, development, and adapta-tion to diverse environmental conditions. Receptor-like cytoplasmic kinases(RLCKs), which lack extracellular ligand-binding domains, have emergedas a major class of signaling proteins that regulate plant cellular activitiesin response to biotic/abiotic stresses and endogenous extracellular signal-ing molecules. By associating with immune RKs, RLCKs regulate multipledownstream signaling nodes to orchestrate a complex array of defense re-sponses against microbial pathogens. RLCKs also associate with RKs thatperceive brassinosteroids and signaling peptides to coordinate growth, pollentube guidance, embryonic and stomatal patterning, floral organ abscission,and abiotic stress responses. The activity and stability of RLCKs are dynami-cally regulated not only by RKs but also by other RLCK-associated proteins.Analyses of RLCK-associated components and substrates have suggestedphosphorylation relays as a major mechanism underlying RK-mediatedsignaling.

267

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https://www.annualreviews.org/doi/full/10.1146/annurev-arplant-042817-040540


Contents

INTRODUCTION . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 268Overview of Plant Receptor Kinases . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 268Receptor-Like Cytoplasmic Kinases in Receptor Kinase–Regulated

Biological Processes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 269RECEPTOR-LIKE CYTOPLASMIC KINASES AS CENTRAL PLAYERS

IN PLANT IMMUNITY . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 273Immune Signaling Downstream of Diverse Pattern Recognition Receptors . . . . . . . . 273Intracellular Sensors for Pathogen Effectors . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 275

RECEPTOR-LIKE CYTOPLASMIC KINASES IN PLANT GROWTH,DEVELOPMENT, AND REPRODUCTION. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 276Sexual Reproduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 277Cell Differentiation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 278Brassinosteroid Signaling . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 278Small-Peptide-Regulated Growth and Development. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 279

RECEPTOR-LIKE CYTOPLASMIC KINASES IN ABIOTIC STRESSES . . . . . . . . 279REGULATORY MECHANISMS UNDERLYING SIGNALING MEDIATED

BY RECEPTOR-LIKE CYTOPLASMIC KINASES . . . . . . . . . . . . . . . . . . . . . . . . . . . . 280Regulation of Receptor-Like Cytoplasmic Kinases in the Receptor Complex . . . . . . . 281Ca2+ Currents During Immune Signaling . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 283Reactive Oxygen Species . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 283Mitogen-Activated Protein Kinase Cascades . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 284The Specificity of Receptor-Like Cytoplasmic Kinase–Mediated Signaling . . . . . . . . 286

CONCLUSIONS AND PERSPECTIVES. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 287

INTRODUCTION

Overview of Plant Receptor Kinases

Transmembrane signaling is crucial for nearly all aspects of plant life. Cell surface–localized recep-tors perceive extracellular signal molecules of various nature—including proteins/peptides, RNAs,classical phytohormones, reactive oxygen species (ROS), sugars, nucleotides, polysaccharides, andions. Upon perception of such molecules, these receptors transduce the signal to the cytoplasm toultimately regulate metabolism and cellular activities (21, 207, 253, 254). Perception of these sig-naling molecules allows land plants to respond to biotic and abiotic factors in the environment toestablish symbiotic relationships with beneficial microbes, activate immune responses to fend offphytopathogenic microbes, and adapt to abiotic stresses. Transmembrane signaling additionallyenables cell-cell communication to accurately control highly sophisticated fertilization processesin flowering plants, establish self-incompatibility in certain angiosperms, maintain shoot and rootapical meristems, and promote cell differentiation and cell growth.

In animals, transmembrane receptors include ion channel–linked receptors, receptor tyrosinekinases (RTKs), Toll-like receptors (TLRs), and G protein–coupled receptors (91, 106, 156).In plants, cell surface–localized receptors consist primarily of receptor-like kinases (RLKs) andreceptor-like proteins (RLPs) (39, 84, 201). RLKs contain a variable ectodomain responsible forligand binding, a single-pass transmembrane domain, an intracellular juxtamembrane domain,and a cytoplasmic kinase domain (185). RLKs in plants belong to the same group of protein

268 Liang · Zhou

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kinases as the Pelle family kinases in animals, whose members include INTERLEUKINRECEPTOR-ASSOCIATED KINASEs (IRAKs) (185). The Arabidopsis and rice genomescontain ∼610 and ∼1,100 RLKs, respectively, which account for ∼2% of the coding genes ineach species (185, 209). Approximately 75% of Arabidopsis RLKs contain both a transmembranedomain and an ectodomain. RLPs contain an ectodomain and a transmembrane domain or aglycosylphosphatidylinositol anchor but lack a kinase domain (56, 118, 182); instead, they arethought to act together with RLKs to mediate transmembrane signaling. There are ∼170 and∼90 RLPs in Arabidopsis and rice, respectively (56, 114), and an increasing number of RLK andRLP superfamily members have been shown to act as cell surface–localized receptors controllinga vast array of biological processes (20, 62, 89, 185, 209, 222). However, not all RLKs and RLPsare receptors; some act as co-receptors, scaffold proteins, or other components in the receptorcomplex (31, 112, 151, 189). RLKs confirmed as receptors are referred to as receptor kinases(RKs) in the rest of text.

Interestingly, a large portion of the RLK superfamily possesses a cytoplasmic kinase domainbut lacks an ectodomain. These members are referred to as receptor-like cytoplasmic kinases(RLCKs). There are 149 and 379 RLCKs in Arabidopsis and rice, respectively (185, 209). Onthe basis of the sequence homology, Arabidopsis and rice RLCKs are divided into 17 subgroupsand are referred to as RLCK-II and RLCK-IV–RLCK-XIX (185). Most RLCKs contain only aSer/Thr kinase domain, while others additionally contain LRR, EGF, WD40, or transmembranedomain(s) (105, 122, 209).

In this review we summarize roles of RLCKs in diverse processes in plants. We aim to discussrelationships between RLCKs and RKs and to highlight RK-mediated signaling mechanismsbrought about through studies on RLCKs.

Receptor-Like Cytoplasmic Kinases in Receptor Kinase–RegulatedBiological Processes

Plant RKs are highly analogous to animal RTKs in both structural organization and mode ofactivation. Both RKs and RTKs carry highly variable ectodomains for ligand binding, single-pass transmembrane domains, and cytoplasmic kinase domains, and both require ligand-inducedoligomerization for activation (70, 78). Additionally, both RKs and RTKs phosphorylate on ser-ine, threonine, and tyrosine residues (82, 107, 120, 154), and both undergo endocytosis and/orubiquitylation-mediated turnover to desensitize the system following activation (131, 168, 171).The RK- and RTK-mediated signaling also share downstream signaling elements such as theactivation of mitogen-activated protein kinase (MAPK) cascades and NADPH oxidase–mediatedproduction of ROS (51, 153, 205, 247).

Despite the aforementioned similarities, RK- and RTK-mediated transmembrane signalingevolved independently and use distinct mechanisms to activate downstream events. Ligand-induced dimerization of RTKs allows autophosphorylation of the kinase domain on tyrosineresidues in specific motifs to recruit and activate downstream components containing Src homol-ogy 2 (SH2) domain and phosphotyrosine binding (PTB) domains (107). Major SH2 and PTBdomain proteins include Src, phospholipase Cγ, and adaptor proteins. Whether a similar mech-anism is used by plant RKs remains unknown, and how different plant RKs regulate downstreamsignaling has been unclear until recently.

Recent advances suggest a key role of RLCKs in RK-mediated signaling (Figure 1).Consistent with this notion, many RLCKs are localized to the plasma membrane throughN-myristoylation or palmitoylation (122). RLCKs function in concert with RKs/RLPs in theregulation of plant innate immunity, adaptation to abiotic stresses, hormone signaling, sexual

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BOTRYTIS-INDUCEDKINASE1 (BIK1):a critical protein kinasethat relays signal frommultiple receptors andactivates defenses

BR SIGNALINGKINASEs (BSKs):a family of proteinsthat relay signal fromBRI1 to regulate plantgrowth

reproduction, stomatal patterning, maintenance of shoot and root meristems, differentiation ofvascular tissues, petal abscission, and other developmental processes (122, 201, 242). For instance,BOTRYTIS-INDUCED KINASE1 (BIK1) and related RLCKs interact directly with severalimmune RKs to regulate defense responses (99, 130, 132, 184, 247). BR SIGNALING KINASEs(BSKs) of the RLCK-XII subfamily directly interact with the LRR-RK BRASSINOSTEROIDINSENSITIVE1 (BRI1), the main brassinosteroid (BR) receptor, to regulate BR signalingin Arabidopsis (96, 188, 202). The Arabidopsis RLCK-VIII member MARIS (MRI) functionsdownstream of two pairs of closely related peptide hormone receptors, ANXUR1 (ANX1) andANX2 and BUDDHA’S PAPER SEALl (BUPS1) and BUPS2, to control pollen tube integrity(11, 59, 117). The Brassica M-LOCUS PROTEIN KINASE (MLPK), an RLCK, interacts withthe female determinant S-LOCUS B-LECTIN RECEPTOR KINASE (SRK) to regulate self-incompatibility (88, 149). RLCKs with reported functions are summarized in Table 1. RLCKsregulate RK- and RLP-mediated signaling not only by phosphorylating various downstreamcomponents but also by regulating the activity of receptor complexes (45, 86, 113, 132). Inaddition, both the activity and stability of RLCKs are tightly regulated (38, 116, 146, 215).

Table 1 Receptor-like cytoplasmic kinases (RLCKs) with known function

Name Species Subgroupa Associated receptorsb Function Reference(s)

BIK1 Arabidopsis VII FLS2, EFR, CERK1,PEPR1, PEPR2, BAK1BRI1

Pattern-triggered immunity,resistance to necrotrophicfungus, ethylene-induceddefenses

Negative regulation of BRsignaling

Root hair growth

28, 35, 38, 87, 113,116, 130, 132,146, 208, 247

PBL1 Arabidopsis VII FLS2, EFR, CERK1,PEPR1, PEPR2, BAK1

Pattern-triggered immunity 35, 130, 132, 164,247

PBL13 Arabidopsis VII FLS2, EFR Pattern-triggered immunity 123

BSK1 Arabidopsis XII FLS2 Pattern-triggered immunity 183

PCRK1PCRK2

Arabidopsis VII FLS2, EFR Pattern-triggered immunity 99, 187

PBL27 Arabidopsis VII CERK1 Pattern-triggered immunity 184, 229

PTI1 Tomato VIII FLS2, FLS3 Pattern-triggered immunity 175

ACIK1 Tomato VII Cf9, Cf4 Pattern-triggered immunity 170

OsRLCK185 Rice VII OsCERK1 Pattern-triggered immunity 212, 230, 232

OsRLCK176 Rice VII OsCERK1, CEBiP,OsLYP4, OsLYP6

Pattern-triggered immunity 6, 252

OsBSR1 Rice VII CEBiP, OsCERK1 Pattern-triggered immunity 49, 90

OsRLCK107OsRLCK57OsRLCK118

Rice VII OsCERK1, CEBiP, Xa21OsBRI1

Resistance to bacteriaPattern-triggered immunityNegative regulation of BRsignaling

115, 252

BSK1 Arabidopsis XII FLS2 Pattern-triggered immunity 183

OsBSK1–2 Rice XII CEBiP, OsCERK1 Pattern-triggered immunity 216

PBL2 Arabidopsis VII ZAR1 (NLR) Effector-triggered immunity 69, 213, 247

RKS1 Arabidopsis XII ZAR1 (NLR) Effector-triggered immunity 213

(Continued )


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Table 1 (Continued )


RIPK Arabidopsis VII RPM1 (NLR)FER

Effector-triggered immunityStomatal defenseRoot development

34, 103, 126, 228

ZED1 Arabidopsis XII ZAR1 (NLR) Effector-triggered immunity 8, 109

ZRK3 Arabidopsis XII ZAR1 (NLR) Effector-triggered immunity 178

CRCK3 Arabidopsis IV SUMM2 (NLR) Effector-triggered immunity 141

Pto Tomato NG Prf (NLR) Effector-triggered immunity 55, 98, 136, 152,176, 204

Fen Tomato NG Prf (NLR) Effector-triggered immunity 1, 152, 169, 227

CaPIK Pepper VII Unknown Resistance to bacteria 92–95

OsRLCK102 Rice VII Xa21OsBRI1

Resistance to bacteriaNegative regulation of BRsignaling

217

Stpk-V Wheat NG Unknown Resistance to fungal pathogen 25

MtSpk Medicago NG Unknown Rhizobial symbiosisestablishment

4

NRRB Rice IX Unknown Negative regulation ofresistance to bacteria

67

RLCK-VI_A3 Arabidopsis VI Unknown Resistance to fungal pathogen 43, 145, 167

HvRBK Barley VI Unknown Resistance to fungal pathogen 80

BSK1BSK3BSK4BSK5BSK6BSK7BSK8

Arabidopsis XII BRI1 BR signaling 64, 96, 188, 202

CDG1 Arabidopsis VII BRI1 BR signaling 95, 150

OsBSK3 Rice XII OsBRI1 BR signaling 244

SSP Arabidopsis XII Unknown Embryonic patterning 9, 37

LIP1LIP2

Arabidopsis VII Unknown Pollen tube guidance 127

ZmPTI1 Maize RLCK-VIII

Unknown Pollen activity 77

MRI Arabidopsis VIII ANX1, ANX2, FER Pollen tube integrity and roothair growth

11, 117

MLPK Brassica NG SRK Self-incompatibility 88, 149

CST Arabidopsis VII HAE1, BAK1 Inhibition of organ abscission 20

ARCK1 Arabidopsis NG CRK36 Negative control of ABAresponse and osmotic stress

200

Esi47 Barley VII Unknown Response to salt stress and ABA 181

OsRLCK253 Rice NG Unknown Abiotic stress tolerance 60

OsGUDK Rice VII Unknown Grain yield and droughttolerance

162, 163

(Continued )

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Table 1 (Continued )


GsRLCK Soybean NG Unknown Salt and drought tolerance 194

CRLK1 Arabidopsis NG Unknown Cold tolerance 234, 236

AtPTI1–2AtPTI1–4

Arabidopsis RLCK-VIII

Unknown Oxidative stress signaling 5, 54

OsPSTOL1 Rice NG Unknown Response to phosphorusdeficiency

57

CRPK1 Arabidopsis NG Unknown Negative regulation of coldtolerance

129

GsCBRLK Soybean IV Unknown ABA response and salt tolerance 233

aSubgroups are classified according to Arabidopsis and rice RLCKs (185). RLCKs specific for other lineages and newly assigned Arabidopsis RLCKs are notgrouped (NG).bReceptors refer to receptor kinases (RKs), receptor-like kinases (RLKs), receptor-like proteins (RLPs), or nucleotide-binding leucine-rich repeatdomain-containing receptors (NLRs) (the latter in parenthesis).

BRASSINO-STEROIDINSENSITIVE1(BRI1): the receptorfor a steroid hormonethat regulates growthin plants

ANXUR1 (ANX1)and ANX2: a pair ofclosely relatedreceptors for severalRALFs; regulatepollen tube growth

Nucleotide-bindingleucine-rich repeatdomain–containingreceptors (NLRs):a class of cytoplasmicimmune receptorsshared by both plantsand animals

The involvement of RLCKs in plant RK signaling is somewhat analogous to the involvementof cytoplasmic kinases Src and IRAKs in animal RTK- and TLR-mediated signaling, respec-tively (Figure 1) (91, 107). However, analyses of RK-mediated immune signaling, BR signaling,and stomatal patterning pathways have uncovered unique mechanisms in plant transmembranesignaling. In this review, we highlight our current understanding of the roles and regulatory mech-anisms by which RLCKs regulate plant biology, discuss similarities and differences among RLCKsinvolved in these processes, and draw comparisons with animal transmembrane signaling.

RECEPTOR-LIKE CYTOPLASMIC KINASES AS CENTRAL PLAYERSIN PLANT IMMUNITY

Although plants do not have specialized immune cells or an adaptive immune system, they dopossess an immune system that is highly analogous to the animal innate immune system, whichrelies on both cell surface and cytoplasmic immune receptors (41). An increasing number ofRKs and RLPs have been shown to serve as pattern recognition receptors (PRRs), which mon-itor the apoplast for immunogenic molecular patterns derived from microbes or plants that arespecifically released during potential pathogen infection (39, 68, 201, 242). The perception ofthese immunogenic patterns triggers immune signaling characterized by transient calcium influx,ROS production, activation of MAPKs and CALCIUM-DEPENDENT PROTEIN KINASEs(CPKs), and transcriptional reprogramming (39, 114, 161), and culminates in an array of defensesrestricting pathogen progression. Successful pathogens also deploy a variety of effector proteinsin the apoplast or cytoplasm of the host plant to assist infection and colonization. It is now wellestablished that many of these effectors do so by evading host recognition or blocking immunesignaling (24, 44). To counter effector-mediated pathogenesis, plants have evolved intracellularimmune receptors, which are nucleotide-binding leucine-rich repeat domain–containing receptors(NLRs), to detect cytoplasmic effector activity and trigger powerful immune responses (85).

Immune Signaling Downstream of Diverse Pattern Recognition Receptors

Plant genomes encode an enormous number of PRRs, which can be classified into different cate-gories on the basis of ectodomain sequence, the largest of which carry leucine-rich repeat (LRR)ectodomains. The LRR-RK and LRR-RLP classes of PRRs recognize plant- or pathogen-derived


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SOMATICEMBRYOGENESISRECEPTORKINASEs (SERKs):a small family ofproteins, includingBAK1; commonco-receptors

flg22: a 22-amino-acid N-terminalsequence conserved inmultiple bacterialflagellin; flg22 peptideis sensed by FLS2

BRI1-ASSOCIATEDKINASE1 (BAK1):a common co-receptorthat teams up withmultiple receptors toperceive externalsignals

FLAGELLINSENSING2 (FLS2):the plant receptor thatsenses the bacterialflagellin protein

CHITINELICITORRECEPTORKINASE1 (CERK1):a common co-receptorfor microbe-derivedoligosaccharidesincluding chitin andpeptidoglycan

PBS1-LIKE (PBL):a family of proteinsrelated to BIK1

peptide epitopes, whereas RKs and RLPs with lysine motif (LysM)-type ectodomains perceivechitin oligosaccharides and/or peptidoglycan. Additionally, S-lectin RKs perceive extracellularnucleotides and bacterial lipopolysaccharides (33, 166). Regardless of ectodomain type, PRRsare assembled complexes that are dynamically regulated upon ligand binding. All PRRs con-taining LRR ectodomains require members of SOMATIC EMBRYOGENESIS RECEPTORKINASEs (SERKs), a small class of LRR-RLKs, as co-receptors, while LRR-RLP PRRs require anadditional LRR-RLK co-receptor, SUPPRESSOR OF BIR1–1 (SOBIR1), also known as EVER-SHED (EVR) (20, 58, 118). SOBIR1 and LRR-RLPs constitutively interact and are proposed toform bipartite RKs, which could then recruit SERKs upon ligand perception (118). As with RTKs,ligand perception leads to dimerization or oligomerization of receptors and co-receptors, which isthought to bring the cytoplasmic kinase domains into the proximity necessary for transphospho-rylation (70, 78, 107). For instance, the Arabidopsis LRR-RKs FLAGELLIN SENSING2 (FLS2)and ELONGATION FACTOR-TU (EF-Tu) RECEPTOR (EFR) bind epitopes from bacterialflagellin (flg22) and EF-Tu (elf18) to recruit the SERK family member BRI1-ASSOCIATED KI-NASE1 (BAK1/SERK3) and form active receptor complexes (31, 75). Similarly, the closely relatedArabidopsis LRR-RKs PEP RECEPTORs (PEPRs) PEPR1 and PEPR2 bind PLANT ELICITORPEPTIDEs (Peps) and recruit BAK1 to form an active receptor complex (100, 211). The Ara-bidopsis LysM-RK LYSINE MOTIF RECEPTOR KINASE5 (LYK5) and the rice LysM-RLPCHITIN ELICITOR-BINDING PROTEIN (CEBiP) bind chitin and recruit the co-receptorCHITIN ELICITOR RECEPTOR KINASE1 (CERK1), a LysM-RLK (26, 89, 128, 143, 211).Chitin binding by the LYK5 or CEBiP receptors leads to dimerization of the CERK1 co-receptor,which is required for immune activation (128).

The RLCK-VII family member BIK1 was initially shown to be required for disease resistanceto the fungal pathogen Botrytis cinerea (208); however, how BIK1 and other members of this RLCKfamily participate in immune signaling was not immediately clear. Subsequent work demonstratedthat BIK1 and its closest homolog, PBS1-LIKE1 (PBL1), directly interact with FLS2 and arerequired for FLS2-mediated defenses (132, 247). The bik1 and pbl1 mutants are diminished inflg22-induced responses, including calcium influx, ROS burst, actin filament bundling, callosedeposition, stomatal closure, and seedling growth inhibition (76, 113, 130, 132, 164, 247). BIK1and PBL1 are required not only for immune signaling mediated by FLS2 but also for immuneresponses mediated by other PRRs including LYK5, PEPR1, PEPR2, and EFR (130, 132, 247).The interaction of BIK1 and PBL1 with PEPR1 is particularly important for ethylene-induceddisease resistance (101, 130), as ethylene is known to accumulate in response to infection by diversepathogens and to induce the expression of ProPep genes, which encode Pep precursors. TOMATOPROTEIN KINASE1b (TPK1b), another RLCK-VII member in tomato, also mediates ethylene-induced responses and disease resistance to B. cinerea infection and Manduca sexta infestation (2).In rice, a number of RLCKs including OsRLCK185 and OsRLCK176 mediate pattern-inducedimmune responses (Table 1).

Consistent with an important role of BIK1 and PBL1 in diverse pattern-triggered immunity,Pseudomonas syringae effector AvrPphB and Xanthomonas campestris effector AvrAC target BIK1 andPBL1 to inhibit pattern-triggered immune responses (52, 247). In particular, targeting of BIK1is required for the virulence function of AvrAC (52, 213), as AvrAC uridylylates the conservedphosphorylation sites in the activation loop of BIK1, thereby inhibiting BIK1 kinase activity andPRR-mediated immune signaling.

The RLCK-VII family contains 46 members, many of which may also function in PRR-mediated immune signaling. Although transgenic expression of AvrAC and AvrPphB, which targetmultiple RLCK-VII members, strongly impairs pattern-triggered immunity, mutations of individ-ual RLCK-VII members only modestly dampen immunity (52, 247). These observations suggest

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that multiple RLCK-VII members act redundantly downstream of PRRs. Indeed, the closelyrelated RLCK-VII members PATTERN-TRIGGERED IMMUNITY COMPROMISEDRECEPTOR-LIKE CYTOPLASMIC KINASE1 (PCRK1) and PCRK2 function downstreamof FLS2 to regulate accumulation of salicylic acid, a key defense hormone (99). The pcrk1 pcrk2double mutant is impaired in pathogen-induced SAR DEFICIENT1 (SARD1), CAM-BINDINGPROTEIN 60-LIKE G (CBP60g), and ISOCHORISMATE SYNTHASE1 (ICS1) expression andis compromised in resistance to P. syringae (99). SARD1 and CBP60g are major transcriptionfactors controlling the expression of ICS1, which encodes an enzyme responsible for salicylicacid biosynthesis (193). Like BIK1, PCRK1 and PCRK2 interact with FLS2, and flg22 treatmenttriggers PCRK2 phosphorylation (99). Likewise, the pepper RLCK-VII member PATHOGEN-INDUCED PROTEIN KINASE 1 (CaPIK1) is required for X. campestris–induced salicylic acidaccumulation (92).

RLCKs involved in PRR-mediated immune signaling are not limited to the RLCK-VII family.The RLCK-XII member BR SIGNALING KINASE1 (BSK1) also interacts with FLS2 and isrequired for flg22-triggered ROS production (183). Mutations in BSK1 result in reduced freesalicylic acid levels upon Golovinomyces cichoracearum and P. syringae infection and reduced diseaseresistance (183). Given that FLS2 is a PRR for bacterial flagellin, it is unlikely to contribute todisease resistance to fungal pathogens, and as different PRRs are believed to trigger immuneresponses through similar mechanisms, BSK1 may also act downstream of fungal PRRs such asLYK5 and CERK1, a possibility that remains to be tested.

While RLCKs are clearly important for RK-mediated immune signaling, their possible rolesin immune signaling downstream of RLP-type PRRs remains unknown. Given that these RLPsact together with RLKs, such as SOBIR1, some RLCKs may associate with these RLKs dur-ing RLP-mediated immune signaling. Indeed, the tomato RLCK AVR9/CF-9 INDUCED KI-NASE 1 (ACIK1) plays a role in disease resistance mediated by the LRR-RLP resistance toCLADOSPORIUM FULVUM 4 (Cf4) and Cf9, although whether ACIK1 exists in the Cf4/9receptor complexes remains unknown (170).

Intracellular Sensors for Pathogen Effectors

For historical reasons, the study of NLR-mediated effector-triggered immunity received greaterattention than did pattern-triggered immunity in the 1990s, and much effort was directed to-ward the cloning of RESISTANCE (R) genes, which are now well known to generally en-code NLRs. Unexpectedly, the first gene to be isolated that mediates effector-triggered im-munity instead encodes the tomato RLCK Pto, so named for its resistance to P. syringae pv.tomato strains carrying the effector AvrPto (136). A typical NLR, PTO RESISTANCE ANDFENTHION SENSITIVITY (Prf ), was also identified as required for AvrPto-triggered im-munity (172). Subsequent analyses showed that Prf interacts with Pto (148), while the lat-ter physically interacts with AvrPto to enable indirect detection of AvrPto by Prf (98, 176,204). Interestingly, Prf also confers resistance to P. syringae strains carrying a truncated ef-fector AvrPtoB that is unrelated to AvrPto (169). This recognition required FENTHIONSENSITIVITY (Fen), an RLCK with a high degree of similarity to Pto. In both cases, Ptoand Fen act as sensors for the effectors, rather than signal transducers, in Prf-mediated immunity.

In addition to Pto and Fen, several other RLCKs also sense effectors and activate NLR-mediated immunity. The Arabidopsis NLR protein RESISTANCE TO PSEUDOMONASSYRINGAE5 (RPS5) confers resistance to P. syringae carrying the effector protein AvrPphB (223),which is a cysteine protease that cleaves the RPS5-associated RLCK-VII member PBS1 (180). Thecleavage of PBS1 leads to a conformational change that triggers RPS5 activation and immunity(3, 180, 197, 223). The P. syringae effector HopAI1 directly targets MAP KINASEs (MPKs) to


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block plant immunity (248). The NLR protein SUPPRESSOR OF MKK1 MKK2, 2 (SUMM2)indirectly detects MPK4 inactivation and triggers immunity (251). A recent study showed thatCALMODULIN-BINDING RECEPTOR-LIKE CYTOPLASMIC KINASE3, an RLCK-IVmember, interacts with SUMM2 and is phosphorylated by MPK4, suggesting that SUMM2monitors the phosphorylation status of CALMODULIN-BINDING RECEPTOR-LIKECYTOPLASMIC KINASE3 to indirectly sense HopAI1 (250).

The Arabidopsis NLR protein HOPZ-ACTIVATED RESISTANCE1 (ZAR1) associateswith multiple ZAR1-ASSOCIATED KINASEs (ZRKs) including HOPZ-ETI-DEFICIENT1(ZED1), ZRK3, and RESISTANCE RELATED KINASE1 (RKS1), all belonging to the RLCK-XII subfamily (109, 178, 213). Each of the aforementioned ZRKs acts as a sensor for a distinctpathogen effector and triggers ZAR1-dependent immunity. Thus, the ZAR1-ZED1 and ZAR1-ZRK3 complexes confer resistance to P. syringae carrying the effectors HopZ1a and HopF2,respectively (109, 178), whereas ZAR1-RKS1 confers resistance to X. campestris carrying AvrAC(213). These findings critically illustrate how different RLCKs act as sensors for different pathogeneffectors to expand the recognition spectrum of a single NLR. ZED1 and ZRK3 may be directsensors for HopZ1a and HopF2, respectively (109, 178). Interestingly, the AvrAC-triggered im-munity additionally requires PBL2, an RLCK-VII member (69, 213). The uridylylation of PBL2on conserved phosphosites in the activation loop leads to the recruitment of PBL2 to the pre-formed ZAR1-RKS1 complex and activation of immunity (213). Here, RKS1 acts as an adaptor,whereas PBL2 acts as a sensor for AvrAC. The involvement of two RLCKs in sensing an effectormay further expand the recognition spectrum of the NLR protein.

Not all NLR-associated RLCKs act as direct sensors for effectors. Arabidopsis NLRRESISTANCE TO PSEUDOMONAS SYRINGAE PV MACULICOLA1 (RPM1) detects P.syringae effector AvrB by monitoring the phosphorylation status of RPM1-INTERACTING4(RIN4). Although AvrB does not appear to possess kinase activity itself, it induces RIN4 phos-phorylation at Thr166 in the presence of the RLCK-VII member RPM1-INDUCED PROTEINKINASE (RIPK) to trigger RPM1-mediated immunity (34, 126). Thus, RIPK acts as a specificmodifier of the sensor protein RIN4 to assist AvrB recognition by RPM1.

The aforementioned observations indicate that RLCKs have been frequently adopted as sensorsor modifiers of sensors of pathogen effectors to regulate NLR-mediated immunity, suggesting thatRLCKs are uniquely important during host-pathogen coevolution. This is consistent with thenotion that plant RLCKs and associated proteins are frequent pathogenesis targets of pathogeneffectors (40, 232, 247). This has driven coevolution in the host plant, resulting in the associationof many NLRs with RLCKs to indirectly monitor effector activity. Indeed, AvrPto, AvrPtoB,AvrPphB, and AvrAC all suppress pattern-triggered immunity and/or are required for virulenceby targeting the kinase domain of PRRs or RLCKs (29, 42, 52, 61, 179, 226, 247).

RECEPTOR-LIKE CYTOPLASMIC KINASES IN PLANT GROWTH,DEVELOPMENT, AND REPRODUCTION

Short- and long-distance communication is crucial for coordination among different cells andorgans during plant growth and development, cell fate determination, and reproduction. Theclassical phytohormone BR and diverse small signaling peptides are perceived by RKs and are ofprofound importance to plant biology. Plants encode more than 1,000 potential secreted peptides,an increasing number of which are being found to act as peptide hormones regulating diversebiological functions (16, 245). While mechanisms by which RKs and RLPs perceive these signalsare well established (70, 78), how these receptors transduce extracellular signals to complex cellularand physiological responses remains poorly understood. In several cases, RLCKs participate in

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FERONIA (FER):a receptor for severalRALFs; regulatesmultiple biologicalprocesses in plants

RAPIDALKALINIZATIONFACTORs (RALFs):a class of peptidehormones that causeextracellularalkalinization andregulate diversebiological processes inplants

RK-mediated regulation of plant growth, development, and reproduction, suggesting that RLCKsare adopted as common signaling modules in transmembrane signaling.

Sexual Reproduction

Successful sexual reproduction in angiosperms is governed by a complex fertilization processtermed double fertilization, during which a female gametophyte joins with two male gametes.Upon landing and germinating on the stigma, a pollen grain forms a pollen tube that penetratesthe style and grows toward the female gametophyte. The tip of the pollen tube accurately entersthe ovule, where it bursts to release the two sperms. In this process, the female gametophyteproduces signals to actively attract and guide the growth of the pollen tube. It is now known thatpollen tube guidance is controlled by ovule-derived, cysteine-rich signal peptides, such as EGGAPPARATUS 1 (EA1) in maize and LUREs in Arabidopsis (155). A search of components involvedin LURE perception identified two close RLCK-VII members, LOST IN POLLEN TUBEGUIDANCE1 (LIP1) and LIP2 required for LURE1-induced pollen tube growth (127). The lip1lip2 double mutant exhibits a partial loss of pollen tube guidance, suggesting that additional RLCKsare also involved (127). Because they lack an ectodomain, LIP1 and LIP2 are postulated to func-tion in concert with receptors to facilitate signal transduction. Recently, two independent groupsidentified LRR-RKs POLLEN-SPECIFIC RECEPTOR-LIKE KINASEs (PRKs), MALEDISCOVERER1 (MDIS1), and MDIS1-INTERACTING RECEPTOR-LIKE KINASEs(MIKs) as likely receptors for LURE1 (199, 218). Whether and how LIP1 and LIP2 functiondownstream of the aforementioned receptors to regulate pollen tube growth remain to beelucidated.

In addition to guided pollen tube growth, the integrity of the pollen tube is also tightly regu-lated both before and upon arrival at the ovule. The Catharanthus roseus RLK1-like (CrRLK1L)subfamily RLKs, including THESEUS1, FERONIA (FER), ANX1, ANX2, BUPS1, and BUPS2,are characterized by malectin-like domains within their ectodomains and are thought to be sen-sors of cell wall integrity (30, 124). Advances in recent years indicate that they are receptors for aclass of peptide hormone called RAPID ALKALINIZATION FACTORs (RALFs) (59, 73, 189).ANX1, ANX2, BUPS1, and BUPS2 are pollen tube–residing receptors for pollen-derived RALF4and RALF19. This perception prevents premature rupture and ensures growth of the pollen tube(13, 59, 144). Interestingly, the ovule-derived RALF34 can compete with RALF4 and RALF19for binding to these receptors and induce pollen tube rupture. An independent study suggestedthat LEUCINE-RICH REPEAT EXTENSIN proteins (LRXs) also play a role in the perceptionof RALF4 and RALF19 and the control of pollen tube growth (138). A forward genetic screenidentified MARIS (MRI), an RLCK-VIII member, as a suppressor for anx1 anx2. Mutation ofArg240 to Cys in the activation loop of MRI restores the defect of pollen tube growth in the anx1anx2 double mutant (11), while the mri loss-of-function mutant phenocopies the anx1 anx2 mutant(117). These results indicated that MRI acts downstream of the ANX-BUPS receptor complexto prevent pollen tube burst, whereas the R240C substitution constitutively activates MRI andpollen tube rupture. FER is required for pollen tube reception, but the underlying mechanism isunknown (46, 50). Given that FER is a receptor for multiple RALFs (73, 189), it is plausible thatFER perceives the pollen tube by sensing pollen tube–derived RALF(s) (73).

Certain angiosperms actively promote outcrossing by deploying the self-incompatibility sys-tems to reject self-pollen. In Brassica, self-incompatibility recognition is controlled mainly bythe pollen coat–derived cysteine-rich peptide S-LOCUS PROTEIN 11 (SP11) and stigmatic S-LOCUS B-LECTIN RECEPTOR KINASE (SRK) (198). The S-LOCUS GLYCOPROTEIN(SLG) shares similarity with the SRK extracellular domain and is required for self-incompatibility(198). SRK forms a complex with SLG to perceive SP11 and mediate self-incompatibility


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YODA (YDA):a MAP kinase kinasekinase that regulatesthe development ofguard cells in plants

signaling (198). ARM REPEAT CONTAINING 1 (ARC1), an E3 ligase, interacts with SRKto positively regulate self-incompatibility (65). ARC1 is proposed to ubiquitinate and degradeEXOCYST SUBUNIT EXO70 FAMILY PROTEIN A1 and possibly other unknown compat-ibility factors to promote incompatibility (173, 191). The RLCK MLPK is a positive regulatorof self-incompatibility (149). MLPK interacts with SRK and ARC, and both SRK and MLPKcan phosphorylate ARC (88). Thus, ARC and MLPK are considered major signal transducersdownstream of the SRK receptor. Precise mechanisms by which MLPK and ARC regulate self-incompatibility remain unknown.

Cell Differentiation

Cell differentiation allows a plant to generate different cell types, tissues, and organs with spe-cialized functions. Signaling peptides and RKs/RLPs play a central role in the determination ofdiverse cell types. For instance, the LRR-RK TDIF RECEPTOR/PHLOEM INTERCALATEDWITH XYLEM (TDR/PXY) perceives the peptide TRACHEARY ELEMENTS DIFFEREN-TIATION INHIBITORY FACTOR (TDIF) to control the differentiation of procambial cellsinto tracheary elements (246). The receptor complex composed of LRR-RK ERECTA (ER),SERKs, and LRR-RLP TOO MANY MOUTH (TMM) (186) perceives members of the EPI-DERMAL PATTERNING FACTOR (EPF) and EPF-LIKE (EPFL) family of secreted cysteine-rich peptides to regulate stomatal patterning, which is achieved through a series of asymmetric celldivisions (71, 72, 81, 192). Similarly, the small cysteine-rich peptide EMBRYO SURROUNDINGFACTOR1 (ESF1) controls embryonic patterning defined by asymmetric division of a zygote cell,giving rise to a large basal cell and a small apical cell; these further divide to generate an embryoand a suspensor, respectively (37). Although the corresponding receptor for the ESF1 peptide hasnot been discovered, a recent study showed that the LRR-RLK ZYGOTIC ARREST1 is requiredfor early embryogenesis (241).

In Arabidopsis, embryonic patterning and stomatal patterning share a MAPK cascade composedof MAPK kinase kinase (MAP3K) YODA (YDA), MAPK kinases (MAP2Ks) MKK4 and MKK5,and MAPKs MPK3 and MPK6 (10, 133). This MAPK cascade positively regulates embryonicpatterning and negatively regulates stomatal patterning. Loss of YDA renders the basal daughtercell unable to differentiate into the embryonic suspensor and increases stomatal density (10, 133).The mpk3 mpk6 double mutant is embryonic lethal, indicating that MPK3 and MPK6 are essentialfor embryonic patterning (214). SHORT SUSPENSOR (SSP), an RLCK-XII member, functionsupstream of YDA to regulate embryonic patterning (9). SSP transcripts are produced in spermcells but translated in the zygote and endosperm. The ssp loss-of-function mutant phenocopiesyda mutants in embryonic patterning. Interestingly, ectopic expression of SSP in leaf epidermismimics the stomatal patterning phenotype caused by a hyperactive YDA, suggesting that SSP orSSP-like RLCKs function downstream of the ER receptor complex to regulate YDA in stomatalpatterning (9).

Brassinosteroid Signaling

As mentioned above, BRs are an important class of phytohormone regulating a wide range ofprocesses including root growth, flowering, cell elongation, senescence, and stress responses (97).The Arabidopsis LRR-RK protein BRI1 is the major receptor for BRs, and bri1 mutants are BR-insensitive and exhibit severe growth defects including dwarfism and delayed flowering (36, 74,110). Genetic, biochemical, and structural studies established BAK1 and SERK1 as co-receptorsfor BR perception (112, 151, 174, 195). Upon BR perception, BRI1 and BAK1/SERK1 interactand transphosphorylate each other to form an active receptor complex (220).

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Subsequent forward genetic screens and biochemical studies uncovered key components inBR signaling including three RLCK-XII members, BSK1, BSK2, and BSK3; an RLCK-VIImember, CONSTITUTIVE DIFFERENTIAL GROWTH1 (CDG1) (95, 150, 202); the pro-tein phosphatase BRI-SUPPRESSOR1 (BSU1); GSK3/Shaggy-like kinase BR-INSENSITIVE2(BIN2); and two homologous transcription activators, BRASSINAZOLE-RESISTANT1 (BZR1)and BRI1-EMS-SUPPRESSOR1 (BES1) (96, 97, 111, 147, 203, 239). CDG1 and BSKs interactwith BRI1 and function as the signal transducers in BR signaling (95, 96). While the initial reversegenetic analysis on individual BSKs suggested a relatively minor role in BR signaling (202), a sub-sequent study of higher-order bsk mutants supported that BSKs collectively play a prominent rolein BR signaling (188). The current model suggests a linear pathway from BR perception to tran-scriptional control of BR response genes (219). In the absence of BR, BIN2 inhibits BR responsegene expression by phosphorylating BZR1 and BES1 (221, 239). Upon BR perception, BRI1phosphorylates Ser423 to activate CDG1, which then phosphorylates BSU1 (95). The phosphor-ylation activates BSU1, which then dephosphorylates BIN2, resulting in the derepression of BRresponse genes (95–97). Upon phosphorylation by BRI1, BSKs also interacted with and activatedBSU1 (96). However, other studies suggested that the Arabidopsis BSKs are inactive kinases (9, 95,188). The precise mechanism by which BSKs regulate BR signaling awaits further investigation.

Small-Peptide-Regulated Growth and Development

In addition to a role in pollen tube reception, FER regulates numerous other biological processesincluding seedling growth, root hair growth, hormone and stress responses, and immunity (47, 50,66, 73, 134, 189, 240). The activation of FER by RALFs leads to phosphorylation and inactivationof H+-ATPase AHA2, consequently inhibiting proton transport, inducing extracellular alkalin-ization, and inhibiting root hair growth (73). A recent study showed that the RLCK-VII memberRIPK is required for RALF1 signaling and functions downstream of FER to regulate primary rootgrowth and root hair growth (45). Interestingly, RIPK and FER interact and transphosphorylateeach other upon RALF treatment, suggesting that RIPK regulates the activity of FER. The RLCKMRI that controls pollen tube integrity also plays a role in FER-regulated root hair growth, asthe mri loss-of-function mutant shows defects in root hair growth (117), and overexpression ofthe MRIR240C mutant partially rescues the defect of fer in root hair growth (11).

Abscission is a programmed developmental process in which plants shed unwanted organs. A se-ries of genetic and biochemical studies revealed that Arabidopsis floral organ abscission is controlledby a signaling pathway consisting of a secreted peptide, INFLORESCENCE DEFICIENT INABSCISSION (IDA); two closely related LRR-RKs, HAESA (HAE) and HAESA-LIKE2 (HSL2);and a MAPK cascade composed of an unknown MAP3K, the MAP2Ks MKK4 and MKK5, andthe MPKs MPK3 and MPK6 (22, 32, 83, 190). HAE and HSL2 are the receptors for IDA, whichdepend on SERKs as co-receptors (23, 140). IDA rapidly triggers the interaction and transphos-phorylation between HAE and SERKs (140). NEVERSHED (NEV), an ADP-ribosylation factorGTPase-activating protein, was identified in a screen for mutants defective in floral shedding.NEV is localized to the trans-Golgi network and endosomes and likely regulates vesicle traffick-ing (119). A forward genetic screen for nev suppressors identified negative regulators of floralorgan abscission SOBIR1/EVR and the RLCK-VII member CAST AWAY (CST) (20, 63, 108).Importantly, CST interacts with both HAE and SOBIR1/EVR, suggesting that CST links theRKs to downstream signaling (20).

RECEPTOR-LIKE CYTOPLASMIC KINASES IN ABIOTIC STRESSES

Adaptation to abiotic stresses including heat, low temperature, drought, and salinity is crucial forthe survival of plants in adverse environments (253). While less characterized than their roles in


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immunity, reproduction, and development, a major role of RLKs in plant responses to variousabiotic stresses has been suggested in recent genetic and transcriptomic studies (135, 159). Cellsurface–localized receptors are unlikely to directly sense temperature, drought, or ion homeo-stasis, and instead RLKs likely perceive secondary signals generated during abiotic stresses orparticipate in the regulation of adaptive responses that reshape stomatal morphology or vascu-lar structure. For example, the Arabidopsis LRR-RLK RECEPTOR-LIKE KINASE1 (RPK1) isrequired for full sensitivity to the hormone abscisic acid (ABA) and is required for ABA-inducedsenescence (104, 157, 158), while the LRR-RLK GUARD CELL HYDROGEN PEROXIDE-RESISTANT1 (GHR1) is required for ABA- and H2O2-induced stomatal closure (79). In addition,several cysteine-rich RLKs (CRKs) have been implicated in the generation and/or perception ofROS signals and shown to be required for plant responses to abiotic stresses (15, 19).

Multiple lines of evidence indicate that RLCKs play an important role in plants’ adaptationto abiotic stresses. Among the 376 rice RLCKs, 86 are differentially expressed under cold, salt,and dehydration conditions (209). Similarly, the Arabidopsis RLCK CALMODULIN-BINDINGRECEPTOR-LIKE CYTOPLASMIC KINASE1 is induced at the transcriptional level undermultiple stress conditions including cold, salt, H2O2, and ABA (235). Esi47, a homolog of Ara-bidopsis PCRK1 in wheatgrass Lophopyrum elongatum, is highly induced by salt stress and ABA (181).In rice, RLCK253 was identified as an interacting protein of STRESS-ASSOCIATED PROTEIN1 (SAP1), an A20/AN1 zinc-finger domain-containing protein conferring abiotic stress tolerancein plants. OsRLCK253 interacts with SAP1 and its homolog SAP11 at the plasma membrane,nuclear membrane, and nuclei. Overexpression of OsRLCK253 in Arabidopsis increases toleranceto salt and drought stresses through an unknown mechanism (60). The rice RLCK GROWTHUNDER DROUGHT KINASE (GUDK) is required for grain yield under drought and normalwater conditions. The gudk mutant exhibits defects in responses to salt stress, osmotic stress, andABA. In vitro assays showed that GUDK interacts with and phosphorylates OsAP37, a transcrip-tional factor involved in drought tolerance (162, 163). GsRLCK, an RLCK from wild soybeanGlycine soja, is highly induced by salt, alkali, drought, and ABA. Overexpression of GsRLCK inArabidopsis leads to increased tolerance to drought and salt stresses (194).

A recent report showed that COLD-RESPONSIVE PROTEIN KINASE1 (CRPK1) is as-sociated with the plasma membrane and negatively regulates cold tolerance (129). Upon coldtreatment, CRPK1 phosphorylates 14-3-3 proteins, and the latter translocate into the nucleus todestabilize COLD-RESPONSIVE C-REPEAT-BINDING FACTORs (CBFs), which are keytranscription factors promoting cold tolerance (129). This exciting finding suggests that low tem-peratures, either directly or indirectly, can be sensed by a cell surface receptor that then regulatesdownstream signaling through CRPK1.

How the majority of the reported RLCKs regulates abiotic stresses remains unknown,but the Arabidopsis ABA- AND OSMOTIC STRESS-INDUCIBLE RECEPTOR-LIKECYTOPLASMIC KINASE1 (ARCK1) interacts with CRK36 to regulate responses to osmoticand ABA stresses. Both the arck1 mutant and CRK36 RNAi transgenic lines showed reduced tol-erance to osmotic and ABA stresses. Further study revealed that CRK36 phosphorylates ARCK1and regulates downstream stress-responsive genes (200). Whether other stress-regulated RLCKsare similarly linked to RLKs in abiotic stress adaptation remains to be shown.

REGULATORY MECHANISMS UNDERLYING SIGNALING MEDIATEDBY RECEPTOR-LIKE CYTOPLASMIC KINASES

Recent advances in the analysis of RLCKs, particularly those associated with immune RKs, areshedding light on the mechanisms by which this important class of signaling proteins regulates

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EXTRA-LARGEGTP-BINDINGPROTEINs (XLGs):noncanonical Gαsubunits ofheterotrimeric Gproteins, whichcontain an extension inthe N terminus

PLANT U-BOX25(PUB25) and PUB26:a pair of closely relatedE3 ligases in plantsthat catalyze proteinubiquitination

transmembrane signaling. It is now apparent that RLCKs are recruited to the kinase domain ofreceptors or co-receptors to regulate downstream components through phosphorylation. Emerg-ing evidence suggests that RLCKs regulate common signaling nodes such as ROS productionand MAPK cascades and are subject to complex regulation at the level of kinase activity and sta-bility (38, 116, 132, 146, 215, 229, 232, 247). The identification and characterization of RLCKsubstrates are uncovering a biochemical basis of transmembrane signaling in plants.

Regulation of Receptor-Like Cytoplasmic Kinases in the Receptor Complex

Existing evidence indicates that the majority of plant RLCKs studied to date interact with RKsin the resting state. Following receptor activation by the ligand, RLCKs become phosphorylatedand dissociate from the RKs. This is true for both BRI1-BSK/CDG1 and FLS2-BIK1/PBL in-teractions (95, 202, 247). One exception to this is the interaction between RIPK and FER, whichis instead induced by RALF1 (45) and enables cross-phosphorylation between FER and RIPK,suggesting a role of RIPK in the activation of the FER receptor complex. The association ofBIK1/PBLs with FLS2 may also contribute to the phosphorylation and activation of the FLS2-BAK1 receptor complex, as it has been shown that BIK1 and BAK1 can transphosphorylate eachother in vitro (132).

The phosphorylation by RKs or co-receptors is essential for RLCK-mediated signaling. Forinstance, BAK1 phosphorylates BIK1 at Tyr243 and Tyr250, and these phosphosites are requiredfor immune function of BIK1 (120). Likewise, BRI1 phosphorylates BSK1 at Ser230 and CDG1at Ser44, Ser47, and Ser234 (95, 96, 202). At least the phosphosites in CDG1 contribute to BRsignaling. These results suggest a phosphorylation relay from the receptor complex to RLCKs asa primary mechanism in plant transmembrane signaling, in contrast to the allosteric activation ofc-Src kinases upon their recruitment to phosphorylated RTKs in animals (107, 237).

Recent studies suggest that BIK1/PBLs are rate-limiting components in pattern-triggeredimmune signaling and are dynamically regulated in both activity and stability before and afteractivation (Figure 2) (39). A yeast two-hybrid screen for EFR-interacting proteins identifiedArabidopsis PP2C38 as a negative regulator of pattern-triggered immunity (38). Further analysisshowed that PP2C38 also interacts with FLS2 and BIK1, and in the resting state, PP2C38 de-phosphorylates BIK1 to maintain BIK1 in a nonactivated state. Upon flg22 or elf18 treatment,PP2C38 is phosphorylated at Ser77 and dissociates from BIK1 to enable BIK1 activation by theFLS2 and EFR receptor complexes (38).

BIK1 is additionally regulated by the ubiquitin-proteasome pathway. A genetic screen forsuppressors of the bak1-5 mutant (an allele of the BAK1 co-receptor that is severely compromisedin immune signaling) identified CALCIUM-DEPENDENT PROTEIN KINASE28 (CPK28)as a negative regulator of immunity that promotes proteasome-dependent degradation of BIK1 inthe resting state, probably by phosphorylating BIK1 at unknown site(s) (146). The cpk28 mutantoveraccumulates BIK1 and displays hyperactive immune responses upon flg22 or elf18 treatment.Several studies showed that Arabidopsis heterotrimeric G protein components—including two non-canonical Gα proteins, EXTRA-LARGE GTP-BINDING PROTEIN2 (XLG2) and XLG3; oneGβ protein, AGB1; and two Gγ proteins, AGG1 and AGG2—act as positive regulators in immuneresponses activated by flg22 and chitin (125, 137, 206). More recent molecular analysis showedthat these G proteins interact with the FLS2-BIK1 complex to positively promote BIK1 proteinaccumulation in the resting state, likely by dampening proteasome-dependent degradation (116).

A recent study uncovered detailed mechanisms for the control of BIK1 homeostasis. BIK1is a substrate of a pair of closely related PLANT U-BOX25 (PUB25) and PUB26, which areubiquitin E3 ligases (215). PUB25 and PUB26 polyubiquitinate and promote degradation of


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FLS2

BAK1/SERKs

FLS2

BAK1/SERKs

flg22BIR2 BIR2

CPK28 CPK28

PUB25PUB26

PUB25PUB26

Proteasome

PP2C38

PP2C38

Proteasome

Gβγ

GαXLG2

P

P

P P

Resting state Activated state

BIK1

BIK1 BIK1

BIK1 BIK1GαXLG2

GβγP

P

Figure 2Multilayered control of BOTRYTIS-INDUCED KINASE1 (BIK1) activity and stability during immune signaling. In the resting state,the BIK1 protein in the FLAGELLIN SENSING2 (FLS2) immune complex is subjected to multiple layers of regulation. In the restingstate, BIK1 is polyubiquitinated by a pair of E3 ligases, PLANT U-BOX25 (PUB25) and PUB26, and degraded through theproteasome system. CALCIUM-DEPENDENT PROTEIN KINASE28 (CPK28) can phosphorylate BIK1 and promote BIK1degradation, although whether this phosphorylation contributes to BIK1 instability remains unknown. The heterotrimeric G proteinscomposed of EXTRA-LARGE GTP-BINDING PROTEIN2 (XLG2) (Gα), AGB1 (Gβ), and AGG1/2 (Gγ) interact with theFLS2-BIK1 complex in the resting state and directly inhibit the E3 ligase activity of PUB25 and PUB26 to stabilize BIK1. In addition,PP2C38 actively dephosphorylates BIK1 in the resting state to prevent premature activation. Upon flg22 perception, CPK28 is furtheractivated to phosphorylate PUB25 and PUB26, which enhances the E3 ligase activity and accelerates the degradation of BIK1. Theactivated BIK1, which is phosphorylated in the activation loop, is protected from PUB25- and PUB26-mediated ubiquitination (Ub)and degradation, allowing it to phosphorylate downstream substrates. In addition, PP2C38 is phosphorylated and dissociated fromBIK1 to allow rapid phosphorylation and activation of BIK1. The perception of flg22 also enables the activation of the heterotrimericG proteins and phosphorylation of XLG2, which subsequently dissociates from the FLS2-BIK1 receptor complex. Thick arrowsindicate greater activities than thin arrows. Circled P represents phosphorylation of proteins. Other abbreviations: BAK1,BRI1-ASSOCIATED KINASE1; BIR2, BAK1-INTERACTING RECEPTOR-LIKE KINASE2; SERKs, SOMATICEMBRYOGENESIS RECEPTOR KINASEs.

nonactivated BIK1, but not activated BIK1, which is phosphorylated in the activation loop.Importantly, CPK28, the aforementioned G proteins, PUB25, and PUB26 form a regulatorymodule to control BIK1 homeostasis (215). In the resting state, the G proteins directly inhibitthe E3 ligase activity of PUB25 and PUB26, likely by steric hindrance, to stabilize BIK1.Following flg22 perception, CPK28 is further activated through an unknown mechanism andphosphorylates PUB25 at Thr94 and PUB26 at Thr95, which enhances the E3 ligase activityof PUB25 and PUB26 and accelerates the degradation of nonactivated BIK1. This depletesBIK1 from the FLS2-BAK1 complex and prevents overaccumulation of activated BIK1 andhyperactive immune responses. The activated BIK1, however, is protected from PUB25- andPUB26-mediated ubiquitination and degradation, allowing it to phosphorylate downstreamtargets. Taken together, these studies highlight a multilayered regulatory mechanism centeredon BIK1 for tight and dynamic control of immune signal output.

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RESPIRATORYBURSTHOMOLOGs(RBOHs): closelyrelated plant proteinsthat are homologousto NADPH oxidases inanimals

Ca2+ Currents During Immune Signaling

Calcium is an important secondary messenger involved in numerous signaling events in eukary-otic cells. Pattern recognition by PRRs triggers a rapid and transient influx of calcium from theapoplast to the cytosol (102). Pharmacological studies have placed this calcium burst upstream ofother immune signaling events including CPK activation, ROS burst, and MAPK activation (165,177). The elevation of cytoplasmic calcium concentration activates multiple CPKs, among whichCPK4, CPK5, CPK6, and CPK11 are required for pattern-triggered defense gene expression(14). Higher-order cpk mutants show reduced flg22-induced ROS burst, defense gene expression,and resistance to bacterial infection. Despite their fundamental importance, the identity of thecalcium channel(s) activated by microbial patterns remains elusive.

Using an aequorin-based reporter, Li et al. (113) showed that the bik1 mutant is severelyreduced in flg22-triggered calcium burst and impaired in flg22-induced CPK5 phosphorylation.An independent forward genetic screen identified multiple pbl1 mutant alleles that are greatlycompromised in calcium burst triggered by immunogenic patterns including flg22, elf18, andPep1, but not chitin (164). The bik1 pbl1 double mutant is further reduced in the pattern-triggeredcalcium burst, indicating that BIK1 and PBL1 play a key role in the regulation of calcium channel(s)downstream of FLS2, EFR, PEPR1, and PEPR2. It is tempting to speculate that BIK1 and PBL1directly or indirectly regulate the yet-to-be-identified calcium channel(s) to orchestrate immunesignaling. The normal calcium current in bik1 pbl1 seedlings in response to chitin raises a possibilitythat other RLCKs may be specifically required for the activation of calcium channel(s) downstreamof CERK1.

Reactive Oxygen Species

ROS are another class of important signaling molecules that are produced in response to diverseenvironmental factors as well as during normal development (142, 210). In higher plants, a familyof RESPIRATORY BURST HOMOLOGs (RBOHs), which are homologous to animal NADPHoxidases, play a crucial role in the generation of ROS in the apoplast (86). Among these, RBOHD isthe main isoform responsible for the production of apoplastic H2O2 upon pattern recognition (40,161, 205, 248). RBOHD-mediated ROS production plays a crucial role in stomatal defense, actinbundling, and callose deposition at the cell wall (161). RBOH-dependent ROS also act as majorsignaling molecules in the regulation of plant growth and development (27, 53, 196). MultipleRBOHs act downstream of FER, ANX1, and ANX2 during the regulation of primary root growth,root hair growth, and pollen tube integrity (12, 30, 46). These findings suggest RBOH-dependentROS as a common node in RK/RLK-mediated signaling in diverse biological processes.

Earlier studies established that localized production of ROS in the emerging root hair cellthrough RBOHC is essential for root hair development (53). Similarly, RBOHH and ROBHJ arerequired for ROS production in the pollen tube tip and for prevention of premature pollen rupture(12). FER is now known to regulate RBOH-dependent ROS in roots through RhoGTPases tocontrol root hair development (47), whereas ANX1 and ANX2 control pollen rupture by actingupstream of RBOHH and ROBHJ (12). This may be reminiscent of the allosteric activation ofNADPH oxidase by the small GTPase Rac downstream of RTKs in animals (7, 107, 160). A recentreport indicates that the ANX1- and ANX2-mediated regulation of ROS signaling involves theRLCK MRI. The constitutively active variant MRIR240C rescues the pollen bursting phenotypenot only in anx1 anx2 but also in rbohH rbohJ (11), suggesting that MRI acts downstream ofRBOH-dependent ROS to regulate pollen rupture. Consistent with this hypothesis, MRI inter-acts with OXIDATIVE SIGNAL INDUCIBLE1 (OXI1), a protein kinase that mediates ROS


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signaling (11, 117). It remains to be tested, however, whether the loss-of-function mri mutantand MRIR240C-expressing plants display altered ROS production in roots or pollen tubes. In roothair development, the generation of cytosolic free calcium is essential for root hair elongation(53, 225), and RBOHC-mediated ROS production is required for the distribution of cytoplasmiccalcium in the root hair tip, suggesting that ROS act upstream of calcium signaling in root hairdevelopment. Whether MRI is necessary for the generation of cytosolic calcium current in roothair remains unknown.

The regulation of RBOH-dependent ROS is better studied in PRR-mediated immune sig-naling. Using protein pull-down coupled with mass spectrometry analysis, researchers identifiedRBOHD as a protein interacting with BIK1, FLS2 and EFR (87, 113). Further biochemical anal-yses demonstrated that BIK1 directly phosphorylates specific sites in RBOHD independent ofan increase of cytoplasmic calcium and CPK5 and that this phosphorylation is required for ROSproduction downstream of FLS2 and EFR and stomatal immunity against P. syringae. Importantly,the BIK1-dependent phosphosites are required but not sufficient for RBOHD activation, as the Nterminus of RBOHD is subject to regulation by additional factors such as calcium binding, phos-phatidic acid binding, and CPK5-mediated phosphorylation, which are required for RBOHD ac-tivation (48, 86, 87, 113, 249). Thus, the BIK1-mediated phosphorylation of RBOHD is proposedto prime RBOHD, which is further regulated by other signaling inputs for full activation (86).

In addition to BIK1 and PBL1, additional RLCKs, including PCRK1, PCRK2, and BSK1,positively or negatively regulate flg22-triggered ROS production (99, 183, 187). BSK1 in particulardoes not appear to possess kinase activity (9, 95, 188), raising a question as to how it regulatesRBOHD activity. OsRLCK57, OsRLCK107, OsRLCK118, and OsRLCK176 in rice interact withOsCREK1 to regulate chitin- and peptidoglycan-induced ROS production (115). OsBSR1, alsonamed OsRLCK278, is required for chitin-induced ROS production and defense gene expression(90). A recent report showed that a tomato RLCK-VIII member, PTO-INTERACTIN 1 (PTI1),is required for flg22-induced ROS production and resistance to P. syringae (175). These resultsindicate that the RLCK-mediated regulation of RBOHs is likely a conserved mechanism in bothmonocots and dicots. Interestingly, the Arabidopsis PBL13 negatively regulates flg22-induced ROSburst by directly interacting with RBOHD (123). Whether PBL13 phosphorylates RBOHD atdifferent sites, interferes with the BIK1-mediated phosphorylation, or modulates RBOHD activitythrough other mechanisms remains to be elucidated.

A recent study showed that the Gα protein XLG2 can directly interact with RBOHD (116).Upon flg22 perception, BIK1 phosphorylates XLG2 at its N terminus, and this phosphorylationis required for optimum ROS production independent of BIK1 stability, suggesting that thephosphorylated XLG2 positively regulates RBOHD (116). The rice RhoGTPase RAC1 alsopromotes RBOH-mediated ROS downstream of CERK1 (224). The regulation of RBOHs byXLG2 in Arabidopsis and by RAC1 in rice is thus similar to the ROP-mediated regulation ofRBOH in root hair development.

Mitogen-Activated Protein Kinase Cascades

MAPK cascades represent another signaling module key to transmembrane signaling in bothanimals and plants (Figure 3). In animals, the phosphorylated RTKs indirectly recruit a class ofguanine nucleotide exchange factors called SOS to activate RAS-GTPases, and the latter recruitthe MAP3K Raf to the plasma membrane, which is sufficient for the activation of Raf and theMAPK cascade (107). Immune activation of TLRs in animals also activates MAPK cascades.The activation of TLR5 recruits IRAKs (see section titled Receptor-Like Cytoplasmic Kinasesin Receptor Kinase–Regulated Biological Processes) through the adaptor protein MyD88 (91).

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MAPKKK5MKK4/5MPK3/6

MEKK1MKK1/2

MPK4

YDAMKK4/5MPK3/6

?MKK4/5MPK3/6

?

MKKMAPK

????

TAK1 MKKMAPK

Raf

TLR5

IRAK4

BAK1/SERKs

HAE/HSL2

CSTSSP

flg22/elf18 Chitin FlagellinEPFs ESF IDA

IRAK1 IRAK2TRAF6

MYD88

EGFR

EGF

Grb2SOSRas

TAB2/3

LYK5 CERK1

PBL27

ERBAK1/SERKs TMM

?

SSP?

FLS2/EFRBAK1/SERKs

PBLs

PPP

PP P

PPP

P

P

P

P

PP

P

PP

P P

a b

Figure 3Receptor-like cytoplasmic kinase (RLCK)-mediated regulation of mitogen-activated protein kinase (MAPK) cascades downstream ofreceptor kinases (RKs). (a) In the chitin-triggered immune pathway, the chitin co-receptor CHITIN ELICITOR RECEPTORKINASE1 (CERK1) phosphorylates the RLCK PBS1-LIKE27 (PBL27), which then phosphorylates the MAPK kinase kinaseMAPKKK5 to activate the MAPK cascade. RLCK-VII members may also mediate MAPK activation by other immune RKs, such asFLAGELLIN SENSING2 (FLS2). In the embryonic patterning pathway, the RLCK SHORT SUSPENSOR (SSP) regulates MAPKkinase kinase YODA (YDA), presumably by phosphorylation. The stomatal patterning pathway also employs the same MAPK cascadeutilized for embryonic patterning, which is probably mediated by SSP-like RLCKs. In plant RK signaling, RLCKs activate MAPKcascades through phosphorylation relay. (b) This contrasts with the MAPK activation by the animal Toll-like receptor (TLR) pathway,which is indirectly regulated by cytoplasmic INTERLEUKIN RECEPTOR-ASSOCIATED KINASEs (IRAKs) and downstreamTRAF6-mediated ubiquitination. It also differs from the receptor tyrosine kinase (RTK)-mediated MAPK activation, in which theactivation of RTKs indirectly recruits the MAPK kinase kinase Raf to the plasma membrane for Raf activation. Circled P representsphosphorylation of proteins. Other abbreviations: BAK1/SERKs, BRI1-ASSOCIATED KINASE1/SOMATIC EMBRYOGENESISRECEPTOR KINASEs; CST, CAST AWAY; EFR, ELONGATION FACTOR-TU (EF-Tu) RECEPTOR; EGF, EPIDERMALGROWTH FACTOR; EGFR, EPIDERMAL GROWTH FACTOR RECEPTOR; EPF, EPIDERMAL PATTERNING FACTOR;ER, ERECTA; ESF, EMBRYO SURROUNDING FACTOR; HAE/HSL2, HAESA/HAESA-LIKE2; IDA, INFLORESCENCEDEFICIENT IN ABSCISSION; LYK5, LYSINE MOTIF RECEPTOR KINASE5; TMM, TOO MANY MOUTH.

IRAKs further recruit the E3 ligase TRAF6, which catalyzes Lys63-linked polyubiquitinationon its targets including TAB2 and TAB3. TAB2 and TAB3 further regulate the MAP3K proteinTAK1 and activate JNK and p38 MAPK cascades to control transcriptional reprogramming (91).The activation of MAPK cascades by plant RKs, however, appears to be more direct. Emergingevidence suggests that plant RLCKs directly activate MAP3Ks downstream of RKs.

The RLCK SSP is required for the activation of the MAPK cascade by acting upstream of YDA(9, 37). A recent study showed that SSP directly interacts with YDA (243), raising a possibilitythat SSP activates YDA and the MAPK cascade through a phosphorylation relay (Figure 3).Although the receptor for ESF remains unknown, a recent study showed that the LRR-RLKZYGOTIC ARREST1 directly interacts with SSP in vitro (241). This finding suggests that SSPlinks the receptor complex, which presumably contains both an unknown receptor and ZYGOTICARREST1, to the MAPK cascade.

Perception of diverse immunogenic patterns activates two conserved MAPK cascades. Onecascade consists of the MAP3K MEKK1, the MAP2Ks MKK1 and MKK2, and the MAPK MPK4.The other cascade consists of an unknown MAP3K, the MAP2Ks MKK4 and MKK5, and theMAPKs MPK3 and MPK6 (139). The identity of the MAP3K for the second cascade has remainedcontroversial. RLCK-VII members appear to be required for pattern-triggered MAPK activation(Figure 3). Flg22-induced MPK activation is slightly reduced in the pcrk1 pcrk2 double mutant,


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whereas the bik1 pbl1 double mutant is slightly diminished in Pep2-induced MAPK activation(231). The weak phenotypes of the pcrk1 pcrk2 and bik1 pbl1 double mutants suggest functionalredundancy of RLCK-VII members in the regulation of MAPK cascades. Consistent with thispossibility, overexpression of AvrAC in Arabidopsis, which is capable of inhibiting multiple RLCK-VII members, significantly impairs flg22-induced activation of MPK3, MPK4, and MPK6 (52).

OsRLCK185 and OsRLCK176 in rice mediate chitin- and peptidoglycan-induced MAPK ac-tivation by interacting with OsCERK1 (6, 232). PBL27, the Arabidopsis ortholog of OsRLCK185,positively regulates chitin-triggered MAPK activation (184). A recent study suggested that theMAP3K MAPKKK5 is specifically required for chitin-induced MPK3 and MPK6 activation (229).It was reported that CERK1 phosphorylates PBL27, which then phosphorylates MAPKKK5 inthe C-terminal regulatory tail in vitro. The phosphosites in the MAPKKK5 C-terminal tail werenecessary for chitin-induced MPK3 and MPK6 activation, although whether this phosphoryla-tion occurs in plants upon chitin perception remains unclear. While this study provides evidencethat an RLCK directly links a PRR to a MAPK cascade, whether the reported mechanism is anisolated case or has broad implications in plant response to diverse patterns remains to be shown.Paradoxically, both PBL27 and MAPKKK5 play a negative role in flg22-triggered MAPK activa-tion (229). More recently, BSK1 was reported to interact with and phosphorylate MAPKKK5 atSer289 to regulate immunity (238). Whether and how this phosphorylation activates the MAPKcascade remain unknown.

The Specificity of Receptor-Like Cytoplasmic Kinase–Mediated Signaling

A key question in transmembrane signaling is how the perception of different extracellular ligandsleads to distinct cytoplasmic signal output. The specificity of signal output is determined by thekinase domain of the RK (17, 74). In the majority of reported cases, different RKs and RLKslargely employ distinct sets of RLCKs (Figure 1), suggesting that different RLCKs regulatedifferent downstream targets.

In several cases, an RLCK can associate with different RKs to regulate distinct cellular processes(Figure 4). BIK1 interacts with both FLS2 and BRI1 (122, 132, 247). Whereas the FLS2-BIK1interaction positively regulates immunity, the BRI1-BIK1 interaction negatively regulates BR-mediated growth. Interestingly, BIK1 also negatively regulates root hair growth (208). This raisesa possibility that BIK1 is additionally regulated by RALFs or other signaling molecules. In additionto BIK1, BSK1 also interacts with both BRI1 and FLS2. Whereas the interactions of BRI withBSKs regulate growth, the FLS2-BSK1 interaction positively regulates immune responses (183,202). The roles of MRI in ANX1- and ANX2-mediated control of pollen tube integrity and FER-mediated regulation of root hair growth represent the third example in which an RLCK regulatesdistinct biological process by associating with different RLK complexes (11, 117). Together, theseresults indicate that the signal output of an RLCK is dictated by the upstream RK complex.

The mechanism by which different RKs determine RLCK signal output remains unknown.BIK1 can be phosphorylated by BRI1 upon BR treatment, in a way similar to its flg22-inducedphosphorylation by the FLS2-BAK1 complex (121). However, the BR-induced phosphorylationof BIK1 does not appear to trigger immune responses, indicating that BIK1 is able to interpretdifferent signal input and gives rise to distinct signal output. It has been shown that the BR-induced phosphorylation of BIK1 is conferred by BRI1 and independent of BAK1 (121), whereasthe flg22-induced BIK1 phosphorylation requires BAK1. It is thus possible that the differentialphosphorylation patterns in BIK1 contribute to different signal output (Figure 4). Alternatively,the context of other signaling components in the RK complexes may play a role in determin-ing the specificity of signaling. Indeed, FLS2 and BRI1 are localized in distinct clusters in the

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P P

BRI1

BAK1/SERKs

FLS2/EFR

BAK1/SERKs

flg22/elf18

CDG1

Growth Immunity

BSK1 BIK1 BSK1 PBLs BIK1 P P P P

BRs

Figure 4Differential receptor-like cytoplasmic kinases (RLCKs) signal output upon association with different receptorkinases. The RLCKs BOTRYTIS-INDUCED KINASE1 (BIK1) and BR SIGNALING KINASE1 (BSK1)are shared by the brassinosteroid (BR) receptor BRASSINOSTEROID INSENSITIVE1 (BRI1) andimmune receptor FLAGELLIN SENSING2 (FLS2). BRs regulate plant growth, but not defenses, throughBRI1-dependent phosphorylation of multiple BSKs, CONSTITUTIVE DIFFERENTIAL GROWTH1(CDG1), and BIK1. The interactions of BRI1 with BSKs and CDG1 mediate BR-induced plant growth,whereas the BRI1-BIK1 interaction negatively regulates BRI1 signaling and plant growth. In contrast, bothFLS2-BSK1 and FLS2-BIK1 interactions positively regulate plant immunity rather than growth promotion.These results support the idea that the signal output downstream of RLCKs depends on the receptorcomplexes in which they reside. Different receptor complexes may differentially phosphorylate an RLCK orpossess different substrates for the RLCK. Circled P represents phosphorylation of proteins. Otherabbreviations: BAK1/SERKs, BRI1-ASSOCIATED KINASE1/SOMATIC EMBRYOGENESISRECEPTOR KINASEs; EFR, ELONGATION FACTOR-TU (EF-Tu) RECEPTOR; PBL, PBS1-LIKE.

plasma membrane (18), suggesting that environments hosting different receptor complexes maycontribute to signal specificity.

CONCLUSIONS AND PERSPECTIVES

RKs are central to plant adaptation to the environment, reproduction, growth, and development.While a great deal is known about how RKs perceive their ligands and downstream cellularchanges, until recently we have had inadequate knowledge concerning how the extracellular signalis transduced from RKs to downstream signaling components. Emerging evidence indicates thatRLCKs are adopted as common signaling nodes that link RKs to downstream signal output. Itis now well established that RLCKs play a central role in regulating immune signaling, sexualreproduction, growth, and development downstream of RKs. A growing literature also supportsthe idea that RLCKs are signal transducers acting downstream of RKs involved in plant adaptationto abiotic stresses. As RK complexes often share similar organization, such as adopting SERKs andSOBIR1 as co-receptors (118), more RK pathways are expected to involve RLCKs as signalingcomponents.

Current results suggest a phosphorylation relay in which, upon ligand perception, RKs phos-phorylate RLCKs, and the latter further phosphorylate major signaling components. Studies ofpattern-triggered immunity have shown complex signaling pathways bifurcating downstream ofRLCKs. Existing evidence indicates that RLCKs regulate multiple signaling nodes including


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MAPK cascades, NADPH oxidases, calcium channels, and heterotrimeric G proteins to orches-trate a variety of immune responses. Furthermore, these nodes are interconnected, as illustratedby the mutual regulation of ROS and calcium signals. Future studies are necessary to elucidatehow RLCKs regulate plant growth, development, and stress responses.

There remain many gaps in our knowledge concerning RLCK-dependent signaling. A majorlimitation in the analysis of the function of RLCKs is their frequent redundancy, as in the caseof BIK1/PBLs in immunity and BSKs in BR signaling. Systematic construction and analysis ofhigher-order RLCK mutants, gain-of-function mutants, or overexpression studies may be neededto uncover their biological functions. Another challenge is the identification of RLCK substrates,in which the genetic approach has had a limited success. With the advance of protein interactomeand phosphoproteomic studies, we should be able to unravel the full spectrum of substrates forthese important kinases and better understand transmembrane signaling in plants.

SUMMARY POINTS

1. Transmembrane signaling by RKs is essential for regulating diverse biological processesin plants, and RLCKs are key components in RK-mediated signaling. Analyses of RLCKsprovide insights into regulatory mechanisms by which RKs regulate these processes.

2. RLCKs are directly activated by RKs and co-receptors following the perception of ex-ternal signals. The activity and stability of RLCKs are additionally subject to dynamicregulation by proteins associated with the receptor complex, including protein phos-phatases, E3 ligases, CPKs, and heterotrimeric G proteins.

3. Analyses of immune signaling indicate that downstream pathways bifurcate after RLCKs,which phosphorylate multiple substrates such as NADPH oxidases, heterotrimeric Gproteins, protein phosphatases, and MAPKKKs.

4. An RLCK can function in different biological processes, and the specificity is determinedby the RK complexes with which the RLCK is associated.

5. Advances in immune RLCK studies may help us understand the mechanisms by whichRLCKs regulate plant growth, development, and abiotic stresses.

DISCLOSURE STATEMENT

The authors are not aware of any affiliations, memberships, funding, or financial holdings thatmight be perceived as affecting the objectivity of this review.

ACKNOWLEDGMENTS

J.M.Z. was supported by grants from the Strategic Priority Research Program of the ChineseAcademy of Sciences (XDB11020200), the Ministry of Science and Technology of the People’sRepublic of China (2016YFD0100601), and the State Key Laboratory of Plant Genomics.

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PP69_FrontMatter ARI 5 April 2018 9:11

Annual Review ofPlant Biology

Volume 69, 2018

Contents

My Secret LifeMary-Dell Chilton � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 1

Diversity of Chlorophototrophic Bacteria Revealed in the Omics EraVera Thiel, Marcus Tank, and Donald A. Bryant � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � �21

Genomics-Informed Insights into Endosymbiotic Organelle Evolutionin Photosynthetic EukaryotesEva C.M. Nowack and Andreas P.M. Weber � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � �51

Nitrate Transport, Signaling, and Use EfficiencyYa-Yun Wang, Yu-Hsuan Cheng, Kuo-En Chen, and Yi-Fang Tsay � � � � � � � � � � � � � � � � � � � � �85

Plant VacuolesTomoo Shimada, Junpei Takagi, Takuji Ichino, Makoto Shirakawa,

and Ikuko Hara-Nishimura � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 123

Protein Quality Control in the Endoplasmic Reticulum of PlantsRichard Strasser � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 147

Autophagy: The Master of Bulk and Selective RecyclingRichard S. Marshall and Richard D. Vierstra � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 173

Reactive Oxygen Species in Plant SignalingCezary Waszczak, Melanie Carmody, and Jaakko Kangasjarvi � � � � � � � � � � � � � � � � � � � � � � � � � � 209

Cell and Developmental Biology of Plant Mitogen-Activated ProteinKinasesGeorge Komis, Olga Samajova, Miroslav Ovecka, and Jozef Samaj � � � � � � � � � � � � � � � � � � � � � 237

Receptor-Like Cytoplasmic Kinases: Central Players in Plant ReceptorKinase–Mediated SignalingXiangxiu Liang and Jian-Min Zhou � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 267

Plant Malectin-Like Receptor Kinases: From Cell Wall Integrity toImmunity and BeyondChristina Maria Franck, Jens Westermann, and Aurelien Boisson-Dernier � � � � � � � � � � � � 301

Kinesins and Myosins: Molecular Motors that Coordinate CellularFunctions in PlantsAndreas Nebenfuhr and Ram Dixit � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 329

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The Oxylipin Pathways: Biochemistry and FunctionClaus Wasternack and Ivo Feussner � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 363

Modularity in Jasmonate Signaling for Multistress ResilienceGregg A. Howe, Ian T. Major, and Abraham J. Koo � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 387

Essential Roles of Local Auxin Biosynthesis in Plant Developmentand in Adaptation to Environmental ChangesYunde Zhao � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 417

Genetic Regulation of Shoot ArchitectureBing Wang, Steven M. Smith, and Jiayang Li � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 437

Heterogeneity and Robustness in Plant Morphogenesis: From Cellsto OrgansLilan Hong, Mathilde Dumond, Mingyuan Zhu, Satoru Tsugawa,

Chun-Biu Li, Arezki Boudaoud, Olivier Hamant, and Adrienne H.K. Roeder � � � � � � 469

Genetically Encoded Biosensors in Plants: Pathways to DiscoveryAnkit Walia, Rainer Waadt, and Alexander M. Jones � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 497

Exploring the Spatiotemporal Organization of Membrane Proteins inLiving Plant CellsLi Wang, Yiqun Xue, Jingjing Xing, Kai Song, and Jinxing Lin � � � � � � � � � � � � � � � � � � � � � � � 525

One Hundred Ways to Invent the Sexes: Theoretical and ObservedPaths to Dioecy in PlantsIsabelle M. Henry, Takashi Akagi, Ryutaro Tao, and Luca Comai � � � � � � � � � � � � � � � � � � � � � � 553

Meiotic Recombination: Mixing It Up in PlantsYingxiang Wang and Gregory P. Copenhaver � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 577

Population Genomics of Herbicide Resistance: Adaptation viaEvolutionary RescueJulia M. Kreiner, John R. Stinchcombe, and Stephen I. Wright � � � � � � � � � � � � � � � � � � � � � � � � � 611

Strategies for Enhanced Crop Resistance to Insect PestsAngela E. Douglas � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 637

Preadaptation and Naturalization of Nonnative Species: Darwin’s TwoFundamental Insights into Species InvasionMarc W. Cadotte, Sara E. Campbell, Shao-peng Li, Darwin S. Sodhi,

and Nicholas E. Mandrak � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 661

Macroevolutionary Patterns of Flowering Plant Speciationand ExtinctionJana C. Vamosi, Susana Magallon, Itay Mayrose, Sarah P. Otto,

and Herve Sauquet � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 685

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When Two Rights Make a Wrong: The Evolutionary Genetics ofPlant Hybrid IncompatibilitiesLila Fishman and Andrea L. Sweigart � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 707

The Physiological Basis of Drought Tolerance in Crop Plants:A Scenario-Dependent Probabilistic ApproachFrancois Tardieu, Thierry Simonneau, and Bertrand Muller � � � � � � � � � � � � � � � � � � � � � � � � � � � � 733

Paleobotany and Global Change: Important Lessons for Species toBiomes from Vegetation Responses to Past Global ChangeJennifer C. McElwain � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 761

Trends in Global Agricultural Land Use: Implications forEnvironmental Health and Food SecurityNavin Ramankutty, Zia Mehrabi, Katharina Waha, Larissa Jarvis,

Claire Kremen, Mario Herrero, and Loren H. Rieseberg � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 789

Errata

An online log of corrections to Annual Review of Plant Biology articles may be found athttp://www.annualreviews.org/errata/arplant

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receptor-like cytoplasmic kinases: central players in plant …biologia.ucr.ac.cr/profesores/garcia...

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