Plant Malectin-Like Receptor Kinases: From Cell Wall Integrity to …biologia.ucr.ac.cr/profesores/Garcia Elmer/Plant malectin... · 2019. 3. 11. · PP69CH11_Boisson-Dernier ARI

PP69CH11_Boisson-Dernier ARI 4 April 2018 11:19

Annual Review of Plant Biology

Plant Malectin-Like ReceptorKinases: From Cell WallIntegrity to Immunity andBeyondChristina Maria Franck,∗ Jens Westermann,∗

and Aurelien Boisson-DernierBiocenter, Botanical Institute, University of Cologne, 50674 Cologne, Germany;email: [email protected]

Annu. Rev. Plant Biol. 2018. 69:301–28

First published as a Review in Advance onMarch 14, 2018

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

https://doi.org/10.1146/annurev-arplant-042817-040557

Copyright c© 2018 by Annual Reviews.All rights reserved

∗These authors contributed equally to this article

Keywords

malectin-like receptor kinases, CrRLK1L, cell growth, cell wall integrity,immunity, comparative genomics

Abstract

Plant cells are surrounded by cell walls protecting them from a myriad ofenvironmental challenges. For successful habitat adaptation, extracellularcues are perceived at the cell wall and relayed to downstream signaling con-stituents to mediate dynamic cell wall remodeling and adapted intracellularresponses. Plant malectin-like receptor kinases, also known as Catharanthusroseus receptor-like kinase 1-like proteins (CrRLK1Ls), take part in theseperception and relay processes. CrRLK1Ls are involved in many differentplant functions. Their ligands, interactors, and downstream signaling part-ners are being unraveled, and studies about CrRLK1Ls’ roles in plant speciesother than the plant model Arabidopsis thaliana are beginning to flourish.This review focuses on recent CrRLK1L-related advances in cell growth,reproduction, hormone signaling, abiotic stress responses, and, particularly,immunity. We also give an overview of the comparative genomics and evo-lution of CrRLK1Ls, and present a brief outlook for future research.

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ANNUAL REVIEWS Further

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https://www.annualreviews.org/doi/full/10.1146/annurev-arplant-042817-040557


RLK: receptor-likekinase

ECD: extracellulardomain

CrRLK1L:Catharanthus roseusreceptor-like kinase 1-like protein

MLD: malectin-likedomain

Contents

1. INTRODUCTION . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3022. FUNCTIONS OF MALECTIN-LIKE RECEPTOR KINASES . . . . . . . . . . . . . . . . . 303

2.1. Cellular Growth and Plant Morphogenesis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3032.2. Plant Reproduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3052.3. Plant Immunity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3062.4. Hormone Signaling. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3092.5. Abiotic Stress Tolerance . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 309

3. SIGNALING PARTNERS OF MALECTIN-LIKE RECEPTOR KINASES . . . . . 3093.1. RALF Peptides as Ligands for Malectin-Like Receptor Kinases . . . . . . . . . . . . . . . 3103.2. Glycosylphosphatidylinositol-Anchored Proteins . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3113.3. Receptor-Like Cytoplasmic Kinase–Mediated Signaling . . . . . . . . . . . . . . . . . . . . . . 3123.4. RAC and Rho-GTPase of Plants Signaling. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3133.5. NADPH-Dependent Reactive Oxygen Species and Ca2+ Signaling. . . . . . . . . . . . 313

4. COMPARATIVE AND FUNCTIONAL GENOMICS OF THEMALECTIN-LIKE RECEPTOR KINASES. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3144.1. Origin of Receptor-Like Kinases and Emergence of the

CrRLK1L Subfamily . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3144.2. Domain Organization and Genomic Evolution of CrRLK1Ls . . . . . . . . . . . . . . . . . 3164.3. Preterrestrial Evolution and the Conquering of Land: Functional

Conservation and Divergence of CrRLK1Ls . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3174.4. Evolutionary Conservation of CrRLK1L-Mediated Signal Transduction . . . . . . 319

1. INTRODUCTION

Plants are sessile organisms that adapt to their environmental conditions. The cell wall is the firstbarrier between a plant cell and its environment, and is extremely versatile. It perceives and relaysbiotic and abiotic, mechanical, and chemical cues from neighboring cells; physically resists posi-tive (turgor) or negative (conductive vessels) pressure; and regulates cell size, shape, and growth.To faithfully execute all its different tasks, the plant cell perceives external cues at the cell walland transduces them into signals to initiate cellular modifications in response. This is executedby receptor-like kinases (RLKs), which generally consist of a transmembrane domain (TMD), avariable extracellular domain (ECD) to sense different cues, and an intracellular kinase domainto relay signals to downstream components. In Arabidopsis thaliana, more than 600 RLKs havebeen identified to date (62). Different types of RLKs, such as wall-associated kinases, proline-richextensin-like RLKs, lectin RLKs, leucine-rich repeat RLKs, and malectin-like RLKs [also knownas the Catharanthus roseus receptor-like kinase 1-like proteins (CrRLK1Ls)], act during cell wallsynthesis, remodeling, and signaling (109, 116, 127, 141). CrRLK1Ls are named after the first iso-lated member CrRLK1 from Madagascar periwinkle (115) and have received increasing attentionover the last two decades. All members of the CrRLK1L subfamily share a similar domain struc-ture with a malectin-like domain (MLD), a TMD, and an intracellular Ser and Thr kinase domain(13, 53, 69, 113). In the plant model A. thaliana, the CrRLK1L subfamily contains 17 members,10 of which have been characterized: THESEUS1 (THE1), HERCULES1 (HERK1), HER-CULES2 (HERK2), FERONIA/SIRENE (FER/SIR), ANXUR1 (ANX1), ANXUR2 (ANX2),ERULUS/[Ca2+]cyt-ASSOCIATED PROTEIN KINASE 1 (ERU/CAP1), CURVY1 (CVY1),BUDDHA’S PAPER SEAL1 (BUPS1), and BUDDHA’S PAPER SEAL2 (BUPS2). These 10

302 Franck ·Westermann · Boisson-Dernier

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KDRIPK

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Figure 1Summary of FER-associated proteins. A schematic representation of FER-associated proteins is shown,including the corresponding FER-binding domains. Abbreviations: ABI2, ABSCISIC ACIDINSENSITIVE 2; BAK1, BRASSINOSTEROID INSENSITIVE 1 ASSOCIATED KINASE 1; EC,extracellular; EN14, EARLY NODULIN 14; eJM, extracellular juxta-membrane domain; FER, FERONIA;flg22, flagellin epitope 22; FLS2, FLAGELLIN SENSING 2; GEF1/4/7/10, GUANINE NUCLEOTIDEEXCHANGE FACTOR 1/4/7/10; IC, intracellular; KD, kinase domain; LRE/LLG1, LORELEI andLORELEI-LIKE GPI-ANCHORED PROTEIN 1; MLD, malectin-like domain; PM, plasma membrane;RALF1/23, RAPID ALKALINIZATION FACTOR 1 and 23; RIPK, RESISTANCE TOPSEUDOMONAS SYRINGAE PV. MACULICOLA 1–INDUCED PROTEIN KINASE; ROP2/11,RHO-GTPASE OF PLANTS 2 and 11; SAM1/2, S-ADENOSYLMETHIONINE SYNTHASE 1 and 2.

CWI: cell wallintegrity

RLKs have versatile roles in cell growth, plant morphogenesis, reproduction, immunity, hormonesignaling, and stress responses. Over the last five years, major advances have been made in thefield, especially in the context of FER. Novel interactors for FER have been discovered, includ-ing some FER ligands (Figure 1). Furthermore, key roles in immunity could be attributed toCrRLK1Ls via their association with major immune receptors. Also, CrRLK1Ls are now beinginvestigated and characterized in other plant species as well. Thus, this review briefly introducesthe characterized CrRLK1Ls (see the full summary in Supplemental Table 1), then focuseson common downstream signaling partners, and subsequently discusses evolutionary aspects ofCrRLK1Ls.

2. FUNCTIONS OF MALECTIN-LIKE RECEPTOR KINASES

2.1. Cellular Growth and Plant Morphogenesis

For growth, plant cells have to closely monitor cell wall integrity (CWI) and coordinate it withtheir internal growth machinery. Cell wall sensors provide feedback to the plant cell regardingthe cell wall’s molecular, chemical, and structural composition, as well as its tension. If its cell wallis too rigid or too loose, the cell can either stall its growth or even lose its integrity. Intriguingly,several CrRLK1Ls are involved in growth processes.

A suppressor screen for the short hypocotyl phenotype of the CELLULOSE SYNTHASE6–deficient mutant procuste1-1 ( prc1-1) seedlings led to the identification of THE1 (42). The

www.annualreviews.org • Plant Malectin-Like Receptor Kinases 303

Supplemental Material

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ROS: reactive oxygenspecies

the1-1 and the1-2 mutations affect only the prc1-1 mutant but not wild-type plants (42). In prc1-1background, the1 mutant plants and THE1-GFP overexpressing plants attenuate and enhancehypocotyl growth inhibition and ectopic lignification, respectively. The T-DNA insertionalallele, the1-3, shows reduced growth inhibition and ectopic lignification in the prc1-1 backgroundas well as in some other cellulose-deficient mutants (42). Interestingly, partial rescue of theshort hypocotyl phenotypes in cellulose-deficient mutants is never accompanied by restorationof cellulose levels. Thus, this founding study (42) revealed that, in the damaged cell wall context,a THE1-dependent pathway is activated to repress growth and that THE1 somehow monitorscell wall status. Furthermore, application of the cellulose biosynthesis-inhibiting herbicideisoxaben triggers a reactive oxygen species (ROS) burst, jasmonic acid accumulation, and ectopiclignification in seedlings (25). Concordantly, the1-1 mutant seedlings are less sensitive to isoxabentreatment (25). Merz et al. (84) recently confirmed that the loss-of-function alleles, the1-1,the1-2, the1-3, and the1-6, are indeed resistant to growth inhibition triggered by a cellulosesynthase deficiency and to isoxaben-induced ectopic lignification. Surprisingly, the T-DNAinsertional allele, the1-4, is a hypermorphic allele, displaying phenotypic effects similar to thoseof the THE1 overexpressor (84). Unfortunately, previous studies have used the the1-4 alleleassuming it was a classical recessive loss-of-function allele (34, 37). In light of the new findings(84), previous studies should be interpreted with caution. For example, Guo et al. (37) reporteddwarfism in herk1-1 the1-4 double mutant plants unlike in the single mutants, concluding thatHERK1 and THE1 might redundantly promote cell elongation. However, herk1-1 might alsoinduce cell wall damage, allowing the hypermorphic the1-4 to inhibit cell elongation. Similarly,the fact that the1-4 can rescue the increased petal size of kinesin-13a mutants (34) could beexplained by cell wall damage in kinesin-13a prompting the1-4 to inhibit cell elongation. Takentogether, these studies indicate that THE1 negatively regulates cell growth upon cell wallperturbation.

The other founding member, FER, also affects cell growth. FER loss-of-function plants aresemi-dwarf, just as are herk1-1 the1-4 plants (37, 54). Furthermore, FER loss-of-function affectstip-growing cells, such as trichomes or root hairs. fer trichomes are distorted, curly, collapsed,or abnormally branched, and most fer root hairs lose their integrity upon emergence or shortlyafter (30). Interestingly, fer leaves have box-shaped epidermal cells (65). Thus, FER also reg-ulates the morphology of leaf epidermal cells by influencing lobe formation. Therefore, FERis a key positive regulator for polar growth and CWI. Additionally, FER is a regulator of rootgrowth. First, fer roots have limited mechanosensitivity and thus exhibit abnormal growth re-sponse to various mechanical stimuli (119). Second, fer-4 roots acidify faster in the growth mediumthan wild type, and under blue-light conditions that stimulate root growth, fer-4 plants displaylonger roots than wild type (41). Moreover, fer roots are insensitive to root growth inhibitiontriggered by the peptide growth regulator RAPID ALKALINIZATION FACTOR 1 (RALF1)(41) (see Section 3.1). Thus, FER has growth-related functions in diverse cell types all over theplant.

Another CrRLK1L mutant, eru, exhibits a short root hair phenotype (41) that can be restored bygrowing plants in NH4

+-depleted medium (5, 6). eru roots have shorter and fewer root hairs withswollen bases during root hair initiation, which display abnormal shapes during the fast growthphase. Also, NH4

+ influx into the eru vacuole is reduced. Thus, ERU is a positive regulator of cellgrowth and is important for cytoplasmic NH4

+ homeostasis. Moreover, ERU is the first and sofar only CrRLK1L member that localizes to the vacuolar membrane (6).

Finally, CVY1 also regulates polar growth. Among other phenotypes, cvy1 mutants have heavilydistorted trichomes and box-shaped epidermal cells, reminiscent of fer mutants (35). However,understanding CVY1’s mode of function during polar growth requires further investigation.


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PT: pollen tube

2.2. Plant Reproduction

Cell-to-cell communication and CWI are also key during plant reproduction. Double fertiliza-tion in flowering plants requires close communication between the female gametophytes (embryosacs) and the male gametophytes [pollen tubes (PTs)]. Similar to trichomes and root hairs, PTselongate rapidly by tip growth. The control of PT growth properties is vital for the plant, be-cause failure in pollen germination or PT growth, competence, guidance, and communicationwith female tissues and gametophytes all lead to more or less severe sterility. Two redundantCrRLK1L members, ANX1 and ANX2, regulate PT growth (15, 86) (Figure 2). anx1 anx2 double

FER

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Figure 2Schematic representation of Catharanthus roseus receptor-like kinase 1-like protein (CrRLK1L)-mediated signaling in plantreproduction for (a) the female gametophyte (FG) and (b) the pollen tube (PT). (a) FER mediates PT reception, possibly throughsensing yet unknown RALF peptides. The GPI-anchored proteins, TUN and EVN, might influence functionality of FER and itspartners through N-glycosylation. Moreover, FER interacts with the GPI-anchored proteins EN14 and LRE. The latter is required forproper FER localization and possibly acts as a coreceptor for FER, which putatively promotes the function of a yet unknowndownstream Rboh protein triggering ROS accumulation in the FG. This might stimulate Ca2+ influx through a Ca2+ channel. Ca2+ isrequired for FER-dependent translocation of the MLO protein, NTA, to the filiform apparatus (FFA). Moreover, the Rsyn changes itsoscillatory Ca2+ signature upon PT arrival. This is initiated by LRE and FER, whereas the oscillation magnitude appears to bemodulated by NTA. (b) ANX1 and ANX2 govern the pollen CWI pathway, recognizing the RALF4 and RALF19 peptides. TUNmediates proper glycosylation of ANX1 and ANX2, preventing precocious degradation in the ER. ANX1 and ANX2 act upstream ofthe reactive oxygen species (ROS)-producing NADPH-oxidases RbohH and RbohJ, which in turn could positively influence theactivity of the receptor-like cytoplasmic kinase MARIS (MRI). The latter might positively regulate Ca2+-channel activity to maintain asteady tip focus Ca2+ gradient, essential for growth. Ca2+ presumably promotes RbohH and RbohJ activity to maintain CWI duringPT growth. BUPS1 and BUPS2 interact with ANX1 and ANX2, forming a receptor complex for RALF4 and RALF19. These peptidesalso interact with the pollen-expressed LRX8, LRX9, LRX10, and LRX11. When PTs arrive in the vicinity of the ovules, ovule-derivedRALF34 competes with RALF4 and RALF19 for the ANX1/2–BUPS1/2 receptor complex. This possibly shuts down the pollen CWIpathway and triggers the release of sperm cells for double fertilization. Solid arrows represent direct positive interactions; dashedarrows represent activation that could be indirect. Abbreviations: ANX1/2, ANXUR1 and 2; BUPS1/2, BUDDHA’S PAPER SEAL1and 2; CWI, cell wall integrity; EN14, EARLY NODULIN 14; ER, endoplasmic reticulum; EVN, EVAN; FER, FERONIA; GPI,glycosylphosphatidylinositol; LRE, LORELEI; LRX8/9/10/11, LEUCINE RICH REPEAT-EXTENSIN GLYCOPROTEIN8, 9,10, 11; MLO, MILDEW RESISTANCE LOCUS O PROTEIN; Nsyn, nonreceptive synergid; NTA, NORTIA; RALF4/19/34 andRALFL, RAPID ALKALINIZATION FACTOR4, 19, and 34 and RAPID ALKALINIZATION FACTOR-LIKE; Rboh, respiratoryburst oxidase homolog; Rsyn, receptive synergid; SCs, sperm cells; TUN, TURAN; VN, vegetative nucleus.


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PTI:pathogen-associatedmolecular pattern(PAMP)-triggeredimmunity

knockout male mutants are sterile due to precocious rupturing of PTs. Also, overexpression ofANX1 and ANX2 triggers cell wall material over-accumulation in PT tips, probably due to overac-tivation of exocytosis. This subsequently leads to PT growth arrest and membrane invaginations(14). Interestingly, a recent report showed that two other partially redundant pollen-expressedCrRLK1L family members named BUDDHA’S PAPER SEAL1 (BUPS1) and BUPS2 are re-quired for CWI during PT growth with BUPS1 being a major contributor (36). BUPS1 andBUPS2 interact and form complexes with ANX1 and ANX2, and all of them can individually bindto the pollen-expressed RALF4 and RALF19 (Figure 2) (36) (see Section 3.1). This is the firstreport of CrRLK1Ls interacting with each other to form a receptor complex (see also Section3.1). Thus, BUPS1 and BUPS2, as well as ANX1 and ANX2 and their closest homolog, FER,maintain CWI to sustain growth in PTs, trichomes, and root hairs, respectively.

FER also plays a role during plant fertilization (Figure 2). Interestingly, the first fer mutantand its allelic variant sirene (srn) were discovered in the context of a phenomenon called PTovergrowth (31, 47, 110). Normally, during PT reception, the PT enters one of the two synergidcells, the receptive synergid. The latter degenerates, and the PT ruptures to deliver the sperm cells,eventually fertilizing the egg and the central cell. However, in fer and srn female gametophyticmutants, the PT and mutant female gametophyte do not communicate properly. Consequently,the PT fails to rupture and continues to grow, resulting in a nonfertilized female gametophyte.

Interestingly, ROS accumulate at the filiform apparatus during female gametophyte develop-ment in wild-type but not in fer female gametophytes (29). Pistil feeding assays with pharmacolog-ical treatments showed that scavenging ROS or depleting Ca2+ levels in the female gametophytetriggers PT overgrowth (29). Furthermore, the synergids have unique complex cytosolic Ca2+

signatures that they precisely coordinate with PT arrival at the filiform apparatus (89). Whenthese signatures are disturbed pharmacologically or genetically, proper PT reception is abolished.Thus, FER orchestrates the complex male-female gametophytic dialogue during PT receptionthrough ROS and Ca2+ signaling (see Section 3.4).

2.3. Plant Immunity

Plant fertilization shares common aspects with successful plant pathogen infection. Both require aclose cell-cell communication between the host cells and the intruders, e.g., PTs or pathogens. Forplant infection, pathogens come in contact and interact with the plant cell wall and thus modify itsstatus. In turn, plant cells have developed cell wall–sensing mechanisms to perceive these changesand try to fend off these intruders (76, 140). The widely expressed FER plays a major role in plantimmunity (Figure 3), but it is only recently that the precise underlying mechanisms have beenapprehended.

A recent study shows that FER can positively influence pathogen-associated molecular pattern(PAMP)-triggered immunity (PTI). fer-2 and fer-4 mutants are less sensitive to the PAMPs elf18-and flg22-induced ROS burst and more susceptible to Pseudomonas syringae pv. tomato DC3000 (PtoDC3000 COR-deficient) infection (126). Furthermore, FER promotes the association of FLAG-ELLIN SENSITIVE2 (FLS2) with BRASSINOSTEROID INSENSITIVE 1–ASSOCIATEDRECEPTOR KINASE 1 (BAK1) and ELONGATION FACTOR TU RECEPTOR (EFR) withBAK1 in response to flg22 and elf18 treatment, respectively (Figure 3a). Cotreatment with thesecreted peptide RALF23 decreases the FLS2/EFR-BAK1 ligand-induced complex formation,showing that RALF23, by binding FER, has an inhibitory effect on plant immunity. RALF23is secreted as proRALF and processed by SITE-1 PROTEASE (S1P) (125, 126) (Figure 3a).Conclusively, FER apparently acts as a scaffold for plasma membrane–localized pattern recog-nition receptor complexes and thus positively regulates immunity. Interestingly, this study also


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shows that RALF peptides can either activate (RALF1 during root elongation or RALF23 duringseedling growth) (41) or repress (RALF23 during PTI responses) FER signaling (126).

An earlier study found FER to be enriched in detergent-resistant membranes after flg22 treat-ment (52). fer seedlings pretreated with flg22 displayed increased ROS production and mitogen-activated protein kinase (MAPK) activation in response to a second flg22 treatment comparedwith wild-type plants (52). This can be explained in the context of the recent findings, with flg22pretreatment inducing the cleavage of RALF23 (126), which inhibits immunity in wild-type plantsbut not in insensitive fer plants. Moreover, fer seedlings show restricted Pto DC3000 growth (52), aseemingly opposite phenotype to the hypersensitivity of 4- to 5-week-old fer plants to Pto DC3000infection (126). A development-stage-dependent role for FER during immune responses couldexplain these differences.

Surprisingly, ANX1 and ANX2, which are preferentially expressed in pollen, were also foundto play a role during immunity in leaf tissues (77). ANX1 and ANX2 appear to negatively regulate

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Figure 3 (Figure appears on preceding page)

Schematic representation of Catharanthus roseus receptor-like kinase 1-like protein (CrRLK1L)-mediated signaling during immunity inleaf and root tissues. (a) Pathogen-associated molecular pattern (PAMP)-triggered immunity (PTI) signaling in leaves. Perception ofthe bacterial PAMPs flg22 and elf18 triggers BAK1 association with the immune receptors FLS2 and EFR, respectively. FER, inputative cooperation with LLG1, acts as a scaffold for FLS2/EFR-BAK1 ligand-induced complex formation. ANX1 and possibly ANX2negatively regulate PTI by putatively competing with FLS2 for interaction with BAK1. BAK1 activates BIK1, which phosphorylatesthe ROS-producing RbohD and also activates immune responses via MAPKs and WRKY46. S1P is required for processingproRALF23 and proRALF33 into their active forms. The latter bind FER and negatively regulate ligand-induced FLS2/EFR-BAK1association. (b) Effector-triggered immunity signaling in leaves. Pseudomonas syringae effectors AvrB, AvrRpm1, and AvrRpt2 aresecreted into the host cell via a type III secretion system. All three effectors target RIN4. AvrB and AvrRpm1 trigger RIN4phosphorylation by RIPK, and AvrRpt2 causes RIN4 degradation. Both RIN4 modifications are sensed by the nucleotide-bindingdomain leucine-rich repeat proteins RPM1 and RPS2, thereby triggering immunity. Phosphorylated RIPK is sensed by RPM1, whiledegraded RIN4 is perceived by RPS2. Additionally, phosphorylated RIN4 activates proton pumps AHA1 and AHA2, triggeringapoplast acidification. Both RPM1 and RPS2 are inhibited by ANX1 and possibly ANX2, which downregulate immunity. (c) Fungalhijacking of immunity signaling in roots. Fusarium oxysporum produces the secreted peptide F-RALF that could mimic RALF1,RALF23, or both. F-RALF likely binds to FER and thereby putatively inhibits PDF1.2 expression, which contributes to immunity, andAHA1 and AHA2 activity. As a result, the apoplastic pH rises, triggering phosphorylation of the F. oxysporum MAPK FMK1, and thehost infection potential increases. In parallel, F-RALF could mimic RALF23-triggered inhibition of FER-dependent immuneresponses. Solid arrows represent direct positive interactions; dashed arrows represent activation that could be indirect; solid blunt-endlines represent direct negative interactions; dashed blunt-end lines represent inhibition that could be indirect. Abbreviations: AHA1/2,ARABIDOPSIS H+-ATPASE 1 and 2; ANX1/2, ANXUR 1 and 2; AvrB, Avirulence protein B; AvrRpm1, Avirulence proteinResistance to Pseudomonas syringae pv. maculicola 1; AvrRpt2, Avirulence protein Resistance to Pseudomonas syringae pv. tomato 2; BAK1,BRASSINOSTEROID INSENSITIVE 1–ASSOCIATED RECEPTOR KINASE 1; BIK1, BOTRYTIS-INDUCED KINASE1;EFR, ELONGATION FACTOR TU RECEPTOR; elf18, elongation factor Tu peptide (first 18 amino acids); FER, FERONIA;flg22, flagellin epitope 22; FLS2, FLAGELLIN SENSITIVE2; FMK1, FUSARIUM OXYSPORUM MITOGEN-ACTIVATEDPROTEIN KINASE 1; LLG1, LORELEI-LIKE GPI-ANCHORED PROTEIN 1; MAPK, MITOGEN-ACTIVATED PROTEINKINASE; P, phosphate group; RAC, plant GTPases related to animal Rac GTPases; RALF23/33, RAPID ALKALINIZATIONFACTOR 23 and 33; RbohD, respiratory burst oxidase homolog D; RIN4, RESISTANCE TO PSEUDOMONAS SYRINGAE PV.MACULICOLA 1–INTERACTING PROTEIN 4; RIPK, RESISTANCE TO PSEUDOMONAS SYRINGAE PV. MACULICOLA1–INDUCED PROTEIN KINASE; ROP, plant GTPases related to animal Rho GTPases; ROS, reactive oxygen species; S1P,SITE-1 PROTEASE; WRKY46, WRKY TRANSCRIPTION FACTOR 46.

both PTI and effector-triggered immunity (77). Indeed anx1, anx2, and anx1 anx2 mutant plantsexhibit increased resistance to Pto DC3000 infection, as well as enhanced ROS production andMAPK activation in response to flg22 compared with wild-type plants. ANX1 associates withFLS2, BAK1, and BOTRYTIS-INDUCED KINASE 1 (BIK1), but flg22 treatment stimulatesANX1 association with BAK1, thereby potentially blocking the FLS2/BAK1 complex formationand subsequently attenuating PTI signaling (Figure 3a). Furthermore, ANX1 associates withthe nucleotide-binding domain leucine-rich repeat (NLR) protein complexes and destabilizesthe NLR protein RPS2 (Figure 3b), thereby suppressing RPS2-mediated cell death and defenseresponses. Thus, FER and ANX1, despite their close homology, function mechanistically antag-onistically in modulating pattern recognition receptor complexes. It would be intriguing to studywhether ANX1-dependent negative regulation of PTI signaling is also modulated by RALF pep-tides and whether ANX1 and FER compete for their association with the FLS2/BAK1 complex.Importantly, ANX1 also negatively regulates effector-triggered immunity responses by interactingwith the NLR receptor complexes, which are yet to be investigated for FER.

In the context of fungal infection, fer mutant plants are more resistant to Golovinomyces oron-tii (54) and Fusarium oxysporum (79). Concordantly, in fer plants, higher transcription levels ofPLANT DEFENSIN 1.2 (PDF1.2), a gene encoding a small peptide with antifungal activity, aredetected (27) (Figure 3c). However, these findings do not necessarily point out that FER nega-tively regulates immunity in this context, but rather that FER and its dependent signaling pathwaysconstitute a potent susceptibility target coveted by some pathogenic fungi (see also Section 3.1).


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2.4. Hormone Signaling

Plant hormones regulate key processes such as plant growth and defense requiring dynamic cellwall remodeling. Thus, it is not surprising that the proposed cell wall sensor subfamily CrRLK1Lis involved in crosstalks with several hormone pathways. For example, seedlings of loss-of-functionmutants in FER or downstream interactors GEF1/4/10 (GUANINE EXCHANGE FACTORS1/4/10) or ROP11/ARAC10 (RHO OF PLANTS 11/RAC-LIKE GTP BINDING PROTEIN 10)are hypersensitive to abscisic acid (ABA) (146). In response to ABA, they display higher ROSlevels in guard cells, increased stomatal closure, and stronger growth inhibition of seedlings androots. FER apparently inhibits ABA signaling via the phosphatase ABA INSENSITIVE 2 (ABI2)(146). Also, ABI2 directly interacts with and dephosphorylates FER to counter RALF1-mediatedFER activation (Figure 1) (20). Thus, FER is a negative regulator of ABA signaling.

In contrast, fer seedlings are insensitive to auxin-stimulated root hair elongation; however, theabsence of elongation in precociously bursting root hairs cannot be specifically attributed to auxin-signaling insensitivity (30, 65). Also, FER is required for transient alkalinization of the extracellularmatrix in roots following auxin treatment (8). This affects cellular root expansion during thegravitropic response. In this case, FER seems to be positively influencing auxin signaling.

Regarding brassinosteroid (BR) signaling, BRs were previously reported to regulate the expres-sion of FER, HERK1, HERK2, and THE1 through the BR-responsive transcription factor BES1(37). fer seedlings are partially BR insensitive in the dark, whereas they are hypersensitive in thelight (27). The FER-dependent BR response likely antagonizes ethylene signaling in hypocotylsof etiolated seedlings (27).

Indeed, fer plants are also hypersensitive to ethylene, showing severe hypocotyl shorteningin the presence of saturating ethylene levels in the dark (27). Additionally, fer mutants containhigher levels of S-adenosylmethionine (SAM) and ethylene, with SAM being part of the ethylenebiosynthetic pathway (78). Interestingly, overexpression of SAM SYNTHASE1 (SAM1) or SAM2trigger growth-related phenotypes similar to those of the fer mutant. Thus, FER might negativelyregulate SAM synthesis by interacting with SAM1 and SAM2 (Figure 1). Taken together, FER’scrosstalk with hormone pathways is complex and offers many points to be addressed in futureresearch. As of now, it is unclear if and how other CrRLK1Ls also modulate hormonal pathways.

2.5. Abiotic Stress Tolerance

Hormone signaling interacts with stress-mediated signaling in plants, and in particular with abi-otic stress responses. For the plant, one important feature during stress responses is synthesisand remodeling of the cell wall. Although abiotic stresses seem to negatively regulate the geneexpression of all CrRLK1Ls (69), so far FER has been almost exclusively implicated in variousabiotic stress responses. For example, fer seedlings are strongly hypersensitive to salt, cold, andheat stress (20), as well as lithium treatment (41). However, when treated with mannitol, they arehyposensitive to osmotic stress (20).

In addition, fer plants are hypersensitive to sucrose and overaccumulate starch (55, 145). Theyalso display sucrose-induced cell wall defects and elevated production of the stress-associatedpigment anthocyanin. Furthermore, fer seedlings are insensitive to phosphate limitation (46).Despite the various implications of FER in abiotic stress responses, it remains to be investigatedhow FER mediates these and whether other CrRLK1Ls are involved in coping with abiotic stress.

3. SIGNALING PARTNERS OF MALECTIN-LIKE RECEPTOR KINASES

Recent studies on the different signaling pathways governed by FER, THE1, ANX1, and ANX2have shed light on the similarities between the different recruited signaling partners. The list


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GPI:glycosylphosphati-dylinositol

RLCK: receptor-likecytoplasmic kinase

of common signaling constituents include RALF peptides, glycosylphosphatidylinositol (GPI)-anchored proteins, RAC/ROP GTPases, and receptor-like cytoplasmic kinases (RLCKs), as wellas ROS and Ca2+ signaling.

3.1. RALF Peptides as Ligands for Malectin-Like Receptor Kinases

RALF1 emerged in a screen for endogenous signaling peptides regulating transient cytoplasmicCa2+ changes (40). The RALF family in Arabidopsis consists of approximately 37 members (16).RALF1 treatment of roots induces a rapid elevation in Ca2+ concentration of the root surface cells.This pointed toward RALF1 mediating Ca2+-dependent signaling events through a cell surfacereceptor. Recently, FER was identified as this cell surface receptor with RALF1 directly binding tothe FER ectodomain (41). Consistently, radio-labeled RALF1 showed reduced binding to fer cellmembranes compared with wild type (41). Also, RALF1 rapidly prompts phosphorylation of FERand ERU/CAP1 (41). Although root and hypocotyl elongations in wild-type seedlings are inhibitedby a 2- to 3-day-long RALF1 treatment (10, 88), fer mutants are insensitive to RALF1 (41). Mu-tants in ERU/CAP1 display a short root hair phenotype but are normally sensitive to RALF1 (41).

RALFs also play a role in plant defense. RALF1 was proposed to regulate cell growth via FER-dependent phosphorylation of the proton pump AHA2 (41). F. oxysporum, among other fungal phy-topathogens (129), produces its own F-RALF to mimic RALF1 (79). Secreted F-RALF presumablybinds FER, leading to negative regulation of AHA2 and thus apoplastic alkalinization (79). ThispH increase promotes phosphorylation of FMK1, a MAPK of F. oxysporum, thereby increasing thehost infection potential (Figure 3c). Interestingly, the closest homolog of F-RALF is RALF23;thus, it is plausible that F-RALF may also influence the assembly of some immune receptorcomplexes.

Recently, more RALFs capable of regulating FER were identified, namely RALF17, RALF23,RALF33, and the more divergent RALF32 (126). RALF23, RALF 33, and RALF32 peptidestrigger FER-dependent seedling growth inhibition similar to that triggered by RALF1. RALF23and RALF33 are more closely related to each other than to RALF32 as both are produced asproRALFs and subsequently cleaved by S1P (125, 126) (Figure 3a). Also, both negatively regulateimmunity, whereas RALF32 does not (126). Like RALF1, RALF23 binds to the FER ectodomain.Interestingly, RALF23, probably through binding to FER, reduces FLS2/BAK1 and EFR/BAK1complex formations induced by flg22 and elf18, respectively. This suggests that the ligand-inducedcomplex formation between FLS2/EFR and their coreceptor BAK1 is promoted by FER andinhibited by RALF23. Moreover, RALF17, which lacks a propeptide region and thus is not atarget of S1P, triggers ROS burst in leaves in a FER-dependent manner (126).

Two recent studies shed further light on the relationships between RALF peptides andCrRLK1Ls (36, 80). First, it was shown that knockdown and knockout mutants for the pollen-expressed RALF4 and RALF19 display PT bursting phenotypes similar to those displayed by anx1anx2 and bups1 bups2 double mutants (36, 80). Genetic studies positioned ANX1 and MARIS (seealso Section 3.3) downstream of RALF4 and RALF19 (80). Concordantly, Ge et al. (36) showedthat RALF4 and RALF19 bind the ECDs of ANX1, ANX2, BUPS1, and BUPS2 with high affini-ties, directly implicating those peptides as ligands for the ANX1/2–BUPS1/2 receptor complex(Figure 2). These studies demonstrate that the CWI pathway that prevents precocious PT burstingduring growth through the female tissues is controlled by a ligand-receptor complex composedof RALF4, RALF19, ANX1, ANX2, BUPS1, and BUPS2 and is a cell-autonomous autocrinepathway. Ge et al. (36) also reported that treatment with RALF34, a RALF homolog expressed inovules, triggers PT bursting in vitro. RALF34 can outcompete RALF4 and RALF19 for bindingANX1, ANX2, BUPS1, and BUPS2 (36). This indicates that ovule-secreted RALF34, and possibly


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other maternal RALFs, could constitute paracrine signals that disrupt the autocrine RALF4/19-dependent pathway during the late stage of fertilization so that the PT precisely ruptures and de-livers its sperm cells when entering the ovules. However, this would contradict the hypothesis thatmaternally derived ROS are directly inducing PT bursting during PT reception (29). Finally, Mec-chia et al. (80) showed that RALF4 also interacts with apoplastic pollen-expressed leucine-rich re-peat extensin proteins (LRXs). Interestingly, loss-of-function triple mutants lrx8 lrx9 lrx10 and lrx8lrx9 lrx11 not only display PT bursting phenotypes similar to those of ralf4 ralf19 (36), but were alsoinsensitive to RALF4-induced PT growth inhibition (Figure 2) (80). How these pollen-expressedLRX proteins and CrRLK1L receptors collaborate to maintain CWI remains to be determined.

In the future, it will be interesting to see whether further roles in immunity, fertilization, orgrowth-related processes will be attributed to other RALF peptides and, naturally, whether otherRALF peptides can bind other CrRLK1Ls. It would be important to study in detail which part ofthe ECD of CrRLK1Ls is important for binding RALF peptides. Nonetheless, the findings that(a) RALF peptides can either activate or repress CrRLK1Ls, (b) several RALF peptides bind tothe same receptor, and (c) different CrRLK1Ls can interact with each other multiply the differentfine-tuning possibilities of the numerous CrRLK1L-dependent pathways.

3.2. Glycosylphosphatidylinositol-Anchored Proteins

In 2008, lorelei (lre) was described as a mutant with the same PT overgrowth phenotype as fer/srn(17). LRE is expressed in the synergid cells prior to fertilization and encodes a small plant-specificputative GPI-anchored protein. It localizes to the filiform apparatus (Figure 2). LRE requiresFER expression in the female gametophyte to be functional for PT reception. Yet FER localizationto the filiform apparatus is dependent on the presence of LRE (72). This indicates that FER andLRE are interdependent of each other and that LRE has a dual function: It chaperones FER onits way from the endoplasmic reticulum (ER) to the filiform apparatus and could act as coreceptorfor FER at the filiform apparatus for a still unidentified ligand (Figure 2). Furthermore, nullmutants of LORELEI-like-GPI-AP1 (LLG1), the closest relative of LORELEI, are fully fertile anddo not exhibit reproductive defects (134). Interestingly, both LLG1 and LRE bind to the ECD ofFER required for FER functionality (65) (Figure 1). LLG1 is expressed in seedlings and interactswith FER in the ER and at the cell surface. llg1 mutants phenocopy the growth, development,and signaling-related phenotypes of fer mutants—except for the LRE-dependent PT reception.Moreover, FER is retained in the ER in llg1 mutants pointing toward a general LLG1/LRE-dependent shuttling of FER from the ER to the cell surface. Also, both RHO-GTPASE OFPLANTS 2 (ROP2) and RALF1 directly interact with FER, LRE, and LLG1. This indicatesthat both LRE and LLG1 act as chaperones and possibly coreceptors for FER. Interestingly,LLG1 also plays a role in immunity (118). llg1 plants are more susceptible to various pathogenattacks. LLG1 associates with FLS2, EFR, and BRASSINOSTEROID INSENSITIVE 1 (BRI1).It also is required for flg22-induced BIK1 phosphorylation and ROS production (Figure 3a)(126). However, it is not clear whether the newly identified role of LLG1 during immunity isdependent on its partner FER. Thus, although LRE and LLG1 are both chaperones and possiblycoreceptors of FER, they act in different contexts. In the future, it would be important to testwhether LRE or any of the LLG1, LLG2, and LLG3 proteins associates with other CrRLK1Lmembers.

Two other mutants displaying PT overgrowth, turan (tun) and evan (evn), were later discovered(68) (Figure 2). Both corresponding proteins are involved in protein N-glycosylation in the ER andpossibly in GPI-anchor synthesis. TUN is a putative UDP-glycosyltransferase protein, and EVN isa putative dolichol kinase. In addition, both display pollen phenotypes: EVN is required for proper


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pollen development, whereas TUN is required for CWI, displaying similar bursting phenotypesas anx1 anx2 mutant pollen. Strikingly, neither ANX1-YFP nor ANX2-YFP fluorescence couldbe detected in transformed tun mutant pollen grains, indicating that the precocious bursting oftun PTs is caused by the absence of ANX1 and ANX2. Thus, TUN seems to be involved inthe proper glycosylation of ANX1 and ANX2, which otherwise are degraded by the endoplasmicreticulum–associated degradation pathway (68). However, how TUN and EVN function duringPT reception awaits further investigation.

Another group of GPI-anchored proteins, the early nodulin-like proteins (ENs) 11–15 arealso essential for fertilization (Figure 2) (45). They accumulate at the filiform apparatus and inRNAi-en mutant ovules; wild-type PTs show fer-like PT overgrowth, albeit at low frequency.Interestingly, EN14, but not EN15, strongly and specifically binds to the FER ECD and weaklyto LRE. Therefore, it remains important to clarify which ENs are really required for PT receptionand how ENs precisely modulate FER function during PT reception.

3.3. Receptor-Like Cytoplasmic Kinase–Mediated Signaling

RLCKs were recently discovered to be involved in CrRLK1L-dependent pathways (12, 28). Inthe context of tip growth, the MARIS (MRI) kinase was identified as a positive regulator ofthe ANX-dependent PT growth pathway following an anx1 anx2 sterility suppressor screen (12)(Figure 2). MRI is a membrane-localized member of the Pto-interacting (Pti)-like subfamily, alsoknown as RLCK-VIII. A strong anx1 anx2 suppressor was identified harboring a R240C mutationin the conserved kinase domain of MRI. Interestingly, MRI loss-of-function mutants display PTbursting like anx1 anx2 plants and root hair bursting like fer mutants (12, 67). Expression of themutant form MRIR240C, but not MRI, could rescue both anx1 anx2 PT and fer root hair burstingphenotypes, showing that MRIR240C is an overactive MRI variant. This MRI variant was alsorecently successfully used to genetically link RALF4 and RALF19 to the ANX1-, ANX2-, andMRI-dependent CWI pathway in PTs (80). Thus, MRI plays a positive role in the ANX1- andANX2-dependent PT and in the FER-dependent root hair CWI pathways.

An RLCK acting downstream of FER is RESISTANCE TO PSEUDOMONAS SYRINGAEPV. MACULICOLA 1–INDUCED PROTEIN KINASE (RIPK). RIPK, a member of the RLCK-VIIa subfamily, directly interacts with FER (Figure 1) but not with ANX1 and ANX2 (28). Inter-estingly, RIPK is phosphorylated by FER in a RALF1-dependent manner (28). ripk mutants havedefects similar to those of fer-4 mutants, regarding RALF1 insensitivity, primary root growth, androot hair development. Also, RIPK overexpression partially rescues these fer-4 defects, showing thatRIPK is indeed a positive downstream component of the RALF1/FER-dependent pathway. Fur-thermore, RIPK phosphorylates RPM1-INTERACTING PROTEIN 4 (RIN4) in the presenceof P. syringae effectors AvrB and AvrRpm1 (70) (Figure 2). In response to RIN4 phosphorylation,AHA1 activity is increased, and stomatal apertures are widened, facilitating pathogen entry on theplant surface (60). However, RIN4 phosphorylation is sensed by the NLR protein RPM1, whichtriggers immunity. Interestingly, another P. syringae effector, AvrRpt2, has previously been shownto mediate degradation of RIN4. Yet the NLR protein RPS2 senses this and triggers immuneresponses (3, 75). In this context, it is noteworthy that ANX1 appears to interact with both RPM1and RPS2. It is unclear whether RIPK also contributes to FER’s positive (126) or ANX1’s negativerole during immunity (77).

The RLCK-VII-member BIK1 should also be mentioned. As described in Section 2.3,FER and ANX1 regulate FLS2-BAK1 complex formation in opposite ways (126), and ANX1interacts with BIK1 (77). Upon flg22 perception, BAK1 phosphorylates BIK1, which directly


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Rboh: respiratoryburst oxidase homolog

ROP: Rho-GTPaseof plants

transphosphorylates BAK1 and FLS2 (73) (Figure 3a). Interestingly, the flg22-induced phos-phorylation of BIK1 requires LLG1 (118). Note that BIK1 also phosphorylates respiratory burstoxidase homolog D (RbohD) in the process (66). However, whether fer hyposensitivity or anx1hypersensitivity to flg22 treatment depends on functional BIK1 remains to be tested.

3.4. RAC and Rho-GTPase of Plants Signaling

RAC and Rho-GTPases of plants (ROPs) are major molecular hubs in plants (91, 92) that activatesignaling pathways by switching between an inactive GDP-bound and an active GTP-bound state.This requires GTPase-activating proteins and guanine exchange factors (GEFs), respectively (11).RAC- and ROP-dependent signaling are important for regulation of polarized cell growth in PTsvia Rop-interactive CRIB motif–containing proteins (RICs) (143) and in root hairs (21) via theRHO dissociation inhibitor SCN1 (19). Furthermore, ROP2 and ROP6 mediate jigsaw puzzleformation in pavement cells via auxin-dependent activation (33, 144). Interestingly, cvy1, fer, andllg1 mutants all display pavement cell shape phenotypes (35, 65). Also, ROPGEF1, ROPGEF7,ROPGEF10, ROPGEF14, and ROP2 directly interact with the FER kinase domain (30)(Figure 1). ROP2 further interacts with the N-terminal part of RbohD (65), although the biolog-ical significance of this interaction remains to be demonstrated. Interestingly, fer mutant seedlingscontain lower levels of active RAC or ROPs compared with wild-type plants, and they accumulatereduced levels of NADPH oxidase-dependent, auxin-regulated ROS in roots. Upregulation ofRAC or ROP signaling rescues the aforementioned phenotypes in the weak fer-5 allele but not inthe strong fer-4 allele (30).

Finally, as described in Section 2.4, FER also interacts with ROP11/ARAC10 and negativelyregulates ABA signaling via ABI2 (Figure 1) (146). The involvement of RAC and ROPs in signalingpathways controlled by CrRLK1Ls other than FER has not yet been established.

3.5. NADPH-Dependent Reactive Oxygen Species and Ca2+ Signaling

Last activated RAC and ROPs target the ROS-producing plant NADPH oxidases (19, 142),termed Rbohs (132). Plant Rbohs consist of a C-terminal NADPH-binding site, a flavin adeninedinucleotide (FAD)-binding region, six TMDs, and a putative EF-hand Ca2+-binding motifin the extended N-terminal region. A. thaliana contains 10 Rbohs with versatile functions,RbohA–RbohJ (9). To date, RbohC, RbohD, RbohF, RbohH, and RbohJ have been implicatedin CrRLK1L-mediated pathways.

RbohC, also known as ROOT HAIR DEFECTIVE 2 (RHD2), produces ROS during root hairgrowth (32). rhd2 mutants exhibit moderately stunted roots and very short root hairs, which seem-ingly lack ROS and a tip-localized Ca2+ gradient. At closer examination, rhd2 root hairs remainshort as they precociously burst, reminiscent of fer root hairs (30, 87). Furthermore, fer roots displaylower ROS levels than wild type, a phenotype rescued by overexpressing ROP2, suggesting thatFER positively regulates RbohC-dependent ROS production through ROP2 signaling (30). How-ever, the genetic interaction between RHD2 and either ROP2 or FER has not been yet established.

RbohD and RbohF putatively act downstream of THE1 in response to cell wall damage (25).Cell wall damage sensing apparently consists of two phases (early and late) with RbohD and -Facting in the late phase (25). THE1, RbohD, and RbohF are required for both isoxaben-inducedectopic lignification and ROS production. In addition, THE1, RbohD, and RbohF repress jas-monic acid production after isoxaben treatment. RbohD is activated by exogenous ROS (131) andsynergistically by phosphorylation and Ca2+ (96). Furthermore, RbohD and RbohF contributeto plant immunity (58, 83, 130), but whether this function belongs to a CrRLK1L-dependentpathway remains to be elucidated.


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Finally, RbohH and RbohJ act downstream of ANX1 and ANX2 in regulating CWI duringPT growth, as ANX1 overexpression phenotypes were at least partially dependent on functionalRbohH and RbohJ (14) (Figure 2). Up to 80% of rbohH rbohJ pollen precociously burst in vitro.The remaining grains produce PTs that eventually lose their integrity. Interestingly, these still-growing PTs display reduced ROS levels and an unsteady tip-focused Ca2+ gradient (14, 51).Concordantly, rbohH rbohJ PTs show an oscillatory growth behavior that is not observed in wild-type PTs (14, 59). Thus, the ANX1- and ANX2-dependent pathway regulates ROS and Ca2+

homeostasis.ROS and Ca2+ are also essential for the dialogue between the PT and female gametophytes dur-

ing PT reception. Synergid-derived ROS mediate PT discharge in a Ca2+-dependent manner (29),and the female gametophyte exhibits distinct Ca2+ signatures from PT arrival to double fertiliza-tion (26, 38, 49, 89). The two synergids show different oscillatory Ca2+ signatures during PT recep-tion (89). The receptive synergid, designated to undergo programmed cell death, changes its Ca2+

dynamics in response to PT growth behavior. Aberrant Ca2+ oscillations in the receptive synergid,as detected in lre or fer mutants, abolish programmed cell death events in both the PT and receptivesynergid and lead to PT overgrowth (Figure 2). Consequently, FER and LRE apparently initiateboth the Ca2+ oscillations in the synergids and the response to changes in PT calcium dynamics.

Ngo et al. (89) further investigated Ca2+ signatures in nortia (nta) mutant synergids. NTA isa protein of the MLO family required for powdery mildew susceptibility (1). It contains a signalpeptide, seven TMDs, and a calmodulin domain for binding Ca2+. Intriguingly, nta mutant plantsdisplay fer-like PT overgrowth (54). Also, relocalization of NTA-containing vesicles to the filiformapparatus is FER dependent (Figure 2) (54). However, unlike FER and LRE, NTA presumablymodulates the magnitude of Ca2+ oscillations in the PT and receptive synergid (89).

Note that, although ROS and Ca2+ play key roles in this complex male-female gametophyticdialogue culminating with the sperm delivery, the underlying Rboh- and Ca2+ channel–encodinggenes have not yet been identified.

4. COMPARATIVE AND FUNCTIONAL GENOMICS OF THEMALECTIN-LIKE RECEPTOR KINASES

Initial CrRLK1L studies focused mainly on the characterization of the A. thaliana family members.Recently however, CrRLK1L homologs have gained increasing attention in a number of strep-tophytes (comprising embryophytes and charophycean green algae), revealing both functionallysimilar and distinct roles of their respective CrRLK1L homologs and shedding more light on thegenomic evolution of the CrRLK1L subfamily.

4.1. Origin of Receptor-Like Kinases and Emergence of theCrRLK1L Subfamily

RLKs show the closest relation to the Pelle gene family of metazoans (multicellular animals). TheRLK/Pelle superfamily itself is thought to be an evolutionarily ancient one, with representativehomologs in unicellular eukaryotes, plants, and animals but not in fungi (61, 121). RLKs, bycontrast, are exclusive to the Viridiplantae (green algae and land plants) and likely expandedearly in streptophytes (112, 120). Certain RLK subfamilies, such as the ECD-lacking RLCKs,are already found in chlorophycean algae (62, 82, 120), the sister clade to all streptophytes; how-ever, CrRLK1Ls most likely arose from an RLK progenitor gene in the streptophyte ancestor(Figure 4). The early expansion and diversification of RLKs may well have been associated withkey events in eukaryote and plant evolution, such as the development of multicellularity or theconquering of terrestrial habitats more than 470 million years ago (120).


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Figure 4 (Figure appears on preceding page)

Catharanthus roseus receptor-like kinase 1-like proteins (CrRLK1Ls) and plant evolution. Schematic representation of the phylogenetichistory of the green plants (Viridiplantae), including the key events of CrRLK1L gene evolution (blue annotations) and evolutionary keyapomorphisms, possibly related to CrRLK1L gene evolution ( yellow annotations). CrRLK1L gene numbers (shown in square brackets)were inferred as follows (left to right): Drosophila melanogaster (63, 120), Chlamydomonas reinhardtii (82), Closterium peracerosum-strigosum-littorale complex (43), Marchantia polymorpha (44, 112), Physcomitrella patens (61, 108), Selaginella moellendorffii (7, 61), Azolla, Picea abies(94), Amborella trichopoda (2), Oryza sativa (103), Arabidopsis thaliana (69), Gossypium raimondii (93), and Solanum lycopersicum (111).Phylogenetic relationships of the single taxa were adopted from the works of Karol (50), Rensing (107), and Wickett et al. (139).Abbreviations: PTO, protein kinase Pto; RLK, receptor-like kinase.

4.2. Domain Organization and Genomic Evolution of CrRLK1Ls

The primary criterion characterizing CrRLK1Ls at the protein level is their unique and evolu-tionarily ancient domain organization pattern. In addition to an intracellular kinase domain and aTMD, which is shared with other RLKs, CrRLK1Ls contain an MLD in their extracellular region;this was first described for the CrRLK1Ls of A. thaliana (13). The MLD is composed of two mod-ules with limited similarity to the disaccharide-binding malectin of animals (Figure 1) (113). PlantMLDs were therefore thought to likely bind carbohydrate-rich ligands, such as cell wall compo-nents or glycosylated proteins. However, no such binding has been reported so far. Nonetheless,a specific ligand family of secreted peptides called RALFs binds to the ECD of CrRLK1Ls (36,41, 126). The ligand family appears to be just as diverse and widespread as its receptors (16).

Upon the establishment of the CrRLK1L receptor type early in plant evolution, this general do-main organization pattern was conserved, and the comparison of CrRLK1L copy number of extantland plants suggests the drastic expansion of the gene subfamily throughout evolution (Figure 4).

4.2.1. Nonseed plants. In the charophycean green alga Closterium and the liverwort Marchan-tia polymorpha, only one CrRLK1L homolog is known (43, 44), whereas the genomes of themoss Physcomitrella patens (108) and the lycophyte Selaginella moellendorffii (7) encode six and twoCrRLK1L homologs (Figure 4), respectively. Unfortunately, little is known to date about thepresence and function of CrRLK1Ls in other major nonseed plant lineages due to the poor cov-erage of sequenced nonseed plant genomes (107). Additionally, the controversial phylogeneticrelations of the bryophyte lineages (39, 139), and the existence of bryophytic genome duplication(108) and gene loss events, impede drawing definite conclusions on the evolution of CrRLK1Lgene numbers in seedless plants. However, considering the relatively high numbers of CrRLK1Lhomologs in seed plants compared with nonseed plants (63), global expansion of CrRLK1Ls haslikely taken place during land plant evolution.

4.2.2. Gymnosperms and early monocots. Although the amount of data on nonseed plantCrRLK1Ls is scarce, more is known for seed plants (Spermatophyta). The genomes of thegymnosperm Picea abies (94) and the early-diverging angiosperm Amborella trichopoda (2) containseven and nine CrRLK1L homologs, respectively (Figure 4). If these gene numbers representthe approximate genomic state of the common spermatophytic ancestor, the CrRLK1L subfamilyappears to have significantly expanded and functionally diversified alongside the evolution fromnonseed to seed plants.

4.2.3. Core monocots and dicots. Data on CrRLK1L gene numbers in angiosperms are quitecomprehensive, pointing toward a drastic gene expansion throughout evolution. Such expansions,most likely through segmental or whole-genome duplication and tandem duplication events, havebeen previously reported for Populus trichocarpa (poplar) (62), Oryza sativa (rice) (62, 90), and


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Arabidopsis RLKs (124). At least three rice CrRLK1Ls have been suggested to be tandemly dupli-cated (90). Despite the high evolutionary distance between Oryza and Arabidopsis of approximately160 million years (the monocot-dicot split), a comparatively high degree of orthology can befound between their CrRLK1L homologs (57, 90, 103). This indicates (a) the establishment oftheir genetic progenitors before the divergence of both species and (b) the putative conservationof similar gene functions among O. sativa and A. thaliana CrRLK1L orthologs. The suggestedancestral gene number of 19 CrRLK1Ls in both Arabidopsis and Oryza (122) might explain suchsimilar gene sets and the orthologous grouping in the recent species.

CrRLK1L gene numbers appear to have been conserved in the dicot lineages, as similar numbersof CrRLK1L homologs can be found in representative asterids [Solanum lycopersicum, 23 homologs(111)] and rosids [Pyrus bretschneideri, 26 homologs (57); A. thaliana, 17 homologs (69)] (Figure 4);exceptions were the cotton species Gossypium raimondii (diploid; 44 homologs) and Gossypium hirsu-tum [tetraploid; 79 homologs (93)], possibly originating from multiple polyploidization events (99,148) and putatively resulting in functional redundancy of cotton CrRLK1Ls (93). Such frequentpolyploidization and genomic expansion events in angiosperms ensure the availability of geneticprecursors (such as CrRLK1L gene copies), major requirements for the establishment of evolu-tionary new functions and morphological traits through genetic neofunctionalization (74, 106).

4.2.4. The Pto/CrRLK1L relationship. Interestingly, CrRLK1Ls of the basal eudicotyledonousspecies Platanus × acerifolia were closely linked to the Pto group of RLKs (first found in thesolanaceous tomato) based on their structural and phylogenetic relationship (101). The tomatoPto kinase is an intracellular receptor for the type III effectors AvrPto and AvrPtoB secreted inplant cells by P. syringae pv. tomato to trigger ETI (97). As Pto-like genes (sensu stricto) only seemto be present in asterids (mostly Solanaceae), the comparatively recent evolution of Pto genesfrom CrRLK1Ls was proposed (101, 136). This idea is further supported by (a) the lack of Pto-like homologs in rosids like A. thaliana, (b) the highest sequence similarity of tomato Pto to theArabidopsis CrRLK1L intracellular domains (Supplemental Table 2), and (c) the high similarityof solanaceous MLD-containing Pto-like proteins to both A. thaliana CrRLK1Ls and tomato Pto(136). Given the similarity between Pto-like proteins and CrRLK1Ls, the physical interactionbetween Pto and RLCKs of the Pti-like group (117) may explain the role of MRI (a Pti-likeRLCK itself) as a downstream component of the ANX1-, ANX2-, and FER-dependent CWIpathways (12). Consequently, CrRLK1L-mediated CWI signaling may include physical bindingof CrRLK1Ls to Pti-like proteins, such as MRI. It will be fascinating to study whether such closerelations can be confirmed in additional nonsolanaceous species. Finally, one could speculate thatasterid plants have developed Pto-like proteins as an adaptive decoy to protect the importantCrRLK1L kinase domains from being manipulated by pathogen effectors.

4.3. Preterrestrial Evolution and the Conquering of Land: FunctionalConservation and Divergence of CrRLK1Ls

Functions for CrRLK1Ls homologs revealed in basal organisms as early as the charophycean greenalgae and in embryophytes other than the model flowering plant A. thaliana are presented here.

4.3.1. Charophycean algae. Modern land plants (embryophytes) likely evolved from a charo-phycean ancestor (50). Some charophycean algae reproduce sexually by sperm cell transmissionthrough osmosis-driven formation of conjugatory papillae, including unicellular, nonflagellatecharophycean algae of the Closterium peracerosum-strigosum-littorale complex. Knocking downthe unique membrane-localized CrRLK1L-homolog CpRLK1 leads to abnormally elongated


Supplemental Material

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https://www.annualreviews.org/doi/suppl/10.1146/annurev-arplant-042817-040557


conjugatory papillae and incapability of gamete release, resulting in reduced reproductive compe-tence (43). Thus, CpRLK1 could regulate osmotic pressure to facilitate a controlled gamete releaseduring successful conjugation. On the basis of these findings, the ancient CrRLK1L progenitorgene may have already functioned as a cell wall sensor (43).

4.3.2. Nonseed land plants. During the conquering of terrestrial habitats, approximately 470million years ago (138), plants had to develop elaborate strategies to meet the demands of theirsessile life style. This included facilitation of substrate anchoring and water and nutrient uptake,as well as horizontal distribution via vegetative growth. In bryophytes, representing descendantsof the earliest land plants, those duties were carried out by specialized cell types that elongate bytip growth, namely rhizoids and protonema (18, 81). Interestingly, in the liverwort M. polymorpha,two RLK homologs were recently identified through an extensive screen for rhizoid growthdefects. Knockout of both the CrRLK1L homolog MpTHE1 and the RLCK homolog MpPti,resulted in loss of CWI in rhizoids (44), similar to the premature bursting of tip-growing PTsand root hairs of A. thaliana anx1 anx2, fer, and mri mutants. These exciting findings suggestthe functional conservation of CWI-sensing mechanisms in tip-growing cells via CrRLK1Lsand Pti-like RLCKs throughout land plant evolution. Considering the multiple functions ofCrRLK1Ls in flowering plants, it would not be surprising that knocking out MpTHE1 results inphenotypes other than bursting rhizoids.

4.3.3. Seed plants. The drastic genomic expansion of the CrRLK1L subfamily also reflects itsfunctional diversification in flowering plants, for example, the diversity in Arabidopsis CrRLK1Lfunctions. Recent CrRLK1L studies of flowering plants nicely document this diversification, assome of these functions are novel compared with those of their Arabidopsis homologs; however, acore set of common functions appears to be governed by CrRLK1Ls throughout flowering plants.

4.3.3.1. Sexual reproduction and cell growth. One example for the latter case is the invention ofmale gamete transmission to the female gametophyte via tip-growing PTs to guarantee efficientfertilization without relying on a watery environment. In rice, this function is governed by theCrRLK1L homolog RUPTURED POLLEN (RUPO or OsCrRLK1L13), which is specificallyexpressed in mature pollen grains. T-DNA insertional mutant rupo/RUPO exhibits a male-specificgametophytic transmission defect with PTs that rupture prematurely (71), very similar to Ara-bidopsis anx1 anx2 and bups1 bups2 mutants (15, 36, 86). Interestingly, RUPO is a direct orthologof AtBUPS1 and AtBUPS2 (71, 90, 103). Moreover, the intracellular domain of RUPO physicallyinteracts with the high-affinity K+ transporters OsHAK1, OsHAK19, and OsHAK20, suggestingthe interplay of CWI sensing and K+ homeostasis in PT growth control, and points toward apossible missing link in the respective Arabidopsis signaling cascade (71).

Fittingly, another recent study of the Chinese white pear identified 26 CrRLK1Ls; 2 of theseappeared to be close homologs to AtANX1, AtANX2, and AtFER and displayed functions in malegamete transmission. Antisense oligonucleotide treatment against PbrCrRLK1L26 (a homologto AtFER) or PbrCrRLK1L3 (a homolog to AtANX1 and AtANX2) resulted in a decrease ofPT length and an increase of ruptured and abnormally formed PTs in vitro, respectively (57).In Zea mays, four CrRLK1L homologs are differentially expressed in the female embryo sacupon pollination, indicating a possible function during male-female gametophyte interactions(137) similar to AtFER function (31). However, their functional roles remain to be studied. InG. raimondii (cotton), 6 out of 44 CrRLK1L homologs were linked to genomic quantitative traitloci related to fiber quality traits, indicating a role in fiber development (93). Because the cottonfiber represents specialized, unicellular trichomes emerging from the ovule epidermis via a linear


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growth mode similar to that of tip-growing cells (104), this further supports a common role ofCrRLK1Ls during cell elongation. Another functional study in rice characterized DWARF ANDRUNTISH SPIKELET1 and 2 (DRUS1 and DRUS2 or OsCrRLK1L8 and OsCrRLK1L5),also named FERONIA-LIKE RECEPTOR1 and 2 (FLR1 and FLR2), which are the closestrice orthologs to AtFER, as regulators of reproductive growth and plant architecture (64, 103).drus1 drus2 double mutants and RNAi lines are defective in stem elongation, florescence andspikelet development, seed setting, and pollen viability, and affect sugar utilization and cell survival,representing novel aspects not covered by other CrRLK1Ls so far (103). As another study revealed,both flr1 drus1 and flr2 drus2 double mutants affected plant architectural traits, such as height,panicle number, and internode length, whereas only flr1 single mutants revealed abortion ofpollen development, resulting in reduced fertility and thus seed yield (64). These findings echothe distinct roles of AtFER during both reproduction and vegetative growth.

4.3.3.2. Circadian signaling and stress response. An expression study in rice suggests a rolefor several CrRLK1L homologs in circadian signaling and in the drought-stress response. Thetwo leaf-expressed rice homologs OsCrRLK1L2 and OsCrRLK1L3 are antagonistically upregu-lated in a diurnal and nocturnal manner, respectively. OsCrRLK1L2 is further upregulated bythe flowering time regulator OsGIGANTEA (OsGI) and downregulated by the AtCONSTANShomolog OsHD1 (90). A rice callus culture with a somaclonal variation in the AtHERK2 orthologOsCrRLK1L15, resulting in a loss of OsCrRLK1L15 function, displayed increased tolerance to-ward salt stress (135). The common bean (Phaseolus vulgaris) contains two CrRLK1L homologs,COK-4-3 and FER-like, which are differentially expressed upon treatment with flg22, suggestinga role in pathogen defense (4, 95), similar to the recent findings for AtFER (126).

4.4. Evolutionary Conservation of CrRLK1L-Mediated Signal Transduction

In addition to the RLCK MpPti and its role during maintenance of rhizoid CWI (44), manyhomologs of signaling components linked to Arabidopsis CrRLK1L-mediated pathways have beenidentified and functionally characterized in a variety of plant species. Despite functions similar tothose of their characterized Arabidopsis homologs, none of these components have been geneticallylinked to CrRLK1L-mediated signaling so far. For the future of CrRLK1L research in plant modelspecies beyond A. thaliana, the study of whether corresponding signal transduction pathways havebeen conserved throughout land plant and seed plant evolution is needed.

4.4.1. RALF homologs. RALF homologs have been identified and characterized in several flow-ering plants (22–24, 85, 100). Recently, a wide-ranging phylogeny of RALF proteins in greenplants was published (16). Interestingly, the RALF homolog SlPRALF and the sugar cane ho-molog SacRALF1 negatively regulate PT elongation in tomato (24) and cell elongation in thehypocotyl (41), respectively. These observations are reminiscent of the functions of AtRALF1(41) and AtRALF4 (80, 88), as well as of AtANX1, AtANX2, and AtFER, and further supporta potential function of (a) Arabidopsis RALFs as upstream effectors of CrRLK1Ls in the respec-tive processes and (b) tomato and sugar cane CrRLK1Ls in the RALF-mediated control of theseprocesses. Interestingly, three RALF homologs are present in M. polymorpha, whereas only oneCrRLK1L member exists (112), suggesting that already in early-diverging plants, a CrRLK1Lmight be differentially regulated by several ligands.

4.4.2. RAC and Rho-GTPase of plant homologs. RAC and ROP homologs have beendescribed and functionally characterized in both seedless (48) and seed-bearing land plants (98,


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105, 114, 128, 142) with their main functions in plant hormone signaling, pathogen defense,CWI, and cell polarity maintenance. The Rop and RAC PpRop2 and the GEF PpRopGEF3regulate polarity in the tip-growing protonema cells of P. patens. Overexpression of PpRop2or PpRopGEF3 leads to loss of anisotropic growth and the subsequent inflation of the apicalprotonema cells (PpRop2 and PpRopGEF3), as well as to malformation of the protonemal crosswall (PpRop2 only) (48). It will be interesting to see whether these phenotypic observations canbe linked to CrRLK1L-mediated signaling, as AtFER functions as an upstream regulator ofRAC-, ROP-, and ROS-mediated root hair development (30). Such a finding would indicatethe functional conservation and deployment of evolutionarily ancient genes by common celltypes (both protonemata and root hairs are tip-growing cells) rather than by a generation phase(protonemata are gametophytic, and root hairs are sporophytic).

4.4.3. Rboh homologs. Rboh homologs have been characterized in a variety of monocots (133,142) and eudicots (56, 102, 123, 147) with roles in ROS- and Ca2+-dependent signaling, pathogendefense, and CWI maintenance. In Nicotiana tabacum, ROS are produced by a NADPH oxidase atthe tip and in a Ca2+-dependent manner to sustain normal PT growth (102), strongly resemblingthe positive regulatory effect on the tip growth of its Arabidopsis homologs RbohC, RbohH, andRbohJ linked to CrRLK1Ls-dependent pathways. Intriguingly, several Oryza Rac members physi-cally bind to the cytosolic N terminus of NADPH oxidases of the Rboh group, supposedly also in aCa2+-dependent manner (142). Taken together, these findings point toward the evolutionary con-servation of a common downstream signaling module under the regulatory control of CrRLK1Ls.

SUMMARY POINTS

1. The malectin-like receptor kinases (a.k.a. CrRLK1Ls) possess a unique domain organi-zation comprising an intracellular Ser and Thr kinase domain coupled to an extracellularMLD that most likely originated in charophyte algae.

2. CrRLK1Ls have been proposed as potential cell wall sensors and as such regulate a varietyof key functions in plants.

3. RALF1 and RALF23 bind to the CrRLK1L member FER to positively modulate itsactivity during primary root growth and seedling growth, respectively. RALF23 alsoinhibits FER-dependent signaling during immunity.

4. RALF4, RALF19, and RALF34 bind to the four CrRLK1L members ANX1, ANX2,BUPS1, and BUPS2 with opposite outcomes for cell wall integrity of PTs, therebyorchestrating PT growth and reception.

5. Both FER and its homolog ANX1 can associate with immune receptors but with oppositeoutcomes.

6. Common signaling partners of CrRLK1Ls have been discovered, including the GPI-anchored proteins, RACs, ROPs, and RLCKs, as well as ROS and calcium signaling-related components.

7. An increasing number of CrRLK1L homologs are being characterized in both seed andnonseed plants. The establishment of the characteristic CrRLK1L domain pattern earlyin plant evolution may explain its functional conservation as a cell wall sensor throughoutland plants.


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8. By contrast, drastic gene duplication events may explain the functional diversification ofCrRLK1Ls in flowering plants.

9. CrRLK1L homologs were shown to regulate a core set of agronomically important func-tions, such as plant architecture, seed yield, and defense against pathogens. Manipulationof CrRLK1L pathways may prove beneficial for sustainable crop improvement.

FUTURE ISSUES

Despite the recent multiplication of CrRLK1L-related studies, the understanding of themalectin-like receptor kinases regarding their structure, activation mechanisms, local andglobal function, signaling partners, and evolution is still rather scarce.

1. Detailed characterization of the RALF-CrRLK1L interaction requires the investigationof the structure and mechanisms of activation or deactivation for the RALF1 and FERand RALF23 and FER pairs, respectively. The same holds true for RALF4, RALF19,and RALF34 binding to ANX1, ANX2, BUPS1, and BUPS2. Unfortunately, no crys-tallography study of the CrRLK1L proteins has been reported so far. How do RALFpeptides bind to the CrRLK1L extracellular domain and how does this interaction pro-mote receptor activation or deactivation? Do RALF peptides compete for the samebinding sites on a given CrRLK1L? Does a given RALF peptide bind to differentCrRLK1Ls?

2. The function of the variable malectin-like domain remains enigmatic. Does it mediatebinding to RALF peptides (and to other ligands)? Does it anchor the CrRLK1Ls in thecell wall? In this regard, note that residual fluorescence derived from THE1-GFP andANX1- and ANX2-YFP fusions appears to remain tightly associated with the cell wallafter plasmolysis (15, 42).

3. Most of the knowledge acquired on CrRLK1Ls concerns only one member of theA. thaliana subfamily, namely FER. We are in dire need of elucidating the functionof other CrRLK1Ls. This should encompass the complete characterization of the wholeA. thaliana subfamily and the identification of new ligands and additional interactionpartners for other CrRLK1Ls.

4. Many homologs of upstream and downstream signaling partners linked to ArabidopsisCrRLK1L-mediated pathways have been identified and functionally characterized ina variety of plant species. However, none of these genes has been genetically linkedto CrRLK1L-mediated signaling. The study of whether such constituents have beenconserved in a common signal transduction module throughout plant evolution and howthey have evolved will be indispensable.

5. Most studied CrRLK1Ls have been linked to agronomically important functions, suchas yield increase, cell wall alteration, pathogen defense, or abiotic stress signaling, all ofwhich are of major interest for human activities, including human and livestock nutrition,as well as the textile, wood, and biofuel industries. Characterization of more CrRLK1Lhomologs in a larger variety of crop species (including crucial staple crops such as maize,wheat, potato, and soybean, as well as nonseed plants) should be fostered.


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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

We are grateful to all members of Martin Hulskamp’s group (University of Cologne, Germany) forsharing their facilities. We thank Ping He (University of Texas, USA), Stefan Rensing (Universityof Marburg, Germany), Cyril Zipfel (The Sainsbury Laboratory, UK), and Martin Stegmann(Technische Universitat Munchen, Germany) for helpful discussions and comments. This workwas supported by the University of Cologne, the Deutsche Forschungsgemeinschaft Grant BO4470/1–1, and a grant from the University of Cologne Centre of Excellence in Plant Sciences toA.B.-D.

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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

vi Contents

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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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Documents

Plant Malectin-Like Receptor Kinases: From Cell Wall Integrity to …biologia.ucr.ac.cr/profesores/Garcia Elmer/Plant malectin... · 2019. 3. 11. · PP69CH11_Boisson-Dernier ARI