The Arabidopsis CLAVATA2 Gene Encodes a Receptor-like Protein Required for the Stability of the CLAVATA1 Receptor-like Kinase

Abstract

The CLAVATA2 ( CLV2 ) gene regulates both meristem and organ development in Arabidopsis. We isolated the CLV2 gene and found that it encodes a receptor-like protein (RLP), with a presumed extracellular domain composed of leucine-rich repeats similar to those found in plant and animal receptors, but with a very short predicted cytoplasmic tail. RLPs lacking cytoplasmic signaling domains have not been previously shown to regulate development in plants. Our prior work has demonstrated that the CLV1 receptor-like kinase (RLK) is present as a disulfide-linked multimer in vivo. We report that CLV2 is required for the normal accumulation of CLV1 protein and its assembly into protein complexes, indicating that CLV2 may form a heterodimer with CLV1 to transduce extracellular signals. Sequence analysis suggests that the charged residue in the predicted transmembrane domain of CLV2 may be a common feature of plant RLPs and RLKs. In addition, the chromosomal region in which CLV2 is located contains an extremely high rate of polymorphism, with 50 nucleotide and 15 amino acid differences between Landsberg erecta and Columbia ecotypes within the CLV2 coding sequence. INTRODUCTIONThe shoot meristem is responsible for the formation of all above-ground organs in higher plants. This task is accomplished by balancing two processes: the maintenance of a population of undifferentiated cells at the center of the shoot meristem and the direction of progeny cells on the flanks of the meristem toward organ formation and eventual differentiation. Mutations in several genes in Arabidopsis have been shown to disrupt this balance (reviewed in Clark, 1997), including SHOOT MERISTEMLESS ( STM ), WUSCHEL ( WUS ), and the genes comprising the CLAVATA loci ( CLV1 , CLV2 , and CLV3 ) (Leyser and Furner, 1992;Barton and Poethig, 1993;Clark et al., 1993Clark et al., , 1995Laux et al., 1996;Kayes and Clark, 1998). Plants carrying mutations at the CLV loci accumulate undifferentiated cells in the shoot and flower meristems, and it has therefore been proposed that the CLV genes either inhibit the division of these cells or promote their transition toward a differentiated state (reviewed in Clark, 1997).The phenotypes of clv1 and clv3 mutants are identical, and these two genes function in the same pathway to regulate meristem development. In addition, the phenotypes of the clv1 and clv3 mutants and the gene expression patterns for CLV1 and CLV3 appear to be specific to the shoot and flower meristems (Clark et al., 1993(Clark et al., , 1995Fletcher et al., 1999). Compared with clv1 and clv3 mutants, all clv2 mutant alleles display weak phenotypes at the shoot and flower meristems (Kayes and Clark, 1998). clv2 mutations also affect the development of several organ types. These include the pedicel, which is elongated in clv2 mutants, and the anthers and valves of the flower, both of which are reduced in clv2 mutants. Genetic analysis indicates that CLV2 functions in the same pathway as CLV1 and CLV3 in the regulation of meristem development but in a separa...

CLAVATA1 controls distinct signaling outputs that buffer shoot stem cell proliferation through a two-step transcriptional compensation loop

“…Both CLV2 and CRN are expressed broadly in inflorescence tissue (see S1B Fig, [15, 16]) but it is not clear if they function in WUS expressing cells of the SAM like CLV1 . I therefore tested the ability of CLV2-myc and CRN-2xmCherry fusion proteins to complement their respective null mutants when expressed from either their native promoters or the WUS promoter.…”

Peptide Signaling in Plant Development

“…This phenotype is the result of an expansion of the stem-cell population in the floral meristem, and analyses of the shoot meristem revealed a similar stem-cell defect there [9-11]. Genetic evidence indicates that three CLV loci act together [12] and the corresponding genes encode components of a signaling pathway: CLV1 , a leucine rich repeat-receptor like kinase (LRR-RLK); CLV2 , an LRR-containing accessory receptor protein; and CLV3 , a novel signal peptide [10,13,14]. …”

Spatiotemporal signalling in plant development

“…Three receptor complexes have been identified: CLAVATA 1 (CLV1) homodimers; CLAVATA 2 (CLV2) and CORYNE (CRN) heterodimers; and RECEPTOR-LIKE PROTEIN KINASE 2 (RPK2) homodimers 12–14 . CLV1 and RPK2 represent typical serine/threonine LRR-RLKs, whereas CLV2 lacks a kinase domain and is a prototypical LRR-RP, requiring CRN for signal transduction 13,15,16 . CRN is kinase-dead, suggesting that it does not have a role in signal transduction, and it is instead proposed to facilitate CLV2 transport or protein scaffolding 17 .…”