DETORQUEO, QUIRKY, and ZERZAUST Represent Novel Components Involved in Organ Development Mediated by the Receptor-Like Kinase STRUBBELIG in Arabidopsis thaliana

Abstract

Intercellular signaling plays an important role in controlling cellular behavior in apical meristems and developing organs in plants. One prominent example in Arabidopsis is the regulation of floral organ shape, ovule integument morphogenesis, the cell division plane, and root hair patterning by the leucine-rich repeat receptor-like kinase STRUBBELIG (SUB). Interestingly, kinase activity of SUB is not essential for its in vivo function, indicating that SUB may be an atypical or inactive receptor-like kinase. Since little is known about signaling by atypical receptor-like kinases, we used forward genetics to identify genes that potentially function in SUB-dependent processes and found recessive mutations in three genes that result in a sub-like phenotype. Plants with a defect in DETORQEO (DOQ), QUIRKY (QKY), and ZERZAUST (ZET) show corresponding defects in outer integument development, floral organ shape, and stem twisting. The mutants also show sub-like cellular defects in the floral meristem and in root hair patterning. Thus, SUB, DOQ, QKY, and ZET define the STRUBBELIG-LIKE MUTANT (SLM) class of genes. Molecular cloning of QKY identified a putative transmembrane protein carrying four C₂ domains, suggesting that QKY may function in membrane trafficking in a Ca²⁺-dependent fashion. Morphological analysis of single and all pair-wise double-mutant combinations indicated that SLM genes have overlapping, but also distinct, functions in plant organogenesis. This notion was supported by a systematic comparison of whole-genome transcript profiles during floral development, which molecularly defined common and distinct sets of affected processes in slm mutants. Further analysis indicated that many SLM-responsive genes have functions in cell wall biology, hormone signaling, and various stress responses. Taken together, our data suggest that DOQ, QKY, and ZET contribute to SUB-dependent organogenesis and shed light on the mechanisms, which are dependent on signaling through the atypical receptor-like kinase SUB. Plant organs, such as flowers or leaves, are made up of distinct cell layers. Although communication across these cell layers is essential for organ development, we have only recently gained some insight into the underlying mechanisms. Receptor-like kinases are cell-surface receptors that perceive and relay intercellular information. In Arabidopsis, the receptor-like kinase STRUBBELIG is required for inter–cell-layer communication during floral development, amongst other functions; little is known, however, concerning its exact signaling mechanism. Here, we identified three new genes called DETORQUEO, QUIRKY, and ZERZAUST. Plants defective in any of these genes strongly resemble the strubbelig mutant, both at the whole-organ and cellular levels. Thus, all four genes may share or contribute to a common signaling pathway essential for plant morphogenesis. Analyses revealed complex interactions between the genes, indicating that each has additional and distinct activities. We provide the molecular nature of QUIRKY; the encoded protein is likely membrane-localised and predicted to require Ca²⁺ for activity. In light of analogous animal models, we speculate that QUIRKY facilitates transport of molecules to the cell boundary and may support a STRUBBELIG-related extracellular signal. These results open new inroads into a molecular understanding of inter-cellular communication during flower development.