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.
Highlights
How intercellular communication mechanisms coordinate the activities of cells during organogenesis is an important topic in biology
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
Summary
How intercellular communication mechanisms coordinate the activities of cells during organogenesis is an important topic in biology. Meristems are organised into three distinct meristematic or histogenic layers, called L1, L2, and L3 [2], and cells of all histogenic layers contribute to organogenesis [3,4]. The L1 layer gives rise to the epidermis while the L2 and L3 layers contribute to internal tissues. In Arabidopsis ovules, for example, the integuments that eventually develop into the seed coat are entirely made up of L1-derived cells, while L2 cells generate the inner tissue [5]. Classic studies have demonstrated that meristematic layers communicate [6,7], but it is only recently that the biological relevance and the molecular mechanisms are being elucidated [8,9,10,11]. Work on the receptor-like kinase (RLK) BRASSINOSTEROID INSENSITIVE 1 (BRI1) has provided evidence that the epidermis both promotes and restricts organ
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