The AGC protein kinase UNICORN controls planar growth by attenuating PDK1 in Arabidopsis thaliana

Abstract

Tissue morphogenesis critically depends on the coordination of cellular growth patterns. In plants, many organs consist of clonally distinct cell layers, such as the epidermis, whose cells undergo divisions that are oriented along the plane of the layer. The developmental control of such planar growth is poorly understood. We have previously identified the Arabidopsis AGCVIII-class protein kinase UNICORN (UCN) as a central regulator of this process. Plants lacking UCN activity show spontaneous formation of ectopic multicellular protrusions in integuments and malformed petals indicating that UCN suppresses uncontrolled growth in those tissues. In the current model UCN regulates planar growth of integuments in part by directly repressing the putative transcription factor ABERRANT TESTA SHAPE (ATS). Here we report on the identification of 3-PHOSPHOINOSITIDE-DEPENDENT PROTEIN KINASE 1 (PDK1) as a novel factor involved in UCN-mediated growth control. PDK1 constitutes a basic component of signaling mediated by AGC protein kinases throughout eukaryotes. Arabidopsis PDK1 is implied in stress responses and growth promotion. Here we show that loss-of-function mutations in PDK1 suppress aberrant growth in integuments and petals of ucn mutants. Additional genetic, in vitro, and cell biological data support the view that UCN functions by repressing PDK1. Furthermore, our data indicate that PDK1 is indirectly required for deregulated growth caused by ATS overexpression. Our findings support a model proposing that UCN suppresses ectopic growth in integuments through two independent processes: the attenuation of the protein kinase PDK1 in the cytoplasm and the repression of the transcription factor ATS in the nucleus.\n\nAuthor SummaryPlant organs, such as petals or roots, are composites of distinct cell layers. As a rule, cells making up a layer, for example the epidermis, the outermost layer of a tissue, divide \"within the plane\" of the layer. This cellular behavior results in the two-dimensional sheet-like or planar growth of the cell layer. The mechanism orchestrating such a growth pattern is poorly understood. In particular, it is unclear how uncontrolled and \"out-of-plane\" growth is avoided. Here we provide insight into this process. Our data indicate that higher than normal activity of a central regulator of growth and stress responses results in wavy and malformed petals and in protrusion-like aberrant outgrowths in the tissue that will develop into the seed coat. It is therefore important to keep this factor in check to allow proper formation of those tissues. We further show that a protein called UNICORN attenuates the activity of this regulator thereby ensuring the sheet-like growth of young petals or the developing seed coat.