Spatial consistency of cell growth direction during organ morphogenesis requires CELLULOSE-SYNTHASE INTERACTIVE1

Abstract

Extracellular matrices generally contain fibril-like polymers that may be organized in parallel arrays. Although their role in morphogenesis has been long recognized, it is still unclear how the subcellular control of fibril synthesis translates into well-defined organ shape. Here, we addressed this question using the Arabidopsis sepal as a model organ. In plants, cell growth is driven by turgor pressure and restrained by the extracellular matrix known as the cell wall. Cellulose is the main load-bearing component of the plant cell wall and cellulose microfibrils are thought to channel growth perpendicularly to their main orientation. Given the key function of CELLULOSE SYNTHASE INTERACTIVE 1 (CSI1) in guidance of cellulose synthesis, we investigated the role of CSI1 in sepal morphogenesis. We observed that sepals from csi1 mutants are shorter, although their newest cellulose microfibrils are more aligned compared to wild type. Surprisingly, cell growth anisotropy was similar in csi1 and wild-type plants. We resolved this apparent paradox using polarized Raman microspectroscopy, live imaging of growing sepals, and bespoke mechanical assays. We found that CSI1 is required for spatial consistency of growth direction across the sepal and for the maintenance of overall organ elongation. Our work illustrates how the subcellular regulation of the extracellular matrix may control morphogenesis at multiple scales.