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

Extracellular matrices generally contain fibril-like polymers that may be organized in parallel arrays. Although their role in morphogenesis has been 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. We investigated the role of the guidance of cellulose synthesis by CELLULOSE SYNTHASE INTERACTIVE 1 (CSI1) in sepal morphogenesis. We observed that sepals are shorter in csi1 mutants, although the newest cellulose microfibrils are more aligned in csi1. Surprisingly, cell growth anisotropy was similar in csi1 and wild-type plants. We resolved this apparent paradox using polarized Raman microspectroscopy and live imaging of growing sepals. We found that CSI1 is required for spatial consistency of growth direction across the sepal and for the maintenance of overall organ elongation. We confirmed our conclusions at sepal scale, notably using bespoke mechanical assays. Our work illustrates how the subcellular regulation of the extracellular matrix may control morphogenesis at multiple scales.