TY - JOUR

T1 - Phosphate starvation regulates cellulose synthesis to modify root growth

AU - Khan, Ghazanfar Abbas

AU - Dutta, Arka

AU - Meene, Allison van de

AU - Frandsen, Kristian E.H.

AU - Ogden, Michael

AU - Whelan, James

AU - Persson, Staffan

N1 - Funding Information: G.A.K. was funded by the Swiss National Science Foundation Fellowship (P2LAP3-168408) and the DECRA Fellowship from the Australian Research Council (DE210101200). K.E.H.F. was funded by a Novo Nordisk Foundation Industrial Biotechnology and Environmental Biotechnology Postdoctoral grant (NNF21OC0071799) and a Villum Foundation Experiment grant (VIL50427). S.P. was funded by a Villum Foundation, 2 Novo Nordisk, and Danish National Research Foundation grants (25915, 19OC0056076, 20OC0060564, and DNRF155, respectively). Publisher Copyright: © The Author(s) 2023. Published by Oxford University Press on behalf of American Society of Plant Biologists.

PY - 2024

Y1 - 2024

N2 - In the model plant Arabidopsis (Arabidopsis thaliana), the absence of the essential macro-nutrient phosphate reduces primary root growth through decreased cell division and elongation, requiring alterations to the polysaccharide-rich cell wall surrounding the cells. Despite its importance, the regulation of cell wall synthesis in response to low phosphate levels is not well understood. In this study, we show that plants increase cellulose synthesis in roots under limiting phosphate conditions, which leads to changes in the thickness and structure of the cell wall. These changes contribute to the reduced growth of primary roots in low-phosphate conditions. Furthermore, we found that the cellulose synthase complex (CSC) activity at the plasma membrane increases during phosphate deficiency. Moreover, we show that this increase in the activity of the CSC is likely due to alterations in the phosphorylation status of cellulose synthases in low-phosphate conditions. Specifically, phosphorylation of CELLULOSE SYNTHASE 1 (CESA1) at the S688 site decreases in low-phosphate conditions. Phosphomimic versions of CESA1 with an S688E mutation showed significantly reduced cellulose induction and primary root length changes in low-phosphate conditions. Protein structure modeling suggests that the phosphorylation status of S688 in CESA1 could play a role in stabilizing and activating the CSC. This mechanistic understanding of root growth regulation under limiting phosphate conditions provides potential strategies for changing root responses to soil phosphate content.

AB - In the model plant Arabidopsis (Arabidopsis thaliana), the absence of the essential macro-nutrient phosphate reduces primary root growth through decreased cell division and elongation, requiring alterations to the polysaccharide-rich cell wall surrounding the cells. Despite its importance, the regulation of cell wall synthesis in response to low phosphate levels is not well understood. In this study, we show that plants increase cellulose synthesis in roots under limiting phosphate conditions, which leads to changes in the thickness and structure of the cell wall. These changes contribute to the reduced growth of primary roots in low-phosphate conditions. Furthermore, we found that the cellulose synthase complex (CSC) activity at the plasma membrane increases during phosphate deficiency. Moreover, we show that this increase in the activity of the CSC is likely due to alterations in the phosphorylation status of cellulose synthases in low-phosphate conditions. Specifically, phosphorylation of CELLULOSE SYNTHASE 1 (CESA1) at the S688 site decreases in low-phosphate conditions. Phosphomimic versions of CESA1 with an S688E mutation showed significantly reduced cellulose induction and primary root length changes in low-phosphate conditions. Protein structure modeling suggests that the phosphorylation status of S688 in CESA1 could play a role in stabilizing and activating the CSC. This mechanistic understanding of root growth regulation under limiting phosphate conditions provides potential strategies for changing root responses to soil phosphate content.

U2 - 10.1093/plphys/kiad543

DO - 10.1093/plphys/kiad543

M3 - Journal article

C2 - 37823515

AN - SCOPUS:85184592531

VL - 194

SP - 1204

EP - 1217

JO - Plant Physiology

JF - Plant Physiology

SN - 0032-0889

IS - 2

ER -