Stelar starch management tailors diurnal and rehydration-related water flows in Pinus pinea needles

Abstract Pine needles contain two vascular cell types unique to gymnosperms: Transfusion parenchyma (tp) and tracheids (tt). Since they form the only connections between vascular bundles and bundle sheath, we hypothesised that they are involved in regulating the needle’s water import and photoassimilate export. Synchrotron-based tomography enabled us to quantify volume changes of tp and tt cells in Pinus pinea needles systematically along the needle and throughout a diurnal day cycle, as well as under rehydration. As a physiological indicator of tp’s carbohydrate status served their starch content. Segmentation of the comprehensive data uncovered dramatic volume changes during dehydration and showed a diurnal course of starch formation and degradation. These changes suggest a yet unknown osmotic water flux between tp and tt, balanced by the former’s carbohydrate status. Confirming our hypothesis, excess of photoassimilates in tp cells went into starch synthesis during the day. Starch mobilisation during the night increased the osmotic potential in tp and led to water intake. According to the decreasing starch fraction from base to needle tip, this mechanism is predominant in the upper needle segments, particularly after rehydration of dehydrated needles. Mechanistically, osmolytes in tp cells maintain tension in tt for the needle’s water import. Highlight Synchrotron tomographic microscopy uncovers diurnal starch fluctuations and osmotic water pumping in inner tissues of pine needles that are utilised at night and when recovering from dehydration