Starch depletion in the xylem and phloem ray parenchyma of grapevine stems under drought

Kyra A Prats; Ana C Fanton; Craig R Brodersen; Morgan E Furze

doi:10.1093/aobpla/plad062

Starch depletion in the xylem and phloem ray parenchyma of grapevine stems under drought

AoB Plants. 2023 Aug 30;15(5):plad062. doi: 10.1093/aobpla/plad062. eCollection 2023 Oct.

Authors

Kyra A Prats^{1

2}, Ana C Fanton³, Craig R Brodersen⁴, Morgan E Furze^{1

2

5}

Affiliations

¹ Department of Botany and Plant Pathology, Purdue University, 915 Mitch Daniels Blvd, West Lafayette, IN 47907, USA.
² Center for Plant Biology, Purdue University, 915 Mitch Daniels Blvd, West Lafayette, IN 47907, USA.
³ Ecophysiologie et Génomique Fonctionnelle de la Vigne, INRAE, 210 Chemin de Leysotte, Villenave-d'Ornon 33140, France.
⁴ School of the Environment, Yale University, 195 Prospect St, New Haven, CT 06511, USA.
⁵ Department of Forestry and Natural Resources, Purdue University, 715 Mitch Daniels Blvd, West Lafayette, IN 47907, USA.

Abstract

While nonstructural carbohydrate (NSC) storage can support long-lived woody plants during abiotic stress, the timing and extent of their use are less understood, as are the thresholds for cell mortality as NSCs and water supplies are consumed. Here, we combine physiological and imaging tools to study the response of Vitis riparia to a 6-week experimental drought. We focused on the spatial and temporal dynamics of starch consumption and cell viability in the xylem and phloem of the stem. Starch dynamics were further corroborated with enzymatic starch digestion and X-ray microcomputed tomography imaging. Starch depletion in the stems of droughted plants was detected after 2 weeks and continued over time. We observed distinct differences in starch content and cell viability in the xylem and phloem. By the end of the drought, nearly all the starch was consumed in the phloem ray parenchyma (98 % decrease), and there were almost no metabolically active cells in the phloem. In contrast, less starch was consumed in the xylem ray parenchyma (30 % decrease), and metabolically active cells remained in the ray and vessel-associated parenchyma in the xylem. Our data suggest that the higher proportion of living cells in the phloem and cambium, combined with smaller potential NSC storage area, rapidly depleted starch, which led to cell death. In contrast, the larger cross-sectional area of the xylem ray parenchyma with higher NSC storage and lower metabolically active cell populations depleted starch at a slower pace. Why NSC source-sink relationships between xylem and phloem do not allow for a more uniform depletion of starch in ray parenchyma over time is unclear. Our data help to pinpoint the proximate and ultimate causes of plant death during prolonged drought exposure and highlight the need to consider the influence of within-organ starch dynamics and cell mortality on abiotic stress response.

Keywords: Drought; nonstructural carbohydrates; phloem; ray parenchyma; xylem.