Duet between sugars and hormones: The molecular dialogue fine-tuning hypoxia acclimation in plants.

Abstract

Hypoxic conditions caused by submergence or soil waterlogging constrain plant growth and productivity. To survive, plants coordinately reprogram both sugar metabolism and phytohormone signaling to trigger adaptive responses; yet, the integrative regulatory frameworks governing this interaction remain unresolved. Here, we synthesize current knowledge on how sugars, acting as both metabolites and signals, intersect with phytohormone networks to regulate growth and survival under low-oxygen stress. Under hypoxia, ethylene and auxin reshape root architecture, while cytokinin mediates sugar-dependent regulation of shoot branching to optimize resource allocation. The dynamic interplay between abscisic acid and sugars is central to maintaining energy balance under cyclic day-night hypoxia. This interaction modulates the stomatal aperture, facilitates controlled starch degradation, and coordinates sucrose transport to sustain metabolism. Furthermore, crosstalk between primary sugars, gibberellin, and brassinosteroid fine-tunes critical developmental transitions, including seed germination and internode elongation. Although individual signaling pathways under hypoxia have been well studied, their integration via sugar-hormone crosstalk remains elusive. To address these issues, we propose integrating synthetic low-oxygen sensors that initially detect hypoxic stress with engineered sugar-hormone balancing circuits that subsequently fine-tune metabolic and hormonal responses, thereby creating closed-loop feedback systems for adaptive stress resilience. Such systems could enable "Sensing, Metabolism, Adaptation, and Regulation Technology" (SMART) crops to autonomously sense and adapt to hypoxia stress. By synthesizing current knowledge and existing gaps, our work proposes future directions to advance the development of hypoxia-resilient crops through optimizing growth and yield stability under stress.