Boosting crop resilience to waterlogging through hormone-regulated root traits

Soil waterlogging can result from excessive rainfall, poor soil drainage, high groundwater tables and inadequate drainage, leading to hypoxic or anoxic environments in crop rhizophores. Oxygen-deprived conditions negatively impact root growth and, in severe cases, lead to root senescence due to detrimental soil physiochemical properties, such as lack of nutrient availability and accumulation of toxic elements (elemental toxicity). As the primary plant tissue affected by waterlogging, plant roots have evolved several adaptive strategies to restore oxygen supply, optimize nutrient acquisition, and mitigate elemental toxicity. Previous research has been primarily focussed on ‘oxygen-to-roots’ traits, such as development of adventitious and lateral roots, formation of aerenchyma (air-filled cavities) and the radial oxygen loss barriers. However, underlying phytohormones regulatory networks in response to waterlogging have often been overlooked. This review synthesizes contemporary research on hormonal regulation of root adaptations under waterlogging, aiming to fill key knowledge gaps by linking hormone signalling to root-based waterlogging and soil toxicity tolerance. We highlight roles of ethylene, ABA, and auxin in regulating aerenchyma formation and development of barrier to reduce radial oxygen loss and show that auxin and cytokinin are vital for lateral and adventitious root development and regulating cellular anatomical adaptations. We propose that ethylene, gibberellins (GAs), and brassinosteroids (BRs) are all crucial hormones that play roles in nodule development for nitrogen supply under waterlogging. Importantly, for the first time, we reviewed crucial roles of phytohormones on regulating elemental toxicity underlying waterlogging tolerance. This review also highlights the mitigating roles of emerging hormones, such as melatonin and strigolactones, in enhancing root-associated adaptation. Our review comprehensively elucidates phytohormones derived waterlogging tolerance mechanisms including linking phytohormones signalling to root-associated traits and provides valuable insights for oriented breeding strategies, aiming to improve crop resilience and ensure sustainable crop production. • Comprehensive review of phytohormonal control of root traits underlying waterlogging tolerance. • Exploration of elemental toxicity tolerance under waterlogging stress, an often-overlooked aspect of hormone signaling. • Propose the influence of plant hormones on nodule development and nitrogen supply contributing to waterlogging tolerance in legume crops. • Focus on the roles of ethylene, ABA, auxin, cytokinin, GAs, and BRs in modulating root adaptations under waterlogging. • Novel insights into breeding strategies targeting hormonal pathways to enhance crop resilience to waterlogging.