‘Against all floods’: plant adaptation to flooding stress and combined abiotic stresses

Abstract

SUMMARYCurrent climate change brings with it a higher frequency of environmental stresses, which occur in combination rather than individually leading to massive crop losses worldwide. In addition to, for example, drought stress (low water availability), also flooding (excessive water) can threaten the plant, causing, among others, an energy crisis due to hypoxia, which is responded to by extensive transcriptional, metabolic and growth‐related adaptations. While signalling during flooding is relatively well understood, at least in model plants, the molecular mechanisms of combinatorial flooding stress responses, for example, flooding simultaneously with salinity, temperature stress and heavy metal stress or sequentially with drought stress, remain elusive. This represents a significant gap in knowledge due to the fact that dually stressed plants often show unique responses at multiple levels not observed under single stress. In this review, we (i) consider possible effects of stress combinations from a theoretical point of view, (ii) summarize the current state of knowledge on signal transduction under single flooding stress, (iii) describe plant adaptation responses to flooding stress combined with four other abiotic stresses and (iv) propose molecular components of combinatorial flooding (hypoxia) stress adaptation based on their reported dual roles in multiple stresses. This way, more future emphasis may be placed on deciphering molecular mechanisms of combinatorial flooding stress adaptation, thereby potentially stimulating development of molecular tools to improve plant resilience towards multi‐stress scenarios.

Research Progress on Plant Responses to Stress Combinations in the Context of Climate Change

“…1. Exploring plant perceptions and prioritization of responses to stress combinations: Studies have shown that one stressor will dominate under a stress combination, and plants will preferentially sense or respond to this primary stressor and react to it, involving complex signaling pathways [ 91 ]. The study of relevant pathways in plants will help us understand plant response mechanisms.…”

Flooding stress and responses to hypoxia in plants

“…While the molecular mechanisms of O 2 sensing in hypoxic conditions are well-described in Arabidopsis (e.g. reviewed in Le ón et al 2021;Loreti and Perata 2023;Renziehausen et al 2024), further research is needed on the specific signalling pathways and the molecular regulation of traits conferring hypoxia tolerance, as well as their functional characterisation and translation of such resources into flooding-sensitive crops. Excitingly, excellent examples of the use of molecular tools characterising genes responsive to hypoxia, tissue metabolic responses to hypoxia, tissue O 2 status, anatomical changes facilitating effective O 2 diffusion, and whole-plant responses to waterlogging, partial or complete submergence, or a combination of flooding with other stress conditions are well described in this Collection on 'Flooding stress and responses to hypoxia in plants'.…”

MEDIATOR SUBUNIT 25 modulates ERFVII-controlled hypoxia responses in Arabidopsis

“…Since flooding impairs oxygen diffusion, aerobic respiration for providing energy equivalents is hampered or even blocked. To adapt, plants will induce an acclimation response, including activation of anaerobic respiration, a process which is under strict transcriptional control (Bailey-Serres et al, 2012; Renziehausen et al, 2024).…”