Flooding is an environmental stress for many natural and man-made ecosystems worldwide. Genetic diversity in the plant response to flooding includes alterations in architecture, metabolism, and elongation growth associated with a low O₂ escape strategy and an antithetical quiescence scheme that allows endurance of prolonged submergence. Flooding is frequently accompanied with a reduction of cellular O₂ content that is particularly severe when photosynthesis is limited or absent. This necessitates the production of ATP and regeneration of NAD⁺ through anaerobic respiration. The examination of gene regulation and function in model systems provides insight into low-O₂-sensing mechanisms and metabolic adjustments associated with controlled use of carbohydrate and ATP. At the developmental level, plants can escape the low-O₂ stress caused by flooding through multifaceted alterations in cellular and organ structure that promote access to and diffusion of O₂. These processes are driven by phytohormones, including ethylene, gibberellin, and abscisic acid. This exploration of natural variation in strategies that improve O₂ and carbohydrate status during flooding provides valuable resources for the improvement of crop endurance of an environmental adversity that is enhanced by global warming.

Summary: Unanticipated flooding challenges plant growth and fitness in natural and agricultural ecosystems. Here we describe mechanisms of developmental plasticity and metabolic modulation that underpin adaptive traits and acclimation responses to waterlogging of root systems and submergence of aerial tissues. This includes insights into processes that enhance ventilation of submerged organs. At the intersection between metabolism and growth, submergence survival strategies have evolved involving an ethylene‐driven and gibberellin‐enhanced module that regulates growth of submerged organs. Opposing regulation of this pathway is facilitated by a subgroup of ethylene‐response transcription factors (ERFs), which include members that require low O₂ or low nitric oxide (NO) conditions for their stabilization. These transcription factors control genes encoding enzymes required for anaerobic metabolism as well as proteins that fine‐tune their function in transcription and turnover. Other mechanisms that control metabolism and growth at seed, seedling and mature stages under flooding conditions are reviewed, as well as findings demonstrating that true endurance of submergence includes an ability to restore growth following the deluge. Finally, we highlight molecular insights obtained from natural variation of domesticated and wild species that occupy different hydrological niches, emphasizing the value of understanding natural flooding survival strategies in efforts to stabilize crop yields in flood‐prone environments. Contents Summary 57 I. Introduction 58 II. Root acclimations that promote root aeration 60 III. Regulating reaeration by active emergence in Rumex palustris and Oryza sativa 62 IV. Limiting O₂ starvation with gas films and underwater photosynthesis 64 V. Key metabolic acclimations to flooding and low‐O₂ stress and their control 65 VI. Managing quiescence in growth during submergence 67 VII. After the deluge 68 VIII. Perspective 69 Acknowledgements 69 References 69

Flooding regimes of different depths and durations impose selection pressures for various traits in terrestrial wetland plants. Suites of adaptive traits for different flooding stresses, such as soil waterlogging (short or long duration) and full submergence (short or long duration – shallow or deep), are reviewed. Synergies occur amongst traits for improved internal aeration, and those for anoxia tolerance and recovery, both for roots during soil waterlogging and shoots during submergence. Submergence tolerance of terrestrial species has recently been classified as either the Low Oxygen Quiescence Syndrome (LOQS) or the Low Oxygen Escape Syndrome (LOES), with advantages, respectively, in short duration or long duration (shallow) flood-prone environments. A major feature of species with the LOQS is that shoots do not elongate upon submergence, whereas those with the LOES show rapid shoot extension. In addition, plants faced with long duration deep submergence can demonstrate aspects of both syndromes; shoots do not elongate, but these are not quiescent, as new aquatic-type leaves are formed. Enhanced entries of O2 and CO2 from floodwaters into acclimated leaves, minimises O2 deprivation and improves underwater photosynthesis, respectively. Evolution of ‘suites of traits’ are evident in wild wetland species and in rice, adapted to particular flooding regimes.

Summary: Flooding is a widespread phenomenon that drastically reduces the growth and survival of terrestrial plants. The dramatic decrease of gas diffusion in water compared with in air is a major problem for terrestrial plants and limits the entry of CO₂ for photosynthesis and of O₂ for respiration. Responses to avoid the adverse effects of submergence are the central theme in this review. These include underwater photosynthesis, aerenchyma formation and enhanced shoot elongation. Aerenchyma facilitates gas diffusion inside plants so that shoot‐derived O₂ can diffuse to O₂‐deprived plant parts, such as the roots. The underwater gas‐exchange capacity of leaves can be greatly enhanced by a thinner cuticle, reorientation of the chloroplasts towards the epidermis and increased specific leaf area (i.e. thinner leaves). At the same time, plants can outgrow the water through increased shoot elongation, which in some species is preceded by an adjustment of leaf angle to a more vertical position. The molecular regulatory networks involved in these responses, including the putative signals to sense submergence, are discussed and suggestions made on how to unravel the mechanistic basis of the induced expression of various adaptations that alleviate O₂ shortage underwater. Contents Summary 213 I. Introduction 213 II. Sensing of submergence 214 III. Internal aeration and underwater photosynthesis 217 IV. Stimulated shoot elongation 219 V. Perspectives 221 Acknowledgements 222 References 222