Abstract
Drought and flooding occur at opposite ends of the soil moisture spectrum yet resulting stress responses that occur in plants share many similarities. Drought limits root water uptake to which plants respond with stomatal closure and reduced leaf gas exchange. Flooding limits root metabolism due to soil anoxia, which also limits root water uptake and leaf gas exchange. As drought and flooding can occur consecutively in the same system and resulting plant stress responses share similar mechanisms, a single theoretical framework that integrates plant responses over a continuum of soil water conditions from drought to flooding is attractive. Based on a review of recent literature, we integrated the main plant eco-physiological mechanisms in a single theoretical model with a focus on plant water transport, plant oxygen dynamics, and leaf gas exchange. We used the Soil-Plant-Atmosphere-Continuum model as “backbone” for our theoretical framework development, and subsequently incorporated interactions between processes that regulate plant water and oxygen status, levels of abscisic acid and ethylene hormones and resulting acclimation strategies in response to drought, waterlogging, and complete submergence. Our theoretical framework provides a basis for the development of mathematical models to describe plant responses to the soil moisture continuum from drought to flooding.
Introduction
Plants are highly sensitive to the water status of the soil in which they grow, with too little soil moisture causing drought stress whereas too much soil moisture causes flooding stress. These stress responses to opposing water conditions can be understood from the fact that plant functioning requires sufficient liquid water uptake from the soil and rapid exchange of CO2 and oxygen with the environment to enable photosynthesis and support metabolic processes (Visser et al., 2003). All plant tissues require sufficient supply of O2and water for the aerobic respiratory processes fueling their maintenance, defense, growth, and reproduction. In addition, leaves also require CO2 from the air for photosynthesis.
A lack of soil moisture results in reduced root water uptake and is typically followed by stomatal closure to limit water loss through transpiration. Stomatal closure subsequently also limits CO2 uptake and photosynthesis. Depending on the extent of stomatal closure and the drought severity, this condition may lead to carbon starvation or still result in hydraulic failure (Adams et al., 2017). Under conditions of excess soil water, oxygen diffusion through the soil is limited and root oxygen status declines over time to trigger a transition from aerobic to anaerobic root metabolism at a specific threshold (Kosmacz & Weits, 2014). This decline in root metabolism initially limits root water transport while prolonged root anoxia may cause root decay or even plant death (Colmer et al., 2014). Despite the apparent opposing character of these two water stresses, both conditions result in a reduction of photosynthesis and transpiration at the leaf level and therefore have similar consequences for fluxes of water and carbon between the vegetation and atmosphere.
Environmental conditions associated with drought and flooding can occur in the same system consecutively. For example, heavy rainfall can occur after prolonged periods of drought in natural ecosystems or repetitive irrigation can be administered under persistent drought in agricultural settings. Continuous development of the land surface component of climate models leads to the inclusion of more detailed plant eco-physiological processes which are relevant for the surface exchange of water, carbon and energy (e.g. , Fisher & Koven, 2020; Harrison et al., 2021). It is therefore suggested that a single model capable of dynamically simulating plant responses in terms of photosynthesis and transpiration to the continuum of soil moisture conditions from drought to flooding would be attractive. However, a model with sufficient mechanistic biological details needed to simulate the interrelated changes in plant water transport, gas exchange and photosynthesis to this range of hydrological conditions is, to our knowledge, currently lacking. To understand and predict responses of individual plants and ecosystems to periods of drought and flooding and propose mitigating measures enhancing ecosystem robustness in future climates, development of such models is essential.
Therefore, the aim of our paper is to develop an integrated mechanistic framework that can describe plant responses across a continuum of moisture conditions that range from drought to flooding, building on the biophysics of plant water transport and gas exchange and its dependence on environmental conditions. Hereto, we review the major known eco-physiological responses of plants to drought and flooding, with a specific focus on mechanisms that govern plant gas exchange via water transport and photosynthesis. Key variables identified are stomatal conductance, shoot and root oxygen levels, as well as shoot and root ethylene levels, given its major role in plant response to flooding stresses (Voesenek & Sasidharan, 2013).
In our review, we first describe the soil-plant-atmosphere-continuum as an eco-physiological basis for the development of our mechanistic framework and define the main conditions that occur from drought to flooding. Second, we briefly review the main plant eco-physiological responses during drought conditions. Third, we derive the mechanisms needed to describe these key plant responses across the moisture continuum with an emphasis on responses that occur during flooding. We specifically focus on feedbacks between adaptive responses in our mechanistic framework and highlight the resulting similarities between drought and flooding responses. We end with a discussion focused on potential research questions that can be addressed with the proposed mechanistic framework.
The soil-plant-atmosphere continuum from drought to flooding
Water transport is an essential aspect of plant life, and a major factor through which plants affect our climate. There is thus a rich scientific tradition aimed at understanding and modeling plant water transport. The most widely acknowledged plant hydraulics theory thus far is the “cohesion-tension theory” (Tyree, 2003). This theory indicates that transpiration drives the upward water movement by creating negative pressure (tension) at the leaf surface, pulling the water column in the xylem through cohesion created by the hydrogen bonds between water molecules. This results in the generation of a water potential gradient along the xylem, with a lower (more negative) potential at the canopy and a higher (less negative) potential at the roots, which take up water from the soil. A typical model that describes plant water transport is the Soil-Plant-Atmosphere Continuum (SPAC) model (Elfving et al., 1972). The model makes use of a so-called “Ohm’s analogy”, essentially treating water flow as current and the soil-plant-atmosphere system as a series of resistances. The water potential of each plant compartment (i.e. , root, stem and canopy) together with the resistance between these compartments determine the amount of water flow (Bonan, 2019). The SPAC model is usually coupled with a photosynthesis model via stomatal behavior to simulate plant hydraulics and leaf-level gas exchange processes during normal growth conditions and drought (Bonan et al., 2014). Therefore, we propose the SPAC-photosynthesis model to serve as the “backbone” of our model framework, which is then extended to couple plant biochemical processes in response to flooding as well.
In our review and theoretical model development, we subsequently separate four distinct conditions along the soil moisture continuum from drought to flooding—drought, non-stressed condition, waterlogging, and complete submergence. These conditions and the corresponding states of the key boundary conditions are defined in figure 1. Under non-stressed soil water conditions in which soil water content is by definition between the wilting point and the field capacity, soil oxygen state is hypoxic due to a proportion of soil pores being waterfilled and microbial activity consuming oxygen, whereas the shoot ambient oxygen and CO2 are at atmospheric level, and light condition is normal at daytime. During drought, soil water content is below wilting point which means that available soil water for plants is lacking, while soil oxygen remains hypoxic and the shoot still has full access to atmospheric oxygen and CO2, and natural light. Waterlogging and complete submergence are two distinct states of flooding. During waterlogging, soil water content surpasses field capacity and soil pores are nearly or fully filled with water (Pan et al., 2021; Sairam et al., 2008) while the shoot remains exposed to air. Gas diffusion coefficients in water are typically 1/10000 of that in air (Armstrong, 1980) and dissolved oxygen is at a very low concentration of 1-15 mg L-1. This largely hampered oxygen diffusion and limited oxygen content in water together with microbial activity lead to soil anoxia within hours after flooding (Kozlowski, 1984). However, as the above-ground shoot is fully aerated, it has full access to atmospheric oxygen and CO2, and natural light. During submergence, the soil is waterlogged and anoxic similar to waterlogging, whereas the aboveground shoot is also in the water. Therefore, the shoot under submergence is only accessible to dissolved oxygen and dissolved CO2 which are limited, while light intensity is limited due to turbidity.