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.