Figure 2 . A general framework of the proposed model with
biological processes to be included. This framework integrates a SPAC
compartment (blue boxes), photosynthesis compartment (yellow boxes), and
flooding-response extension (green boxes). In the SPAC compartment the
plant is divided into root, stem, and leaf, for each of which we
consider water potential and water conductance as variables. The
promotion and inhibition relationship between these variables are
summarized based on the equations provided in Bonan (2019). In order to
capture an/isohydric strategies, ABA levels in root and leaf (blue round
boxes) are also included as variables in the SPAC framework. The
photosynthesis compartment follows the Farquhar model, where the
photosynthesis rate is determined by the minimum of two processes, the
rubisco-catalyzed carboxylation rate representing light-independent
reactions and the electron transport rate representing light-dependent
reactions (Farquhar et al., 1980; Von Caemmerer, 2013). In the
flooding-response extension the plant is divided into root and shoot,
for which oxygen and ethylene levels are key variables. Root and shoot
ethylene levels (green round boxes) are core variables triggering either
the “escape” or “quiescence” strategy. The objective of this
integrated framework is to link the flooding-response extension to the
SPAC-photosynthesis framework. The SPAC compartment and
flooding-response extension can be linked through (1) the crosstalk
between ABA and ethylene, which will be discussed in the discussion
section, (2) root oxygen deficit inhibiting root water conductance
through the gating of aquaporin, and (3) the controlling effect of shoot
ethylene on stomatal conductance. The Farquhar model and
flooding-response extension can be bridged through the production of
oxygen in shoot through photosynthesis and the sustaining effect of
“escape” strategy on photosynthesis.
Plant species differ in their tendency to decrease stomatal conductance
in response to drought stress. On one end of the spectrum are plant
species using a so-called isohydric strategy (e.g. , maize and
pea) (Bates & Hall, 1981; Tardieu, 1993) in which plants produce more
ABA and downregulate their stomatal conductance during soil water
dry-down (Coupel-Ledru et al., 2017), thus maintaining a relatively high
(less negative) and stable leaf water potential but sacrificing
photosynthesis rate (Bonan, 2019). On the other end of the spectrum are
plant species employing an anisohydric strategy (e.g. , soybean
and wheat) (Allen et al., 1994; Henson et al., 1989), in which less ABA
is produced in the xylem (Coupel-Ledru et al., 2017), and plants
maintain relatively high photosynthesis rate by keeping their stomatal
conductance relatively stable, resulting in leaf water potential
becoming very negative and thereby rendering the plant prone to
desiccation in case of prolonged drought (Bonan, 2019).
3.2 Generic responses to water logging and complete
submergence
The fundamental plant physiological stress that results from soil
waterlogging is root oxygen deficit, which forces a conversion from
aerobic to anaerobic root metabolism
(Geigenberger,
2003).
According to the so-called Pasteur effect, to generate the same amount
of ATP, 15 times as much glucose is required in anaerobic respiration as
in aerobic respiration, and plants are therefore prone to mortality from
energy exhaustion (Geigenberger, 2003). Meanwhile, root oxygen deficit
causes dysfunction of root water uptake due to the gating of aquaporins
(Törnroth-Horsefield et al., 2006). As the shoot remains well-oxygenated
due to exposure to the atmosphere, the loss in root water uptake,
similar to the case under drought stress can then lead to the imbalance
between transpiration demand and limited internal plant water transport
(Aroca et al., 2012). Therefore, water potential in root, stem, and
canopy becomes more negative, and xylem water conductance is reduced
(Ashraf, 2012; Nicolás et al., 2005). To reduce the resulting risk to
desiccation of the above-ground tissues, plants downregulate their
stomatal conductance, which ultimately results in lower photosynthesis
level (Ahmed et al., 2002; Jackson & Drew, 1984; Liu et al., 2014).
Oxygen transport from shoot to root is limited due to the high
resistance of shoot-root gas diffusion (Armstrong & Armstrong, 2014).
Additionally, the waterlogged root suffers from radial oxygen loss to
the anoxic soil (Armstrong, 1971). These effects further trap roots in
hypoxic and even anoxic conditions under prolonged waterlogging.
Under complete submergence in which the plant shoot is also underwater,
the hampered shoot-level gas exchange is another major physiological
threat besides root oxygen deficit. Particularly, photosynthesis is
reduced by the limited CO2 level and diffusion in water
and the also often lowered light intensity due to turbidity (Voesenek et
al., 2006). Additionally, transpiration is blocked by the surrounding
floodwater and therefore internal plant water transport is minor.
Reduced photosynthesis together with very limited oxygen content and
oxygen diffusion in water cause shoot hypoxia. With less oxygen supply
from the shoot, roots often suffer from anoxia within 24 hours after
complete submergence (Winkel et al., 2013).
Flooding-adaptive plants have developed specialized acclimation
mechanisms to survive under waterlogging and complete submergence.
Ethylene serves as the central phytohormone that mediates these
mechanisms (Shiono et al., 2008; Voesenek & Sasidharan, 2013). Ethylene
is a gaseous hormone, and during flooding its outward diffusion is
largely inhibited by the surrounding floodwater (Stünzi & Kende, 1989),
causing an abrupt increase of endogenous ethylene in submerged plant
tissues (Sasidharan et al., 2018). Endogenous ethylene accumulation
induces the expression of ethylene response factor (ERF) encoding genes
that triggers low-oxygen acclimation mechanisms (Bailey-Serres et al.,
2012; Van Dongen & Licausi, 2015). There are two major acclimation
mechanisms. One mechanism, termed as “escape”, often witnessed in
deep-water rice, promotes plant endogenous oxygenation and maintained
photosynthesis through aerenchyma formation, adventitious root
development, and shoot elongation (J. Bailey-Serres & Voesenek, 2008).
The “escape” strategy is energy-consuming, whereas another acclimation
mechanism termed as “quiescence” is more conservative and
energy-saving (Pradhan & Mohanty, 2013). This strategy involves the
repression of energy and carbon consumption, including the
aforementioned “escape” strategy, thereby promoting maintenance of
carbohydrates and energy reserve levels (Voesenek & Bailey-Serres,
2015). We have integrated these processes in a conceptual model, with
plant endogenous oxygen and ethylene in shoot and root as variables, and
their interactions with “escape” and “quiescence” strategies,
displayed in figure 2, flooding-response extension compartment.
Integrating these biophysical and biochemical processes, our model
framework (figure 2) connects plant hydraulics (blue boxes),
photosynthesis (yellow boxes), and flooding responses based on plant
endogenous oxygen levels (green boxes) that includes hormonal variables
(round boxes) and different response strategies (i.e. , “escape”
and “quiescence”). Further details on the processes involved in the
flooding-response extension, particularly the “escape” and
“quiescence” strategies, will be discussed in the following section.
3.3 Specialized flooding responses—the “escape” and
“quiescence” strategy
Waterlogged soil immediately leads to root endogenous ethylene
accumulation, followed by the root oxygen deficiency that induces the
biosynthesis of the ethylene precursor 1-aminocyclopropane-1-carboxylic
acid (ACC) (Rodrigues et al., 2014). ACC can be converted to ethylene
through oxygenation, and therefore prolonged waterlogging that results
in root oxygen deficiency can lead to ACC accumulation
(Van der straeten
& van Der Straeten,
2017).
ACC can be transported to shoot in dissolved form through xylem
(Vanderstraeten & van Der Straeten, 2017), enabling ethylene
biosynthesis in the shoot, which serves as another source besides direct
diffusion of root ethylene for shoot ethylene under waterlogging.
Ethylene can activate the plasma membrane-located respiratory burst
oxidase homolog (RBOH) protein that converts molecular oxygen to
apoplastic reactive oxygen species (ROS) (Steffens, 2014). The
apoplastic ROS further leads to programmed cell death in the parenchyma
and epidermis, inducing aerenchyma formation and adventitious root
development, respectively (Steffens, 2014). The aerenchyma can largely
reduce the resistance to plant internal gas diffusion and thus promote
plant internal oxygen diffusion from shoot to root. Adventitious roots
serve as an aerated root system alternative to the waterlogged primary
root system; it is aerenchyma-rich, and can therefore transport oxygen
at low resistance (Voesenek & Bailey-Serres, 2015). The development of
aerenchyma and aerenchyma-rich adventitious roots takes approximately
3-7 days after the onset of flooding
(Brailsford et
al., 1993; Guan et al.,
2019).
Under complete submergence, entrapment effect by floodwater results in
abrupt increase of endogenous ethylene in both root and shoot (Voesenek
et al., 1993). In some plant species, the accumulation of shoot ethylene
induces gibberellin signaling that promotes petiole/internode
elongation, thereby outgrowing the floodwater and maintaining
photosynthesis to “escape” the submergence (Fukao et al., 2006). With
the aerenchyma formed in the elongated shoot and adventitious roots
(Bailey-Serres & Voesenek, 2008), oxygen can be diffused to the root,
thus maintaining energy production through aerobic metabolism and root
functioning. This is a mechanism typically observed in deep-water rice
ecotype (Bashar et al., 2019), in which the SNORKEL (SK )
locus encodes two ethylene inducible group VII ERFs, SK 1 andSK 2, that regulate the “escape” strategy (Bailey-Serres et al.,
2012). The induction of the “escape” strategy and its relationship
with plant endogenous oxygen levels and photosynthesis are displayed in
figure 3.