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.