International Journal of

Molecular Sciences

Review
The Role of Phytohormones in Plant Response to Flooding
Xin Wang 1 and Setsuko Komatsu 2, *

1 College of Agronomy and Biotechnology, China Agricultural University, Beijing 100193, China;
[email protected]
2 Faculty of Environmental and Information Sciences, Fukui University of Technology, Fukui 910-8505, Japan
* Correspondence: [email protected]; Tel.: +81-766-29-2466

Abstract: Climatic variations influence the morphological, physiological, biological, and biochemical
states of plants. Plant responses to abiotic stress include biochemical adjustments, regulation of
proteins, molecular mechanisms, and alteration of post-translational modifications, as well as signal
transduction. Among the various abiotic stresses, flooding stress adversely affects the growth of
plants, including various economically important crops. Biochemical and biological techniques,
including proteomic techniques, provide a thorough understanding of the molecular mechanisms
during flooding conditions. In particular, plants can cope with flooding conditions by embracing an
orchestrated set of morphological adaptations and physiological adjustments that are regulated by
an elaborate hormonal signaling network. With the help of these findings, the main objective is to
identify plant responses to flooding and utilize that information for the development of flood-tolerant
plants. This review provides an insight into the role of phytohormones in plant response mechanisms
to flooding stress, as well as different mitigation strategies that can be successfully administered to
improve plant growth during stress exposure. Ultimately, this review will expedite marker-assisted
genetic enhancement studies in crops for developing high-yield lines or varieties with flood tolerance.

Keywords: flooding; plants; rice; soybean; phytohormones; ethylene; abscisic acid

Citation: Wang, X.; Komatsu, S. The

Role of Phytohormones in Plant 1. Introduction
Response to Flooding. Int. J. Mol. Sci.
Climatic conditions around the world are rapidly changing and causing imbalances in
2022, 23, 6383. https://doi.org/
the environment [1]. Environmental variations are responsible for changes in precipitation
10.3390/ijms23126383
patterns, which lead to negative effects on the development and production of crops [2].
Academic Editor: Massimo Maffei Flooding is the most serious abiotic stress, as it induces growth retardation, yield reduction,
and plant death [3]. Flooding causes complete or partial submergence stress, which has a
Received: 22 April 2022
Accepted: 6 June 2022
deteriorative effect on seed germination, vegetative composition, and reproductive develop-
Published: 7 June 2022
ment of plants [4]. Flooding induces oxygen-deficient conditions, which adversely alter the
growth stages of the plant life cycle [5]. Low oxygen conditions alter plant metabolism from
Publisher’s Note: MDPI stays neutral aerobic respiration to anaerobic fermentation, and these metabolic changes are responsible
with regard to jurisdictional claims in
for the impairment of plant development [6,7]. These findings clearly indicate that plant
published maps and institutional affil-
growth and reproductive development are seriously impaired by reduced oxygen during
iations.
exposure to flooding stress.
On the other hand, plants have several strategies to survive submergence conditions.
One strategy is quiescence, where plants do not elongate shoots under flooding conditions
Copyright: © 2022 by the authors.
to minimize energy and carbohydrate consumption, and regrow when the flood recedes.
Licensee MDPI, Basel, Switzerland.
This strategy is efficiently implemented by plants such as soybean and Rumex acetosa, both
This article is an open access article of which can survive relatively deep and transient floods [8–12]. Another strategy is escape,
distributed under the terms and where plants rapidly extend their petioles or stems to allow leaves to reach the surface of
conditions of the Creative Commons the water in order to aerate the remainder of the plant. This strategy is utilized by plants
Attribution (CC BY) license (https:// such as deepwater rice and Rumex palustris [13–17]. These reports indicate that plants have
creativecommons.org/licenses/by/ developed several strategies to cope with the adverse consequences of flooding conditions.
4.0/).

Int. J. Mol. Sci. 2022, 23, 6383. https://doi.org/10.3390/ijms23126383 https://www.mdpi.com/journal/ijms

Int. J. Mol. Sci. 2022, 23, 6383 2 of 23

Under flooding stress, plants differentially regulate proteins involved in hormone

metabolism, signal transduction, transcriptional control, glucose degradation/sucrose
accumulation, alcohol fermentation, gamma-aminobutyric acid shunt, suppression of reac-
tive oxygen species (ROS) scavenging, mitochondrial impairment, ubiquitin/proteasome-
mediated proteolysis, and cell-wall loosening [18–20]. In some of these events, plants
balance the synthesis and transport of phytohormones and regulate the responses to water-
logging via complex signaling processes [21]. These reports indicate that plants can cope
with flooding conditions by embracing an orchestrated set of physiological adjustments,
which are regulated by an elaborate hormonal signaling network.
Phytohormones, such as ethylene, abscisic acid (ABA), and gibberellic acid (GA),
orchestrate the acclimation response to flooding in rice [22]. Physical entrapment and
biosynthesis of ethylene upon flooding have been proven to initiate the plant growth re-
sponse. Low levels of ethylene induce Sub1A-1 expression, which triggers the limitation of
ethylene production during submergence [23]. In deepwater rice, flooding triggers degra-
dation of ABA, which is an antagonist of GA, leading to enhancement of the GA response
and the promotion of shoot elongation [24]. A decrease in ABA and an increase in GA
biosynthesis were demonstrated in response to flooding that promoted the elongation of
shoots necessary for leaf emergence from water [25]. Furthermore, ABA efficiently delayed
ethylene-induced and GA-promoted cell death [26]. These results indicate that phytohor-
mones such as ethylene, ABA, and GA act synergistically to confer plant adaptations to
flooding conditions.
Phytohormones function as the central regulators for plant growth, development, and
stress adaptation during flooding stress, and the signaling responses to phytohormones
display crosstalk. During the past decades, the strategies employed by plants to adapt
to or survive submergence have been revealed through quantitative trait locus mapping
and omics approaches, highlighting the master roles of phytohormones. Herein, the
morphophysiological changes of plants exposed to flooding are summarized, and plant
adjustments to flood are revealed by phytohormone signaling induced by ethylene, ABA,
GA, and others. Furthermore, the interplays of various phytohormone-mediated plant
adaptation and survival strategies during flooding are discussed. This review focuses on
phytohormonal response mechanisms of plants to flooding conditions which will open
new opportunities for agricultural applications to improve plant growth under different
flooding circumstances.

2. Morphophysiological Changes of Plants during Flooding

Flooding leads to either partial or complete submergence stress, and it imposes haz-
ards for plant growth and development from seed germination to grain filling. Leaf
petiole movement, stomatal closure, shoot elongation, and formation of adventitious
roots/lateral roots/aerenchyma are obvious morphological alterations induced by hy-
poxia [13,27]. Carbon/nitrogen metabolism, photosynthesis, ion homeostasis, programmed
cell death, hormone signaling, as well as other cellular metabolisms work in synergy in
flooded plants [28,29]. Herein, the morphophysiological responses of plants to flooding are
summarized (Table 1).
Int. J. Mol. Sci. 2022, 23, 6383 3 of 23

Table 1. Morphophysiological responses of plants to flood conditions.

Species Morphophysiological Response Ref.

Waterlogging induced hyponastic leaf growth mediated by ACO5 involved in ethylene
[30]
biosynthesis.
Hypoxia enhanced the angle of root bending by altering auxin signaling at root apex. [31]
Ability to maintain ROS homeostasis was required for post-flooding tolerance, and ethylene
[32]
accelerated dehydration and senescence of plants during recovery.
Arabidopsis Waterlogging retarded seedling growth and a dense cuticle layer protected plants from diverse
[33]
water conditions.
Epigenetic regulation was associated with sensitization to flood from juvenility to adulthood. [34]
Proper phosphorylation of PINs and auxin transport direction were essential for AR formation in
[35]
pre-etiolated flooding seedlings.
Hypoxia induced potassium limitation and CIPK25 modified potassium flux in seedling roots. [36]
GA sensitivity or transport was involved in leaf expansion and internode elongation in O. sativa. [37]
Partial submergence promoted internodal elongation of O. grandiglumis stem segments to the
[38]
same extent as completely submerged O. sativa stem segments.
Auxin signaling mediated by miR393a was involved in coleoptile elongation and stomatal
[39]
development during seed germination and seedling establishment.
Increased activity of amylase and decreased activities of ADH/PDC facilitated direct-seeded rice
[40]
under waterlogging.
Increased GA4 , whose biosynthesis was transcriptionally mediated by ethylene-responsive factor,
[41]
promotes internode elongation in deepwater rice to adapt periodic flooding.
Rice JA metabolism participated in submergence-mediated internode elongation in deepwater rice. [42]
Reduced chlorophyll content of leaves and induced leaf senescence in seedlings were relieved by
[43]
ethylene precursor.
Acetic, propionic, butyric, and hexanoic acids triggers inducible barrier to ROL in rice under
[44]
waterlogging conditions.
Stagnant flooding reduced grain yield and tiller number, but it increased plant weight and
[45]
ethylene production.
Shallower root growth angle enhanced rice yield in saline paddy field. [46]
ABA induced formation of suberin lamellae in exodermis contributed to ROL barrier formation [47]
in rice.
Accumulation of starch granules and plastoglobules play roles in flooding tolerance. [48]
Amounts of lateral roots and total root mass influenced photon emission in flooded soybean. [49]
Reduced chlorophyll content was rescued by exogenous GAs via an increase in bioactive GA and
[50]
enhancement of ABA biosynthesis.
Well-developed aerenchyma cells in stele and AR contribute to flooding tolerance. [51]
Soybean
ABA content, sugar levels, and circadian clock work to fine-tune photosynthesis and energy
[52]
utilization in flooded plants.
Flooding caused a decrease in asparagine and a concomitant accumulation of GABA. [53]
Flooding suppressed plant height, root structure area, chlorophyll content, chlorophyll
[54]
fluorescence, and amino acid content; however, these were rescued by exogenous ethylene.
ABA and ethylene coordinated transcriptomic energy-saving processes in response to flood. [55]
Hypoxia-induced NO was essential for aerenchyma development, and it accelerated ROS
[56]
production, lipid peroxidation, and protein tyrosine nitration in wheat.
Submergence induced faster leaf degradation and higher levels of phytol/malondialdehyde in
[57]
sensitive cultivars than tolerant wheat.
Waterlogging at tillering impaired photosynthetic activity in leaves and determined oxidative
[58]
injury of roots.
Wheat Well-developed aerenchyma was formed after 72 h of waterlogging, and it started in the
[59]
mid-cortex cells and was regulated by ROS.
Waterlogging increased ROS content in endosperm cells and eventually accelerated PCD. [60]
Waterlogging elevated the degree of emulsification and the degradation rate of endosperm cells;
[61]
however, it reduced the number of amyloplasts in the endosperm.
Waterlogging reduced internode lignin content and cytokinin mediated lignin deposition in
[62]
plant biomass.
Int. J. Mol. Sci. 2022, 23, 6383 4 of 23

Table 1. Cont.

Species Morphophysiological Response Ref.

N-end rule pathway was a key regulator of the waterlogging response in barley, and reduced
HvPRT6 expression enhanced plant tolerance with sustained biomass, enhanced yields, and [63]
Barley retention of chlorophyll.
Hypoxia-induced potassium loss in roots was correlated with cell ability. [64]
Compared with shoots, the roots were more impaired by waterlogging as evidenced by reduced
[65]
length, area, and biomass.
Hypoxia limited root function by perturbing auxin flow and distribution for establishment of an
Maize oxidized redox in the quiescent center, but these impacts were alleviated by overexpression of [66]
phytoglobin.
Enhancement of chlorophyll biosynthesis by ZmCAO1 confers maize tolerance to waterlogging. [67]
Lateral roots were able to form a barrier to ROL as sites for oxygen loss under hypoxic conditions. [68]
IAA allowed enhancement of root hydraulic conductivity in mycorrhizal plants under hypoxic
[69]
conditions.
ABA depletion improved water absorption during long-term waterlogging and maintained the
Tomato [70]
relative water content in leaves.
Reduced alcohol fermentation and enhanced glycolysis induced by hypoxia stress priming was
[71]
crucial for flood tolerance.
Levels of ethylene, auxin, and ROS accumulated in waterlogged plants; ROS mediated ethylene-
Cucumber [72]
and auxin-induced AR formation.
Increased accumulation of GABA, succinic acid, and alanine at initial hypoxia remained at high
Grapevine [73]
levels within one week after recovery.
Waterlogging reduced the number of stem/leaves, dry biomass of shoot/root, and chlorophyll
[74]
fluorescence in tetraploid lotus.
Lotus
Water-repellent leaves became greasy, petioles of newly developed leaves became slim and long
[75]
within the initial submergence, and almost all leaves fell off after stress was expended.
Waterlogging decreased accumulation of raffinose, sucrose, hexoses, and pentoses in roots, and it
Barrel clover [76]
increased starch, sugar, and phenolics content in leaves.
Petiole reorientation towards vertical under partial and full submergence; however, constant rate
Melilotus siculus [77]
of petiole extension and accumulation of sugar were only present during partial submergence.
Soil water table with middle level promoted formation of knee roots via induced ethylene and
Taxodium ascendens [78]
IAA production.
Ref, reference; ABA, abscisic acid; ADH, alcohol dehydrogenase; AOC5, ACC oxidase 5; AR, adventitious root;
CIPK25, calcineurin β-like interacting protein kinase 25; CAO, chlorophyll A oxygenase; GA, gibberellic acid;
GABA, gamma-aminobutyric acid; IAA, indole acetic acid; JA, jasmonic acid; PCD, programmed cell death; PDC,
pyruvate decarboxylase; PIN, PIN-FORMED; ROL, radial oxygen loss; ROS, reactive oxygen species.

2.1. Arabidopsis
Arabidopsis attune morphological adaptation and physiological responses to flooding
to maximize their efficacy or minimize stress impacts. The root is the first organ to sense
flooding and the plants can replace the original root system with adventitious roots if the
oxygen supply is scare [79]. Hypoxia inhibits growth of the main roots, while adventi-
tious roots facilitate oxygen supply, resulting in improvement of root growth and plant
survival. It was elucidated that auxin played an essential role in adventitious rooting by the
hypocotyls of pre-etiolated flooded seedlings of Arabidopsis through activation of auxin
transport by PIN-FORMED and AUXIN RESISTANT1/LIKE AUX1 [35]. The group VII
ethylene response factor (ERFVII) HRE2 promoted elongation of emerging adventitious
roots [80], but inhibited hypoxia-induced root bending [31]. Additionally, a set of physio-
logical responses are induced by hypoxia in Arabidopsis seedlings. For example, oxygen
shortage resulted in potassium starvation in plant roots, and calcium-dependent signaling
by CIPK25 improved seedling capacity to maintain ion homeostasis [36]. ROS homeostasis,
stomatal aperture, and chlorophyll degradation ultimately influence plant recovery from
submergence through the activation of SENESCENCEASSOCIATED GENE113, ORESARA1,
and RESPIRATORY BURST OXIDASE HOMOLOG D [32]. These studies show that inter-
play of hormone signaling with ROS homeostasis contributes to morphological alterations
in response to flood and post-recovery flooding conditions.
Int. J. Mol. Sci. 2022, 23, 6383 5 of 23

2.2. Rice
Under flooding, deepwater rice accelerated underwater internode elongation via a
boost in GA production with the aid of ethylene; however, semi-dwarf rice grown in
paddy fields displayed short stems due to the low efficiency of GA biosynthesis, but
sufficient GA was produced in the uppermost stem node to allow internode elongation in
order to produce floral clusters above the leaf canopy during flowering [81,82]. In wild
rice, Oryza grandiglumis, quiescence was not mediated by Sub1A as previously reported for
deepwater rice, and the escape response based on internode elongation was induced by high
moisture content instead of ethylene [38]. A comparative study between deepwater and
non-deepwater rice showed that GA biosynthesis, trehalose biosynthesis, fermentation, cell
wall modification, ethylene signaling, and jasmonic acid (JA) metabolism were significantly
different between these two cultivars, and JA participated in internode elongation during
the submergence of deepwater rice [42]. Aside from stem elongation, the formation of
radial oxygen loss (ROL) in rice roots is an induced by waterlogging, and ABA-induced
suberin lamellae formation in the exodermis facilitated ROL barrier formation [47,83].
Meanwhile, low concentrations of organic acids, specifically acetic, propionic, butyric, and
hexanoic acid, triggered a ROL barrier in roots but with a slight effect on root extension [44].
Additionally, rice roots developed on the soil surface to protect plants from stresses in paddy
fields and increase rice yields based on the regulation of DEEPER ROOTING 1 involved
in root system architecture [46]. These findings suggest that cross talk of GA, ethylene,
and JA directs stem elongation, and ABA and organic acids meditate ROL formation in
flooded rice.

2.3. Soybean
The influence of flooding stress on soybean morphological alterations are evidenced by
the suppression on radicle protrusion, root structure, stem elongation, and photosynthesis
pigment [84]. Oxygen deficiency suppressed nitrogen fixation by the nodules of soybeans
due to the reduced activity of nitrogenase and downregulation of asparagine synthetase and
glutamic acid decarboxylase; however, these effects were reversible after draining [53]. Flood-
ing induced a reduction in net photosynthesis that could be relieved by the accumulation
of starch granules and the application of exogenous ethephon [48,54]. A comparative study
between a waterlogging tolerant soybean line and a sensitive line showed better develop-
ment of adventitious roots/aerenchyma cells in stele and a higher ethylene production
ratio contributed to flourishing plants during waterlogging [51]. In addition, a series of
physiological responses was responsible for retarded growth in flooded soybeans, such as
mitochondrial impairment, cell wall loosening, proteosome-mediated degradation, and
sucrose accumulation [85]. However, enhancement of transcriptional regulation/protein
homeostasis, suppression of cell death, and activation of auxin-triggered transcriptomic
modifications for saving energy worked synergistically to help soybean survive short-term
flooding [55,84]. These findings show that auxin and ethylene are involved in soybean
adaptation to flood conditions through the regulation of adventitious root formation and
energy conservation.

2.4. Wheat
In wheat, cell death in seminal roots and the short length of adventitious roots induced
by hypoxia resulted in a low root:shoot ratio, and deficient nitrogen efficiency hampered
shoot growth and grain yield [86]. An increase in adventitious root number and aerenchyma
formation within these roots are characteristic of wheat tolerance to waterlogging, and
nitric oxide was necessary to induce aerenchyma, either upstream of or in parallel with
ethylene [56,86]. Aerenchyma formed 10 mm from the root tip and was mediated by ROS
that initially accumulated in mid-cortex cells [59]. Waterlogging also induced ROS acceler-
ated programmed cell death in endosperm cells when wheat seedlings were exposed to
stress at the flowering stage [60]. Similarly, during seed germination, the degree of emulsifi-
cation and endosperm cell degradation was increased and the number of amyloplasts was
Int. J. Mol. Sci. 2022, 23, 6383 6 of 23

reduced in waterlogged wheat compared with the control [61]. Additionally, a comparative
study was carried out in two wheat cultivars with contrasting submergence tolerance, and
leaf gradation was faster and phytol/malondialdehyde content was higher in the sensitive
cultivar compared the tolerant genotype, indicating that deprivation of ROS contributed
to wheat tolerance to submergence [57]. These reports highlight the detrimental effects of
flooding on seed germination and leaf senescence, but the acceleration of ROS scavenging
might relieve these symptoms in stressed wheat.

2.5. Other Plants

The effects of flooding stress on plant growth and development have also been ob-
served in other plants. In barley, the average yield was reduced up to 50% by waterlog-
ging [87]; however, sustained biomass, increased yield, and retention of chlorophyll were
observed in barley with loss-of-function of proteolysis6 [63]. Activation of depolarization-
activated outward-rectifying potassium channels can improve potassium retention and
confer hypoxia stress tolerance in barley [64]. In maize, waterlogging exerts severe impacts
on the roots rather than the shoots [65], limiting root function due to hypoxia perturbed
auxin flow/distribution, which is required to establish a quiescent center, and suppressing
phytoglobins that can stabilize root performance under low oxygen conditions [66]. In
addition, an improvement in root architecture and enhancement of chlorophyll biosynthe-
sis through overexpression of ZmCAO1 enhanced maize tolerance to waterlogging [67].
Moreover, adventitious root formation, carbohydrate metabolism, ROS accumulation, and
hormone signaling were responsible for hypoxic conditions in tomato, cucumber, grapevine,
and lotus [69,70,72,73,75], indicating that flooding stress can induce general alterations
in plants.

3. Ethylene Signaling in Plants during Flooding

Flooding is detrimental for plants mainly due to restricted gas exchange underwa-
ter, which further induces rapid accumulation of ethylene in plant cells [88]. Ethylene
is considered the major regulator of plant adaptation to flooding stress, such as raising
plants by aerenchyma, facilitating gas diffusion by adventitious roots, directing antithetical
strategies for plant survival by shoot elongation, and elevating leaves above water based on
hyponastic growth [89]. Ethylene is also extensively characterized as an essential phytohor-
mone for recovery after hypoxia by replenishing tricarboxylic acid cycle substrates [90,91],
and post-submergence induced ethylene could interplay with ROS, photoinhibition, and
desiccation to modulate plant growth during anoxia reoxygenation [32,92]. In this section,
ethylene signaling in plant responses to flooding stress are summarized (Figure 1, Table 2).
Table 2. Ethylene signaling in plants during flooding stress.

Plant Species Ethylene Signaling during Flood Ref.

Ethylene increased water transport rate in leaf cells by enhancing
[93]
S280/S283 phosphorylation at the C terminus of PIP2;1.
Ethylene inhibited formation of adventitious roots and overrode
[31]
HRE2-induced adventitious root elongation.
Arabidopsis
Hypoxia induced the primary roots to grow sidewise, and it was inhibited
[80]
by RAP2.12.
Leaf movement was reduced by root flooding in seedlings with
[30]
loss-of-function of aco5.
Int. J. Mol. Sci. 2022, 23, 6383 7 of 23

Table 2. Cont.

Plant Species Ethylene Signaling during Flood Ref.

Accumulation of ethylene did not induce internode elongation in Oryza
[38]
grandiglumis.
Ethylene signaling played a negative role in seed germination, but
improved seedling tolerance to submergence through regulation of the [43]
antioxidant response.

Rice Stagnant flooding accelerated ethylene production and sub1-introgression

[45]
into rice cultivar increased plant sensitivity to stagnant flooding.
OsEIL1a specifically bound to SD1 promoter, resulting in increased GA
[41]
content, and allowed deepwater rice tolerance to submergence.
Sub1a governed distinct responses to submergence in mature and
[94]
growing leaves through regulation of ethylene, ABA, JA, and auxin.
Sub1a promoted precocious photoautotrophy and restricted underwater
[95]
elongation during seed germination.
Exogenous ethylene promoted soybean growth during initial flooding
[96]
through regulation of protein phosphorylation.
Exogenous ethylene mitigated waterlogging stress in soybean with
increased root surface, improved photosynthesis, and higher [54]
accumulation of protein/glutathione S-transferase.
Soybean Ethylene was associated with cell wall remodeling in flooded soybean
[97]
through regulation of expression of GmXTHs.
Ratio of ethylene production was higher in a waterlogging tolerant line
[51]
than sensitive soybean.
Expression of genes related to ethylene biosynthesis were enhanced in
[98]
roots of flood-tolerant soybean.
ZmEREB180 positively regulated maize waterlogging tolerance through
Maize [99]
regulation of adventitious root formation and ROS homeostasis.
Waterlogging effects on root growth, emergence and elongation of axile
Wheat and lateral roots, and aerenchyma formation were associated with [100]
upregulation of ACS7 and ACO2 involved in ethylene biosynthesis.
Tomato Flooding stress induced ERF.E1, E2, E3, and E4 in tomato seedlings. [101]
Accumulation of ethylene induces formation of adventitious roots during
Cucumber waterlogging and stimulated accumulation of auxin, which in turn [72]
increased ethylene content.
Expression levels of NnACSs involved in ethylene biosynthesis were
Lotus [75]
significantly upregulated in lotus during initial submergence.
Overexpression of AdRAP2.3 enhanced tobacco tolerance to waterlogging
Kiwifruit [102]
via enhanced activities of PDC and ADH.
PhERF2 bound to ADH1-2 promoter and positively contributed to
Petunia waterlogging tolerance through modulation of programmed cell death [103]
and fermentation.
High levels of ethylene accumulated in waterlogging tolerant variety
Chrysanthemum
morifolium compared with sensitive lines during waterlogging and reoxygenation [104]
conditions.
Exogenous ethylene improved water transport via increased expression
Populus tremuloides levels of PIP2;4 and PIP2;5 in roots of trembling aspen under hypoxic [105]
conditions.
Ethylene was induced by the middle water table, resulting in an
Taxodium ascendens enhancement of flood tolerance through the improvement of root [78]
ventilation.
Ref, reference; ABA, abscisic acid; ACO, 1-aminocyclopropane-1-carboxylic acid oxidase; ACS, 1-
aminocyclopropane-1-carboxylic acid synthase; ADH, alcohol dehydrogenase; EIL, ethylene insensitive like;
ERF, ethylene response factor; GA, gibberellic acid; HRE, hypoxia responsive ERF; JA, jasmonic acid; RAP, related
to apetala; PDC, pyruvate decarboxylase; PIP, plasma membrane intrinsic protein; ROS, reactive oxygen species;
SD, SEMI-DWARF; Sub1, Submergence1; XTH, xyloglucan endotransglycosylases/hydrolases.
 egies for plant survival by shoot elongation, and elevating leaves above water based on
hyponastic growth [89]. Ethylene is also extensively characterized as an essential phyto‐
hormone for recovery after hypoxia by replenishing tricarboxylic acid cycle substrates
[90,91], and post‐submergence induced ethylene could interplay with ROS, photoinhibi‐
tion, and desiccation to modulate plant growth during anoxia reoxygenation [32,92]. In
Int. J. Mol. Sci. 2022, 23, 6383 8 of 23
this section, ethylene signaling in plant responses to flooding stress are summarized (Fig‐
ure 1, Table 2).

Figure 1. Ethylene signaling involved in plant response to flooding. Flooding increases ethylene
amount and subsequently induces RAP2.3, ERF2, Sub1A, EILa/b, PIP2;1/2;4/2;5 to modulate fermenta-
tion, root architecture, GA homeostasis, and water transport capacity in Arabidopsis, rice, soybean,
Actinidia deliciosa, Petunia (Petunia × hybrida), and Populus tremuloides. ADH, alcohol dehydrogenase;
ERF2, ethylene response factor2; EIL, ethylene insensitive like; GA, gibberellic acid; PCD, programmed
cell death; PDC, pyruvate decarboxylase; PIP, plasma membrane intrinsic protein; RAP2.3, related
to apetala 2.3; SD1, SEMI-DWARF1; SK1/SK2, SNORKEL1/SNORKEL2; Sub1A, Submergence1A; XTH,
xyloglucan endotransglycosylases/hydrolases.

3.1. Arabidopsis
Aquaporins help plants maintain water balance and gas transport under hypoxic con-
ditions, and ethylene promotes water transport rate via phosphorylation of AtPIP2;1 [93];
in addition, the abundance of RAP2.12, an ERF-VII factor, is involved in the regulation of
aquaporin activity under the control of HCR1 [106]. RAP2.12 negatively regulated root
bending induced by hypoxia, showing that the growth direction of primary roots is antago-
nistically regulated by low oxygen and hypoxia-activated ERF-VIIs [31]. Overexpression of
HRE2, a member of the ERF-VIIs, induces elongation of adventitious roots, suggesting that
ERF-VII transcription factors enhance the establishment of adventitious roots under the
negative control of ethylene [80]. Ethylene stimulates auxin synthesis in cotyledons, which
was then translated to epidermal cell layers in the hypocotyl and interacted with GA and
brassinosteroid (BR) to induce hypocotyl elongation [107]. Besides the roles of ethylene
in root architecture and hypocotyl elongation, ethylene signaling was also responsible
for leaf movement, as evidenced by the ethylene-SHYG-ACO5 loop for the onset of rapid
petiole cell expansion during waterlogging stress [30]. These results show that ethylene
has versatile roles in root architecture, hypocotyl elongation, and leaf movement via the
diverse functions of ERF-VIIs.

3.2. Rice
A plethora of findings have demonstrated the effects of ethylene on seed germina-
tion and plant growth in rice exposed to flooding. Rice seeds can germinate in absence
of sufficient oxygen with lengthening of the coleoptile due to smart sugar management
mediated by cross interaction of alpha-amylase activity, calcium signaling, and trehalose-6-
P-phosphate content [108,109]. A reduction in the germination rate during submergence
stress could be mitigated by blocking ethylene signaling; however, ethylene priming
improved seedling survival during submergence through the activation of antioxidant
responses mediated by hydrogen peroxide [43]. Ethylene effects on plant height have been
Int. J. Mol. Sci. 2022, 23, 6383 9 of 23

addressed by studies on ERFs such as Sub1A [110], SNORKEL1/2 [15], and OsEIL1a [41].
Sub1A dampens ethylene production and GA responses, leading to quiescent growth of
seedlings during submergence [23], and SNORKEL1/2 and OsEIL1a boosted stem elonga-
tion via enhancement of GA and conferred an escape strategy on deepwater rice [15,41].
However, not all rice varieties respond to submergence dependent on ethylene. For ex-
ample, the wild rice Oryza grandiglumis displayed enhanced growth based on internode
elongation during partial submergence of mature plants, but no significant ethylene accu-
mulation was observed at the internode; similarly, the growth of shoots was not improved
by complete submergence or exogenous ethylene owing to a lack of Sub1A [38,111]. These
reports highlight the importance of ethylene signaling for rice adaptation to flooding and
address how ethylene directs stem elongation.

3.3. Soybean
Compared with the excellent works in rice, the roles of ERFs in soybean have not been
reported yet; however, a series of studies indicate that ethylene signaling participates in the
soybean response to flooding. Soybean seeds are sensitive to sowing fields with uneven
soil leveling, resulting in the poor performance of germination and seedling establish-
ment [112,113]. Initial flooding during seed germination suppressed root growth, whereas
application of ethylene promoted soybean growth through the enhancement of protein
phosphorylation in root tips [76]. Similarly, exogenous ethylene relieved waterlogging
induced symptoms via activated adventitious root initiation, increased root surface area,
improved photosynthesis pigment, and an enhanced capacity for ROS scavenging [54]. The
expressions of GmXTHs, which plays a role in cell wall extensibility through the modifica-
tion of xyloglucan chains or catalysis of the hydrolysis of xyloglucan, were associated with
ethylene and flooding, suggesting that ethylene signaling participated in flood-induced cell
wall loosening [97]. A comparative study between flood-tolerant and -sensitive soybean
showed that the genes related to ethylene biosynthesis were induced by the onset of stress
and to higher levels in the roots of the tolerant genotype [98]. In another study, inconsis-
tent changes in hormone profiles were observed based on the characteristics of soybean
tolerance to waterlogging, and of note, a higher ratio of ethylene production was observed
in the tolerant variety than the sensitive lines [51]. These reports indicate that a high level
of ethylene accumulation correlates with improved tolerance to flooding stress through the
modification of protein phosphorylation, ROS scavenging, and cell wall loosening.

3.4. Other Plants

Flood-induced ethylene signaling is responsible for root architecture, water transport,
energy metabolism, and programmed cell death in maize, wheat, tomato, cucumber, lotus,
and kiwifruit. Ethylene signaling responds to the onset of submergence stress with a
sharp upregulation of the ACC synthases involved in ethylene biosynthesis [75]; meanwhile,
increased ethylene levels stimulate auxin accumulation, which in turn, increases ethylene
production to facilitate the formation of adventitious roots [72]. Ethylene regulation in
flooded plants has been further proved with the identification of ERFs. For example, ERF
ZmEREB180 improved maize survival during waterlogging through prompt primordial
root initiation and activated ROS scavenging [99]. Similarly, ectopic expression of AdRAP2.3,
a member of ERFs in kiwifruit, enhanced tobacco tolerance to waterlogging with increased
survival rate/plant biomass and prompt formation of aerial roots with the aid of increased
activities of pyruvate decarboxylase and alcohol fermentation compared with wild type
seedlings [102]. A study in petunia found that PhERF2 could bind to the ADH1-2 promoter
and gain-of-function of PhERF2 increased seedling tolerance to waterlogging, indicating
that ethylene signaling participated in anaerobic fermentation to generate energy for proper
functioning [103]. These reports show versatile roles of ERFs are involved in plant tolerance
to flooding based on ROS scavenging, alcohol fermentation, and initiation of aerial roots.
Int. J. Mol. Sci. 2022, 23, 6383 10 of 23

4. Abscisic Acid Signaling in Plants during Flooding

It is widely accepted that plant responses to flooding stress are mainly regulated by
ethylene signaling, and the interplays of ethylene and other phytohormones have been
documented [27]. ABA signaling is associated with quiescent or escape strategies employed
by plants based on the differential induction of ABA-dependent pathways, which can direct
stem elongation though interactions with ethylene and GA [114]. Although the roles of
ABA in flooding responses have been overshadowed by ethylene and GA, it participates
in the emergence of adventitious roots, formation of secondary aerenchyma, hyponastic
growth under hypoxia, as well as recovery from hypoxia [115,116]. ABA signaling in plant
response to flood is presented below (Figure 2, Table 3).

Table 3. ABA signaling in plants to flooding stress.

Plant Species ABA Signaling during Flood Ref.

ABA interacted with ethylene to control stomata opening, dehydration, and
[32]
senescence through SAG113 and ORE1 during submergence recovery.
Application of ABA (10 µM) negatively regulated the expression of pyruvate
[117]
decarboxylase1 in response to waterlogging stress.
Arabidopsis Hypoxia induced AKIN10 and controlled protein stability of AtMYC2, which
[118]
was activated by ABA signaling in response to seawater flooding.
ABA signaling was a determinant for plant sensitivity to submergence and
impaired ABA signaling due to loss-of-function of abi2-1 enhanced plant [34]
survival during submergence.
Inhibition of ABA biosynthesis suppressed the formation of a ROL barrier and
[47]
development of suberin lamellae under stagnant conditions.

Rice ABA suppressed expression of miR393a, which regulated coleoptile elongation

[39]
for seed germination during submergence.
ABA content fluctuated at a low level during seed germination when
[119]
submerged, which was mediated by OsVP1.
ABA inhibited elongation of cells derived from phellogen during secondary
[120]
aerenchyma formation induced by flooding.
Flooding reduced ABA content in leaves of plants during flooding, especially
[48]
the tolerant cultivar exposed to flooding for 15 days.
Downregulation of ABA in response to flooding contributed to well-developed
[51]
aerenchyma cells.
Diurnal expression of TOC1 was found in soybean exposed to flooding, and
[52]
higher expression of TOC1 coincided with elevated ABA content.

Soybean Application of ABA (100 µM) could not protect plants from 14 days of
[54]
waterlogging.
Submergence reduced the abundance of bioactive ABA in roots and leaves in
seedlings, and a low amount of ABA was sufficient to trigger ABA effects [55]
involved in quiescence.
Application of ABA (10 µM) improved soybean tolerance during initial and
survival stages of flooding through regulation of energy conservation, [22,121–123]
enhanced cell wall integrity, and inhibition of cytochrome P450 77A1.
ABA signaling affected soybean responses to initial flood through
phosphorylation of BTB domain containing protein 47, glycine rich protein, [124]
and rRNA processing protein Rrp5 in root tips.
Int. J. Mol. Sci. 2022, 23, 6383 11 of 23

Table 3. Cont.

Plant Species ABA Signaling during Flood Ref.

ABA depletion positively regulated plant tolerance to short-term waterlogging
[70]
via improved gas exchange, activated NO metabolism, and ERF-VII stability.
Tomato
ABA was decreased in the roots of flooded mycorrhizal and non-mycorrhizal
[69]
plants, whereas no significant difference was observed in leaves.
In a waterlogging-sensitive cultivar, ABA content in waterlogged hypocotyls
Cucumber decreased approximately 63.9% compared with the control, but no significant [125]
difference was observed in the tolerant variety.
Decrease in ABA was implied by downregulation of NcNCEDs and
Lotus upregulation of NnCYP707A, which was related to ABA biosynthesis and [75]
degradation, respectively, in response to initial submergence.
Enhanced ABA signaling facilitated growth suppression in Rumex acetosa
Rumex acetosa [9]
through a combination of maintained ABA levels and elevated receptor levels.
Drop in ABA was examined in stem and adventitious root primordia tissue in
Solanum dulcamara flooded plants, whereas ABA application (1 mM) prevented activation of [126]
adventitious root formation induced by flooding.
ABA depletion constituted a specific response to flooding, and the conjugation
Carrizo citrange involved in ABA metabolism was complementary to degradation in order to [127]
maintain ABA homeostasis.
Ref, Reference; ABA, abscisic acid; ABI, ABA insensitive; ERF, ethylene response factor; NCED, 9-cis epoxy-
Int. J. Mol. Sci. 2022, 23, x FOR PEER REVIEW 10 of 21
carotenoid dioxygenase; OsVP1, Oryza sativa Viviparous1; ROL, radial oxygen loss; SAG, senescence-associated
gene; TOC1, Timing of CAB expression1.

Figure 2. ABA
Figure ABA signaling
signalinginvolved
involvedininplant
plantresponse
responseto to
flooding stress.
flooding Flooding
stress. alters
Flooding ABAABA
alters content
content
with different
with different accumulation
accumulationpatterns.
patterns.The
Theimpact
impactof of
exogenous
exogenous ABA ABAon flooded plants
on flooded during
plants seedseed
during
germination and seedling establishment are summarized based on reported genes and proteins re‐
germination and seedling establishment are summarized based on reported genes and proteins
lated to coleoptile elongation, root growth, cell wall integrity, energy provision, and stomatal open‐
related to coleoptile
ing in Arabidopsis, elongation,
rice, root
and soybean. growth,
ABA, cellacid;
abscisic wall integrity,
CDC5, energycycle
cell division provision, andchap‐
5; Chap20, stomatal
opening
erone 20;in Arabidopsis,
ENO, rice, and
enolase; GRPs, soybean.
glycine ABA, NAC,
rich proteins; abscisic acid; CDC5,
nascent cell division
polypeptide cycle
associated 5; Chap20,
complex;
chaperone 20; ENO,
PDC1, pyruvate enolase; GRPs,
decarboxylase1; glycine
PGIP, rich proteins; NAC,
polygalacturonase nascentprotein;
inhibiting polypeptide
Rrp5,associated
RNA bindingcomplex;
rRNA processing
PDC1, pyruvate decarboxylase1; PGIP, senescence‐associated
protein 5; SAG113, gene 113; ZFPs,
polygalacturonase inhibiting zincRrp5,
protein; fingerRNA
proteins.
binding rRNA
processing protein 5; SAG113, senescence-associated gene 113; ZFPs, zinc finger proteins.
Table 3. ABA signaling in plants to flooding stress.

Plant Species ABA Signaling during Flood Ref.

ABA interacted with ethylene to control stomata opening, dehydration, and senescence through
[32]
SAG113 and ORE1 during submergence recovery.
Application of ABA (10 μM) negatively regulated the expression of pyruvate decarboxylase1 in re‐
[117]
sponse to waterlogging stress.
Int. J. Mol. Sci. 2022, 23, 6383 12 of 23

4.1. Arabidopsis
Ethanolic fermentation is essential to mitigate the energy crisis induced by flood-
ing [13]. The enzyme pyruvate decarboxylase plays pivotal roles in fermentation [128],
and overexpression of kiwifruit pyruvate decarboxylase1 in Arabidopsis conferred tolerance
to waterlogging on seedlings, whereas the application of ABA caused a drop in the tran-
scriptional level of pyruvate decarboxylase and resulted in inhibition of seed germination
and root growth [117]. AKIN10 is a conserved energy sensor, and its activity has an inverse
modulatory role in plant adaptation to seawater through the regulation of ABRE and RD22
promoter activities based on the protein stability of AtMYC2 [118]. Furthermore, ABA
signaling has been associated with plant tolerance to post-recovery flood. For example,
ABA signaling was a determinant for sensitivity to flooding in abi2-1 mutant plants, which
were ABA insensitive and presented better survival during submergence than wild-type
adult seedlings, indicating that enhanced ABA sensitivity has a negative impact on post-
submergence recovery [34]. In addition, expression of SAG113, a positive regulator of
ethylene signaling, was elevated during flood recovery, but was decreased by the treatment
of an ABA antagonist, suggesting interplays of ABA and ethylene on stomatal opening and
dehydration [32]. These results show that ABA signaling appears to negatively regulate
tolerance of Arabidopsis for flooding.

4.2. Rice
ABA signaling has been proved to contribute to oxygen transport, anaerobic germi-
nation, and stem elongation in flooded rice. A barrier to ROL enhances oxygen transport
to the root apex and ABA signaling induced suberin lamellae formation in the exodermis;
additionally, ABA application rescued the barrier that could not form in the mutant osaba1
exposed to waterlogged soil [47]. It has been verified that miR393a contributed to retar-
dation of coleoptile elongation and inhibition of stomatal development when seeds were
submerged during germination. ABA application also promoted expression of miR393a,
which was inhibited by submergence [39]. Furthermore, OsVP1, a transcription factor
involved in ABA signaling, was a potential candidate for improving anaerobic germination
tolerance in rice [119]. In addition, ABA signaling is responsible for suppression of stem
elongation in rice during submergence. The accumulation of ethylene in flooded stems
functions as an initial signal to enhance internodal elongation; it also reduces the amount
of ABA and leads to an enhancement of GA-induced stem elongation, conferring an escape
strategy on deepwater rice [129]. These reports show that increased ABA content inhibits
seed germination and stem elongation during flooding by either working alongside or
interacting with GA responses.

4.3. Soybean
Flooding stress reduces the accumulation of ABA in roots and leaves of soybean
seedlings in spite of tolerance to flood, and a lower level of ABA was observed in flood-
tolerant varieties than sensitive lines [48,55]. ABA signaling in flooded soybean appears
controversial. Similar to the findings for Arabidopsis and rice, ABA is a negative player in
conferring soybean flooding tolerance. For example, ABA inhibited the elongation of cells
derived from phellogen during secondary aerenchyma formation in flooded soybean [120],
which was consistent with the finding that downregulation of ABA contributed to well-
developed aerenchyma cells [51]. On the other hand, application of ABA improved soybean
flood tolerance in response to initial stress and during post-recovery stages. ABA content
did not change in response to flooding during seedling establishment [22], but ABA altered
the phosphorylation status of nuclear proteins in response to initial flooding stress [124].
In another study, application of ABA (10 µM) increased soybean tolerance to initial flood
through activation of proteins involved in protein synthesis and RNA regulation [121].
Furthermore, exogenous ABA (10 µM) improved plant survival during flood through
the modulation of energy conservation, enhancement of lignification, and inhibition of
cytochrome P450 77A1 [121–123]. Although the role of ABA signaling in soybean flood
Int. J. Mol. Sci. 2022, 23, 6383 13 of 23

tolerance seems contentious, ABA (10 µM) application could be utilized to improve plant
tolerance to short-term flooding.

4.4. Other Plants

Survival strategies employed by flooded plants have been studied in the wild dicot
species Rumex acetosa and Rumex palustris with the finding that accumulated ethylene
induced enhancement of ABA signaling and reduced GA in R. acetosa, resulting in growth
suppression and quiescence; in contrast, high amounts of ethylene downregulated ABA and
upregulated GA to initiate the growth response in R. palustris [25,114,130]. ABA depletion
induced by flooding stress has also been found in tomato [69,70], lotus [75], cucumber [125],
Solanum dulcamara [126], and Carrizo citrange [127]. In tomato seedlings, 24h waterlogging
caused a reduction in ABA content and induced expression of ABA receptors and ABA-
dependent transcription factors; when stress was terminated, a reduction in gas exchange
parameters was only observed in wild-type plants but not in the ABA-deficient genotype,
suggesting that ABA depletion functions as a positive player in tomato responses to short-
term flooding [70]. A comparative study was performed in cucumber seedlings with
contrasting tolerance to waterlogging and the authors found that waterlogging exerted a
dramatic drop in ABA in the hypocotyls of the tolerant variety compared with untreated
seedlings due to accumulated ethylene; however, no significant ABA alterations were
observed in the sensitive cultivar, resulting in suppressed growth of adventitious roots [125].
These results show that enhanced ABA signaling is a negative player in the formation of
adventitious roots induced by flood.

5. Other Phytohormone Signaling in Plant during Flooding

A series of publications has proven that ethylene is the primary signal for plant adap-
tation to flooding; additionally, ethylene modulates a hormone cascade of ABA, GA, and
auxin to induce adventitious rooting, internode elongation, and carbohydrate degrada-
tion [109,131]. Additionally, the effects of BR, JA, and salicylic acid (SA) on improving plant
tolerance to flood are either independent or dependent on ethylene signaling to facilitate
plant growth through activation on formation of adventitious roots, shoot elongation,
photosynthetic pigment, and ROS scavenging [132–135]. Herein, phytohormone signaling,
including GA, auxin, BR, JA, and SA, is described (Figure 3; Table 4).

Table 4. Effects of GA, auxin, BR, JA, and SA in plants during flooding stress.

Hormones Plant Species Hormone Signaling Ref.

Flooding increased GA1 and GA4 content due to activation of
OsGA20ox2, and GA induced internode elongation during the [37]
six-leaf stage in deepwater rice.
SD1 largely increased the content of GA4 via interaction with
[41]
OsEILa and promoted internode elongation in deepwater rice.
Rice
GA promoted elongation of the internode based on the
[42]
reduction of JA content in deepwater rice.
DEC1 and ACE1 inhibited and accelerated stem elongation,
respectively, through GA-mediated cell division in the [81]
GA internode.
GA signaling was activated by initial submergence of both of
Rumex acetosa/R. palustris Rumex acetosa and R. palustris, whereas sensitization to GA [9]
prior to its accumulation was induced in R. palustris.
Sln1d.8 allele, which encodes DELLA that can be degraded by
Barley GAs, improved seedling tolerance to flooding independent of [136]
root porosity.
Application of GA4+7 (50 µM) ameliorated the effects of
Soybean short-term flooding through enhancement of glutathione [50]
activity, chlorophyll content, and NO signaling.
Slight increase in GA within the first 24 h of submergence was
Lotus [75]
partly due to upregulation of NnGA3OX1/2/3/4.
Int. J. Mol. Sci. 2022, 23, 6383 14 of 23

Table 4. Cont.

Hormones Plant Species Hormone Signaling Ref.

Hypoxia reduced protein abundance of PIN2, and
[31]
overexpression of RAR2.12 rescued this symptom.
Arabidopsis Activation of PIN1/AUX1/AFB2 and suppression of
LAX1/LAX3/PIN4/PIN7 improved the development of [35]
adventitious roots.
Submergence inhibited expression of miR393a, which
Rice negatively regulated auxin receptors OsTIR1 and OsAFB2 to [39]
mediate elongation and stomatal development in coleoptiles.
Auxin ZmPgb1.1 sustained PIN-mediated auxin and oxidized
Maize environment in the quiescent center of root apical meristems of [66]
seedlings during hypoxia.
Waterlogging increased auxin-enhanced ethylene biosynthesis
Cucumber and they synergistically promoted formation of adventitious [72]
roots.
Compared with partial submergence, complete submergence
Solanum dulcamara impaired the growth of adventitious root due to disruption of [137]
auxin instead of ABA and JA.
During submergence, rice bearing Sub1A had a high content of
Rice BRs, which resulted in lower amounts of GA to restrict shoot [132]
elongation.
24-epibrassinolide (10 nM) relieved effects of waterlogging on
BR Soybean soybean with improved root anatomy, photosynthetic pigment, [133]
ROS scavenging, and increased biomass.
A general downregulation of genes related to BR, auxin, and
Grapevine GA biosynthesis was induced by waterlogging along with [73]
inhibition of root growth and lateral expansion.
Rapid accumulation of JA during post-recovery of
submergence interacted with antioxidant pathways to enhance [134]
seedling tolerance through JA-activated MYC2.
Arabidopsis Overexpression of RAP2-4 isolated from Mentha arvensis
JA enhanced Arabidopsis tolerance to waterlogging, and its
[138]
expression was induced by JA via interaction with the JA
response element.
Overexpression of ZmPgb1.2 conferred plant waterlogging
Maize tolerance and induced genes related to JA biosynthesis in the [139]
meristematic region of roots.
Application of SA (1 mM) improved wheat tolerance to
waterlogging and its promotion of axile root formation and
SA Wheat [135]
aerenchyma was ethylene independent and dependent,
respectively.
Ref, Reference; ACE1, ACCELERATOR OF INTERNODE ELONGATION1; AFB, auxin signaling F-box; AUX,
auxin resistant; BR, brassinosteroid; DEC1, DECELERATOR OF INTERNODE ELONGATION1; EIL, ethylene
insensitive like; GA, gibberellic acid; JA, jasmonic acid; LAX, like AUX; Pgb, phytoglobin; PIN, plasma membrane
intrinsic protein; ROS, reactive oxygen species; SD1, SEMI-DWARF1; Sub1, Submergence1; TIR, transport
inhibitor resistant.

GA is associated with plant responses to flooding, which is evident in the biosynthesis

and signal transduction of GA in flooded plants [131]; additionally, exogenous GA relieves
the hazardous effects of flooding on plant growth [50]. The role of GAs in plant adaptation
to flooding has been well documented in rice and Rumex species, both of which are able to
utilize quiescent and escape strategies to survive hypoxic conditions based on interplay
with ethylene [9,15,23,110]. For the quiescent strategy, increased amounts of ethylene
induced by flooding exert a reduction of GA along with an enhancement of ABA signaling,
resulting in inhibition of plant growth in Rumex acetosa [9]. For the escape strategy, flooding
increased ethylene, leading to an increase in GA to promote stem elongation; consequently,
increased GA signals activate ethylene biosynthesis, resulting in positive feedback for
ethylene and GA [131]. It has been observed that activation of OsGA20ox2 facilitated the
biosynthesis of GA and activated internode elongation in deepwater rice at the six-leaf
stage [37]. Furthermore, SD1, which specifically binds OsEIL1a, was proven to increase
GA accumulation in deepwater rice [41]. The antagonistic regulation of the GA response
Int. J. Mol. Sci. 2022, 23, x FOR PEER REVIEW
6383 13
15of 21
of 23

degradation
by [109,131].
stem elongation Additionally,
in rice was proven thewith
effects
two ofgenes
BR, JA, and salicylic
named DEC1 andacidACE1,
(SA) on im‐
which
proving plant
inhibited tolerancestem
and boosted to flood are either
elongation, independent
respectively, or dependent
based on ethylene
on GA-mediated signal‐
cell division
independent of plant
ing to facilitate ethylene signaling
growth through[81]. These reports
activation illuminate
on formation the essential roots,
of adventitious roles of GA
shoot
in mediatingphotosynthetic
elongation, stem elongation in flooded
pigment, andplants; in particular,[132–135].
ROS scavenging the outcomes obtained
Herein, from
phytohor‐
deepwater rice should
mone signaling, shedGA,
including light on other
auxin, BR, crops.
JA, and SA, is described (Figure 3; Table 4).

Figure 3.
Figure 3. Interplays
Interplays of of GA,
GA,ABA,
ABA,auxin,
auxin,BR,
BR,ethylene,
ethylene,andandJAJAsignaling
signaling involved
involved in in plant
plant response
response to
to flooding. The scheme of GA, ABA, auxin, BR, ethylene, and JA signaling associated
flooding. The scheme of GA, ABA, auxin, BR, ethylene, and JA signaling associated with coleoptile with coleop‐
tile growth,
growth, adventitious
adventitious rooting,
rooting, andand stem
stem elongation
elongation wasconstructed
was constructedbased
basedononidentified
identified genes
genes inin
Arabidopsis, rice, and maize. Flooding suppresses expression of miR393, which inhibits OsTIR and
Arabidopsis, rice, and maize. Flooding suppresses expression of miR393, which inhibits OsTIR and
OsAFB, altering auxin mediated coleoptile growth during seed germination. Although auxin recep‐
OsAFB, altering auxin mediated coleoptile growth during seed germination. Although auxin receptors
tors and transports are affected differently by flooding, activation of PIN1/AUX1/AFB2 and sup‐
and transports
pression are affected differently
of LAX1/LAX3/PIN4/PIN7 by flooding,
improves activation
adventitious of PIN1/AUX1/AFB2
rooting and suppression
through auxin signaling. Mean‐
of LAX1/LAX3/PIN4/PIN7
while, improvesactivates
gain‐of‐function of RAP2.12 adventitious
AtPIN2rooting through
for auxin auxin signaling.
transport. Meanwhile,
The interaction between gain-
JA
of-function
and auxin is RAP2.12in
of evident activates AtPIN2 for auxin
the enhancement of JA transport.
biosynthesis Theininteraction between JA and
plants overexpressing auxin is
ZmPgb1.2.
Floodingininduces
evident expressionofofJASub1A
the enhancement and riceinbearing
biosynthesis Sub1A presented
plants overexpressing high amounts
ZmPgb1.2. of BR,
Flooding lead‐
induces
ing to a reduction
expression of Sub1A in GA
andcontent. Furthermore,
rice bearing flood‐induced
Sub1A presented ethyleneofactivates
high amounts BR, leading to a that
OsEIL1a binds
reduction
to GA
in SD1,content.
leading Furthermore,
to an increaseflood-induced
in GA, which ethylene
modulates stem elongation
activates through
OsEIL1a that bindsACE1 andleading
to SD1, DEC1.
ABA, abscisic acid; ACE1, ACCELERATOR OF INTERNODE ELONGATION1;
to an increase in GA, which modulates stem elongation through ACE1 and DEC1. ABA, abscisic AFB, auxin signaling
F‐box; AUX, auxin resistant; BR, brassinosteroid; DEC1, DECELERATOR OF INTERNODE ELONGA‐
acid; ACE1, ACCELERATOR OF INTERNODE ELONGATION1; AFB, auxin signaling F-box; AUX,
TION1; EIL1a, ethylene insensitive like1a; GA, gibberellic acid; JA, jasmonic acid; LAX, like AUX; Pgb,
auxin resistant; BR, brassinosteroid; DEC1, DECELERATOR OF INTERNODE ELONGATION1; EIL1a,
phytoglobin; PIN, plasma membrane intrinsic protein; RAP2.12, related to apetala 2.12; SD1, SEMI‐
ethylene
DWARF1; insensitive like1a; GA, gibberellic
Sub1A, Submergence1A; acid; JA,
TIR, transport jasmonic
inhibitor acid; LAX, like AUX; Pgb, phytoglobin;
resistant.
PIN, plasma membrane intrinsic protein; RAP2.12, related to apetala 2.12; SD1, SEMI-DWARF1; Sub1A,
Submergence1A;
Table 4. Effects TIR,of GA,transport
auxin, inhibitor resistant.
BR, JA, and SA in plants during flooding stress.

Hormones Plant Species Hormone

AuxinSignaling
has been implicated in promoting adventitious rooting by flooded plants. Ref.In
Flooding increased GA and GA content due to activation of OsGA20ox2,
wheat seedlings, upregulation of TDC, YUC1, and PIN9 involved in auxin biosynthesis
1 4 and GA in‐
[37]
duced
and internode
transport elongation during
contributed to high the six‐leaf
levels of stage
auxin,in deepwater
which wasrice.
required for nodal root in-
SD1 largely
duction increased
during hypoxia the [100].
contentInofArabidopsis,
GA4 via interaction with OsEILa
loss-of-function of and
aux1promoted
reducedinter‐
the number
[41]
node
of elongation
adventitious in deepwater
roots, whereas rice.
this symptom was rescued by exogenous auxin; addition-
Rice
GA promoted
ally, enhancementelongation of the internode based
of AUX1/AFB2/PIN1 and onsuppression
the reduction of
of JA content in deep‐
LAX1/LAX3/PIN4/PIN7
GA [42]
water rice.
improved adventitious rooting by pre-etiolated flooded seedlings [35]. In rice, auxin re-
DEC1 and
ceptors ACE1 and
OsTIR1 inhibited
OsAFB2,and accelerated
which are stem elongation,
negatively respectively,
regulated through participated
by miR393a, GA‐
[81]in
mediated cell
elongation anddivision
stomatal in the internode. in coleoptiles during seed germination and seedling
development
Rumex acetosa/R. establishment
GA signaling was activated
during by initial submergence
submergence of both interplays
[39]. Furthermore, of Rumex acetosa and R.
between palus‐and ethy-
auxin [9]
palustris tris, whereas sensitization to GA prior to its accumulation was induced in
lene have been identified that improve plant adaptation to flooding. For example, hypoxia R. palustris.
Int. J. Mol. Sci. 2022, 23, 6383 16 of 23

reduced the abundance of auxin efflux carrier PIN2; however, overexpression of RAR2.12
exacerbated this symptom, indicating the antagonistic control of auxin and ethylene [31].
In addition, ROS signaling was proven to mediate adventitious rooting inwaterlogged
cucumber through the regulation of auxin and ethylene signaling [72]. These results eluci-
date interactions of the auxin response, ethylene signaling, and ROS homeostasis in root
architecture and coleoptile growth in plants under hypoxic conditions.
An overall downregulation of genes related to auxin, BR, and GA biosynthesis was
observed in the roots of waterlogged grapevine, indicating a general inhibition of root
growth [73]. However, application of 24-epibrassinolide minimized the adverse impact of
waterlogging on soybean through the improvement of root/leaf anatomy, an increase in
chlorophyll accumulation, and enhancement of ROS scavenging [133]. BR biosynthesis was
regulated in Sub1A-dependent manner and BR limited GA levels during shoot elongation
in rice during submergence [132]. Additionally, JA and SA have also been verified as
regulators of plant adaptation to flood via modulation of antioxidant metabolism and
root architecture [134,135]. Gain-of-function of RAP2-4 enhanced Arabidopsis seedling
tolerance to waterlogging and its expression was induced by JA through interaction with
the JA response element [138]. Similarly, JA synthesis in the meristematic region of roots
was inducible by ZmPgb1.2, which positively regulated maize tolerance to anaerobic condi-
tions [139]. Regarding SA enhancement of wheat tolerance to waterlogging, it was revealed
that SA promoted formation of axile roots independently of ethylene, but its effect on
adventitious rooting was ethylene-dependent [135]. These findings suggest that BR, JA,
and SA appear to be positive players for plant flooding responses, though the transport and
signaling pathways need further investigation to address their function in plant adaptation
to flood.

6. Conclusions and Future Perspective

The elucidation summarized in this review suggests that phytohormones play major
roles during plant response to flood and post-recovery submergence, ranging from signal
transduction to cellular metabolism arrangements underlying seed germination, root archi-
tecture, stem elongation, petiole movement, and other processes (Figure 4). Furthermore,
exogenous phytohormones have been proved to mitigate the effects of flooding on plants
through the activation of flood tolerance capacity, suggesting that pre-treatment of phy-
tohormones can be used to evoke flood-tolerance strategies for agricultural applications.
Phytohormone signaling that mediates two contrasting responses to flooding has been
well-elucidated in rice and Remix species based on the identification of several genes, such
as Sub1A, SNORKEL1/2, OsEIL1a, SD1, DEC1, and ACE1, which direct the quiescence re-
sponse or rapid internode elongation to help plant survival during submergence. Although
fruitful achievements regarding hormone signaling in flooded rice could shed light on other
plants, few genes contributing to flood tolerance have been identified due to the shortage of
flood-tolerant materials and the complexity of tolerance characteristics, particularly for root
structure. Currently, our understanding of the phytohormonal response to flood is mainly
derived from ethylene, ABA, GA, and auxin, which could function alongside one another
or in conjunction with other compounds. However, signaling transduction induced by
BR, JA, and SA in flooded plants are still elusive because the receptors and transporters
involved with these phytohormones remain ambiguous. With continuous advancements,
multiple disciplines have boosted the development of omics, which have accelerated our
understanding of plant responses to flooding stress. Therefore, new tools, including high-
throughput interpretation of tolerant traits, single-cell based omics, and gene editing, will
dissect the genes related to phytohormone signaling in flooded plants and assist in solving
the complicated interplays among different phytohormones, facilitating the development
of flood-tolerant plants based on the adaptive responses mediated by phytohormones.
 ous advancements, multiple disciplines have boosted the development of omics, which
have accelerated our understanding of plant responses to flooding stress. Therefore, new
tools, including high‐throughput interpretation of tolerant traits, single‐cell based omics,
and gene editing, will dissect the genes related to phytohormone signaling in flooded
plants and assist in solving the complicated interplays among different phytohormones,
Int. J. Mol. Sci. 2022, 23, 6383 17 of 23
facilitating the development of flood‐tolerant plants based on the adaptive responses me‐
diated by phytohormones.

Figure 4.4. Summarizing

Figure Summarizing overview
overview ofof phytohormone-mediated
phytohormone‐mediated morphophysiological
morphophysiological alteration
alteration in
in
flooded plants. Phytohormone‐mediated
flooded Phytohormone-mediatedmorphological
morphological adaptation
adaptationin in
flooded plants,
flooded including
plants, col‐
including
eoptile growth,
coleoptile root
growth, architecture,
root stem
architecture, stemelongation, and
elongation, andleaf petiole
leaf movement,
petiole movement, is summarized.
is summarized. In
addition,
In addition,physiological adjustments
physiological adjustmentsinduced
inducedby by
phytohormones
phytohormones under
underflooding areare
flooding indicated, in‐
indicated,
cluding water
including waterabsorption, anaerobic
absorption, anaerobicrespiration, cellcell
respiration, wall loosening,
wall photosynthetic
loosening, pigment,
photosynthetic car‐
pigment,
bohydrate degradation, programmed cell death, and antioxidant metabolism. ABA, abscisic acid;
carbohydrate degradation, programmed cell death, and antioxidant metabolism. ABA, abscisic acid;
BR, brassinosteroid; CHO, carbohydrate; Eth, ethylene; GA, gibberellic acid; JA, jasmonic acid; SA,
BR, brassinosteroid; CHO, carbohydrate; Eth, ethylene; GA, gibberellic acid; JA, jasmonic acid; SA,
salicylic acid; PS, photosynthetic.
salicylic acid; PS, photosynthetic.
Author Contributions: Conceptualization, S.K.; writing—original draft preparation, X.W. and S.K.;
writing—review
Author and editing,
Contributions: X.W. and S.K.S.K.;
Conceptualization, All authors have read draft
writing—original and agreed to the published
preparation, ver‐
X.W. and S.K.;
sion of the manuscript.
writing—review and editing, X.W. and S.K. All authors have read and agreed to the published version
of the manuscript.
Funding: This research received no external funding.
Funding: This research received no external funding.
Institutional Review Board Statement: Not applicable.
Institutional Review Board Statement: Not applicable.
Informed Consent Statement: Not applicable.
Informed Consent Statement: Not applicable.
Data Availability Statement: Not applicable.
Data Availability Statement:
Acknowledgments: Not applicable.
X.W. is grateful to the 2115 Talent Development Program of China Agricultural
University.
Acknowledgments: X.W. is grateful to the 2115 Talent Development Program of China Agricultural
University.
Conflicts of Interest: The authors declare no conflict of interest.
Conflicts of Interest: The authors declare no conflict of interest.
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