Introduction
Most terrestrial
plants are capable of forming reciprocal symbiosis (arbuscular mycorrhizas,
AMs) with soil arbuscular mycorrhizal fungi (AMF), belonging to Glomeromycotina
(Plassard et al. 2019). Under a suitable soil environment, spores of AMF
germinate and form hyphopodia on the root surface of host plants. After passing
through the outer-cell layers, mycorrhizal fungal hyphae in the inner cortical
cells establish highly branched arbuscules (Keymer and Gutjahr 2018). In
addition, AMs develop external hyphae outside the root system, which is 10 to 40-fold
more extensive than the roots and whose length ranges from 10 to 22 m per plant
(Ferrol et al. 2019). The external hyphae also colonize neighbor plants
to establish common mycorrhizal networks between plants, which can deliver the signaling
of disease resistance (Zhang et al. 2019). In roots, plant sugars and
lipids are transferred to AMF for its growth, and in return, AMs aid in
nutrient acquisition of host plants. Such beneficial roles of AMs, positively
stimulate plant growth performance and partly mitigate damage caused by abiotic
and biotic stresses on host plants (Wu and Zou 2017).
Many studies have shown a beneficial effect of AMF on increasing
tolerance of abiotic stress in plants, associated with anatomical changes of
the plants, physiological changes in the antioxidant protective system, osmotic
adjustment, polyamine, fatty acid, and nutrient and water acquisition, and
molecular changes in aquaporin (AQP)
genes, the
Overview of AQPs
in plants
AQPs belong to the
major intrinsic proteins (MIPs) in many organisms for transporting certain
small molecules across biological membranes (Maurel et al. 2015). There
are a large number of homologues of AQPs in dicotyledons and monocotyledons, as
well as in C3 and C4 metabolic plants. These plant AQPs show abundant diversity
and high abundance. According to amino acid sequence homology and subcellular
localization, plant AQPs are classed into five categories: plasma intrinsic
proteins (PIPs), tonoplast intrinsic proteins (TIPs), NOD26-like intrinsic
proteins (NIPs), small intrinsic proteins (SIPs), and Glps-like intrinsic
proteins (GIPs) (Johansson et al. 2001). In Sphaerotheciella
sphaerocarpa, two new AQP types, hybrid intrinsic proteins (HIP) and
uncharacterized intrinsic (XIPs) proteins were identified (Bienert et al. 2011).
The PIPs are highly conserved and narrow in pores, and they are typical
high-moisture-selective channel proteins, including PIP1, PIP2, and PIP3 (Marty 1999). TIPs are located on the tonoplast, which contain five
subclasses viz., α, β, γ, δ, and ε (Johansson et
al. 2001). NIPs are located on the symbiotic membrane of soybean nodules
and bacteria, and are divided into three categories: NIP I, NIP II, and NIP III
(Mitani-Ueno et al. 2011). SIPs are the smallest family of plant AQPs, located
on the endoplasmic reticulum membrane, and divided into SIP1 and SIP2 (Ishikawa
et al. 2005). At present, AQP genes have been
found and cloned in various plants such as Arabidopsis thaliana (Quigley et al. 2001), Oryza sativa (Sakurai 2005), Zea mays (Chaumont 2001), Citrus sinensis (Martins et al. 2015) etc. The discovery of these AQPs provides important guidance in systematic
analysis of AQP diversity. These identified AQPs are the most abundant
transporters of H2O, as well as glycerol, urea, NH3, CO2,
silicon, antimony, arsenite, boron, hydrogen peroxide, etc. (Afzal et al. 2016).
Meanwhile, PIPs can transport glycerol, hydrogen peroxide, water, and urea.
TIPs function in the permeability of water. NIPs possess less activity of water
transport, but are responsible for permeability of organic molecules. For
example, NIP1 in Medicago truncatula is
functioned in the inner membrane of symbiotic cells (Uehlein et al. 2007), and NIP1;1 transports both
glycerol and silicon (Bárzana et al. 2014).
Overview of AQPs
in AMF and their potential roles
In addition to
plants, mycorrhizal fungi also have AQPs. In an ectomycorrhizal fungus Laccaria bicolor, six AQPs including one
orthodox aquaporin and five aquaglyceroporins were identified and showed water
transport capacity (Dietz et al. 2011). In 2009, Aroca et al.
(2009) first reported an AQP gene isolated from an AM fungus G. intraradices, named as GintAQP1.
GintAQP1 expression and host AQP expressions are a compensatory way. For example, under salt stress,
the GintAQP1 gene expression was not changed, while PIPs expression of P. vulgaris up-regulated. Both drought and cold did not regulate
expression of GintAQP1, whereas
two of four PIP genes in P. vulgaris down-regulated their
expression. After being heterologously expressed in Xenopus
laevis oocytes, GintAQP1 did not transport water. Therefore,
the location of GintAQP1 and its hypothetical transporter substrates
need to be further studied.
Li et al. (2013) also isolated two full-length putative AQP
genes in G. intraradices,
GintAQPF1 and GintAQPF2. GintAQPF1 is 1093 bp and located
in the plasma membrane of yeast. GintAQPF2 is located in both plasma and
intracellular membranes without any introns, supporting the roles in regulating
water flux across plasma membranes for water transfer (Xu et al. 2013).
Drought stress strongly induced the expression of GintAQPF1 and GintAQPF2
in maize. Moreover, the fungal AQPs were enriched in cortical cells having
arbuscules. This suggested potential water transport by fungal AQPs to host
plants, further illuminating the AMF role in drought tolerance of plants.
Kikuchi et al. (2016) also identified three putative AQP genes
from Rhizophagus clarus, viz.,
RcAQP1, RcAQP2, and RcAQP3, which are most similar to GintAQPF1, GintAQP1, and
GintAQP2 of R. irregularis, respectively. Additionally, the fungal
aquaglyceroporin RcAQP3 is most
highly expressed in intraradical hyphae to transport water across the plasma
membrane, as well as to accelerate transpiration and polyp translocation towards
the roots. Despite all this, the structure, function, and regulation of AQP in
AMF are elusive.
When analyzing expression of fungal AQP genes, host AQP gene
expressions are also considered (Ruiz-Lozano and Aroca 2017). For example, Li
and Chen (2012) analyzed expression of host PIPs
and GintAQP1 in maize roots
inoculated with G. intraradices exposed to soil water
deficit. They revealed the enhanced expression of eight ZmPIP genes, accompanied with the up-regulated expression of GintAQP1. Other studies also showed the
enhanced expression of mycorrhizal fungal AQPs
under the conditions of soil water deficit in this article, providing further
evidence to support water movement in mycorrhizal plants by fungal AQPs. However, more AQPs from AMF need to be
identified, and the functions of fungal AQPs remain to be examined.
Interestingly, based on transcriptomic data, Giovannetti et al. (2012)
found two up-regulated AQP genes, LjNIP1
and LjXIP1, in Gigaspora margarita-colonized roots of Lotus japonicus. Among
them, LjNIP1 was expressed
exclusively in inner membrane systems of arbuscule-enriched cells. This
indicated that LjNIP1 could be used
as an indicator of mycorrhizal status at arbuscule-developed process.
In short, fungal AQPs and their roles were identified to support the
involvement in water transport and nutrient acquisition of mycorrhizal
symbiosis, which is possibly important for mycorrhizal responses to abiotic
stress.
Collective physiological
roles of both aquaporins and arbuscular mycorrhizas
Water transport in
roots: There are three
types of water absorption in mycorrhizal plants: (i) the apoplast pathway in
which the water moves through the cell wall and the intercellular space without
involving the cytoplasm, (ii) the symplastic or transmembrane pathway in which
the water moves from one cell to another through the plasma membrane twice and
through the vacuolar membrane, and (iii) the symbiotic
pathway in which mycorrhizas provide a special way to absorb water by
mycorrhizal hyphae from soils to root cortical cells (Zhu et al. 2015). Early
studies indicated a significantly higher water transport speed of mycorrhizal
pine seedlings than that of the non-mycorrhizal control, providing evidence for
mycorrhiza-reduced water transport resistance (Tataranni et al. 2012).
Ruth et al. (2011) used a high-resolution online water content sensor to
quantitatively analyze mycorrhizal water contribution, accounting for 20% in whole
water absorption rate of plants. AMF possesses multi-nucleated, diaphragm-free
mycelium, which quickly transferred water with little resistance in the
mycelium. After reaching the top of the mycelium, water seeped into cells of
the host root, and shortened the water transport path in the root. As a result,
mycorrhizal hyphae provided a special water absorption channel. In addition,
mycorrhizal symbiosis affects root branching, root diameter, and root density
without change in the total root biomass, which provide greater water absorptive
capacity of mycorrhizal hosts subjected to adversity (Kabouw et al. 2012).
Many AQPs as efficient transport membrane
proteins are highly expressed in roots to transport water, while 70 to 90% of
the water transport through roots is derived from AQPs and water
transport via AQPs is mainly transmembrane transport (Kaldenhoff and Fischer 2006).
In roots of Hordeum vulgare, cortical
cells of lateral roots have the highest water conductivity, and the smallest
water conductivity is in the mature zone and transition zone of main roots, while
the cortical cells of the adventitious root transition zone have relatively higher
water conductivity (Knipfer et al. 2011), which is consistent with
expression of HvPIP2;2, HvPIP2;5, and HvTIP1;1. After being
treated by water channel protein inhibitors, the water flow decreased by 83 to
95%, indicating that high expression of these
AQPs in cortical cells is the main reason for maintaining high
water conductivity. A recent study also showed that AQPs contributed 79 and
85% root water conductivity in rice roots when water was sufficient or deficient,
respectively (Grondin et al. 2016). This suggested that AQPs are
important in root water transport under a stress environment.
Plant growth responses: AMF can promote
plant growth behavior in various abiotic stress conditions (Lü et al. 2018). Inoculation with AMF greatly improves root architecture
(root length, surface area and volume) of host plants, and the
mycorrhiza-improved root morphological changes are associated with both the AMF
species used and mycorrhiza-induced changes in carbohydrates in host plants (Wu et al. 2011). The increase of
shoot and root biomass in cucumber plants was 24 and 13% respectively after AMF
treatment (Wang et al. 2003), which was related with AMF-increased
nutrient acquisition. Higher gas exchange in both transpiration rate and
stomatal conductance was found in mycorrhizal citrus versus non-mycorrhizal
citrus after inoculation with G. fasciculatus during water stress and
stress recovery (Levy and Krikun 1980). As a result, mycorrhizal fungi
facilitated water transport more smoothly and rapidly, thus maintaining normal
plant growth under water deficit conditions.
AQP expressions
are closely related with cell proliferation. For example, the expression
pattern of TIP1;1 in A.
thaliana is associated with the cell elongation of roots, hypocotyls,
leaves, and flower stems, and TIP1;1 also
participates in the exchange of water and solutes (Ludevid et al. 1992).
In addition, overexpression of PIP1;2
from Arabidopsis significantly promoted plant growth in tobacco (Peng et
al. 2007). Expression of PIPs in Vitis berlanderi × V. rupestris was the highest
in the tip of roots and decreased in the root-hair zone of roots (Gambetta et
al. 2013). This suggested that
AQP expression might
promote the transport of mineral elements and water in roots, thereby further
stimulating cell proliferation and subsequent plant growth.
Phytohormone
regulation: As an important
chemical signal substance, endogenous hormones regulate plant growth and root
development in order to alleviate environmental stress (Fahad et al.
2015). AM symbiosis alters the levels of phytohormones such as cytokinin,
auxin, auxin-related substances, abscisic acid (ABA), and jasmonic acid
(Ludwig-Müller 2010). Cruz et al. (2000) observed that mycorrhizal
symbiosis increased the content of IAA, gibberellins, and CTK in host plants, while
it decreased ABA and ethylene concentrations under drought stress. On the other
hand, hyphae of AMF also produce ABA (Esch et
al. 1994). Hence, AM symbiosis regulates
phytohormone levels of host plants to respond to environmental stress.
Drought-induced ABA not only stimulates stomatal closure, but also
regulates the water channel function in plants (Peret et al.
2012). Exogenous ABA treatment had
a positive effect on root water conductivity and reduced the phosphorylation of
several PIP2 in Arabidopsis (Kline et al. 2010). IAA inhibits expressions of most PIP genes at transcription and translation levels through the auxin
response factor 7-dependent pathway (Yamada et al. 1995), and also reduces the water conductivity of root contical cells
(Hose et al. 2000). Salicylic acid regulates PIP
expression and root water conductivity through a mechanism mediated by reactive
oxygen species (Boursiac et al. 2008). Expression of RhPIP1;1
in leaves of Chinese rose was increased after being treated by exogenous GA3
application, while it was reduced by exogenous ABA (Yin et al. 2014). Hence, environment stress-induced hormonal
changes are associated with plant hydraulics, and thus mycorrhizas alter hydraulic
characteristics of plants through regulation of plant hormones.
Osmotic regulation:
Osmotic regulation refers to
the accumulation of solutes in plant cells to decrease osmotic potential and
maintain cell turgor pressure, and thus reduces stress damage and promotes
plant growth. Solutes involved in osmotic regulation are divided into two
categories: organic solutes, such as polyols, betaines, polyamines, proline,
free amino acids, sugars, and alcohols, and inorganic ions, including Na+,
K+, Mg2+, Ca2+, and H+ (Zeng et al. 2015). Previous studies showed that mycorrhizal
inoculation improved the ability of osmotic regulation in host plants in
response to a stress environment (Wu et al. 2013a; Yang et al. 2018; Zhang et al. 2018). In a study conducted by Zhao et al. (2017), AMF inoculation increased concentrations of soluble
sugar, soluble protein, and free proline in alfalfa under salt stress, which
resulted in the promotion of water and nutrients and the stabilization of
proteins and enzyme activities. Similarly, AQPs are not only involved in water absorption
in plants, but also in the regulation of osmosis between vacuoles and the
cytoplasm or between the cytoplasm and the apoplast (Yang et al. 2005). AQPs can prevent water loss under stress
environments. PIP1 is rich in the plasma membrane of mesophyll cells in Arabidopsis
in order to regulate water exchange (Beebo et al. 2009). In crux, AMF and AQPs are collectively involved
in the osmotic regulation of plants. AMF enhances stress resistance by
increasing solute contents, while AQPs strive for time to synthesize osmotic
solutes by increasing water permeability and preventing water loss.
Responses of AQPs
to mycorrhization under abiotic stress
Both AMF and AQPs can respond to stress environments,
but their mechanisms are not identical. The mechanisms of AMF-associated stress
tolerance are mostly at the physiological level: water absorption of extraradical
hyphae, enhancement of nutrient acquisition, superior root architecture, greater
osmotic regulation and antioxidant protective systems, and improvement of the soil
structure by mycorrhiza-released glomalin (Wu et al. 2013b; Zhang et al. 2018 a,b). Since most
mycorrhiza-induced changes are in the cytoplasmic or vacuolar membrane of cells
in roots, it is expected to find genes encoding membrane related proteins such
as AQPs (Sade et al. 2009). The accumulation pattern of AQPs in roots by mycorrhization
versus non-mycorrhization has different roles in physiological regulation (Fig.
1). Therefore, many studies focused on whether AQP genes
respond differently to abiotic stress under mycorrhization (Table 1).
Drought stress: Porcel et al. (2006) investigate the expression
patterns of AQP genes in AMF-colonized and non-AMF-colonized soybean and
lettuce roots exposed to drought stress. They found down-regulating expression
of PIP genes in AM plants in response to drought stress. However, Alguacil et
al. (2009) carried out a research, where Lactuca sativa seedlings
were inoculated with G. intraradices
or Pseudomonas mendocina and also subjected to two water regimes and two
atmospheric CO2 levels. They showed that mycorrhizal treatment increased
expression of the LsPIP2 gene under
two water regimes and two CO2 levels, while G. intraradices was more
effective than P. mendocina.
This indicated that AMF may up- or down-regulate AQP gene expression in response to drought stress. Marulanda et al. (2003) reported that G. intraradices inoculation
elevated water absorption via maintaining high levels of PIP gene expression, while G. mosseae seemed to protect plants against drought stress
through down-regulating expression of PIP
genes.
Table 1: Aquaporin responsive patterns of host plants under drought stress,
salt stress, and cold stress after inoculation with AMF
|
Abiotic stress |
Host plant |
Plant tissue |
Species of AMF |
Gene expression |
Reference |
|
Drought stress |
Glycine max |
Root |
Glomus mosseae |
GmPIP2↓ |
Porcel et al. 2006 |
|
Lactuca sativa |
Root |
G.
mosseae |
LsPIP2↓ |
Porcel et al. 2006 |
|
|
|
Root |
G.
intraradices |
LpPIP2↑ |
Alguacil et al. 2009 |
|
|
Populus × canadensis |
Leaf |
Rhizophagus irregularis |
PIP1;1↑; PIP1;2↑;
PIP1;3↑; PIP1;4↑; PIP1;5↑; PIP2;2↑; PIP2;3↓ |
Liu et al. 2016 |
|
|
Poncirus trifoliata |
Root |
Funneliformis mosseae |
PtTIP1;2↑; PtTIP1;3↑;
PtTIP4;1↑; P TIP2;1↓; PtTIP5;1↓; PtTIP1;1ns; PtTIP2;2ns |
He et al. 2019 |
|
|
Zea mays |
Root |
R.
irregularis |
Short-term drought ZmTIP1;2↑; ZmPIP1;4↑;
ZmTIP2;4↑; ZmNIP2;1↑; ZmTIP2;3↑; ZmPIP2;2↑;
ZmTIP1;1↑; ZmPIP1;2↑; ZmTIP1;6↑; ZmSIP2;1↑;
ZmNIP1;1ns; ZmTIP4;1ns; ZmTIP4;2ns; ZmPIP1;1ns; ZmPIP1;3ns; ZmNIP2;2ns. Sustained drought ZmPIP1;4↓; ZmPIP1;3↓;
ZmNIP2;2↓; ZmTIP1;2↓; ZmPIP2;2↓; Zm
TIP1;1↓; ZmNIP1;1↑; ZmTIP4;1↑; ZmTIP4;2↑; ZmPIP1;4ns;
ZmPIP2;4ns; ZmNIP2;1ns; ZmTIP2;3ns; ZmPIP1;2ns; ZmPIP1;6ns; ZmSIP2;1ns.
|
Bárzana et al. 2014 |
|
|
|
Root |
G.
intraradices |
Drought-sensitive cultivar ZmPIP1;1↓; ZmPIP1;3↓;
Zm PIP1;6↓;Zm PIP2;2↓; ZmPIP2;4↓; ZmTIP1;1↓;
ZmTIP2;3↓; ZmTIP4;1ns; Zm NIP2;1ns Drought-tolerant cultivar ZmPIP1;1↑;
ZmTIP4;1↑; ZmPIP2;4↑; ZmPIP1;3↓;
ZmTIP1;1ns; ZmTIP2;3ns; ZmNIP2;1ns; ZmPIP1;6ns; ZmPIP2;2ns; |
Quiroga et al. 2017 |
|
|
Salinity stress |
Lycopersicon esculentum |
Leaf and Root |
mixture of G. geosporum and G. intraradices |
LePIP1↓; LeTIP↓;
LePIP2ns |
Ouziad et al. 2006 |
|
|
Root |
G.
mosseae |
LePIP1↓; LePIP2↓;
LeTRAMP↓; LeTIP↓; LeAQP2↑ |
He et al. 2011 |
|
|
Phaseolus vulgaris |
Root |
G.
intraradices |
PvPIP1;2↓;
PvPIP1;1↑; PvPIP1;3↑; PvPIP2;1↑ |
Aroca et al. 2009 |
|
|
Poncirus trifoliata |
Root |
Paraglomus occultum |
PtTIP1;1↓; PtTIP1;3↓;
PtTIP2;2↓; PtTIP1;2↓; PtTIP2;1↓; Pt TIP4;1↑; Pt TIP5;1ns |
Ding et al. 2019 |
|
|
Cold stress |
Oryza sativa |
Root |
G.
intraradices |
OsPIP1;1↑; OsPIP1;3↑;
OsPIP2;1↑; OsPIP2;2↑; OsPIP1;2ns; OsPIP2;3ns |
Liu et al. 2014 |
|
Phaseolus vulgaris |
Root |
G.
intraradices |
PvPIP1;1↓; PvPIP1;2↓;
PvPIP1;3ns; PvPIP2;1ns |
Aroca et al. 2007 |
Note: the symbol “↑”,
“↓” and “ns” means the up and down-regulation, and no changes in this
aquaporin gene expression after mycorrhizal colonization
In addition to water transport, researchers also tried to a whole set
of AQP gene expression patterns and transporting
other molecules. Bárzana et al. (2014) revealed that AMF symbiosis
regulated expression of a number of AQP
genes in host plants, including members of different AQP subfamilies.
AMF-modulated AQP expression patterns
depended on the soil water status and the applied drought severity. In a short-term
soil water deficit, AM symbiosis up-regulated the expression of 10 AQP genes, while 6 AQP gene expressions were not affected. In contrast, when the soil
water deficit lasted, 6 AQP genes
were down-regulated, 7 AQP were
unaffected, and only 3 AQP genes were
up-regulated. However, the AQP response was down-regulated in non-AMF plants by
drought stress, regardless of the intensity of drought stress. Some AQP gene expressions can be modulated by
the soil water deficit degree under mycorrhization suggests that AMF-regulated
AQP expression might take part in water physiology and other potential physiological
activities. In addition, functional
characterization showed that
different subtypes of AQPS can transport water, glycerol, urea, NH3,
B, and H2O2. Quiroga et al. (2017) showed that more
host AQP genes were inhibited by AM
symbiosis in the drought-sensitive cultivar of maize under drought stress, as
compared with that in the drought-tolerant cultivar of maize. The
down-regulation of AQPs by mycorrhization
is a way to minimize water loss, thus, producing drought tolerance of plants (Min
et al. 2016). Recently, Quiroga et al. (2019) analyzed the
accumulation of phosphorylated PIP2s in maize inoculated with R.
irregularis subjected or not to water stress. They found that during water deficit
stress, phosphorylation levels of PIP2 were increased in mycorrhizal plants, indicating
that mycorrhizal symbiosis induces a relatively higher activity of PIP
Salinity stress: Expression or activity of AQPs is also correlated with salt
sensitivity of plants. Ouziad et al. (2006) compared tomato AQP expression under the condition of
AMF inoculation and NaCl treatment. Transcript levels of both a TIP and a PIP gene were reduced by salt stress, while this effect was
distinctly enhanced by AMF colonization. In another study by He et al. (2011), AMF
symbiosis under salt stress promoted plant growth and water uptake of tomato under
NaCl stress, followed with the decreased expression of AQP genes. Ding et al.
(2020) reported that except for PtTIP4;1 and PtTIP5;1,
transcription levels of the other five TIP
genes were down-regulated by the colonization of Paraglomus occultum
under NaCl stress. However, the biomass and water potential of AMF-colonized
plants were higher than those of non-AMF plants subjected to NaCl, indicating
that the water absorption of mycelium might be more important than AQPs. In
addition, in a two-chambered rootbox, expression of GintAQP1 in the root compartment of carrot roots was higher than in
the hyphal compartment, when the hyphal compartment was treated by additional NaCl
(Aroca et al. 2009). When the root compartment was applied by additional
NaCl, the hyphal compartment had higher expression of GintAQP1 than the root compartment in monoxenic culture. Such
results implied that fungal GintAQP1 and host AQPs might be regulated by certain signal substances between NaCl-treated
and untreated hyphae. Hence, mycorrhiza-regulated AQP expression patterns under salinity are a complex network
depending on AMF species, AQP types, and host plant species.
Cold stress: Low temperatures generally reduce root water uptake by
decreasing hydraulic conductivity of roots. At the same time, expression levels
of several AQP genes are considered
to modulate plant water response to cold stress. For example, two PIP genes in rice roots were up-regulated after subjected to low
temperature for several days (Kuwagata et al. 2012). In rice, low
temperature stress and mycorrhizal treatment collectively increased four PIP homologous gene expressions (Liu et
al. 2014). At the same time, GintAQPF1 and GintAQPF2 were over
expressed by low temperature treatment. This confirmed that both fungal AQP activities and host AQP gene expression could be
collectively induced to transport water under cold stress. The PIP gene expression was also studied by Aroca et al. (2007) in roots of Phaseolus
vulgaris under three stresses environments and mycorrhization. They observed that only under cold treatment conditions,
mycorrhizal inoculation down-regulated the expressions of PIP1;1 and PIP1;2 genes but did not alter the expressions of PIP1;3 and PIP2;1
genes. It suggests that mycorrhizas induced diverse expression patterns of PIP homologous gene in response to cold
stress. More studies still need to analyze the
AMF species, stress conditions and relationship between host AQPs and
mycorrhizal AQPs.
Contribution of mycorrhiza-regulated AQP
expression to host plants exposed to abiotic stress
%20786-794%20Rev_files/image002.jpg)
Fig. 1: The response pattern of AQPs by mycorrhization under abiotic stress. When
plants are subjected to abiotic stress, mycorrhization up-regulates host AQPs
expression to increase cell membrane permeability and improve transport of
water and other solutes. Mycorrhizal symbiosis also down-regulates host AQPs
expression to reduce both cell membrane permeability and the loss of water and
other solutes in plants. On the other hand, mycorrhizal fungal AQPs (GintAQP,
GintAQPF1, and GintAQPF2 from G.
intraradices, and RcAQP1, RcAQP2, and RcAQP3 from Rhizophagus clarus) respond to abiotic stress with a complementary
mechanism, relative to host AQP
expressions
%20786-794%20Rev_files/image004.png)
Fig. 2: A proposed synergistic mechanisms of both AMF and plant aquaporins to
describe water movement. Here, mycorrhizal extraradical hyphae absorb water
from growth substrates, and the water is further transferred in arbuscules of
cortical cells. Fungal aquaporins located in arbuscules and intra-radical
hyphae are involved in water movement across the membrane into cortical cells
containing arbuscules. On the other hand, host aquaporin genes are induced to improve
transport of water, resulting in the increasing of root hydraulic conduction;
host aquaporin genes are down-regulated to reduce the loss of water or cell
membrane permeability. The responses of both fungal and plant aquaporins
collectively finish water absorption of hosts under abiotic stress
Under abiotic stress, host AQP gene expressions are modulated by mycorrhization, suggesting
the change of water physiological activities in plants. The induction or inhibition of host AQPs
by AMF could reflect plant water strategy in any case. There are two opposite
mechanisms by which AMF regulates the expression of AQPs in dehydration stress responses. Host AQP expression
is induced by mycorrhization under dehydration stress, indicating the
improvement of water permeability of the membrane and the promotion of water
transport; the down-regulation of host AQP
expression by mycorrhization under dehydration stress means a decrease of membrane
permeability and consequently water retention by cells, thereby reducing water
loss (Fig. 1) (Ruiz-Lozano et al. 2008).
Additionally, mycorrhiza-regulated PIP
expression patterns were clearly correlated with enhanced root hydraulic
conductivity of maize plants after soil water deficit and water recovery (Fig.
2) (Ruiz-Lozano et al. 2009). Lee et al. (2010) found that
mycorrhizal effects on root PIP transcriptional
levels could stimulate the increase in cell-to-cell water transport in roots,
which was closely associated with root hydraulic conductivity. As a result,
mycorrhiza-affected host AQP
expression takes part in root hydraulic conductivity of drought-stressed
plants, which is an important mechanism (Fig. 2).
Fungal AQP expressional
patterns may be a compensatory way for host AQP
expression under stressed conditions (Aroca et al. 2009): fungal GintAQP1
expression was unchanged; host PIPs
were induced. And, host AQP
expressional patterns may be a compensatory way for water absorption of
extraradical hyphae of arbuscular mycorrhiza under stressed conditions (Zou et
al. 2019): water absorptive rate of extraradical mycorrhizal hyphae was
enhanced by drought stress; host AQP
expressions were inhibited or unchanged.
In the association of
soil–fungus–plant pathway of water transport, mycorrhizal fungal AQPs also contribute to
efficient water absorption in mycorrhizal plants subjected to abiotic stress (Fig. 2) (Xu et al. 2013), which is also
an important mechanism of stress tolerance. In the identified AQPs of AMF, GintAQP1 gene does not
transport water, whereas GintAQPF1 and GintAQPF2 gene is
involved in water transport (Aroca et al. 2009; Li et al. 2013). In addition, drought
stress induced the expressions of GintAQPF1 and GintAQPF2 in cortical cells containing arbuscules to
regulate water flux across plasma membranes (Li et al. 2013). RcAQP3
and LjNIP1 also expressed in
mycorrhizal hyphae or inner membrane systems of arbuscule-enriched cells to
take part in water transport across plasma membranes (Kikuchi et al. 2016).
In brief, fungal and host AQPs could be regulated by abiotic
stress for water absorption in mycorrhizal plants through root hydraulic
conductivity, as well as for the regulation of osmosis between cytoplasms or
between the cytoplasm and the apoplast (Yang et al. 2005). Fungal AQP genes take part in the water movement
across the membrane into cortical cells containing arbuscules (Fig. 2). Host AQP genes are induced to improve
transport of water, resulting in the increasing of root hydraulic conduction;
host AQP genes are down-regulated to
reduce the loss of water or cell membrane permeability (Fig. 2). The responses
of both fungal and plant AQPs synergistically finish water absorption of hosts
under abiotic stress.
Conclusion and outlook
AMF up- or down-regulates the plant AQP gene expression levels to increase
root hydraulic conductivity or reduce water loss under stress conditions (Fig. 1). Fungal and host
AQP genes collectively take part in water movement across the membrane (Fig. 2). AQP expression in some host
plants are unchanged by mycorrhization under one kind of stress conditions,
while they are induced under other stress conditions, indicating the complex behavior of AQP expression in response to mycorrhization under various stresses. More plant AQP isoforms should be studied to determine the regulation
networks. AQPs are a multifunctional protein family from MIPs, some of which
transport glycerol, urea, mineral nutrients, lactic acid, and hydrogen peroxide
in addition to water. Future work should pay more attention to the role of AQP
genes on solute transport under stress conditions. On the other hand, subcellular
locations of AQPs in host should be analyzed to clarify their mycorrhizal roles
in plant hydraulics, nutrient acquisition, and stressed responses. Currently, a
small number of AQPs from G. intraradices and R. clarus only have been identified,
but they are not enough to understand the AMF-enhanced tolerance in response to
abiotic stress by mycorrhization with regard to AQPs. Future work should be
done on other AMF species, and the location of these fungal AQPs in the
mycorrhizal hyphae and the symbiotic cell organisms is also a hot research
direction in the future.
Acknowledgements
This study was
supported by the Hubei Provincial Department of Education (T201604), the National
Key Research and Development Program of China (2018YFD1000300), and the University of Hradec Kralove (Faculty of Science,
VT2019-2021).
References
Afzal Z, TC Howton, YL Sun, MM
Shahid (2016). The roles of aquaporins in plant stress responses. J Dev Biol
4:9–30
Alguacil MDM, J Kohler, F Caravaca,
R Antonio (2009). Differential effects of Pseudomonas mendocina and Glomus
intraradices on lettuce plants physiological response and aquaporin PIP2 gene expression under elevated
atmospheric CO2 and drought. Microbiol Ecol 58:942–951
Aroca R, A Bago, M Sutka, JA Paz, C
Cano, G Amodeo, JM Ruiz-Lozano (2009). Expression analysis of the first
arbuscular mycorrhizal fungi aquaporin described reveals concerted gene expression
between salt-stressed and nonstressed mycelium. Mol Plant-Microbe Interact
22:1169–1178
Aroca R, R Porcel, JM Ruiz-Lozano (2007).
How does arbuscular mycorrhizal symbiosis regulate root hydraulic properties
and plasma membrane aquaporins in Phaseolus
vulgaris under drought, cold, or salinity stresses? New Phytol 173:808–816
Bárzana G, R Aroca, GP Bienert, F
Chaumont, JM Ruiz-Lozano (2014). New insights into the regulation of aquaporins
by the arbuscular mycorrhizal symbiosis in maize plants under drought stress
and possible implications for plant performance. Mol Plant Microbe Interact 27:349–363
Beebo A, D Thomas, C Der, L
Sanchez, N Leborgne-Castel, F Marty, B Schoefs, K Bouhidel (2009). Life with
and without attip1;1, an arabidopsis aquaporin preferentially localized in the
apposing tonoplasts of adjacent vacuoles. Plant Mol Biol 70:193–209
Bienert GP, MD Bienert, TP Jahn, M
Boutry, F Chaumont (2011). Solanaceae XIPs are plasma membrane aquaporins that
facilitate the transport of many uncharged substrates. Plant J 66:306–317
Boursiac
Y, S Prak, J Boudet, O Postaire, DT Luu, C Tournaire-Roux, V Santoni, C Maurel (2008). The response of
Arabidopsis root water transport to a challenging environment implicates
reactive oxygen species and phosphorylation-dependent internalization of
aquaporins. Plant Signal Behav 3:1096–1098
Calvo-Polanco M, S Molina, AM
Zamarreno, JM Garcia-Mina, R Aroca (2014). The symbiosis with the arbuscular
mycorrhizal fungus Rhizophagus
irregularis drives root water transport in flooded tomato plants. Plant
Cell Physiol 55:1017–1029
Chaumont F (2001). Aquaporins constitute a large and
highly divergent protein family in maize. Plant Physiol 125:1206–1215
Cruz AF,
T Ishii, K Kadoya (2000). Effects
of arbuscular mycorrhizal fungi on tree growth, leaf water potential and levels
of 1-aminocyclopropane-1-carboxylic acid and ethylene in the roots of papaya
under water-stress conditions. Mycorrhiza 10:121–123
Dietz S, J von
Bülow, E Beitz, U Nehls (2011). The aquaporin gene family of the ectomycorrhizal fungus
Laccaria bicolor: lessons for symbiotic functions. New Phytol 190:927–940
Ding YE, QF Fan, JD He, HH Wu, YN
Zou, QS Wu, K Kuča (2020). Effects of mycorrhizas on physiological
performance and root TIPs expression
in trifoliate orange under salt stress. Arch Agron
Soil Sci 66:182–192
Esch H,
B Hundeshagen, H Schneider-Poetsch, H Bothe (1994). Demonstration of abscisic acid in spores
and hyphae of the arbuscular-mycorrhizal fungus Glomus and in the N2-fixing cyanobacterium Anabaena variabilis. Plant Sci 99:9–16
Fahad S, S Hussain, A
Matloob, FA Khan, A Khaliq, S Saud, S Hassan, D Shan, MR Khan, AK Tareen, A
Khan, A Ullah, Nasrullah, JL Huang (2015). Phytohormones and plant responses to
salinity stress: A review. Plant Growth Regul 75:391–404
Ferrol N, C Azcon-Aguilar, J
Perez-Tienda (2019). Arbuscular mycorrhizas as key players in sustainable plant
phosphorus acquisition: An overview on the mechanisms involved. Plant Sci
280:441–447
Gambetta GA, J Fei,
TL Rost, T Knipfer, MA Matthews, KA Shackel, MA Walker, AJ Mcelrone (2013).
Water uptake along the length of grapevine fine roots: developmental anatomy,
tissue-specific aquaporin expression and pathways of water transport. Plant Physiol
163:1254–1265
Giovannetti M, R
Balestrini, V Volpe, M Guether, D Straub, A Costa, U Ludewig, P Bonfante (2012).
Two putative-aquaporin genes are differentially expressed during arbuscular
mycorrhizal symbiosis in Lotus japonicus.
BMC Plant Biol 12:186–199
Grondin A, R Mauleon, V Vadez, A
Henry (2016). Root aquaporins contribute to whole plant water fluxes under
drought stress in rice (Oryza sativa L.). Plant Cell Environ 39:347–365
He F, H Zhang, M Tang (2016).
Aquaporin gene expression and physiological responses of Robinia
pseudoacacia L. to the mycorrhizal fungus Rhizophagus irregularis
and drought stress. Mycorrhiza 26:311–323
He JD, T
Dong, HH Wu, YN Zou, QS Wu, K Kuca (2019).
Mycorrhizas induce diverse responses of root TIP aquaporin gene expression to drought stress in trifoliate
orange. Sci Hortic 243:64–69
He ZQ, CX He, Y Yan, ZB Zhang, HS
Wang, HX Li, HR Tang (2011).
Regulative effect of arbuscular mycorrhizal fungi on water absorption and expression
of aquaporin genes in tomato under salt stress. Acta Hortic Sin 38:273–280
Hose E, E Steudle, W Hartung (2000).
Abscisic acid and hydraulic conductivity of maize roots: a study using cell-
and root-pressure probes. Planta 211:874–882
Ishikawa F, S Suga, T Uemura, MH
Sato, M Maeshima (2005). Novel type aquaporin SIPs are mainly localized to the
ER membrane and show cell-specific expression in Arabidopsis thaliana. FEBS Lett 579:5814–5820
Johansson U, M Karlson, I
Johansson, S Gustavsson, S Sjovall, L Fraysse, AR Weig, P Kjellbom (2001). The
complete set of genes encoding major intrinsic proteins in Arabidopsis provides
a framework for a new nomenclature for major intrinsic proteins in plants. Plant
Physiol 126:1358–1369
Kabouw P, NV Dam, WH Van, A Biere (2012).
How genetic modification of roots affects rhizosphere processes and plant
performance. J Exp Bot 63:3475–3483
Kaldenhoff R, M Fischer (2006).
Aquaporins in plants. Acta Physiol Plantarum 187:169–176
Keymer A, C Gutjahr (2018).
Cross-kingdom lipid transfer in arbuscular mycorrhiza symbiosis and beyond. Curr
Opin Plant Biol 44:137–144
Kikuchi Y, N Hijikata, R Ohtomo, Y
Handa, M Kawaguchi, K Saito, C Masuta, T Ezawa (2016). Aquaporin-mediated
long-distance polyphosphate translocation directed towards the host in
arbuscular mycorrhizal symbiosis: application of virus-induced gene silencing. New
Phytol 211:1202–1208
Kline
KG, GA Barrett-Wilt, MR Sussman (2010). In planta changes in protein
phosphorylation induced by the plant hormone abscisic acid. P Natl A Sci 107:15986–15991
Knipfer T, M
Besse, JL Verdeil, W Fricke (2011). Aquaporin-facilitated water uptake in barly (Hordeum
vulgare L.) roots. J Exp Bot 62:4115–4126
Krajinski F, A
Biela, D Schubert, V Gianinazzi-Pearson, R Kaldenhoff, P Franken (2000). Arbuscular mycorrhiza development
regulates the mRNA abundance of MtAQP1
encoding a mercury-insensitive aquaporin of Medicago
truncatula. Planta 211:85–90
Kuwagata T, J Ishikawa-Sakurai, H
Hayashi, K Nagasuga, K Fukushi, A Ahamed, K Takasugi, M Katsuhara, M
Murai-Hatano (2012). Influence of low air humidity and low root temperature on
water uptake growth and aquaporin expression in rice plants. Plant Cell
Physiol 53:1418–1431
Levy Y, J Krikun (1980).
Effect of vesicular-arbuscular mycorrhiza on Citrus jambhiri water relations. New Phytol 85:25–31
Li T, BD Chen (2012). Arbuscular
mycorrhizal fungi improving drought tolerance of maize plants by up-regulation
of aquaporin gene expressions in roots and the fungi themselves. Chin J
Plant Ecol 36:973–981
Li T, YJ Hu, ZP Hao, H Li, YS Wang,
BD Chen (2013). First cloning and characterization of two functional aquaporin
genes from an arbuscular mycorrhizal fungus Glomus
intraradices. New Phytol 197:617–630
Liu T, Z Li, C Hui, M Tang, H Zhang
(2016). Effect of Rhizophagus irregularis on osmotic adjustment,
antioxidation and aquaporin PIP genes expression of Populus × canadensis
‘Neva’ under drought stress. Acta Physiol Plantarum 38:191–199
Liu Z, L Ma, X He, C Tian (2014).
Water strategy of mycorrhizal rice at low temperature through the regulation of
pip aquaporins with the involvement of trehalose. Appl Soil Ecol 84:185–191
Lü LH,
YN Zou, QS Wu (2018).
Relationship between arbuscular mycorrhizas and plant growth: improvement or
depression?. In: Root Biology, pp: 451–464. Giri B, R. Prasad, A Varma (eds.). Springer, Dordrecht, The Netherlands
Ludevid D, H Höfte, E
Himelblau, MJ Chrispeels (1992). The expression pattern of the tonoplast
intrinsic protein γ-TIP in Arabidopsis
thaliana is correlated with cell enlargement. Plant Physiol 100:1633–1639
Ludwig-Müller J (2010). Hormonal
responses in host plants triggered by arbuscular mycorrhizal fungi. In:
Arbuscular Mycorrhizas: Physiology and Function, pp: 169–190. Koltai H, Y
Kapulnik (eds.). Springer, Dordrecht, The Netherlands
Martins CPS, AM Pedrosa, DL Du, LP
Gonçalves, QB Yu, FG Gmitter, MGC Costa (2015). Genome-wide characterization
and expression analysis of major intrinsic proteins during abiotic and biotic
stresses in sweet orange (Citrus sinensis
L. Osb.). PLoS One 10:e0138786
Marty F (1999). Plant vacuoles. Plant
Cell 11:587–599
Marulanda A, R Azcón, JM Ruiz-Lozano (2003). Contribution
of six arbuscular mycorrhizal fungal isolates to water uptake by Lactuca
sativa plants under drought stress. Physiol Plantarum 119:526–533
Maurel C, Y Boursiac, DT Luu, V Santoni, Z
Shahzad, L Verdoucq (2015). Aquaporins in plants. Physiol Rev 95:1321–1358
Min HW, CX Chen, SW Wei, XL Shang,
MY Sun, R Xia, XG Liu, DY Hao, HB Chen, Q Xie (2016). Identification of drought
tolerant mechanisms in maize seedlings based on transcriptome analysis of
recombination inbred lines. Front Plant Sci 7:1080
Mitani-Ueno N, N Yamaji, FJ Zhao, JF
Ma (2011). The aromatic/arginine selectivity filter of NIP aquaporins
plays a critical role in substrate selectivity for silicon, boron, and arsenic.
J Exp Bot 62:4391–4398
Navarro-Ródenas A, G Bárzana, E
Nicolás, A Carra, A Schubert, A Morte (2013). Expression analysis of aquaporins
from desert truffle mycorrhizal symbiosis reveals a fine-tuned regulation under
drought. Mol Plant Microbe Interact 26:1068–1078
Ouziad F, P Wilde, E Schmelzer, U
Hildebrandt, H Bothe (2006). Analysis of expression of aquaporins and Na+/H+
transporters in tomato colonized by arbuscular mycorrhizal fungi and affected
by salt stress. Environ Exp Bot 57:177–186
Peng Y, W Lin, CR
Arora (2007). Overexpression of a panax ginseng tonoplast aquaporin alters salt
tolerance, drought tolerance and cold acclimation ability in transgenic Arabidopsis
plants. Planta 226:729–740
Peret B,
G Li, J Zhao, LR Band, U Voss, O Postaire, DT Luu, OD Ines, I Casimiro, M
Lucas, DM Wells, L Lazzerini, P Nacry, JR King, OE Jensen, AR Schaffner, C
Maurel, MJ Bennett (2012). Auxin
regulates aquaporin function to facilitate lateral root emergence. Natl.
Cell Biol 14:991–998
Plassard C, A Becquer, K Garcia (2019).
Phosphorus transport in mycorrhiza: how far are we? Trends Plant Sci 24:794–801
Porcel R, R Aroca, R Azcón, JM
Ruiz-Lozano (2006). PIP aquaporin gene expression in arbuscular mycorrhizal Glycine
max and Lactuca sativa
plants in relation to drought stress tolerance. Plant Mol Biol 60:389–404
Quigley F, JM Rosenberg, Y
Shachar-hill, JB Hans (2001). From genome to function: the Arabidopsis
aquaporins. Genome Biol 3:858–871
Quiroga G, G Erice, L Ding, F
Chaumont, R Aroca, JM Ruiz-Lozano (2019). The arbuscular mycorrhizal
symbiosis regulates aquaporins activity and improves root cell water
permeability in maize plants subjected to water stress. Plant Cell Environ 42:2274–2290
Quiroga G, G Erice, R Aroca, F
Chaumont, JM Ruiz-Lozano (2017). Enhanced drought stress tolerance by the
arbuscular mycorrhizal symbiosis in a drought-sensitive maize cultivar is
related to a broader and differential regulation of host plant aquaporins than
in a drought-tolerant cultivar. Front Plant Sci 8; Article 01056
Roussel H, S Bruns, V
Gianinazzi-Pearson, K Hahlbrock, P Franken (1997). Induction of a membrane
intrinsic protein-encoding mRNA in arbuscular mycorrhiza and
elicitor-stimulated cell suspension cultures of parsley. Plant Sci 126:203–210
Ruiz-Lozano JM, R Aroca (2017). Plant aquaporins and mycorrhizae: Their regulation and involvement in plant
physiology and performance. In: Plant Aquaporins: from Transport to Signaling,
pp: 333–353. Chaumont F, SD Tyerman (eds.). Springer, Dordrecht, The Netherlands
Ruiz-Lozano JM MM Alguacil, G Barzana, P Vernieri, R
Aroca (2009). Exogenous ABA accentuates the differences in root hydraulic
properties between mycorrhizal and nonmycorrhizal maize plants through
regulation of PIP aquaporins. Plant Mol Biol 70:565–579
Ruiz-Lozano JM, R Porcel, R Aroca (2008). Evaluation of
the possible participation of drought-induced genes in the enhanced tolerance
of arbuscular mycorrhizal plants to water deficit. In: Mycorrhiza, pp: 185–205. Varma A (eds.). Springer, Berlin, Heidelberg,
Germany
Ruth B, M
Khalvati, U Schmidhalter (2011). Quantification of mycorrhizal water uptake via
high-resolution on-line water content sensors. Plant Soil 342:459–468
Sade N, BJ Vinocur, A Diber, A
Shatil, G Ronen, H Nissan, R Wallach, H Karchi, M Moshelion (2009). Improving
plant stress tolerance and yield production: Is the tonoplast aquaporin
SlTIP2;2 a key to isohydric to anisohydric conversion? New Phytol 181:651–661
Safir GR, JS Boyer, JW Gerdemann (1971).
Mycorrhizal enhancement of water transport in soybean. Science 172:581–583
Sakurai J (2005). Identification of
33 rice aquaporin genes and analysis of their expression and function. Plant
Cell Physiol 46:1568–1577
Tataranni G, G Montanaro, B Dichio,
C Xiloyannis (2012). Effects of mycorrhizas on hydraulic conductivity in
micrografted myrobolan 29C rootstocks. Acta Hortic 966:235–240
Uehlein N, K
Fileschi, M Eckert, GP Bienert, A Bertl, R Kaldenhoff (2007). Arbuscular
mycorrhizal symbiosis and plant aquaporin expression. Phytochemistry 68:122–129
Wang CX, L Qin, G
Feng, XL Li (2003). Effects of three arbuscular mycorrhizal fungi on growth of
cucumber seedings. J Agron-Environ Sci 22:301–303
Wu QS, JD He, AK Srivastava, YN Zou, K Kuca
(2019). Mycorrhizas enhance drought tolerance of citrus by altering root fatty
acid compositions and their saturation levels. Tree Physiol 39:1149–1158
Wu QS, YN Zou, XH He, P Luo (2011).
Arbuscular mycorrhizal fungi can alter some root characters and physiological
status in trifoliate orange (Poncirus trifoliate
L. Raf.) seedlings. Plant Growth Regul 65:273–278
Wu QS, YN Zou (2017). Arbuscular
mycorrhizal fungi and tolerance of drought stress in plants. In: Arbuscular
Mycorrhizas and Stress Tolerance of Plants, pp: 25–42. Wu QS (eds.).
Springer Nature Pte Ltd, Singapora
Wu QS, YN Zou, XH He (2013a).
Mycorrhizal symbiosis enhances tolerance to NaCl stress through selective
absorption but not selective transport of K+ over Na+ in
trifoliate orange. Sci Hortic 160:366–374
Wu QS, AK Srivastava, YN Zou (2013b).
AMF-induced tolerance to drought stress in citrus: A review. Sci Hortic
164:77–87
Xu H, JEK Cooke, JJ Zwiazek (2013).
Phylogenetic analysis of fungal aquaporins provides insight into their possible
role in water transport of mycorrhizal associations. Botany 9:495–504
Yamada S,
M Katsuhara, WB Kelly, CB Michalowski, HJ Bohnert (1995). A family of
transcripts encoding water channel proteins: Tissue-specific expression in the
common ice plant. Plant Cell 7:1129–1142
Yang SS, L Shan, AG Guo, DQ Sun, YJ
Shao (2005). Aquaporins and drought resistance of the plant. Agric Res Arid
Areas 23:215–218
Yang X, A Rasheed, H Yan, C
Zhou, Q Shang (2018). Effects of nitrogen forms and osmotic stress on
root aerenchyma formation of japonica rice and its relationship with water
absorption. Intl J Agric Biol 20:2287–2292
Yin X, W Chen, L Wang, RY Yang, JQ
Xue, JP Gao (2014). Regulation of the rose RhPIP1;1
promoter activity by hormones and abiotic stresses. Acta Hortic Sin 41:107–117
Zeng YL, L Li, RR Yang, XY Yi, BH
Zhang (2015). Contribution and distribution of inorganic ions and organic
compounds to the osmotic adjustment in halostachys caspica response to salt
stress. Sci Rep 5:13639
Zhang F, JD He, QD Ni, QS Wu, YN Zou
(2018a). Enhancement of drought tolerance in trifoliate orange by mycorrhiza:
Changes in root sucrose and proline metabolisms. Not Bot Hortic Agrobo 46:270–276
Zhang F, YN Zou, QS Wu (2018b).
Quantitative estimation of water uptake by mycorrhizal extraradical hyphae in
citrus under drought stress. Sci Hortic 229:132–136
Zhang F, YN Zou, QS Wu, K Kuča (2020).
Arbuscular mycorrhizas modulate root polyamine metabolism to enhance drought
tolerance of trifoliate orange. Environ
Exp Bot 171:103962
Zhang YC, YN Zou, LP Liu, QS Wu (2019).
Common mycorrhizal networks activate salicylic acid defense responses of
trifoliate orange (Poncirus trifoliata).
J Integr Plant Biol
61:1099–1111
Zhao X, L Ye, XW Na, GC Li (2017).
Influence of arbuscular mycorrhizal fungus on the osmotic adjustment substance
and antioxidant system of Medicago sativa
under salt-alkaline stress. Jiangsu J Agric Sci 33:782–787
Zhu Y, JL Xiong, GC Lü, A Batool, ZB
Wang, PF Li, YC Xiong (2015). Effects of arbuscular mycorrhizal fungi and plant
symbiosis on plant water relation and its mechanism. Acta Ecol Sin 35:2419–2427
Zou YN,
HH Wu, B Giri, QS Wu, K Kuča (2019). Mycorrhizal symbiosis down-regulates
or does not change root aquaporin expression in trifoliate orange under drought
stress. Plant Physiol Biochem 144:292–299