Open access peer-reviewed chapter

TIP Aquaporins in Plants: Role in Abiotic Stress Tolerance

Written By

Marzena Małgorzata Kurowska

Submitted: May 27th, 2020 Reviewed: September 23rd, 2020 Published: October 22nd, 2020

DOI: 10.5772/intechopen.94165

From the Edited Volume

Abiotic Stress in Plants

Edited by Shah Fahad, Shah Saud, Yajun Chen, Chao Wu and Depeng Wang

Chapter metrics overview

406 Chapter Downloads

View Full Metrics

Abstract

Tonoplast Intrinsic Proteins (TIP) are one of five subfamilies of aquaporins in higher plants. Plants typically contain a large number of TIP genes, ranging from 6 to 35 compared to humans. The molecular weight of the TIP subfamily members ranges from 25 to 28 kDa. Despite their sequence diversity, all TIP monomers have the same structure, which consists of six transmembrane helices and five inter-helical loops that form an hourglass shape with a central pore. Four monomers form tetramers, which are functional units in the membrane. TIPs form channels in the tonoplast that basically function as regulators of the intracellular water flow, which implies that they have a role in regulating cell turgor. TIPs are responsible for precisely regulating the movement of not only water, but also some small neutral molecules such as glycerol, urea, ammonia, hydrogen peroxide and formamide. The expression of TIPs may be affected by different environmental stresses, including drought, salinity and cold. TIPs expression is also altered by phytohormones and the appropriate cis-regulatory motifs are identified in the promotor region of the genes encoding TIPs in different plant species. It was shown that manipulating TIP-encoding genes expression in plants could have the potential to improve abiotic stress tolerance.

Keywords

  • aquaporins
  • tonoplast intrinsic proteins
  • abiotic stress
  • drought
  • salinity
  • cold
  • phytohormones
  • gene expression analysis
  • cis-regulatory motifs
  • plants

1. Introduction

Aquaporins (aqua-pore, AQP), which are members of the major intrinsic proteins (MIPs) superfamily, facilitate the bidirectional flux of water and non-aqua substrates across the cell membranes [1, 2, 3, 4]. These transmembrane proteins form pores in the lipid bilayers of archaea, bacteria, fungi, plants, non-mammalian metazoans and mammals including humans. In plants, the first AQP Noduline-26 (GmNOD26) was identified in soybean (Glycina maxL.) [5], whereas their ability to conduct water in plants was demonstrated for the first time for an Arabidopsis tonoplast intrinsic protein homologue (AtTIP1; 1, gamma-TIP) viaits heterologous expression in Xenopusoocytes [6]. In higher plants, MIPs are divided into five evolutionarily distinct subfamilies in terms of the similarities of their amino acid sequence and intercellular localisation: plasma membrane intrinsic proteins (PIPs), tonoplast intrinsic proteins (TIPs), nodulin-26 like intrinsic proteins (NIPs), small basic intrinsic proteins (SIPs) and X intrinsic proteins / uncharacterised-intrinsic proteins (XIPs) [7]. In turn, the TIP subfamily can be further divided into different subgroups. In Arabidopsis (Arabidopsis thaliana), the TIP subfamily has been divided into five subgroups from TIP1 to TIP5. Each subgroup is then again divided into different isoforms. In Arabidopsis, the TIP subfamily consists of 11 isoforms. Some of these have synonymous name such as TIP1;1 (gamma-TIP, γ-TIP, RB7), TIP1;2 (gamma-TIP2, γ-TIP2), TIP2;1 (delta-TIP, δ-TIP), TIP3;1 (alpha-TIP, α-TIP) and TIP3;2 (beta-TIP, β-TIP) [8].

Water, whose transport is facilitated by aquaporins and, among them TIPs, is their most important substrate. TIPs are responsible for precisely regulating the movement of not only water, but also some small neutral molecules that have great physiological significance such as glycerol, urea, ammonia, hydrogen peroxide (H2O2) and formamide [7]. The transport of these substrates was predicted using a bioinformatic analysis and some of them have also been proven experimentally by using their in vitroexpression in yeast or in a Xenopusoocyte system in which the expression of gene of interest led to, for example, an increase water permeability (Table 1).

SpeciesTIP nameSubstrateReferences
Water (H2O)Hydrogen peroxide (H2O2)UreaAmmonia (NH3)Glycerol (GLY)
Arabidopsis (Arabidopsis thaliana)AtTIP1;1
AtTIP1;2
AtTIP2;1
AtTIP2;3
AtTIP4;1
AtTIP5;1
+
+
+
+
+
+
+
+
+
+
+
[6, 9, 10, 11, 12, 13]
Barley (Hordeum vulgareL.)HvTIP1;1
HvTIP1;2
HvTIP2;3
+
+
+
[14]
Bread wheat (Triticum aestivumL.)TaTIP2;1
TaTIP2;2
+
+
[15, 16, 17]
Maize (Zea maysL.)ZmTIP1;1
ZmTIP1;2
ZmTIP2;3
ZmTIP4;4
+
+
+
+
+
+
+
+
+
+
-
-
[18, 19, 20]
Rice (Oryza sativaL.)OsTIP1;2
OsTIP2;2
OsTIP3;2
OsTIP4;1
OsTIP5;1
+
+
+
+
+
+
+
[21]
Radish (Raphanus sativus)RsTIP1;1
RsTIP2;1
+
+
[22]
Sunflower (Helianthus annuusL.)TIP7
TIP20
+
+
[23]
Tobacco (Nicotiana tabacumL.)NtTIPa+++[24]

Table 1.

The transport of different substrates by TIPs, which was demonstrated viatheir in vitroexpression in yeast or oocytes.

+ transport of the substrate has been confirmed, − transport of the substrate has been excluded.

The central vacuole occupies most of the intracellular space of most mature plant cells [25]. The plant vacuole plays important roles not only in space filling, but also in osmotic adjustment, storage and digestion [26, 27]. TIPs form channels in the vacuolar membrane (tonoplast) that basically function as regulators of the intracellular water flow, which implies that they have a role in regulating cell turgor. It has been proposed that the presence of a specific TIP isoform may define the function of the vacuole and that specific TIP proteins could be used as markers for the different types of vacuoles that occur in different tissue types or in response to developmental and environmental stimuli [28, 29]. Vacuoles whose tonoplast contains TIP2;1 (delta-TIP, δ-TIP) are used by plant cells to store pigments and vegetative storage proteins (VSPs) [28]. Moreover, in vegetative tissues, the lytic or degradative vacuoles (LVs) are marked by the presence of TIP1;2 (gamma-TIP, γ-TIP) [26, 28, 30]. TIP1;2 may be expressed primarily at the time when the large central vacuoles are being formed during cell enlargement [30], while the protein storage vacuoles (PSVs) in mature seeds are marked by the presence of TIP3;1 (alpha-TIP, α-TIP) [26, 31, 32].

TIP proteins are most abundant in the tonoplast, but some isoforms have also been detected in the chloroplast, e.g. on the luminal site of the thylakoid, the chloroplast membranes or the envelope fraction using mass-spectrometry-based proteomics. Such a location was detected for TIP1;1, TIP1;2 and TIP2;1 in Arabidopsis [33, 34, 35].

Advertisement

2. Structure and diversity of TIPs

Although it has been suggested that AQPs and, among them, TIPs are multifunctional proteins, their structure is unique across all kingdoms of life. Despite their sequence diversity, all TIPs have a similar structure that consists of six transmembrane helices (TM1 to TM6) with five connecting inter-helical loops (LA to LE) and two half helices that contain one highly conserved Asn-Pro-Ala (NPA) motif each of which forms its functional pore (Figure 1). The hydrophobic NPA motif is located at the first intracellular (loop B) and the third extracellular loop (loop E) and the overlap in the middle of the lipid bilayer (‘hourglass’ model) and forms two hemipores that generate a narrow part of the channel [7, 36]. A second filter region is the aromatic/Arginine (ar/R) selectivity filter, which includes four amino acids (aa), which are located at the non-cytosolic end of the pore [37]. These two constriction regions are very important for the transport selectivity of the channel, which have been predicted based on structural knowledge combined with simulation studies [38, 39]. Both filters at the pore “mouth” constitute barriers to the passage of inorganic cations (such as Na+ and K+) and protons [39]. The NPA motif not only plays a role in regulating membrane transport but also in protein localisation [40]. The substrate selectivity of AQPs is controlled by the amino acid residues of the NPA and ar/R filters as well as another conserved region, which is known as the Froger’s residues, which consist of five conserved residues [41]. This region enables the aquaglyceroporins that transport glycerol from the AQPs that facilitate the transport of water to be distinguished [39].

Figure 1.

The structure of aquaporin as represented by the crystal structure of spinach SoPIP2;1 (PDB 1Z98). The view from different sides of the holoprotein, which consists of four monomers. (a) the side view, (b) the tetrameric assembly from the cytoplasmic side. Each monomer functions as a single channel pore.

All MIP sequences take on a typical hour-glass MIP helical fold with six transmembrane helices and two half-helices [42]. This fold has been maintained during evolution via its conservation around 40 positions within the transmembrane region [42]. The stability of the functionally important half-helix is modulated by a stabilising intra-helical salt-bridge interaction and/or two helix destabilising residues, glycine and proline, which was demonstrated by an analysis of the loop E region of 1468 MIP sequences and their structural models from six different groups of organisms [43]. In the cell membrane, MIPs are grouped as homotetramers that are located in the lipid bilayer (Figure 1). Each monomer functions independently as a single channel pore [44]. In plants, the only the crystal structure of the MIPs for two species is currently available in the Protein Data Bank (PDB: http://www.pdb.org), the spinach (Spinacia oleracea) aquaporin SoPIP2;1 was in its closed confirmation at a 2.1 Å resolution and its open confirmation at a 3.9 Å resolution [45] and the Arabidopsis aquaporins AtPIP2;4 at a 3.7 Å resolution [46] all of which were determined using X-ray diffraction, which showed their structural identity. However, the functions and regulation of the majority of the MIP channels have not yet been fully characterised [42].

A large number of MIPgenes and, among them TIPgenes, have been identified in the genomes of different plant species. In plants, the MIP family contains around 2008 members while the TIP subfamily contains 585 members from different plant species, which have been deposited in the MIPDB [47, 48]. The length of the TIP sequences ranges from 55 to 780 aa. Plants typically contain a large number of AQPsgenes and among them the TIPgenes, when are compared with for example humans, ranges from 6 to 35 in moso bamboo (Phyllostachys edulis) and oilseed rape (Brassica napusL.), respectively [49, 50] (Table 2). The molecular weights of the TIP subfamily members ranges from 25 to 28 kDa [47].

SpeciesGenome size/ploidy x/no. of chromosomes*AQPPIPTIPNIPSIPXIPReferences
Arabidopsis (Arabidopsis thaliana)~135 Mbp
2n = 2x = 10
3813111130[8]
Barley (Hordeum vulgareL.)~5.3 Gbp;
2n = 2x = 14
391811820[51]
Bread wheat (Triticum aestivumL.)~17 Gb
2n = 6x = 42, AABBDD, hexaploid
113
(65-A, 42-B, 36-D)
51292940[52]
Cucumber (Cucumis sativusL.)~350 Mbp
2n = 2x = 14
39198921[53]
Foxtail millet (Setaria italicaL.)~490 Mb
2n = 2x = 18
3912111330[54]
Maize
(Zea maysL.)
2.4 Gb
2n = 2x = 20
411218830[55]
Potato (Solanum tuberosumL.)~840 Mb
2n = 4x = 48
4115111038[56]
Rice Japonica (Oryza sativaL.)500 Mb
2n = 2x = 24
3311101020[57]
Sorghum (Sorghum bicolor)~730 Mb
2n = 2x = 20
3713111120[58]
Tomato
(Solanum lycopersicumL.)
~828 Mb
2n = 2x = 24
4714111246[59]

Table 2.

The number of AQP isoforms in the selected plant species.

Based on the Ensemble Plants Database.


The number of Tonoplast Intrinsic Proteins (TIP) has been marked in bold.

Advertisement

3. Study of the tissue- and developmental-dependent expression of TIPs

Aquaporins are postulated to be the main water transporter protein in plants. However their presence and expression may vary among plant species, tissues and time during development. In plants, AQPs are present in almost all organs, including the roots, leaves, stems, flowers, fruits, seeds, dry seeds [60], pollen [13, 61, 62, 63], anther and specific cells such as the guard cells [64, 65]. Moreover, some TIPsare expressed in specific tissues, e.g. AtTIP5;1was localised in the pollen mitochondria, which are probably involved in the remobilisation of N via the transport of mitochondrial urea to the cytoplasm [61] as well as in a time-specific manner, e.g. the RsTip1;1(gamma-VM23) gene expression was high not only in the hypocotyls but also in the developing tap roots and young growing leaves and the pattern of its expression was connected with cell elongation [22] (Table 3).

SpeciesTIP nameOrgan/tissue/processReferences
Arabidopsis
(Arabidopsis thaliana)
AtTIP1;3, AtTIP5;1
Pollen mitochondria
[61, 66, 67]
AtTIP3;2
Senescence
AtTIP3;1
Seed-specific
AtTIP1;1
Entire vegetative body
AtTIP2;1
Developing vascular tissue, primary shoot
Barley (Hordeum vulgareL.)HvTIP1;1, HvTIP2;3, HvTIP1;2, HvTIP3;1
Leaf
[14]
HvTIP1;1, HvTIP2;3, HvTIP1;2Root
Bread wheat (Triticum aestivumL.)TaTIP1;12
Root-specific
[52]
TaTIP2;22Root-specific
Eucalyptus (Eucalyptus grandisL.)EgTIP1;1, EgTIP2;1
Flower bud
[68]
EgTIP1;1, EgTIP1;4, EgTIP2;1, EgTIP2;2
Flower
EgTIP1;4
Root
EgTIP1;1, EgTIP1;2, EgTIP4;1
Stem
EgTIP1;3
Cambium
EgTIP1;2, EgTIP3;2
Leaf
EgTIP3;1, EgTIP3;2Fruit
Maize
(Zea maysL.)
ZmTIP2;3Root-specific[20]
Radish (Raphanus sativus)RsTip1;1 (gamma-VM23)
Hypocotyl of seedlings, developing tap roots and young growing leaves
[22]
RsTIP2;1 (delta-VM23)Not expressed in young roots or leaf mesophyll
Rice
(Oryza sativaL.)
OsTIP3;2
Mature seed, spikelet, callus
[21, 69]
OsTIP1;1Shoots, roots
Sunflower (Helianthus annuusL.)TIP7 (delta-TIP)
Guard cells
[23]
TIP27 (delta-TIP)Guard cells
Tobacco
(Nicotiana tabacumL.)
NtTIP1;1 (TobRB7)Root-specific[70]

Table 3.

The expression of the selected TIPgenes in different plant tissues.

Advertisement

4. Study of the expression of TIPsunder abiotic stress or phytohormone treatment, and their role in maintaining cell homeostasis under stress conditions

The gene expression is the process in which gene information is converted into a protein [7]. Analysing the gene expression profiles is a prerequisite for determining the physiological function of a gene [71]. The function of AQPs can generally be modified in two ways: by regulating the gene expression, which leads to changes in protein abundance or by changing its permeability – gating. However, it should be kept in mind that changes in the mRNA expression level often reflect the protein abundance, but that this is not necessarily strictly connected in any cell or tissue [37]. In term, AQP trafficking and activity could be affected by the post-translational modifications (PTMs), like deamination, phosphorylation, methylation, ubiquitination and acetylation [37]. Water homeostasis is fundamental for cell survival [72]. AQP facilitate the transport of water and play roles in response to abiotic stress conditions during which the cell homeostasis is disturbed. Different studies have suggested that a low abundance of the AQP proteins reduces the water permeability of membranes and that a high abundance of them increases it. Although it can be assumed that all AQPs are able to transport water, an experimental study was performed for only a few members of the TIP subfamily in different plant species (Table 1). The expression of TIPs may be affected by different environmental conditions, including drought, salinity and cold and this has been investigated in many plant species. Comparative transcriptome studies using RNA sequencing (RNA-seq), which is a next generation sequencing technology, could lead to the discovery of a differential expression of multiple aquaporin homologues in different tissues and/or in different conditions of growth, e.g. under abiotic stress. The transcriptome defines as a set of coding and non-coding RNA molecules that are present in a single cell or a population of cells [73]. Nowadays, RNA-seq technology is used more and more frequently [74, 75]. On the other hand, the reverse-transcription quantitative PCR (RT-qPCR) technique still serves as the method of choice to perform the expression analysis of specific genes in many researches.

Abiotic stresses, which have a significant impact on the plants, are involved in changes at the transcriptome, cellular and physiological levels. When the stress is prolonged, plant growth and productivity are severely diminished [76, 77]. The response of plants is very complicated and many mechanisms are initiated simultaneously to restore cellular homeostasis and promote survival [78]. Aquaporins are thought to be responsive to the stress signalling pathways and are also thought to be involved in the stress-coping mechanisms such as altering the tissue hydraulic conductivity [79, 80]. Drought and salinity are two major factors that significantly limit plant growth and productivity [81, 82]. The huge yield losses caused by drought stress ranging 45–92 (%) have been reported in major field crops like maize (Zea maysL.), wheat (Triticum aestivumL.), rice (Oryza sativaL.), chickpea (Cicer arietinumL.), soybean (Glycine maxL.), sunflower (Helianthus annuusL.) [83]. Cold is also often associated with climate change [84]. Drought, salinity and freezing stresses cause a changing water status in plant cells and all of these result in cellular dehydration [85]. In order to improve the tolerance of crop plants to unfavourable environmental conditions, a detailed understanding of their stress responses is required.

4.1 Drought, salinity and cold stress

Aquaporins are responsible for precisely regulating the movement of water and therefore may play a crucial role in the drought-stress response as well as in drought-stress tolerance [78]. A transcriptome analysis of the leaf and root tissues in plant species revealed significant changes in the expression of the TIPgenes in response to drought stress. Under drought stress, when water is limited, the down-regulation of the TIPgenes can lead to a decrease in the water permeability of the tonoplast in order to avoid water loss and to minimise the water flow through the cell membranes in order to prevent the further loss of leaf turgor. This expression pattern has been shown in many studies. In Nicotiana glauca, the NgMIP2and NgMIP3genes, which are homologous to TIP, were down-regulated in leaves under drought stress when the leaves were wilting, usually three to four days after water was withheld [86] and in Arabidopsis, the levels of AtTIP1;1, AtTIP1;2, AtTIP2;1and AtTIP2;2were more than four-fold down-regulated after 12 days of drought [87]. In contrast to these results, the expression level of AtTIP1;1and AtTIP2;1under drought treatment was up-regulated, but the time that the stress was applied was only 24 hours [88]. Moreover, in barley (Hordeum vulgareL.), the expression of five HvTIPaquaporins in leaves: HvTIP1;1, HvTIP1;2, HvTIP2;1, HvTIP2;2and HvTIP2;3was down-regulated after ten days of severe drought treatment [89]. In turn, in Festucaspecies, the transcript level of the TIP1;1aquaporin decreased in leaves after 11 days of a water deficit [90]. The possible functional role of coffee (Coffea arabicaL.) TIPs in in regulating the water balance has been explored by measuring the TIPgene expression in leaf and root tissues that had been subjected to drought [91]. In root tissue, the expression of three CsTIPgenes (CaTIP1;1, CsTIP2;1, CsTIP4;1) decreased as the severity of the drought stress increased. In the leaf, a similar expression profile of their expression was obtained only for of CaTIP1;1[91]. By contrast, the level of TIPexpression increased in response to drought in some plant species. In soybean (Glycine max), transcriptome analysis data revealed that under dehydration stress, the expression of GmTIP2;1, GmTIP1;7and GmTIP1;8was up-regulated. The authors suggested that these three genes are probably the major AQPs that are involved in the stress response [75].

Interestingly, the expression profile of TIPgenes can be compared for cultivars that have contrasting responses to drought stress under control and stress conditions. In two cultivars of strawberry (Fragariax ananassa) that have contrasting drought stress phenotypes, the gene expression of FaTIPsin the roots was analysed [79]. During severe drought stress, the FaTIPswere only up-regulated in the drought-tolerant cultivar. This was connected with a gradual stomatal closure in this cultivar, which was further associated with conservative water use [79]. In turn, in soybean (Glycine max), the difference in gene expression was investigated using RNA-seq and it was found that the expression level of seven TIPgenes (GmTIP2;1, 2;2, 2;3, 2;4, 2;5, 3;2and 5;1) in the leaves was lower in the slow-wilting soybean lines, but that it increased in the fast-wilting soybean lines after drought stress [74]. Slow wilting is an important physiological parameter that is used in stress tolerance studies of plants. A cultivar-specific TIPexpression under drought has also been observed in the common bean (Phaseolus vulgarisL.) [92]. In this study, the expression of PvTIP1;1and PvTIP4;1decreased under drought compared to the control conditions in two cultivars, which has different phenotypes in terms of their tolerance to drought and yield at harvest, which were determined by time that was required for the plants to wilt after withholding water. Interestingly, the gene expression of PvTIP4;1during drought was cultivar specific with greater down-regulation of these gene in the drought-tolerant cultivar [92]. The differences in the relative water content (RWC) and water potential of leaves between these cultivars indicate that there is greater prevention of water loss in the tolerant cultivar during drought, which may be associated with the rapid and adequate down-regulation of the AQPs[92]. However, it should be kept in mind that the adaptive mechanism for reducing the effects of water deficit stress in which the TIPor other AQPexpression is changed should be further analysed by a functional characterisation of these candidate genes or proteins [52].

The regulation of water transport has been postulated as being the most important and the best recognised function of all of the AQPs including TIPs under drought stress. A second important function could be their involvement in the movement of hydrogen peroxide (H2O2), which is one of the reactive oxygen species (ROS), which include the unstable, highly reactive molecules that are produced during abiotic stress, e.g. drought [83, 93]. This activity makes the AQPs important players in both the redox signalling network and in H2O2 detoxification [94]. TIPs can facilitate the movement of H2O2 across the membranes that have already been shown by their in vitroexpression in the yeast or oocyte (Table 1). In barley under drought stress, the expression of the HvTIP3;1gene increase 5000-fold compared to their expression under optimal water conditions [89].

Soil salination and a high salt accumulation affects the growth, development and metabolism and yield of plants [95]. A wide range of physiological and biochemical alterations in plants are induced by salinity, which causes a lower water potential in the soil solution, ionic disequilibrium and also a higher accumulation of reactive oxygen species (ROS) [96]. Salinity stress leads to changes in the expression profiles of the TIPgenes, which was shown in many plant species. In Arabidopsis (Arabidopsis thaliana), the plants were treated with 100 mm NaCl, which led to osmotic stress. Macroarray experiments with gene-specific tags were performed to investigate the expression of all of the AQPsincluding the TIPsubfamily in roots that had been under salt treatment for 24 hours [97]. The AtTIP1;1, AtTIP1;2, AtTIP2;2and AtTIP2;3genes were highly expressed in the roots and their expression was maximally reduced at 6 h of treatment and remained low until 24 h of treatment, except for AtTIP1;1. In turn, in Festuca arundinacea,the plants were exposed to salt stress by irrigating them with 250 mM NaCl solution over 21 days, which resulted in an increase in the abundance of the FaTIP1;1transcript in two contrasting salt tolerance genotypes compared to the control conditions. This increase was noticed earlier on day six of the NaCl treatment in the high-salt tolerant (HST) genotypes and later on day 11 in the low-salt tolerant (LST) genotype [90].

Similar to water and salt stresses, cold stress is an important abiotic stress factor that significantly limits plant growth and development [98]. In Festuca pratensis, cold acclimation was associated with a lower transcript level of the FpTIP1;1gene in the leaves in both the high and low frost-tolerant genotypes. The authors concluded that the down-regulation of these isoforms during the exposure to cold may be one of the cold-acclimation components that prevents frost-induced cellular dehydration [90]. A similar pattern of expression was observed in roots in rice (Oryza sativaL.) under cold treatment. A 4°C treatment caused a decrease in the transcript level of the OsTIP1;1and OsTIP2;2genes. The mRNA levels of these genes started to decrease after 48 hours and continued to decrease after 72 hours of a chilling treatment [57]. One more example of a change in the expression of the TIPmember genes comes from the cold treatment of cotton (Gossypium hirsutum). The GhTIP1;1transcripts mainly accumulated in the roots and hypocotyls under normal conditions, but were dramatically up-regulated in the cotyledons and down-regulated in the roots within a few hours after the cotton seedlings had been cold treated [99].

4.2 Phytohormone treatment

Phytohormones play vital roles in the ability of plants to acclimatise to varying environments, by mediating growth, development, and nutrient allocation [100]. Interestingly, it has been shown that the TIPsexpression is also altered by phytohormones, including abscisic acid (ABA), cytokinin (CK), gibberellins (GA), and jasmonates (JA). Abscisic acid (ABA) is a plant growth regulator that plays an essential role in the abiotic stress response mainly during water stress [101]. It regulates the movement of the stomatal guard cells [102]. Jasmonates act as stress hormones that play an important role in the plant response to biotic and abiotic stresses [103]. In general, JA inhibits plant growth and modulate many growth and developmental processes of plants including root, shoot and leaf growth, trichome and tuber formation, fruit ripening and leaf senescence [104]. The gibberellins stimulate the growth of most organs via cell elongation and also respond to abiotic stresses [105]. Cytokinins play a role in regulating plant growth, development and their acclimation to environmental stresses [106, 107].

Cytokinin has been reported to influence the expression of the aquaporin genes. The expression of PgTIP1from ginseng (Panax ginseng) was positively regulated by applying cytokinin in suspension-cultured hormone-autotrophic ginseng cells [108]. Methyl jasmonate treatment caused a decrease in the nitrogen content in barley leaves, which was associated with an increased expression of the four tonoplast aquaporin genes (HvTIP1;2, HvTIP2;2, HvTIP4;1and HvTIP4;2), which are predicted to transport the nitrogen compounds from the vacuole to the cytosol. The up-regulation of the nitrogen-transporting HvTIPsmay lead to a vacuolar unloading of ammonia and urea, which could both be remobilised when the nitrogen content in barley leaves decreases [109]. In barley, the changes in the expression of all of the investigated HvTIPsin response to MeJA treatment were associated with the presence of the cis-regulatory elements in their promotor regions, which are recognised by the jasmonate-related transcription factors [109]. Other types of elements that possibly participate in the response to phytohormones in the HvTIPpromotor regions such as abscisic acid (ABA), gibberellins (GA) and auxin were also identified [89]. In barley, the effect of ABA and GA on the expression of the HvTIP1;2, HvTIP2;1, HvTIP2;2, HvTIP2;3and HvTIP4;1genes after 24 hours of treatment was studied in both the shoots and roots using quantitative real-time RT-PCR [110]. Interestingly, the exogenous application of ABA increased the expression of HvTIP2;1and HvTIP4;1,while the GA-treatment led to an increase of HvTIP1;2and HvTIP4;1in the roots compared to the control conditions. However, in the shoots, the ABA treatment decreased the expression of HvTIP1;2, while the GA treatment led to the up-regulation of HvTIP4;1[110].

Advertisement

5. Genetic manipulation of the TIP-encoding genes

The tonoplast intrinsic proteins genes have been reported to be involved in the increasing the abiotic stress tolerance in several plant species using genetic modification technology (Table 4). It was shown that manipulations of the expression of the TIP-encoding genes in plants could have the potential to improve their abiotic stress tolerance (Table 4). In tomato (Solanum lycopersicumL.), overexpression of SlTIP2;2has been shown to substantially improve the water homeostasis under drought stress. Conversely, this overexpression also promoted more prodigal water use [112]. Another gene, TIP1;1, was artificially manipulated in a few studies viagenetic engineering (Table 4). It is not only believed to be play an important role during plant growth and development, but also to be beneficial for growth under stress when it is overexpressed. The overexpression of the PgTIP1;1gene from Panax ginsengin Arabidopsis led to a general acceleration of plant development, which included a faster growth, precocious flowering and a higher accumulation of biomass compared to the wild type (wt), or the accumulation of more Na+ under salt stress and also caused a superior performance under drought stress compared to wt [85, 108]. The authors concluded that PgTIP1;1 plays an important role in the growth and development of plant cells and suggested that regulating it in the water movement across the tonoplast has a great impact on plant vigour under favourable growth conditions and also in the responses of plants to drought, salt and cold stresses [85]. Therefore, TIP1;1might be a potential target in biotechnology and agriculture. It was interesting to determine whether silencing this gene would have the opposite effect on growth in control and stress condition. First, it was shown that the down-regulation of AtTIP1;1using RNA interference (RNAi) resulted in early senescence and plant death [118]. However, later research using transposon insertion did not confirm these results [119]. A single mutant (tip1;1–1) that had been generated using transposon insertion showed any significant effect on the metabolism or elemental composition of the plants. Additionally, a double mutant in the AtTIP1;1and AtTIP1;2genes (tip1;1–1 tip1;2–1) had a small increase in its anthocyanin content and a decrease in its catalase activity, but showed no changes in its water status. Moreover, the mutant was alive and thriving [119].

TIP name/speciesMethod/expression in speciesPhenotypeReferences
AQUA1 (TIP) Populus albaL.OX
Populus alba
Increased plant growth rate and water use efficiency under excess Zn conditions[111]
SlTIP2;2
Solanum lycopersicumL.
OX
Solanum lycopersicum
Increased drought tolerance due to the ability of plant to regulate its transpiration under drought stress conditions, improved CO2 uptake and a balanced nutrient supply[112]
SlTIP2;2
Solanum lycopersicumL.
OX
Arabidopsis thaliana
Enhances the tolerance to salt stress[113]
PgTIP1
Panax ginseng
OX
Glycine max
Higher tolerance to salinity[114]
PgTIP1
Panax ginseng
OX
Arabidopsis thaliana
Acceleration of plant development, with faster growth, precocious flowering and a higher accumulation of biomass, increased seed size and seed mass, greatly increased growth rate[85]
PgTIP1
Panax ginseng
OX
Arabidopsis thaliana
Accumulated more Na + under salt stress, and exhibited superior performance under drought stress[108]
CsTIP2;1
Citrus spp.
OX
Nicotiana tabacum
Increased plant growth and tolerance to drought and salinity[115]
JcTIP1;3
Jatropha curcas
OX
Arabidopsis thaliana
Increased tolerance to drought and salinity, improved germination under high salt and mannitol stress[116]
AtTIP5;1
Arabidopsis thaliana
OX
Arabidopsis thaliana
Increased tolerance to boron toxicity[117]
AtTIP1;1
Arabidopsis thaliana
Down-regulation /RNAi technologyEarly senescence and plant death[118]
AtTIP1;1 -mutant
AtTIP1;2 and AtTIP1;2 -double mutant
Arabidopsis thaliana
KO
Transposon insertion
Single mutant -no significant effect on the metabolism or elemental composition of the plants
Double mutant -minor increase in the anthocyanin content, and a decrease in catalase activity, no changes in the water status, mutant alive and thriving
[119]
AtTIP2;2
Arabidopsis thaliana
KO
T-DNA insertion
Less sensitive to abiotic stresses (mannitol, NaCl and PEG)[120]

Table 4.

Genetic manipulation of the TIPgenes in different plant species and its effect on the phenotype.

OX-overexpression, KO- knockout, RNAi-RNA interference, PEG- polyethylene glycol.

Advertisement

6. Conclusions

It is believed that aquaporins and, among them, the tonoplast intrinsic proteins may be important players in the plant water relations at the cell, tissue, organ and whole plant levels. TIP proteins could have a vast impact on the acquisition of knowledge about plant tolerance against abiotic stress and could serve as a target sequence for genetic modifications. A drawback in this approach is that in the genome of each plant species, many genes encode the same subgroup of isoforms. It is possible that some of these have a redundant function. Taken together, TIPs probably play complex and diversified roles in the response of plants to abiotic stresses depending on TIP isoforms and the type and degree of stress treatment.

Advertisement

Acknowledgments

This work was supported by the National Science Centre, Poland, SONATA project 2015/19/D/NZ1/03441.

Advertisement

Conflict of interest

The author declares no conflict of interest.

References

  1. 1. Maurel C, Chrispeels MJ. Aquaporins. A molecular entry into plant water relations. Plant Physiol. 2001;125(1):135-138. DOI: 10.1104/pp.125.1.135 PMID:11154316
  2. 2. Li C, Wang W. Molecular Biology of Aquaporins. Adv Exp Med Biol. 2017;969:1-34. DOI: 10.1007/978-94-024-1057-0
  3. 3. Sutka M, Amodeo G, Ozu M. Plant and animal aquaporins crosstalk: what can be revealed from distinct perspectives. Biophys Rev. 2017; 9(5):545-562. DOI: 10.1007/s12551-017-0313-3
  4. 4. Bezerra-Neto JP, de Araújo FC, Ferreira-Neto JRC, da Silva MD, Pandolfi V, Aburjaile FF, et al. Plant Aquaporins: Diversity, Evolution and Biotechnological Applications. Curr Protein Pept Sci. 2019; 20 (4):368-395. DOI: 10.2174/1389203720666181102095910
  5. 5. Fortin MG, Morrison NA, Verma DP. Nodulin-26, a peribacteroid membrane nodulin is expressed independently of the development of the peribacteroid compartment. Nucleic Acids Res. 1987;15(2):813-824. DOI: 10.1093/nar/15.2.813
  6. 6. Maurel C, Reizer J, Schroeder JI, Chrispeels MJ. The vacuolar membrane protein gamma-TIP creates water specific channels in Xenopus oocytes, EMBO J. 1993;12: 2241-2247
  7. 7. Kapilan R, Vaziri M, Zwiazek JJ. Regulation of aquaporins in plants under stress. Biol Res. 2018; 16; 51 (1):4. DOI: 10.1186/s40659-018-0152-0
  8. 8. Quigley F, Rosenberg JM, Shachar-Hill Y, Bohnert HJ. From genome to function: the Arabidopsis aquaporins. Genome Biol. 2002;3(1). DOI: 10.1186/gb-2001-3-1
  9. 9. Liu LH, Ludewig U, Gassert B, Frommer WB, von Wirén N. Urea transport by nitrogen-regulated tonoplast intrinsic proteins in Arabidopsis. Plant Physiol. 2003;133(3):1220-1228. DOI: 10.1104/pp.103.027409
  10. 10. Klebl F, Wolf M, Sauer N. A defect in the yeast plasma membrane urea transporter Dur3p is complemented by CpNIP1, a Nod26-like protein from zucchini (Cucurbita pepoL.), and by Arabidopsis thaliana delta-TIP or gamma-TIP. FEBS Lett. 2003;547(1-3):69-74. DOI: 10.1016/s0014-5793(03)00671-9
  11. 11. Loqué D, Ludewig U, Yuan L, von Wirén N. Tonoplast intrinsic proteins AtTIP2;1 and AtTIP2;3 facilitate NH3 transport into the vacuole. Plant Physiol. 2005;137(2):671-680. DOI: 10.1104/pp.104.051268
  12. 12. Bienert GP, Møller AL, Kristiansen KA, et al. Specific aquaporins facilitate the diffusion of hydrogen peroxide across membranes. J Biol Chem. 2007;282(2):1183-1192. DOI: 10.1074/jbc.M603761200
  13. 13. Soto G, Alleva K, Mazzella MA, Amodeo G, Muschietti JP. AtTIP1;3 and AtTIP5;1, the only highly expressed Arabidopsis pollen-specific aquaporins, transport water and urea. FEBS Lett. 2008;582(29):4077-4082. DOI: 10.1016/j.febslet.2008.11.002
  14. 14. Besse M, Knipfer T, Miller A, Verdeil JL, Jahn TP, Fricke W. Developmental pattern of aquaporin expression in barley (Hordeum vulgare L.) leaves. J Exp Bot. 2011; 62(12):4127-42. DOI: 10. 1093/jxb/err175
  15. 15. Jahn TP, Møller AL, Zeuthen T, et al. Aquaporin homologues in plants and mammals transport ammonia. FEBS Lett. 2004;574(1-3):31-36. DOI: 10.1016/j.febslet.2004.08.004
  16. 16. Holm LM, Jahn TP, Møller AL, et al. NH3 and NH4+ permeability in aquaporin-expressing Xenopus oocytes. Pflugers Arch. 2005;450(6):415-428. DOI: 10.1007/s00424-005-1399-1
  17. 17. Bertl A, Kaldenhoff R. Function of a separate NH3-pore in Aquaporin TIP2;2 from wheat. FEBS Lett. 2007;581(28):5413-5417. DOI: 10.1016/j.febslet.2007.10.034
  18. 18. Bárzana G, Aroca R, Bienert GP, Chaumont F, Ruiz-Lozano JM. 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. 2014;27(4):349-363. DOI: 10.1094/MPMI-09-13-0268-R
  19. 19. Gu R, Chen X, Zhou Y, Yuan L. Isolation and characterization of three maize aquaporin genes, ZmNIP2;1, ZmNIP2;4 and ZmTIP4;4 involved in urea transport. BMB Rep. 2012;45(2):96-101. DOI: 10.5483/BMBRep.2012.45.2.96
  20. 20. Lopez F, Bousser A, Sissoëff I, Hoarau J, Mahé A. Characterization in maize of ZmTIP2-3, a root-specific tonoplast intrinsic protein exhibiting aquaporin activity. J Exp Bot. 2004;55(396):539-541. DOI: 10.1093/jxb/052
  21. 21. Li GW, Peng YH, Yu X, et al. Transport functions and expression analysis of vacuolar membrane aquaporins in response to various stresses in rice. J Plant Physiol. 2008;165(18):1879-1888. DOI: 10.1016/j.jplph.2008.05.002
  22. 22. Higuchi T, Suga S, Tsuchiya T, et al. Molecular cloning, water channel activity and tissue specific expression of two isoforms of radish vacuolar aquaporin. Plant Cell Physiol. 1998;39(9):905-913. DOI: 10.1093/oxfordjournals.pcp.a029453
  23. 23. Sarda X, Tousch D, Ferrare K, et al. Two TIP-like genes encoding aquaporins are expressed in sunflower guard cells. Plant J. 1997;12(5):1103-1111. DOI: 10.1046/j.1365-313x.1997.12051103.x
  24. 24. Gerbeau P, Güçlü J, Ripoche P, Maurel C. Aquaporin Nt-TIPa can account for the high permeability of tobacco cell vacuolar membrane to small neutral solutes. Plant J. 1999;18(6):577-587. DOI: 10.1046/j.1365-313x.1999.00481.x
  25. 25. Marty F. Plant vacuoles. Plant Cell. 1999;11(4):587-600. DOI: 10.1105/tpc.11.4.587
  26. 26. Paris N, Stanley CM, Jones RL, Rogers JC. Plant cells contain two functionally distinct vacuolar compartments. Cell. 1996;85(4):563-572. DOI: 10.1016/s0092-8674(00)81256-8
  27. 27. Wink M. The plant vacuole: a multifunctional compartment. J. Exp. Bot. (supplement), 44, 231-246 (1993).
  28. 28. Jauh GY, Fischer AM, Grimes HD, Ryan CA Jr, Rogers JC. delta-Tonoplast intrinsic protein defines unique plant vacuole functions. Proc Natl Acad Sci U S A. 1998;95(22):12995-12999. DOI: 10.1073/pnas.95.22.12995
  29. 29. Jauh GY, Phillips TE, Rogers JC. Tonoplast intrinsic protein isoforms as markers for vacuolar functions. Plant Cell. 1999;11(10):1867-1882. DOI: 10.1105/tpc.11.10.1867
  30. 30. Ludevid D, Höfte H, Himelblau E, Chrispeels MJ. The Expression Pattern of the Tonoplast Intrinsic Protein gamma-TIP in Arabidopsis thaliana Is Correlated with Cell Enlargement. Plant Physiol. 1992;100(4):1633-1639. DOI: 10.1104/pp.100.4.1633
  31. 31. Johnson KD, Herman EM, Chrispeels MJ. An abundant, highly conserved tonoplast protein in seeds. Plant Physiol. 1989;91(3):1006-1013. DOI: 10.1104/pp.91.3.1006
  32. 32. Hoh B, Hinz G, Jeong BK, Robinson DG. Protein storage vacuoles form de novo during pea cotyledon development. J Cell Sci. 1995;108 ( Pt 1):299-310.
  33. 33. Zybailov, B.L.; Rutschow, H.; Friso, G.; Rudella, A.; Emanuelsson, O.; Sun, Q .; Van Wijk, K.J. Sorting Signals, N-Terminal Modifications and Abundance of the Chloroplast Proteome. PLoS ONE 2008; 3, e1994. DOI: 10.1371/journal.pone.0001994.
  34. 34. Ferro, M.; Brugière, S.; Salvi, D.; Seigneurin-Berny, D.; Court, M.; Moyet, L.; Ramus, C.; Miras, S.; Mellal, M.; Le Gall, S.; et al. AT_CHLORO, a comprehensive chloroplast proteome database with subplastidial localization and curated information on envelope proteins. Mol. Cell. Proteom. 2010; 9, 1063-84. DOI: 10.1074/mcp.M900325-MCP200.
  35. 35. Simm, S.; Papasotiriou, D.G.; Ibrahim, M.; Leisegang, M.S.; Müller, B.; Schorge, T.; Karas, M.; Mirus, O.; Sommer, M.S.; Schleiff, E. Defining the core proteome of the chloroplast envelope membranes Front. Plant Sci. 2013; 4, 11. DOI: 10.3389/fpls.2013.00011
  36. 36. Jung JS, Preston GM, Smith BL, Guggino WB, Agre P. Molecular structure of the water channel through aquaporin CHIP. The hourglass model. J Biol Chem. 1994;269(20):14648-14654.
  37. 37. Fox AR, Maistriaux LC, Chaumont F. Toward understanding of the high number of plant aquaporin isoforms and multiple regulation mechanisms. Plant Sci. 2017;264:179-187. DOI: 10.1016/j.plantsci.2017.07.021
  38. 38. Sui H, Han BG, Lee JK, Walian P, Jap BK. Structural basis of water-specific transport through the AQP1 water channel. Nature. 2001;414(6866):872-878. DOI: 10.1038/414872a
  39. 39. Wu B, Steinbronn C, Alsterfjord M, Zeuthen T, Beitz E. Concerted action of two cation filters in the aquaporin water channel. EMBO J. 2009;28(15):2188-2194. DOI: 10.1038/emboj.2009.182
  40. 40. Guan XG, Su WH, Yi F, et al. NPA motifs play a key role in plasma membrane targeting of aquaporin-4. IUBMB Life. 2010;62(3):222-226. DOI: 10.1002/iub.311
  41. 41. Froger A, Tallur B, Thomas D, Delamarche C. Prediction of functional residues in water channels and related proteins. Protein Sci. 1998;7(6):1458-1468. DOI: 10.1002/pro.5560070623
  42. 42. Verma RK, Gupta AB, SankararamakrishnanR. majorintrinsic protein superfamily: channels with unique structural features and diverse selectivity filters. Methods Enzymol. 2015a;557:485-520. DOI: 10.1016/bs.mie.2014.12.006
  43. 43. Verma RK, Prabh ND, Sankararamakrishnan R. Intra-helical salt-bridge and helix destabilizing residues within the same helical turn: Role of functionally important loop E half-helix in channel regulation of major intrinsic proteins. Biochim Biophys Acta. 2015b;1848(6):1436-1449. DOI: 10.1016/j.bbamem.2015.03.013
  44. 44. Gomes D, Agasse A, Thiébaud P, Delrot S, Gerós H, Chaumont F. Aquaporins are multifunctional water and solute transporters highly divergent in living organisms. Biochim Biophys Acta. 2009;1788(6):1213-1228. DOI: 10.1016/j.bbamem.2009.03.009
  45. 45. Törnroth-Horsefield S, Wang Y, Hedfalk K, et al. Structural mechanism of plant aquaporin gating. Nature. 2006;439(7077):688-694. DOI: 10.1038/nature04316
  46. 46. Wang H, Schoebel S, Schmitz F, Dong H, Hedfalk K. Characterization of aquaporin-driven hydrogen peroxide transport. Biochim Biophys Acta Biomembr. 2020;1862(2):183065. DOI: 10.1016/j.bbamem.2019.183065
  47. 47. Data base for Major Intrinsic Proteins,http://mipdb.genouest.org/e107_plugins/mipdb_project/project.php, Accessed: 2020-07-23
  48. 48. El Karkouri K, Gueuné H, Delamarche C. MIPDB: a relational database dedicated to MIP family proteins. Biol Cell. 2005;97(7):535-543. doi:10.1042/BC20040123
  49. 49. Sun H, Li L, Lou Y, Zhao H, Gao Z. Genome-wide identification and characterization of aquaporin gene family in moso bamboo (Phyllostachys edulis). Mol Biol Rep. 2016;43(5):437-450. DOI: 10.1007/s11033-016-3973-3
  50. 50. Yuan D, Li W, Hua Y, King GJ, Xu F, Shi L. Genome-Wide Identification and Characterization of the Aquaporin Gene Family and Transcriptional Responses to Boron Deficiency inBrassica napus. Front Plant Sci. 2017;8:1336. DOI: 10.3389/fpls.2017.01336
  51. 51. Hove RM, Ziemann M, Bhave M. Identification and Expression Analysis of the Barley (Hordeum vulgare L.) Aquaporin Gene Family. PLoS One. 2015;10(6):e0128025. DOI: 10.1371/journal.pone.0128025
  52. 52. Madrid-Espinoza J, Brunel-Saldias N, Guerra FP, Gutiérrez A, Del Pozo A. Genome-Wide Identification and Transcriptional Regulation of Aquaporin Genes in Bread Wheat (Triticum aestivum L.) under Water Stress. Genes (Basel). 2018;9(10):497. DOI: 0.3390/genes9100497
  53. 53. Zhu YX, Yang L, Liu N, et al. Genome-wide identification, structure characterization, and expression pattern profiling of aquaporin gene family in cucumber. BMC Plant Biol. 2019;19(1):345. DOI: 10.1186/s12870-019-1953-1
  54. 54. Singh RK, Shweta S, Muthamilarasan M, Rani R, Prasad M. Study on aquaporins of Setaria italica suggests the involvement of SiPIP3;1 and SiSIP1;1 in abiotic stress response. Funct Integr Genomics. 2019;19(4):587-596. DOI: 10.1007/s10142-018-00653-0
  55. 55. Bari A, Farooq M, Hussain A, Tahir ul Qama Mr, Waseem Abbas M, Mustafa G, Karim A, Ahmed I, Hussain T. Genome-Wide Bioinformatics Analysis of Aquaporin Gene Family in Maize (Zea mays L.). Journal of Phylogenetics & Evolutionary Biology 2018;6:2. DOI: 0.4172/2329-9002.1000197
  56. 56. Venkatesh J, Yu JW, Park SW. Genome-wide analysis and expression profiling of the Solanum tuberosum aquaporins. Plant Physiol Biochem. 2013;73:392-404. DOI: 10.1016/j.plaphy.2013.10.025
  57. 57. Sakurai J, Ishikawa F, Yamaguchi T, Uemura M, Maeshima M. Identification of 33 rice aquaporin genes and analysis of their expression and function. Plant Cell Physiol. 2005;46(9):1568-1577. DOI: 10.1093/pcp/pci172
  58. 58. Azad AK, Ahmed J, Alum MA, et al. Genome-Wide Characterization of Major Intrinsic Proteins in Four Grass Plants and Their Non-Aqua Transport Selectivity Profiles with Comparative Perspective. PLoS One. 2016;11(6):e0157735. DOI: 10.1371/journal.pone.0157735
  59. 59. Reuscher S, Akiyama M, Mori C, Aoki K, Shibata D, Shiratake K. Genome-wide identification and expression analysis of aquaporins in tomato. PLoS One. 2013;8(11):e79052. DOI: 10.1371/journal.pone.0079052
  60. 60. Vander Willigen C, Postaire O, Tournaire-Roux C, Boursiac Y, Maurel C. Expression and inhibition of aquaporins in germinating Arabidopsis seeds. Plant Cell Physiol. 2006;47(9):1241-1250. DOI: 10.1093/pcp/pcj094
  61. 61. Soto G, Fox R, Ayub N, Alleva K, Guaimas F, Erijman EJ, Mazzella A, Amodeo G, Muschietti J. TIP5;1 is an aquaporin specifically targeted to pollen mitochondria and is probably involved in nitrogen remobilization in Arabidopsis thaliana. Plant J. 2010; 64, 1038-1047 DOI: 10.1111/j.1365-313X.2010.04395
  62. 62. Pérez Di Giorgio JA, Barberini ML, Amodeo G, Muschietti JP. Pollen aquaporins: What are they there for? Plant Signal Behav. 2016;11(9):e1217375. DOI: 10.1080/15592324.2016.1217375
  63. 63. Sato R, Maeshima M. The ER-localized aquaporin SIP2;1 is involved in pollen germination and pollen tube elongation in Arabidopsis thaliana. Plant Mol Biol. 2019;100(3):335-349. DOI: 10.1007/s11103-019-00865-3
  64. 64. Rodrigues O, Reshetnyak G, Grondin A, et al. Aquaporins facilitate hydrogen peroxide entry into guard cells to mediate ABA- and pathogen-triggered stomatal closure. Proc Natl Acad Sci U S A. 2017;114(34):9200-9205. DOI: 10.1073/pnas.1704754114
  65. 65. Ding L, Chaumont F. Are Aquaporins Expressed in Stomatal Complexes Promising Targets to Enhance Stomatal Dynamics?. Front Plant Sci. 2020;11:458. DOI: 10.3389/fpls.2020.00458
  66. 66. Höfte H, Hubbard L, Reizer J, Ludevid D, Herman EM, Chrispeels MJ. Vegetative and Seed-Specific Forms of Tonoplast Intrinsic Protein in the Vacuolar Membrane of Arabidopsis thaliana. Plant Physiol. 1992;99(2):561- DOI: 10.1104/pp.99.2.561
  67. 67. Daniels MJ, Chaumont F, Mirkov TE, Chrispeels MJ. Characterization of a new vacuolar membrane aquaporin sensitive to mercury at a unique site. Plant Cell. 1996;8(4):587-599. DOI: 10.1105/tpc.8.4.587
  68. 68. Rodrigues MI, Takeda AA, Bravo JP, Maia IG. The Eucalyptus Tonoplast Intrinsic Protein (TIP) Gene Subfamily: Genomic Organization, Structural Features, and Expression Profiles. Front Plant Sci. 2016;7:1810. DOI: 10.3389/fpls.2016.01810570. doi:10.1104/pp.99.2.561
  69. 69. Liu Q , Umeda M, Uchimiya H. Isolation and expression analysis of two rice genes encoding the major intrinsic protein. Plant Mol Biol. 1994;26(6):2003-2007. DOI: 10.1007/BF00019511
  70. 70. Yamamoto YT, Taylor CG, Acedo GN, Cheng CL, Conkling MA. Characterization of cis-acting sequences regulating root-specific gene expression in tobacco. Plant Cell. 1991;3(4):371-382. DOI: 10.1105/tpc.3.4.371
  71. 71. Singh RK, Deshmukh R, Muthamilarasan M, Rani R, Prasad M. Versatile roles of aquaporin in physiological processes and stress tolerance in plants. Plant Physiol Biochem. 2020;149:178-189. DOI: 10.1016/j.plaphy.2020.02.009
  72. 72. Nesverova V, Törnroth-Horsefield S. Phosphorylation-Dependent Regulation of Mammalian Aquaporins. Cells. 2019;8(2):82. DOI: 10.3390/cells8020082
  73. 73. Yang, I.; Kim, S. Analysis of whole transcriptome sequencing data: Workflow and software. Genom. Inform.2015, 13, 119-125. DOI: 10.5808/GI.2015.13.4.119
  74. 74. Song L, Nguyen N, Deshmukh RK, et al. Soybean TIP Gene Family Analysis and Characterization of GmTIP1;5 and GmTIP2;5 Water Transport Activity. Front Plant Sci. 2016;7:1564. DOI: 10.3389/fpls.2016.01564
  75. 75. Zhang DY, Kumar M, Xu L, et al. Genome-wide identification of Major Intrinsic Proteins inGlycine sojaand characterization of GmTIP2;1 function under salt and water stress Sci Rep. 2017;7(1):4106. DOI: 10.1038/s41598-017-04253-z
  76. 76. Atkinson NJ, Urwin PE. The interaction of plant biotic and abiotic stresses: from genes to the field. J. Exp. Bot. 2014;63, 3523-43. DOI: 10.1093/jxb/ers100
  77. 77. Osakabe Y, Osakabe K, Shinozaki K, Tran LS. Response of plants to water stress. Front. Plant Sci. 2014; DOI: 10.3389/fpls.2014.00086
  78. 78. Golldack D, Li C, Mohan H, Probst N. Tolerance to drought and salt stress in plants, unraveling the signaling networks. Front. Plant Sci. 2014; DOI: 10.3389/fpls.2014.00151.
  79. 79. Merlaen B, De Keyser E, Ding L, Leroux O, Chaumont F, Van Labeke MC. Physiological responses and aquaporin expression upon drought and osmotic stress in a conservative vs prodigal Fragaria x ananassa cultivar. Plant Physiol Biochem. 2019;145:95-106. DOI: 10.1016/j.plaphy.2019.10.030
  80. 80. Qiao Y, Ren J, Yin L, Liu Y, Deng X, Liu P, Wang S. Exogenous melatonin alleviates PEG-induced short-term water deficiency in maize by increasing hydraulic conductance. BMC Plant Biol. 2020;14,20(1):218. DOI: 10.1186/s12870-020-02432-1
  81. 81. Cominelli E, Conti L, Tonelli C, Galbiati M. Challenges and perspectives to improve crop drought and salinity tolerance. N Biotechnol. 2013;30(4):355-361. DOI: 10.1016/j.nbt.2012.11.001
  82. 82. Singh B, Kukreja S, Goutam U. Milestones achieved in response to drought stress through reverse genetic approaches. F1000Res. 2018;7:1311. DOI: 10.12688/f1000research.15606.1
  83. 83. Fahad S, Bajwa AA, Nazir U, Anjum SA, Farooq A, Zohaib A, Sadia S, NasimW, Adkins S, Saud S, Ihsan MZ, Alharby H,Wu C,Wang D, Huang J. Crop production under drought and heat stress: Plant responses and Management Options. Front Plant Sci. 2017; 8:1147. DOI: 10.3389/fpls.2017.01147
  84. 84. Dolferus R. To grow or not to grow: a stressful decision for plants. Plant Sci. 2014;229:247-261. DOI: 10.1016/j.plantsci.2014.10.002
  85. 85. Peng Y, Lin W, Cai W, Arora R. Overexpression of a Panax ginseng tonoplast aquaporin alters salt tolerance, drought tolerance and cold acclimation ability in transgenic Arabidopsis plants. Planta. 2007;226(3):729-740. DOI: 10.1007/s00425-007-0520-4
  86. 86. Smart LB, Moskal WA, Cameron KD, Bennett AB. MIP genes are down-regulated under drought stress inNicotiana glauca. Plant Cell Physiol. 2001; 42(7):686-93. DOI: 10.1093/pcp/pce085
  87. 87. Alexandersson E, Fraysse L, Sjo¨ vall-Larsen S, Gustavsson S, Fellert M, Karlsson M, et al. Whole gene family expression and drought stress regulation of aquaporins. Plant Mol Biol. 2005; 59(3):469-84. DOI: 10.1007/s11103-005-0352-1
  88. 88. Feng ZJ, Xu SC, Liu N, Zhang GW, Hu QZ, Xu ZS, et al. Identification of the AQP members involved in abiotic stress responses from Arabidopsis. Gene. 2018; 10;646:64-73. DOI: 10.1016/j.gene.2017.12.048
  89. 89. Kurowska MM, Wiecha K, Gajek K, Szarejko I. Drought stress and re-watering affect the abundance of TIP aquaporin transcripts in barley. PLoS One. 2019;14(12):e0226423. DOI: 10.1371/journal.pone.0226423
  90. 90. Pawłowicz I, Rapacz M, Perlikowski D, Gondek K, Kosmala A. Abiotic stresses influence the transcript abundance of PIP and TIP aquaporins in Festuca species. J Appl Genet. 2017; 58(4):421-435. DOI: 10.1007/s13353-017-0403-8
  91. 91. Miniussi M, Del Terra L, Savi T, Pallavicini A, Nardini A. Aquaporins inCoffea arabicaL.: Identification, expression, and impacts on plant water relations and hydraulics. Plant Physiol Biochem. 2015;95:92-102. DOI: 10.1016/j.plaphy.2015.07.024
  92. 92. Zupin M, Sedlar A, Kidrič M, Meglič V. Drought-induced expression of aquaporin genes in leaves of two common bean cultivars differing in tolerance to drought stress. J Plant Res. 2017;130(4):735-745. DOI: 10.1007/s10265-017-0920-x
  93. 93. Choudhury, F.K.; Rivero, R.M.; Blumwald, E.; Mittler, R. Reactive oxygen species, abiotic stress and stress combination. Plant J. 2017, 90, 856-867. DOI: 10.1111/tpj.13299
  94. 94. Bienert GP, Chaumont F. Aquaporin-facilitated transmembrane diffusion of hydrogen peroxide. Biochim Biophys Acta. 2014; 1840(5):1596-604. DOI: 10.1016/j.bbagen.2013.09.017 PMID:24060746
  95. 95. Nabati J., Kafi M., Nezami A., Moghaddam P.R., Ali M., Mehrjerdi M.Z. Effect of salinity on biomass production and activities of some key enzymatic antioxidants in Kochia (Kochia scoparia) Pak. J. Bot. 2011;43:539-548.
  96. 96. Kamran M, Parveen A, Ahmar S, et al. An Overview of Hazardous Impacts of Soil Salinity in Crops, Tolerance Mechanisms, and Amelioration through Selenium Supplementation. Int J Mol Sci. 2019;21(1):148. DOI: 10.3390/ijms21010148
  97. 97. Boursiac Y, Chen S, Luu DT, Sorieul M, van den Dries N, Maurel C. Early effects of salinity on water transport in Arabidopsis roots. Molecular and cellular features of aquaporin expression. Plant Physiol. 2005;139(2):790-805. DOI: 10.1104/pp.105.065029
  98. 98. Afzal Z, Howton TC, Sun Y, Mukhtar MS. The Roles of Aquaporins in Plant Stress Responses. J Dev Biol. 2016;4(1):9. DOI: 10.3390/jdb4010009
  99. 99. Li DD, Tai FJ, Zhang ZT, et al. A cotton gene encodes a tonoplast aquaporin that is involved in cell tolerance to cold stress. Gene. 2009;438(1-2):26-32. DOI: 10.1016/j.gene.2009.02.023
  100. 100. Fahad S, Hussain S, Matloob A, Khan FA, Khaliq A, Saud S, Hassan S, Shan D, Khan F, Ullah N, Faiq M, Khan MR, Tareen AK, Khan A, Ullah A, Ullah N, Huang J. Phytohormones and plant responses to salinity stress: A review. Plant Growth Regul. 2014; 75(2):391-404. DOI: 10.1007/s10725-014-0013-y
  101. 101. Yoshida T, Christmann A, Yamaguchi-Shinozaki K, Grill E, Fernie AR. Revisiting the Basal Role of ABA - Roles Outside of Stress. Trends Plant Sci. 2019;24(7):625-635. DOI: 10.1016/j.tplants.2019.04.008
  102. 102. Cai S, Chen G, Wang Y, et al. Evolutionary Conservation of ABA Signaling for Stomatal Closure. Plant Physiol. 2017;174(2):732-747. DOI: 10.1104/pp.16.01848
  103. 103. Jang G, Yoon Y, Choi YD. Crosstalk with Jasmonic Acid Integrates Multiple Responses in Plant Development. Int J Mol Sci. 2020;21(1):305. DOI: 10.3390/ijms21010305
  104. 104. Yang J, Duan G, Li C, et al. The Crosstalks Between Jasmonic Acid and Other Plant Hormone Signaling Highlight the Involvement of Jasmonic Acid as a Core Component in Plant Response to Biotic and Abiotic Stresses. Front Plant Sci. 2019;10:1349. DOI: 10.3389/fpls.2019.01349
  105. 105. Colebrook EH, Thomas SG, Phillips AL, Hedden P. The role of gibberellin signalling in plant responses to abiotic stress. J Exp Biol. 2014;217:67-75. DOI: 10.1242/jeb.089938.
  106. 106. Lubovská Z, Dobrá J, Storchová H, Wilhelmová N, Vanková R. Cytokinin oxidase/dehydrogenase overexpression modifies antioxidant defense against heat, drought and their combination in Nicotiana tabacum plants. J Plant Physiol. 2014;171(17):1625-1633. DOI: 10.1016/j.jplph.2014.06.021
  107. 107. Ullah A, Manghwar H, Shaban M, et al. Phytohormones enhanced drought tolerance in plants: a coping strategy. Environ Sci Pollut Res Int. 2018;25(33):33103-33118. DOI: 10.1007/s11356-018-3364-5
  108. 108. Lin W, Peng Y, Li G, et al. Isolation and functional characterization of PgTIP1, a hormone-autotrophic cells-specific tonoplast aquaporin in ginseng. J Exp Bot. 2007;58(5):947-956. DOI: 10.1093/jxb/erl255
  109. 109. Kurowska MM, Daszkowska-Golec A, Gajecka M, Kościelniak P, Bierza W, Szarejko I. Methyl Jasmonate Affects Photosynthesis Efficiency, Expression of HvTIP Genes and Nitrogen Homeostasis in Barley. Int J Mol Sci. 2020;21(12):4335. DOI: 10.3390/ijms21124335
  110. 110. Ligaba A, Katsuhara M, Shibasaka M, Djira G. Abiotic stresses modulate expression of major intrinsic proteins in barley (Hordeum vulgare). C R Biol. 2011; 334(2):127-139. DOI: 10.1016/j.crvi.2010.11.005 PMID: 21333943
  111. 111. Ariani A, Francini A, Andreucci A, Sebastiani L. Over-expression of AQUA1 in Populus alba Villafranca clone increases relative growth rate and water use efficiency, under Zn excess condition. Plant Cell Rep. 2016;35(2):289-301. DOI: 10.1007/s00299-015-1883-9
  112. 112. Sade N, Vinocur BJ, Diber A, et al. Improving plant stress tolerance and yield production: is the tonoplast aquaporin SlTIP2;2 a key to isohydric to anisohydric conversion?. New Phytol. 2009;181(3):651-661. DOI: 10.1111/j.1469-8137.2008.02689.x
  113. 113. Xin S, Yu G, Sun L, Qiang X, Xu N, Cheng X. Expression of tomato SlTIP2;2 enhances the tolerance to salt stress in the transgenic Arabidopsis and interacts with target proteins. J Plant Res. 2014;127(6):695-708. DOI: 10.1007/s10265-014-0658-7
  114. 114. An, J.; Hu, Z.; Che, B.; Chen, H.; Yu, B.; Cai, W. Heterologous expression of Panax ginseng PgTIP1 confers enhanced salt tolerance of soybean cotyledon hairy roots, composite, and whole plants. Front. Plant Sci., 2017, 8, 1232. DOI: 10.3389/fpls.2017.01232
  115. 115. Martins, C.P.S.; Neves, D.M.; Cidade, L.C.; Mendes, A.F.S.; Silva,D.C.; Almeida, A.A. F.; Coelho-Filho, M.A.; Gesteira, A.S.; Soares-Filho, W.S.; Costa, M.G.C. Expression of the citrus CsTIP2;1 gene improves tobacco plant growth, antioxidant capacity and physiological adaptation under stress conditions. Planta, 2017, 245(5), 951-963. DOI: 10.1007/s00425-017-2653-4
  116. 116. Khan, K.; Agarwal, P.; Shanware, A.; Sane, V.A. Heterologous expression of two jatropha aquaporins imparts drought and salt tolerance and improves seed viability in transgenic Arabidopsis thaliana. PLoS One, 2015, 10(6), e0128866. DOI: 10.1371/journal.pone.0128866
  117. 117. Pang, Y.; Li, L.; Ren, F.; Lu, P.; Wei, P.; Cai, J.; Xin, L.; Zhang, J.; Chen, J.; Wang, X. Overexpression of the tonoplast aquaporin At-TIP5;1 conferred tolerance to boron toxicity in Arabidopsis. J. Genet. Genomics., 2010, 37(6), 389-397. DOI: 10.1016/S1673-8527(09)60057-6
  118. 118. Ma S, Quist TM, Ulanov A, Joly R, Bohnert HJ. Loss of TIP1;1 aquaporin in Arabidopsis leads to cell and plant death. Plant J. 2004;40(6):845-859. DOI: 10.1111/j.1365-313X.2004.02265.x
  119. 119. Schüssler MD, Alexandersson E, Bienert GP, et al. The effects of the loss of TIP1;1 and TIP1;2 aquaporins in Arabidopsis thaliana. Plant J. 2008;56(5):756-767. DOI: 10.1111/j.1365-313X.2008.03632.x
  120. 120. Feng, Z.J.; Xu, S.C.; Liu, N.; Zhang, G.W.; Hu, Q .Z.; Xu, Z.S.; Gong, Y.M. Identification of the AQP members involved in abiotic stress responses from Arabidopsis. Gene, 2018, 646, 64-73 DOI: 10.1016/j.gene.2017.12.048

Written By

Marzena Małgorzata Kurowska

Submitted: May 27th, 2020 Reviewed: September 23rd, 2020 Published: October 22nd, 2020