New challenges in plant aquaporin biotechnology

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ARTICLE IN PRESS Model

SL 8904 1–7

Plant Science xxx (2013) xxx– xxx

Contents lists available at ScienceDirect

Plant Science

jo ur nal home p age: www.elsev ier .com/ locate /p lantsc i

eview

ew challenges in plant aquaporin biotechnology

aria del Carmen Martinez-Ballesta ∗, Micaela Carvajalepartment of Plant Nutrition, Centro de Edafología y Biología Aplicada del Segura – CSIC, Campus de Espinardo, 30100 Murcia, Spain

a r t i c l e i n f o

rticle history:eceived 24 July 2013eceived in revised form 4 December 2013ccepted 5 December 2013vailable online xxx

a b s t r a c t

Recent advances concerning genetic manipulation provide new perspectives regarding the improvementof the physiological responses in herbaceous and woody plants to abiotic stresses. The beneficial or neg-ative effects of these manipulations on plant physiology are discussed, underlining the role of aquaporinisoforms as representative markers of water uptake and whole plant water status. Increasing water useefficiency and the promotion of plant water retention seem to be critical goals in the improvement of

eywords:quaporinarbon nanotubestress resistanceater use efficiency

plant tolerance to abiotic stress. However, newly uncovered mechanisms, such as aquaporin functionsand regulation, may be essential for the beneficial effects seen in plants overexpressing aquaporin genes.Under distinct stress conditions, differences in the phenotype of transgenic plants where aquaporinswere manipulated need to be analyzed. In the development of nano-technologies for agricultural prac-tices, multiple-walled carbon nanotubes promoted plant germination and cell growth. Their effects onaquaporins need further investigation.

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© 2013 Published by Elsevier Ireland Ltd.

ontents

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 002. Plant responses to aquaporin suppression . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 003. Plant responses to aquaporin overexpression. Cases of successful improvement of plant tolerance to abiotic stress and causes of failure . . . . . . 00

3.1. PIP manipulation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 003.2. TIP manipulation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00

4. Innovative approaches affecting plant aquaporins . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 005. Concluding remarks . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00

Conflict of interest . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00Acknowledgments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00

. Introduction

The importance of water movement in living organisms hased to studies of water transport through biological membranes,

matter of ongoing investigations. Aquaporins, proteins belongingo MIP (Membrane Intrinsic Proteins) family facilitate the bidirec-ional transport of water through biological membranes. However,ther molecules such as glycerol, ammonia, boric acid, silicic acid,O2, or even arsenic acid can also be transported [1–3]. They per-

orm fundamental functions in plants, especially related to the

membrane-; TIPs, tonoplast-; NIPs, nodulin-26-like-; SIPs, smalland basic-; and XIPs, uncharacterized-intrinsic proteins. Reversegenetics and overexpression are effective tools in plants, for inves-tigating the physiological functions of each aquaporin isoform andfor understanding their roles in water transport and abiotic stressresponses [7].

Under abiotic stress, such as water deficit or salinity, stom-ata closure is considered to be the first mechanism that the plantemploys to preserve water. However, the level of productivity isrelated to the higher rate of transpiration and leaf growth [8]. Thus,

Please cite this article in press as: M.d.C. Martinez-Ballesta, M. Carvajal, Nhttp://dx.doi.org/10.1016/j.plantsci.2013.12.006

daptation under variable environments [4–6].Aquaporins are classified into five families depending on

embrane localization and amino acid sequence: PIPs, plasma

∗ Corresponding author. Tel.: +34 968 39 62 29; fax: +34 968 39 63 13.E-mail addresses: [email protected] (M.d.C. Martinez-Ballesta),

[email protected] (M. Carvajal).

168-9452/$ – see front matter © 2013 Published by Elsevier Ireland Ltd.ttp://dx.doi.org/10.1016/j.plantsci.2013.12.006

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an optimal balance between water status, nutrient uptake, photo-synthesis, and transpiration rate is needed in plants.

Enhancing water absorption by the roots is one of the mainmechanisms by which plants can maintain their water content

ew challenges in plant aquaporin biotechnology, Plant Sci. (2013),

under stress conditions [9] and aquaporins are related to the regu-lation of the hydraulic conductivities that finally affect plant wateruptake ability. For this reason, transgenic plants overexpressingaquaporins in their roots were obvious candidates as breeding

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dx.doi.org/10.1016/j.plantsci.2013.12.006


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ARTICLESL 8904 1–7

M.d.C. Martinez-Ballesta, M. Carv

argets to improve abiotic stress tolerance. However, these trans-ormed plants failed to cope with mild and severe stresses [10–12]hich focused research efforts on the ability of aquaporins – to

ncrease water use efficiency (WUE). It has been suggested thatncreases in both carbon gain and WUE are the most efficient strat-gy that allows plants to cope with abiotic stress [13,14]. Thus, anyactor involved in both processes could be a main target for manip-lation. For this reason, aquaporins, having the dual function ofater and CO2 transport, as well as alternative isoforms to PIP, such

s TIPs that allow a tight cell osmoregulation under stress, are nowbjectives for breeding.

The search for new nanomaterials has recently brought surpris-ng results in the area of plant biotechnology. The new results athe nanoscale may provide solutions to problems concerning planthysiology focusing on aquaporins [15].

The aim of the present review is, therefore, to explore the recentdvances in the role of specific aquaporin isoforms, through thetudy of aquaporin suppression in transformed plants. The reviewlso underlines the successful cases for plant tolerance to stresschieved through aquaporin overexpression, as well as an analysisf the causes of failure, in particular cases. The future perspectivesor the use of new materials are also discussed.

. Plant responses to aquaporin suppression

The cellular and tissue hydraulic function of each aquaporin iso-orm has been studied using genetic manipulation during the lastecade. The development of knockout plants for aquaporin genesIP or TIP has been important for allowing measurements of waterermeabilities and ion transport compared to those of wild type.hese mutations have exerted a wide range of different effects onransformants sometimes difficult to explain due to the complexityf the maintenance of plant cell homeostasis.

Physcomitrella patens pip2;1 and pip2;2 knockouts decreasednternal protoplast osmotic water potential under moderated

ater stress, whereas wild type plants had no differences in waterotential between the inside of the cell and the external medium16]. They concluded that, under moderate water stress, these twoquaporins may act as constitutive isoforms for water transport,elaying water loss by a facilitated water flux through the cell sur-ace that is in contact with the liquid water phase.

Arabidopsis has been used for the majority of the aquaporinsnockout studies. Thus, Arabidopsis T-DNA mutants, lacking bothtTIP1;1 and AtTIP1;2 were without phenotypic differences com-ared to the wild type [17,18]. The authors proposed that these

soforms are not essential aquaporins under optimal growth con-itions – since other members of the TIP family may facilitate theater flow through the tonoplast – but AtTIP1;1 and AtTIP1;2 appear

o be indispensable under environmental stress [18]. These resultsuestion the previous use of interference RNAs (RNAi) as toolso characterize the function of specific aquaporin genes, since anrtifact effect, due to the silencing of non-target transcripts, wasssociated with senescence and plant death after AtTIP1;1 sup-ression [19]. In this regard, the use of antisense constructions haseen applied as an effective approach to characterize the role ofquaporins as water channels [20].

Plants with knockouts of AtPIP2;2, another abundant plasmaembrane aquaporin, were compared with wild type plants

21,22]. There was similar osmotic water transport in roots, butower hydrostatic root water transport in the mutants, whichould have significant repercussions for the whole plant hydraulics.

Please cite this article in press as: M.d.C. Martinez-Ballesta, M. Carvajal,

http://dx.doi.org/10.1016/j.plantsci.2013.12.006

owever, results with Atpip1;2 suppression revealed that thisquaporin affected root hydrostatic hydraulic conductivity butsmotic water transport was not altered. The role of this isoformn mesophyll water transport was also demonstrated contributing

PRESSPlant Science xxx (2013) xxx– xxx

approximately 20% of hydraulic conductivity of leaf rosettes [23].Similarly, AtPIP2;1 contributed to water flux into the Arabidopsisrosette and both AtPIP2;1 and AtPIP2;2 isoforms may participatein water relocation from the roots to the leaves [22]. Other aqua-porin functions were proposed in Arabidopsis leaf tissues, based onthe study of knockout plants. Thus, the expression of three PIP aqua-porins (AtPIP2;1, AtPIP1;2 and AtPIP2;6) in leaf veins contributed togrowth, due to the effect on total rosette water transport [24]. Con-versely, antisense NtAQP1 well watered tobacco plants did not havea characteristic phenotype, but under stress this isoform seems tobe involved in the reduction of root hydraulic resistance, resultingin enhanced cell water permeability [25].

Aquaporins have important functions as CO2 transporters[13,26–28]. However, few reports have demonstrated whetherspecific aquaporin suppression limits CO2 transport. Such studiesmay be confounded by collateral effects of the mutation on plantanatomy and by the pleiotropic effects on closely related genes.Internal CO2 conductance and leaf photosynthesis were stronglydecreased in T-DNA insertion lines of the Atpip1;2 knockout [29].However, when the authors produced the mutation in the AtPIP2;3isoform, which is not a CO2 transporter, no effect on the CO2 relatedprocesses was found. These results show that the AtPIP1;2 aqua-porin is highly involved in the transport of CO2 within the cell andthat this is a rate limiting process. Also, EgPIP1 and EcPIP2 expres-sion in Eucalyptus trees, was co-suppressed by a Raphanus sativusaquaporin (RsPIP1;1). A low rate of CO2 assimilation was observedwhich decreased the rate of photosynthesis in these knockdownmutants [30].

Nodulin-26-like intrinsic proteins (NIPs), a subfamily of theaquaporins proteins, facilitate the transport of silicic acid Si(OH)4(AtNIP2;1) [31], boric acid (AtNIP5;1) [32], and arsenic acid(AtNIP7;1) [33]. Their transport functions have been assessed bydirect mutagenesis and by expression in oocytes. Thus, lower Buptake was observed in two T-DNA insertion mutant lines ofAtNIP5;1 with respect to the non-transformed plants. The sub-stitution of a residue in the aromatic/arginine region in the fifthhelix position of two NIP aquaporins; the silicic acid (Si) trans-porter OsLsi1 (OsNIP2;1) from rice and the boric acid (B) transporterAtNIP5;1 from Arabidopsis; completely inhibited the transport ofB and Si but not that of As in Xenopus oocytes. Osmotic waterpermeability in individual aquaporin knockout cells decreased incomparison with the wild type [34], as well as in protoplasts iso-lated from knockout plants [20,24,25,16,35]. This indicates thataquaporins are involved in adaptation in response to stresses, andmaintaining the homeostasis – necessary for growth.

Finally, transcription factors were identified that modulate theexpression of aquaporin genes, and other genes. These transcrip-tions factors may be useful in the study of the molecular basisof plant water homeostasis in response to stress, as well as thesignaling network involved in this stress response. The use of

knockouts of these transcriptions factors, that regulate differ-ent genes involved in the stress response offers, in this sense,a biotechnological approach to the improvement of crop toler-ance. Microarray transcriptional profiling of the double knockoutlines and overexpression of the transcription factors RAP2.4B andRAP2.4, belonging to the abiotic stress associated DREB A-6 cladein Arabidopsis, were used to ascertain the mechanisms of aqua-porin regulation in response to abiotic stress [36]. Double knockoutline of rap2.4b and rap2.4 when growing under drought stress, haddownregulated expression of eight aquaporin genes. Overexpres-sion of the rap2.4 gene resulted in the upregulation of six aquaporingenes. This indicated that aquaporins were positively regulated by

New challenges in plant aquaporin biotechnology, Plant Sci. (2013),

RAP2.4B and RAP2.4 as part of the very early response to dehydra-tion.

There is a discrepancy between these findings and other workthat found the opposite result (downregulation) for the same genes,

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amely AtPIP2;1, AtPIP2;2, AtPIP2;3, AtTIP1;1, and AtTIP2;2 [37],ointed that the age of the plants, growing media and differenturation of drought stress are important issues that contributed tohe different results.

. Plant responses to aquaporin overexpression. Cases ofuccessful improvement of plant tolerance to abiotic stressnd causes of failure

.1. PIP manipulation

Aquaporins have been used as target proteins in geneticanipulation in attempts to improve plant water relations under

nvironmental stress, with numerous examples in the literatureTables 1 and 2). Thus, Vicia faba PIP1 (VfPIP1) expression inransgenic Arabidopsis thaliana improved drought resistance by aecrease of water loss through transpiration, due to an inducementf stomatal closure [38]. This control of the stomatal behavior waslso described when SlTIP2;1 was overexpressed in tomato plants,onferring resistance to salt and water stress [39]. Most VfPIP1xpression level was found in roots [38]. Therefore, a hydraulicignal between root and shoot could exist. Deeper knowledge ofoot water uptake and transport is necessary. In the same way,verexpression of RWC3 in transgenic lowland rice (Oryza sativa.) plants [40] improved resistance to osmotic stress imposed byolyethylene glycol (PEG) through higher root osmotic hydrauliconductivity and lower leaf water potential. Similarly in rice,ncreased root hydraulic conductivity conferred salt stress resis-ance after the moderate overexpression of OsPIP1;1 [41].

Nevertheless, plant aquaporin overexpression did not alwaysmprove abiotic stress tolerance [10–12,42]. Arabidopsis andobacco plants overexpressing Arabidopsis PIP1;4 or PIP2;5 hadncreased water flow in individual root cortical cells under coldtress, along with an increased percentage of germination, relativeo the non-transformed plants. These transformants had increasedater loss, under drought conditions, together with reductions in

rowth, with lower germination rates [43]. Similarly, the overex-ression of an Arabidopsis aquaporin gene (AtPIP1b) in Nicotianaabacum under favorable conditions resulted in increased growthates, gas exchange and stomatal density in plants, but underrought stress it provoked faster wilting [10].

Different responses to stress were observed after overexpres-ion of AtPIP1b, RWC3 and NtAQP1 isoforms in tobacco, rice orrabidopsis plants in spited of a high homology between theirmino acidic sequences [38]. These distinct responses indicate aomplex aquaporin regulation mechanism, where the increasedr decreased expression of a PIP gene, in a spatial and temporalanner, is required to cope with stress.Anatomical differences may results from aquaporin gene

verexpression. The stomatal density was increased in trans-enic AtPIP1b-tobacco plants, enhancing transpiration, whereast remained unmodified in transgenic NtAQP1-Arabidopsis plants44], relative to the wild type. Greater water loss may occurnder stress condition, at higher stomatal density. By contrast,educed stomatal density contributed to improved WUE underalt stress in basil (Ocimum basilicum L.) [45] and strawberry (Fra-aria × ananassa Duch.) preventing an excessive water loss [46].herefore, morphological changes resulted critical for plant adap-ation to salinity and a correlation between plant tolerance andeduced transpirational flux – due to low stomatal density – wasstablished [46].


A reduction in the root/shoot fresh weight ratio was alsobserved in transgenic AtPIP1b – tobacco plants, with respect toon-transformed control plants, whereas plants overexpressingfPIP1 had longer lateral and primary roots than controls [38],

PRESSlant Science xxx (2013) xxx– xxx 3

which affected root hydraulic conductivity. Therefore, root growthis directly related to the whole plant water transport efficiency,highlighting that the phenotypic changes produced by aquaporinoverexpression should be considered as a key factor that influencesstress tolerance, in addition to the nature, level, and duration of thestress.

In addition, differential PIP functionality cannot be discountedin distinct transgenic plants as being due to the interaction withother membrane aquaporins, since co-expression and formationof heterotetramers between PIP1 and PIP2 has been attributedto isoforms functionality [47]. Also, the overexpression of a for-eign aquaporin may improve stress tolerance through cooperationwith endogenous aquaporins. Thus, the overexpression of durumwheat TdPIP1;1 in tobacco plants enhanced stress tolerance throughincreased root growth and leaf area of the plants, even thoughthis isoform showed no functionality when expressed in Xenopusoocytes [48]. In a similar manner, overexpression of the Brassicanapus BnPIP1 gene in transgenic tobacco increased water stresstolerance at the whole-plant level, by increasing the water conduc-tance at the cellular level [49]. This positive effect may be related tothe formation of heterotetramers, but it is not clear whether phys-ical contact between ectopic and endogenous proteins occurred.

Also, the expression in one plant species of an aquaporin genefrom different species may differentially affect the expression pat-terns and distribution of endogenous aquaporin genes, dependingon the target PIP isoform as well as the nature of the foreignprotein, conditioning the response to stress [43]. Thus, the expres-sion of CfPIP2;1, a figleaf gourd (Cucurbita ficifolia) aquaporin gene,increased the survival rate of Arabidopsis plants under drought [50].The expression of cucumber (Cucumis sativus) aquaporin genesCsPIP1;1, or CfPIP2;1 also enhanced the seed germination underhigh salinity. The authors concluded that, the PIP2 subfamily wasaffected more by ectopic expression under environmental stressthan the PIP1 members. The endogenous expression patterns ofCfPIP2;1 and CsPIP1;1 under drought stress could be reflected intheir influence as ectopic aquaporins. The nature of stress alsoinfluenced the expression patterns of each individual isoform[50]. However, there was no clear evidence whether the foreignaquaporin specifically modified the endogenous Arabidopsis PIPresponse to stress or whether it first altered the endogenous PIPexpression and that this modification was responsible for theresponse to stress.

The overexpression of the exogenous RsPIP2;1 in Eucalyptustrees induced higher CO2 assimilation under normal conditions,increasing the water use efficiency when compared with non-transformed lines. However, RsPIP2;1 had no water channelactivity when expressed in yeast [51]; thus, it may have acted as afunctional water channel when it was expressed with the endoge-nous Eucalyptus PIP2 [30].

It has been suggested that dual activity of aquaporin isoformNtAQP1 attenuates the reduction of root hydraulic conductivityand maintains leaf CO2 assimilation in tomato plants overexpress-ing NtAQP1 under salt (100 mM NaCl)-stress. Thus, an increasedWUE contributed to the enhancement of plant biomass and yieldunder salinity in overexpressing plants, compared to the non-transformed controls [52]. In fact, a role for NtAQP1 has beenproposed in leaf CO2 transport [26]. A new aquaporin McMIPBhas recently been identified in Mesembryanthemum crystallinum.It enhanced CO2 diffusion, mesophyll and stomatal conductance,leaf photosynthesis, and plant growth under well-watered condi-tions [53]. The protein was classified as a PIP1 that may possiblyinteract with PIP2 aquaporins as hetero-tetramers. Thus, the co-


expression of PIP2 and PIP1 may increase the activity of PIP1not only for water flow but also for CO2 diffusion [54]. However,under prolonged soil water deficit, the overexpression of McMIPBresulted in a decreased rate of photosynthesis. The induction of

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ARTICLE IN PRESSG Model

PSL 8904 1–7

4 M.d.C. Martinez-Ballesta, M. Carvajal / Plant Science xxx (2013) xxx– xxx

Table 1Examples in the literature of success and failure regarding the improvement of plant tolerance to abiotic stress, for the model plant Arabidopsis thaliana.

Aquaporingene isoform

Aquaporinoverexpressing plant

Promoter Stress condition Response Reference

AtPIP1;b Nicotiana tabacum 35S Salinity (90 mM NaCl, 40 d) More sensitive Aharon et al. [10]VfPIP1 Arabidopsis thaliana 35S Drought (soil drying by withholding water) Resistance Cui et al. [39]AtPIP1;4,AtPIP2;5

Arabidopsis thaliana,Nicotiana tabacum

35S Water stress (100–400 mM mannitol 12–24 h, withholdingwater 15 d)Salinity (50 mM NaCl 14 d)Cold (10 ◦C, 24 h)

No effectNo effectNo effect

Jang et al. [43]

PgTIP1 Arabidopsis thaliana 35S Salinity (100 mM, 1 week)Drought (withholding irrigation for 10 d, 10 cm deeppots)Drought (withholding irrigation for 4 weeks, 45 cm deep

8 and

ResistanceMore sensitiveResistanceMore sensitive

Peng et al. [59]

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pots)Cold (−6, −7, −

At TIP5;1 Arabidopsis thaliana 35S Boron toxicity (3

cMIPB expression ameliorated the decreases of stomatal conduc-ance and photosynthesis rate under water deficit compared withhose observed in non-transformed plants [53]. Similarly, the over-xpression in rice of the aquaporin gene, HvPIP2;1,- from barleyesulted in a greater sensitivity to salinity [52], even though theverexpression of the same barley gene enhanced internal CO2 con-uctance and CO2 assimilation [55]. However, in both McMIPB andvPIP2;1 overexpressing plants, a reduced shoot/root biomass ratioas observed under stress. An inability of root water uptake to

atisfy the water demand of the aerial parts cannot be discounted.It has been suggested that the overexpression of aquaporin

soforms that are induced by stress may lead to plant stress resis-ance [52]. By contrast, the overexpression of aquaporins thatre down-regulated by stress resulted in greater damage thann non-transformed plants under stressful conditions. The loss ofown-regulation in the leaf tissues may increase cell water losshrough the stomata. They demonstrated that the control of stom-tal conductance and the net photosynthetic rate by NtAQP1 wasndependent of the root signals [52]. Therefore, elucidation of howoot-to-shoot signals may influence the effect of aquaporin overex-ression in the roots on the behavior of stomata could also providen indication about the transgenic plant response to stress. Thereatment of grape (Vitis vinifera) overexpressing the VvPIP2;4Nquaporin with ABA – to close stomata – prevented the negativeffect of the root overexpression of VvPIP2;4N on plant water statusnder water stress [11]. They proposed that alternative mecha-isms to the hydraulic conductance of cell membranes may operate



hat control water flow through the plant under water stress. In fact,t was recently observed that the overexpression of wheat TaAQP7ene, in tobacco increased the activity of detoxification enzymesuch as SOD and CAT, improving the antioxidant defense system

able 2xamples in the literature of success and failure regarding the improvement of plant tole

Aquaporingene isoform

Aquaporinoverexpressing plant

Promoter Stress condition

VvPIP2;4N Vitis vinifera 35S Water stress (soil dryin14 d)

StPIP1 Nicotiana tabacum 35Srd29A

Water stress (25% PEG

RWC3 Oryza sativa SWPA2 Water stress (PEG treaOsPIP1;1 Oryza sativa 35S Salinity (100 mM NaClSlTIP2;2NtAQP1

Solanum lycopersicumSolanum lycopersicum

EVO20535S

Salinity (180–200 mM

Drought (30–35% soiSalinity (100 mM, 3 d

HvPIP2;1 Oryza sativa 35S Salinity (100 mM NaClTdPIP1;1 Nicotiana tabacum – Salinity (250 mM NaCl

Water stress (300 mMBnPIP1 Nicotiana tabacum 35S Drought (stop irrigatioTaAQP7 Nicotiana tabacum 35S Drought (water depriv

Osmotic stress (150–

−9 ◦C)/L boric acid, 18 d) Resistance Pang et al. [60]

and reducing the H2O2 levels under drought/osmotic stress [56].TaAQP7 encodes a PIP2 subgroup of aquaporins in wheat and addi-tional mechanisms, other than the well-known improvement ofWUE and plant water retention, may contribute to the abiotic stresstolerance of transgenic plants overexpressing aquaporins.

It has also been suggested that there are anatomical modifi-cations at the leaf [55] and root level [10] under abiotic stressconditions, when aquaporin levels exceed an expression threshold,affecting the whole plant water balance. In accordance with this,low or moderate overexpression of OsPIP1;1 in rice enhances plantresistance to salt stress. OsPIP1;1 expression naturally increasedin leaves but was reduced in roots under salinity. However, highoverexpression of OsPIP1;1 produced sterile rice seeds – through areduction of reproductive growth – and OsPIP1;1 function as a com-ponent of water conductance was rather limited [41]. A disruptionof the plasma membrane structure by OsPIP1;1 with subsequentalteration of the endogenous PIP, has been proposed [41].

Thus, the ability of each overexpressed aquaporin isoform toconfer (or not) resistance to a specific stress may depend on itscontribution to the plant control of water loss by transpiration orits ability to maintain CO2 assimilation or increase water uptake(Fig. 1). The mode of action of a particular isoform on other endoge-nous aquaporins may produce an overall response to the stress.

3.2. TIP manipulation


It has been predicted that the selection of the suitable aqua-porin isoforms for genetic manipulation is a decisive factor forsuccess in improving abiotic stress tolerance [39]. The TIPs (Tono-plast Intrinsic Proteins) are considered as important elements of

rance to abiotic stress, for different crops.

Response Reference

g by withholding water, More sensitive Perrone et al. [11]

6000) More sensitive Wu et al. [60]

tment, 10 h) Resistance Lian et al. [40], 14 d) Resistance Liu et al. [41]NaCl)l volumetric water content))

ResistanceResistanceResistance

Sade et al. [57]Sade et al. [58]Sade et al. [52]

, 2 weeks) More sensitive Katsuhara et al. [42], 30 d)

mannitol, 30 d)ResistanceResistance

Ayadi et al. [49]

n, 20% PEG8000) Resistance Yu et al. [50]ation, 20 d)300 mM mannitol, 7–12 d)

ResistanceResistance

Zhou et al. [56]

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ig. 1. Effects of aquaporins overexpression conferring plant resistance or sensitivity higher water uptake at the root level, lower water loss by transpiration, and/or mhe case of OSPIP1;1, no involvement in plant water hydraulics is observed.

he mechanism that controls cell water homeostasis through theast water exchanges between the vacuole and cytoplasm [39,57].

An efficient computational approach in which the expressionatterns for different aquaporin gene families were consideredogether with plant anatomy, developmental stage, and abiotictress, was used to predict aquaporin isoform candidates for plantbiotic stress improvement [39]. They then demonstrated thathe overexpression of SlTIP2;2 in tomato (Solanum lycopersicum.) attenuated the reduction of plant transpiration under stress,llowing an adequate balance between CO2 uptake and water andutrient supply. The experiments were carried out in the field underalt (180–200 mM NaCl) and drought (plants irrigated once a weekntil soil saturation) conditions and the duration to exposure tohe stress and the stress intensity were important factors to deter-

ining the plant recovery rate. This behavior was attributed tohe high tonoplast osmotic water permeability that enhanced thesmoregulation ability of the vacuole. Previously, overexpressionf the tonoplast aquaporin, PgTIP1 from Panax ginseng, in Ara-idopsis plants increased plant growth, but only under optimalonditions or very low drought stress [58]. The mechanisms byhich the overexpression of different PIP and TIP subfamilies hadistinct effects on the stress response need further investigation,ut the rapid water exchange in the vacuole of plants overexpress-

ng TIPs may facilitate greater Na+ accumulation in the case of salttress.

The selection of aquaporin isoforms involved not only in waterransport, but which also influence processes such as ion transport

ay improve stress tolerance. Thus, the overexpression of tono-last aquaporin TIP5;1 in Arabidopsis increased tolerance to high

evels of borate, through the involvement of this isoform in borateompartmentation in the vacuole [59]. In a similar way, the over-xpression of wheat nodulin 26-like intrinsic protein gene, TaNIP,


n Arabidopsis plants favored Na+ extrusion from the cytoplasm tohe extracellular matrix, whereas it increased K+ and Ca2+ con-ents in the plant tissues, hence improving salinity tolerance aboveon-transformed plants [60].

iotic stress. Overexpression of a specific aquaporin isoform may provide resistanceined CO2 assimilation. When overexpression exceeds a threshold in the plant, as in

Differences in the experimental design, the nature, intensityand duration of the stress and the developmental stage of theplants, must be considered in plants overexpressing aquaporinsresponse to abiotic stress. For example, Arabidopsis plants over-expressing PgTIP1 were resistant to water stress compared to thenon-transformed plants when they were grown in 45 cm deep pots,whereas they were more sensitive when grown in 10 cm deep pots,as consequence of faster drying of the rooting medium [58].

4. Innovative approaches affecting plant aquaporins

It is well documented that alterations of aquaporin functionand/or expression affect human health, and natural products fromplants or drugs can prevent diseases by acting upon aquaporins (forreview see [61]). Similarly, exogenous compounds such as thiourea[62], dopamine [63], glycine-betaine [64], and sinigrine [65] candown or up-regulate aquaporins in Brassica juncea, O. sativa, Zeamays, and Brassica oleracea, plants respectively. The aquaporinexpression pattern conferred on all the above species were relatedto greater stress tolerance.

Also, the interest in the biological and biomedical effects of newnanomaterials has recently increased. Nanoscale materials interactwith animal tissues (even tumor cells; [66]) and plant cells [67] bypenetration through the cell wall and membranes or allowing thedelivery of biological molecules into plant cells. Carbon nanotubeshave been particularly studied, due to their unique physical, chem-ical, and electronic properties for biotechnological applications –such as biomolecule delivery and tissue engineering [67–69] – morethan other nanoparticles such as nano-TiO2 and nano-Al [70,71].

Single or multiple-walled carbon nanotubes are often toxic tohumans [72], while their application to plants has beneficial effects.The plant–nanoparticle interactions are quite complex and require


further investigation. However, there are some evidence for aneffect on gene transcription, positively affecting plant responsegrowth [69,73,74]. Multiple-walled carbon nanotubes are takenup by tomato plants, increasing their total gene expression and

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articularly aquaporins [75]. The effects of carbon based struc-ures were compared: activated carbon, graphene-with singlend multiple-walled carbon nanotubes. There was an increase inrowth due to the carbon nanotubes treatments, especially inhe multi-wall treated plants [15,69,73,74]. The authors also sug-ested that the increase in aquaporin expression had an impactn the germination and growth. It was concluded that the abilityf multiple-walled carbon nanotubes to penetrate cell walls [69]nd their promotion of cell division/extension, involving aquapor-ns, needs further in depth investigation of the mechanisms andignaling pathways and cascades involved.

All these preliminary results open a new research area at thenterface between nanomaterials and plant biology, with multipleossibilities in the genetic engineering and improvement of planttress tolerance that could be beneficial to the development of newiotechnologies. However, the safety profile has to be defined andhe environmental and health risk evaluated before considering thextended use of nanotubes in the agri-food sector.

. Concluding remarks

The development of knockout and overexpressing aquaporinutants has been an efficient tool for studying the contribution

f individual isoforms to plant water flow. In general, aquaporinsay delay water loss by promoting cell water retention under unfa-

orable conditions. It has been determined using reverse geneticpproaches that some TIP and PIP members seems to be redundantn optimal culture conditions but are essential under environmen-al stress, with specific isoforms making a significant contributiono whole plant hydraulics. However, different factors have to beaken into account for successful plant tolerance of abiotic stresshen aquaporins are overexpressed. Thus, distinct phenotypes of

quaporin overexpressing plants may depend on the combinationf water transport ability, transpiration rate, and stomatal aper-ure – which are in turn related with plant anatomy. It seems thathe overexpression of aquaporins that are down-regulated undertress fails to confer tolerance. The influence of ectopic expressionn endogenous aquaporins and the formation of active heteromerseed further investigation, as the interactions between differ-nt aquaporin isoforms and their coupled response/functionalitynder stress conditions still need to be elucidated. The multiplic-

ty of aquaporin isoforms and their involvement in the response totress depend on the nature, intensity and duration of the stress,ecessitating a selection “on demand” of the aquaporin geneticanipulation to solve a specific environmental problem for each

articular cultivar.Finally, the use of carbon nanotubes offers a new challenge to be

nvestigated. The application of nanotechnology to crops in ordero improve their responses to different environmental stresses rep-esents a new research area.

onflict of interest

No conflict of interest.

cknowledgments

The authors thank Dr. David J. Walker for correction of the writ-en English in the manuscript. M.C. Martínez-Ballesta thanks thepanish Ministerio de Ciencia e Innovación for funding through theRamón y Cajal” program [Ref. RYC-2009-04574].



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New challenges in plant aquaporin biotechnology

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