Regulation of root water uptake under abiotic stress conditions

15 Pages·2011·0.36 MB·English

JournalofExperimentalBotany,Vol.63,No.1,pp.43–57,2012
doi:10.1093/jxb/err266 AdvanceAccesspublication13September,2011
REVIEWPAPER
Regulation of root water uptake under abiotic stress
conditions
Ricardo Aroca*, Rosa Porcel and Juan Manuel Ruiz-Lozano
DepartamentodeMicrobiologı´adelSueloySistemasSimbio´ticos,Estacio´nExperimentaldelZaidı´n(CSIC),ProfesorAlbareda1,18008,
Granada,Spain D
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*Towhomcorrespondenceshouldbeaddressed.E-mail:[email protected] n
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Received3June2011;Revised26July2011;Accepted1August2011 d
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Abstract ttp
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A common effect of several abiotic stresses is to cause tissue dehydration. Such dehydration is caused by the ca
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imbalance between root water uptake and leaf transpiration. Under some specific stress conditions, regulation of e
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root water uptake is more crucial to overcome stress injury than regulation of leaf transpiration. This review first ic
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describes present knowledge about how water is taken up by roots and then discusses how specific stress u
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situations such as drought, salinity, low temperature, and flooding modify root water uptake. The rate of root water .co
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uptakeofagivenplantistheresultofitsroothydrauliccharacteristics,whichareultimatelyregulatedbyaquaporin /jx
activity and, to some extent, by suberin deposition. Present knowledge about the effects of different stresses on b/a
these features is also summarized. Finally, current findings regarding how molecular signals such as the plant rtic
hormones abscisic acid, ethylene, and salicylic acid, and how reactive oxygen species may modulate the final le-a
responseofrootwateruptakeunderstressconditionsarediscussed. bs
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Keywords: Abioticstresses,abscisicacid,aquaporins,ethylene,reactiveoxygenspecies,rootwateruptake,salicylicacid, t/6
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suberin. /1
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Introduction b
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Plants are sessile organisms that cannot escape from stress conditions (Zhang and Zhang, 1994; Aroca et al., e
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environmentalconstraintsand,asaresult,theyhaveevolved 2001, 2007; Wahid and Close, 2007). Under some environ- t o
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numerous adaptive responses to cope with environmental mental conditions, dehydration is the first signal that 3
0
stresses. Most environmental stresses share common effects induces the plant to respond (Jia et al., 2002; Christmann M
a
and responses such as a reduction in growth and photosyn- et al., 2007), and the importance of the hydration state of rc
h
thesis, oxidative damage, hormonal changes, and the accu- tissues in the response of the plant to different stresses is 2
0
1
mulationofnumerousstress-relatedproteins.Thesechanges wellsupportedbyexperimentalevidence(Arocaetal.,2001; 9
areusuallytheresultoftissuedehydration(Kacperska,2004; Bouchabke-Coussaet al., 2008;Matsuo et al.,2009).
Dobraetal.,2010).Tissuedehydrationoccurswhenthereis The importance of root water uptake capacity in coping
an imbalance between root water uptake and leaf transpira- with several abiotic stress conditions is supported by the
tion (Aroca et al., 2001; Jackson et al., 2003). When leaves work of Aroca et al. (2001) who found that two maize
begin to dehydrate plants generally start closing their genotypes differing in chilling sensitivity also differed in the
stomata; however, under some environmental situations or response of their root water uptake rate to chilling stress.
in specific plant genotypes, modification of root water Hence,whilethetolerantgenotypekeptitsleaftranspiration
uptakecapacityplaysamoreimportantrolecomparedwith and root water uptake rates unchanged during chilling
stomatal closure in avoiding stress-induced growth reduc- periods, the sensitive genotype became dehydrated because
tion (Matsuo et al., 2009). Water deficit occurs in tissues it decreased first its root water uptake rate and then its leaf
under drought, low temperature, heat, salt, or flooding transpiration. Also, Matsuo et al. (2009), comparing three
ªTheAuthor[2011].PublishedbyOxfordUniversityPress[onbehalfoftheSocietyforExperimentalBiology].Allrightsreserved.
ForPermissions,pleasee-mail:[email protected]
44 | Aroca et al.
ricegenotypes,foundagoodcorrelationbetweenrootwater Ehwald(2011)demonstratedthatinsomespeciesandunder
uptake capacity (estimated as root hydraulic conductivity, some conditions water flowing by the cell-to-cell path could
L) and shoot dry weight under water-limited conditions. In accountforalmostthewholeradialrootwatertransporteven
the same way, Hattori et al. (2008) found that the under transpiring conditions.However,it is possiblethatthe
ameliorative effect of silicon application in the response of above-mentioned findings only apply to barley (Hordeum
sorghum plants to osmotic stress was mainly caused by an vulgare) as previously found by Steudle and Jeschke (1983).
improvement of root water uptake capacity, avoiding water Obviously, although more research is needed to clarify the
imbalance caused by the osmotic stress imposed. The predominant water movement path under various environ-
studies cited above are examples that support the impor- mental conditions, these recent results highlight the impor-
tance of root water uptake capacity to overcome abiotic tance of the cell-to-cell path in the overall radial root water
stress-induced tissue dehydration. transport. However, the role of root morphology and
The present review aims to highlight recent advances in anatomy in the overall root water transport capacity cannot
our knowledge of how several abiotic stresses, namely beunderestimated(Bramleyetal.,2009).
drought, salt, low temperature, and flooding, modulate the Independently of the radial water pathway that predom-
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root water uptake capacity of vascular plants. First a brief inates under specific environmental conditions, the role of o
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description of the basic concepts of root water uptake will aquaporins in root water uptake has been abundantly n
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be presented, followed by the specific effects of each documented (Kaldenhoff et al., 1998; Javot et al., 2003; a
d
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particular stress on root water uptake properties. Finally, Postaire et al., 2010). Aquaporins first described in plants d
the possible involvement of some regulatory mechanisms by Maurel et al. (1993) are membrane intrinsic proteins fro
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common to all of these stresses will be postulated. It is found in all living organisms (Agre et al., 1993) that h
intended that this review will open up new avenues in the facilitate the passage of water by forming a proteinaceious ttps
research fieldof root water uptake properties. pore in the membrane. Osmotic gradients drive water ://a
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transport through aquaporins. In plants, aquaporins are ad
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divided into five families: PIPs, plasma membrane intrinsic m
ic
Root water uptake concepts proteins; TIPs, tonoplast intrinsic proteins; NIPs, nodulin- .ou
26-like intrinsic proteins; SIPs, small and basic intrinsic p
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Two main forces regulate the root water uptake rate, proteins; and XIPs, uncharacterized intrinsic proteins. The om
namely osmotic and hydrostatic forces. Hydrostatic force is numberofaquaporingenespresentinaplantspeciesisvery /jx
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generated by the transpiration stream, whereas osmotic high, ranging from 30 to >70 (Maurel et al., 2008; Park /a
force is generated by the root pressure (active transport of et al., 2010). At the same time, although aquaporins were rticle
solutes or biosynthesis of new osmolytes). Root water first characterized as water channels, it has now been -a
b
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transport is divided into radial and axial transport. The demonstrated that some specific plant aquaporins also tra
axial transport consists of the water moving along the transport other small neutral solutes such as glycerol or ct/6
xylem vessels to aerial parts, and it does not contribute in ammonia, nutrients such as boron or silicon, gases such as 3
/1
a major way to the resistance of water transport through CO , or metalloids such as arsenic (Bienert et al., 2008; /4
2 3
the whole plant (Doussan et al., 1998; Knipfer and Fricke, Tanaka et al., 2008; Maurel et al., 2009). Moreover, the /5
5
5
2011). In woody plants, this axial transport can be an localization of each aquaporin protein inside the plant cells 9
3
important determinant of resistance because of cavitation varies among cell membranes. At the same time, the 6 b
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events (Dalla-Salda et al., 2009). On the other hand, radial membrane aquaporin location in the cell is dynamic since g
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water flow from the soil solution to the root xylem vessels some transport of them from internal membranes to the e
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hashighresistancetorootwatertransportandinvolvesthree plasma membrane has been found (Zelazny et al., 2007; t o
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dynamically exchangeable paths (Steudle and Peterson, Wudick et al., 2009). For recent reviews about cellular 3
0
1998). The apoplastic path comprises water moving through functionality and localization of plant aquaporins, see M
a
the pores between the fibrils of the cell wall and through the Katsuhara et al. (2008), Maurel et al. (2008, 2009), and rc
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intercellular spaces. The symplastic path consists of Wudick etal. (2009). 2
0
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water moving through the cytoplasm and through plasmo- To estimate the root water uptake capacity of a single 9
desmata between cells. Finally, the transmembrane path root or of the whole root system, L measurements are
comprises water moving through the cytoplasm and the undertaken, and a direct correlation between L values and
vacuolescrossingtheplasmaandvacuolarmembranes.Since rootwater uptakerates hasbeenobserved (Nobel and Alm,
empirically the symplastic and transcellular paths cannot 1993;Gallardo etal.,1996;NardiniandPitt,1999;Lietal.,
be discriminated, the sum of these two paths is called the 2005). In this sense, the contribution of aquaporins to L
cell-to-cellpath(SteudleandPeterson,1998). values has been tested by several approaches. In the 1990s,
It was assumed that under transpiring conditions the the involvement of aquaporins in L regulation was assayed
main route for radial water transport was the apoplastic by the inhibition of L by mercurial reagents (Maggio and
path, and under conditions where transpiration is reduced, Joly, 1995; Carvajal et al., 1996), since several plant
the main route would be the cell-to-cell path (Steudle and aquaporins have a cysteine residue sensitive to Hg (Daniels
Peterson, 1998; Javot and Maurel, 2002). However, more etal.,1996).However,notallplantaquaporinsaresensitive
recently, Knipfer and Fricke (2010, 2011) and Fritz and to Hg (Daniels et al., 1994), and Hg could have other
Root water uptake regulation | 45
secondary effects as well (Gaspar et al., 2001). More potential does not fall below the water potential of roots.
conclusive approaches involved the use of transgenic plants Anyway, the signals (hydraulics or chemicals) that regulate L
in which the expression of some aquaporins was inhibited. behaviourunderdroughtconditionsarestillunknown.
Siefritz et al. (2002) and Postaire et al. (2010) found that As previously indicated, L behaviour is regulated par-
a specific plasma membrane aquaporin (PIP) of tobacco tially by aquaporin function, specifically by PIPs (Javot
and Arabidopsis, respectively, regulated L under hydrostatic et al., 2003; Postaire et al., 2010). However, looking at
forces. On the other hand, again Siefritz et al. (2002) and many studies, it is hard to find a common response of root
Javot et al. (2003) found that a specific PIP of tobacco and PIP aquaporin expression and PIP protein abundance
Arabidopsis, respectively, regulated L under osmotic forces. underdroughtconditions.Theresultsofninerepresentative
These findings clearly support the involvement of PIP studies where PIP expression under drought conditions
aquaporins in the regulation of L under both osmotic and wasmeasuredinrootswereanalysed(Table1).Amongthe
hydrostatic forces and, therefore, their involvement in the 37 PIP genes studied, 15 were down-regulated, 13 up-
wholerootwater uptake rate. regulated, and nine unaltered. Even in the same experiment
some PIP genes were down-regulated, others up-regulated,
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and others unaltered (Aroca et al., 2007; Ruiz-Lozano et al., o
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2009). So, based on expression studies it is difficult to assign n
Root water uptake under drought conditions lo
aroleforPIPgenesinregulatingL during droughtstress.In a
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Plants experience drought stress when a fixed percentage of fact,thereisevidencethateachPIPgenecouldhaveaspecific d
volumetric soil water content is not replenished by natural function under specific stress circumstances. For example, fro
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rainfall or irrigation (Bre´da et al., 1995; Chen et al., 2010). Jang et al. (2007a, b) found that the overexpression of h
From this point onward, transpiration and root water a certain PIP aquaporin gene induced tolerance to some ttps
uptake start to decline (Bre´da et al., 1995; Duursma et al., environmental stresses but sensitivity to others. Similarly, ://a
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2008). Thus, overall root water uptake under drought Aharon et al. (2003) found that the overexpression of ad
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conditions depends on soil, soil–root air gaps, and L. L aforeignPIPaquaporingeneintransgenictobaccoimproved m
ic
limits overall root water uptake in the initial phases of plant vigour under favourable growth conditions but not .o
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drought periods, and soil conductivity and the lack of underdroughtorsaltstressconditions. p
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contact between root and soil are limiting to water Different regulation of PIP protein abundance in root om
movementwhendroughtbecomesmorepronounced(Nobel tissues under drought conditions has also been observed /jx
b
and Cui, 1992; North and Nobel, 1997). Researchers (Table 1). Commonly a decrease in abundance of PIP2 /a
consistently report a decline of L under drought conditions proteins has been recorded (Aroca et al., 2006, 2007; rticle
(Nobel and Cui, 1992; Rieger, 1995; North et al., 2004; Ruiz-Lozano et al., 2009), but an accumulation of PIP1 -a
b
s
Trifiloetal.,2004;Arocaetal.,2006,2008b;YXGaoetal., proteinsunderdroughtconditionshasalsobeenfound(Lian tra
2010). et al., 2004; Aroca et al., 2007). Anyway, a correlation ct/6
The initial decrease of L under drought conditions could between PIP protein abundance and L behaviour has not 3
/1
be a mechanism to avoid water flow from root to soil while always been observed. Zhang et al. (2007) found an /4
3
soil water potential is decreasing progressively. However, accumulationofPIP2proteininrootmembranesofJatropha /5
5
5
soil drying does not occur at the same rate at different curcas upon exposure to osmotic stress simulated by poly- 9
3
depths, and the drying rate is more pronounced in the ethylene glycol, but at the same time these authors found 6 b
y
superficial soil layers than in the deeper ones. Thus, plants a decrease in L values. This discrepancy could be caused by g
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able to develop a deeper root system usually are more a different subcellular localization of PIP proteins (invagina- e
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tolerant to drought than plants with a more superficial root tionsoftheplasmamembrane;Boursiacetal.,2005,2008)or t o
n
system (Pinheiro et al., 2005; Alsina et al., 2011). In fact, by different PIP protein localization along the root axis 3
0
some plant species are able to transport water from wetter (Benabdellahetal.,2009). M
a
deeper soil to superficial drier soils, a mechanism known as Vandeleur et al. (2009) found that theanisohydric(plants rc
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hydraulic lift; this ability could be crucial in some circum- that vary their leaf water potential during the day) 2
0
1
stancesto toleratedroughtstress(Wan etal.,2000). grapevine cultivar Chardonnay increased the expression of 9
Although L decreases upon root exposure to drought, a PIP1 gene in its roots upon exposure to drought,
under some specific drought circumstances an increase in correlating with an increase in the cortical cell L. However,
L has been reported. Singh and Sale (2000) found that white the same authors also found a diminution in the whole root
clover plants well supplied with phosphorus increased their L system hydrostatic L. These results confirmed the hypothe-
(estimated by the Hagen–Poiseuille equation which takes into sis of Steudle and Peterson (1998) that when the transpira-
account the vessels’ diameters) after drought treatment (soil tion is restricted (such as during drought), the cell-to-cell
moisture depletion down to –1.5 MPa). Also, Siemens and path should dominate. At the same time, the diminution of
Zwiazek (2004) found thatPopulus tremuloidestrees subjected overall L observed by Vandeleur et al. (2009) could be
to mild drought stress (exposing roots to a high humidity air caused by suberin and lignin depositions restricting the
chamber for 17 h) showed an up-regulation of L measured apoplastic water flow which was not compensated by the
under hydrostatic forces. This up-regulation of L could be cell-to-cell path water flow. However, other authors have
a mechanism to absorb water from soil when soil water found that under drought conditions, the diminution of
46 | Aroca et al.
Table1. SummaryofdroughtstresseffectsonPIPgeneexpression,proteinabundance,andLindifferentexperimentalset-upsand
plantspecies
Species Treatment PIPexpresio´n Proteinregulation L Source
Arabidopsisthaliana (4–48h)250mM AtPIP1;3,1;2,2;1,2;5UP ? ? Jangetal.(2004)
mannitol
AtPIP1;1,1;2,1;5,2;2,
2;3,2;4,2;6,2;7,2;8DOWN
Lactucasativa 10dat75%offield LsPIP2DOWN ? DOWN Arocaetal.(2008b)
watercapacity
Vitisberlandieri3 7dwithstomatal VvPIP1;1,1;2,2;1EQUAL ? ? Galme´setal.(2007)
Vitisrupestris conductancedownto
55–18%ofcontrolplants VvPIP1;3,2;2UP
Nicotianatabacum 24hat–0.35MPaby NtPIP1;1,2;1DOWN ? DOWN Mahdiehetal.(2008)
applyingPEG6000 NtAQP1(PIP1)UP D
o
Phaseolusvulgaris 4dwithoutwatering PvPIP1;1EQUAL PIP1sUP DOWN Arocaetal.(2007) w
n
PvPIP1;3,2;1UP PIP2sDOWN lo
a
d
PvPIP1;2DOWN e
d
Vitisvinifera 8–10dwithoutwatering VvPIP2;2EQUAL ? Wholeroot Vandeleuretal.(2009) fro
VvPIP1;1UP systemLDOWN m
CellLUP http
Oryzasativa 10hwith20%PEG6000 OsPIP1;3UP UP ? Lianetal.(2004) s
Zeamays 4dwithoutwatering ZmPIP1;1UP ZmPIP1;2EQUAL EQUAL Ruiz-Lozanoetal.(2009) ://a
c
a
ZmPIP2;5,2;6DOWN ZmPIP2;1,2;5DOWN d
e
ZmPIP1;2,1;5,2;1,2;2 m
ic
EQUAL .o
u
Gossypiumhirsutum DifferentPEGtreatments GhPIP1;1,2;1UP ? ? Lietal.(2009) p
.c
GhPIP2;2EQUAL o
m
/jx
b
whole root system L is correlated with an increase in the effect of salinity is most intense in arid and semi-arid /a
proportionofwatermovingbytheapoplasticpath(Siemens climatic areas because the amount of salt increases as rtic
le
and Zwiazek, 2003, 2004). These discrepancies could be a result of irrigation and in soils used for intensive -a
b
causedbythedifferentstrategiestoovercomedroughtstress agriculture because the use water reservoirs already having stra
by the different plants species or cultivars. In fact, high amounts of salts (Mostafazadeh-Fard et al., 2009). c
t/6
Vandeleur et al. (2009) found an opposite behaviour in the Commonly, root water uptake decreases upon exposure to 3
/1
isohydric grapevine cultivar Grenache. It is clear that more saltstress.Thisdecreasecanbecausedbybothosmoticand /4
3
research is needed in order to ascertain which signals toxic effects, depending on the salt concentration present. /5
5
(hydraulics or chemicals) are responsible for L and PIP Silva et al. (2008) found that pepper plants treated with 59
3
aquaporin regulation during drought stress. At the end of a low concentration (30 mM) of NaCl, or with a nutrient 6
b
this review a section is devoted to this topic. solution with the same osmotic value, decreased their root y g
Ontheotherhand,theoverexpressionofTIPaquaporinsin water uptake rate and L values to the same extent. ue
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plantsalsoproducesplantswithdifferenttolerancetodrought However, when the NaCl concentration was further in- t o
n
stress.Thishasbeenattributedtoabiggerrootsystemcapable creased to 60 mM and the osmotic pressure of the nutrient 3
0
of exploring more soil to capture water, since cell elongation solution rose to the same value (–0.290 MPa), only plants M
a
requires a vacuolar membrane with high water permeability treated with NaCl decreased their root water uptake rate rc
h
capacity(Pengetal.,2007),ortoastimulation ofanisohydric and L values further. So, the decrease in the root water 2
0
plant behaviour (Sade et al., 2009). However, Wang et al. uptakerateandLunderhigherconcentrationsofNaClwas 19
(2011) found that Arabidopsis plants overexpressing a TIP caused by specific toxic effects due to the accumulation of
aquaporinfromsoybeanweremoresusceptibletodehydration Na+ and Cl– ions in root tissues, or by the imbalance in the
stress. Thus, TIPs and possibly other kinds of aquaporins acquisition of other nutrients.
besides PIPs could be involved in the response of plants to A decrease of L under saline conditions has been
drought stress. However, at present, not very much informa- observed frequently (Azaizeh et al., 1992; Navarro et al.,
tionaboutthesetopicsisavailable. 2003;Boursiacetal.,2005;Silvaetal.,2008;Nedjimi,2009;
Wan, 2010; Muries et al., 2011; Sutka et al., 2011). The
initial L decrease upon salt exposure may be caused by an
osmotic shock as a result of an aquaporin conformational
Root water uptake under salt conditions
change caused by negative pressures (Wan et al., 2004).
Soil salinity is one of the most important factors that Moreover, applying a final NaCl concentration of 50 mM
restrict agricultural production in the world. The negative to maize roots in two steps (25 mM each) reduced the L
Root water uptake regulation | 47
value of cortical cells to a lesser extent than when 50 mM
NaCl was applied all at once. The 50 mM application would
produce a higher osmotic shock (Wan, 2010). At the same
time, L could decrease as the result of a direct effect of Na+
ions in aquaporin functioning (Carvajal et al., 1999). The
decrease of L under salt stress conditions could be a strategy
to diminish water flow from roots to soil while the soil
osmotic potential is lower than that of the roots. A similar
response also operates under drought conditions (see above).
The initial diminution of L was correlated with a down-
regulation of PIP aquaporin genes (Mart´ınez-Ballesta et al.,
2003a;Boursiacetal.,2005).Mostinterestingweretheresults
of Boursiac et al. (2005) who observed internalization of
plasma membrane vesicles containing PIP proteins; this
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resulted in a decrease in L. The decrease in L in the initial o
w
phase of salt stress was correlated with an increment in the n
lo
percentageofwatermovingviatheapoplasticpath(Mart´ınez- a
d
e
Ballesta et al., 2003a). Thus, in the initial phase (a few hours) d
of salt stress a decrease in L is caused mainly by an osmotic fro
m
slroehswopcorkan,tsweibholeifchwfoacrtoetrrhreuelpalttoaewskewtrtithahnatsapridermeactairoeinnasseraafitnteerc(oMsratlaitcraat´ılpnpceelzil-clBaLtai.lolTenshtiaes Frpeoisgsp.so1ibn.lsyDecsiaatugosraesmadltbr.eyApltoretwhseeerninatiitnqiagularspotaoogtrinehsy(Pd(wrIPaitu)hlaiicnctchivooitnuydr,suin)c,ittLiaandllyceecrer(eLsau)slteinsg, https://ac
etal.,2003a,b),anditfollowstheapoplasticpath. fromanosmoticshockorioniceffects.Atlaterstages(withindays), ade
At later stages of salt stress (after few days), a partial or m
Lcouldrecoverbythesumoftheosmoticadjustment,releaseof ic
total recovery of L has been described in some species ioniceffects,andtheincreaseintheactivityofPIPaquaporins.‘?’ .ou
(Mart´ınez-Ballesta et al., 2003a; Wan, 2010). Thus, maize p
anddashedarrowsindicateasyetunidentifiedsignals. .c
root cortical cells recovered their L values after 6 d of om
exposure to 50 mM NaCl (Wan, 2010). Also, Arabidopsis /jx
b
plants partially recovered their L values after 3 d of case, the recovery of L after some days of salt application /a
exposure to 60 mM NaCl (Mart´ınez-Ballesta et al., 2003). can only take place if the root cells also overcome other rticle
This recovery of L after a long exposure to salt conditions toxic effects of salt stress such as the production of reactive -a
b
s
observed in some species is accompanied by an increase in oxygen species(ROS;Boursiac et al.,2008). tra
suberin contents in endodermal and/or exodermal root cells Itisworthnotingthatsomeplantspecies/ecotypesdonot ct/6
(Schreiber et al., 2005), potentially diminishing apoplastic decrease their L values upon exposure to salt. Sutka et al. 3
/1
water flow and Na+ and Cl– entrance into xylem vessels (2011) found that a particular ecotype of Arabidopsis /4
3
(Zimmermann et al., 2000; Ranathunge and Schreiber, (Monte-Tosso-0, Mr-0) did not change its L value after /5
5
5
2011). Thus, this partial L recovery observed after a long exposure of roots to 100 mM NaCl for 4 h. The authors 9
3
exposure to salt could be caused by an enhancement of the stated that this particular ecotype is more tolerant to 6 b
cell-to-cell pathway, since water flowing by the apoplastic drought stress, but no data supporting this fact were shown y g
u
pathway is restricted. In fact, accumulation of PIP proteins in their report. Therefore, whether such behaviour is linked e
s
in roots of salt-treated plants for long periods (from 3 d to tosalt tolerance isat themoment unknown. t o
n
15 d)has been found (Marulanda etal.,2010;Muries etal., Also, apart from the role of PIP aquaporins in the 3
0
2011), which could favour the cell-to-cell pathway. Also, regulation of water uptake under salt stress, the role of M
a
Lo´pez-Pe´rez et al. (2009) found that plasma membranes of other aquaporin subfamilies in the tolerance of plants to rc
h
broccoli roots subjected for 15 d to 80 mM NaCl increased salinity has been observed. Hence, Peng et al. (2007) found 2
0
1
their unsaturated fatty acid ratio: the membranes became that Arabidopsis plants overexpressing a TIP aquaporin 9
more fluid, which also could have an additive effect to the from seeds from the ginger plant were capable of germinat-
function ofPIPaquaporins. ing and the seedlings grew even at 150 mM NaCl. In
The increase in L due to the cell-to-cell path should be contrast, Wang et al. (2011) found that Arabidopsis plants
accompanied by an osmotic adjustment of the root cells overexpressing a TIP aquaporin from soybean were more
(accumulation of compatible solutes) in order to avoid cell sensitive to salt stress. This apparently contradictory result
dehydration (Wan, 2010). However, although under salt could possibly be explained as follows: Peng et al. (2007)
conditions an osmotic adjustment has been seen eventually used a TIP1 aquaporin isoform and Wang et al. (2011)
in root tissues (Rodr´ıguez et al., 1997; An et al., 2002), in a TIP2 isoform for their work. Perhaps the two types of
these studies no L measurements were undertaken. Thus, TIPs are localized in different kind of vacuoles (lytic for
which chemical signals are behind this L acclimation under TIP1 and protein storage for TIP2), or differ in their tissue
salt stress remains to be explored. Nevertheless, a picture of localization along the root axis (Gattolin et al., 2010). At
how L responds to salinity can be drawn (Fig. 1). In any the same time, it is known that the overexpression of one
48 | Aroca et al.
foreignaquaporin in aplantalters the pattern of expression a break point in the Arrhenius plot experiments was
of theendogenousaquaporins (Jang et al.,2007b). observed (see table 1 of Murai-Hatano et al., 2008). These
The role of TIP aquaporins under salt stress conditions break points are attributed to membrane injury, most
couldbetoequilibratetheosmoticpotentialofthecytoplasm probably caused by a phase transition of membrane lipids
by the exchange of water with the vacuole (Kjellbom et al., (Nishida and Murata,1996).
1999). Z Gao et al. (2010) found that Arabidopsis plants Hence, as for salt stress, it seems that the decline in L at
overexpressing a NIP aquaporin from wheat were more the initial phase (within a few hours) of low temperature
tolerant to salt stress than untransformed plants. The trans- stress is also caused by a diminution of aquaporin activity.
formed plants had better root growth under salt conditions, However, Murai-Hatano et al. (2008) did not find any
as well as higher accumulation of Ca2+ and lower levels of significant changes in the amount of several PIP and TIP
Na+.Theprecisemechanismofthistoleranceenhancementis proteins in root tissues of rice during the first 5 h of low
unknown. Obviously, more research is needed to understand temperature treatment, whereas they observed an abrupt
completely the role of other plant aquaporins (beside PIPs) decline of L. Therefore, they hypothesized that the decrease
intheresponsesofplantstosaltstress. in L observed could be caused by closure of aquaporin
D
pores rather than by a decrease in protein amounts. One o
w
possibility could be a closure of aquaporins due to n
lo
Root water uptake under low temperature acidification of the cytosol during low temperature periods ad
e
(Kawamura 2008), as this response has been demonstrated d
conditions under hypoxiaconditions (Tournaire-Rouxet al., 2003). fro
m
Inthissectionlowtemperaturereferstotemperaturesbetween Several low temperature-tolerant plant species (or geno- h
0 (cid:1)C and 15 (cid:1)C, and studies dealing with temperatures below types of a particular plant species) are able to recover their ttps
0 (cid:1)C,knownasfreezingtemperatures,arenotincluded.Thus, L after a prolonged time (a few days) of exposure to low ://a
c
itiswellestablishedthatlowtemperatureconditionscauseleaf temperature (Bigot and Boucaud, 1996; Fennell and ad
e
dehydrationinsensitiveplants(Pardossietal.,1992;Janowiak Markhart, 1998; Aroca et al., 2001, 2003, 2005; Vernieri m
ic
and Markowski, 1994; Aroca et al., 2001; Nagasuga et al., et al., 2001; Nagasuga et al., 2011). Based on HgCl2 .ou
2011). As for other stresses, this leaf dehydration is caused by experiments, it was hypothesized that this recovery could p
.c
the imbalance between water lost by leaf transpiration and be caused by an enhancement of aquaporin activity (Aroca om
water uptake by roots (Pardossi et al., 1992; Aroca et al., et al., 2001). Aroca et al. (2005) found that a maize low /jx
b
2001; Vernieri et al., 2001). Hence, although the transpiration temperature-tolerant genotype accumulated PIP proteins in /a
rate decreases under low temperature conditions because of its roots after 3 d of exposure to 5 (cid:1)C, concomitantly with rticle
a decrease in the vapour pressure difference (VPD) between an increase in the phosphorylation state of the PIP2 -a
b
s
the leaf surface and the atmosphere (Aroca et al., 2003), proteins. This PIP accumulation was correlated with even tra
stomataofthesensitiveplantsremainopen,whilethoseofthe higher L values of the low temperature-treated maize plants. ct/6
tolerant plants close more rapidly (Aroca et al., 2001, 2003; Aquaporin phosphorylation has been shown to enhance 3
/1
Bloom et al., 2004). At the same time, root water uptake also aquaporinactivity(Maureletal.,1995)bykeepingaquaporin /4
3
decreases drastically when the temperature goes down, poresintheopenstate(DanielsandYeager,2005;Tornroth- /5
5
5
because of the decrease in the VPD (Aroca et al., 2003) and Horsefield et al., 2006). Aroca et al. (2005) also found the 9
3
the increase in the viscosity of water (Bloom et al., 2004). same PIP aquaporin response in a low temperature-sensitive 6 b
y
However, the increase in water viscosity cannot fully explain maize genotype, which kept its L at very low levels during g
u
the decrease in the root water uptake rate (Wan et al., 2001; low temperature stress. So, the response of PIP aquaporins e
s
Bloom et al., 2004). Also, L decreases faster than stomatal to low temperature stress was not the only explanation for t o
n
conductance when only the roots were subjected to low the different L behaviour between the sensitive and the 3
0
temperature stress (Wan et al., 2001). So, the reduction of L tolerant maize genotypes. Aroca etal. (2005)alsofoundthat M
a
under low temperature conditions not only has a physical therootmembranesofthesensitivegenotypewereinjuredby rc
h
explanation, but also has biological–metabolic causes. Thus, the low temperature treatment. Hence, to tolerate low 2
0
1
based on Arrhenius plot studies (plotting the logarithmic temperature stress it was not sufficient to accumulate more 9
values of L against the inverse of temperature in Kelvin PIP proteins in the root membranes. The tolerant genotype
degrees), it has been suggested that the decrease in L upon also possessed robust mechanisms against membrane injury
exposuretolowtemperaturescouldbecausedbyaninhibition causedbylowtemperatureconditions.
of aquaporin activity (Wan et al., 2001; Murai-Hatano et al., In agreement with the accumulation of PIP proteins in
2008;Ionenkoetal.,2010).Thesestudieswereperformedwith rootsduringlowtemperatureperiods,otherresearchersalso
excisedrootssubjectedtolowtemperatureconditions.Infact, found that some plants grown at low temperatures had
under high irradiance conditions that induced higher transpi- higher L than plants grown at higher temperatures, when L
rationrates,thedecreaseinLofrootcellscausedbylowroot was measured at the higher temperatures (Bigot and
temperature was higher, and an increase in the water flowing Boucaud, 1994; Wan et al., 1999; Lee et al., 2005b). Also,
bytheapoplasticpathwasalsoobserved(Leeetal.,2008). Matsumoto et al. (2009) found that rice plants overexpress-
In some species or in plants grown under particular ing one PIP1 aquaporin were more tolerant to low
conditions before the low temperature treatment is applied, temperature stress than untransformed plants. So, it seems
Root water uptake regulation | 49
that accumulation of PIP proteins is crucial to tolerate low different experimental set-ups. Araki (2006) found that
temperaturestress. soybean plants only decreased their L values when, besides
However, other factors besides PIP aquaporin expression low O partial pressure in the soil, it was accompanied by
2
or abundance may govern L during low temperature an elevated CO partial pressure. However, CO partial
2 2
periods. Indeed, Lee et al. (2005b) found that a low pressure is usually not recorded in flooding experiments
temperature-sensitive plant species (Cucumis sativus) accu- (Table 2). Thus, CO accumulated during flooding condi-
2
mulated more suberin in both root exo- and endodermis tions by soil root respiration could be transformed to its
than a tolerant species (Cucurbita ficifolia). This higher acid form (H CO ), transported to the cytoplasm of root
2 3
suberin accumulation was correlated with lower L values cells, and inhibit aquaporin activity. In fact, cytosolic
under low temperature conditions of the sensitive species. acidification is one of the main causes of the inhibition of L
Moreover, Lee et al. (2005a) also observed a more pro- caused by anaerobiosis resulting from flooding conditions
nounced and constant increase in the double bond index of (Tournaire-Rouxetal.,2003),asaresultoftheprotonation
the root plasma membrane in C. ficifolia plants than in that of a histidine residue in loop D of PIP proteins. However,
of C. sativus under low temperature conditions. Such an the exact mechanism of L inhibition by CO is still
2
D
increase was caused by raising the amount of linolenic acid unknown. o
w
and by diminishing the amount of stearic acid. The increase Theinhibitionofaerobicrespirationbyfloodingmayalso n
lo
in the double bond index could be correlated with the cause the inhibition of L (Kamaluddin and Zwiazek, 2001; a
d
e
higherLobservedinC.ficifoliathaninC.sativusunderlow Tournaire-Roux et al., 2003). However, how the accumula- d
temperature conditions (Lee et al., 2005b; Lo´pez-Pe´rez tion of several toxic compounds in the root cells, such as fro
m
et al.,2009). ethanol, acetaldehyde, or lactic acid, under flooding condi- h
Insummary,althoughtheinvolvementofPIPaquaporins tions(Mustroph et al., 2006; Zaidi et al., 2007) may affect L ttps
seemstobecrucialtomaintainrootwateruptakeunderlow has not been explored yet. Plants adapted to withstand ://a
c
temperature conditions and avoiding leaf dehydration, floodingconditionsareabletodevelopsuberindepositionsin ad
e
other aspects contributing to the regulation of root water the exo- and/or endodermis to avoid radial O loss from the m
2 ic
uptake are also involved, including maintenance of mem- root surface (De Simone et al., 2003; Enstone and Peterson, .o
u
brane integrity, degree of fatty acid saturation, suberin 2005).Thissuberindepositioncouldalsopotentiallydecrease p
.c
content, or cytoplasmic acidosis. Therefore, more research L values under flooding conditions (Ranathunge and om
is needed to elucidate how these factors contribute to the Schreiber, 2011). Ranathunge et al. (2011) recently found /jx
b
regulation of root water uptake properties during low that these suberin depositions in rice roots do not alter L /a
temperatureperiods. values but decrease solutetransport to the xylem. Moreover, rticle
the response of the overall L to flooding conditions depends -a
b
s
on the main radial water transport pathway used by each tra
Root water uptake under flooding conditions plant species. Namely, in species such as lupins in which ct/6
radial water transport is dominated by the apoplastic path, 3
/1
It is well documented that flooding paradoxically can cause floodingstressdidnotchangeL.Incontrast,inwheatplants, /4
3
leafdehydration(Ruiz-Sa´nchezetal.,1996;Domingoetal., in which the cell-to-cell path dominates radial water trans- /5
5
5
2002; Nicola´s et al., 2005). However, this symptom of port,floodingstressdecreasesL(Bramleyetal.,2010). 9
3
flooding does not always appear, and depends on the soil As shown in Table 2, in some special circumstances an 6 b
y
O2 and CO2 partial pressures and on the plant species up-regulation of L after the initial decrease was observed g
u
(Blanke and Cooke, 2004; Araki, 2006). In fact, one of the (Else et al., 1995; Gibbs et al., 1998). At the same time, e
s
problemswithsummarizingtheeffectsoffloodingonplants some flooding-tolerant species exposed for several days to t o
n
and their water relations is the wide diversity of treatments flooding conditions are able to develop new adventitious 3
0
employed, different soil O partial pressures, and no record rootswithhighLvalues(IslamandMacDonald,2004).The M
2 a
of the soil CO concentration in most of the studies (Araki, recovery of L values or the high L observed in adventitious rc
2 h
2006;Table2).Themostcommoneffectoffloodingstressis rootsoftamaracktrees(IslamandMacDonald,2004)could 2
0
1
a reduction in leaf transpiration; that is, an increase in be caused by the accumulation of aquaporins in their cell 9
stomatal closure (Blanke and Cooke, 2004; Yetisir et al., membranes. Thus, although stomatal conductance would
2006; Atkinson et al., 2008), most probably mediated by remain low and consequently apoplastic water flow would
chemical signals (Jackson et al., 2003; Araki, 2006; Else be restricted, cell-to-cell water flow could be favoured by
et al., 2006). However the exact nature of the possible the accumulation of aquaporins. However, only the report
chemical signals is still unknown. In contrast, initial ofZouetal.(2010)foundanup-regulation oftheexpression
stomatal closure could be attributed to leaf dehydration in ofonePIP1geneafterprolongedfloodingconditionsinroots
some species(Else etal., 2001). of maize plants. Most recently, Rodr´ıguez-Gamir et al.
At the same time that stomatal conductance is restricted (2011) found a down-regulation of two PIP aquaporin genes
by flooding conditions, L is also changed—usually decrea- of Carrizo citrange plants after 35 d of flooding, correlating
sed—uponexposuretoflooding.Inseveralcasesnochanges witha large decrease inL. Asfar asisknown, no otherdata
or even an overshoot have been observed (Table 2). As about flooding regulation of root aquaporins at the gene or
noted above, these different results could be caused by proteinlevelsareavailable.
50 | Aroca et al.
Table2. SummaryofhowdifferentfloodingtreatmentsmodifyLindifferentplantspecies
pO andpCO indicatepartialpressuresofO andCO ,respectively.
2 2 2 2
Species L [O ]orpO [CO ]orpCO Source
2 2 2 2
Triticumaestivum RootandcellLDOWN 50lM Notdetermined Bramleyetal.(2010)
LupinusluteusandLupinusangustifolia RootLUNCHANGED,CellLDOWN 50lM Notdetermined Bramleyetal.(2010)
Glycinemax RootLUNCHANGED 2kPa 0.4kPa Araki(2006)
Glycinemax RootLDOWN 2kPa 2kPa Araki(2006)
Piceamariana RootLDOWN Notdetermined Notdetermined IslamandMacDonald(2004)
Larixlaricina RootLUNCHANGED Notdetermined Notdetermined IslamandMacDonald(2004)
Arabidopsisthaliana RootLDOWN Notdetermined Notdetermined Tournaire-Rouxetal.(2003)
Ricinuscommunis RootLDOWN 2–12kPa Notdetermined Elseetal.(2001)
Gerberajamesonii RootLDOWN 190lM Notdetermined Olivellaetal.(2000)
Zeamays RootLDOWNTRANSIENTLY 50lM Notdetermined Gibbsetal.(1998)
D
Solanumlycopersicum RootLUNCHANGED Notdetermined Notdetermined Jacksonetal.(1996) o
w
Solanumlycopersicum RootL,initialDOWN,laterUP 0–8kPa 9–12kPa Elseetal.(1995) n
lo
Zeamays RootLDOWN 0–13lM Notdetermined BirnerandSteudle(1993) a
d
Vacciniumcorymbosum RootLDOWN Notdetermined Notdetermined DaviesandFlore(1986) e
d
fro
m
h
In summary, although the most common effect of flood- been observed (Rodr´ıguez-Gamir et al., 2011). Hence, it is ttp
s
ing in root water transport properties is the inhibition of L, possible that ABA may regulate, at least in part, L changes ://a
and the molecular features of such inhibition have been under stress conditions. However, ABA addition and ca
d
elucidated (Tournaire-Roux et al., 2003), several aspects of drought stress usually have opposite effects on L. Thus, e
m
the regulation of L during flooding conditions are still while ABA usually increases L, drought inhibits it (Aroca ic
.o
unresolved. These open questions would include, among et al., 2006). This apparent contradiction could possibly be up
others, which chemical compounds really inhibit L during explained by assuming that exogenous application of ABA .co
m
flooding and what are the molecular aspects of the recovery to the roots causes an excess of ABA or a different cellular /jx
b
of L observed in some species at late stages of flooding location of the ABA (Aroca et al., 2003). Nevertheless, /a
stress. under some specific drought conditions, an increase in L rtic
le
values has been observed (Singh and Sale, 2000; Siemens -a
b
and Zwiazek, 2004), although in these studies ABA levels s
tra
were not determined. c
Signals regulating root water uptake under t/6
Most recently, Wan (2010) found that external applica- 3
stress conditions /1
tion of ABA inhibited the negative effect of NaCl on cell L, /4
3
The concentration of a number of molecules increases in and explained this by suggesting that ABA promoted cell /5
5
root cells upon exposure to environmental stresses. Among osmotic adjustment. However, no direct measurements 59
3
them, the focus here is on some plant hormones [abscisic supporting that osmotic adjustment were presented. Exoge- 6 b
acid (ABA), ethylene (ET), and salicylic acid (SA)] and on nous ABA also modulates root PIP aquaporin expression y g
ROS. andproteinabundance(Jangetal.,2004;Arocaetal.,2006, ue
s
It is well known that ABA modifies root hydraulic 2008b; Mahdieh and Mostajeran, 2009; Ruiz-Lozano et al., t o
n
properties. The most common effect is an increase in L 2009). When expression of four PIP genes was studied in 3
0
whenABAisaddedtotherootmedium(Zhangetal.,1995; ABA-deficient tomato plants, it was found that under well- M
a
Aroca, 2006; Mahdieh and Mostajeran, 2009; Ruiz-Lozano wateredconditions,twoPIPgenesremainedunchangedand rc
h
etal.,2009).Nevertheless,insomecasesnoeffect(Wanand two other PIP genes were up-regulated by ABA depletion. 2
0
Zwiazek, 2001) or even a decrease in L (Aroca et al., 2003) In contrast, under drought conditions, three PIP genes were 19
was observed. The most robust evidence about the role of down-regulated and only one gene was up-regulated (Aroca
ABA in regulating L comes from studies of ABA-deficient et al., 2008a). However, no protein data are available from
plants or ABA-overproducing plants. Thus, ABA-deficient this study. Hence, it is clear that ABA is involved in the
tomato plants have lower whole-plant hydraulic conduc- response of L and PIP aquaporins to different abiotic
tance, as well as a lower root exudation rate (Nagel et al., stresses, although the mechanism behind such regulation is
1994). Also, Thompson et al. (2007) found that tomato still far from being understood.
plants overproducing ABA had higher L values than wild- ET,anotherstress-relatedplanthormone,couldalso play
type plants. ABA is known to accumulate in root cells a role in the regulation of root water uptake under several
exposed to abiotic stresses such as drought (Simonneau abiotic stress conditions. It is known that ET levels vary
et al., 1998), salt (Jia et al., 2002), low temperature (Aroca under different abiotic stress conditions such as drought
etal.,2003),orflooding(Olivellaetal.,2000).Inthecaseof (Liang, 2003), salt (Quinet et al., 2010), or flooding (Huang
flooding stress, a decrease of root ABA contents has also et al., 1997). For example, Kamaluddin and Zwiazek (2002)
Root water uptake regulation | 51
aquaporin pores (Ye and Steudle, 2006), or formation of
plasma membrane vesicles containing PIP aquaporins
(Boursiac et al., 2008) have been postulated. However, in
specific plant species or genotypes (more precisely, plants
tolerant to low temperature conditions), no effect of
exogenous H O on L was observed (Aroca et al., 2005;
2 2
Rhee et al., 2007). In addition, Benabdellah et al. (2009)
foundthatlowconcentrationsofexogenousH O increased
2 2
L in Phaseolus vulgaris plants. Consequently, ROS may
serve as signals in controlling L behaviour under abiotic
stress conditions, stimulating or inhibiting L depending on
their cellular concentration. This hypothesis is also sup-
ported by the fact that the L response to ABA is modified
by the addition of antioxidants (Aroca, 2006). Obviously,
D
moreresearchisneededinordertoascertainhowROSmay o
w
be involved inL regulation under severalstress conditions. n
lo
a
d
Fig.2. Diagramshowingwhichcellcomponentsaremodulated ed
byenvironmentalstresses,andhowtheinteractionamongthese fro
Concluding remarks m
componentsmaymodulatetherootwateruptakerateundersuch h
stresses.Othercomponentssuchasrespirationorprotein It is clear that root water uptake is crucial to overcoming ttps
phosphorylationwhichdonotappearinthefiguremayalso abiotic stress conditions and that the expression of PIP ://a
c
influencerootwateruptakerate. aquaporins is an important factor that regulates L under ad
e
stress conditions. However, it is also clear that there are m
and Islam et al. (2003) found an enhancement of L values many unknown processes that affect root water uptake rate ic.o
u
byanexogenousapplicationofETinseveraltreespecies.In during and after environmental stresses. How aquaporins p.c
contrast, YS Li et al (2009) found a negative effect of ET besides PIPs may regulate L and stress tolerance is almost om
application on L values in Medicago falcata plants. No unexplored. Completely unresolved is the nature of the /jx
b
oEtTh.erThdearteafoarree,tahveaciloanbtlreasatbinogutreLsurltesgduelastciroibnedbyabeoxvoegecnoouulds cthelelruelairssisgonmalestihnaftomrmeadtiiaotnethoenfihnoalwresapqounaspeoorifnL,gaelntehsouagrhe /article
be caused by different concentration, time of exposure, or, regulatedunderstressconditionsandhowaquaporinactivity -ab
s
simply, the different plant species used. Qaderi et al. (2007) ismodulated.Nevertheless,asshowninFig. 2, environmen- tra
found that canola plants with low levels of ET production talstressesmaymodifyanumberofcellularpropertiessuch ct/6
have lower L values under non-stressed conditions. How- as osmolytes (quantity and quality), cytoplasmic pH, or 3/1
ever, no data about the effect of ET on PIP aquaporin water content, which may also modify the concentration of /4
3
expression at the root level are available. Another stress- other compounds such as ROS or hormones. The interac- /55
5
relatedplanthormonethatregulatesLisSA.Boursiacetal. tion among these cell changes and other as yet unknown 9
3
(2008) found that exogenous SA inhibited L in Arabidopsis biochemical changes may modify suberin deposition and 6 b
y
plants by causing invaginations of plasma membranes aquaporin activity leading to the observed L regulation. g
u
containing PIP proteins, as occurs under salt stress con- Obviously,thepossiblecontributionofeachofthepotential e
s
ditions. Moreover, Volobueva et al. (2004) found that SA mechanisms behind regulation of root water uptake under t o
n
treatment inhibited symplastic water transport in maize abiotic stress conditions should be the focus of future 3
0
roots. Apartfrom theaboveresults,no more informationis investigations. M
a
available about how other plant hormones could regulate To bring clarity to this field it will be necessary to make rc
h
root water uptake under abiotic stressconditions. more extensive use of mutants in which the expression of 2
0
1
Other groups of molecules that may govern root water specific aquaporinsis is down-regulated. It is also necessary 9
uptake under abiotic stress conditions are the ROS. ROS to know which aquaporins are expressed in which cell types
are generated in root tissues under different abiotic stress so that the results obtained with those mutants can be
conditions (Blokhina et al., 2001; Aroca et al., 2005; interpreted. To create the tools necessary to make progress,
Katsuhara et al., 2005; Bian and Jiang, 2009). Among researchers will need to make transgenic plants with cell
ROS, hydrogen peroxide (H O ) is the most studied type- or tissue-specific promoters.
2 2
molecule in relation to root water uptake properties (Lee
et al., 2004; Aroca et al., 2005; Ye and Steudle, 2006; Rhee
et al., 2007; Boursiac et al., 2008; Benabdellah et al., 2009).
Acknowledgements
In the earlier studies of Lee et al. (2004) and Aroca et al.
(2005), it was shown that exogenous application of H O TheauthorsthankProfessorM.J.Chrispeels(Universityof
2 2
inhibited cell and root L, respectively. Several mechanisms California San Diego) for editing the manuscript. The work
including membrane damage (Aroca etal.,2005), closure of at our laboratory is supported by MICIN-FEDER
52 | Aroca et al.
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root-derivedacetaldehydeandethanolinForsythia.Environmentaland
ExperimentalBotany64,196–205.
AzaizehH,GunseB,SteudleE.1992.EffectsofNaClandCaCl on
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