Underwater Photosynthesis and Internal Aeration of Submerged

13 Pages·2013·0.29 MB·English

Underwater Photosynthesis and Internal
Aeration of Submerged Terrestrial Wetland
Plants
OlePedersenandTimothyD.Colmer
Abstract Submergenceimpedesplantgasexchangewiththeenvironment.Survival
depends upon internal aeration to provide O throughout the plant body, although
2
short-term anoxia can betolerated.Duringnights, plants relyonO entryfromthe
2
floodwaterandpO inrootsdeclinessothatsometissuesbecomeseverelyhypoxicor
2
even anoxic. Underwater photosynthesis is the main daytime O source and also
2
providessugars.Capacityforphotosynthesisunderwater,likeinair,isdeterminedby
available CO and light;however, slowdiffusioninwateroften limits CO supply.
2 2
Underwater photosynthesis in some wetland species is enhanced by gas films on
superhydrophobicleafsurfaces.Leafgasfilmsalsoincreasenight-timeO uptakeby
2
submergedplants.Floodingeventsareforecasttoincreaseandunderstandingofplant
submergence toleranceshouldenable predictions ofpossibleimpacts onvegetation
communitiesandalsoaidbreedingofimprovedsubmergencetoleranceinrice.
1 The Submergence Environment
The slow diffusion of gases in water compared with in air presents a challengeto
submergedterrestrialplants(Armstrong1979)asoxygen(O )andcarbondioxide
2
(CO ) uptake are greatly impeded. Diffusion of gases in water is approximately
2
10,000-foldslower than inair,sothatsince the diffusiveboundary layers (DBLs)
O.Pedersen(*)
FreshwaterBiologicalLaboratory,UniversityofCopenhagen,Universitetsparken4,3rdfloor,
2100Copenhagen,Denmark
InstituteofAdvancedStudies,TheUniversityofWesternAustralia,Crawley,WA6009,
Australia
SchoolofPlantBiology,TheUniversityofWesternAustralia,Crawley,WA6009,Australia
e-mail:[email protected]
T.D.Colmer
SchoolofPlantBiology,TheUniversityofWesternAustralia,Crawley,WA6009,Australia
J.T.vanDongenandF.Licausi(eds.),Low-OxygenStressinPlants,PlantCell 315
Monographs21,DOI10.1007/978-3-7091-1254-0_16,©Springer-VerlagWien2014
316 O.PedersenandT.D.Colmer
adjacent to surfaces are of similar thickness in both environments, the resulting
apparentresistancetogasexchangeis10,000-foldhigherwhenunderwater(Vogel
1994). Submerged aquatic plants have thus developed adaptive features of their
leavestoreducetheDBL,andalsotoreduceotherresistances(e.g.thincuticleand
thin leaves), to facilitate gas exchange in the aqueous environment (Sculthorpe
1967;Colmeretal.2011).
In addition to the slow diffusion of gases, the solubility of O in water is
2
relatively low; 1 L of air contains 33-fold more O than 1 L of water at 20 (cid:1)C at
2
sea level (Stumm and Morgan 1996). The amount of dissolved O in a particular
2
water body is determined by a combination of the water temperature and salinity
andthesurroundingO partialpressure(pO ).ThepO intheatmospheredecreases
2 2 2
with elevation (at atmospheric equilibrium, less O is dissolved in the water of a
2
mountain lake than at sea level) and increases with depth (the absolute pressure
increases with 101 kPa per 10 m depth). Temperature and salinity can differ
substantially in the various habitats of terrestrial wetland plants (e.g. freshwater
tohypersalinewetlands;near-freezingtowarmwatersat,e.g.40(cid:1)C).LikeforO ,
2
the solubility of CO also decreases with increasing temperature and salinity and
2
increases with pressure. The chemistry of CO in water is more complicated than
2
forO ,asCO reactswithwateritselfwhenitdissolvesandformsapH-dependent
2 2
(cid:3)
equilibriumwhereCO dominatesbelowpH6.3,HCO betweenpH6.3and10.2
2 3
and above pH 10.2 CO 2(cid:3) dominates and this form cannot be utilised by photo-
3
syntheticorganisms.
InadditiontosevereCO limitation,thephotosynthesisofinundatedplantscan
2
alsobelimitedbylight.Lightisattenuatedinanexponentialfashionduetowater
itself, but more importantly due to suspended particles, pigments in planktonic
algae and dissolved humic substances (Kirk 1994). In turbid floodwaters, light
absorption can be as much as 90 % in the upper 0.1 m, but more typical values
for a 90 % reduction of light penetration in floodwaters is 0.5–2 m (Vervuren
etal.2003;Winkeletal.2013).
2 Leaf Adaptations for Underwater Gas Exchange
LeafmorphologydeterminesDBLresistancestoexchangeofdissolvedgasesand
ions(MadsenandSand-Jensen1991).TheDBLresistancetoCO uptakereduces
2
underwater photosynthesis in submerged plants and is a large component of the
overallapparentresistancetogasexchangebetweenchloroplastsandthesurround-
ing floodwater (Black et al. 1981). Morphological traits that reduce the effective
DBLresistance,bydecreasingthedistancetothe‘leading-edge’(Vogel1994)and
thus reducing the path-length across the DBL, include leaf shapes of small, dis-
sected/lobedand/orstrap-likeleaves(Sculthorpe1967).Inaddition,aquaticleaves
lack trichomes thus facilitating water movement adjacent to the surfaces and so
avoiding development of thicker DBLs. Leaves of aquatic species also tend to be
UnderwaterPhotosynthesisandInternalAerationofSubmergedTerrestrial... 317
thin,inextremecasesbeingonlytwocelllayersthick,shorteninginternaldiffusion-
path lengths and thus reducing the overall resistance to CO diffusion to chloro-
2
plasts(MadsenandSand-Jensen1991;MaberlyandMadsen2002).
Inadditiontothesemorphologicaltraits,leavesofaquaticspeciesalsohavevery
reduced cuticles, or this layer can even be absent. Diffusion into and across the
epidermisisthepathwayfordissolvedgas-exchangeasaquaticleaveslackstomata
(Sculthorpe 1967), or if present, the stomata are non-functional (Pedersen and
Sand-Jensen 1992). Diffusion path-length to chloroplasts is also minimised by
having these organelles in all epidermal cells and in sub-epidermal cells the
chloroplastsarepositionedtowardstheexterior(Sculthorpe1967).
Submergedaquaticplantsalsodisplayphysiologicaladaptationstoincreasethe
CO concentration at Rubisco, the site of carboxylation; these are referred to as
2
carbon concentrating mechanisms (CCMs) (Maberly and Madsen 2002; Raven
(cid:3)
et al. 2008). In submerged aquatic plants, CCMs include HCO use (Prins and
3
Elzenga 1989), C (Magnin et al. 1997), C –C intermediates (Keeley 1999) and
4 3 4
CAMphotosynthesis(Keeley1998).CCMsincreaseunderwaternetphotosynthesis
(P ) in CO limited aquatic environments. In addition, CAM has been shown to
N 2
diminish photorespiration in the aquatic species, Isoetes australis (Pedersen
etal.2011b).
Leavesofterrestrialwetlandplantslackmostofthefeaturesdescribedabovefor
aquaticspeciesandsosufferfromlargerdiffusionresistancesthatlimitCO uptake
2
for photosynthesis when under water. Some terrestrial species, however, can
produce submergence acclimated leaves (Mommer and Visser 2005) and some
possess leaf gas films (Raskin and Kende 1983; Colmer and Pedersen 2008b),
Fig. 1; features which can also reduce the apparent resistance to CO uptake by
2
these species when submerged. Below, we evaluate in more detail underwater P
N
byleavesofterrestrialwetlandplants.
3 Underwater Photosynthesis in Leaves
of Terrestrial Plants
TheoverallbeneficialeffectsofaquaticleaftraitsforunderwaterP ,aswellasthe
N
generally poor performance of leaves of terrestrial plants, were clearly demon-
stratedinSand-Jensenetal.(1992).Theseauthorshighlightedthat:(1)underwater
P on a mass basis increased from terrestrial, then amphibious, to aquatic leaf
N
types; and (2) that Danish low-land stream waters commonly contain CO above
2
air-equilibriumvalues,allowingevensometerrestrialspeciestohaveadequateP
N
forgrowthwhensubmergedinthesehabitats.Thispioneeringstudyisconsideredin
detailinColmeretal.(2011).
Speciesofmanyterrestrialwetlandplantsproducenewleaveswhensubmerged
and these can display some acclimation to enhance underwater gas exchange
(Mommer et al. 2005, 2007). The best example is the 69-fold higher underwater
318 O.PedersenandT.D.Colmer
Fig. 1 Microelectrode set up in an experimental field pond at the International Rice Research
Institute(ThePhilippines)tomeasurerootpO duringcompletesubmergence(a),bubbleformation
2
duetoextensiveunderwaterphotosynthesis(b),andgasfilmonthesuperhydrophobicleafsurface
ofsubmergedrice,Oryzasativa(c).ThesystemwassetupwithO microelectrodespositionedinto
2
adventitious roots in the soil and then the field was flooded to completely submerge plants.
DatafromtheexperimentareshowninFigs.3and4.PhotosbyOlePedersen
P due to a reduction in cuticle resistance in Rumex palustris (Mommer
N
et al. 2006b). Mommer et al. (2007) found that seven terrestrial wetland species
formedathinnercuticleasaresponsetosubmergenceleadingtoenhancedunder-
water gas exchange, but the degree of this response was not correlated with
submergence tolerance. These acclimations in submerged leaves of terrestrial
species are much more subtle than the altered leaf development displayed by
some amphibious heterophyllous species, which produce true aquatic leaf types
whenunderwater(Nielsen1993).
Here, we consider for terrestrial wetland plants how rates of underwater P
N
compare with those in air. The few data available show that P under water is
N
substantiallylowerthaninair(Colmeretal.2011).RatesofunderwaterP varynot
N
only with species, but also with environmental conditions. Rice leaves at the
ambient CO of 70 mmol m(cid:3)3 in a submergence field pond at the International
2
RiceResearchInstitute(ThePhilippines)resultedinP underwateratonly5%of
N
the rate in air (Winkel et al. 2013). However, CO enrichment several-fold above
2
the level in these ponds has been recorded in flooded rice fields in Thailand;
20–180-fold air-equilibrium (Setter et al. 1987) and in India; 31–217-fold
UnderwaterPhotosynthesisandInternalAerationofSubmergedTerrestrial... 319
(Rametal.1999).At200mmolCO m(cid:3)3,underwaterP byricewas27%ofthat
2 N
in air (Pedersen et al. 2009). Similar to rice, at 200 mmol CO m(cid:3)3 Hordeum
2
marinumgrownathighmineralnutritionalsohadunderwaterP at28%ofthatin
N
air(Pedersenetal.2010).Bycontrast,field-collectedleavesofthreeotherwetland
species (Phalaris arundinacea, Typha latifolia and Phragmites australis) had
underwater P at 200 mmol CO m(cid:3)3 (Colmer and Pedersen 2008b) estimated to
N 2
beapproximately15%ofthatinair(Colmeretal.2011).
Inthecaseswhereunderwaterrespirationofthelaminahasalsobeenmeasured,
acrude24hC-balanceofthistissuecanbeestimated.At200mmolCO m(cid:3)3and
2
assuming12hlightand12hdarkness,apositiveC-balanceofabout100mmolC
m(cid:3)2 d(cid:3)1 is estimatedfor lamina ofrice (Pedersen et al. 2009).The C-balancesof
submergedlaminaoffourotherwetlandspeciescanbeestimatedalsoat200mmol
CO m(cid:3)3 and ranged from approximately 35 to 70 mmol C m(cid:3)2 d(cid:3)1; calculated
2
fromColmerandPedersen(2008b).Thus,althoughP underwaterissubstantially
N
lessthaninair,thelaminaC-balanceappearstobepositive.
Theimportanceofphotosynthesisduringsubmergenceisfurtherhighlightedby
enhanced plant survival when light is provided, e.g. rice (Adkins et al. 1990; Das
et al. 2009). Light also enhances survival during submergence of other wetland
species(Vervurenetal.1999,2003;Mommeretal.2006a).Similarly,survivalof
Arabidopsis thaliana was improved two- to threefold by light (16 h d(cid:3)1) as
comparedwithincontinuousdarkness(Vashishtetal.2011).Someshadingstudies
have found that survival of submerged rice was highest under moderate levels of
light(Adkinsetal.1990;Dasetal.2009).Adkinsetal.(1990)highlightedthatat
highlightextensivealgalgrowthresultsincompetitionwithriceforlightandCO
2
duringthedayandforO duringthenight.
2
In some situations, underwater photosynthesis will be CO limited, rather than
2
limited by light (Mommer and Visser 2005). For submerged terrestrial wetland
plants, CO limitation is severe when near air-equilibrium (approximately
2
10–15 mmol CO m(cid:3)3). Underwater photosynthesis only becomes CO saturated
2 2
at 100-fold concentrations higher than air-equilibrium in Phragmites australis
(ColmerandPedersen2008b)andat20-foldhigherconcentrationsforrice(Pedersen
etal.2009).Asdiscussedabove,CO enrichmentaboveair-equilibriumiscommon
2
in many water bodies, including in flooded rice fields in Thailand at 20–180-fold
air-equilibrium(Setter et al. 1987) and inIndia at 31–217-fold (Ram et al. 1999).
The beneficialeffects ofhigher dissolvedCO on submergence tolerance (growth
2
and/orsurvival)havebeendocumentedforrice(Setteretal.1989)andforHordeum
marinum(Pedersenetal.2010).Inthecaseofsubmergedrice,CO enrichmentto
2
approximately 290 mmol m(cid:3)3 enhanced by twofold the growth of two cultivars,
comparedwithwateratair-equilibriumwhichwouldhavecontainedapproximately
10mmolCO m(cid:3)3,at30(cid:1)C(Setteretal.1989).Thus,CO levelsinthefloodwaters
2 2
determine rates of underwater P with consequences for tissue sugar levels,
N
e.g. Hordeum marinum (Pedersen et al. 2010), O supply to roots,
2
e.g. Eriophorum angustifolium (Gaynard and Armstrong 1987), growth and ulti-
mately survival, e.g. rice and Hordeum marinum (Setter et al. 1989; Pedersen
et al. 2010). Hence, Pedersen et al. (2010) suggested that future assessments of
320 O.PedersenandT.D.Colmer
submergence tolerance in plants should be conducted at defined CO levels and
2
controlled environment treatments might require CO enrichment of the water to
2
betterreflectmanyfieldenvironments.
4 Leaf Gas Films and Underwater Photosynthesis
Leafsurfacehydrophobicity(i.e.waterrepellence)isafeaturethatshedsoffwater
inwetaerialenvironments(SmithandMcClean1989;BrewerandSmith1997)and
promotes ‘self cleansing’, enhancing leaf performance and reputably lowering
susceptibility to pathogens (Neinhuis and Barthlott 1997). Several terrestrial wet-
land plants possess superhydrophobic leaves that retain a thin gas film when
submerged (Fig. 1b, c) (Raskin and Kende 1983; Colmer and Pedersen 2008b).
Theleafgasfilmshavebeenshowntoenhanceunderwatergasexchange(CO and
2
O in light and O in darkness), functioning as a ‘physical gill’ similar to those
2 2
known for aquatic insects and spiders (Thorpe and Crisp 1947; Raven 2008;
Pedersen and Colmer 2012). CO that enters the gas film can rapidly diffuse to
2
stomata. By contrast, for leaves without gas films, a major proportion of the CO
2
and O entry might transverse the cuticle (Mommer et al. 2004). O (Frost-
2 2
Christensen et al. 2003) and CO (Frost-Christensen and Floto 2007) both can,
2
albeitrelativelyslowly,permeatecuticlesofamphibiousplants.
The beneficial effect of leaf gas films on underwater P was not only demon-
N
stratedbythemarkeddecreasesofP whenthegasfilmswereremoved(Fig.2),but
N
alsoleaveswithgasfilmshadhigherratesofunderwaterP thanleavesofspecies
N
withoutgas films(Colmer andPedersen2008b;Colmer etal. 2011).Atdissolved
CO concentrations ofrelevancetofieldconditions,underwater P wasenhanced
2 N
four- to fivefold by gas films on leaves of rice (Fig. 2). When gas films were
removedartificiallyfromleavesofcompletelysubmergedrice,tissuesugarlevels
declined (Pedersen et al. 2009; Winkel et al. 2013). Thus, leaf gas films enhance
underwaterP andsubmergencetolerance.
N
5 Sources of O in the Light
2
Several studies have documented that terrestrial plants survive complete submer-
gence better in natural light–dark-cycles compared with complete darkness
(Vervuren et al. 2003; Mommer et al. 2007; Vashisht et al. 2011). The enhanced
survival presumably results from a combination of better internal aeration (O
2
producedinphotosynthesis)aswellasthesugarsproduced.
Forsubmergedrice(Fig.3),rootaerationisgreatlyenhancedalreadysoonafter
sunrisewhereadventitiousrootpO increasesfrom<1to>10kPainlessthan2h.
2
The data also show that root pO continues to be a function of incoming light
2
throughout the day (transient reductions in light are followed by transient steep
UnderwaterPhotosynthesisandInternalAerationofSubmergedTerrestrial... 321
Fig.2 Underwaternetphotosynthesis(P )versusdissolvedCO forriceleafsegmentswithor
N 2
without gas films. Underwater P was measured as net O evolution from leaf segments of
N 2
approximately 2 cm2 in closed glass vials with a range of dissolved CO concentrations and
2
PARof350μmolphotonsm(cid:3)2s(cid:3)1(formethods,seePedersenetal.2013).Leafgasfilmswere
either intact or removed experimentally by brushing with a dilute detergent. Reproduced from
Pedersenetal.(2009)
declines in root pO ) and at dusk, root pO declines rapidly to predawn levels
2 2
(Fig.3).Similarrelationshipsbetweenlightandinternalaerationhavebeenshown
in several other in situ field studies both of aquatic plants (e.g. Greve et al. 2003;
Borum et al. 2005; Sand-Jensen et al. 2005; Holmer et al. 2009; Pedersen
etal.2011a;Richetal.2013)andcompletelysubmergedterrestrialwetlandplants
(Pedersenetal.2006;Winkeletal.2011).Therelationshipbetweenincominglight
(and thus underwater P ) is reinforced by the data analyses in Fig. 4a where root
N
pO is graphed against light. This example taken from the field study by Winkel
2
et al. (2013) demonstrates the strong dependence on light for root aeration of
completelysubmergedrice.
TransientpeaksintissuepO atdawncanoccurinsubmergedterrestrialwetland
2
plants.SuchpeaksintissuepO arelikelytoarisefromenhancedinitialP fuelled
2 N
by accumulated respiratory CO following a dark period with net respiration
2
(Waters et al. 1989;Colmer and Pedersen 2008a). In the case of rice, these peaks
occurred in artificial dark-light switches in laboratory experiments (Waters
etal.1989;ColmerandPedersen2008a)butwerenotobservedinfieldrecordings
of submerged rice in which O increased markedly but without a transient peak
2
(Winkeletal.2013).Interestingly,alargetransientpeakwasobservedinsitufora
stem-succulenthalophyte(Tecticorniapergranulata)submergedinasaltlakeeven
thoughtheincreaseinmorninglightwasmoregradualthanthesuddenswitchesin
laboratory experiments. The succulent tissues with impeded gas exchange with
the surrounding floodwater might have contributed to this dawn peak in
T. pergranulata (Pedersen et al. 2006). Regardless of species and environmental
conditions,anypeaksinpO areonlytransientastheunderwaterP soonbecomes
2 N
CO limited as determined by the rate of CO entry from the floodwater, so that
2 2
tissuepO decreasestoanewquasisteady-state.
2
322 O.PedersenandT.D.Colmer
Fig.3 Incidentlight(a)
androotpO ofcompletely
2
submergedrice(b)
measuredinsituinafield
experiment(Fig.1).AnO
2
microelectrodewasinserted
intotheadventitiousroot
approximately10mm
belowtheroot–shoot
junctionwhichwasabout
50mmbelowthesoil
surface.Dataextractedfrom
Winkeletal.(2013)forthe
firstfulldayof
submergence
Fig.4 RootpO asa
2
functionofincidentlight
duringtheday(a)andof
floodwaterpO duringthe
2
night(b)forricewhen
completelysubmergedina
fieldsituation(Fig.1).Data
shownareextractedfrom
Fig.3.Datareproduced
fromWinkeletal.(2013)
UnderwaterPhotosynthesisandInternalAerationofSubmergedTerrestrial... 323
The implications of dynamics in tissue pO are of interest to consider further.
2
Day-nightdynamicshavebeenshowntohaveconsequencesforenergymetabolism.
Duringlightperiods,rootsofcompletelysubmergedricehadadequateenergyforroot
extensionwhenphotosyntheticallyderivedO reachedroottips,whereasduringdark
2
periods O declined, root extension ceased and ethanolic fermentation occurred
2
(Waters et al. 1989). Increased night-time activity of pyruvate decarboxylase in
roots ofsubmerged rice(Mohanty and Ong 2003) supportsthe earlier observations
of ethanol production during dark periods (Waters et al. 1989) and presumably
contributes to survival of anoxia (Gibbs and Greenway 2003). An area requiring
study is whether the rapid morning increases in tissue pO result in any oxidative
2
stress,thisbeinganintriguingpossibilitysinceemphasishasbeenplacedonincreased
reactiveoxygenspecies(ROS)followingO re-entryuponde-submergence,e.g.for
2
rice (Ushimaru et al. 1994; Santosa et al. 2007). In addition, damage from ROS in
hypoxic tissues of submerged rice might also occur (Santosa et al. 2007), and the
possibleaggravationofsuchprocessesbyfluctuatingpO insubmergedriceshould
2
be evaluated. The dynamics in pO within tissues of submerged plants would also
2
presumably influence how putative O -sensing (Bailey-Serres et al. 2012) might
2
contributetoacclimationofplantsduringsubmergence.
6 Sources of O in the Dark
2
During night-time, completely submerged plants rely on an influx of O from the
2
surrounding floodwater to sustain aerobic respiration in shoots and roots. The O
2
initiallypresentintheaerenchymaatnightfallhasbeenshowntobeinsufficientto
sustain respiration; in Zostera marina, the O in the aerenchyma can only sustain
2
respiration for 8–13 min (Sand-Jensen et al. 2005). Figure 4b shows that internal
rootaerationofsubmergedriceduringthenightreliesonfloodwaterpO diffusing
2
intotheshootandfurtherdowntotheroots.Extrapolationoftheregressionlinein
Fig. 4b to the intercept on the x-axis suggests that even at this position measured
only 10 mm from the root–shoot junction, anoxia would occur if floodwater pO
2
haddecreasedbelowapproximately4.5kPa.However,rootpO willdependon,in
2
addition to floodwater pO , other environmental and plant factors. Firstly, the
2
second key environmental parameter after floodwater pO is mixing of the water;
2
flow/turbulence results in erosion of the DBLs around the leaves and thereby a
higher flux of O into the shoot at the same external bulk floodwater pO (Binzer
2 2
et al. 2005). Important plant factors include (1) internal resistance to longitudinal
O diffusion, determined by tissue porosity and the diffusion path-length
2
(Armstrong 1979), (2) respiration (also influenced by temperature) (Armstrong
1979), (3) radial O loss along the diffusion pathway (from roots but potentially
2
also the buried sheath bases (both dependent upon sediment demand for O and
2
whetherrootspossess abarrier toROL(Armstrong1979;Colmer 2003;Pedersen
etal.2011a)and(4)theshoot-to-rootratio,i.e.capacityofshootuptaketosatisfy
thesinkdemandinroots(andrhizomesifpresent)(Borumetal.2006).
324 O.PedersenandT.D.Colmer
LeafgasfilmshavebeenshowntoenhanceO uptakefromfloodwaterwhenin
2
darkness. Laboratory experiments with completely submerged rice showed that
quasisteady-staterootpO wasapproximately3.4kPa(10–15mmbehindtheroot
2
tip) and declined essentially to zero upon removal of the leaf gas films (Pedersen
etal.2009).Similarly,insitumeasurementsofrhizomepO inthetidalhalophyte,
2
Spartina anglica, showedthat during tidal inundation at night-time pO remained
2
higherinplantswithgasfilms(5–7kPa)thaninthosewherethegasfilmshadbeen
removed(approximately1kPa)(Winkeletal.2011).
7 Outlook
Underwater photosynthesis and internal aeration are crucial to plant survival of
submergence. Studies are few of underwater photosynthesis and O dynamics in
2
completely submerged terrestrial plants, whereas mechanisms of internal aeration
of below-ground organs are well understood. Underwater photosynthesis leads to
dynamic changes in pO within submerged plants as light availability changes
2
during the daytime and photosynthesis ceases each night. Plants must cope with
theselargeinternalfluctuationsinO andespeciallyroottissueswillhavelowpO
2 2
(or even be anoxic) during nights and a resupply of O in the daytime. Finally,
2
improved knowledge on C budgets of submerged terrestrial plants is needed to
provide a more complete understanding of the contribution of underwater photo-
synthesisbeyondthebenefitstosubmergedplantsofimprovedO status.Flooding
2
events are predicted to increase in the future, so understanding of submergence
toleranceshouldaideffortsaimedatbreedingofricetobetterwithstandfloods.
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