plants-11-02174.pdf

Citation:Bramley,H.;Ranawana,S.R.W.M.C.J.K.;Palta,J.A.;Stefanova,K.;Siddique,K.H.M.TranspirationalLeaf Cooling Effect Did NotContribute Equally to BiomassRetention in Wheat Genotypes underHigh Temperature.Plants 2022,11,2174.https:/doi.org/10.3390/plants11162174Academic Editor:Daniela TronoReceived:7 July 2022Accepted:18 August 2022Published:21 August 2022Publishers Note:MDPI stays neutralwith regard to jurisdictional claims inpublished maps and institutional affil-iations.Copyright:2022 by the authors.Licensee MDPI,Basel,Switzerland.This article is an open access articledistributedunderthetermsandconditions of the Creative CommonsAttribution(CC BY)license(https:/creativecommons.org/licenses/by/4.0/).plantsArticleTranspirational Leaf Cooling Effect Did Not ContributeEqually to Biomass Retention in Wheat Genotypes underHigh TemperatureHelen Bramley1,2,*,S.R.W.M.Chandima J.K.Ranawana1,3,*,Jairo A.Palta1,4,Katia Stefanova1and Kadambot H.M.Siddique11The UWA Institute of Agriculture,The University of Western Australia,Perth,WA 6001,Australia2Plant Breeding Institute,School of Life and Environmental Sciences,The University of Sydney,Narrabri,NSW 2390,Australia3Department of Export Agriculture,Faculty of Animal Science and Export Agriculture,Uva Wellassa University,Badulla 90000,Sri Lanka4CSIRO Agriculture,Private Bag No.5,Wembley,WA 6913,Australia*Correspondence:(H.B.);chandimauwu.ac.lk(S.R.W.M.C.J.K.R.)Abstract:Hightemperatureandwaterdeficitarethemostcriticalyield-limitingenvironmentalfactorsfor wheat in rainfed environments.It is important to understand the heat avoidance mechanisms andtheir associations with leaf morpho-physiological traits that allow crops to stay cool and retain highbiomass under warm and dry conditions.We examined 20 morpho-physiologically diverse wheatgenotypes under ambient and elevated temperatures(Tair)to investigate whether increased water useleads to high biomass retention due to increased leaf cooling.An experiment was conducted underwell-watered conditions in two partially controlled glasshouses.We measured plant transpiration(Tr),leaf temperature(Tleaf),vapor pressure deficit(VPD),and associated leaf morpho-physiologicalcharacteristics.High water use and leaf cooling increased biomass retention under high temperatures,but increased use did not always increase biomass retention.Some genotypes maintained biomass,irrespective of water use,possibly through mechanisms other than leaf cooling,indicating theiradaptation under water shortage.Genotypic differences in leaf cooling capacity did not alwayscorrelate with Tr(VPD)response.In summary,the contribution of high water use or the leaf coolingeffect on biomass retention under high temperature is genotype-dependent and possibly due tovariations in leaf morpho-physiological traits.These findings are useful for breeding programs todevelop climate resilient wheat cultivars.Keywords:abiotic stress;leaf temperature;morpho-physiological characteristics;water use1.IntroductionCrop productivity under the projected increased intensity and frequency of extremeclimate events,including high temperature,vapor pressure deficit(VPD),and droughtspells,needsgeneticimprovementstargetingspecificenvironmentalconditions.Identifyinggenotypic variability in morpho-physiological responses to environmental conditionsand the underlying mechanisms contributing to those variable responses are importantprerequisites for genetic improvement.Wheat is highly sensitive to heat stress 1,2,and increasing air temperature(Tair)threatens wheat production 3,4.High temperatures can negatively affect plant growthand development and reduce biomass accumulation leading to yield penalties 57.Shortor long-term exposure to high ambient temperatures(35C)can significantly reducewheat yield 8,9 due to accelerated senescence 10,shortened grain-filling duration,re-stricted carbon assimilation 11,pollen sterility 12,floret abortion 13,and infertility 14.Tolerance to high temperatures has been widely studied and mechanisms identified,es-pecially those supporting better photosynthetic capacity and longer grain-filling periods,Plants 2022,11,2174.https:/doi.org/10.3390/plants11162174https:/ 2022,11,21742 of 22such as stay green 15,16,reduced respiratory O2consumption under day 17 and nightwarming 18,and remobilization of stem reserves 19.Moreover,studies have demon-strated that genetic improvements in heat tolerance can be made through the incorporationof some of these traits from wild relatives of wheat 15,16.Although improving heat tolerance is clearly important for wheat production,otherstrategies of adaptation may be just as important,but have been less explored 20,21.Forexample,less stress under high temperatures may be experienced through mechanismsthat help prevent overheating,called“heat avoidance”22.Transpiration(Tr)is one suchheat avoidance mechanism through its contribution to leaf cooling 2325.Tris a complexbiophysical process where water evaporates into the surrounding air through stomata.This liquid-to-vapor conversion requires energy supplied by the heat energy absorbedby the leaf 26.During Tr,considerable heat is dissipated from leaves allowing themto remain several degrees cooler than Tair2729.Therefore,genotypes that use morewater through Trmay avoid heat stress and be more productive under higher temperaturesby maintaining cooler canopies than those that use less water.However,the role of Trin regulating plant temperature is controversial.Some studies have suggested that theTrcontribution(latent heat loss)for regulating plant temperature is less than other heatdissipation mechanisms,especially under limited water conditions 3032.Conversely,other studies have suggested that Trplays a major role in dissipating heat energy andlowering leaf temperature 29,3335.However,comparing leaf and air temperatures mayunderestimate the role of Trin leaf cooling as the absorption coefficients differ for leafand air,as plants have a relatively higher capacity to absorb light than air 34.Thesecontrasting views on the role of Trin ameliorating leaf temperature necessitate closerexamination of this phenomenon to determine whether this could be a suitable trait totarget for wheat breeding.Grain yield is a function of biomass and the harvest index(HI).Therefore,grainyield can be increased either by increasing the biomass,or the HI,or both 36.A highpositive correlation between grain yield and accumulated biomass was reported in severalcrops including rice,wheat,and maize 3739.Modern cereal breeding programs havehighlighted the possibility of increasing grain yield by selecting genotypes with higherbiomass production 4042.However,it is challenging to increase biomass accumulationparticularly under sub-optimum growing conditions.Therefore,improvement in grainyield potential through increased biomass production can be achieved under favorableconditions,and maintaining a high HI could be more important than increasing biomassproduction for higher grain yield under sub-optimum conditions 43.Biomass has beenreported to decrease substantially under high temperature and the decrease in biomassunder high temperature may be attributed to accelerated leaf chlorophyll degradation,reduced leaf photosynthesis,and a smaller leaf area index 44.Moreover,variationin biomass accumulation is associated with differential soil water extraction by roots,variation in evapotranspiration(ET),and differences in net carbon assimilation per unitof water transpired(Transpiration Efficiency)or ratio of biomass to ET 45,46.Biomassaccumulation tends to be linearly related to plant Tr47,48.Thus,effective water-use via Tris important for increasing biomass under water stress 49,50.However,using more waterto maintain cooler canopies and increase biomass accumulation is problematical becausemost wheat production occurs under rainfed conditions in water-limited environments,where water scarcity is expected to increase 5153.Therefore,it is critical to determinewhether increased water use via Tralways contributes to high biomass accumulation andidentify genotypes that can maintain cooler canopies and high biomass irrespective ofwater use.Leaf temperature(Tleaf)has been associated with several plant traits,including stom-atal conductance(gs)54,capacity of vascular system to support Tr55,plant waterstatus 56,rooting depth 57,and yield 58,59.Cooler canopies are considered to indicatebetter hydration status and greater capacity to extract water from deeper soil profiles 60,but a direct link between these traits has not been studied.Thus,Tleafis being widely usedPlants 2022,11,21743 of 22as a selection tool for screening heat-and drought-tolerant genotypes,as it reflects genotypefitness in a given environment 55,58,61.However,the relationship between Tleafand Triscomplex as both traits are influenced by a multitude of morpho-physiological and environ-mental variables,including leaf glaucousness,canopy architecture,VPD,radiation,andsoil water availability 54,55,6264.Wheat genotypes may not respond equally to elevatedtemperature and temperature-coupled environmental changes due to differences in theirmorpho-physiological attributes.Systematic characterization of the morpho-physiologicaldifferences and changes in Tr,Tleaf,and biomass accumulation among wheat genotypeswill improve our understanding of these complex relationships.This study aimed to investigate the relationship between Tr,Tleaf,and biomass pro-duction under elevated temperature in a morpho-physiologically diverse set of 20 wheatgenotypes.We aimed to determine whether increased water use under high temperatureimproves maintenance of shoot biomass retention(smaller reduction in biomass)in wheatdue to increased leaf cooling.It was expected that elevated temperature would reducebiomass accumulation due to high temperature-induced senescence and genotypes withhigher Trwould be cooler and thus,have slower leaf senescence and better biomass reten-tion.It is hypothesized that biomass accumulation is less reduced in genotypes with highwater use as canopy cooling inhibits leaf senescence.The study also aimed to elucidate theresponses of Tr,Tleaf,and associated morpho-physiological characteristics in warm and dryatmospheric conditions and determine whether variable responses in the instantaneousrate of Trto VPD affect Tleafregulation in wheat.2.Results2.1.MorphoPhysiological Responses under Elevated Temperature2.1.1.Daily TrThere was no genotypetemperature regime interaction for daily Trper plant inBatch 01(p=0.731;Figure 1)or Batch 02(p=0.604;Figure 1).The average daily Trdifferedsignificantly between genotypes in both batches(Batch 01,p=0.006;Batch 02,p 0.0001).Plants 2022,11,x FOR PEER REVIEW 3 of 24 Leaf temperature(Tleaf)has been associated with several plant traits,including sto-matal conductance(gs)54,capacity of vascular system to support Tr 55,plant water status 56,rooting depth 57,and yield 58,59.Cooler canopies are considered to indicate better hydration status and greater capacity to extract water from deeper soil profiles 60,but a direct link between these traits has not been studied.Thus,Tleaf is being widely used as a selection tool for screening heat-and drought-tolerant genotypes,as it reflects geno-type fitness in a given environment 55,58,61.However,the relationship between Tleaf and Tr is complex as both traits are influenced by a multitude of morpho-physiological and environmental variables,including leaf glaucousness,canopy architecture,VPD,radia-tion,and soil water availability 54,55,6264.Wheat genotypes may not respond equally to elevated temperature and temperature-coupled environmental changes due to differ-ences in their morpho-physiological attributes.Systematic characterization of the mor-pho-physiological differences and changes in Tr,Tleaf,and biomass accumulation among wheat genotypes will improve our understanding of these complex relationships.This study aimed to investigate the relationship between Tr,Tleaf,and biomass pro-duction under elevated temperature in a morpho-physiologically diverse set of 20 wheat genotypes.We aimed to determine whether increased water use under high temperature improves maintenance of shoot biomass retention(smaller reduction in biomass)in wheat due to increased leaf cooling.It was expected that elevated temperature would reduce biomass accumulation due to high temperature-induced senescence and genotypes with higher Tr would be cooler and thus,have slower leaf senescence and better biomass reten-tion.It is hypothesized that biomass accumulation is less reduced in genotypes with high water use as canopy cooling inhibits leaf senescence.The study also aimed to elucidate the responses of Tr,Tleaf,and associated morpho-physiological characteristics in warm and dry atmospheric conditions and determine whether variable responses in the instantane-ous rate of Tr to VPD affect Tleaf regulation in wheat.2.Results 2.1.MorphoPhysiological Responses under Elevated Temperature 2.1.1.Daily Tr There was no genotype temperature regime interaction for daily Tr per plant in Batch 01(p=0.731;Figure 1)or Batch 02(p=0.604;Figure 1).The average daily Tr differed significantly between genotypes in both batches(Batch 01,p=0.006;Batch 02,p 0.05)in the average daily rate of Trbetween the two temperature regimes.Plants 2022,11,21744 of 22TheaveragedailyTrrangedfrom94.8gplant1d1inWyalkatchemto112.4 g plant1d1in Downey in Batch 01,and 117.5 g plant1d1in Kukri to 162.1 g plant1d1in Espada inBatch 02.The elevated temperature treatment(T2)significantly increased the average dailyTr(p 0.05,Figure 1).2.1.2.Leaf GlaucousnessThere were noticeable differences in the presence/absence of wax and the amountof wax deposition on leaf surfaces among genotypes(Figure 2).The cultivars Downey,Einkorn,Glossy-Huguenot,and Janz had no visual signs of glaucousness,except Janzunder T2,where some whitish/blue wax was deposited on the abaxial leaf surface,closeto the leaf base.T2 induced whitish/blue wax deposition on the adaxial leaf surface ofcultivar Magenta,relative to T1,where it only exhibited glaucousness on the abaxial sideof the leaf.Drysdale,Espada,Gladius,Glennson 81,Hartog,and RAC 875 leaves wereglaucous on both leaf surfaces under both temperature regimes.Plants 2022,11,x FOR PEER REVIEW 4 of 24 duration of the temperature treatment.Error bars indicate SEM;n=4.The letters“ns”indicate no significant difference(p 0.05)in the average daily rate of Tr between the two temperature regimes.The average daily Tr ranged from 94.8 g plant1 d1 in Wyalkatchem to 112.4 g plant1 d1 in Downey in Batch 01,and 117.5 g plant1 d1 in Kukri to 162.1 g plant1 d1 in Espada in Batch 02.The elevated temperature treatment(T2)significantly increased the average daily Tr(p 0.05,Figure 1).2.1.2.Leaf Glaucousness There were noticeable differences in the presence/absence of wax and the amount of wax deposition on leaf surfaces among genotypes(Figure 2).The cultivars Downey,Ein-korn,Glossy-Huguenot,an