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Citation:Wang,X.-Q.;Zeng,Z.-L.;Shi,Z.-M.;Wang,J.-H.;Huang,W.Variation in Photosynthetic Efficiencyunder Fluctuating Light betweenRose Cultivars and its Potential forImproving Dynamic Photosynthesis.Plants 2023,12,1186.https:/doi.org/10.3390/plants12051186Academic Editors:Lorenzo Ferroniand Marek ZivcakReceived:31 January 2023Revised:9 February 2023Accepted:21 February 2023Published:6 March 2023Copyright:2023 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/).plantsArticleVariation in Photosynthetic Efficiency under Fluctuating Lightbetween Rose Cultivars and its Potential for ImprovingDynamic PhotosynthesisXiao-Qian Wang1,2,Zhi-Lan Zeng2,3,Zi-Ming Shi4,Ji-Hua Wang4and Wei Huang2,*1School of Life Sciences,Northwest University,Xian 710069,China2Kunming Institute of Botany,Chinese Academy of Sciences,Kunming 650201,China3University of Chinese Academy of Sciences,Beijing 100049,China4Flower Research Institute of Yunnan Academy of Agricultural Sciences,Kunming 650205,China*Correspondence:These authors contributed equally to this work.Abstract:Photosynthetic efficiency under both steady-state and fluctuating light can significantlyaffect plant growth under naturally fluctuating light conditions.However,the difference in photo-synthetic performance between different rose genotypes is little known.This study compared thephotosynthetic performance under steady-state and fluctuating light in two modern rose cultivars(Rose hybrida),“Orange Reeva”and“Gelato”,and an old Chinese rose plant Rosa chinensis cultivar,“Slaters crimson China”.The light and CO2response curves indicated that they showed similarphotosynthetic capacity under steady state.The light-saturated steady-state photosynthesis inthese three rose genotypes was mainly limited by biochemistry(60%)rather than diffusionalconductance.Under fluctuating light conditions(alternated between 100 and 1500mol photonsm2m1every 5 min),stomatal conductance gradually decreased in these three rose genotypes,while mesophyll conductance(gm)was maintained stable in Orange Reeva and Gelato but de-creased by 23%in R.chinensis,resulting in a stronger loss of CO2assimilation under high-lightphases in R.chinensis(25%)than in Orange Reeva and Gelato(13%).As a result,the variation inphotosynthetic efficiency under fluctuating light among rose cultivars was tightly related to gm.These results highlight the importance of gmin dynamic photosynthesis and provide new traitsfor improving photosynthetic efficiency in rose cultivars.Keywords:chlorophyll fluorescence;CO2assimilation;mesophyll conductance;photosyntheticlimitation;stomatal conductance1.IntroductionPlants use photosynthesis to convert light energy into stable chemical energy by photo-synthetic electron transport and the Calvin-Benson cycle.Plants with high photosyntheticefficiency usually have relatively fast growth rate and high levels of biomass and pro-ductivity.The light-saturated photosynthetic capacity under steady state is thought tobe the critical determinant of plant growth.For example,the higher steady-state photo-synthetic capacity in C4plants facilitates their higher productivity than C3plants underoptimal conditions 1,2.Photosynthesis can be limited by CO2diffusional conductanceand biochemical factors 3.Stomatal conductance(gs)and mesophyll conductance(gm)to-gether determine the CO2diffusion from air into chloroplast and thus influence chloroplastCO2concentration 48.Biochemical factors represent the capacity for the Calvin-Bensoncycle and photosynthetic electron flow.High values of gsand gmare the prerequisitesof high CO2assimilation rate(AN)in plants grown under high nitrogen condition andhigh light 6,8.Generally,photosynthetic capacity in angiosperms is mainly limited bybiochemical factors and gmrather than gswhen measured under favorite conditions 5,9.Plants 2023,12,1186.https:/doi.org/10.3390/plants12051186https:/ 2023,12,11862 of 15However,gmimposes the major limitation on ANin sclerophyllous oaks 10,Rhododendronspecies 11 and Orchid species 12.Therefore,the major limiting factor of ANmightlargely differ between species.Modern rose is one of the most important fresh cut flowersall over the world,owing to its high values in ornamental,food and material industry.However,the major limiting factor of light-saturated ANunder steady state in modern rosecultivars is not well known.In nature,leaves usually experience fluctuating light due to cloud,wind,andshading from other leaves 13,14.In addition to steady-state photosynthetic capacity,dynamic photosynthesis under fluctuating light significantly affects plant growth andbiomass 1519.Upon transitioning from low to high light,net CO2assimilation rate(AN)gradually increases,but the time required to fulfill light induction largely differsamong different plants and cultivars 9,16,18,2022.For example,C3plants needed lesstime to accomplish the photosynthetic induction than C4plants 23.Large variations inthe rates of photosynthetic induction were observed in genotypes of African cassava,rice,wheat,and canola 15,18,20,21.Therefore,improving photosynthetic performanceunder fluctuating light has a great potential in crop improvement.When irradiance sharply increases,photosynthetic induction is tightly relatedto four steps:(1)the induction rate of photosynthetic electron flow,which can beaccomplished in 2 min 19,24;(2)the activation of ribulose bisphosphate carboxy-lase/oxygenase(Rubisco),which needs approximately 510 min 21,25;(3)the inductionkinetics of gm,which needs approximately 520 min 25,26;(4)the induction kineticsof gs,which needs time up to 1 h to reach the maximum value 9,13,18.Notably,theinduction rates of gsand gmare much slower than those of photosynthetic electronflow and Rubisco.Therefore,in theory,gsand gmlikely exert the major limitationsof photosynthesis under fluctuating light 18,26.Indeed,the induction kinetics of gssignificantly affected the induction rate of ANin Arabidopsis thaliana 19,rice 24,andAfrican cassava 18.A recent study reported that gmsignificantly restricted ANduringlight induction in Arabidopsis thaliana and tobacco 26.Furthermore,the induction ofANwas more related to gminduction rather than gsinduction in tomato 27.Therefore,the major limitation of ANunder fluctuating light differs between species.Natural sunlight is the major light source for the cultivation of modern rose cultivars,but their dynamic photosynthesis under fluctuating light is little known.In the breedingof modern rose,some old rose species are usually used as a parent of hybridization,butthe photosynthetic characteristics of old rose species are poorly understood.Modernrose cultivars have much higher productivity than old rose plants,but the underlyingphotosynthetic mechanisms have not yet been clarified.Specifically,it is unclear whethermodern rose cultivars have higher photosynthetic capacity under steady state or havesuperior photosynthetic performance under fluctuating light to old rose species.Based onthe results that crop cultivars usually had similar steady-state photosynthesis but variedin dynamic photosynthesis 17,we hypothesize that modern rose cultivars have higherdynamic photosynthetic efficiency than old rose species.In the present study,photosynthetic characteristics were measured under steadystate and fluctuating light in two modern rose(Rose hybrida)cultivars,“Orange Reeva”and“Gelato”,and an old Chinese rose plant Rosa chinensis,“Slaters crimson China”.The aims of this study are:(1)to quantify the limitation of steady-state ANin rosecultivars;and(2)to explore whether modern rose cultivars have superior photosyntheticperformance under fluctuating light to the old rose germplasm.The results indicatedthat that photosynthetic capacity under steady state did not differ significantly amongthese three rose genotypes,and the steady-state photosynthesis was mainly limited bythe biochemical capacity in them.However,the two modern Rose hybrida cv.“OrangeReeva”and“Gelato”showed stronger photosynthetic performance under fluctuatinglight than the old germplasm Rosa chinensis.Therefore,the improved photosyntheticefficiency under fluctuating light partially contributes to the stronger growth potentialof modern rose cultivars.Plants 2023,12,11863 of 152.Results2.1.Photosynthetic Characteristics under Steady-State Differ Slightly between Rose GenotypesThe basal leaf functional traits of the three studied rose genotypes were measuredand displayed in Table 1.Chlorophyll content(SPAD value)was significantly higher inRosa hybrida cv.Orange Reeva and Gelato than in Rosa chinensis.Orange Reeva displayedthe highest value of leaf mass per area(LMA),followed by Rosa chinensis and Gelato.Leaf N,K,P content in Orange Reeva and Gelato were significantly higher than those inRosa chinensis.At a high light of 1500mol m2s1,values for steady state ANwere 23.4,21.7,and 20.7mol m2s1in Orange Reeva,Gelato,and Rosa chinensis,respectively.Concomitantly,no significant difference in gswas observed among these three rosegenotypes,but Orange Reeva and Gelato had significantly higher gmthan Rosa chinensis.Dark respiration rate(Rd)did not significantly differ among these rose genotypes,whilethe maximum rate of RuBP carboxylation(Vcmax)was significantly higher in Orange Reevathan Gelato and Rosa chinensis.Generally,the light response curves indicated that these threerose genotypes showed similar ANand gsat a given light intensity(Figure 1).Therefore,thesteady-state photosynthesis differed only slightly among different rose genotypes.Plants 2023,12,x FOR PEER REVIEW 3 of 16 “Gelato”showed stronger photosynthetic performance under fluctuating light than the old germplasm Rosa chinensis.Therefore,the improved photosynthetic efficiency under fluctuating light partially contributes to the stronger growth potential of modern rose cul-tivars.2.Results 2.1.Photosynthetic Characteristics under Steady-State Differ Slightly between Rose Genotypes The basal leaf functional traits of the three studied rose genotypes were measured and displayed in Table 1.Chlorophyll content(SPAD value)was significantly higher in Rosa hybrida cv.Orange Reeva and Gelato than in Rosa chinensis.Orange Reeva displayed the highest value of leaf mass per area(LMA),followed by Rosa chinensis and Gelato.Leaf N,K,P content in Orange Reeva and Gelato were significantly higher than those in Rosa chinensis.At a high light of 1500 mol m2 s1,values for steady state AN were 23.4,21.7,and 20.7 mol m2 s1 in Orange Reeva,Gelato,and Rosa chinensis,respectively.Concomi-tantly,no significant difference in gs was observed among these three rose genotypes,but Orange Reeva and Gelato had significantly higher gm than Rosa chinensis.Dark respiration rate(Rd)did not significantly differ among these rose genotypes,while the maximum rate of RuBP carboxylation(Vcmax)was significantly higher in Orange Reeva than Gelato and Rosa chinensis.Generally,the light response curves indicated that these three rose geno-types showed similar AN and gs at a given light intensity(Figure 1).Therefore,the steady-state photosynthesis differed only slightly among different rose genotypes.Figure 1.Light intensity dependence of leaf net CO2 assimilation rate(AN)(A)and stomatal con-ductance(gs)(B)in two modern rose cultivars(Orange Reeva and Gelato)and the old Chinese rose plant Rosa chinensis.Data are means SE(n=5).Figure 1.Light intensity dependence of leaf net CO2assimilation rate(AN)(A)and stomatal conduc-tance(gs)(B)in two modern rose cultivars(Orange Reeva and Gelato)and the old Chinese rose plantRosa chinensis.Data are meansSE(n=5).Based on the CO2response curves,ANdiffered very slightly between these threerose genotypes at Cibelow 300mol mol1(Figure 2A).However,when Ciwas higherthan 300mol mol1,Rosa hybrida cv.Orange Reeva had significantly higher ANthanRosa hybrida cv.Gelato and Rosa chinensis(Figure 2A).Concomitantly,electron transportrate through PSII(JPSII)was higher in Orange Reeva than the other two rose genotypes(Figure 2B).At an atmospheric CO2concentration of 400mol mol1,ANjust reached4050%of the maximum value,but JPSIIreached approximately 80%of the maximum valuePlants 2023,12,11864 of 15(Figure 2A,B).Therefore,the major limitation imposed on ANat 1500mol m2s1and400mol mol1CO2was Rubisco carboxylation rather than RuBP regeneration(i.e.,elec-tron transport rate).The quantitative analysis indicated that the relative limitation imposedon ANby biochemical capacity was approximately 0.6 in the three rose genotypes,the rela-tive limitation of gsor gmwas approximately 0.2 in them(Figure 2C).Therefore,in the threestudied rose genotypes,biochemistry was the major limitation of ANunder atmosphericCO2concentration and high light,followed by diffusional conductance.Plants 2023,12,x FOR PEER REVIEW 5 of 16 Figure 2.Response of leaf net CO2 assimilation rate(AN;A)and electron transport rate(ETR;B)to intracellular CO2 concentration in two modern rose cultivars(Orange Reeva and Gelato)and the old Chinese rose plant Rosa chinensis.Quantitative analysis of relative limitation imposed on AN in these three rose genotypes.ls,stomatal conductance limitation,lm,mesophyll conductance limi-tation,and lb,biochemistry limitation.All A/Ci curves were measured under a saturating light of 1500 mol photons m2 s1.Data are means SE(n=5).2.2.Modern Rose cultivars use Fluctuating Light more Efficiently Than the Old Rose Species During the three low/high light cycles,Orange Reeva and Gelato had significantly higher AN in high-light phases than Rosa chinensis,while the value of AN in low-light phases did not differ between them(Figure 3A).Such difference in AN in high-light phases led to the higher carbon gain under fluctuating light in Orange Reeva and Gelato(Figure 3B).During the 30 min fluctuating light treatment,gs gradually decreased with prolonged illumination under fluctuating light in all these three rose genotypes(Figure 3C),and the average gs under fluctuating light was significantly higher in Orange Reeva and Gelato than Rosa chinensis(Figure 3D).Upon transitioning to high light,gm gradually increased in the subsequent 5 min(Figure 3E).No significant difference in gm was observed at low light,while Orange Reeva and Gelato had significantly higher gm at high-light phases than Figure 2.Response of leaf net CO2assimilation rate(AN;A)and electron transport rate(ETR;B)tointracellular CO2concentration in two modern rose cultivars(Orange Reeva and Gelato)and the oldChinese rose plant Rosa chinensis.(C)Quantitative analysis of relative limitation imposed on ANinthese three rose genotypes.ls,stomatal conductance limitation,lm,mesophyll conductance limitation,and lb,biochemistry limitation.All A/Cicurves were measured under a saturating light of 1500molphotons m2s1.Data are meansSE(n=5).Plants 2023,12,11865 of 15Table 1.Photosynthetic characteris