Effects of drought treatment on photosystem II activity in the ephemeral plant Erodium oxyrhinchum.pdf

J Arid Land(2023)15(6):724739 https:/doi.org/10.1007/s40333-023-0058-8 Science Press Springer-Verlag Corresponding author:YANG Chunhong(E-mail:);ZHANG Yuanming(E-mail:)The first and second authors contributed equally to this work.Received 2022-11-19;revised 2023-03-08;accepted 2023-03-20 Xinjiang Institute of Ecology and Geography,Chinese Academy of Sciences,Science Press and Springer-Verlag GmbH Germany,part of Springer Nature 2023 http:/; Effects of drought treatment on photosystem II activity in the ephemeral plant Erodium oxyrhinchum CHEN Yingying1,2,LIN Yajun1,2,ZHOU Xiaobing1,ZHANG Jing1,YANG Chunhong3,4*,ZHANG Yuanming1*1 State Key Laboratory of Desert and Oasis Ecology/Key Laboratory of Ecological Safety and Sustainable Development in Arid Lands,Xinjiang Institute of Ecology and Geography,Chinese Academy of Sciences,Urumqi 830011,China;2 University of Chinese Academy of Sciences,Beijing 100049,China;3 Key Laboratory of Plant Resources and Beijing Botanical Garden,Institute of Botany,Chinese Academy of Sciences,Beijing 100093,China;4 Zhejiang Lab,Hangzhou 311121,China Abstract:Drought is a critical limiting factor affecting the growth and development of plants in arid and semi-arid areas.Photosynthesis,one of the most important physiological processes of plants,can be significantly inhibited by drought.Photosystem II(PSII)is considered the main attack target when photosynthesis is affected by drought.To clarify how PSII components of the ephemeral plant Erodium oxyrhinchum(grown in the Gurbantunggut Desert,China)respond to drought treatment,we evaluated the functional activity of PSII by determining chlorophyll fluorescence and gas exchange parameters under different drought treatment levels(control(400 mL),moderate drought(200 mL),and severe drought(100 mL).Under moderate drought treatment,significant decreases were found in net photosynthetic rate(Pn),effective quantum yield of PSII(Y(II),relative electron transfer rate of PSII(rETR(II),oxygen-releasing complex,probability of an absorbed exciton moving an electron into the electron transport chain beyond primary quinone receptor QA(Eo),probability of a trapped exciton moving an electron into the electron transport chain beyond primary quinone receptor QA(Eo),and performance index of PSII(PIabs).Compared to control treatment,marked increases were observed in water use efficiency(WUE),relative variable fluorescence at the J step(VJ),initial fluorescence(Fo),and dissipated energy per active reaction center(DIo/RC)under moderate drought treatment,but there were no substantial changes in semi-saturated light intensity(IK),active reaction centers per cross-section(RC/CS),and total performance index of PSII and PSI(PItotal,where PSI is the photosystem I).The changes of the above parameters under severe drought treatment were more significant than those under moderate drought treatment.In addition,severe drought treatment significantly increased the absorbed energy per active reaction center(ABS/RC)and trapping energy per active reaction center(TRo/RC)but decreased the energy transmission connectivity of PSII components,RC/CS,and PItotal,compared to moderate drought and control treatments.Principle component analysis(PCA)revealed similar information according to the grouping of parameters.Moderate drought treatment was obviously characterized by RC/CS parameter,and the values of Fo,VJ,ABS/RC,DIo/RC,and TRo/RC showed specific reactions to severe drought treatment.These results demonstrated that moderate drought treatment reduced the photochemical activity of PSII to a certain extent but E.oxyrhinchum still showed strong adaptation against drought treatment,while severe drought treatment seriously damaged the structure of PSII.The results of CHEN Yingying et al.:Effects of drought treatment on photosystem II activity in the 725 this study are useful for further understanding the adaptations of ephemeral plants to different water conditions and can provide a reference for the selection of relevant parameters for photosynthesis measurements of large samples in the field.Keywords:chlorophyll fluorescence;drought treatment;electron transport;photosynthesis;photosystem II;Erodium oxyrhinchum;Gurbantunggut Desert Citation:CHEN Yingying,LIN Yajun,ZHOU Xiaobing,ZHANG Jing,YANG Chunhong,ZHANG Yuanming.2023.Effects of drought treatment on photosystem II activity in the ephemeral plant Erodium oxyrhinchum.Journal of Arid Land,15(6):724739.https:/doi.org/10.1007/s40333-023-0058-8 1 Introduction Ephemeral plants,which are widely distributed in the Gurbantunggut Desert of China(Duan et al.,2017),are usually annual herbs with short growth cycle and high photosynthetic rate(Qiu et al.,2007;Tu et al.,2016;Wu et al.,2020).As drought sensitive species,ephemeral plants are sensitive to water availability;they can quickly complete their life cycle by using ice and snow melting water in winter and precipitation in early spring before the arrival of dry and hot summer(Zhang and Chen,2002).Lan et al.(2008)reported that the adaptation of annual early spring ephemeral plants to the arid environment occurs not just through the specialization of internal structures,but also due to their unique physiological characteristics within their short life history.For example,adaptations against drought can be achieved by simply adjusting leaf movements to reduce leaf temperature and water loss through respiration(Forseth and Ehleringer,1980;Yuan and Tang,2010a)or by regulating leaf osmotic potential(Forseth and Ehleringer,1982;Zhou et al.,2010).Some studies have shown that a reduction in condensate water can decrease the transpiration and net photosynthetic rate(Pn),but have no obvious impact on the intercellular CO2 concentration and water use efficiency(WUE),reflecting a stable water utilization strategy for ephemeral plants(Gong et al.,2017;Liu et al.,2018).Zhou et al.(2010)also demonstrated that drought significantly reduces Pn in Malcolmia africana.A recent study showed that increasing precipitation can promote the photosynthetic efficiency in ephemeral plants(Zhang et al.,2022).Ephemeral plants have evolved distinct adaptative mechanisms under drought conditions in the desert environment;however,the specific photosynthetic responses to drought remain unclear,especially for photosystem II(PSII).PSII activity is a sensitive indicator to evaluate the external environmental stress for plants(Kalaji et al.,2016).PSII is considered the primary target of attack in photosynthesis under external environmental stress(Liu et al.,2018).Chlorophyll fluorescence can be used to quantify the energy distribution dynamics of PSII and determine the photosynthetic physiological status of plants(Krause and Weis,1991).Furthermore,the rapid chlorophyll fluorescence induction kinetic curve(OJIP)can reflect the changes in primary photochemical reactions of PSII,as well as the structure and state of the photosynthetic mechanisms(Strasser et al.,1995,2004).Drought stress strongly alters the shape of the OJIP,which manifests its effects on plant physical responses in various patterns and forms the induction transient(Li,2007;Kalaji et al.,2016).It is accepted that the L(0.010.30 ms),K(0.012.00 ms),H(2.0030.00 ms),and G(30.001000.00 ms)bands can be used to represent different transient stages to analyze the changes in each stage of the OJIP in more detail(Strasser et al.,2004;Stirbet and Govindjee,2012).Based on the thylakoid membrane energy flux theory,Strasser et al.(2004)developed a data processing method for the OJIP(i.e.,the JIP test).The analysis of the energy flux,flux ratio per reaction center,and unit leaf cross-section in the JIP test can provide detailed information on the redox state of PSII(Strasser et al.,2010;Stirbet and Govindjee,2011;Kalaji et al.,2016).Chlorophyll fluorescence has been widely used to analyze the response of PSII to drought stress(Zivcak et al.,2013;Zhou et al.,2019;Bano et al.,2021).In the Gurbantunggut Desert,Erodium oxyrhinchum dominates the layer of ephemeral plants 726 JOURNAL OF ARID LAND 2023 Vol.15 No.6 and is limited by water during the growing period(Wang et al.,2006;Li et al.,2020;Mu et al.,2021).In this paper,E.oxyrhinchum was selected to investigate the effects of drought treatment on its PSII activity.At present,some researchers have studied the effects of precipitation on the isochronous germination of E.oxyrhinchum(Liu et al.,2021),the influences of snow on its seedling growth(Wu et al.,2018),and the impacts of water and nitrogen additions on its life history(Chen et al.,2019).In terms of photosynthesis,the impacts of precipitation on chlorophyll fluorescence(Zhang et al.,2022)and the influences of biological soil crusts on photosynthetic characteristics(Zhuang and Zhang,2017)are the only topics that have been studied so far.There are few studies on the photosynthesis of E.oxyrhinchum under drought treatment,especially with respect to PSII.Thus,a drought simulation experiment of E.oxyrhinchum was designed in this study.The response characteristics of leaf photosynthesis and chlorophyll fluorescence of E.oxyrhinchum to drought treatment were analyzed to clarify how the components of PSII respond to drought treatment.This study can provide a theoretical basis for improving the stress resistance and photosynthetic efficiency of E.oxyrhinchum,as well as other ephemeral plants in the Gurbantunggut Desert.2 Materials and methods 2.1 Plant materials and experimental design The experiment was carried out in a sunlight room with natural sunlight and indoor temperature of 25C from April to June of 2021 in Xinjiang Institute of Ecology and Geography,Chinese Academy of Sciences,Urumqi,China.Seeds of E.oxyrhinchum and the cultivated sand soil were collected from the Gurbantunggut Desert(44114620N,84319000E)in early June 2020.The collected seeds were dried with natural air and then preserved in the laboratory.The outer seed coat was cut with a plant-dissecting knife to break the physical dormancy of seeds before sowing.We set the control treatment based on the average precipitation amount and precipitation frequency during the growing season of 20172019 in the Gurbantunggut Desert reported by Min(2020).We further set two drought treatments,with 50%of the control treatment as the moderate drought and 25%of the control treatment as the severe drought.The actual cumulative precipitation from March to June was calculated to be close to 50.0 mm,and the precipitation frequency was 6 d.That is,about 3.3 mm of precipitation occurred every 6 d.Based on the volume of the flowerpot(height of 25 cm and diameter of 17 cm),we finally set the irrigation volume as follows:400 mL of water for the control treatment,200 mL for the moderate drought treatment,and 100 mL for the severe drought treatment for every 6 d.Each drought treatment had 5 replicates,with a total of 15 flowerpots.Approximately 7 or 8 seeds were sown in each flowerpot.In the early stage,seeds were sufficiently watered every 6 d using an artificial sprayer,with about 3.3 mm(400 mL as the control)tap water totally on each flowerpot.Once the seeds have germinated,3 robust seedlings were kept in each flowerpot and the excess seedlings were pulled out.After one and a half months of growth,when the plants reached the leaf-expansion stage,drought treatment lasted for 12 d,watering every 6 d.Measurements of parameters were conducted during this period(i.e.,after one and a half months of growth).2.2 Leaf gas exchange measurements Leaf gas exchange parameters were measured with Li-6400(Li-COR Inc.,Lincoln,Nebraska,USA)on a sunny day from 09:00 to 12:00(LST)in the morning.The measured parameters included Pn,transpiration rate(Tr),stomatal conductance(Gs),and WUE(which was calculated from the ratio of Pn to Tr),and the values were recorded after stabilization for 10.00 min.The cuvette settings were as follows:1500.00 mol photons/(m2s)for photosynthetic photon flux density(PPFD),500.00 mmol/s for flow rate,and 400.00 mmol/mol for CO2,and the cuvette fan was set to fast mode.After measurements,the leaves were photographed using the software Image J(Rawak Software,Carlsbad,CA,USA)to determine the leaf areas.Then,the parameters of Pn(mol/(m2s),Tr(mmol/(m2s),and Gs(mmol/(m2s)can be obtained by the measuring CHEN Yingying et al.:Effects of drought treatment on photosystem II activity in the 727 instrument and software directly.Each drought treatment is an average of five replicates.2.3 Chlorophyll fluorescence measurements We adjusted the plants dark-adapted for 30.00 min before measurements using a portable PAM-2500 fluorometer(Heinz Walz GmbH,Effeltrich,Germany),according to the methods of Schreiber et al.(1986).The measured light intensity was 0.15 mol photons/(m2s),the saturated pulse intensity was 10,000.00 mol photons/(m2s)for 0.80 s,and the pulse interval was 20.00 s.The gradient of light intensity was set as 0.00,5.00,93.00,201.00,514.00,877.00,1381.00,1647.00,1967.00,2362.00,and 2862.00 mol photons/(m2s);in turn,the duration of the applied light for each light intensity was 300.00 s,and the instrument measurement software can automatically calculate the effective quantum yield of PSII(Y(II),photochemical quenching(qP),closure degree of PSII(1qP),quantum yield of regulated energy dissipation in PSII(Y(NPQ),and quantum yield of nonregulated energy dissipation in PSII(Y(NO).The fluorescence parameters were calculated as follows(Krall and Edwards,1992;Kramer et al.,2004;Klughammer and Schreiber,2008):(II)()/,YFmFsFm=(1)()/(),oqPFmFsFmF=(2)()/1,Y NPQFm Fm=(3)()/,Y NOFs Fm=(4)where Fm and Fm represent the maximal fluorescence from dark-adapted and light-adapted leaves,respectively;Fo represents the minimal fluorescence from light-adapted leaves;and Fs represents the steady state fluorescence yield from light adaptation.The fast light response curve of relative electron transfer rate of PSII(rETR(II);mol/(m2s)was fitted using the equation described by Platt et al.(1980).The gradient of light intensity was set as 0.00,5.00,45.00,93.00,145.00,201.00,385.00,514.00,877.00,1115.00,1381.00,1647.00,1967.00,2362.00,and 2862.00 mol photons/(m2s);in turn,the duration of the applied light for each light intensity was 30.00 s,and the instrument measurement software can automatically calculate the rETR(II).The relevant parameters obtained from the fit equation were the maximum electron transfer rate(ETRmax;mol/(m2s),semi-saturated light intensity(IK;mol/(m2s),initial slope of the fast light response curve(),and photosynthetically active radiation(PAR;mol/(m2s).Each treatment is an average of five replicates.ETR(II)(II)PAR0.84 0.5,rY=(5)maxETR/.KI=(6)2.4 Rapid chlorophyll fluorescence measurements We monitored the rapid chlorophyll fluorescence induction kinetics in situ artificially with plant efficiency analyzer(HandyPEA,Hansatech Instruments Ltd.,Norfolk,UK),according to the method described by Strasser et al.(2004).After dark adaptation for 30.00 min,the fluore