Please wait a minute...
Journal of Arid Land
Journal of Arid Land  2023, Vol. 15 Issue (6): 724-739    DOI: 10.1007/s40333-023-0058-8
Research article     
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,*()
1State 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
2University of Chinese Academy of Sciences, Beijing 100049, China
3Key Laboratory of Plant Resources and Beijing Botanical Garden, Institute of Botany, Chinese Academy of Sciences, Beijing 100093, China
4Zhejiang Lab, Hangzhou 311121, China
Download: HTML     PDF(2233KB)
Export: BibTeX | EndNote (RIS)      

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- (Φ(Eo)), probability of a trapped exciton moving an electron into the electron transport chain beyond primary quinone receptor QA- (ψ(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 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.

Key words： chlorophyll fluorescence      drought treatment      electron transport      photosynthesis      photosystem II      Erodium oxyrhinchum      Gurbantunggut Desert     
Received: 19 November 2022      Published: 30 June 2023
Corresponding Authors: * YANG Chunhong (E-mail: yangch@ibcas.ac.cn);ZHANG Yuanming (E-mail: zhangym@ms.xjb.ac.cn)
About author: First author contact:

The first and second authors contributed equally to this work.
Service
E-mail this article
Add to my bookshelf
Add to citation manager
E-mail Alert
RSS
Articles by authors
CHEN Yingying
LIN Yajun
ZHOU Xiaobing
ZHANG Jing
YANG Chunhong
ZHANG Yuanming
Cite this article:

CHEN Yingying, LIN Yajun, ZHOU Xiaobing, ZHANG Jing, YANG Chunhong, ZHANG Yuanming. Effects of drought treatment on photosystem II activity in the ephemeral plant Erodium oxyrhinchum. Journal of Arid Land, 2023, 15(6): 724-739.

URL:

http://jal.xjegi.com/10.1007/s40333-023-0058-8     OR     http://jal.xjegi.com/Y2023/V15/I6/724

Fig. 1 Phenotype of Erodium oxyrhinchum grown under different drought treatment levels. (a), control treatment; (b), moderate drought treatment; (c), severe drought treatment.
Fig. 2 Leaf gas exchange parameters of E. oxyrhinchum under different drought treatment levels. (a), net photosynthetic rate (Pn); (b), stomatal conductance (Gs); (c), transpiration rate (Tr); (d), water use efficiency (WUE). Different lowercase letters indicate significant differences among drought treatments at P<0.05 level based on the Duncan's test. Bars mean standard deviations.
Fig. 3 Light response curves of E. oxyrhinchum under different drought treatment levels. (a), effective quantum yield of photosystem II (PSII) (Y(II)); (b), closure degree of PSII (1-qP); (c), quantum yield of regulated energy dissipation in PSII (Y(NPQ)); (d), quantum yield of nonregulated energy dissipation in PSII (Y(NO)). PPFD, photosynthetic photon flux density. Bars mean standard deviations.
Fig. 4 Fitted light response curves of (a) relative electron transfer rate of PSII (rETR(II)), (b) maximum electron transfer rate (ETRmax), (c) initial slope of the fast light response curve (α), and (d) semi-saturated light intensity (IK) of E. oxyrhinchum under different drought treatment levels. Different lowercase letters indicate significant differences among drought treatments at P<0.05 level based on the Duncan's test. Bars mean standard deviations.
Fig. 5 Rapid chlorophyll fluorescence induction kinetics curve (OJIP) of E. oxyrhinchum under different drought treatment levels. The first rise from the origin is denoted as "O", which ascends to an intermediate state "K" step (at 0.30 ms) and "J" step (at 2.00 ms), followed by a second slower rise involving a second intermediate state "I" step (at 30.00 ms), while the "P" step is the maximum fluorescence measured. (a), relative variable fluorescence at stages O-P (VOP); (b), relative variable fluorescence after normalization at stages O-P (ΔVOP); (c), relative variable fluorescence at stages O-J (VOJ); (d), relative variable fluorescence of K band after normalization at stages O-J (ΔVOJ); (e), relative variable fluorescence at stages O-K (VOK); (f), relative variable fluorescence of L band after normalization at stages O-K (ΔVOK); (g) relative variable fluorescence at stages J-I (VJI); (h), relative variable fluorescence of H band after normalization at stages J-I (ΔVJI); (i) relative variable fluorescence at stages I-P (VIP); (j), relative variable fluorescence of G band after normalization at stages I-P (ΔVIP). Relative variable fluorescence was calculated as Vt=(Ft-Fo)/(Fm-Fo) (where, Fo is the minimum fluorescence; Fm is the maximum fluorescence; and Ft is the fluorescence at t time) and relative variable fluorescence after normalization was determined as ΔVt=Vt-Vcontrol (where Vt is the relative variable fluorescence at t time; and Vcontrol is the relative variable fluorescence at t time under control treatment).
Fig. 6 Data processing method for the OJIP (JIP test) parameters of E. oxyrhinchum under different drought treatment levels. The rapid chlorophyll fluorescence parameters under control treatment were taken as 1 and the rapid chlorophyll fluorescence parameters under moderate drought and severe drought treatments were expressed as the proportion of that under control treatment. Different lowercase letters in the parentheses indicate significant differences at P<0.05 level based on the Duncan's test. Fv/Fm, the maximal photochemical efficiency (where Fv is the variable fluorescence); ABS/RC, absorbed energy per active reaction center; DIo/RC, dissipated energy per active reaction center; TRo/RC, trapping energy per active reaction center; REo/RC, electron flux from the active reaction center to the PSI acceptor side; RC/CS, active reaction centers per cross-section; VJ, relative variable fluorescence at the J step; Sm, the size of the plastoquinone (PQ) pool on the PSII receptor side; ψ(Eo), probability of a trapped exciton moving an electron into the electron transport chain beyond primary quinone receptor QA-; Φ(Eo), probability of an absorbed exciton moving an electron into the electron transport chain beyond primary quinone receptor QA-; δRo, probability of an electron being transported from reduced PQ to the electron acceptor side of photosystem I (PSI); PIabs, the performance index of PSII; PItotal, the total performance index of PSII and PSI.
Parameter PC1 PC2
Fo -0.2849# -0.1477
Fv/Fm 0.2804# -0.0230
ABS/RC -0.2799# 0.1460
DIo/RC -0.2792# 0.1512
TRo/RC -0.2756# 0.1429
ψ(Eo) 0.2847# -0.0581
Φ(Eo) 0.2840# -0.0241
PIabs 0.2842# 0.0401
PItotal 0.2609# -0.0174
VJ -0.2871# -0.0095
Sm 0.2523# 0.0939
Pn 0.2858# 0.1200
RC/CS 0.0732 0.9280#
IK 0.2537# -0.1506
Table 1 Contributions of different chlorophyll fluorescence and gas exchange parameters of E. oxyrhinchum to the total variance of principal components (PCs)
Fig. 7 Biplot of principal component analysis (PCA) showing the separation of the chlorophyll fluorescence and gas exchange parameters of E. oxyrhinchum under different drought treatment levels. PC1, the first principal component; PC2, the second principal component.
[1]   Azhar A, Makihara D, Naito H, et al. 2021. Sago palm (Metroxylon sagu Rottb.) response to drought condition in terms of leaf gas exchange and chlorophyll a fluorescence. Plant Production Science, 24(1): 65-72.
doi: 10.1080/1343943X.2020.1794914
[2]   Bano H, Athar H R, Zafar Z U, et al. 2021. Linking changes in chlorophyll a fluorescence with drought stress susceptibility in mung bean [Vigna radiata (L.) Wilczek]. Physiologia Plantarum, 172(2): 1244-1254.
[3]   Chen Y F, Zhang L W, Shi X, et al. 2019. Life history responses of spring- and autumn-germinated ephemeral plants to increased nitrogen and precipitation in the Gurbantunggut Desert. Science of The Total Environment, 659: 756-763.
doi: 10.1016/j.scitotenv.2018.12.368
[4]   Çiçek N, Pekcan V, Arslan Ö, et al. 2019. Assessing drought tolerance in field-grown sunflower hybrids by chlorophyll fluorescence kinetics. Brazilian Journal of Botany, 42: 249-260.
doi: 10.1007/s40415-019-00534-1
[5]   Duan C, Wu L, Wang S M, et al. 2017. Analysis of spatio-temporal patterns of ephemeral plants in the Gurbantunggut Desert over the last 30 years. Acta Ecologica Sinica, 37(8): 2642-2652. (in Chinese)
[6]   Eppel A, Shaked R, Eshel G, et al. 2014. Low induction of non-photochemical quenching and high photochemical efficiency in the annual desert plant Anastatica hierochuntica. Physiologia Plantarum, 151(4): 544-558.
doi: 10.1111/ppl.2014.151.issue-4
[7]   Farquhar G D, Sharkey T D. 1982. Stomatal conductance and photosynthesis. Annual Review of Plant Physiology, 33: 317-345.
doi: 10.1146/arplant.1982.33.issue-1
[8]   Fernández-Marín B, Gulías J, Figueroa C M, et al. 2020. How do vascular plants perform photosynthesis in extreme environments? An integrative ecophysiological and biochemical story. Plant Journal, 101(4): 979-1000.
doi: 10.1111/tpj.v101.4
[9]   Forseth I N, Ehleringer J R. 1980. Solar tracking response to drought in a desert annual. Oecologia, 44(2): 159-163.
doi: 10.1007/BF00572673 pmid: 28310550
[10]   Forseth I N, Ehleringer J R. 1982. Ecophysiology of two solar tracking desert winter annuals. Oecologia, 54(1): 41-49.
doi: 10.1007/BF00541105 pmid: 28310989
[11]   Gomes M T G, Da Luz A C, Dos Santos M R, et al. 2012. Drought tolerance of passion fruit plants assessed by the OJIP chlorophyll a fluorescence transient. Scientia Horticulturae, 142: 49-56.
doi: 10.1016/j.scienta.2012.04.026
[12]   Gong X W, Lü G H, Welp M, et al. 2017. Water and photosynthetic physiology of Lappula semiglabra seedlings under different dew input amounts. Chinese Journal of Ecology, 36(8): 2198-2205. (in Chinese)
[13]   Kalaji H M, Jajoo A, Oukarroum A, et al. 2016. Chlorophyll a fluorescence as a tool to monitor physiological status of plants under abiotic stress conditions. Acta Physiologiae Plantarum, 38: 102, doi: 10.1007/s11738-016-2113-y.
doi: 10.1007/s11738-016-2113-y
[14]   Klughammer C, Schreiber U. 2008. Complementary PS II quantum yields calculated from simple fluorescence parameters measured by PAM fluorometry and the Saturation Pulse method. PAM Application Notes, 1: 27-35.
[15]   Krall J P, Edwards G E. 1992. Relationship between photosystem II activity and CO2 fixation in leaves. Physiologia Plantarum, 86(1): 180-187.
doi: 10.1111/ppl.1992.86.issue-1
[16]   Kramer D M, Johnson G, Kiirats O, et al. 2004. New fluorescence parameters for the determination of QA redox state and excitation energy fluxes. Photosynthesis Research, 79: 209-218.
doi: 10.1023/B:PRES.0000015391.99477.0d pmid: 16228395
[17]   Krause G H, Weis E. 1991. Chlorophyll fluorescence and photosynthesis: the basics. Annual Review of Plant Physiology and Plant Molecular Biology, 42: 313-349.
doi: 10.1146/arplant.1991.42.issue-1
[18]   Li D X, Zhang D Y, Zhang L W, et al. 2020. Biological seed characteristics of spring-emergence and autumn-emergence Erodium oxyrhinchum. Arid Zone Research, 37(06): 1562-1568. (in Chinese)
[19]   Li P M, Gao H Y, Strasser R J. 2005. Application of the fast chlorophyll fluorescence induction dynamics analysis in photosynthesis study. Physiology and Molecular Biology of Plants, 31(6): 559-566. (in Chinese)
[20]   Li P M. 2007. Application of chlorophyll a fluorescence transient in study of plant physiology under stress conditions. PhD Dissertation. Tai'an: Shandong Agricultural University. (in Chinese)
[21]   Li Y H, Liu J H, Zhao B P, et al. 2020. Effect of drought stress on oat growth and leaf photosystem II activity. Acta Botanica Boreali-Occidentalia Sinica, 40(10): 1706-1713. (in Chinese)
[22]   Lima C S, Ferreira-Silva S L, Carvalho F E L, et al. 2018. Antioxidant protection and PSII regulation mitigate photo-oxidative stress induced by drought followed by high light in cashew plants. Environmental and Experimental Botany, 149: 59-69.
doi: 10.1016/j.envexpbot.2018.02.001
[23]   Liu H L, Chen Y F, Zhang L W, et al. 2021. Is the life history flexibility of cold desert annuals broad enough to cope with predicted climate change? The case of Erodium oxyrhinchum in Central Asia. Biology, 10(8): 780, doi: 10.3390/biology10080780.
doi: 10.3390/biology10080780
[24]   Liu J, Guo Y Y, Bai Y W, et al. 2018. Effects of drought stress on the photosynthesis in maize. Russian Journal of Plant Physiology, 65(6): 849-856.
doi: 10.1134/S1021443718060092
[25]   Liu Z D, Ran Q Y, Chen Y, et al. 2018. Ecological effects of condensed water to ephemeral plants Lappula semiglabra in desert. Arid Zone Research, 35(6): 1290-1298. (in Chinese)
[26]   Lu J Z, Yin Z P, Lu T, et al. 2020. Cyclic electron flow modulate the linear electron flow and reactive oxygen species in tomato leaves under high temperature. Plant Science, 292: 110387, doi: 10.1016/j.plantsci.2019.110387.
doi: 10.1016/j.plantsci.2019.110387
[27]   Luo H H, Tsimilli-Michael M, Zhang Y L, et al. 2016. Combining gas exchange and chlorophyll a fluorescence measurements to analyze the photosynthetic activity of drip-irrigated cotton under different soil water deficits. Journal of Integrative Agriculture, 15(6): 1256-1266.
doi: 10.1016/S2095-3119(15)61270-9
[28]   Ma L, Zhang Z H, Yao B Q, et al. 2021. Effects of drought and heat on the productivity and photosynthetic characteristics of alpine meadow plants on the Qinghai-Tibetan Plateau. Journal of Mountain Science, 18(8): 2079-2093.
doi: 10.1007/s11629-020-6561-x
[29]   Manaa A, Goussi R, Derbali W, et al. 2021. Photosynthetic performance of quinoa (Chenopodium quinoa Willd.) after exposure to a gradual drought stress followed by a recovery period. Biochimica et Biophysica Acta (BBA)-Bioenergetics, 1862(5): 148383, doi: 10.1016/j.bbabio.2021.148383.
doi: 10.1016/j.bbabio.2021.148383
[30]   Min X J. 2020. Photosynthetic response and growth adaptation strategies of desert herbaceous plants to rainfall variation. PhD Dissertation. Beijing: University of Chinese Academy of Sciences. (in Chinese)
[31]   Mu X H, Huang G, Li Y, et al. 2021. Population dynamics and life history response to precipitation changes for a desert ephemeral plant with biseasonal germination. Frontiers in Plant Science, 12: 625475, doi: 10.3389/fpls.2021.625475.
doi: 10.3389/fpls.2021.625475
[32]   Paunov M, Koleva L, Vassilev A, et al. 2018. Effects of different metals on photosynthesis: cadmium and zinc affect chlorophyll fluorescence in durum wheat. International Journal of Molecular Sciences, 19(3): 787, doi: 10.3390/ijms19030787.
doi: 10.3390/ijms19030787
[33]   Pinheiro C, Chaves M M. 2011. Photosynthesis and drought: can we make metabolic connections from available data? Journal of Experimental Botany, 62(3): 869-882.
[34]   Platt T, Gallegos C L, Harrison W G. 1980. Photoinhibition of photosynthesis in natural assemblages of marine phytoplankton. Journal of Marine Research, 38(4): 687-701.
[35]   Qiu J, Tan D Y, Fan D Y. 2007. Characteristics of photosynthesis and biomass allocation of spring ephemerals in the Junggar Desert. Chinese Journal of Plant Ecology, 31(5): 883-891. (in Chinese)
doi: 10.17521/cjpe.2007.0111
[36]   Redillas M C F R, Strasser R J, Jeong J S, et al. 2011. The use of JIP test to evaluate drought-tolerance of transgenic rice overexpressing OsNAC10. Plant Biotechnology Reports, 5: 169-175.
doi: 10.1007/s11816-011-0170-7
[37]   Schreiber U, Schliwa U, Bilger W. 1986. Continuous recording of photochemical and non-photochemical chlorophyll fluorescence quenching with a new type of modulation fluorometer. Photosynthesis Research, 10(1-2): 51-62.
doi: 10.1007/BF00024185 pmid: 24435276
[38]   Shi S B, Li T C, Li M, et al. 2015. Interaction effect analysis of soil drought and strong light on PSII non-photochemical quenching in Kobresia pygmaea leaves. Plant Physiology Journal, 51(10): 1678-1686. (in Chinese)
[39]   Stirbet A, Govindjee. 2011. On the relation between the Kautsky effect (chlorophyll a fluorescence induction) and Photosystem II: Basics and applications of the OJIP fluorescence transient. Journal of Photochemistry and Photobiology B: Biology, 104(1-2): 236-257.
doi: 10.1016/j.jphotobiol.2010.12.010
[40]   Stirbet A, Govindjee. 2012. Chlorophyll a fluorescence induction: a personal perspective of the thermal phase, the J-I-P rise. Photosynthesis Research, 113(1): 15-61.
doi: 10.1007/s11120-012-9754-5
[41]   Strasser R J, Srivastava A, Govindjee. 1995. Polyphasic chlorophyll a fluorescence transient in plants and cyanobacteria. Photochemistry and Photobiology, 61(1): 32-42.
doi: 10.1111/php.1995.61.issue-1
[42]   Strasser R J, Srivastava A, Tsimilli-Michael M. 2000. The fluorescence transient as a tool to characterize and screen photosynthetic samples. In: Yunus M, Pathre U, Mohanty P. Probing Photosynthesis: Mechanism, Regulation and Adaptation. London: Taylor and Francis Press, 445-483.
[43]   Strasser R J, Tsimilli-Michael M, Srivastava A. 2004. Analysis of the chlorophyll a fluorescence transient. In: Papageorgiou G C, Govindjee. Chlorophyll a Fluorescence. Advances in Photosynthesis and Respiration. Dordrecht: Springer, 321-362.
[44]   Strasser R J, Tsimilli-Michael M, Qiang S, et al. 2010. Simultaneous in vivo recording of prompt and delayed fluorescence and 820-nm reflection changes during drying and after rehydration of the resurrection plant Haberlea rhodopensis. Biochimica et Biophysica Acta-Bioenergetics, 1797(6-7): 1313-1326.
doi: 10.1016/j.bbabio.2010.03.008
[45]   Talbi S, Rojas J A, Sahrawy M, et al. 2020. Effect of drought on growth, photosynthesis and total antioxidant capacity of the saharan plant Oudeneya africana. Environmental and Experimental Botany, 176: 104099, doi: 10.1016/j.envexpbot.2020.104099.
doi: 10.1016/j.envexpbot.2020.104099
[46]   Tu W F, Li Y, Liu W, et al. 2016. Spring ephemerals adapt to extremely high light conditions via an unusual stabilization of photosystem II. Frontiers in Plant Science, 6: 1189, doi: 10.3389/fpls.2015.01189.
doi: 10.3389/fpls.2015.01189
[47]   Vincent C, Schaffer B, Rowland D. 2018. Water-deficit priming of papaya reduces high-light stress through oxidation avoidance rather than anti-oxidant activity. Environmental and Experimental Botany, 156: 106-119.
doi: 10.1016/j.envexpbot.2018.04.016
[48]   Wang C, Gu Q L, Zhao L J, et al. 2022. Photochemical efficiency of photosystem II in inverted leaves of soybean [Glycine max (L.) Merr.] affected by elevated temperature and high light. Frontiers in Plant Science, 12: 772664, doi: 10.3389/fpls.2021.772644.
doi: 10.3389/fpls.2021.772644
[49]   Wang F L, Chai C W, Zhao P, et al. 2021. Photosynthetic and chlorophyll fluorescence responses of three desert species to drought stress and evaluation of drought resistance. Acta Botanica Boreali-Occidentalia Sinica, 41(10): 1755-1765. (in Chinese)
[50]   Wang J W, Liu Y, Xu Y X, et al. 2022. Sexual differences in gas exchange and chlorophyll fluorescence of Torreya grandis under drought stress. Trees, 36: 283-294.
doi: 10.1007/s00468-021-02205-9
[51]   Wang W, Huang L N, Chen Q X. 2014. Rapid detection of photosynthetic capacity on cultivars of Yellow phalaenopsis. Subtropical Plant Science, 43(1): 4-7. (in Chinese)
[52]   Wang X Q, Jiang J, Wang Y C, et al. 2006. Responses of ephemeral plant germination and growth to water and heat conditions in the southern part of Gurbantunggut Desert. Chinese Science Bulletin, 51(Suppl. 1): 110-116.
doi: 10.1007/s11434-006-8214-z
[53]   Wang Z B, Li G F, Sun H Q, et al. 2018. Effects of drought stress on photosynthesis and photosynthetic electron transport chain in young apple tree leaves. Biology Open, 7(11): bio035279, doi: 10.1242/bio.035279.
doi: 10.1242/bio.035279
[54]   Wilson S, Ruban A V. 2020. Enhanced NPQ affects long-term acclimation in the spring ephemeral Berteroa incana. Biochimica et Biophysica Acta-Bioenergetics, 1861(4): 148014, doi: 10.1016/j.bbabio.2019.03.005.
doi: 10.1016/j.bbabio.2019.03.005
[55]   Wu L S, Zhang L, Tu W F, et al. 2020. Photosynthetic inner antenna CP 47 plays important roles in ephemeral plants in adapting to high light stress. Journal of Plant Physiology, 251: 153189, doi: 10.1016/j.jplph.2020.153189.
doi: 10.1016/j.jplph.2020.153189
[56]   Wu N, Zhang J, Wang Y, et al. 2018. Effects of snow cover and arbuscular mycorrhizal fungi network on the seedling growth of Erodium oxyrrhynchum. Arid Zone Research, 35(3): 624-632. (in Chinese)
[57]   Xu N, Meng X X Y, Zhao X M, et al. 2017. Responses of photosynthetic characteristics in leaves of Physocarpus amurensis and P.opulifolius to drought stress. Chinese Journal of Applied Ecology, 28(6): 1955-1961. (in Chinese)
[58]   Yuan S F, Tang H P. 2010a. Research advances in the eco-physiological characteristics of ephemerals adaptation to habitats. Acta Prataculturae Sinica, 19(1): 240-247. (in Chinese)
[59]   Yuan S F, Tang H P. 2010b. Patterns of ephemeral plant communities and their adaptations to temperature and precipitation regimes in Dzungaria Desert, Xinjiang. Biodiversity Science, 18(4): 346-354. (in Chinese)
doi: 10.3724/SP.J.1003.2010.346
[60]   Yue Z W, Li C D, Li L, et al. 2020. Responses of leaf morphology and fluorescence parameters of Alhagi sparsifolia in different light environments. Arid Zone Research, 37(3): 722-728. (in Chinese)
[61]   Zagorchev L, Traianova A, Teofanova D, et al. 2020. Influence of Cuscuta campestris Yunck. on the photosynthetic activity of Ipomoea tricolor Cav. - in vivo chlorophyll a fluorescence assessment. Photosynthetica, 58: 422-432.
doi: 10.32615/ps.2020.004
[62]   Zhang L Y, Chen C D. 2002. On the general characteristics of plant diversity of Gurbantunggut Sandy Desert. Acta Ecologica Sinica, (11): 1923-1932. (in Chinese)
[63]   Zhang Y L, Yin B F, Tao Y, et al. 2022. Effects of the first rainfall timing and amount on morphological characteristics and chlorophyll fluorescence of two ephemeral species in the Gurbantünggüt Desert, northwestern China. Chinese Journal of Plant Ecology, 46(4): 428-439. (in Chinese)
doi: 10.17521/cjpe.2020.0385
[64]   Zhou R H, Kan X, Chen J J, et al. 2019. Drought-induced changes in photosynthetic electron transport in maize probed by prompt fluorescence, delayed fluorescence, P700 and cyclic electron flow signals. Environmental and Experimental Botany, 158: 51-62.
doi: 10.1016/j.envexpbot.2018.11.005
[65]   Zhou X B, Zhang Y M, Wang S S, et al. 2010. Combined effects of simulated nitrogen deposition and drought stress on growth and photosynthetic physiological responses of two annual desert plants in Junggar Basin, China. Chinese Journal of Plant Ecology, 34(12): 1394-1403. (in Chinese)
[66]   Zhuang W W, Zhang Y M. 2017. Effects of biological soil crusts on the photosynthetic characteristics of three desert herbs in Gurbantunggut Desert. Plant Science Journal, 35(3): 387-397. (in Chinese)
[67]   Zivcak M, Brestic M, Balatova Z, et al. 2013. Photosynthetic electron transport and specific photoprotective responses in wheat leaves under drought stress. Photosynthesis Research, 117(1-3): 529-546.
doi: 10.1007/s11120-013-9885-3 pmid: 23860828
[1] Teame G KEBEDE, Emiru BIRHANE, Kiros-Meles AYIMUT, Yemane G EGZIABHER. Arbuscular mycorrhizal fungi improve biomass, photosynthesis, and water use efficiency of Opuntia ficus-indica (L.) Miller under different water levels[J]. Journal of Arid Land, 2023, 15(8): 975-988.
[2] LIU Yaxuan, ZENG Yong, YANG Yuhui, WANG Ning, LIANG Yuejia. Competition, spatial pattern, and regeneration of Haloxylon ammodendron and Haloxylon persicum communities in the Gurbantunggut Desert, Northwest China[J]. Journal of Arid Land, 2022, 14(10): 1138-1158.
[3] WANG Chunyuan, YU Minghan, DING Guodong, GAO Guanglei, ZHANG Linlin, HE Yingying, LIU Wei. Size- and leaf age-dependent effects on the photosynthetic and physiological responses of Artemisia ordosica to drought stress[J]. Journal of Arid Land, 2021, 13(7): 744-758.
[4] Anlifeire ANNIWAER, SU Yangui, ZHOU Xiaobing, ZHANG Yuanming. Impacts of snow on seed germination are independent of seed traits and plant ecological characteristics in a temperate desert of Central Asia[J]. Journal of Arid Land, 2020, 12(5): 775-790.
[5] ZHOU Honghua, CHEN Yaning, ZHU Chenggang, YANG Yuhai, YE Zhaoxia. Water transport and water use efficiency differ among Populus euphratica Oliv. saplings exposed to saline water irrigation[J]. Journal of Arid Land, 2019, 11(6): 866-879.
[6] Lianlian FAN, Junxiang DING, Xuexi MA, Yaoming LI. Ecological biomass allocation strategies in plant species with different life forms in a cold desert, China[J]. Journal of Arid Land, 2019, 11(5): 729-739.
[7] Hai ZHU, Shunjun HU, Jingsong YANG, KARAMAGE Fidele, Hao LI, Sihua FU. Spatio-temporal variation of soil moisture in a fixed dune at the southern edge of the Gurbantunggut Desert in Xinjiang, China[J]. Journal of Arid Land, 2019, 11(5): 685-700.
[8] Yonggang LI, Xiaobing ZHOU, Yuanming ZHANG. Shrub modulates the stoichiometry of moss and soil in desert ecosystems, China[J]. Journal of Arid Land, 2019, 11(4): 579-594.
[9] Shanlin YANG, Xiang SHI, Shaoming WANG, Jiashu LIU, Fanxiang MENG, Wei PANG. Is bi-seasonal germination an optimal choice for an ephemeral plant living in a cold desert?[J]. Journal of Arid Land, 2019, 11(2): 280-291.
[10] RUDIKOVSKII Alexandr, RUDIKOVSKAYA Elena, DUDAREVA Lyubov. Impact of air drought on photosynthesis efficiency of the Siberian crabapple (Malus baccata L. Borkh.) in the forest-steppe zone of Transbaikalia, Russia[J]. Journal of Arid Land, 2019, 11(2): 255-266.
[11] Gang HUANG, Yan LI, Xiaohan MU, Hongmei ZHAO, Yanfeng CAO. Water-use efficiency in response to simulated increasing precipitation in a temperate desert ecosystem, of Xinjiang, China[J]. Journal of Arid Land, 2017, 9(6): 823-836.
[12] Fengqin JIA, TIYIP Tashpolat, Nan WU, Changyan TIAN, Yuanming ZHANG. Characteristics of soil seed banks at different geomorphic positions within the longitudinal sand dunes of the Gurbantunggut Desert, China[J]. Journal of Arid Land, 2017, 9(3): 355-367.
[13] Jie MA, Ran LIU, Yan LI. Abiotic contribution to total soil CO2 flux across a broad range of land-cover types in a desert region[J]. Journal of Arid Land, 2017, 9(1): 13-26.
[14] QiQiang GUO, WenHui ZHANG, HuiE LI. Comparison of photosynthesis and antioxidative protection in Sophora moorcroftiana and Caragana maximovicziana under water stress[J]. Journal of Arid Land, 2014, 6(5): 637-645.
[15] Tao ZHANG, ChangYan TIAN, Yu SUN, DengSha BAI, Gu FENG. Dynamics of arbuscular mycorrhizal fungi associated with desert ephemeral plants in Gurbantunggut Desert[J]. Journal of Arid Land, 2012, 4(1): 43-51.