Welcome to Acta Agronomica Sinica,

Acta Agronomica Sinica ›› 2019, Vol. 45 ›› Issue (6): 949-956.doi: 10.3724/SP.J.1006.2019.81081

• RESEARCH NOTES • Previous Articles     Next Articles

Responses of leaf gas exchange to high temperature and drought combination as well as re-watering of winter wheat under doubling atmospheric CO2 concentration

Li-Li GUO1,*,Xi-Xi ZHANG1,*,Li-Hua HAO1,*(),Ya-Jun QIAO2,Wen-Na CHEN3,Yun-Ze LU3,Fei LI1,Xu CAO1,Qing-Tao WANG3,Yun-Pu ZHENG1,*()   

  1. 1 School of Water Conservancy and Hydropower, Hebei University of Engineering, Handan 056038, Hebei, China
    2 Ecology and Environment Bureau of Xiong’an New District in Hebei, Xiong’an 071700, Hebei, China;
    3 School of Landscape and Ecological Engineering, Hebei University of Engineering, Handan 056038, Hebei, China
  • Received:2018-11-04 Accepted:2019-01-19 Online:2019-06-12 Published:2019-06-12
  • Contact: Li-Li GUO,Xi-Xi ZHANG,Li-Hua HAO,Yun-Pu ZHENG E-mail:haolihua_000@sina.com;zhengyunpu_000@sina.com
  • Supported by:
    This study was supported by the National Key Research and Development Program of China(2017YFD0300905);the Hebei Province Foundation for Returnees(CN201702);the Innovation Capability Upgrading Plan of Hebei Province(18965307H);the Hebei Province Graduate Student Innovation Ability Subsidized Project(CXZZSS2018077);the Drought Meteorological Science Research Foundation Project(IAM201702)


Understanding the responsible mechanisms of crops to combined environmental stresses such as elevated CO2 concentration, climate warming, and drought is critical to improve the accuracy of ecological process models, and thus accurately predict the impacts of global climate change on the Net Primary Production (NPP) and ecosystem service function of farmlands. Four environmental growth chambers accurately controlling CO2 concentration and temperature were employed to investigate the combined effects of high temperature and drought stresses on the stomatal traits and leaf gas exchange during re-watering under doubling CO2 concentration. We found that elevated CO2 concentration (E) increased the stomatal density, decreased the stomatal width and made the spatial distribution pattern of stomata irregular on the abaxial leaf surface, while enhanced the net photosynthetic rates (Pn), stomatal conductance (Gs), transpiration rates (Tr), and water use efficiency (WUE). The stomatal length, width, perimeter and area were substantially decreased under the combined high temperature and drought stress (HD), resulting in dramatic decline of leaf gas exchange parameters. Doubling CO2 concentration made the leaf gas exchange parameters enhanced under the HD treatment, suggesting that elevated CO2 concentration can compensate the negative impacts of heat and drought on the physiological processes of winter wheat. Additionally, the leaf gas exchange of winter wheat subjected to the high temperature and drought stresses was enhanced after re-watering, but these parameters were still lower than those of Control, suggesting that the photosynthetic apparatus may be damaged by the combined high temperature and drought stresses.

Key words: CO2 concentration, high temperature and drought, re-watering, gas exchange parameters, stomatal traits

Table 1

Effects of the combined stress of high temperature and drought on stomatal parameters of winter wheat under doubling CO2 concentration"

Stomatal parameter
Leaf surface
Stomatal density (No. mm-2)
近轴面Adaxial 53.7±1.5 c 53.5±4.6 c 74.1±5.5 a 64.6±8.2 b 0.001
远轴面Abaxial 33.1±1.1 b 41.7±1.2 a 44.1±8.5 a 48.1±2.9 a 0.008
Stomatal length (μm)
近轴面Adaxial 37.3±3.2 a 38.1±1.8 a 31.7±3.3 b 36.1±2.0 a 0.007
远轴面Abaxial 34.1±2.7 ab 31.9±2.8 b 31.9±3.9 b 36.0±2.4 a 0.003
Stomatal width (μm)
近轴面Adaxial 3.5±0.6 a 3.1±0.4 b 3.1±0.5 b 2.6±0.3 c 0.000
远轴面Abaxial 2.8±0.3 ab 3.1±0.4 a 2.6±0.4 b 2.6±0.4 b 0.041
Stomatal perimeter (μm)
近轴面Adaxial 77.5±7.2 a 79.6±3.7 a 67.3±6.2 b 76.2±7.4 a 0.007
远轴面Abaxial 71.6±6.0 ab 66.5±6.2 bc 65.8±7.6 c 76.2±4.8 a 0.005
Stomatal area (μm2)
近轴面Adaxial 119.4±18.7 a 109.7±11.7 a 87.3±11.0 b 94.3±11.8 b 0.000
远轴面Abaxial 87.0±12.8 ab 92.2±14.9 a 79.7±16.2 b 95.8±14.8 a 0.067
Stomatal shape index (%)
近轴面Adaxial 14.0±1 a 13.1±1 b 13.9±1 a 13.0±1 b 0.002
远轴面Abaxial 13.0±1 bc 14.5±1 a 13.5±1 b 12.8±1 c 0.001

Fig. 1

Effects of the combined stress of high temperature and drought on spatial distribution pattern of stomata on the adaxial (a) and abaxial (b) leaf surface of winter wheat under doubling CO2 concentration The upper 95% means the upper boundary of the 95% confidence envelope, the lower 95% means the lower boundary of the 95% confidence envelope. The Lhat(d) value is the nearest neighbor distance, and stomata follow a regular distribution at the scale when the Lhat(d) value is lower than the 95% boundary with the smaller the minimum Lhat(d) value, the more regular spatial distribution pattern of stomata."

Fig. 2

Effects of the combined stress of warming and drought as well as re-watering on the net photosynthetic rate of winter wheat under doubling CO2 concentration"

Fig. 3

Effects of the combined stress of high temperature and drought as well as re-watering on stomatal conductance of winter wheat under doubling CO2 concentration"

Fig. 4

Effects of the combined stress of high temperature and drought as well as re-watering on transpiration rate of winter wheat under doubling CO2 concentration"

Fig. 5

Effects of the combined stress of high temperature and drought as well as re-watering on water use efficiency of winter wheat under doubling CO2 concentration"

[1] IPCC. Climate Change:the Physical Science Basis.Cambridge: Cambridge University Press, 2007.
[2] Lin E, Xiong W, Hui J, Xu Y L, Li Y, Bai, L P, Xie, L Y . Climate change impacts on crop yield and quality with CO2 fertilization in China. Philos Trans R Soc London Ser B, 2005,360:2149-2154.
doi: 10.1098/rstb.2005.1743 pmid: 16433100
[3] 司福艳, 乔匀周, 姜净卫, 董宝娣, 师长海, 刘孟雨 . 干旱高温及高浓度CO2复合胁迫对冬小麦生长的影响. 应用生态学报, 2014,25:2605-2612.
Si F Y, Qiao Y Z, Jiang J W, Dong B D, Shi C H, Liu M Y . Effects of drought stress, high temperature and elevated CO2 concentration on the growth of winter wheat. Chin J Appl Ecol, 2014,25:2605-2612 (in Chinese with English abstract).
[4] Salvucci M E , Crafes-brander S J. Inhibition of photosynthesis by heat stress: the activation state of rubisco as a limiting factor in photosynthesis. Physiol Plant, 2004,120:179-186.
doi: 10.1111/j.0031-9317.2004.0173.x pmid: 15032851
[5] Collins W D, Craig A P, Truesdale J E, Divittari A V, Jones A D, Bond-Lambery B, Calvin K V, Edmond J A, Kim S H, Thomson A M, Patel P, Zhou Y, Mao J, Shi X, Thornton P E, Chini L P, Hrrtt G C . The integrated earth system model (iESM): formulation and functionality. Geosci Model Dev, 2015,8:2203-2219.
doi: 10.5194/gmd-8-2203-2015
[6] Shi Y F, Zhang X S . The impact of climate change on the surface water resources in arid area of Northwest China and future trend. Sci China, Series B Chem, 1995,25:968-977.
[7] 张存杰, 王胜, 宋艳玲, 蔡雯悦 . 我国北方地区冬小麦干旱灾害风险评估. 干旱气象, 2014,32:883-893.
Zhang C J, Wang S, Song Y L, Cai W Y . Research of drought risk assessment for winter wheat in Northern China. J Arid Meteorol, 2014,32:883-893 (in Chinese with English abstract).
[8] Chen Y J, Yu J J, Huang B R . Effects of elevated CO2 concentration on water relations and photosynthetic responses to drought stress and recovery during rewatering in Tall Fescue. J Am Soc Hort Sci, 2015,140:19-26.
[9] Nilsen E T, Orcutt D M . The physiology of Plants under Stress. New York: John Wiley  Sons, Ins., 2000. pp 105-109.
[10] Reddy, A R ,Rasineni G K, Raghavendra A S . The impact of global elevated CO2 concentration on photosynthesis and plant productivity. Curr Sci, 2010,99, 46-57.
doi: 10.1371/journal.pone.0011405
[11] Xu M . The optimal atmospheric CO2 concentration for the growth of winter wheat (Triticum aestivum). J Plant Physiol, 2015,184:89-97.
[12] 胡田田, 康绍忠 . 植物抗旱性中的补偿效应及其在农业节水中的应用. 生态学报, 2005,25:885-891.
Hu T T, Kang S Z . The compensatory effect in drought resistance of plants and its application in water-saving agriculture. Acta Ecol Sin, 2005,25:885-891 (in Chinese with English abstract).
[13] 倪胜利, 李兴茂, 王亚翠, 任根深 . 旱后复水对冬小麦生长发育及水分利用效率的影响. 灌溉排水学报, 2018,37(11):20-25.
Ni S L, Li X M, Wang Y C, Ren G S . Effects of rewatering after drought on growth and water use efficiency of winter wheat. J Irrig Drain, 2018,37(11):20-25 (in Chinese with English abstract).
[14] Robredo A ,Pérez-lópez U, Maza H S D L, González-Moro B, Lacueata M, Mena-Petite A, Muñoz-Rueda A . Elevated CO2 alleviates the impact of drought on barley improving water status by lowering stomatal conductance and delaying its effects on photosynthesis. Environ Exp Bot, 2007,59:252-263.
doi: 10.1016/j.envexpbot.2006.01.001
[15] 廖建雄, 王根轩 . 干旱、CO2和温度升高对春小麦光合、蒸发蒸腾及水分利用效率的影响. 应用生态学报, 2002,13:547-550.
Liao J X, Wang G X . Effects of drought, CO2 concentration and temperature increasing on photosynthesis rate, evapotranspiration, and water use efficiency of spring wheat. Chin J Appl Ecol, 2002,13:547-550 (in Chinese with English abstract).
[16] Zheng Y P, Xu M, Hou R X, Shen R C, Qiu S, Ouyang Z . Effects of experimental warming on stomatal traits in leaves of maize (Zea may L.). Ecol Evol, 2013,3:3095-3111.
doi: 10.1002/ece3.674 pmid: 24101997
[17] Xu L X, Yu J J, Han L B, Huang B R . Photosynthetic enzyme activities and gene expression associated with drought tolerance and post-drought recovery in Kentucky bluegrass. Environ Exp Bot, 2013,89:28-35.
doi: 10.1016/j.envexpbot.2012.12.001
[18] 李继文, 王进鑫, 张慕黎, 吉增宝, 薛设 . 干旱及复水对刺槐叶水势的影响. 西北林学院学报, 2009,24(3):33-36.
Li J W, Wang J X, Zhang M L, Ji Z B, Xu S . Effect of drought and rewater on leaf water potential of Robinia pseudoacacia. J Northwest For Univ, 2009,24(3):33-36 (in Chinese with English abstract).
[19] 叶波, 吴永波, 邵维, 杨静 . 高温干旱复合处理及复水对构树 (Broussonetia papyrifera) 幼苗光合特性和叶绿素荧光参数的影响. 生态学杂志, 2014,33:2343-2349.
Ye B, Wu Y B, Shao W, Yang J . Effects of combined stress of elevated temperature and drought and of re-watering on the photosynthetic characteristics and chlorophyll fluorescence parameters of Broussonetia papyrifera seedlings. Chin J Ecol, 2014,33:2343-2349 (in Chinese with English abstract).
[20] Inamullahai I, Isoda A . Adaptive responses of soybean and cotton to water stress: I. Transpiration changes in relation to stomatal area and stomatal conductance. Plant Prod Sci, 2005,8:16-26.
doi: 10.1626/pps.8.131
[21] Kang S Z, Zhang F C, Hu X T, Hang J H . Benefits of CO2 enrichment on crop plants are modified by soil water. Plant Soil, 2002,238:69-77.
doi: 10.1023/A:1014244413067
[22] 于海秋, 武志海, 沈秀瑛, 徐克章 . 水分胁迫下玉米叶片气孔密度、大小及显微结构的变化. 吉林农业大学学报, 2003,25:239-242.
Yu H Q, Wu Z H, Shen X Y, Xu K Z . Changes of stomatal density, length, width and microstructure of maize leaves under water stress. J Jilin Agric Univ, 2003,25:239-242 (in Chinese with English abstract).
[23] 朱玉, 黄磊, 郑云普, 郝立华, 姜国斌, 王贺新, 李根柱, 张自川, 弓晓杰 . 高温对高丛越橘叶片气孔特征和气体交换参数的影响. 果树学报, 2016,33:444-456.
Zhu Y, Huang L, Zheng Y P, Hao L H, Jiang G B, Wang H X, Li G Z, Zhang Z C, Gong X J . Effects of high temperatures on leaf stomatal traits and gas exchanges of high bush blueberries. J Fruit Sci, 2016,33:444-456 (in Chinese with English abstract).
[24] Wang W J, Duan B, Zhang Y . Effects of experimental warming on growth, biomass allocation, and needle chemistry of Abies faxoniana in even-aged monospecific stands. Plant Ecol, 2012,213:47-55.
doi: 10.1007/s11258-011-0005-1
[25] Gan Y, Zhou L, Shen Z J, Shen Z X, Zhang Y Q, Wang G X . Stomatal clustering, a new marker for environmental perception and adaptation in terrestrial plants. Bot Studies, 2010,51:325-336.
doi: 10.1007/s00280-006-0217-6
[26] 郑云普, 徐明, 王建书, 邱帅, 王贺新 . 玉米叶片气孔特征及气体交换过程对气候变暖的响应. 作物学报, 2015,41:601-612.
Zheng Y P, Xu M, Wang J S, Qiu S, Wang H X . Responses of the stomatal traits and gas exchange of maize leaves to climate warming. Acta Agron Sin, 2015,41:601-612 (in Chinese with English abstract).
[27] 樊良新, 刘国彬, 薛萣, 杨婷, 张昌胜 . CO2浓度倍增及干旱胁迫对紫花苜蓿光合生理特性的协同影响. 草地学报, 2014,22(1):85-93.
Fan L X, Liu G B, Xue S, Yang T, Zhang C S . Synergistic effects of doubled CO2 concentration and drought stress on the photosynthetic characteristics of Medicago sativa. Acta Agrest Sin, 2014,22(1):85-93 (in Chinese with English abstract).
[28] 张凯, 王润元, 王鹤龄, 赵鸿, 齐月, 赵福年, 陈斐, 雷俊 . CO2浓度升高对半干旱区春小麦生长发育及产量影响的试验研究. 干旱气象, 2017,35:306-312.
Zhang K, Wang R Y, Wang H L, Zhao H, Qi Y, Zhao F N, Chen F, Lei J . Effects of elevated CO2 concentration on growth and yield of spring wheat based on observational experiment in semi-arid area. J Arid Meteorol, 2017,35:306-312 (in Chinese with English abstract).
[29] Mittler R . Abiotic stress the field environment and stress combination. Trends Plant Sci, 2006,11:15-19.
doi: 10.1016/j.tplants.2005.11.002 pmid: 16359910
[30] 刘振山 . 小麦苗期干旱、高温和旱热共胁迫转录表达谱及ABD部分同源基因表达分化分析. 中国农业大学博士学位论文, 北京, 2015.
Liu Z S . Transcriptome Profiling and Differential Homeologous Genes Expression Analysis of Wheat (Triticum aestivum L.) seedlings During Drought Stress, Heat Stress and Their Combination . PhD Dissertation of China Agricultural University, Beijing,China, 2015 (in Chinese with English abstract).
[31] 李伏生, 康绍忠, 张富仓 . CO2浓度、氮和水分对春小麦光合、蒸散及水分利用效率的影响. 应用生态学报, 2003,14:387-393.
Li F S, Kang S Z, Zhang F C . Effects of CO2 enrichment, nitrogen and water on photosynthesis, evapotranspiration and water use efficiency of spring wheat. Chin J Appl Ecol, 2003,14:387-393 (in Chinese with English abstract).
[32] Hamerlynck E P, Huxman T E, Loik M E, Smith S D . Effects of extreme high temperature, drought and elevated CO2 on photosynthesis of the Mojave Desert evergreen shrub,Larreatriden-tate. Plant Ecol, 2000,148:183-193.
[33] 刘璇, 吴永波, 邵维 . 高温干旱复合处理及复水对刺槐幼苗水分运输的影响. 生态科学, 2018,37(2):100-105.
Liu X, Wu Y B, Shao W . The combined stress of elevated temperature and drought and rewatering on water transportation of Robinia pseudoqcacia Linn. seedling. Ecol Sci, 2018,37(2):100-105 (in Chinese with English abstract).
[34] Wu D X, Wang G X, Bai Y F, Liao J X . Effects of elevated CO2 concentration on growth, water use, yield and grain quality of wheat under two soil water levels. Agric Ecosyst Environ, 2004,104:493-507.
doi: 10.1016/j.agee.2004.01.018
[35] 徐俊增, 彭世彰, 魏征, 缴锡云 . 节水灌溉水稻叶片细胞间CO2浓度及气孔与非气孔限制. 农业工程学报, 2010,26(7):76-80.
Xu J Z, Peng S Z, Wei Z, Jiao X Y . Intercellular CO2 concentration and stomatal or non-stomatal limitation of rice under water saving irrigation. Trans CSAE, 2010,26(7):76-80 (in Chinese with English abstract).
[36] Farquhar G D, Sharkey T D . Stomatal conductance and photosynthesis. Annu Rev Plant Physiol, 1982,33:317-345.
[1] LI A-Li, FENG Ya-Nan, LI Ping, ZHANG Dong-Sheng, ZONG Yu-Zheng, LIN Wen, HAO Xing-Yu. Transcriptome analysis of leaves responses to elevated CO2 concentration, drought and interaction conditions in soybean [Glycine max (Linn.) Merr.] [J]. Acta Agronomica Sinica, 2022, 48(5): 1103-1118.
[2] Fei LI,Liang LIU,Hao ZHANG,Qing-Tao WANG,Li-Li GUO,Li-Hua HAO,Xi-Xi ZHANG,Xu CAO,Wei-Jia LIANG,Yun-Pu ZHENG. Effects of CO2 Concentrations on Stomatal Traits and Gas Exchange in Leaves of Soybean [J]. Acta Agronomica Sinica, 2018, 44(8): 1212-1220.
[3] Hai-Xia WU,Li-Li GUO,Li-Hua HAO,Hao ZHANG,Qing-Tao WANG,Dong-Juan CHENG,Zheng-Ping PENG,Fei LI,Xi-Xi ZHANG,Shu-Bin LI,Ming XU,Yun-Pu ZHENG. Effects of Water and CO2 Concentration on Stomatal Traits, Leaf Gas Exchange, and Biomass of Winter Wheat [J]. Acta Agronomica Sinica, 2018, 44(10): 1570-1576.
[4] ZHENG Yun-Pu,XU Ming,WANG Jian-Shu,QIU Shuai,WANG He-Xin. Responses of the Stomatal Traits and Gas Exchange of Maize Leaves to Climate Warming [J]. Acta Agron Sin, 2015, 41(04): 601-612.
[5] XU Yo-Ban, CHEN Yu-Fang, LI Shi-Qing. Effect of Elevated CO2 Concentration and Nitrogen Application on Translocation of Dry Matter and Nitrogen Restored before Anthesis in Winter Wheat [J]. Acta Agron Sin, 2011, 37(08): 1465-1474.
[6] LIU Rui-Xian;GUO Wen-Qi;CHEN Bing-Lin;ZHOU Zhi-Guo. Effects of Nitrogen on the Antioxidant Enzyme Activities and Endogenous Hormone Contents of Cotton Leaf under Drought Stress and after Soil Re-Watering during the Flowering and Boll-Forming Stage [J]. Acta Agron Sin, 2008, 34(09): 1598-1607.
[7] LIN Fan-Yun;WANG Shi-Qiang;HU Yin-Gang;HE Bei-Ru. Cloning of A S-Adenosylmethionine Synthetase Gene from Broomcorn Millet (Panicum miliaceum L.) and Its Expression during Drought and Re-Watering [J]. Acta Agron Sin, 2008, 34(05): 777-782.
[8] LI Yan;ZHAO Xiao-Ming;XIA Xiu-Ying;LUAN Yu-Shi;DU Yu-Guang;LI Feng-Lan. Effects of Oligochitosan on Photosynthetic Parameter of Brassica napus Seedlings under Drought Stress [J]. Acta Agron Sin, 2008, 34(02): 326-329.
[9] KANG Gong-Ping;XU Guo-Yun;CHEN Zhi;XU Meng-Liang;CHEN Liang-Bi. Photosynthetic Characteristics of Chaling Wild Rice [J]. Acta Agron Sin, 2007, 33(09): 1558-1562.
Full text



No Suggested Reading articles found!