Welcome to Acta Agronomica Sinica,

Acta Agron Sin ›› 2015, Vol. 41 ›› Issue (04): 601-612.doi: 10.3724/SP.J.1006.2015.00601

• TILLAGE & CULTIVATION · PHYSIOLOGY & BIOCHEMISTRY • Previous Articles     Next Articles

Responses of the Stomatal Traits and Gas Exchange of Maize Leaves to Climate Warming

ZHENG Yun-Pu1,2,4,XU Ming2,*,WANG Jian-Shu3,QIU Shuai2,WANG He-Xin3   

  1. 1 School of water conservancy and hydropower, Hebei University of Engineering, Handan 056038, China; 2 Key Laboratory of Ecosystem Network Observation and Modeling, Institute of Geographical Sciences and Natural Resources, Chinese Academy of Sciences, Beijing 100101, China; 3School of agriculture, Hebei University of Engineering, Handan 056038, China; 4Institute of Modern Agricultural Research, Dalian University, Dalian 116622, China?
  • Received:2014-11-03 Revised:2015-02-06 Online:2015-04-12 Published:2015-03-03
  • Contact: 徐明,E-mail: mingxu@igsnrr.ac.cn E-mail:zhengyunpu_000@sina.com

Abstract:

Stomata are the pores on leaf surfaces controlling gas exchanges, mainly CO2 and water vapor, between the atmosphere and plants, and thus regulate carbon and water cycles in various ecosystems. This study investigated the effects of experimental warming on the stomatal frequency, stomatal aperture size and shape, and stomatal distribution pattern, and their relationships with the leaf gas exchange rates of maize (Zea may L.) leaves through a field manipulative warming experiment with infrared heaters in a typical agriculture ecosystem in the North China Plain. Our results showed that experimental warming had little effect on stomatal density, but increased stomatal index by 12% (P<0.05) due to the reduction in the number of epidermal cells under the warming treatment. Warming also decreased stomatal aperture length by 18% (P<0.01) and increased stomatal aperture width 26% (P<0.01). As a result, experimental warming increased the average stomatal aperture area by 31% (P<0.01) and stomatal aperture circumference by 13% (P<0.05), and resulted in a more regular stomatal distribution on both the adaxial and abaxial surfaces in leaves with an increased average nearest neighbor distance between stomata. In addition, experimental warming also affacted the gas exchange of maize leaves. Experimental warming significantly increased net photosynthetic rate (Pn), stomatal conductance (Gs), and transpiration rate (Tr) by 52% (P<0.05), 163% (P<0.001), and 81% (P<0.05), respectively. Meanwhile, experimental warming decreased the leaf dark respiration(Rd) by 24% (P<0.01), but had no significant effects on intercellular CO2 concentration (Ci) and water use efficiency (WUE; P>0.05). In conclusion, the experimental warming may affect the gas exchange of maize leaves through the changes of the stomatal traits including stomatal frequency, stomatal aperture size and shape, and stomatal distribution on leaves.

Key words: Global warming, Maize, Stomatal traits, Gas exchange, The North China Plain

[1]Woodward F I. Stomatal numbers are sensitive to increases in CO2 from preindustrial levels. Nature, 1987, 327: 617–618



[2]Hetherington A M, Woodward F I. The role of stomata in sensing and driving environmental change. Nature, 2003, 424: 901–908



[3]Franks P J, Beerling D J. Maximum leaf conductance driven by CO2 effects on stomatal size and density over geologic time. Proc Natl Acad Sci USA, 2009, 106: 10343–10347



[4]Haworth M, Heath J, McElwain J C. Differences in the response sensitivity of stomatal index to atmospheric CO2 among four genera of Cupressaceae conifers. Ann Bot, 2010, 105: 411–418



[5]Taylor S H, Franks P J, Hulme S P. Photosynthetic pathway and ecological adaptation explain stomatal trait diversity amongst grasses. New Phytol, 2012, 193: 387–396



[6]Lake J A, Woodward F I. Response of stomatal numbers to CO2 and humidity: control by transpiration rate and abscisic acid. New Phytol, 2008, 179: 397–404



[7]Ciais P, Denning A S, Tans P P. A three-dimensional synthesis of vegetation feedbacks in doubled CO2 climate experiments. J Geophys Res, 1997, 102: 5857–5872



[8]Buckley T N, Farquhar G D, Mott K A. Qualitative effects of patchy stomatal conductance distribution features on gas-exchange calculations. Plant Cell Environ, 1997, 20: 867–880



[9]Apple M E, Olszyk D M, Ormrod D P. Morphology and stomatal function of douglas fir needles exposed to climate change: Elevated CO2 and temperature. Int J Plant Sci, 2000, 161: 127–132



[10]Hovenden M J. The influence of temperature and genotype on the growth and stomatal morphology of southern beech, Nothofagus cunninghamii (Nothofagaceae). Aust J Bot, 2001, 49: 427-434



[11]Kouwenberg L L R, Kürschner W M, McElwain J C. Stomatal frequency change over altitudinal gradients: Prospects for paleoaltimetry. Rev Mineral Geochem, 2007, 66: 215–241



[12]Fraser L H, Greenall A, Carlyle C. Adaptive phenotypic plasticity of Pseudoroegneria spicata: response of stomatal density, leaf area and biomass to changes in water supply and increased temperature. Ann Bot, 2009, 103: 769–775



[13]Beerling D J, Chaloner W G. The impact of atmospheric CO2 and temperature change on stomatal density: Observations from Quercus robur Lammas leaves. Ann Bot, 1993, 71: 231–235



[14]Ferris R, Nijs I, Behaeghe T. Elevated CO2 and temperature have different effects on leaf anatomy of perennial ryegrass in spring and summer. Ann Bot, 1996, 78: 489–497



[15]Reddy K R, Robana R R, Hodges H F. Interactions of CO2 enrichment and temperature on cotton growth and leaf characteristics. Environ Exp Bot, 1998, 39: 117–129



[16]Xu Z Z, Zhou G S, Shimizu H. Effects of soil drought with nocturnal warming on leaf stomatal traits and mesophyll cell ultrastructure of a perennial grass. Crop Sci, 2009, 49: 1843–1851



[17]Xu Z Z, Zhou G S. Effects of water stress and high nocturnal temperature on photosynthesis and nitrogen level of a perennial grass Leymus chinensis. Plant Soil, 2005, 269: 131–139



[18]张立荣, 牛海山, 汪诗平, 李英年, 赵新全. 增温与放牧对矮嵩草草甸4种植物气孔密度和气孔长度的影响. 生态学报, 2010, 30: 6961–6969



Zhan  L R, Niu H S, Wang S P, Li Y N, Zhao X Q. Effects of temperature increase and grazing on stomatal density and length of four alpine Kobresia meadow species, Qinghai-Tibetan Plateau. Acta Ecol Sin, 2010, 30: 6961–6969 (in Chinese with English abstract)



[19]Croxdale J L. Stomatal patterning in monocotyledons: Tradescantia as a model system. J Exp Bot, 1998, 49: 279–292



[20]Berger D, Altmann T. A subtilisin-like serine protease involved in the regulation of stomatal density and distribution in Arabidopsis thaliana. Genes Dev, 2000, 14: 1119–1131



[21]Croxdale J L. Stomatal patterning in angiosperms. Am J Bot, 2000, 87: 1069–1080



[22]Bergermann D C, Lukowitz W, Somerville C R. Stomatal development and pattern controlled by a MAPKK Kinase. Science, 2004, 304: 1494–1497



[23]Juarez M, Twigg R, Timmermans M. Specification of adaxial cell fate during maize leaf development. Development, 2004, 131: 4533-4544



[24]Wang H, Ngwenyama N, Liu Y. Stomatal development and patterning are regulated by environmentally responsive mitogen-actived protein kinases in Arabidopsis. Plant Cell, 2007, 19: 63–73



[25]Casson S A, Hetherington A M. Environmental regulation of stomatal development. Curr Opin Plant Biol, 2010, 13: 90–95



[26]Ciha A J, Brun W A. Stomatal size and frequency in soybeans. Crop Sci, 1975, 15: 309–313



[27]Green R L, Beard J B, Casnoff D M. Leaf blade stomatal characterizations and evapotranspiration rates of 12 cool-season perennial grasses. HortScience, 1990, 25: 760–761



[28]Driscoll S P, Prins A, Olmos E. Specification of adaxial and abaxial stomata, epidermal structure and photosynthesis to CO2 enrichment in maize leaves. J Exp Bot, 2006, 57: 381–390



[29]Salisbury E J. On the causes and ecological significance of stomatal frequency, with special reference to the woodland flora. Philos Trans R Soc Lond B Biol Sci, 1927, 216: 1–65



[30]Sharma G K, Dunn D B. Environmental modifications of leaf surface traits in Datura stramonium. Can J Bot, 1969, 47: 1211–1216



[31]Tichá I. Photosynthetic characteristics during ontogenesis of leaves. 7. Stomata density and sizes. Photosynthetica, 1982, 16: 375–471



[32]Zacchini M, Morini S, Vitagliano C. Effect of photoperiod on some stomatal characteristics of in vitro cultured fruit tree shoots. Plant Cell Tissue Organ Cult, 1997, 49: 195–200



[33]Stancato G C, Mazzoni-Viveiros S C, Luchi A E. Stomatal characteristics in different habitat forms of Brazilian species of Epidendrum (Orchidaceae). Nord J Bot, 1999, 19: 271–275



[34]Tao F, Yokozawa M, Xu Y, Hayashi Y, Zhang Z. Climate changes and trends in phenology and yields of field crops in China, 1981–2000. Agric For Meteorol, 2006, 138: 82–92



[35]Lin E. Agricultural vulnerability and adaptation to global warming in China. Water Air Soil Pollut, 1996, 92: 63–73



[36]Mo X G, Liu S X, Lin Z H, Guo R P. Regional crop yield, water consumption and water use efficiency and their responses to climate change in the North China Plain. Agric Ecosyst Environ, 2009, 134: 67–78



[37]Liu S X, Mo X G, Lin Z H, Xu Y Q, Ji J J, Wen G, Richey J. Crop yield responses to climate change in the Huang-Huai-Hai Plain of China. Agric Water Manage, 2010, 97: 1195–1209



[38]Tao F L, Zhang S, Zhang Z. Spatiotemporal changes of wheat phenology in China under the effects of temperature, day length and cultivar thermal characteristics. Eur J Agron, 2012, 43: 201–212



[39]Hou R X, Ou-Yang Z, Li Y S. Is the change of winter wheat yield under warming caused by shortened reproductive period? Ecol Evol, 2012, 2: 2999–3008



[40]Lobell D B, Field C B. Global scale climate–crop yield relationships and the impacts of recent warming. Environ Res Lett, 2007, 2: 1–7



[41]Ripley B D. The second-order analysis of stationary processes. J Appl Prob, 1976, 13: 255–266



[42]Lomax B H, Woodward F I, Leitch I J. Genome size as a predictor of guard cell length in Arabidopsis thaliana is independent of environmental conditions. New Phytol, 2009, 181: 311–314



[43]Djanaguiraman M, Prasad P V V, Boyle D L. High-temperature stress and soybean leaves: leaf anatomy and photosynthesis. Crop Sci, 2011, 51: 2125–2131

[1] Liang Jin-Yu, Yin Jia-De, Wang Hong-Li, Zhang Guo-Ping, Hou Hui-Zhi, Dong Bo, Ma Ming-Sheng. Estimation of leaf nitrogen content in dryland forage maize using UAV-based hyperspectral imaging and machine learning [J]. Acta Agronomica Sinica, 2026, 52(6): 1788-1801.
[2] Yang Xin-Yu, Cui Wen-Tao, Dilinigeer Alimu, Wang Kai-Xiang, Wu Peng-Hao, Ren Jiao-Jiao. Genome-wide association and genomic selection analysis of the number of leaves above the ear in maize [J]. Acta Agronomica Sinica, 2026, 52(5): 1573-1590.
[3] Han Ya-Xin, He Guan-Hua, Zhang Xiao-Qiong, Zhang Deng-Feng, Li Yong-Xiang, Liu Xu-Yang, Wang Tian-Yu, Li Yu, Zou Hua-Wen, Li Chun-Hui. Identification of maize lateral root density genes resources through integrated RNA-seq and BSA-seq analyses [J]. Acta Agronomica Sinica, 2026, 52(5): 1341-1352.
[4] Sun Shu-Feng, Xu Zhen-Nan, Huang Jia-Xin, Weng Jian-Feng, Li Xin-Hai. Genome-wide identification of the maize MAPK gene family and its response to Fusarium verticillioides infection [J]. Acta Agronomica Sinica, 2026, 52(5): 1291-1308.
[5] Zhang Ning-Ning, Teng Yu-Fei, Ren Na-Na, Wei Xing-Zhuo, Yan Shu-Hao, Fan Ke-Xin, Wang Yong-Hong, Chen Wen-Kang, Zhang Xing-Hua, Zhu Wan-Chao, Xu Shu-Tu, Xue Ji-Quan. Phenotypic evaluation and plasticity analysis of drought resistance in 201 maize inbred lines [J]. Acta Agronomica Sinica, 2026, 52(5): 1309-1325.
[6] Zhang Hong-Rong, Wang Fei-Er, Li Pan, Qiu Hai-Long, Zhu Jing, Zhao Lian-Hao, Nan Yun-You, He Wei, Fan Zhi-Long, Hu Fa-Long, Chai Qiang, Yin Wen. Photosynthetic characteristics of 20% reduced irrigation combined with 25% organic substitution for chemical fertilizer in increasing silage maize yield [J]. Acta Agronomica Sinica, 2026, 52(5): 1487-1500.
[7] Yang Yang, Chang Shi-Hui, Tian Hong-Li, Yi Hong-Mei, Wang Lu, Ren Jie, Fan Ya-Ming, Liu Ya-Wei, Wang Feng-Ge, Zhao Jiu-Ran. Genetic diversity analysis of nationally approved maize varieties in different ecological regions [J]. Acta Agronomica Sinica, 2026, 52(5): 1352-1364.
[8] Li Kun, Ji Ya-Teng, Tian Yin-Shuai, Hu Min-Hang, Liu Liang, Li Fei, Li Guo-Qiang, Hao Li-Hua, Zheng Yun-Pu. Effects of CO2 and NaCl on stomatal traits, photosynthetic performance, and antioxidant systems in soybean [J]. Acta Agronomica Sinica, 2026, 52(4): 1251-1267.
[9] Cai Hong-Wei, Yu Ai-Zhong, Jiang Ke-Qiang, Wang Peng-Fei, Wang Yu-Long, Huo Jian-Zhe, Pang Xiao-Neng, Yin Bo, Shang Yong-Pan. Key mechanisms underlying the enhancement of sweet maize yield through partial substitution of chemical fertilizers with organic manure in arid irrigation districts [J]. Acta Agronomica Sinica, 2026, 52(4): 1166-1180.
[10] Tian Hong-Li, Yang Yang, Fan Ya-Ming, Yi Hong-Mei, Guo Dan-Dan, Wang Feng-Ge, Zhao Jiu-Ran. A novel set of tri-allelic variant SNP loci suitable for maize variety identification [J]. Acta Agronomica Sinica, 2026, 52(4): 993-1005.
[11] Guo Xiang-Yang, Tu Liang, Wang Dong, Liu Peng-Fei, Wang An-Gui, Yi Qiang, Ren Hong, Li Gang, Zhu Yun-Fang, Wu Xun, Jiang Yu-Lin, Tian Feng, Chen Ze-Hui. Application and prospects of Suwan germplasm in maize breeding in China [J]. Acta Agronomica Sinica, 2026, 52(3): 655-664.
[12] Meng Cheng, Wang Zhe. Genome-wide identification and expression analysis of the ZmPFK gene family under biotic and abiotic stresses in maize [J]. Acta Agronomica Sinica, 2026, 52(3): 764-779.
[13] Li Xin-Hao, Xing Meng-Ke, Zhou Zi-Hui, Li Si-Ye, Ren Hao, Wang Hong-Zhang, Lai Hua-Jiang. Exogenous melatonin enhances heat tolerance of maize at the seedling stage by coordinating light and dark reactions [J]. Acta Agronomica Sinica, 2026, 52(3): 839-856.
[14] Ma Liang, Ma Lu, Zhang Shu-Yu, Zhang Hui-Min, Wang Ren-Ming, Song Xu-Dong, Zhang Zhen-Liang, Mao Yu-Xiang, Lu Hu-Hua, Chen Guo-Qing, Hao De-Rong, Zhou Guang-Fei. Transcriptome analysis and identification of candidate genes associated with husk number in maize [J]. Acta Agronomica Sinica, 2026, 52(3): 790-801.
[15] Liu Ji-Chang, Li Si-Ye, Li Xue-Ting, Wang Hong-Zhang, Liu Peng, Zhang Ji-Wang, Zhao Bin, Ren Bai-Zhao, Ren Hao. Effects of salt stress on root growth and nutrient absorption efficiency of different salt-tolerant summer maize varieties [J]. Acta Agronomica Sinica, 2026, 52(2): 565-577.
Viewed
Full text


Abstract

Cited

  Shared   
  Discussed   
No Suggested Reading articles found!