The coordinated relationship of stomatal and leaf economic traits in dicotyledonous plants of the Qinghai-Tibet Plateau and their response to environmental changes

GONG Baocao; WANG Xiangtai; YIN Bing; LUO Shuaiwei; DU Guozhen

doi:10.11829/j.issn.1001-0629.2023-0727

Pratacultural Science > 2025 > Accepted Manuscript > DOI: 10.11829/j.issn.1001-0629.2023-0727

GONG B C, WANG X T, YIN B, LUO S W, DU G Z. The coordinated relationship of stomatal and leaf economic traits in dicotyledonous plants of the Qinghai-Tibet Plateau and their response to environmental changes. Pratacultural Science, 2025, 42(0): 1-10. DOI: 10.11829/j.issn.1001-0629.2023-0727

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The coordinated relationship of stomatal and leaf economic traits in dicotyledonous plants of the Qinghai-Tibet Plateau and their response to environmental changes

GONG Baocao^{1, 2,},
WANG Xiangtai^{1, 2},
YIN Bing^{1, 2},
LUO Shuaiwei^{1, 2},
DU Guozhen^{1, 2, ,}

1.
College of Ecology, Lanzhou University, Lanzhou, 730000, Gansu, China
2.
State Key Laboratory of Herbage Improvement and Grassland Agro-ecosystem, Lanzhou, 730000, Gansu, China

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Corresponding author:
DU Guozhen　E-mail: guozdu@slzu.edu.cn
Received Date: December 27, 2023
Accepted Date: January 28, 2024
Available Online: April 14, 2025

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Abstract

Abstract

Stomata, as important portals between the leaves and atmosphere, define the water and gas exchange-related abilities in plants. Leaf dry mass per area (LMA), as the core leaf economic trait, reflects plant resource utilization efficiency. Therefore, studying the coordination between these two traits and how it changes with environmental factors is of particular significance, potentially contributing to our understanding of plant adaptation and community assembly. In this study, we investigated stomatal trait variabilities, correlations between stomatal traits and LMA, and the response pattern of these correlations along the environmental gradients of 58 common dicotyledon species in the alpine meadow of the Qinghai-Tibet Plateau. Our results demonstrated the following: 1) Higher-level stomatal trait variations could be observed on the dicotyledon leaf upper epidermis than on the lower surface. Moreover, stomatal density variation and the stomatal pore index (SPI) values were the highest on the upper epidermis. 2) A strong coordination could be detected between LMA and stomatal traits (i.e., stomatal density and SPI) (P < 0.05). 3) The correlation between LMA and stomatal traits changed along the environmental gradient. The coordination increased with soil water content reduction and soil pH increase. In summary, this study provides new insights into the interactions between plant leaf traits and adaptation strategies in response to the climate change.
- leaf dry mass per area,
- stomatal traits,
- coordination,
- environmental gradient,
- Qinghai-Tibet Plateau,
- amphistomy,
- alpine meadow

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[1]	ACKERLY D D, KNIGHT C A, WEISS S B, BARTON K E, STARMER K P. Leaf size, specific leaf area and microhabitat distribution of chaparral woody plants: contrasting patterns in species level and community level analyses. Oecologia, 2002, 130(3): 449-457. doi: 10.1007/s004420100805
[2]	LUNDGREN M R, MATHERS A, BAILLIE A L, DUNN J A, WILSON M J, HUNT L, PAJOR R, FRADERA-SOLER M, ROLFE S A, OSBORNE C P, STURROCK C J, GRAY J E, MOONEY S J, FLEMING A J. Mesophyll porosity is modulated by the presence of functional stomata. Nature Communications, 2019, 10: 2825. doi: 10.1038/s41467-019-10826-5
[3]	BLACKMAN C J, ASPINWALL M J, DE DIOS V R, SMITH R A, TISSUE D T. Leaf photosynthetic, economics and hydraulic traits are decoupled among genotypes of a widespread species of eucalypt grown under ambient and elevated CO₂. Functional Ecology, 2016, 30(9): 1491-1500. doi: 10.1111/1365-2435.12661
[4]	SACK L, COWAN P D, JAIKUMAR N S, HOLBROOK N M. The ‘hydrology’ of leaves: co-ordination of structure and function in temperate woody species. Plant Cell and Environment, 2003, 26(8): 1343-1356. doi: 10.1046/j.0016-8025.2003.01058.x
[5]	WRIGHT I J, REICH P B, WESTOBY M, ACKERLY D D, BARUCH Z, BONGERS F, CAVENDER-BARES J M, CHAPIN T, CORNELISSEN J H, DIEMER M W, FLEXAS J, GARNIER E, GROOM P K, GULÍAS J, HIKOSAKA K, LAMONT B B, LEE T D, LEE W, LUSK C H, MIDGLEY J J, NAVAS M, NIINEMETS Ü, OLEKSYN J, OSADA N, POORTER H, POOT P, PRIOR L D, PYANKOV V I, ROUMET C, THOMAS S C, TJOELKER M G, VENEKLAAS E J, VILLAR R. The worldwide leaf economics spectrum. Nature, 2004, 428: 821-827. doi: 10.1038/nature02403
[6]	FRESCHET G T, CORNELISSEN J H, VAN LOGTESTIJN R S, AERTS R. Evidence of the ‘plant economics spectrum’ in a subarctic flora. Journal of Ecology, 2010, 98(2): 362-373. doi: 10.1111/j.1365-2745.2009.01615.x
[7]	HE J S, WANG Z H, WANG X P, SCHMID B, ZUO W Y, ZHOU M, ZHENG C Y, WANG M F, FANG J Y. A test of the generality of leaf trait relationships on the Tibetan Plateau. New Phytologist, 2006, 170(4): 835-848. doi: 10.1111/j.1469-8137.2006.01704.x
[8]	王瑞丽, 于贵瑞, 何念鹏, 王秋凤, 赵宁, 徐志伟. 气孔特征与叶片功能性状之间关联性沿海拔梯度的变化规律—以长白山为例. 生态学报, 2016, 36(8): 2175-2184. WANG R L, YU G R, HE N P, WANG Q F, ZHAO N, XU Z W. Altitudinal variation in the covariation of stomatal traits with leaf functional traits in Changbai Mountain. Acta Ecologica Sinica, 2016, 36(8): 2175-2184.
[9]	YIN Q L, WANG L, LEI M L, DANG H, QUAN J X, TIAN T T, CHAI Y F, YUE M. The relationships between leaf economics and hydraulic traits of woody plants depend on water availability. Science of The Total Environment, 2018, 621: 245-252. doi: 10.1016/j.scitotenv.2017.11.171
[10]	史作民, 冯秋红, 程瑞梅, 刘世荣. 叶肉细胞导度研究进展. 生态学报, 2010, 30(17): 4792-4803. SHI Z M, FENG Q H, CHENG R M, LIU S R. The research progress of mesophyll conductance. Acta Ecologica Sinica, 2010, 30(17): 4792-4803.
[11]	SHIPLEY B, LECHOWICZ M J, WRIGHT I J, REICH P B. Fundamental trade-offs generating the worldwide leaf economics spectrum. Ecology, 2006, 87(3): 535-541. doi: 10.1890/05-1051
[12]	刘明秀, 梁国鲁. 植物比叶质量研究进展. 植物生态学报, 2016, 40(8): 847-860. doi: 10.17521/cjpe.2015.0428 LIU M X, LIANG G L. Research progress on leaf mass per area. Chinese Journal of Plant Ecology, 2016, 40(8): 847-860. doi: 10.17521/cjpe.2015.0428
[13]	WITKOWSKI E T, LAMONT B B. Leaf specific mass confounds leaf density and thickness. Oecologia, 1991, 88: 486-493. doi: 10.1007/BF00317710
[14]	VILLAR R, ROBLETO J R, DE JONG Y A, POORTER H. Differences in construction costs and chemical composition between deciduous and evergreen woody species are small as compared to differences among families. Plant, Cell and Environment, 2006, 29(8): 1629-1643. doi: 10.1111/j.1365-3040.2006.01540.x
[15]	HIKOSAKA K. Interspecific difference in the photosynthesis–nitrogen relationship: patterns, physiological causes, and ecological importance. Journal of Plant Research, 2004, 117(6): 481-494. doi: 10.1007/s10265-004-0174-2
[16]	DRAKE P L, DE BOER H J, SCHYMANSKI S J, VENEKLAAS E J. Two sides to every leaf: water and CO₂ transport in hypostomatous and amphistomatous leaves. New Phytologist, 2019, 222(3): 1179-1187. doi: 10.1111/nph.15652
[17]	SOHEILI F, HEYDARI M, WOODWARD S, NAJI H R. Adaptive mechanism in Quercus brantii Lindl. leaves under climatic differentiation: morphological and anatomical traits. Scientific Reports, 2023, 13: 3580. doi: 10.1038/s41598-023-30762-1
[18]	ROSAS T, MENCUCCINI M, BARBA J, COCHARD H, SAURA-MAS S, MARTÍNEZ-VILALTA J. Adjustments and coordination of hydraulic, leaf and stem traits along a water availability gradient. New Phytologist, 2019, 223(2): 632-646. doi: 10.1111/nph.15684
[19]	王常顺, 孟凡栋, 李新娥, 姜丽丽, 白玲, 汪诗平. 青藏高原草地生态系统对气候变化的响应. 生态学杂志, 2013, 32(6): 1587-1595. WANG C S, MENG F D, LI X E, JIANG L L, BAI L, WANG S P. Responses of alpine grassland ecosystem on Tibetan Plateau to climate change: a mini review. Chinese Journal of Ecology, 2013, 32(6): 1587-1595.
[20]	HEBERLING J M, FRIDLEY J D. Invaders do not require high resource levels to maintain physiological advantages in a temperate deciduous forest. Ecology, 2015, 97(4): 874-884.
[21]	LI L, MCCORMACK M L, MA C G, KONG D L, ZHANG Q, CHEN X Y, ZENG H, NIINEMETS Ü, GUO D L. Leaf economics and hydraulic traits are decoupled in five species-rich tropical-subtropical forests. Ecology Letters, 2015, 18(9): 899-906. doi: 10.1111/ele.12466
[22]	YIN H, TARIQ A, ZHANG B, LYU G H, ZENG F J, GRACIANO C, SANTOS M G, ZHANG Z H, WANG P, MU S Y. Coupling relationship of leaf economic and hydraulic traits of Alhagi sparsifolia shap. in a hyper-arid desert ecosystem. Plants, 2021, 10(9): 1867. doi: 10.3390/plants10091867
[23]	段媛媛, 宋丽娟, 牛素旗, 黄婷, 杨改河, 郝文芳. 不同林龄刺槐叶功能性状差异及其与土壤养分的关系. 应用生态学报, 2017, 28(1): 28-36. DUAN Y Y, SONG L J, NIU S Q, HUANG T, YANG G H, HAO W F. Variation in leaf functional traits of different-aged Robinia pseudoacacia communities and relationships with soil nutrients. Chinese Journal of Applied Ecology, 2017, 28(1): 28-36.
[24]	BRAY S, REID D M. The effect of salinity and CO₂ enrichment on the growth and anatomy of the second trifoliate leaf of Phaseolus vulgaris. Botany, 2002, 80: 349-359.
[25]	MA L, SUN X D, KONG X X, GALVÁN J V, LI X, YANG S H, YANG Y Q, YANG Y P, HU X Y. Physiological, biochemical and proteomics analysis reveals the adaptation strategies of the alpine plant Potentilla saundersiana at altitude gradient of the Northwestern Tibetan Plateau. Journal of Proteomics, 2015, 112: 63-82. doi: 10.1016/j.jprot.2014.08.009
[26]	金伊丽, 王皓言, 魏临风, 侯颖, 胡景, 吴铠, 夏昊钧, 夏洁, 周伯睿, 李凯, 倪健. 青藏高原植物群落样方数据集. 植物生态学报, 2022, 46(7): 846-854. doi: 10.17521/cjpe.2022.0174 JIN Y L, WANG H Y, WEI L F, HOU Y, HU J, WU K, XIA H J, XIA J, ZHOU B R, LI K, NI J. A plot-based dataset of plant community on the Qingzang Plateau. Chinese Journal of Plant Ecology, 2022, 46(7): 846-854. doi: 10.17521/cjpe.2022.0174
[27]	PAN Y L, TANG H P, LIU D, MA Y G. Geographical patterns and drivers of plant productivity and species diversity in the Qinghai-Tibet Plateau. Plant Diversity, 2023. [https://doi.org/10.1016/j.pld.2023.06.007]
[28]	王媛媛, 马素辉, 蔡琼, 安丽华, 吉成均. 青藏高原和内蒙古高原典型草地植物叶片肾型和哑铃型气孔器气孔特征及其与环境的关系. 西北植物学报, 2018, 38(6): 1048-1057. doi: 10.7606/j.issn.1000-4025.2018.06.1048 WANG Y Y, MA S H, CAI Q, AN L H, JI C J. Leaf stomatal characters of kidney-shaped stomata and dumb-bell-shaped stomata and their relationships with environmental factors in the typical plants of the Tibetan and Inner Mongolian Plateau. Acta Botanica Boreali-Occidentalia Sinica, 2018, 38(6): 1048-1057. doi: 10.7606/j.issn.1000-4025.2018.06.1048
[29]	CHEN H, LUO S W, LI G X, JIANG W, QI W, HU J, MA M J, DU G Z. Large-scale patterns of soil nematodes across grasslands on the Tibetan Plateau: Relationships with climate, soil and plants. Diversity, 2021, 13(8): 369. doi: 10.3390/d13080369
[30]	MILLER-RUSHING A J, PRIMACK R B, TEMPLER P H, RATHBONE S, MUKUNDA S. Long-term relationships among atmospheric CO₂, stomata, and intrinsic water use efficiency in individual trees. American Journal of Botany, 2009, 96(10): 1779-1786.
[31]	BEAULIEU J M, LEITCH I J, PATEL S G, PENDHARKAR A, KNIGHT C A. Genome size is a strong predictor of cell size and stomatal density in angiosperms. New Phytologist, 2008, 179(4): 975-986. doi: 10.1111/j.1469-8137.2008.02528.x
[32]	LIU C C, SACK L, LI Y, ZHANG J H, YU K L, ZHANG Q Y, HE N P, YU G R. Relationships of stomatal morphology to the environment across plant communities. Nature Communications, 2023, 14(1): 6629. doi: 10.1038/s41467-023-42136-2
[33]	ABRAMOFF M D, MAGALHAES P J, RAM S J. Image processing with ImageJ. 2004.
[34]	FELSENSTEIN J. Phylogenies and the comparative method. The American Naturalist, 1985, 125(1): 1-15. doi: 10.1086/284325
[35]	TAYLOR S H, FRANKS P J, HULME S P, SPRIGGS E L, CHRISTIN P A, EDWARDS E J, WOODWARD F I, OSBORNE C P. Photosynthetic pathway and ecological adaptation explain stomatal trait diversity amongst grasses. New Phytologist, 2012, 193(2): 387-396. doi: 10.1111/j.1469-8137.2011.03935.x
[36]	MUIR C D. Light and growth form interact to shape stomatal ratio among British angiosperms. New Phytologist, 2018, 218(1): 242-252. doi: 10.1111/nph.14956
[37]	WILLMER C M, FRICKER M D. Stomata. Netherlands: Springer, 1996.
[38]	RICHARDSON F, BRODRIBB T J, JORDAN G J. Amphistomatic leaf surfaces independently regulate gas exchange in response to variations in evaporative demand. Tree Physiology, 2017, 37(7): 869-878. doi: 10.1093/treephys/tpx073
[39]	HETHERINGTON A M, WOODWARD F I. The role of stomata in sensing and driving environmental change. Nature, 2003, 424: 901-908. doi: 10.1038/nature01843
[40]	FRANKS P J, BEERLING D J. Maximum leaf conductance driven by CO₂ effects on stomatal size and density over geologic time. Proceedings of the National Academy of Sciences, 2009, 106: 10343-10347. doi: 10.1073/pnas.0904209106
[41]	唐楠, 李苗苗, 唐道城. 青藏高原不同海拔高度下全缘叶绿绒蒿叶表皮特征研究. 植物研究, 2019, 39(2): 161-168. doi: 10.7525/j.issn.1673-5102.2019.02.001 TANG N, LI M M, TANG D C. Characteristics of leaf epidermis of Meconopsis integrifolia under different altitudes in the Qinghai-Tibet Plateau. Bulletin of Botanical Research, 2019, 39(2): 161-168. doi: 10.7525/j.issn.1673-5102.2019.02.001
[42]	李全发, 王宝娟, 安丽华, 吉成均. 青藏高原草地植物叶解剖特征. 生态学报, 2013, 33(7): 2062-2070. doi: 10.5846/stxb201112151922 LI Q F, WANG B J, AN L H, JI C J. Leaf anatomical characteristics of the plants of grasslands in the Tibetan Plateau. Acta Ecologica Sinica, 2013, 33(7): 2062-2070. doi: 10.5846/stxb201112151922
[43]	DU B M, ZHU Y H, KANG H Z, LIU C J. Spatial variations in stomatal traits and their coordination with leaf traits in Quercus variabilis across Eastern Asia. Science of The Total Environment, 2021, 789: 147757. doi: 10.1016/j.scitotenv.2021.147757
[44]	KLEYER M, TRINOGGA J, CEBRIÁN-PIQUERAS M A, TRENKAMP A, FLØJGAARD C, EJRNAES R, BOUMA T J, MINDEN V, MAIER M, MANTILLA-CONTRERAS J, ALBACH D C, BLASIUS B. Trait correlation network analysis identifies biomass allocation traits and stem specific length as hub traits in herbaceous perennial plants. Journal of Ecology, 2018, 107(2): 829-842.
[45]	胡选萍. 黄帚橐吾叶片气孔特征及对高寒环境的响应. 草地学报, 2016, 24(6): 1283-1289. HU X P. The leaf stomatal characters of Ligularia virgaure and their responses to alpine climate. Acta Agrestia Sinica, 2016, 24(6): 1283-1289.
[46]	TOMÁS M, FLEXAS J, COPOLOVICI L O, GALMÉS J, HALLIK L, MEDRANO H, RIBAS-CARBÓ M, TOSENS T, VISLAP V, NIINEMETS Ü. Importance of leaf anatomy in determining mesophyll diffusion conductance to CO₂ across species: quantitative limitations and scaling up by models. Journal of Experimental Botany, 2013, 64: 2269-2281. doi: 10.1093/jxb/ert086
[47]	GALMEÉS J, OCHOGAVIÍA J M, GAGO J, ROLDÁN E J, CIFRE J, CONESA M À. Leaf responses to drought stress in Mediterranean accessions of Solanum lycopersicum: anatomical adaptations in relation to gas exchange parameters. Plant, Cell and Environment, 2013, 36(5): 920-935. doi: 10.1111/pce.12022
[48]	NIINEMETS U, DIAZ-ESPEJO A, FLEXAS J, GALMÉS J, WARREN C R. Role of mesophyll diffusion conductance in constraining potential photosynthetic productivity in the field. Journal of Experimental Botany, 2009, 608: 2249-2270.
[49]	KUYPERS M M, MARCHANT H K, KARTAL B. The microbial nitrogen-cycling network. Nature Reviews Microbiology, 2018, 16: 263-276. doi: 10.1038/nrmicro.2018.9

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The coordinated relationship of stomatal and leaf economic traits in dicotyledonous plants of the Qinghai-Tibet Plateau and their response to environmental changes

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