四种常见树木叶片光合模型关键参数对臭氧浓度升高的响应

doi:10.17521/cjpe.2021.0295

摘要/Abstract

摘要：

随着城市化进程的加快, 臭氧(O₃)已经成为中国夏季首要大气污染物。已有研究表明O₃通过气孔进入叶片显著抑制光合作用, 影响陆地生态系统碳水循环过程。但是O₃浓度升高对植物光合和气孔导度模型关键参数影响的研究仍然缺乏。该研究利用开顶式气室, 设置两个O₃处理(CF, 过滤空气; E-O₃, 未过滤空气+ 60 nmol·mol^-1O₃), 选用4种常见的树木(茶(Camellia sinensis)、复叶槭(Acer negundo)、栾树(Koelreuteria paniculata)和蒙古栎(Quercus mongolica)), 通过测定叶片气体交换参数, 探究O₃浓度升高对植物光合和气孔导度模型关键参数的影响。结果表明: O₃浓度升高显著降低了4种植物的饱和光合速率和光合生化模型参数叶肉导度, 但是O₃对光合生化模型参数最大羧化速率和最大电子传递速率的负效应在不同树种间存在差异。此外, 不同植物气孔导度对O₃的响应也存在差异。通过对最优化气孔导度模型进行参数化, 结果表明O₃显著提高了蒙古栎和复叶槭的斜率参数(g₁), 并显著增加了茶的气孔导度模型截距参数(g₀), 但降低了复叶槭的g₀。在不同O₃处理下4种树木的内源水分利用效率与g₁呈显著线性负相关关系。综上所述, O₃浓度升高显著影响光合生化和气孔导度模型关键参数。

关键词: 臭氧, 木本植物, 光合生化模型, 气孔导度模型

Abstract:

Aims With fast urbanization in China, ground-level ozone (O₃) has become the major atmospheric pollutant in summer. It was documented that O₃ enters leaves through stomata, inhibits photosynthesis, and alters the carbon and water cycles in terrestrial ecosystems. However, few studies have investigated the key parameters of photosynthetic and stomatal conductance models in response to elevated O₃concentration.
Methods In this study, plants of four common tree species (Camellia sinensis, Acer negundo, Koelreuteria paniculata and Quercus mongolica) were exposed to two O₃ treatments (CF, charcoal-filtered air; E-O₃, ambient air + 60 nmol·mol^-1 O₃) in open top chambers. The effects of elevated O₃ concentration on key parameters of photosynthetic and stomatal conductance models were explored using data from leaf gas exchange measurements.
Important findings Our results indicated that elevated O₃ concentration significantly decreased the light-saturated photosynthesis and mesophyll conductance in the four species. However, species showed distinct responses of the maximum rate of Rubisco carboxylation and the maximum rate of electron transport to elevated O₃ concentration. The response of stomatal conductance to O₃ was also different among species. We found that elevated O₃ concentration significantly increased the slope parameters (g₁) of Q. mongolica and A. negundo; however, the intercept parameter of stomata model in C. sinensis was decreased in A. negundo. The intrinsic water- use efficiency of the four species was negatively correlated with g₁ across O₃ treatments. All in all, elevated O₃ concentration significantly affected key parameters of the photosynthetic and stomatal conductance models. This study could provide the foundation and support for improving the accuracy of terrestrial ecosystem models under elevated O₃concentration.

Key words: ozone, woody plant, photosynthetic model, stomatal conductance model

马艳泽, 杨熙来, 徐彦森, 冯兆忠. 四种常见树木叶片光合模型关键参数对臭氧浓度升高的响应. 植物生态学报, 2022, 46(3): 321-329. DOI: 10.17521/cjpe.2021.0295

MA Yan-Ze, YANG Xi-Lai, XU Yan-Sen, FENG Zhao-Zhong. Response of key parameters of leaf photosynthetic models to increased ozone concentration in four common trees. Chinese Journal of Plant Ecology, 2022, 46(3): 321-329. DOI: 10.17521/cjpe.2021.0295

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链接本文: https://www.plant-ecology.com/CN/10.17521/cjpe.2021.0295

https://www.plant-ecology.com/CN/Y2022/V46/I3/321

图/表 5

表1 臭氧浓度升高对不同树种叶片性状影响的方差分析结果(p值)

Table 1 Variance analysis results of effects of ozone (O3), species, and their interaction on gas exchange traits (p value)

	臭氧 O₃	树种 Species	臭氧×树种 O₃ × Species
饱和光合速率 A_sat	<0.01	0.02	0.26
气孔导度 g_s	<0.01	<0.01	0.01
胞间CO₂浓度 C_i	0.43	0.05	0.25
内源水分利用效率 iWUE	0.25	0.02	0.08
最大羧化速率 V_cmax	<0.01	0.11	0.04
最大电子传递速率 J_max	<0.01	0.30	<0.01
J_max/V_cmax	0.25	<0.01	0.18
叶肉导度 g_m	<0.01	<0.01	0.06

图1 臭氧浓度升高(E-O3)对4种树木饱和光合速率(Asat)(A)、气孔导度(gs)(B)、胞间CO2浓度(Ci)(C)和内源水分利用效率(iWUE)(D)的影响(平均值±标准差)。图中不同小写字母表示差异显著(p < 0.05)。CF, 活性炭过滤空气。

Fig. 1 Effects of elevated ozone concentration (E-O3) on light-saturated net photosynthesis (Asat)(A), stomatal conductance to H2O (gs)(B), CO2 concentration in the leaf intercellular spaces (Ci)(C), and intrinsic water-use efficiency (iWUE)(D) of four tree species (mean ± SD). Different lowercase letters in the figures indicate significant differences (p < 0.05). CF, charcoal-filtered air.

图2 臭氧浓度升高(E-O3)对4种树木最大羧化速率(Vcmax)(A)、最大电子传递速率(Jmax)(B)、Jmax/Vcmax (C)和叶肉导度(gm)(D)的影响(平均值±标准差), 图中不同小写字母表示差异显著(p < 0.05)。CF, 活性炭过滤空气。

Fig. 2 Effects of elevated ozone concentration (E-O3) on the maximum rates of Rubisco carboxylation (Vcmax)(A), the maximum rate of ribulose 1,5 bisphosphate regeneration (Jmax)(B), Jmax/Vcmax (C), and mesophyll conductance (gm)(D) of four tree species (mean ± SD). Different lowercase letters in the figures stand for the significant differences (p < 0.05). CF, charcoal-filtered air.

图3 4种木本植物的气孔导度(gs)与最优化模型指数的关系。CF, 活性炭过滤空气; E-O3, 未过滤的环境空气增加60 nmol·mol-1 O3。Slope, 气孔导度模型斜率参数(g1); Intercept, 气孔导度模型截距参数(g0)。An, 叶片光合速率; Ca, 环境CO2浓度; VPD, 饱和水汽压匮缺值。

Fig. 3 Relationship between stomatal conductance (gs) and the index of the optimal stomatal conductance (1.6 An/(Ca$\sqrt{\text{VPD}}$)) of four tree species. CF, charcoal-filtered air; E-O3, ambient air + 60 nmol·mol–1 O3. An, leaf photosynthetic rate; Ca, environmental CO2 concentration; VPD, vapor pressure defict.

图4 不同处理下4种树木水分利用效率(iWUE)与气孔导度模型斜率参数(g1)的关系。CF, 活性炭过滤空气; E-O3, 未过滤的环境空气增加60 nmol·mol-1 O3。

Fig. 4 Relationship between water use efficiency (iWUE) and the slope parameters of stomata model (g1) of four tree species under different treatments. CF, charcoal-filtered air; E-O3, ambient air + 60 nmol·mol-1 O3.

参考文献 44

[1]	Ainsworth EA (2017). Understanding and improving global crop response to ozone pollution. The Plant Journal, 90, 886-897. DOI URL
[2]	Agathokleous E, Feng ZZ, Oksanen E, Sicard P, Wang Q, Saitanis CJ, Araminiene V, Blande JD, Hayes F, Calatayud V, Domingos M, Veresoglou SD, Peñuelas J, Wardle DA, de Marco A, et al. (2020). Ozone affects plant, insect, and soil microbial communities: a threat to terrestrial ecosystems and biodiversity. Science Advances, 6, eabc1176. DOI: 10.1126/sciadv.abc1176. DOI URL
[3]	Bernacchi CJ, Portis AR, Nakano H, Caemmerer SV, Long SP (2002). Temperature response of mesophyll conductance. Implications for the determination of Rubisco enzyme kinetics and for limitations to photosynthesis in vivo. Plant Physiology, 130, 1992-1998. PMID
[4]	Bernacchi CJ, Singsaas EL, Pimentel C, Portis Jr AR, Long SP (2001). Improved temperature response functions for models of Rubisco-limited photosynthesis. Plant, Cell & Environment, 24, 253-259.
[5]	Calatayud A, Iglesias DJ, Talón M, Barreno E (2006). Effects of long-term ozone exposure on citrus: chlorophyll a fluorescence and gas exchange. Photosynthetica, 44, 548-554. DOI URL
[6]	Dai LL, Li P, Shang B, Liu S, Yang AZ, Wang YN, Feng ZZ (2017). Differential responses of peach (Prunus persica) seedlings to elevated ozone are related with leaf mass per area, antioxidant enzymes activity rather than stomatal conductance. Environmental Pollution, 227, 380-388. DOI URL
[7]	Eichelmann H, Oja V, Rasulov B, Padu E, Bichele I, Pettai H, Möls T, Kasparova I, Vapaavuori E, Laisk A (2004). Photosynthetic parameters of birch (Betula pendula Roth) leaves growing in normal and in CO₂- and O₃-enriched atmospheres. Plant, Cell & Environment, 27, 479-495.
[8]	Farquhar GD, von Caemmerer S, Berry JA (1980). A biochemical model of photosynthetic CO₂assimilation in leaves of C₃ species. Planta, 149, 78-90. DOI PMID
[9]	Feng ZZ, Hu EZ, Wang XK, Jiang LJ, Liu XJ (2015). Ground- level O₃ pollution and its impacts on food crops in China: a review. Environmental Pollution, 199, 42-48. DOI URL
[10]	Feng ZZ, Li P, Yuan XY, Gao F, Jiang LJ, Dai LL (2018). Progress in ecological and environmental effects of ground- level O₃ in China. Acta Ecologica Sinica, 38, 1530-1541.
	[冯兆忠, 李品, 袁相洋, 高峰, 姜立军, 代碌碌 (2018). 我国地表臭氧生态环境效应研究进展. 生态学报, 38, 1530-1541.]
[11]	Feng ZZ, Niu JF, Zhang WW, Wang XK, Yao FF, Tian Y (2011). Effects of ozone exposure on sub-tropical evergreen Cinnamomum camphora seedlings grown in different nitrogen loads. Trees, 25, 617-625. DOI URL
[12]	Feng ZZ, Sun JS, Wan WX, Hu EZ, Calatayud V (2014). Evidence of widespread ozone-induced visible injury on plants in Beijing, China. Environmental Pollution, 193, 296-301. DOI URL
[13]	Flexas J, Barbour MM, Brendel O, Cabrera HM, Carriquí M, Díaz-Espejo A, Douthe C, Dreyer E, Ferrio JP, Gago J, Gallé A, Galmés J, Kodama N, Medrano H, Niinemets Ü, et al. (2012). Mesophyll diffusion conductance to CO₂: an unappreciated central player in photosynthesis. Plant Science, 193-194, 70-84.
[14]	Flexas J, Ribas-Carbó M, Diaz-Espejo A, Galmés J, Medrano H (2008). Mesophyll conductance to CO₂: current knowledge and future prospects. Plant, Cell & Environment, 31, 602-621.
[15]	Franks PJ, Bonan GB, Berry JA, Lombardozzi DL, Holbrook NM, Herold N, Oleson KW (2018). Comparing optimal and empirical stomatal conductance models for application in earth system models. Global Change Biology, 24, 5708-5723.
[16]	Goumenaki E, Taybi T, Borland A, Barnes J (2010). Mechanisms underlying the impacts of ozone on photosynthetic performance. Environmental and Experimental Botany, 69, 259-266. DOI URL
[17]	Harley PC, Loreto F, Di Marco G, Sharkey TD (1992). Theoretical considerations when estimating the mesophyll conductance to CO₂ flux by analysis of the response of photosynthesis to CO₂. Plant Physiology, 98, 1429-1436. DOI PMID
[18]	Hoshika Y, Haworth M, Watanabe M, Koike T (2020). Interactive effect of leaf age and ozone on mesophyll conductance in Siebold’s beech. Physiologia Plantarum, 170, 172-186. DOI URL
[19]	Hoshika Y, Watanabe M, Inada N, Koike T (2013). Model- based analysis of avoidance of ozone stress by stomatal closure in Siebold’s beech (Fagus crenata). Annals of Botany, 112, 1149-1158 DOI URL
[20]	IPCC (Intergovernmental Panel on Climate Change) (2013). Climate Change 2013: the Physical Science Basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge, UK.
[21]	Kinose Y, Fukamachi Y, Watanabe M, Izuta T (2020). Ozone- induced change in the relationship between stomatal conductance and net photosynthetic rate is a factor determining cumulative stomatal ozone uptake by Fagus crenata seedlings. Trees, 34, 445-454. DOI URL
[22]	Knauer J, Zaehle S, de Kauwe MG, Bahar NHA, Evans JR, Medlyn BE, Reichstein M, Werner C (2019). Effects of mesophyll conductance on vegetation responses to elevated CO₂concentrations in a land surface model. Global Change Biology, 25, 1820-1838. DOI URL
[23]	Leung F, Williams K, Sitch S, Tai APK, Wiltshire A, Gornall J, Ainsworth EA, Arkebauer T, Scoby D (2020). Calibrating soybean parameters in JULES 5.0 from the US-Ne2/3 FLUXNET sites and the SoyFACE-O₃ experiment. Geoscientific Model Development, 13, 6201-6213. DOI URL
[24]	Li H, Peng L, Bi F, Li L, Bao JM, Li JL, Zhang H, Chai FH (2019). Strategy of coordinated control of PM_2.5 and ozone in China. Research of Environmental Sciences, 32, 1763-1778.
	[李红, 彭良, 毕方, 李陵, 鲍捷萌, 李俊玲, 张浩, 柴发合 (2019). 我国PM_2.5与臭氧污染协同控制策略研究. 环境科学研究, 32, 1763-1778.]
[25]	Li P, Feng ZZ, Catalayud V, Yuan XY, Xu YS, Paoletti E (2017). A meta-analysis on growth, physiological, and biochemical responses of woody species to ground-level ozone highlights the role of plant functional types. Plant, Cell & Environment, 40, 2369-2380.
[26]	Lin YS, Medlyn BE, Duursma RA, Prentice IC, Wang H, Baig S, Eamus D, de Dios VR, Mitchell P, Ellsworth DS, Beeck MO, Wallin G, Uddling J, Tarvainen L, Linderson ML, et al. (2015). Optimal stomatal behaviour around the world. Nature Climate Change, 5, 459-464. DOI URL
[27]	Long SP, Postl WF, Bolhár-Nordenkampf HR (1993). Quantum yields for uptake of carbon dioxide in C₃ vascular plants of contrasting habitats and taxonomic groupings. Planta, 189, 226-234.
[28]	Masutomi Y, Kinose Y, Takimoto T, Yonekura T, Oue H, Kobayashi K (2019). Ozone changes the linear relationship between photosynthesis and stomatal conductance and decreases water use efficiency in rice. Science of the Total Environment, 655, 1009-1016. DOI
[29]	Medlyn BE, Duursma RA, Eamus D, Ellsworth DS, Prentice IC, Barton CVM, Crous KY, Angelis PD, Freeman M, Wingate L (2011). Reconciling the optimal and empirical approaches to modelling stomatal conductance. Global Change Biology, 17, 2134-2144. DOI URL
[30]	Reid CD, Fiscus EL (1998). Effects of elevated [CO₂] and/or ozone on limitations to CO₂ assimilation in soybean (Glycine max). Journal of Experimental Botany, 49, 885-895. DOI URL
[31]	Shang B, Xu YS, Dai LL, Yuan XY, Feng ZZ (2019). Elevated ozone reduced leaf nitrogen allocation to photosynthesis in poplar. Science of the Total Environment, 657, 169-178. DOI
[32]	Sitch S, Cox PM, Collins WJ, Huntingford C (2007). Indirect radiative forcing of climate change through ozone effects on the land-carbon sink. Nature, 448, 791-794. DOI URL
[33]	Sun JD, Feng ZZ, Ort DR (2014). Impacts of rising tropospheric ozone on photosynthesis and metabolite levels on field grown soybean. Plant Science, 226, 147-161. DOI URL
[34]	von Caemmerer S (2000). Biochemical Models of Leaf Photosynthesis. Csiro Publishing, Collingwood, VIC, Australia.
[35]	von Caemmerer S, Farquhar GD (1981). Some relationships between the biochemistry of photosynthesis and the gas exchange of leaves. Planta, 153, 376-387. DOI PMID
[36]	Warren CR, Löw M, Matyssek R, Tausz M (2007). Internal conductance to CO₂ transfer of adult Fagus sylvatica: variation between sun and shade leaves and due to free-air ozone fumigation. Environmental and Experimental Botany, 59, 130-138. DOI URL
[37]	Watanabe M, Kamimaki Y, Mori M, Okabe S, Arakawa I, Kinose Y, Nakaba S, Izuta T (2018). Mesophyll conductance to CO₂ in leaves of Siebold’s beech (Fagus crenata) seedlings under elevated ozone. Journal of Plant Research, 131, 907-914. DOI PMID
[38]	Wittig VE, Ainsworth EA, Long SP (2007). To what extent do current and projected increases in surface ozone affect photosynthesis and stomatal conductance of trees? A meta-analytic review of the last 3 decades of experiments. Plant, Cell & Environment, 30, 1150-1162.
[39]	Wolz KJ, Wertin TM, Abordo M, Wang D, Leakey ADB (2017). Diversity in stomatal function is integral to modelling plant carbon and water fluxes. Nature Ecology & Evolution, 1, 1292-1298.
[40]	Xu YS, Feng ZZ, Shang B, Dai LL, Uddling J, Tarvainen L (2019). Mesophyll conductance limitation of photosynthesis in poplar under elevated ozone. Science of the Total Environment, 657, 136-145. DOI URL
[41]	Xu YS, Shang B, Feng ZZ, Tarvainen L (2020). Effect of elevated ozone, nitrogen availability and mesophyll conductance on the temperature responses of leaf photosynthetic parameters in poplar. Tree Physiology, 40, 484-497. DOI URL
[42]	Xu YS, Shang B, Peng JL, Feng ZZ, Tarvainen L (2021). Stomatal response drives between-species difference in predicted leaf water-use efficiency under elevated ozone. Environmental Pollution, 269, 116137. DOI: 10.1016/j.envpol.2020.116137. DOI URL
[43]	Yan H, Zhang W, Hou M, Li YS, Gao P, Xia Q, Meng XY, Fan LY, Ye DQ (2020). Sources and control area division of ozone pollution in cities at prefecture level and above in China. Environmental Science, 41, 5215-5224.
	[闫慧, 张维, 侯墨, 李银松, 高平, 夏青, 孟晓艳, 范丽雅, 叶代启 (2020). 我国地级及以上城市臭氧污染来源及控制区划分. 环境科学, 41, 5215-5224.]
[44]	Yuan XY, Calatayud V, Gao F, Fares S, Paoletti E, Tian Y, Feng ZZ (2016). Interaction of drought and ozone exposure on isoprene emission from extensively cultivated poplar. Plant, Cell & Environment, 39, 2276-2287.