Elevated CO2 offsets the alteration of foliar chemicals (n-icosane, geranyl acetate, and elixene) induced by elevated O3 in three taxa of O3-tolerant eucalypts

Eka Novriyanti , Qiaozhi Mao , Evgenios Agathokleous , Makoto Watanabe , Yasuyuki Hashidoko , Takayoshi Koike

Journal of Forestry Research ›› 2020, Vol. 32 ›› Issue (2) : 789 -803.

PDF
Journal of Forestry Research ›› 2020, Vol. 32 ›› Issue (2) : 789 -803. DOI: 10.1007/s11676-020-01133-7
Original Paper

Elevated CO2 offsets the alteration of foliar chemicals (n-icosane, geranyl acetate, and elixene) induced by elevated O3 in three taxa of O3-tolerant eucalypts

Author information +
History +
PDF

Abstract

Eucalypts are important forest resources in southwestern China, and may be tolerant to elevated ground-level ozone (O3) concentrations that can negatively affect plant growth. High CO2 may offset O3-induced effects by providing excess carbon to produce secondary metabolites or by inducing stomatal closure. Here, the effects of elevated CO2 and O3 on leaf secondary metabolites and other defense chemicals were studied by exposing seedlings of Eucalyptus globulus, E. grandis, and E. camaldulensis ×  E. deglupta to a factorial combination of two levels of O3 (< 10 nmol mol−1 and 60 nmol mol−1) and CO2 (ambient: 370 μmol mol−1 and 600 μmol mol−1) in open-top field chambers. GC-profiles of leaf extracts illustrated the effect of elevated O3 and the countering effect of high CO2 on compounds in leaf epicuticular wax and essential oils, i.e., n-icosane, geranyl acetate and elixene, compounds known as a first-line defense against insect herbivores. n-Icosane may be involved in tolerance mechanisms of E. grandis and the hybrid, while geranyl acetate and elixene in the tolerance of E. globulus. Elevated O3 and CO2, singly or in combination, affected only leaf physiology but not biomass of various organs. Elevated CO2 impacted several leaf traits, including stomatal conductance, leaf mass per area, carbon, lignin, n-icosane, geranyl acetate and elixene. Limited effects of elevated O3 on leaf physiology (nitrogen, n-icosane, geranyl acetate, elixene) were commonly offset by elevated CO2. We conclude that E. globulus, E. grandis and the hybrid were tolerant to these O3 and CO2 treatments, and n-icosane, geranyl acetate and elixene may be major players in tolerance mechanisms of the tested species.

Cite this article

Download citation ▾
Eka Novriyanti, Qiaozhi Mao, Evgenios Agathokleous, Makoto Watanabe, Yasuyuki Hashidoko, Takayoshi Koike. Elevated CO2 offsets the alteration of foliar chemicals (n-icosane, geranyl acetate, and elixene) induced by elevated O3 in three taxa of O3-tolerant eucalypts. Journal of Forestry Research, 2020, 32(2): 789-803 DOI:10.1007/s11676-020-01133-7

登录浏览全文

4963

注册一个新账户 忘记密码

References

[1]

Agathokleous E, Calabrese EJ. A global environmental health perspective and optimisation of stress. Sci Total Environ, 2020, 704: 135263.

[2]

Agathokleous E, Saitanis CJ. Plant susceptibility to ozone: a tower of Babel?. Sci Total Environ, 2020, 703: 134962.

[3]

Agathokleous E, Saitanis CJ, Stamatelopoulos D, Mouzaki-Paxinou A-C, Paoletti E, Manning WJ. Olive oil for dressing plant leaves so as to avoid O3 injury. Water Air Soil Pollut, 2016, 227: 282.

[4]

Agathokleous E, Saitanis CJ, Wang X, Watanabe M, Koike T. A review study on past 40 years of research on effects of tropospheric O3 on belowground structure, functioning, and processes of trees: a linkage with potential ecological implications. Water Air Soil Pollut, 2016, 227: 33.

[5]

Agathokleous E, Belz RG, Calatayud V, De Marco A, Hoshika Y, Kitao M, Saitanis CJ, Sicard P, Paoletti E, Calabrese EJ. Predicting the effect of ozone on vegetation via the linear non-threshold (LNT), threshold and hormetic dose-response models. Sci Total Environ, 2019, 649: 61-74.

[6]

Agathokleous E, Belz RG, Kitao M, Koike T, Calabrese EJ. Does the root to shoot ratio show a hormetic response to stress? An ecological and environmental perspective. J For Res, 2019, 30: 1569-1580.

[7]

Ainsworth EA, Long SP. What have we learned from 15 years of free-air CO2 enrichment (FACE)? A meta-analytic review of the responses of photosynthesis, canopy properties and plant production to rising CO2. New Phytol, 2005, 165: 351-372.

[8]

Ainsworth EA, Rogers A, Leakey AD, Heady LE, Gibon Y, Stitt M, Schurr U. Does elevated atmospheric [CO2] alter diurnal C uptake and the balance of C and N metabolites in growing and fully expanded soybean leaves?. J Exp Bot, 2007, 58: 579-591.

[9]

Araminienė V, Varnagirytė-Kabašinskienė I, Stakėnas V. Pilot study on the effects of elevated air temperature and CO2 on artificially defoliated silver birch saplings. J For Res, 2018, 29: 1507-1518.

[10]

Bate-Smith EC. Astringent tannins of Acer species. Phytochemistry, 1977, 16: 1421-1426.

[11]

Bernacchi CJ, Singsaas EL, Pimentel C, Portis AR, Long SP. Improved temperature response functions for models of Rubisco-limited photosynthesis. Plant Cell Environ, 2001, 24: 253-259.

[12]

Bidart-Bouzat MG, Imeh-Nathaniel A. Global change effects on plant chemical defences against insect herbivores. J Integr Plant Biol, 2008, 50: 1339-1354.

[13]

Blaschke L, Forstreuter M, Sheppard LJ, Leith IK, Murray MB, Polle A. Lignification in beech (Fagus sylvatica) grown at elevated CO2 concentrations: interaction with nutrient availability and leaf maturation. Tree Physiol, 2002, 22: 469-477.

[14]

Bloom AJ, Burger M, Asensio JSR, Cousins AB. Carbon dioxide enrichment inhibits nitrate assimilation in wheat and Arabidopsis. Science, 2010, 328: 899-903.

[15]

Booker FL. Influence of carbon dioxide enrichment, ozone and nitrogen fertilization on cotton (Gossypium hirsutum L.) leaf and root composition. Plant Cell Environ, 2001, 23: 573-583.

[16]

Booker FL, Maier CA. Atmospheric carbon dioxide, irrigation, and fertilization effects on phenolic and nitrogen concentrations in loblolly pine (Pinus taeda) needles. Tree Physiol, 2001, 21: 609-616.

[17]

Booker F, Muntifering R, McGrath M, Burkey K, Decoteau D, Fiscus E, Manning W, Krupa S, Chappelka A, Grantz D. The ozone component of global change: potential effects on agricultural and horticultural plant yield, product quality and interactions with invasive species. J Integr Plant Biol, 2009, 51: 337-351.

[18]

Box GEP, Cox DR. An analysis of transformations. J R Stat Soc B, 1964, 26: 211-252.

[19]

Broadmeadow MSJ, Heath J, Randle TJ. Environmental limitations to O3 uptake—some key results from young trees growing at elevated CO2 concentrations. Water Air Soil Pollut, 1999, 116: 299-310.

[20]

Bryant JP, Chapin FSIII, Klein DR. Carbon/nutrient balance of boreal plants in relation to vertebrate herbivory. Oikos, 1983, 40: 357-368.

[21]

Carpino S, Mallia S, La Terra S, Melilli C, Licitra G, Acree TE, Barbano DM, Van Soest PJ. Composition and aroma compounds of ragusano cheese: native pasture and total mixed rations. J Dairy Sci, 2004, 87: 816-830.

[22]

Centritto M, Jarvis PG. Long-term effects of elevated carbon dioxide concentration and provenance on four clones of Sitka spruce (Picea sitchensis). II. Photosynthetic capacity and nitrogen use efficiency. Tree Physiol, 1999, 19: 807-814.

[23]

Chater C, Peng K, Movahedi M, Dunn JA, Walker HJ, Liang YK, McLachlan DH, Casson S, Isner JC, Wilson I, Neill SJ, Hedrich R, Gray JE, Hetherington AM. Elevated CO2-induced responses in stomata require ABA and ABA signaling. Curr Biol, 2015, 25: 2709-2716.

[24]

Coûteaux MM, Kurz C, Bottner P, Raschi A. Influence of increased atmospheric CO2 concentration on quality of plant material and litter decomposition. Tree Physiol, 1999, 19: 301-311.

[25]

Dubis EN, Dubis AT, Popławski J. Determination of the aromatic compounds in plant cuticular waxes using FT-IR spectroscopy. J Mol Struct, 2001, 596: 83-88.

[26]

Dusenge ME, Duarte AG, Way DA. Plant carbon metabolism and climate change: elevated CO2 and temperature impacts on photosynthesis, photorespiration and respiration. New Phytol, 2019, 221: 32-49.

[27]

Eguchi N, Karatsu K, Ueda T, Funada R, Takagi K, Hiura T, Sasa K, Koike T. Photosynthetic responses of birch and alder saplings grown in a free air CO2 enrichment system in northern Japan. Trees, 2008, 22: 437-447.

[28]

Evans JR. Photosynthesis and nitrogen relationships in leaves of C3 plants. Oecologia, 1989, 78: 9-19.

[29]

Farquhar GD, von Caemmerer S, Berry JA. A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species. Planta, 1980, 149: 78-90.

[30]

Fowler D, Cape JN, Coyle M, Flechard C, Kuylenstierna J, Hicks K, Derwent D, Johnson C, Stevenson D. The global exposure of forests to air pollutants. Water Air Soil Pollut, 1999, 116: 5-32.

[31]

Ghini R, MacLeod REO, Santos MS, Silva CEO. Elevated atmospheric carbon dioxide concentration increases eucalyptus plantlets growth and reduces diseases severity. Proc Environ Sci, 2015, 29: 206-207.

[32]

Gleadow RM, Foley WJ, Woodrow IE. Enhanced CO2 alters the relationship between photosynthesis and defence in cyanogenic Eucalyptus cladocalyx F. Muell. Plant Cell Environ, 1998, 21: 12-22.

[33]

Grams TEE, Anegg S, Haberle K-H, Langebartels C, Matyssek R. Interactions of chronic exposure to elevated CO2 and O3 levels in the photosynthetic light and dark reactions of European beech (Fagus sylvatica). New Phytol, 1999, 144: 95-107.

[34]

Herms DA, Mattson WJ. The dilemma of plants: to grow or defend. Q Rev Biol, 1992, 67: 283-335.

[35]

Hikosaka K. Interspecific difference in the photosynthesis–nitrogen relationship: patterns, physiological causes, and ecological importance. J Plant Res, 2004, 117: 481-494.

[36]

Hikosaka K, Onoda Y, Kinugasa T, Nagashima H, Anten NPR, Hirose T. Plant responses to elevated CO2 concentration at different scales: leaf, whole plant, canopy, and population. Ecol Res, 2005, 20: 243-253.

[37]

Hoshika Y, De Carlo A, Baraldi R, Neri L, Carrari E, Agathokleous E, Zhang L, Fares S, Paoletti E. Ozone-induced impairment of night -time stomatal closure in O3-sensitive poplar clone is affected by nitrogen but not by phosphorus enrichment. Sci Total Environ, 2019, 692: 713-722.

[38]

Howell DC, McConaughy SH. Nonorthogonal analysis of variance: putting the question before the answer. Educ Psychol Meas, 1982, 42: 9-24.

[39]

IPCC. Metz B, Davidson OR, Bosch PR, Dave R, Meyer LA. Summary for policy makers. Climate change 2007: mitigation. Contribution of Working Group III to the Fourth Assessment Report of the Intergovernmental panel on Climate Change, 2007, New York: Cambridge University Press.

[40]

Julkunen-Tiitto R. Phenolic constituents in the leaves of northern willows: methods for the analysis of certain phenolics. J Agric Food Chem, 1985, 33: 213-217.

[41]

Kanagendran A, Pazouki L, Niinemets Ü. Differential regulation of volatile emission from Eucalyptus globulus leaves upon single and combined ozone and wounding treatments through recovery and relationships with ozone uptake. Environ Exp Bot, 2018, 145: 21-38.

[42]

Karabourniotis G, Liakopoulos G, Nikolopoulos D, Bresta P, Stavroulaki V, Sumbele S. “Carbon gain vs. water saving, growth vs. defence”: two dilemmas with soluble phenolics as a joker. Plant Sci, 2014, 227: 21-27.

[43]

Karnosky DF, Percy KE, Xiang B, Callan B, Noormets A, Mankovska B, Hopkin A, Sober J, Jones W, Dickson RE, Isebrands JG. Interacting elevated CO2 and tropospheric O3 predisposes aspen (Populus tremuloides Michx.) to infection by rust (Melampsora medusae f. sp. tremuloidae). Glob Change Biol, 2002, 8: 329-338.

[44]

Karnosky DF, Zak DR, Pregitzer KS, Awmack CS, Bockheim JG, Dickson RE, Hendrey GR, Host GE, King JS, Kopper BJ, Kruger EL, Kubiske ME, Lindroth RL, Mattson WJ, McDonald EP, Noormets A, Oksanen E, Parsons WFJ, Percy KE, Podila GK, Riemenschneider DE, Sharma P, Thakur R, Sôber A, Sôber J, Jones WS, Anttonen S, Vapaavuori E, Mankovska B, Heilman W, Isebrands JG. Tropospheric O3 moderates responses of temperate hardwood forests to elevated CO2: a synthesis of molecular to ecosystem results from the Aspen FACE project. Funct Ecol, 2003, 17: 289-304.

[45]

Kitao M, Löw M, Heerdt C, Grams TEE, Häberle K-H, Matyssek R. Effects of chronic elevated ozone exposure on gas exchange responses of adult beech trees (Fagus sylvatica) as related to the within-canopy light gradient. Environ Pollut, 2009, 157: 537-544.

[46]

Kitao M, Komatsu M, Yazaki K, Kitaoka S, Tobita H. Growth overcompensation against O3 exposure in two Japanese oak species, Quercus mongolica var. crispula and Quercus serrata, grown under elevated CO2. Environ Pollut, 2015, 206: 133-141.

[47]

Koike T, Lei TT, Maximov TC, Tabuchi R, Takahashi K, Ivanov BI. Comparison of the photosynthetic capacity of Siberian and Japanese birch seedlings grown in elevated CO2 and temperature. Tree Physiol, 1996, 16: 381-385.

[48]

Koike T, Mao Q, Inada N, Kawaguchi K, Hoshika Y, Kita K, Watanabe M. Growth and photosynthetic responses of cuttings of a hybrid Larch (Larix gmelinii var. japonica x L. kaempferi) to elevated ozone and/or carbon dioxide. Asian J Atmos Environ, 2012, 6: 104-110.

[49]

Kopper B, Lindroth R. Effects of elevated carbon dioxide and ozone on the phytochemistry of aspen and performance of an herbivore. Oecologia, 2003, 134: 95-103.

[50]

Larcher W. Physiological plant ecology: ecophysiology and stress physiology of functional groups, 2003 4 Berlin: Springer.

[51]

Lawler IR, Foley WJ, Woodrow IE, Cork SJ. The effects of elevated CO2 atmospheres on the nutritional quality of Eucalyptus foliage and its interaction with soil nutrient and light availability. Oecologia, 1996, 109: 59-68.

[52]

Li P, Feng Z, Calatayud V, Yuan X, Xu Y, Paoletti E. 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 Environ, 2017, 40: 2369-2380.

[53]

Lindroth R. Impacts of elevated atmospheric CO2 and O3 on forests: Phytochemistry, trophic interactions, and ecosystem dynamics. J Chem Ecol, 2010, 36: 2-21.

[54]

Liu B, dos Santos BM, Kanagendran A, Jakobsen Neilson EH, Niinemets Ü. Ozone and wounding stresses differently alter the temporal variation in formylated phloroglucinols in Eucalyptus globulus leaves. Metabolites, 2019, 9: 46.

[55]

Long SP, Bernacchi CJ. Gas exchange measurements, what can they tell us about the underlying limitations to photosynthesis? Procedures and sources of error. J Exp Bot, 2003, 54: 2393-2401.

[56]

Manning WJ. Establishing a cause and effect relationship for ambient ozone exposure and tree growth in the forest: progress and an experimental approach. Environ Pollut, 2005, 137: 443-454.

[57]

Matsuki S, Sano Y, Koike T. Chemical and physical defence in early and late leaves in three heterophyllous birch species native to Northern Japan. Ann Bot, 2004, 93: 141-147.

[58]

Mattson JW, Julkunen-Tiitto R, Herms DA. CO2 enrichment and carbon partitioning to phenolics: do plant responses accord better with the protein competition or the growth differentiation balance models?. Oikos, 2005, 111: 337-347.

[59]

Matyssek R, Schnyder H, Obwald W, Ernst D, Munch JC, Pretzsch H. Growth and defence in plants: resource allocation at multiple scales, 2012, Heidelberg: Springer 470

[60]

McKiernan AB, O'Reilly-Wapstra JM, Price C, Davies NW, Potts BM, Hovenden MJ. Stability of plant defensive traits among populations in two Eucalyptus species under elevated carbon dioxide. J Chem Ecol, 2012, 38: 204-212.

[61]

Monk RJ, Murray F. The relative tolerance of some Eucalyptus species to ozone exposure. Water Air Soil Pollut, 1995, 85: 1405-1411.

[62]

Murray TJ, Ellsworth DS, Tissue DT, Riegler M. Interactive direct and plant-mediated effects of elevated atmospheric [CO2] and temperature on a eucalypt-feeding insect herbivore. Glob Chang Biol, 2013, 19: 1407-1416.

[63]

Norby RJ, Cotrufo MF, Ineson P, Neill EGO, Canadell JG. Elevated CO2, litter chemistry, and decomposition: a synthesis. Oecologia, 2001, 127: 153-165.

[64]

Novriyanti E, Watanabe M, Kitao M, Utsugi H, Uemura A, Koike T. High nitrogen and elevated [CO2] effects on the growth, defense and photosynthetic performance of two eucalypt species. Environ Pollut, 2012, 170: 124-213.

[65]

Novriyanti E, Watanabe M, Makoto K, Takeda T, Hashidoko Y, Koike T. Photosynthetic nitrogen and water use efficiency of acacia and eucalypt seedlings as afforestation species. Photosynthetica, 2012, 50: 273-281.

[66]

O’Connor JA, Parbery DG, Strauss W. The effects of phytotoxic gases on native Australian plant species: part 2. Acute injury due to ozone. Environ Pollut, 1975, 7: 7-23.

[67]

Oksanen E, Riikonen J, Kaakinen S, Holopainen T, Vapaavuori E. Structural characteristics and chemical composition of birch (Betula pendula) leaves are modified by increasing CO2 and ozone. Glob Change Biol, 2005, 11: 732-748.

[68]

Ong B-L, Koh CK-K, Wee Y-C. Effects of CO2 on growth and photosynthesis of Pyrrosia piloselloides (L.) Price gametophytes. Photosynthetica, 1998, 35: 21-27.

[69]

Ormrod DP, Lesser VM, Olszyk DM, Tingey DT. Elevated temperature and carbon dioxide affect chlorophylls and carotenoids in Douglas-fir seedlings. Int J Plant Sci, 1999, 160: 529-534.

[70]

Orwa C, Mutua A, Jamnadass R, Anthony S. Agroforestry database: a tree reference and selection guide version 4.0, 2009, Nairobi: World Agroforestry Centre http://www.worldagroforestry.org/output/agroforestree-database

[71]

Paoletti E, Grulke NE. Does living in elevated CO2 ameliorate tree response to ozone? A review on stomatal responses. Environ Pollut, 2005, 137: 483-493.

[72]

Pearson M. Effects of ozone on growth and gas exchange of Eucalyptus globulus seedlings. Tree Physiol, 1995, 15: 207-210.

[73]

Peñaflor M, Erb M, Robert C, Miranda L, Werneburg A, Dossi F, Turlings T, Bento J. Oviposition by a moth suppresses constitutive and herbivore-induced plant volatiles in maize. Planta, 2011, 234: 207-215.

[74]

Percy KE, Legge AH, Krupa SV. Karnosky DF, Percy KE, Chapelka AH, Simpson C, Pikkarainen J. Tropospheric ozone: a continuing threat to global forest?. Air pollution, global change and forest in the new millennium, 2003, Oxford: Elsevier 85 118

[75]

Plett JM, Kohler A, Khachane A, Keniry K, Plett KL, Martin F, Anderson IC. The effect of elevated carbon dioxide on the interaction between Eucalyptus grandis and diverse isolates of Pisolithus sp. is associated with a complex shift in the root transcriptome. New Phytol, 2015, 206: 1423-1436.

[76]

Pritchard SG, Ju Z, van Santen E, Qiu J, Weaver DB, Prior SA, Rogers HH. The influence of elevated CO2 on the activities of antioxidative enzymes in two soybean genotypes. Austral J Plant Physiol, 2000, 27: 1061-1068.

[77]

Proietti C, Anav A, De Marco A, Sicard P, Vitale M. A multi-sites analysis on the ozone effects on gross primary production of European forests. Sci Total Environ, 2016, 556: 1-11.

[78]

Quentin AG, Crous KY, Barton CVM, Ellsworth DS. Photosynthetic enhancement by elevated CO2 depends on seasonal temperatures for warmed and non-warmed Eucalyptus globulus trees. Tree Physiol, 2015, 35: 1249-1263.

[79]

Roden JS, Ball MC. The effect of elevated [CO2] on growth and photosynthesis of two Eucalyptus species exposed to high temperatures and water deficits. Plant Physiol, 1996, 111: 909-919.

[80]

Saitanis CJ, Riga-Karandinos AN, Karandinos MG. Effects of ozone on chlorophyll and quantum yield of tobacco (Nicotiana tabacum L.) varieties. Chemosphere, 2001, 42: 945-953.

[81]

Sandermann H Jr, Ernst D, Heller W, Langebartels C. Ozone: An abiotic elicitor of plant defence reactions. Trends Plant Sci, 1998, 3: 47-50.

[82]

Schulze E-D, Beck E, Müller-Hohenstein K. Plant ecology, 2005, Berlin: Springer.

[83]

Shang B, Yuan X, Li P, Xu Y, Feng Z. Effects of elevated ozone and water deficit on poplar saplings: changes in carbon and nitrogen stocks and their allocation to different organs. For Ecol Manag, 2019, 441: 89-98.

[84]

Shang B, Xu Y, Dai L, Yuan X, Feng Z. Elevated ozone reduced leaf nitrogen allocation to photosynthesis in poplar. Sci Total Environ, 2019, 657: 169-178.

[85]

Shi C, Eguchi N, Meng F, Watanabe T, Satoh F, Koike T. Retranslocation of foliar nutrients of deciduous tree seedlings in different soil condition under free-air O3 fumigation. iForest, 2016, 9: 835-841.

[86]

Shi C, Watanabe T, Koike T. Leaf stoichiometry of deciduous tree species in different soils exposed to free-air O3 enrichment over two growing seasons. Environ Exp Bot, 2017, 138: 148-163.

[87]

Singh AA, Agrawal SB. Tropospheric ozone pollution in India: effects on crop yield and product quality. Environ Sci Pollut Res, 2017, 24: 4367-4382.

[88]

Sitch S, Cox PM, Collins WJ, Huntingford C. Indirect radiative forcing of climate change through ozone effects on the land-carbon sink. Nature, 2007, 448: 791-794.

[89]

Tissue DT, Griffin KL, Ball JT. Photosynthetic adjustment in field-grown ponderosa pine trees after six years of exposure to elevated CO2. Tree Physiol, 1999, 19: 221-228.

[90]

Uddling J, Karlsson PE, Glorvigen A, Selldén G. Ozone impairs autumnal resorption of nitrogen from birch (Betula pendula) leaves, causing an increase in whole-tree nitrogen loss through litter fall. Tree Physiol, 2006, 26: 113-120.

[91]

Wang YN, Koike T. Current status of eucalypts and broadleaved trees in southeastern part of China and their future. For Tech, 2019, 932: 30-33. (in Japanese)

[92]

Wang CF, Yang K, Zhang HM, Cao J, Fang R, Liu ZL, Du SS, Wang YY, Deng ZW, Ligang Z. Components and insecticidal activity against the Maize Weevils of Zanthoxylum schinifolium fruits and leaves. Molecules, 2011, 16: 3077-3088.

[93]

Watanabe M, Watanabe Y, Kitaoka S, Utsugi H, Kita K, Koike T. Growth and photosynthetic traits of hybrid larch F1 (Larix gmelinii var. japonica × L. kaempferi) under elevated CO2 concentration with low nutrient availability. Tree Physiol, 2011, 31: 965-975.

[94]

Xu H, Xie H, Wu S, Wang Z, He K. Effects of elevated CO2 and increased N fertilization on plant secondary metabolites and chewing insect fitness. Front Plant Sci, 2019, 10: 739.

[95]

Yuan X, Calatayud V, Jiang L, Manning WJ, Hayes F, Tian Y, Feng Z. Assessing the effects of ambient ozone in China on snap bean genotypes by using ethylenediurea (EDU). Environ Pollut, 2015, 205: 199-208.

[96]

Yuan X, Calatayud V, Gao F, Fares S, Paoletti E, Tian Y, Feng Z. Interaction of drought and ozone exposure on isoprene emission from extensively cultivated poplar. Plant Cell Environ, 2016, 39: 2276-2287.

[97]

Zheng Y, Li F, Hao L, Yu J, Guo L, Zhou H, Ma C, Zhang X, Xu M. Elevated CO2 concentration induces photosynthetic down-regulation with changes in leaf structure, non-structural carbohydrates and nitrogen content of soybean. BMC Plant Biol, 2019, 19: 255.

AI Summary AI Mindmap
PDF

195

Accesses

0

Citation

Detail

Sections
Recommended

AI思维导图

/