Elevated CO2 protects poplar (Populus trichocarpa × P. deltoides) from damage induced by O3: identification of mechanisms
Simon D. L. Gardner A D , Peter H. Freer-Smith B , J. Tucker C and Gail Taylor CA School of Biological Sciences, University of Sussex, Falmer, East Sussex, BN1 9QG, UK.
B Forest Research, Alice Holt Lodge, Wrecclesham, FARNHAM, Surrey, GU10 4LH, UK.
C School of Biological Sciences, Bassett Crescent East, University of Southampton, SO16 7PX, UK.
Corresponding author. Email: g.taylor@soton.ac.uk
D Present address: Environment Agency, Rio House, Waterside Drive, Aztec West, Almondsbury, BRISTOL, BS32 4UD, UK.
Functional Plant Biology 32(3) 221-235 https://doi.org/10.1071/FP04131
Submitted: 16 July 2004 Accepted: 13 January 2005 Published: 5 April 2005
Abstract
CO2 concentrations in the Earth’s atmosphere will rise to between 550 and 700 μL L–1 by 2100 (IPCC 2001). In much of the world, ozone (O3) is the air pollutant most likely to be having adverse effects on the growth of plants. Here we describe the impacts of CO2 and O3 episodes (rising to 100 nL L–1), singly and in mixtures on the growth and physiology of an interamerican hybrid poplar (Populus trichocarpa L. (Torr. & Gray ex Hook.) × P. deltoids Bartr. ex Marsh). 700 μL L–1 CO2 increased all growth variables relative to values in 350 μL L–1. Mainstem dry weight showed a 38% increase in year 1 and a 32% increase in year 2. Ozone episodes reduced mainstem dry mass by 45% in 350 μL L–1 CO2 and by 34% in 700 μL L–1 CO2. A / Ci analysis showed limited effects on photosynthetic efficiency of 700 μL L–1 CO2 but in contrast, Vcmax was reduced by O3 episodes. CO2 tended to increase leaf expansion but O3 episodes reduced expansion rates generally although a short period of increased leaf expansion in response to O3 was also observed. O3 reduced leaf solute potentials (Ψs) and increased turgor (P) in young leaves. Cell wall properties (elasticity and plasticity) were both stimulated by ozone and this was associated with increased leaf expansion. A new mechanism is proposed which suggests that O3 may act directly on the cell wall, attacking polysaccharides in the wall that result in altered cell wall properties and leaf growth. O3 episodes increased leaf loss, elevated CO2 delayed abscission and O3 was less effective at accelerating leaf loss in elevated CO2. Overall CO2 increased growth, O3 caused decreases and the treatment combination gave intermediate effects. Thus O3 episodes are less likely to be detrimental to P. trichocarpa × P. deltoides in the CO2 concentrations of the future.
Keywords: CO2, O3, leaf growth, water relations, poplar, biomass accumulation.
Acknowledgments
Financial support from The Royal Society, University of Sussex Development Fund, BBSRC (PG085/0524) and the Forestry Commission is acknowledged. SDL Gardner thanks BBSRC for the award of a studentship. Help and advice from Dr Mark Broadmeadow is also gratefully acknowledged.
Bernacchi C,
Calfapietra C,
Davey PA,
Wittig VE,
Scarascia-Mugnozza GE,
Raines CA, Long SP
(2003) Photosynthesis and stomatal conductance repsonses of poplars to free-air CO2 enrichment (PopFACE) during the first growth cycle and immediately following coppice. New Phytologist 159, 609–621.
| Crossref | GoogleScholarGoogle Scholar |
Bosac C,
Gardner SDL,
Taylor G, Wilkins D
(1995) Elevated CO2 and hybrid poplar: a detailed investigation of root and shoot physiology of P. euramericana, ‘Primo’. Journal of Forest Ecology and Management 74, 103–116.
| Crossref | GoogleScholarGoogle Scholar |
Broadmeadow M,
Freer-Smith PH, Jackson S
(1998) Climate change – the evidence so far and predictions for tree growth. Journal of The Society of Irish Foresters 55, 122–132.
Broadmeadow M, Jackson SB
(2000) Growth responses of Quercus petraea, Fraxinus excelsior and Pinus sylvestris to elevated carbon dioxide, ozone and water supply. New Phytologist 146, 437–451.
| Crossref | GoogleScholarGoogle Scholar |
Calfapietra C,
Gielen B,
Galema ANJ,
Lukac M,
Moscatelli MC,
Ceulemans R, Scarascia-Mugnozza G
(2003) Free-air CO2 enrichment (FACE) enhances biomass production in a short-rotation poplar plantation (POPFACE). Tree Physiology 23, 805–814.
| PubMed |
Carlson RW, Bazzaz FA
(1982) Photosynthetic and growth response to fumigation with SO2 at elevated CO2 in C3 and C4 plants. Oecologia 54, 50–54.
| Crossref | GoogleScholarGoogle Scholar |
Ceulemans R, Mousseau M
(1994) Effects of elevated atmospheric CO2 on woody plants. Tansley Review No. 71. New Phytologist 127, 425–446.
Cleland RE
(1984) The Instron technique as a measure of immediate past wall extensibility. Planta 160, 514–520.
| Crossref | GoogleScholarGoogle Scholar |
Dickson RE,
Coleman MD,
Riemenschneider DE,
Isebrands JG,
Hogan GD, Karnosky DF
(1998) Growth of five hybrid poplar genotypes exposed to interacting elevated CO2 and O3. Canadian Journal of Forestry Research 28, 1706–1716.
| Crossref | GoogleScholarGoogle Scholar |
Ferris R,
Long L,
Bunn SM,
Robinson KM,
Bradshaw HD,
Rae AM, Taylor G
(2002) Leaf stomatal and epidermal cell development: identification of putative quantitative trait loci in relation to elevated carbon dioxide concentration in poplar. Tree Physiology 22, 633–640.
| PubMed |
Freer-Smith PH, Dobson MC
(1989) Ozone flux to Picea sitchensis (Bong) Carr and Picea abies (L) Karst. during short episodes and the effects of thee on transpiration and photosynthesis. Environmental Pollution 59, 161–196.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Frost DL,
Taylor GE, Davis WJ
(1991) Biophysics of leaf growth of hybrid poplar: impact of O3. New Phytologist 118, 407–415.
Fry SC
(1998) Oxidative scission of plant cell wall polysaccharides by ascorbate-induced hydroxyl radicals. The Biochemical Journal 332, 507–515.
| PubMed |
Fry SC,
Dumville JC, Miller JG
(2001) Fingerprinting of polysaccharides attacked by hydroxyl radicals in vitro and in the cell walls of ripening pear fruit. The Biochemical Journal 357, 729–735.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Fuhrer J,
Skarby L, Ashmore MR
(1997) Critical loads of ozone effects on vegetation in Europe. Environmental Pollution 97, 91–106.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Gardner SDL,
Bosac C, Taylor G
(1995) Leaf growth of hybrid poplar following exposure to elevated CO2. New Phytologist 131, 81–90.
Heath, RL ,
and
Taylor, GE (1997). Physiological processes and plant responses to ozone exposure. In ‘Forest decline and zone. Springer Ecological Studies No. 127’. pp. 369–377. (Springer: Berlin)
Hogsett WE,
Weber JE,
Tingey D,
Herstrom A,
Lee EH, Laurence JA
(1997) Environmental auditing: an approach for characterizing tropospheric ozone risk to forests. Environmental Management 21, 105–120.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
IPCC
(2001)
Karnosky DF,
Zak DR,
Pregitzer KS,
Awmack CS, Bockheim JG , et al.
(2003) Tropospheric O3 moderates responses of temperate hardwood forests to elevated CO2: a synthesis of molecular to ecosystem results from the aspen FACE project. Functional Ecology 17, 289.
| Crossref | GoogleScholarGoogle Scholar |
Karnosky DF,
Podila GK,
Gagnon Z,
Pechter P,
Akkapeddi A,
Sheng Y,
Riemenschneider DE,
Coleman MD,
Dickson RE, Isebrands JG
(1998) Genetic control of responses to interacting tropospheric ozone and CO2 in Populus tremuloides. Chemosphere 36, 807–812.
| Crossref | GoogleScholarGoogle Scholar |
Keller T
(1988) Growth and premature leaf fall in American aspen as bioindications for ozone. Environmental Pollution 52, 183–192.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Krupa SC,
McGrath MT,
Anderson CP,
Brooker FL,
Burkey KU,
Chappelka AH,
Chevone BI,
Pell EJ, Zilinskas BA
(2001) Ambient ozone and plant health. Plant Disease 85, 4–12.
Kull O,
Sober A,
Coleman MD,
Dickson RE,
Isebrands JG,
Gagnon Z, Karnosky DF
(1996) Photosynthetic responses of aspen clones to simultaneous exposures of ozone and CO2. Canadian Journal of Forestry Research 26, 639–648.
Kull, O ,
Tulva, I ,
and
Vapaavuori, E (2004). Consequences of elevated CO2 and O3 on birch canopy structure: implementation of a canopy growth model. In ‘Proceedings of the 3rd international workshop on functional–structural tree and stand models’. (Sustainable Forest Management Network: Alberta, Canada)
Lucas PW, Diggle PJ
(1997) The use of longitudinal data analysis to study the multi-seasonal growth responses of Norway and Sitka spruce to summer exposure to ozone: implications for the determination of critical levels. New Phytologist 137, 315–323.
| Crossref |
Loats KV, Rebbeck J
(1999) Interactive effects of ozone and elevated carbon dioxide on the growth and physiology of black cherry, green ash and yellow poplar seedlings. Environmental Pollution 106, 237–248.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
McMurtire RE, Wang Y-P
(1993) Mathematical models of the photosynthetic response of stands to rising CO2 concentrations and temperature. Plant, Cell and Environment 16, 1–13.
Mooi J
(1981) Influence of ozone and sulphur dioxide on defoliation and growth of poplars. Mitt. Forsh. Bun 137, 45–51.
Mortensen LM
(1995) Effect of carbon-dioxide concentration on biomass production on biomass production and partitioning in Betula pubescens EHRH seedlings at different ozone and temperature regimes. Environmental Pollution 87, 337–343.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
NEGTAP
(2001) ‘Transboundary air pollution: acidification, eutrophication and ground-level ozone in the UK.’ Report of the National Group on Transboundary Air Pollution. Department of Environment, Food and Rural Affairs, London.
Norby RJ,
Wullschleger SD,
Gunderson CA,
Johnson DW, Ceulemans R
(1999) Tree responses to rising CO2 in field experiments: implications for the future forest. Plant, Cell and Environment 22, 638–714.
| Crossref |
Polle A,
Pfirrmann T,
Chakrabarti S, Rennenberg H
(1993) The effects of enhanced ozone and enhanced carbon-dioxide concentrations on biomass, pigments and antioxidative enzymes in spruce needles (Picea abies L.). Plant, Cell and Environment 16, 311–316.
Radoglou KM, Jarvis PG
(1990) Effects of CO2 enrichment on four poplar clones. I. Growth and leaf anatomy. Annals of Botany 65, 627–632.
Rae AM,
Robinson KM,
Street NR, Taylor G
(2004) Morphological and physiological traits influencing biomass productivity in short rotation coppice poplar. Canadian Journal of Forest Research 34, 1488–1498.
| Crossref |
Reich PB, Lassoie JP
(1985) Influence of low concentrations of ozone on growth, biomass partitioning and leaf senescence in young hybrid poplar plants. Environmental Pollution 39, 39–51.
Ridge CR,
Hinckley TM,
Stettler RF, Van Volkenburgh E
(1986) Leaf growth characteristics of fast growing hybrid poplar Populus trichocarpa x P. deltoides. Tree Physiology 1, 209–216.
| PubMed |
Schneider SH
(1989) The greenhouse effect: Science and policy. Science 243, 771–781.
Smith P,
Powlson DS,
Smith JU,
Falloon P and
Coleman K
(2000)
The greenhouse effect: Science and policy.
Global Change Biology Vol. 6, 525–539.
Strain B
(1987) Direct effects of increasing CO2 on plants and ecosystems. Trends in Ecology and Evolution 2, 18–21.
| Crossref | GoogleScholarGoogle Scholar |
Taylor G, Frost DL
(1992) Impact of gaseous air pollution on leaf growth of hybrid poplar. Forest Ecology and Management 51, 151–162.
| Crossref | GoogleScholarGoogle Scholar |
Taylor G,
Gardner SDL,
Bosac C,
Flowers TJ,
Crookshanks M, Dolan L
(1995) Effects of elevated CO2 on cellular mechanisms, growth and development of trees with particular reference to hybrid poplar. Forestry 68, 379–390.
Taylor G,
Tricker PJ,
Zhang FZ,
Alston VJ,
Miglietta F, Kuzminsky E
(2003) Spatial and temporal effects of free-air CO2 enrichment (POPFACE) on leaf growth, cell expansion, and cell production in a closed canoy of poplar. Plant Physiology 131, 177–185.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Tricker PJ,
Calfapietra C,
Kuzminsky E,
Puleggi R,
Ferris R,
Nathoo M,
Pleasants LJ,
Alston V,
de Angelis P, Taylor G
(2004) Long-term acclimation of leaf production, development, longevity and quality following 3 yr exposure to free-air CO2 enrichment during canopy closure in Populus. New Phytologist 162, 413–426.
| Crossref | GoogleScholarGoogle Scholar |
Tuskan GA, Walsh ME
(2001) Short-rotation woody crop systems, atmospheric carbon dioxide and carbon management. A US case study. Forestry Chronicle 77, 259–264.
