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How important is woody tissue photosynthesis in EuCahetus dunnii Maiden and Osmanthus fragrans (Thunb.) Lour. under O3 stress?

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Abstract

Numerous studies have demonstrated the negative effects of elevated O3 on leaf photosynthesis. Within trees, a portion of respired CO2 is assimilated by woody tissue photosynthesis, but its response to elevated O3 remains unclear. Saplings of two evergreen tree species, EuCahetus dunnii Maiden (E. dunnii) and Osmanthus fragrans (Thunb.) Lour. (O. fragrans), were exposed to non-filtered air (NF), 100 nmol mol−1 O3 air (E1) and 150 nmol mol−1 O3 air (E2) in open-top chambers from May 5 to September 5, 2016 (8 h a day; 7 days a week) in subtropical China. In this study, O3 fumigation significantly reduced leaf net photosynthesis rate in both two tree species on most measurements. However, compared with leaf net photosynthesis rate, woody tissue gross photosynthesis rate showed less negative response to O3 fumigation and was even stimulated to increase. Refixation rate reflects the utilization efficiency of the respired CO2 by woody tissue photosynthesis. During the experiment period, E1 and E2 both increased refixation rate in O. fragrans compared with NF. Whereas for E. dunnii, E1 increased refixation rate until 81 days after starting of fumigation and then decreased it, and E2 decreased it all the time. Refixation rate had a significant positive correlation with woody tissue chlorophyll contents, indicating that the response of refixation rate to elevated O3 may relate to chlorophyll contents. All these suggested that under O3 fumigation, when atmospheric CO2 uptake and fixation by leaf is limited, woody tissue photosynthesis can contribute more to the total carbon assimilation in trees. The findings help to understand the significance of woody tissue photosynthesis under elevated O3 conditions.

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Abbreviations

Chl:

Chlorophyll

O. fragrans :

Osmanthus fragrans (Thunb.) Lour.

E. dunnii :

EuCahetus dunnii Maiden

OTCs:

Open-top chambers

NF:

Non-filtered air

E1:

100 nmol mol−1 O3 air

E2:

150 nmol mol−1 O3 air

DAF:

Days after starting of fumigation

PAR:

Photosynthetically active radiation

R l :

CO2 efflux rate in the light

R d :

CO2 efflux rate in the dark

P g :

The gross photosynthesis rate

Pn:

Net photosynthesis rate

Gs:

Stomatal conductance

RMANOVA:

Repeated measures analysis of variance

AOT40:

Accumulated O3 exposure over a threshold of 40 nmol mol−1

DMA8:

The daily maximum 8-h average concentrations of O3

NOx:

Nitrogen oxides

VOCs:

Volatile organic compounds

References

  • Aschan G, Pfanz H (2003) Non-foliar photosynthesis—a strategy of additional carbon acquisition. Flora 198:81–97

    Article  Google Scholar 

  • Ávila E, Herrera A, Tezara W (2014) Contribution of stem CO2 fixation to whole-plant carbon balance in nonsucculent species. Photosynthetica 52:3–15

    Article  Google Scholar 

  • Berveiller D, Kierzkowski D, Damesin C (2007) Interspecific variability of stem photosynthesis among tree species. Tree Physiol 27:53–61

    Article  CAS  Google Scholar 

  • Bloemen J, Anne McGuire M, Aubrey DP, Teskey RO, Steppe K (2013) Internal recycling of respired CO2 may be important for plant functioning under changing climate regimes. Plant Signal Behav 8:555–565

    Article  Google Scholar 

  • Calatayud A, Iglesias DJ, Talón M, Barreno E (2003) Effects of 2-month ozone exposure in spinach leaves on photosynthesis, antioxidant systems and lipid peroxidation. Plant Physiol Bioch 41:839–845

    Article  CAS  Google Scholar 

  • Calatayud A, Iglesias DJ, Talón M, Barreno E (2004) Response of spinach leaves (Spinacia oleracea L.) to ozone measured by gas exchange, chlorophyll a fluorescence, antioxidant systems, and lipid peroxidation. Photosynthetica 42:23–29

    Article  CAS  Google Scholar 

  • Cao J, Shang H, Chen Z, Tian Y, Yu H (2016) Effects of elevated ozone on stoichiometry and nutrient pools of Phoebe Bournei (Hemsl.) Yang and Phoebe Zhennan S. Lee et FN Wei seedlings in subtropical China. Forests 7:78

    Article  Google Scholar 

  • Castagna A, Di Baccio D, Ranieri AM, Sebastiani L, Tognetti R (2015) Effects of combined ozone and cadmium stresses on leaf traits in two poplar clones. Environ Sci Pollut R 22:2064–2075

    Article  CAS  Google Scholar 

  • Cernusak LA, Marshall JD, Comstock JP, Balster NJ (2001) Carbon isotope discrimination in photosynthetic bark. Oecologia 128:24–35

    Article  Google Scholar 

  • Chen Z, Shang H, Cao J, Yu H (2015) Effects of ambient ozone concentrations on contents of nonstructural carbohydrates in Phoebe bournei and Pinus massoniana seedlings in subtropical China. Water Air Soil Poll 226:310

    Article  Google Scholar 

  • China National Environmental Monitoring Centre (2013) Air Quality Report in 74 Chinese Cities in March and the First half of 2013 Available: http://www.cnemc.cn/publish/106/news/news_37027.html (in Chinese)

  • Damesin C (2003) Respiration and photosynthesis characteristics of current-year stems of Fagus sylvatica: from the seasonal pattern to an annual balance. New Phytol 158:465–475

    Article  Google Scholar 

  • Eyles A, Pinkard EA, O’Grady AP, Worledge D, Warren CR (2009) Role of corticular photosynthesis following defoliation in Eucalyptus globulus. Plant Cell Environ 32:1004–1014

    Article  CAS  Google Scholar 

  • Feng ZZ, Yao FF, Chen Z, Wang XK, Zheng QW, Feng ZW (2007) Response of gas exchange and yield components of field-grown Triticum aestivum L. to elevated ozone in China. Photosynthetica 45:441–446

    Article  CAS  Google Scholar 

  • Feng Z, Wang L, Pleijel H, Zhu J, Kobayashi K (2016) Differential effects of ozone on photosynthesis of winter wheat among cultivars depend on antioxidative enzymes rather than stomatal conductance. Sci Total Environ 572:404–411

    Article  CAS  Google Scholar 

  • Grantz DA, Farrar JF (2000) Ozone inhibits phloem loading from a transport pool: compartmental efflux analysis in Pima cotton. Funct Plant Biol 27:859–868

    Article  CAS  Google Scholar 

  • Harmens H, Hayes F, Sharps K, Mills G, Calatayud V (2017) Leaf traits and photosynthetic responses of Betula pendula saplings to a range of ground-level ozone concentrations at a range of nitrogen loads. J Plant Physiol 211:42–52

    Article  CAS  Google Scholar 

  • Hoshika Y, Katata G, Deushi M, Watanabe M, Koike T, Paoletti E (2015) Ozone-induced stomatal sluggishness changes carbon and water balance of temperate deciduous forests. Sci Rep 5:9871

    Article  CAS  Google Scholar 

  • Ismail I, Basahi J, Hassan I (2014) Gas exchange and chlorophyll fluorescence of pea (Pisum sativum L.) plants in response to ambient ozone at a rural site in Egypt. Sci Total Environ 497:585–593

    Article  Google Scholar 

  • Karnosky D, Pregitzer K, Zak D, Kubiske M, Hendrey G, Weinstein D, Nosal M, Percy K (2005) Scaling ozone responses of forest trees to the ecosystem level in a changing climate. Plant Cell Environ 28:965–981

    Article  CAS  Google Scholar 

  • Kinose Y, Fukamachi Y, Okabe S, Hiroshima H, Watanabe M, Izuta T (2017) Photosynthetic responses to ozone of upper and lower canopy leaves of Fagus crenata Blume seedlings grown under different soil nutrient conditions. Environ Pollut 223:213–222

    Article  CAS  Google Scholar 

  • LA C (2000) Photosynthetic refixation in branches of western white pine. Funct Ecol 14:300–311

    Article  Google Scholar 

  • Lee JB, Cha JS, Hong SC, Choi JY, Myoung JS, Park RJ, Woo JH, Ho C, Han JS, Song CK (2015) Projections of summertime ozone concentration over East Asia under multiple IPCC SRES emission scenarios. Atmos Environ 106:335–346

    Article  CAS  Google Scholar 

  • Li J, Lu K, Lv W, Li J, Zhong L, Ou Y, Chen D, Huang X, Zhang Y (2014) Fast increasing of surface ozone concentrations in Pearl River Delta characterized by a regional air quality monitoring network during 2006-2011. J Environ Sci 26:23–36

    Article  Google Scholar 

  • Matyssek R, Sandermann H (2003) Impact of ozone on trees: an ecophysiological perspective. Prog Bot 64:349–404

    CAS  Google Scholar 

  • Matyssek R, Günthardt-Goerg M, Maurer S, Christ R (2002) Tissue structure and respiration of stems of Betula pendula under contrasting ozone exposure and nutrition. Trees 16:375–385

    Article  CAS  Google Scholar 

  • Matyssek R et al (2010) Enhanced ozone strongly reduces carbon sink strength of adult beech (Fagus sylvatica)—resume from the free-air fumigation study at Kranzberg Forest. Environ Pollut 158:2527–2532

    Article  CAS  Google Scholar 

  • Paoletti E (2007) Ozone impacts on forests. CAB reviews: perspectives in agriculture, veterinary science. Nutr Nat Resour 2(68):13

    Google Scholar 

  • Penrod A, Zhang Y, Wang K, SY W, Leung LR (2014) Impacts of future climate and emission changes on US air quality. Atmos Environ 89:533–547

    Article  CAS  Google Scholar 

  • Percival GC, Sheriffs CN (2002) Identification of drought-tolerant woody perennials using chlorophyll fluorescence. J Arboricult 28:215–223

    Google Scholar 

  • Pfanz H (2008) Bark photosynthesis. Trees 22:137–138

    Article  Google Scholar 

  • Pfanz H, Aschan G, Langenfeld-Heyser R, Wittmann C, Loose M (2002) Ecology and ecophysiology of tree stems: corticular and wood photosynthesis. Sci Nat 89:147–162

    Article  CAS  Google Scholar 

  • Porra R, Thompson W, Kriedemann P (1989) Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy. Biochim Biophys Acta 975:384–394

    Article  CAS  Google Scholar 

  • Ritter W, Andersen C, Matyssek R, Grams T (2011) Carbon flux to woody tissues in a beech/spruce forest during summer and in response to chronic O3 exposure. Biogeosciences 8:3127–3138

    Article  CAS  Google Scholar 

  • Ritter W, Lehmeier CA, Winkler JB, Matyssek R, Grams TEE (2015) Contrasting carbon allocation responses of juvenile European beech (Fagus sylvatica) and Norway spruce (Picea abies) to competition and ozone. Environ Pollut 196:534–543

    Article  CAS  Google Scholar 

  • Saveyn A, Steppe K, Ubierna N, Dawson TE (2010) Woody tissue photosynthesis and its contribution to trunk growth and bud development in young plants. Plant Cell Environ 33:1949–1958

    Article  CAS  Google Scholar 

  • Steppe K, Sterck F, Deslauriers A (2015) Diel growth dynamics in tree stems: linking anatomy and ecophysiology. Trends Plant Sci 20:335–343

    Article  CAS  Google Scholar 

  • Teskey RO, Saveyn A, Steppe K, McGuire MA (2008) Origin, fate and significance of CO2 in tree stems. New Phytol 177:17–32

    CAS  Google Scholar 

  • Tjoelker M, Volin J, Oleksyn J, Reich P (1995) Interaction of ozone pollution and light effects on photosynthesis in a forest canopy experiment. Plant Cell Environ 18:895–905

    Article  CAS  Google Scholar 

  • Vandegehuchte MW, Bloemen J, Vergeynst LL, Steppe K (2015) Woody tissue photosynthesis in trees: salve on the wounds of drought? New Phytol 208:998–1002

    Article  Google Scholar 

  • Wang Y, Wang ZL, Wang H, Guo C, Bao W (2012) Rainfall pulse primarily drives litterfall respiration and its contribution to soil respiration in a young exotic pine plantation in subtropical China. Can J For Res 42:657–666

    Article  Google Scholar 

  • Wittmann C, Pfanz H (2008) Antitranspirant functions of stem periderms and their influence on corticular photosynthesis under drought stress. Trees 22:187–196

    Article  CAS  Google Scholar 

  • Wittmann C, Aschan G, Pfanz H (2001) Leaf and twig photosynthesis of young beech (Fagus sylvatica) and aspen (Populus tremula) trees grown under different light regime. Basic Appl Ecol 2:145–154

    Article  Google Scholar 

  • Wittmann C, Matyssek R, Pfanz H, Humar M (2007) Effects of ozone impact on the gas exchange and chlorophyll fluorescence of juvenile birch stems (Betula pendula Roth.) Environ Pollut 150:258–266

    Article  CAS  Google Scholar 

  • Zhang J, Ferdinand J, Vanderheyden D, Skelly J, Innes J (2001) Variation in gas exchange within native plant species of Switzerland and relationships with ozone injury: an open-top experiment. Environ Pollut 113:177–185

    Article  CAS  Google Scholar 

  • Zhang W, Niu J, Wang X, Tian Y, Yao F, Feng Z (2011) Effects of ozone exposure on growth and photosynthesis of the seedlings of Liriodendron chinense (Hemsl.) Sarg, a native tree species of subtropical China. Photosynthetica 49:29–36

    Article  Google Scholar 

  • Zhang W, Feng Z, Wang X, Niu J (2012) Responses of native broadleaved woody species to elevated ozone in subtropical China. Environ Pollut 163:149–157

    Article  CAS  Google Scholar 

  • Zhang W, Feng Z, Wang X, Niu J (2014) Impacts of elevated ozone on growth and photosynthesis of Metasequoia glyptostroboides Hu et Cheng. Plant Sci 226:182–188

    Article  CAS  Google Scholar 

  • Zheng Y, Lyons T, Ollerenshaw JH, Barnes JD (2000) Ascorbate in the leaf apoplast is a factor mediating ozone resistance in Plantago major. Plant Physiol Bioch 38:403–411

    Article  CAS  Google Scholar 

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Acknowledgements

Special thanks go to Qianyanzhou Ecological Station of Chinese Academy of Sciences for providing the experimental site. We are grateful to the staffs in this station, particularly to Mr. Shanyuan Yin, for their assistance in the field work.

Funding

This work was supported by the National Public Benefit Special Fund of China for Forestry Research (No. 201304313) and the Lecture and Study Program for Outstanding Scholars from Home and Abroad (CAFYBB2011007).

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Correspondence to He Shang.

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Responsible editor: Philippe Garrigues

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Yu, H., Shang, H., Cao, J. et al. How important is woody tissue photosynthesis in EuCahetus dunnii Maiden and Osmanthus fragrans (Thunb.) Lour. under O3 stress?. Environ Sci Pollut Res 25, 2112–2120 (2018). https://doi.org/10.1007/s11356-017-0584-z

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