Skip to main content
Log in

Growth and photosynthetic response of two larches exposed to O3 mixing ratios ranging from preindustrial to near future

  • Published:
Photosynthetica

Abstract

In this study, we questioned whether ground-level ozone (O3) induces hormesis in Japanese larch (Larix kaempferi) and its hybrid F1 (L. gmelinii var. japonica × L. kaempferi). In order to answer the question, we exposed seedlings of both taxa to four O3 treatments [ranging from ≈10 to 60 nmol(O3) mol–1] in open-top chambers for two consecutive growing seasons. We found a hormetic response in maximum photosynthetic rate (PNmax) at 1700 μmol(CO2) mol–1 and maximum rates of carboxylation (Vcmax) and electron transport (Jmax) in both larches. Stimulation of PNmax, Vcmax, and Jmax did not lead to suppressed plant productivity in Japanese larch, which followed a stress-tolerant strategy, but it did lead to suppressed plant productivity in hybrid larch which followed a competitive strategy. These findings are the first to suggest that stimulation of physiological functions by low O3 exposures may have negative consequences for larch reproduction.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

Abbreviations

CF:

charcoal-filtered air

Chl:

chlorophyll

E :

transpiration rate

g s :

stomatal conductance

GLM:

general linear model

HL:

hybrid larch

HSD:

Tukey’s honest significance difference

JL:

Japanese larch

J max :

maximum electron transport rate

NF:

nonfiltered air

NF40:

NF enriched with O3 to reach 40 nmol mol–1

NF60:

NF enriched with O3 to reach 60 nmol mol–1

NOAEL:

no observed adverse effect level

OTCs:

open-top chambers

P N :

net photosynthetic rate

P Nmax :

maximum photosynthetic rate at 1,700 μmol(CO2) mol–1

RGR:

relative growth rate

ROS:

reactive oxygen species

V cmax :

maximum rate of carboxylation

WUE:

water-use efficiency

References

  • Agathokleous E.: Perspectives for elucidating the ethylenediurea (EDU) mode of action for protection against O3 phytotoxicity. — Ecotox. Environ. Safe. 142: 530–537, 2017.

    Article  CAS  Google Scholar 

  • Agathokleous E., Saitanis C.J., Wang X. et al.: 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 Poll. 227: 1–28, 2016a.

    Article  CAS  Google Scholar 

  • Agathokleous E., Saitanis C.J., Stamatelopoulos D. et al.: Olive oil for dressing plant leaves so as to avoid O3 injury. — Water Air Soil Poll. 227: 282, 2016b.

    Article  CAS  Google Scholar 

  • Agathokleous E., Watanabe M., Eguchi N. et al.: Root production of Fagus crenata blume saplings grown in two soils and exposed to elevated CO2 concentration: an 11-year freeair-CO2 enrichment (FACE) experiment in northern Japan. — Water Air Soil Poll. 227: 187, 2016c.

    Article  CAS  Google Scholar 

  • Agathokleous E., Vanderstock A., Kita K. et al.: Stem and crown growth of Japanese larch and its hybrid F1 grown in two soils and exposed to two free-air O3 regimes. — Environ. Sci. Pollut. R. 24: 6634–6647, 2017.

    Article  CAS  Google Scholar 

  • Ainsworth E.A., Yendrek C.R., Sitch S. et al.: The effects of tropospheric ozone on net primary productivity and implications for climate change. — Annu. Rev. Plant Biol. 63: 637–661, 2012.

    Article  PubMed  CAS  Google Scholar 

  • Ainsworth E.A., Long S.P.: 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. 165: 351–372, 2005.

    Article  PubMed  Google Scholar 

  • Akimoto H., Mori Y., Sasaki K. et al.: Analysis of monitoring data of ground-level ozone in Japan for long-term trend during 1990–2010: causes of temporal and spatial variation. — Atmos. Environ. 102: 302–310, 2015.

    Article  CAS  Google Scholar 

  • Box G.E.P., Cox D.R.: An analysis of transformations. — J. Roy. Stat. Soc. B-Met 26: 211–252, 1964.

    Google Scholar 

  • Calabrese E.J.: Biphasic dose responses in biology, toxicology and medicine: Accounting for their generalizability and quantitative features. — Environ. Pollut. 182: 452–460, 2013.

    Article  PubMed  CAS  Google Scholar 

  • Calabrese E.J.: Hormesis: a fundamental concept in biology. — Microb. Cell 1: 145–149, 2014.

    Article  PubMed  PubMed Central  Google Scholar 

  • Calabrese E.J.: Hormesis: principles and applications. — Homeopathy 104: 69–82, 2015.

    Article  PubMed  Google Scholar 

  • Calatayud V., Marco F., Cerveró J. et al.: Contrasting ozone sensitivity in related evergreen and deciduous shrubs. — Environ. Pollut. 158: 3580–3587, 2010.

    Article  PubMed  CAS  Google Scholar 

  • Cedergreen N., Streibig J.C., Kudsk P. et al.: The occurrence of hormesis in plants and algae. — Dose-Response 5: 150–162, 2007.

    Article  CAS  Google Scholar 

  • Chatani S., Amann M., Goel A. et al.: Photochemical roles of rapid economic growth and potential abatement strategies on tropospheric ozone over South and East Asia in 2030. — Atmos. Chem. Phys. 14: 9259–9277, 2014.

    Article  CAS  Google Scholar 

  • Eamus D., Barnes J.D., Mortensen L. et al.: Persistent stimulation of CO2 assimilation and stomatal conductance by summer ozone fumigation in Norway spruce. — Environ. Pollut. 63: 365–379, 1990.

    Article  PubMed  CAS  Google Scholar 

  • Farquhar G.V., von Caemmerer S.V., Berry J.A.: A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species. — Planta 149: 78–90, 1980.

    Article  PubMed  CAS  Google Scholar 

  • Feng Z., Hu E., Wang X. et al.: Ground-level O3 pollution and its impacts on food crops in China: a review. — Environ. Pollut. 199: 42–48, 2015.

    Article  PubMed  CAS  Google Scholar 

  • Flowers M.D., Fiscus E.L., Burkey K.O. et al.: Photosynthesis, chlorophyll fluorescence, and yield of snap bean (Phaseolus vulgaris L.) genotypes differing in sensitivity to ozone. — Environ. Exp. Bot. 61: 190–198, 2007.

    Article  CAS  Google Scholar 

  • Fuhrer D., Skärby L., Ashmore M.R.R.: Critical levels for ozone effects on vegetation in Europe. — Environ. Pollut. 97: 91–106, 1997.

    Article  PubMed  CAS  Google Scholar 

  • Gower S.T., Richards J.H.: Larches: deciduous conifers in an evergreen world. — BioScience 40: 818–826, 1990.

    Article  Google Scholar 

  • Grantz D.A., Gunn S., Vu H.B.: O3 impacts on plant development: a meta-analysis of root/shoot allocation and growth. — Plant Cell Environ. 29: 1193–1209, 2006.

    Article  PubMed  CAS  Google Scholar 

  • Grime J.P.: Evidence for the existence of three primary strategies in plants and its relevance to ecological and evolutionary theory. — Am. Nat. 111: 1169–1194, 1977.

    Article  Google Scholar 

  • Gyu K.D., Shi C., Watanabe M. et al.: Growth of Japanese and hybrid larch seedlings grown under free-air O3 fumigation — an initial assessment of the effects of adequate and excessive nitrogen. — J. Agr. Meteorol. 71: 239–244, 2015.

    Article  Google Scholar 

  • Hartmann D.L., Klein Tank A.M.G., Rusticucci M., et al.: Observations: atmosphere and surface. — In: Stocker T.F., Qin D., Plattner G.-K. et al. (ed.): 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, New York 2013.

    Google Scholar 

  • Hoffmann W.A., Poorter H.: Avoiding bias in calculations of relative growth rate. — Ann. Bot.-London 90: 37–42, 2002.

    Article  Google Scholar 

  • Hopkins W.G.: A new view of statistics. — Internet Society for Sport Science. Available at http://newstats.org, 2000.

    Google Scholar 

  • Hoshika Y., Watanabe M., Inada N. et al.: Model-based analysis of avoidance of ozone stress by stomatal closure in Siebold’s beech (Fagus crenata). — Ann. Bot.-London 112: 1149–1158, 2013.

    Article  CAS  Google Scholar 

  • IGBP: The terrestrial carbon cycle: Implication for the Kyoto Protocol. — Science 280: 1393–1394, 1998.

    Article  Google Scholar 

  • Kalabokas P.D., Thouret V., Cammas J.-P. et al.: The geographical distribution of meteorological parameters associated with high and low summer ozone levels in the lower troposphere and the boundary layer over the eastern Mediterranean (Cairo case). — Tellus B 67: 27853, 2015.

    Article  CAS  Google Scholar 

  • Kita K., Fujimoto T., Uchiyama K. et al.: Estimated amount of carbon accumulation of hybrid larch in three 31-year-old progeny test plantations. — J. Wood Sci. 55: 425–434, 2009.

    Article  CAS  Google Scholar 

  • Kitao M., Yasuda Y., Kominami Y. et al.: Increased phytotoxic O3 dose accelerates autumn senescence in an O3-sensitive beech forest even under the present-level O3. — Sci. Rep. 6: 32549, 2016.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Koike T., Mao Q., Inada N. et al.: 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. 6: 104–110, 2012.

    Article  CAS  Google Scholar 

  • Koike T., Watanabe M., Hoshika Y. et al.: Effects of ozone on forest ecosystems in East and Southeast Asia. — In: Matyssek R., Clarke N., Cudlin P., et al. (ed.): Climate Change, Air Pollution and Global Challenges: Understanding and Solutions from Forest Research, A COST Action. Pp. 371–390. Elsevier, Oxford 2013.

    Google Scholar 

  • Küppers M.: Ecological significance of above-ground architectural patterns in woody plants: A question of costbenefit relationships. — Trends Ecol. Evol. 4: 375–379, 1989.

    Article  PubMed  Google Scholar 

  • Kurinobu S.: Forest tree breeding for Japanese larch. — Eurasian J., For. Res. 8: 127–134, 2005.

    Google Scholar 

  • Liancourt P., Callaway R.M., Michalet R.: Stress tolerance and competitive-response ability determine the outcome of biotic interactions. — Ecology 86: 1611–1618, 2005.

    Article  Google Scholar 

  • Long S.P., Bernacchi C.J.: Gas exchange measurements, what can they tell us about the underlying limitations to photosynthesis? Procedures and sources of error. — J. Exp. Bot. 54: 2393–2401, 2003.

    Article  PubMed  CAS  Google Scholar 

  • Manninen S., Huttunen S., Vanhatalo M. et al.: Inter-and intraspecific responses to elevated ozone and chamber climate in northern birches. — Environ. Pollut. 157: 1679–1688, 2009.

    Article  PubMed  CAS  Google Scholar 

  • Matyssek R., Bytnerowicz A., Karlsson P.E. et al.: Promoting the ozone flux concept for European forest trees. — Environ. Pollut. 146: 587–607, 2007.

    Article  PubMed  CAS  Google Scholar 

  • Matyssek R., Schulze E.-D.: Heterosis in hybrid larch (Larix decidua x L., leptolepis). — Trees 1: 225–231, 1987.

    Article  Google Scholar 

  • Osawa A., Zyryanova O.A., Matsuura Y. et al. (ed.): Permafrost Ecosystems: Siberian Larch Forests. — Ecological Studies 209. Pp. 502. Springer, Dordrecht 2010.

    Google Scholar 

  • Paoletti E.: Impact of ozone on Mediterranean forests: A review. — Environ. Pollut. 144: 463–474, 2006.

    Article  PubMed  CAS  Google Scholar 

  • Paoletti E., Manning W.J.: Toward a biologically significant and usable standard for ozone that will also protect plants. — Environ. Pollut. 150: 85–95, 2007.

    Article  PubMed  CAS  Google Scholar 

  • Paoletti E., Ranieri A., Lauteri M.: Moving toward effective ozone flux assessment. — Environ. Pollut. 156: 16–19, 2008.

    Article  PubMed  CAS  Google Scholar 

  • Pell E.J., Temple P.J., Friend A.L. et al.: Compensation as a plant response to ozone and associated stresses: an analysis of ROPIS experiments. — J. Environ. Qual. 23: 429–436, 1994.

    Article  CAS  Google Scholar 

  • Qu L.: Ecophysiological study on the natural regeneration of the two larch species with special references to soil environment in larch forests. — Eurasian J., For. Res. 19: 1–51, 2016.

    Google Scholar 

  • Ryu K., Watanabe M., Shibata H. et al.: Ecophysiological responses of the larch species in northern Japan to environmental changes as a basis for afforestation. — Landsc. Ecol. Eng. 5: 99–106, 2009.

    Article  Google Scholar 

  • Schneider C.A., Rasband W.S., Eliceiri K.W.: NIH Image to ImageJ: 25 years of image analysis. — Nat. Methods 9: 671–675, 2012.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Šesták Z., (ed.): Photosynthesis during Leaf Development. Pp. 396. Springer, Dordrecht, Boston 1985.

    Book  Google Scholar 

  • Shinano T., Lei T.T., Kawamukai T. et al.: Dimethylsulfoxide method for the extraction of chlorophylls a and b from the leaves of wheat, field bean, dwarf bamboo, and oak. — Photosynthetica 32: 409–415, 1996.

    CAS  Google Scholar 

  • Sicard P., Serra R., Rossello P.: Spatiotemporal trends in groundlevel ozone concentrations and metrics in France over the time period 1999–2012. — Environ. Res. 149: 122–144, 2016.

    Article  PubMed  CAS  Google Scholar 

  • Vázquez-Ybarra J.A., Peña-Valdivia C.B., Trejo C. et al.: Promoting growth of lettuce plants (Lactuca sativa L.) with sublethal ozone doses applied to culture medium. — Rev. Fitotec. Mex. 38: 405–413, 2015.

    Google Scholar 

  • Verstraeten W.W., Neu J.L., Williams J.E. et al.: Rapid increases in tropospheric ozone production and export from China. — Nature Geosci. 8: 690–695, 2015.

    Article  CAS  Google Scholar 

  • Whitehead F.H., Myerscough P.J.: Growth analysis of plants. The ratio of mean relative growth rate to mean relative rate of leaf area increase. — New Phytol. 61: 314–321, 1962.

    Article  Google Scholar 

  • Yamaguchi M., Watanabe M., Matsumura H. et al.: Experimental studies on the effects of ozone on growth and photosynthetic activity of Japanese forest tree species. — Asian J., Atmos. Environ. 5: 65–78, 2011.

    Article  CAS  Google Scholar 

  • Yendrek C.R., Leisner C.P., Ainsworth E.A.: Chronic ozone exacerbates the reduction in photosynthesis and acceleration of senescence caused by limited N availability in Nicotiana sylvestris. — Glob. Change Biol. 19: 3155–3166, 2013.

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to E. Agathokleous or T. Koike.

Additional information

Acknowledgements: This study was supported by a Type B Grant-in-Aid (No. 26292075, to T. Koike) from Japan Society for the Promotion of Science (JSPS). E. Agathokleous is a JSPS International Research Fellow (ID No: P17102). JSPS is a nonprofit organization.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Sugai, T., Kam, DG., Agathokleous, E. et al. Growth and photosynthetic response of two larches exposed to O3 mixing ratios ranging from preindustrial to near future. Photosynthetica 56, 901–910 (2018). https://doi.org/10.1007/s11099-017-0747-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11099-017-0747-7

Additional key words

Navigation