Hostname: page-component-848d4c4894-hfldf Total loading time: 0 Render date: 2024-06-11T13:38:11.841Z Has data issue: false hasContentIssue false
  • English
  • Français

Effect of Glomus aggregatum on photosynthetic function of snap bean in response to elevated ozone

Published online by Cambridge University Press:  18 February 2015

S. G. WANG ,
X. J. DIAO ,
Y. W. LI  and
L. M. MA
S. G. WANG*
Affiliation:
Department of Environmental Engineering and Science, Beijing University of Chemical Technology, Beijing 100029, P.R. China
X. J. DIAO
Affiliation:
Appraisal Center for Environment and Engineering, Ministry of Environmental Protection, Beijing 100012, P.R. China
Y. W. LI
Affiliation:
State Key Laboratory of Environmental Criteria and Risk Assessment, Chinese Research Academy of Environmental Sciences, Beijing 100012, P.R. China
L. M. MA
Affiliation:
Department of Environmental Engineering and Science, Beijing University of Chemical Technology, Beijing 100029, P.R. China
*
*To whom all correspondence should be addressed. Email: shgwang2013@126.com
Get access Rights & Permissions [Opens in a new window]

Summary

Snap bean genotypes (Phaseolus vulgaris L.) with different ozone (O3) sensitivities (line S156: O3-sensitive; line R123: O3-tolerant) were grown for 70 days with or without inoculation of arbuscular mycorrhizal (AM) fungi under ambient (CAMB = 20 nanolitres (nl)/l and elevated (CMID = '50 nl/l and CHIG = 80 nl/l) O3. Sequential determinations (leaf injury, pigment concentration, chlorophyll fluorescence, photosynthesis, etc) were carried out during plant growth to evaluate mycorrhizal influence on the photosynthetic function of the two genotypes under elevated O3. Inoculation with AM fungi alleviated leaf injury in both genotypes and delayed time of injury manifestation (TIM) in the R123 line at the blooming stage (growth stage (GS): 61-65 (Zadoks scale, Zadoks et al. 1974), 30–35 days after the onset of O3 fumigation), but mycorrhizal effect was slight at the initial growth stage (GS 11–13, 0–5 days after onset of O3 fumigation). Relative to the non-mycorrhizal plant, AM fungi inoculation increased the concentrations of chlorophyll (Chl) a, Chl b and carotenoids in S156 plants, regardless of O3 levels, while in R123 plants a similar effect was observed only in the CAMB treatment. At the blooming (GS 61–65) and the pod filling (GS 71–77, 45–50 days after starting O3 fumigation) stages, photosynthetic rate, stomatal conductance and transpiration rate for the two genotypes decreased with elevated O3 in all treatments, although the effect was reduced in CAMB and CMID treatments in AM-inoculated plants; however, the mycorrhizal effect was slight in the CHIG treatment. Intercellular carbon dioxide concentration increased with elevated O3 regardless of AM fungi inoculation, but it was lower in the mycorrhizal plants than in the non-mycorrhizal plants, in most cases. Furthermore, AM fungi inoculation significantly increased the maximum quantum yield of photosystem II (PS II) photochemistry (Fv/Fm) and electron transport rate in both genotypes in the CHIG treatment. The present study indicated that in some cases, AM fungi inoculation can enhance plant tolerance to elevated O3 through improving plant photosynthetic function, but the effect was reduced by serious O3 stress.

Type
Climate Change and Agriculture Research Papers
Information
The Journal of Agricultural Science , Volume 153 , Issue 5 , July 2015 , pp. 837 - 852
Check for updates
Copyright
Copyright © Cambridge University Press 2015 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Abbott, L. K. & Gazey, C. (1994). An ecological view of the formation of VA mycorrhizas. Plant and Soil 159, 69–78.CrossRefGoogle Scholar
Augé, R. M. (2001). Water relations, drought and VA mycorrhizal symbiosis. Mycorrhiza 11, 3–42.Google Scholar
Augé, R. M., Toler, H. D., Sams, C. E. & Nasim, G. (2008). Hydraulic conductance and water potential gradients in squash leaves showing mycorrhiza-induced increases in stomatal conductance. Mycorrhiza 18, 115–121.CrossRefGoogle ScholarPubMed
Avnery, S., Mauzerall, D. L., Liu, J. & Horowitz, L. W. (2011). Global crop yield reductions due to surface ozone exposure: 2. Year 2030 potential crop production losses and economic damage under two scenarios of O3 pollution. Atmospheric Environment 45, 2297–2309.CrossRefGoogle Scholar
Bagheri, V., Shamshiri, M. H., Shirani, H. & Roosta, H. R. (2011). Effect of mycorrhizal inoculation on ecophysiological responses of pistachio plants grown under different water regimes. Photosynthetica 49, 531–538.CrossRefGoogle Scholar
Bermejo, V., Gimeno, B. S., Sanz, J., De La Torre, D. & Gil, J. M. (2003). Assessment of the ozone sensitivity of 22 native plant species from Mediterranean annual pastures based on visible injury. Atmospheric Environment 37, 4667–4677.CrossRefGoogle Scholar
Bilger, W. & Björkman, O. (1991). Temperature dependence of violaxanthin de-epoxidation and non-photochemical fluorescence quenching in intact leaves of Gossypium hirsutum L. and Malva parviflora L. Planta 184, 226–234.CrossRefGoogle ScholarPubMed
Biswas, D. K., Xu, H., Li, Y. G., Sun, J. Z., Wang, X. Z., Han, X. G. & Jiang, G. M. (2008). Genotypic differences in leaf biochemical, physiological and growth responses to ozone in 20 winter wheat cultivars released over the past 60 years. Global Change Biology 14, 46–59.CrossRefGoogle Scholar
Black, K. G., Mitchell, D. T. & Osborne, B. A. (2000). Effect of mycorrhizal-enhanced leaf phosphate status on carbon partitioning, translocation and photosynthesis in cucumber. Plant, Cell and Environment 23, 797–809.CrossRefGoogle Scholar
Black, V. J., Stewart, C. A., Roberts, J. A. & Black, C. R. (2012). Timing of exposure to ozone affects reproductive sensitivity and compensatory ability in Brassica campestris. Environmental and Experimental Botany 75, 225–234.CrossRefGoogle Scholar
Boldt, K., Pörs, Y., Haupt, B., Bitterlich, M., Kühn, C., Grimm, B. & Franken, P. (2011). Photochemical processes, carbon assimilation and RNA accumulation of sucrose transporter genes in tomato arbuscular mycorrhiza. Journal of Plant Physiology 168, 1256–1263.CrossRefGoogle ScholarPubMed
Bortier, K., De Temmerman, L. & Ceulemans, R. (2000). Effects of ozone exposure in open-top chambers on poplar (Populus nigra) and beech (Fagus sylvatica): a comparison. Environmental Pollution 109, 509–516.CrossRefGoogle ScholarPubMed
Brewer, P. F. & Heagle, A. S. (1983). Interactions between Glomus geosporum and exposure of soybeans to ozone or simulated acid rain in the field. Phytopathology 73, 1035–1040.CrossRefGoogle Scholar
Calatayud, A., Alvarado, J. W. & Barreno, E. (2002). Differences in ozone sensitivity in three varieties of cabbage (Brassica oleracea L.) in the rural Mediterranean area. Journal of Plant Physiology 159, 863–868.CrossRefGoogle Scholar
Calatayud, A., Iglesias, D. J., Talon, M. & Barreno, E. (2004). Response of spinach leaves to ozone measured by gas exchange, chlorophyll a fluorescence, antioxidant systems, and lipid peroxidation. Photosynthetica 42, 23–29.CrossRefGoogle Scholar
Chen, Z., Wang, X. K., Feng, Z. Z., Xiao, Q. & Duan, X. N. (2009). Impact of elevated O3 on soil microbial community function under wheat crop. Water, Air and Soil Pollution 198, 189–198.CrossRefGoogle Scholar
Cho, K., Toler, H., Lee, J., Ownley, B., Stutz, J. C., Moore, J. L. & Augé, R. M. (2006). Mycorrhizal symbiosis and response of sorghum plants to combined drought and salinity stresses. Journal of Plant Physiology 163, 517–528.CrossRefGoogle ScholarPubMed
Cui, X. C., Hu, J. L., Lin, X. G., Wang, F. Y., Chen, R. R., Wang, J. H. & Zhu, J. G. (2013). Arbuscular mycorrhizal fungi alleviate ozone stress on nitrogen nutrition of field wheat. Journal of Agricultural Science and Technology 15, 1043–1052.Google Scholar
Demmig-Adams, B., Adams, W. W., Heber, U., Neimanis, S., Winter, K., Krüger, A., Czygan, F. C., Bilger, W. & Björkman, O. (1990). Inhibition of zeaxanthin formation and of rapid changes in radiationless energy dissipation by dithiothreitol in spinach leaves and chloroplasts. Plant Physiology 92, 293–301.CrossRefGoogle ScholarPubMed
Drew, E. A., Murray, R. S. & Smith, S. E. (2006). Functional diversity of external hyphae of AM fungi: ability to colonise new hosts is influenced by fungal species, distance and soil conditions. Applied Soil Ecology 32, 350–365.CrossRefGoogle Scholar
Duckmanton, L. & Widden, P. (1994). Effect of ozone on the development of vesicular-arbuscular mycorrhizae in sugar maple saplings. Mycologia 86, 181–186.CrossRefGoogle Scholar
Estrada-Luna, A. A. & Davies, F. T. Jr (2003). Arbuscular mycorrhizal fungi influence water relations, gas exchange, abscisic acid and growth of micropropagated chile ancho pepper (Capsicum annuum) plantlets during acclimatization and post-acclimatization. Journal of Plant Physiology 160, 1073–1083.CrossRefGoogle ScholarPubMed
Fangmeier, A., De Temmerman, L., Black, C., Persson, K. & Vorne, V. (2002). Effects of elevated CO2 and/or ozone on nutrient concentrations and nutrient uptake of potatoes. European Journal of Agronomy 17, 353–368.CrossRefGoogle Scholar
Feng, Z. Z., Kobayashi, K. & Ainsworth, E. A. (2008). Impact of elevated ozone concentration on growth, physiology and yield of wheat (Triticum aestivum L.): a meta-analysis. Global Change Biology 14, 2696–2708.CrossRefGoogle Scholar
Finnan, J. M., Donnelly, A., Burke, J. I. & Jones, M. B. (2002). The effects of elevated concentrations of carbon dioxide and ozone on potato (Solanum tuberosum L.) yield. Agriculture, Ecosystems and Environment 88, 11–22.CrossRefGoogle Scholar
Fiscus, E. L., Booker, F. L. & Burkey, K. O. (2005). Crop responses to ozone: uptake, modes of action, carbon assimilation and partitioning. Plant, Cell and Environment 28, 997–1011.CrossRefGoogle Scholar
Flowers, M. D., Fiscus, E. L., Burkey, K. O., Booker, F. L. & Dubois, J.-J. B. (2007). Photosynthesis, chlorophyll fluorescence, and yield of snap bean (Phaseolus vulgaris L.) genotypes differing in sensitivity to ozone. Environmental and Experimental Botany 61, 190–198.CrossRefGoogle Scholar
Francini, A., Nali, C., Picchi, V. & Lorenzini, G. (2007). Metabolic changes in white clover clones exposed to ozone. Environmental and Experimental Botany 60, 11–19.CrossRefGoogle Scholar
Gauss, M., Myhre, G., Isaksen, I. S. A., Grewe, V., Pitari, G., Wild, O., Collins, W. J., Dentener, F. J., Ellingsen, K., Gohar, L. K., Hauglustaine, D. A., Iachetti, D., Lamarque, F., Mancini, E., Mickley, L. J., Prather, M. J., Pyle, J. A., Sanderson, M. G., Shine, K. P., Stevenson, D. S., Sudo, K., Szopa, S. & Zeng, G. (2006). Radiative forcing since preindustrial times due to ozone change in the troposphere and the lower stratosphere. Atmospheric Chemistry and Physics 6, 575–599.CrossRefGoogle Scholar
Genty, B., Briantais, J. M. & Baker, N. R. (1989). The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochimica et Biophysica Acta: General Subjects 990, 87–92.CrossRefGoogle Scholar
Georgieva, K. & Lichtenthaler, H. K. (1999). Photosynthetic activity and acclimation ability of pea plants to low and high temperature treatment as studied by means of chlorophyll fluorescence. Journal of Plant Physiology 155, 416–423.CrossRefGoogle Scholar
Guidi, L., Bongi, G., Ciompi, S. & Soldatini, G. F. (1999). In Vicia faba leaves photoinhibition from ozone fumigation in light precedes a decrease in quantum yield of functional PSII centres. Journal of Plant Physiology 154, 167–172.CrossRefGoogle Scholar
Heath, R. L. & Taylor, G. E. (1997). Physiological processes and plant responses to ozone exposure. In Forest Decline and Ozone (Eds Sandermann, H., Wellburn, A. R. & Heath, R. L.), pp. 317–368. Ecological Studies vol. 127. Berlin: Springer-Verlag.CrossRefGoogle Scholar
IPCC (2007). Climate Change 2007: The Physical Science Basis. Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change (Eds Solomon, S., Qin, D., Manning, M., Chen, Z., Marquis, M., Averyt, K. B., Tignor, M. & Miller, H. L.). Cambridge, UK and New York: Cambridge University Press.Google Scholar
Karnosky, D. F., Zak, D. R., Pregitzer, K. S., Awmack, C. S., Bockheim, J. G., Dickson, R. E., Hendrey, G. R., Host, G. E., King, J. S., Kopper, B. J., Kruger, E. L., Kubiske, M. E., Lindroth, R. L., Mattson, W. J., Mcdonald, E. P., Noormets, A., Oksanen, E., Parsons, W. F. J., Percy, K. E., Podila, G. K., Riemenschneider, D. E., Sharma, P., Thakur, R., Sôber, A., Sôber, J., Jones, W. S., Anttonen, S., Vapaavuori, E., Mankovska, B., Heilman, W. & Isebrands, J. G. (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, 289–304.CrossRefGoogle Scholar
Kollner, B. & Krause, G. H. M. (2000). Changes in carbohydrates, leaf pigments and yield in potatoes induced by different ozone exposure regimes. Agriculture, Ecosystems and Environment 78, 149–158.CrossRefGoogle Scholar
Leitao, L., Dizengremel, P. & Biolley, J. P. (2008). Foliar CO2 fixation in bean (Phaseolus vulgaris L.) submitted to elevated ozone: distinct changes in Rubisco and PEPc activities in relation to pigment content. Ecotoxicology and Environmental Safety 69, 531–540.CrossRefGoogle ScholarPubMed
Lichtenthaler, H. K. (1987). Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Methods in Enzymology 148, 350–382.CrossRefGoogle Scholar
Lichtenthaler, H. K. & Buschmann, C. (1987). Chlorophyll fluorescence spectra of green bean leaves. Journal of Plant Physiology 129, 137–147.CrossRefGoogle Scholar
Liu, F., Wang, X. K. & Zhu, Y. G. (2009). Assessing current and future ozone-induced yield reductions for rice and winter wheat in Chongqing and the Yangtze River Delta of China. Environmental Pollution 157, 707–709.CrossRefGoogle Scholar
Liu, Q., Lam, K. S., Jiang, F., Wang, T. J., Xie, M., Zhuang, B. L. & Jiang, X. Y. (2013). A numerical study of the impact of climate and emission changes on surface ozone over South China in autumn time in 2000–2050. Atmospheric Environment 76, 227–237.CrossRefGoogle Scholar
Mathur, N. & Vyas, A. (1995). I. Influence of VA mycorrhizae on net photosynthesis and transpiration of Ziziphus mauritiana. Journal of Plant Physiology 147, 328–330.CrossRefGoogle Scholar
Maxwell, K. & Johnson, G. N. (2000). Chlorophyll fluorescence-a practical guide. Journal of Experimental Botany 345, 659–668.CrossRefGoogle Scholar
McCool, P. M. & Menge, J. A. (1984). Interaction of ozone and mycorrhizal fungi on tomato as influenced by fungal species and host variety. Soil Biology and Biochemistry 16, 425–427.CrossRefGoogle Scholar
McGonigle, T. P., Miller, M. H., Evans, D. G., Fairchild, G. L. & Swan, J. A. (1990). A new method which gives an objective measure of colonization of roots by vesicular-arbuscular mycorrhizal fungi. New Phytologist 115, 495–501.CrossRefGoogle ScholarPubMed
Miller, J. E., Shafer, S. R., Schoeneberger, M. M., Pursley, W. A., Horton, S. J. & Davey, C. B. (1997). Influence of a mycorrhizal fungus and/or rhizobium on growth and biomass partitioning of subterranean clover exposed to ozone. Water, Air and Soil Pollution 96, 233–248.CrossRefGoogle Scholar
Mills, G., Wagg, S. & Harmens, H. (2013). Ozone Pollution: Impacts on Ecosystem Services and Biodiversity. Report prepared by the ICP Vegetation. Bangor, UK: ICP Vegetation Programme Coordination Centre & Centre for Ecology and Hydrology.Google Scholar
Morgan, P. B., Ainsworth, E. A. & Long, S. P. (2003). How does elevated ozone impact soybean? A meta-analysis of photosynthesis, growth and yield. Plant, Cell and Environment 26, 1317–1328.CrossRefGoogle Scholar
Nawahda, A. & Yamashita, K. (2013). The effect of ground level ozone on vegetation: the case of spatial variability of crops in the People's Republic of China. International Journal of Society Systems Science 5, 82–98.CrossRefGoogle Scholar
Osmond, C. B. (1994). What is photoinhibition? Some insights from comparisons of shade and sun plants. In Photoinhibition of Photosynthesis: from Molecular Mechanisms to the Field (Eds Baker, N. R. & Bowyer, J. R.), pp. 1–24. Oxford, UK: BIOS Scientific Publishers.Google Scholar
Paradi, I., Bratek, Z. & Lang, F. (2003). Influence of arbuscular mycorrhiza and phosphorus supply on polyamine content, growth and photosynthesis of Plantago lanceolata. Biologia Plantarum 46, 563–569.CrossRefGoogle Scholar
Pereira, W. E., De Siqueira, D. L., Martinez, C. A. & Puiatti, M. (2000). Gas exchange and chlorophyll fluorescence in four citrus rootstocks under aluminium stress. Journal of Plant Physiology 157, 513–520.CrossRefGoogle Scholar
Rai, M. K., Shende, S. & Strasser, R. J. (2008). JIP test for fast fluorescence transients as a rapid and sensitive technique in assessing the effectiveness of arbuscular mycorrhizal fungi in Zea mays: analysis of chlorophyll a fluorescence. Plant Biosystems 142, 191–198.CrossRefGoogle Scholar
Read, D. J., Duckett, J. G., Francis, R., Ligrone, R. & Russell, A. (2000). Symbiotic fungal associations in “lower” land plants. Philosophical Transactions of the Royal Society of London Series B-Biological Sciences 355, 815–830.CrossRefGoogle ScholarPubMed
Richards, B. L., Middleton, J. T. & Hewitt, W. B. (1958). Air pollution with relation to agronomic crops: V. Oxidant stipple of grape. Agronomy Journal 50, 559–561.CrossRefGoogle Scholar
Royal Society (2008). Ground-Level Ozone in the 21st Century: Future Trends, Impacts and Policy Implications. Science Policy Report 15/08. London: The Royal Society. Available from: https://royalsociety.org/policy/publications/2008/ground-level-ozone/ (accessed December 2014).Google Scholar
Schoefts, B. & Bertrand, M. (2000). The formation of chlorophyll from chlorophyllide in leaves containing proplastids is a four-step process. FEBS Letters 486, 243–246.CrossRefGoogle Scholar
Shafer, S. R. & Schoeneberger, M. M. (1991). Mycorrhizal mediation of plant-response to atmospheric change - air-quality concepts and research considerations. Environmental Pollution 73, 163–177.CrossRefGoogle ScholarPubMed
Smith, S. E. & Read, D. (2008). Mycorrhizal Symbiosis, 3rd edn. London: Academic Press.Google Scholar
Streets, D. G., Fu, J. S., Jang, C. J., Hao, J. M., He, K. B., Tang, X. Y., Zhang, Y. H., Wang, Z. F., Li, Z. P., Zhang, Q., Wang, L. T., Wang, B. Y. & Yu, C. (2007). Air quality during the 2008 Beijing Olympic Games. Atmospheric Environment 41, 480–492.CrossRefGoogle Scholar
Talaat, N. B. & Shawky, B. T. (2014). Protective effects of arbuscular mycorrhizal fungi on wheat (Triticum aestivum L.) plants exposed to salinity. Environmental and Experimental Botany 98, 20–31.CrossRefGoogle Scholar
Tang, G., Li, X., Wang, Y., Xin, J. & Ren, X. (2009). Surface ozone trend details and interpretations in Beijing, 2001–2006. Atmospheric Chemistry and Physics 9, 8813–8823.CrossRefGoogle Scholar
Tsimilli-Michael, M., Eggenberg, P., Biro, B., Köves-Pechy, K., Vörös, I. & Strasser, R. J. (2000). Synergistic and antagonistic effects of arbuscular mycorrhizal fungi and Azospirillum and Rhizobium nitrogen-fixers on the photosynthetic activity of alfalfa, probed by the polyphasic chlorophyll a fluorescence transient O-J-I-P. Applied Soil Ecology 15, 169–182.CrossRefGoogle Scholar
Wang, H. X., Kiang, C. S., Tang, X. Y., Zhou, X. J. & Chameides, W. L. (2005). Surface ozone: a likely threat to crops in Yangtze delta of China. Atmospheric Environment 39, 3843–3850.Google Scholar
Wang, S. G., Feng, Z. Z., Wang, X. K. & Gong, W. L. (2011). Arbuscular mycorrhizal fungi alter the response of growth and nutrient uptake of snap bean (Phaseolus vulgaris L.) to O3. Journal of Environmental Sciences 23, 968–974.CrossRefGoogle ScholarPubMed
Wang, S. G., Wang, F., Diao, X. J. & He, L. S. (2014). Effects of elevated O3 on microbes in the rhizosphere of mycorrhizal snap bean with different O3 sensitivity. Canadian Journal of Microbiology 60, 93–103.CrossRefGoogle ScholarPubMed
Wang, X. K., Manning, W., Feng, Z. W. & Zhu, Y. G. (2007). Ground-level ozone in China: distribution and effects on crop yields. Environmental Pollution 147, 394–400.CrossRefGoogle Scholar
Wu, Q. S. & Xia, R. X. (2006). Arbuscular mycorrhizal fungi influence growth, osmotic adjustment and photosynthesis of citrus under well-watered and water stress conditions. Journal of Plant Physiology 163, 417–425.CrossRefGoogle ScholarPubMed
Xiao, J. X., Hu, C. Y., Chen, Y. Y., Yang, B. & Hua, J. (2014). Effects of low magnesium and an arbuscular mycorrhizal fungus on the growth, magnesium distribution and photosynthesis of two citrus cultivars. Scientia Horticulturae 177, 14–20.CrossRefGoogle Scholar
Yoshida, L. C., Gamon, J. A. & Andersen, C. P. (2001). Differences in above- and below-ground responses to ozone between two populations of a perennial grass. Plant and Soil 233, 203–211.CrossRefGoogle Scholar
Zadoks, J. C., Chang, T. T. & Konzak, C. F. (1974). A decimal code for the growth stages of cereals. Weed Research 14, 415–421.CrossRefGoogle Scholar
Zheng, J. Y., Zhang, L. J., Che, W. W., Zheng, Z. Y. & Yin, S. S. (2009). A highly resolved temporal and spatial air pollutant emission inventory for the Pearl River Delta region, China and its uncertainty assessment. Atmospheric Environment 43, 5112–5122.CrossRefGoogle Scholar
Zhu, X. C., Song, F. B., Liu, S. Q. & Liu, T. D. (2011). Effects of arbuscular mycorrhizal fungus on photosynthesis and water status of maize under high temperature stress. Plant and Soil 346, 189–199.CrossRefGoogle Scholar
Zuccarini, P. (2007). Mycorrhizal infection ameliorates chlorophyll content and nutrient uptake of lettuce exposed to saline irrigation. Plant, Soil and Environment 53, 283–289.CrossRefGoogle Scholar