Influence of multicomponent contamination on the content of photosynthetic pigments in the leaves of woody plants commonly planted for greening of cities

V. P. Bessonova; A. S. Chongova; A. V. Sklyarenko

doi:10.15421/012026

V. P. Bessonova Dnipro State Agrarian and Economic University http://orcid.org/0000-0002-4310-0971
A. S. Chongova Dnipro State Agrarian and Economic University http://orcid.org/0000-0002-4292-8427
A. V. Sklyarenko Dnipro State Agrarian and Economic University http://orcid.org/0000-0002-4954-5007

DOI: https://doi.org/10.15421/012026

Keywords: technogenic conditions; trees; leaf plates; chlorophyll; carotenoids.

Abstract

Woody plants, as an important element of optimization of the urban environment, respond negatively to the ever-increasing technogenic pressure in cities. Therefore, it is necessary to assess their vital status, the most sensitive indicator of which being the content of plastid pigments. In this article we analyze the effects of multicomponent contamination on quantitative fluctuation of the level of photosynthetic pigments in the leaves of woody plants and identify sensitive species for the purpose of phytoindication in order to assess the state the environment is currently in. For the purposes of our research we chose the most widespread tree species in the city of Dnipro (Steppe zone of Ukraine), growing in the area of intensive industrial pollution and high levels of emissions by vehicles. We determined the content of photosynthetic pigments (chlorophylls a and b, a + b, carotenoids) in the leaves of woody plants during different months of the growing season (June, July, August) and afterwards this data was used to compare the given parameters against the values taken from trees in the control area. The sum of chlorophyll levels a + b for the majority of plants was decreasing compared to the control. A more significant decrease in the content given by the sum of the a and b chlorophyll levels is observed in the assimilation organs of Aesculus hippocastanum L., Pinus pallasiana (D. Don) and Picea abies (L.) H. The most significant changes in the content of pigments in the leaves of plants under study were detected at the end of the growing season (in August). The content of green pigments in the leaves of Robinia pseudoacacia L., Platanus orientalis L. remains virtually unchanged. Under the influence of multicomponent contamination, the amount of pigments in the case of chlorophyll a in the majority of woody plant species decreases more rapidly compared to the control than in the case of chlorophyll b. The most noticeable drop in the content of chlorophyll a occurs in the leaves of Betula pendula Roth, Ae. hippocastanum, P. pallasiana, Acer platanoides L. and Tilia cordata Mill. The needles of P. abies and Picea pungens Engelm. 'Glauca’ on the contrary suffer from a significant reduction in the concentration of chlorophyll b. The species most resistant to multicomponent contamination in terms of changes in the content of chlorophyll in the leaf blade are R. pseudoacacia, P. orientalis. The concentration of carotenoids in the leaves of plants such as B. pendula, Ae. hippocastanum, A. platanoides, T. cordata, P. abies is lower than that of species growing in the relatively clean zone. The concentration of pigments in Populus alba L., P. pungens 'Glauca’ was higher during all of the months elapsed since the beginning of our study, whereas Ulmus laevis Pall., P. orientalis and R. pseudoacacia – had their concentrations reach an all time high in the second half of the growing season. Therefore, the peculiarities of quantitative fluctuation of photosynthetic pigments in plants, which are characterized by the variable resistance ability against the effects of technogenic multicomponent contamination, have been identified.

References

Asada, K., Kiso, K., & Yoshikawa, R. (1974). Univalent reduction of molecular oxygen by spinach chloroplasts on illumination. Journal of Biological Chemistry, 249(7), 2175–2181.

Barahteneva, L. A., & Nikolaevskij, B. C. (1988). Vlijanie sernistogo gaza na fotosintez rastenij [The effect of sulfur dioxide on plant photosynthesis]. Nauka, Novosibirsk (in Russian).

Baumgardner, D., Varela, S., Escobedo, F. J., Chacalo, A., & Ochoa, C. (2012). The role of a peri-urban forest on air quality improvement in the Mexico City megalopolis. Environmental Pollution, 163, 174–183.

Bessonova, V. P. (1999). Citofiziologicheskie effekty vozdejstvija tjazhelyh metallov na rost i razvitie rastenij: monografija [Cytophysiological effects of heavy metals on plant growth and development]. ZGU, Zaporozhe (in Russian).

Bessonova, V. P. (2006). Vlijanie tjazhelyh metallov na fotosintez rastenij [The effect of heavy metals on plant photosynthesis]. DGAU, Dnepropetrovsk (in Russian).

Bessonova, V. P., & Ivanchenko, O. Y. (2007). Otsinka funktsionalnoho stanu derevnykh nasadzhen parkiv mista Dnipro za pokaznykamy intensyvnosti vilnoradykalnoho okysnennia ta vmistu prolinu [Assessment of the functional state of tree stands of Dnipro parks by the intensity of free radical oxidation and proline content]. Ukrainian Journal of Ecology, 7(3), 146–153 (in Ukrainian).

Bessonova, V. P., & Yakovleva-Nosar, S. O. (2004). Stan asymiliatsiinoho aparatu i netto-fotosyntez virhinilnykh derevnykh roslyn za umov priorytetnoho zabrudnennia khlorystymy spolukamy [State of assimilation apparatus and net photosynthesis of virgin woody plants under priority contamination by chlorine compounds]. Problemy Ekologii i Ohrany Prirody Tehnogennogo Regiona, 4, 157–162 (in Ukrainian).

Bessonova, V. P., Kapelyush, N. V., Ovcharenko, S. V., & Pismenchuk, V. D. (2004). Vlijanie polikomponentnyh vybrosov avtomobil’nogo transporta na soderzhanie hlorofilla v list’jah drevesnyh rastenij [The effect of multicomponent emissions of automobile transport on the content of chlorophyll in the leaves of woody plants]. Biuleten Derzhavnoho Nikitskoho Botanichnoho Sadu, 89, 73–75 (in Russian).

Bessonova, V., & Grytsay, Z. (2018). Content of plastid pigments in the needles of Pinus pallasiana D. Don in different forest growth conditions of anti-erosion planting. Ekológia (Bratislava), 37(4), 338–344.

Bessonova, V., Dzhyhan, O., Ivanchenko, O., & Ponomarova, O. (2020). The phytotoxic effects of lead, cadmium and sodium chloride on the morphological and characteristics of ornamental herbaceous plants. In: Landi, M., Shemet, S. A., & Fedenko, V. S. (Eds.). Metal toxicity in higher plants. Nova Science Publishers, New York. Pp. 157–202.

Borisova-Mubarakshina, M. M., Vetoshkina, D. V., & Ivanov, B. N. (2019). Antioxidant and signaling functions of the plastoquinone pool in higher plants. Physiologia Plantarum, 166, 181–198.

Buharina, I. L., Kuzmin, P. A., & Gibadulina, I. I. (2013). Analiz soderzhanija fotosinteticheskih pigmentov v list’jah drevesnyh rastenij v uslovijah gorodskoj sredy (g. Naberezhnye Chelny) [Analysis of the content of photosynthetic pigments in the leaves of woody plants in an urban environment (Naberezhnye Chelny)]. Vestnik Udmurdskogo Universiteta, 1, 20–25 (in Russian).

Buharina, I. L., Povarnicina, T. M., & Vedernikov, K. E. (2007). Еkologo-biologicheskie osobennosti drevesnyh rastenij v urbanizirovannoj srede [Ecological and biological characteristics of woody plants in an urbanized environment]. IzhGSHA, Izhevsk (in Russian).

Calfapietra, C., Peñuelas, J., & Niinemets, Ü. (2015). Urban plant physiology: Adaptation-mitigation strategies under permanent stress. Trends in Plants Science, 20(2), 72–75.

Candekova, O. L., & Neverova, O. A. (2010). Vlijanie vybrosov avtotransporta na pigmentnyj kompleks list’ev drevesnyh rastenij [The effect of vehicle emissions on the pigment complex of leaves of woody plants]. Izvestija Samarskogo Nauchnogo Centra RAN, Biologicheskie Resursy: Flora, 1(3), 853–856 (in Russian).

Chuhai, A. V., Cherniakova, O. I., & Bazyka, Y. V. (2018). Analiz tekhnohennoho navantazhennia na povitrianyi basein okremykh promyslovo-miskykh ahlomeratsii skhidnoi Ukrainy (na prykladi mista Dnipro) [The analysis of the current navantazhennia on povitrianyi basein okremykh promyslovo-miskykh ahlomeratsii skhidnoi Ukrainy (on the example of the Dnipro city)]. Visnyk Kharkivs’kogo Nacional’nogo Universitetu Imeni V. N. Karazina, Ekolohiia, 19, 75–81 (in Ukrainian).

Croce, R., Miller, M. G., Bassi, R., & Holzwath, A. R. (2001). Carotenoid-to-chlorophyll energy transfer in recombinant major light-harvesting complex (LHCII) of higher plants. I. Femtosecond transient absorption measurements. Biophysical Journal, 80(2), 901–915.

Dall'Osto, L., Cazzaniga, S., Havaux, M., & Bassi, R. (2010). Enhanced photoprotection by protein-bound vs free xanthophyll pools: A comparative analysis of chlorophyll b and xanthophyll biosynthesis mutants. Molecular Plant, 3(3), 576–593.

Dymova, V., & Golovko, T. K. (2007). Sostojanie pigmentnogo apparata rastenij zhivuchki polzuchej v svjazi s adaptaciej k svetovym uslovijam proizrastanija [The state of the pigment apparatus of tenacious creeping plants in connection with adaptation to the light conditions of growth]. Fiziologija Rastenij, 54(1), 47–53 (in Russian).

Edge, R., & Truscott, G. (2010). Properties of carotenoid radicals and excited states and their potential role in biological systems. In: Landrum, J. T. (Ed.). Carotenoids: Physical, chemical, and biological functions and properties. Taylor & Francis. Рр. 283–307.

Edge, R., McGarvey, D. J., & Truscott, T. G. (1997). The carotenoids as anti-oxidants – a review. Journal of Photochemistry Photobiology B, 41(3), 189–200.

Escobedo, F. J., Kroeger, T., & Wagner, J. E. (2011). Urban forests and pollution mitigation: Analyzing ecosystem services and disservices. Environmental Pollution, 159(8–9), 2078–2087.

Faly, L. I., & Brygadyrenko, V. V. (2014). Patterns in the horizontal structure of litter invertebrate communities in windbreak plantations in the steppe zone of the Ukraine. Journal of Plant Protection Research, 54(4), 414–420.

Formaggio, E., Cinque, G., & Bassi, R. (2001). Functional architecture of the major light-harvesting complex from higher plants. Journal of Molecular Biology, 314(5), 1157–1166.

Frank, H. A. (1999). Іncorporation of carotenoids into reaction center and light-harvesting pigmen-protein complexes. In: Frank, H. A., Young, A., Britton, G., & Cogdell, R. J. (Eds.). Photochemistry of carotenoids. Kluwer Academic Publishers, Dordrecht. Рp. 235–244.

Frolov, A. K., & Gorishina, T. K. (1982). Osobennosti fotosinteticheskogo apparata nekotoryh drevesnyh porod v gorodskih uslovijah [Features of the photosynthetic apparatus of some tree species in urban environments]. Botanicheskij Zhurnal, 67(5), 599–609 (in Russian).

Gavrilenko, V. F., & Zhigalova, T. V. (2003). Bol’shoj praktikum po fotosintezu [Great workshop on photosynthesis]. Akademija, Moscow (in Russian).

Getko, N. V. (1989). Rastenija v tehnogennoj srede [Plants in a technogenic environment]. Nauka i Tehnika, Minsk (in Russian).

Gill, S. S., & Tuteja, N. (2010). Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiology and Biochemistry, 48(12), 909–930.

Havaux, M. (1998). Carotenoids as membrane stabilizers in chloroplasts. Trends in plant science, 3(4), 147–151.

Hnativ, P. S. (2014). Funktsionalna diahnostyka v dendrolohii [Functional diagnostics in dendrology]. Kamula, Lviv (in Ukrainian).

Host, S., Chatignoux, E., Leal, C., & Grémy, I. (2012). Health risk assessment of traffic-related air pollution near busy roads. Revue d’Epidemiologie et de Sante Publique, 60(4), 321–330 (in French).

Il’kun, G. M. (1971). Gazoustojchivost’ rastenij [Gas resistance of plants]. Naukova Dumka, Kiev (in Russian).

Il’kun, G. M. (1978). Zagrjazniteli atmosfery i rastenija [Air pollutants and plants]. Naukova Dumka, Kiev (in Russian).

Jim, C. Y., & Chen, W. Y. (2008). Assessing the ecosystem service of air pollutant removal by urban trees in Guangzhou (China). Journal of Environmental Economics and Management, 88(4), 665–676.

Kabar, A. M. (2015). Kataloh roslyn Botanichnoho sadu Dnipropetrovskoho natsional’noho universytetu imni Olesia Honchara [Catalog of Plants of the Botanical Garden of Oles Honchar Dnipropetrovsk National University]. Lira, Dnipropetrovsk (in Ukrainian).

Kolupaev, Y. E., & Karpec, Y. V. (2019). Aktivnye formy kisloroda, antioksidanty i ustojchivost’ rastenij k dejstviju stressorov [Active forms of oxygen, antioxidants and plant resistance to stress]. Logos, Kiev (in Russian).

Korshikov, I. I. (1996). Adaptacija rastenij k uslovijam tehnogenno zagrjaznennoj sredy [Adaptation of plants to the conditions of anthropogenic polluted environment]. Naukova Dumka, Kiev (in Russian).

Kulagin, A. Y., & Shahmetova, R. I. (2016). Osobennosti soderzhanija fotosinteticheskih pigmentov v hvoe sosny obyknovennoj v uslovijah neftjanogo zagrjaznenija [Features of the content of photosynthetic pigments in the needles of common pine under oil pollution]. Izvestija Samarskogo Nauchnogo Centra RAN, 18(2), 434–437 (in Russian).

Kurchii, B. O. (2000). Abstsyzova kyslota yak kintsevyi produkt antyokysniuval’noho metabolizmu ksantofiliv, zumovlenoho diieiu dykvatu [Abscisic acid as a final product of the antioxidant metabolism of xanthophylls caused by the action of diquat]. Fiziologiya i Biohimiya Kulturnyh Rastenij, 32(4), 334–338 (in Ukrainian).

Ladygin, V. G., & Shirshikova, G. N. (2006). Sovremennoe predstavlenie o funkcional’noj roli karotinoidov v hloroplastah eukariot [Current understanding of the functional role of carotenoids in eukaryotic chloroplasts]. Zhurnal Obshhej Biologi, 67(3), 163–189 (in Russian).

Li, Z., Chen, D., Cai, S., & Che, S. (2018). The ecological services of plant communities in parks for climate control and recreation – A case study in Shanghai, China. PLoS One, 13(4), e0196445.

Lindahl, M., Yang, D. H., & Anderson, B. (1995). Regulatory proteolysis of the major light-harvesting chlorophyll a/b protein complex of photosystem II by a light-induced membrane associated enzymic system. European Journal of Biochemistry, 231, 503–509.

Livesley, S. J., McPherson, G. M., & Calfapietra, C. (2016). The urban forest and ecosystem services: Impacts on urban water, heat, and pollution cycles at the tree, street, and city scale. Journal of Environmental Quality, 45(1), 119–124.

Lovett, G. M., Tear, T. H., Evers, D. C., Findlay, S. E., Cosby, B. J., Dunscomb, J. K., Driscoll, C. T., & Weathers, K. C. (2009). Effects of air pollution on ecosystems and biological diversity in the Eastern United States. Annals of the New York Academy of Sciences, 1162, 99–135.

McNutly, I. B., & Newman, D. W. (1964). Mechanism of fluoride induced chlorosis. Plant Physiology, 36(4), 121–124.

Mihajlova, T. A., & Berezhnaya, N. S. (2000). Ocenka sostojanija sosnovyh lesov pri dlitel’nom vozdejstvii vybrosov aljuminievogo zavoda [Assessment of the state of pine forests during the long-term exposure to emissions from an aluminum smelter]. Geografija i Prirodnye Resursy, 1, 43–50 (in Russian).

Miller, R. R., Miller, G. J., & Mclntyre, K. R. (1976). The light-harvesting chlorophyll-protein complex of photosystem II. Its location in the photosynthetic membrane. Journal of Cell Biology, 71(2), 624–638.

Nobel, P. (1974). Ozone effects on chlorophylls a and b. Paturwissenschaften, 2, 80–81.

Ovechkina, V. S., & Shahmetova, R. I. (2015). Vlijanie antropogennyh faktorov na soderzhvnie pigmentov sosny obyknovennoj v letnij period na territorii Nizhevartovskogo rajona [The influence of anthropogenic factors on the content of pigments of Scots pine in the summer in the Nizhevartovsky district]. Izvestija Samarskogo Nauchnogo Centra RAN, 17(6), 236–241 (in Russian).

Parmar, P., Nilima, K., & Vinay, S. (2013). Structural and functional alterations in photosynthetic apparatus of plants under cadmium stress. Botanica Studies, 54(45), 1–6.

Pascal, A. A., Liu, Z., Broess, K., van Oort, B., van Amerongen, H., Wang, C., Horton, P., Robert, B., Chang, W., & Ruban, A. (2005). Molecular basis of photoprotection and control of photosynthetic light-harvesting. Nature, 436(7047), 134–137.

Pinzino, C., Capocchi, A., Galleschi, L., Saviozzi, F., Nanni, B., & Zandomeneghi, M. (1999). Aging, free radicals, and antioxidants in wheat seeds. Journal of Agricultural and Food Chemistry, 47(4), 1333–1339.

Popek, R., Przybysz, A., Gawrońska, H., Klamkowski, K., & Gawroński, S. W. (2018). Impact of particulate matter accumulation on the photosynthetic apparatus of roadside woody plants growing in the urban conditions. Ecotoxicology and Environmental Safety, 163, 56–62.

Rai, P. K. (2016). Impacts of particulate matter pollution on plants: Implications for environmental biomonitoring. Ecotoxicology and Environmental Safety, 129, 120–136.

Salmond, J. A., Tadaki, M., Vardoulakis, S., Arbuthnott, K., Coutts, A., Demuzere, M., Dirks, K. N., Heaviside, C., Lim, S., Macintyre, H., McInnes, R. N., & Wheeler, B. W. (2016). Health and climate related ecosystem services provided by street trees in the urban environment. Environmental Health, 15(Suppl 1), 36.

Schwela, D. (2000). Air pollution and health in urban areas. Reviews on Environmental Health, 15(1–2), 13–42.

Sen, A., Khan, I., Kundu, D., Das, K., & Datta, J. K. (2017). Ecophysiological evaluation of tree species for biomonitoring of air quality and identification of air pollution-tolerant species. Environmental Monitoring and Assessment, 189(6), 262.

Sergejchik, S. A. (1994). Ustojchivost’ drevesnyh rastenij v tehnogennoj srede [The resistance of woody plants in a technogenic environment]. Nauka i tehnika, Minsk (in Russian).

Sergejchik, S. A., Sergejchik, A. A., & Sidorovich, E. A. (1998). Ekologicheskaja fiziologija hvojnyh porod Belarusi v tehnogennoj srede [Ecological physiology of coniferous species in Belarus in a technogenic environment]. Belaruskaja Navuka, Minsk (in Russian).

Shlyk, A. A. (1963). Issledovanie metabolizma hlorofilla v zelenom rastenii radioizotopnym metodom [Research of a chlorophyll metabolism in a green plant by a radioisotope method]. Akademija Nauk SSSR, Institut Biohimii Imeni A. N. Baha, Moscow (in Russian).

Shmatkov, H. H., & Minkov, Y. I. (2011). Otsinka zabrudnennia atmosfernoho povitria vykydamy pylu vid statsionarnykh dzherel promyslovykh pidpryiemstv, yaki roztashovani v m. Dnipropetrovsku [Assessment of atmospheric air pollution by dust from stationary sources of industrial enterprises located in Dnepropetrovsk]. Ekolohiia i Pryrodokorystuvannia, 14, 72–75 (in Ukrainian).

Shulman, M. V., Pakhomov, O. Y., & Brygadyrenko, V. V. (2017). Effect of lead and cadmium ions upon the pupariation and morphological changes in Calliphora vicina (Diptera, Calliphoridae). Folia Oecologica, 44(1), 28–37.

Sklyarenko, А. V., & Bessonova, V. P. (2018). Accumulation of sulfur and glutathione in leaves of woody plants growing under the conditions of outdoor air pollution by sulfur dioxide. Biosystems Diversity, 26(4), 334–338. http://doi.org/10.15421/011849

Smolikova, G. N., & Medvedev, S. S. (2015). Karotinoidy semjan, sintez, raznoobrazie i funkcii [Seed carotenoids, synthesis, diversity and function]. Fiziologija Rastenij, 62(1), 3–16 (in Russian).

Strilets, R. O. (ed.). (2019). Ekolohichnyi pasport Dnipropetrovskoi oblasti za 2018 rik [Environmental passport of Dnipropetrovsk region for 2018]. Dnipro (in Ukrainian).

Suvorova, G. G., Oskorbina, M. V., Kopytova, L. D., Yankova, L. S., & Popova, E. V. (2011). Sezonnye izmenenija fotosinteticheskoj aktivnosti i zelenyh pigmentov u sosny obyknovennoj i eli sibirskoj v optimume i ekstremal’nyh uslovijah uvlazhnenija [Seasonal changes in photosynthetic activity and green pigments in Scots pine and Siberian spruce under optimum and extreme conditions of moisture]. Sibirskij Jekologicheskij Zhurnal, 6, 851–859 (in Russian).

Tarabrin, V. P. (1980). Fiziologija ustojchivosti drevesnyh rastenij v uslovijah zagriaznenija okruzhajushhej sredy tiazhelymi metallami [The physiology of resistance of woody plants under environmental pollution by heavy metals]. In: Mikroelementy v Okruzhajushhej Srede. Naukova Dumka, Kiev. Pp. 17–19 (in Russian).

Tarchevskij, I. A. (2002). Signal’nye sistemy kletok rastenij [Signaling systems of plant cells]. Nauka, Moscow (in Russian).

Tuzhilkina, V. V., Bobkova, K. S., & Martynyuk, Z. P. (1998). Hlorofill’nyj indeks i i fotosinteticheskij stok ugleroda v hvojnye fitocenozy na evropejskom Severe Rossii [Chlorophyll index and photosynthetic carbon sink to coniferous phytocenoses in the European North of Russia]. Fiziologija Rastenij, 45(4), 594–600 (in Russian).

Tymko, S. M. (2016). Bioindikacionnoe znachenie koncentracii pigmentov v list’jah berezy povisloj v uslovijah gorodskoj sredy g. Barnaula [Bioindication value of the concentration of pigments in birch leaves hanging in the urban environment of Barnaul]. Trudy Molodyh Uchenyh Altajskogo Universitetaju, 13, 30–34 (in Russian).

Tyutereva, E. V., Dmitrieva, V. A., & Vojcehovskaya, O. V. (2017). Hlorofill b kak istochnik signalov, regulirujushhih razvitie i produktivnost’ rastenij [Chlorophyll b as a source of signals regulating the development and productivity of plants]. Sel’skohozjajstvennaja Biologija, 52(5), 843–455 (in Russian).

Vieira, J., Matos, P., Mexia, T., Silva, P., Lopes, N., Freitas, C., Correia, O., Santos-Reis, M., Branquinho, C., & Pinho, P. (2018). Green spaces are not all the same for the provision of air purification and climate regulation services: The case of urban parks. Environmental Research, 160, 306–313.

Wen, D., Kuang, Y., & Zhou, G. (2004). Sensitivity analyses of woody species exposed to air pollution based on ecophysiological measurements. Environmental Science And Pollution Research, 11(3), 165–170.

Yahia, M. W., Johansson, E., Thorsson, S., Lindberg, F., & Rasmussen, M. I. (2018). Effect of urban design on microclimate and thermal comfort outdoors in warm-humid Dar es Salaam. Tanzania. International Journal of Biometeorology, 62(3), 373–385.