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, Volume 26, Issue 2, pp 363–375 | Cite as

Anatomical responses of leaves of Black Locust (Robinia pseudoacacia L.) to urban pollutant gases and climatic factors

  • Farahnaz Rashidi
  • Adel Jalili
  • Sasan Babaie Kafaki
  • Khosro Sagheb-Talebi
  • John Hodgson
Original Paper

Abstract

This study investigates responses in the leaf anatomy of Black Locust (Robinia pseudoacacia L.) to the atmospheric pollutants, SO2, NO2 and O3 and climate in Tehran. The anatomical variables studied include thickness of the leaf lamina and of its main constituent tissues and the length and density of stomata. We present evidence that, in response to urban air pollution, the spongy mesophyll layer is thinner, the upper cuticle of the leaf thicker and stomatal density and the ratio of palisade parenchyma to spongy parenchyma are increased. Similar responses were also detected in relation to a climatic gradient. Stomatal density and thickness of the leaf lamina and of its mesophyll layer were all higher under warmer drier conditions. This overlap in anatomical response to two very different suites of environmental variables may reflect a functional overlap between mechanisms designed to restrict water loss in dry climates and those that minimize the uptake of toxic gases in polluted habitats.

Keywords

Leaf anatomy Climate Urban pollutant gases Black Locust, Tehran city 

Notes

Acknowledgments

The authors thank the Islamic Azad University Science and Research Branch for providing financial support for this project and Research Institute of Forest and Rangelands for technical support. Appreciation is extended to Ali Dargahi, who helped during the collection and analysis of samples, and to R. Azimi and F. Ghasemi for assistance in laboratory tests.

References

  1. Aasamaa K, Sober A, Rahi M (2001) Leaf anatomical characteristics associated with shoot hydraulic conductance, stomatal conductance and stomatal sensitivity to changes of leaf water status in temperate deciduous trees. Aust J Plant Physiol 28:765–774Google Scholar
  2. Abrams MD, Kubriske ME (1990) Leaf structure characteristics of 31 hardwood and conifer tree species in Central Wisconsin: influence of light regime and shade-tolerance rank. For Ecol Manag 31:245–253CrossRefGoogle Scholar
  3. Aguiar MO, Preisinger H (2000) Traits of leaf anatomy of Crotou lanjouwensis Jab. (Euphorbiaceae) in different strata of the plant. German-Brazilian workshop on Neotropical ecosystems of cooperative research, Hamburg, September 3–8Google Scholar
  4. Ahmad SH, Reshi Z, Ahmad J, Iqbal MZ (2005) Morpho-anatomical responses of Trigonella foenum graecum Linn. to induced cadmium and lead stress. J Plant Biol 48:64–84CrossRefGoogle Scholar
  5. Ali EA (1993) Damage to plants due to industrial pollution and their use as bioindicators in Egypt. Environ Pollut 81:251–255PubMedCrossRefGoogle Scholar
  6. Alves ES, Moura BB, Domingos M (2008) Structural analysis of Tillandsia usneoides L. exposed to air pollutants in São Paulo City–Brazil. Water Air Soil Pollut 189:61–68CrossRefGoogle Scholar
  7. Anonymous (1996) Air quality criteria for ozone and related photochemical oxidants. U.S. Environmental Protection Agency, Office of Research and Development. Research Triangle Park, North CarolinaGoogle Scholar
  8. Anyia AO, Herzogi H (2004) Water-use efficiency, leaf area and leaf gas exchange of cowpeas under mid-season drought. Eur J Agron 20:327–339CrossRefGoogle Scholar
  9. Bacelar EA, Correia CM, Mount inho-Pereira JM, Goncalves BC, Lopes JI, Torres-Per eira JMG (2003) Sclerophylly and leaf anatomical traits of five field grown olive cultivars growing under drought conditions. Tree Physiol 24:233–239CrossRefGoogle Scholar
  10. Barnes JD, Davison AW, Booth TA (1988) Ozone accelerates structural degradation of epicuticular wax on Norway spruce needles. New Phytol 110:309–318CrossRefGoogle Scholar
  11. Bengston C, Larsson S, Liljenberg C (1978) Effect of water stress on cuticular transpiration rate and amount and composition of epicuticular wax in seedlings of six oat varieties. Physiol Plant 44:319–324CrossRefGoogle Scholar
  12. Berry CR, Ripperton LA (1963) Ozone as possible cause of white pine emergence tipburn. J Phytopathol 53:552–557Google Scholar
  13. Bettarini I, Vaccari P, Miglietta F (1998) Elevated CO2 concentrations and stomatal density: observations from 17 plant species growing in a CO2 spring in central Italy. Glob Change Biol 4:17–22Google Scholar
  14. Bolea V, Chira D (2001) Resistance of chestnut (Castanea sativa Mill.) to SO2 in comparison with other tree species. For Snow Landsc Res 76:420–424Google Scholar
  15. Bondada BR, Oosterhuis DM, Murphy JB, Kim KS (1996) Effect of water stress on the epicuticular wax composition and ultrastructure of cotton (Gossypium hirsutum L.) leaf, bract, and boll. Environ Exp Bot 36:61–69CrossRefGoogle Scholar
  16. Bosabalidis AM, Kofidis G (2002) Comparative effects of drought stress on leaf anatomy of two olive cultivars. Plant Sci 163:375–379CrossRefGoogle Scholar
  17. Bussotti F, Ferretti M (2009) Visible injury, crown condition and growth responses of selected Italian forests in relation to ozone exposure. Environ Pollut 157:1427–1437PubMedCrossRefGoogle Scholar
  18. Calfapietra C, Fares S, Loreto F (2009) Volatile organic compounds from Italian vegetation and their interaction with ozone. Environ Pollut 157:1478–1486PubMedCrossRefGoogle Scholar
  19. Cameron KD, Teece MA, Smart LB (2006) Increased accumulation of cuticular wax and expression of lipid transfer protein in response to periodic drying events in leaves of tree tobacco. Plant Physiol 140:176–183PubMedCrossRefGoogle Scholar
  20. Chabot BF, Chabot JF (1977) Effects of light and temperature on leaf anatomy and photosynthesis in Fragaria vesca. Oecologia 26(4):363–377CrossRefGoogle Scholar
  21. Chartzoulakis K, Patakas A, Kofidis A, Bosabalidis A, Nastou A (2002) Water stress affects leaf anatomy, gas exchange, water relations and growth of two avocado cultivars. Sci Hortic 95:39–50CrossRefGoogle Scholar
  22. Dann MS, Pell EJ (1989) Decline of activity and quantity of ribu-lose isphosphate carboxylase/oxygenase and net photosynthesis in ozone-treated potato foliage. Plant Physiol 9:427–432CrossRefGoogle Scholar
  23. Dineva SB (2004) Comparative studies of the leaf morphology and structure of white ash Fraxinus americana L. and London plane tree Platanus acerifolia Willd growing in polluted area. Dendrobiology 52:3–8Google Scholar
  24. Ebel B, Rosenkranz J, Schiffgens A, Lütz C (1990) Cytological observation on spruce needles after prolonged treatment with ozone and acid mist. Environ Pollut 64:323–335PubMedCrossRefGoogle Scholar
  25. Elkiey T, Ormrod DP (1979) Physiological and morphological mechanisms of ozone and sulphur dioxide sensitivity in Petunia. Plant Physiol Suppl 63:150–161Google Scholar
  26. Evans LS, Ting IP (1974) Ozone sensitivity of leaves: relationship to leaf water content, gas transfer resistance and anatomical characteristics. Am J Bot 61:592–597CrossRefGoogle Scholar
  27. Evans LS, Albury K, Jennings N (1996) Relationships between anatomical characteristics and ozone sensitivity of leaves of several herbaceous dicotyledonous plant species at Great Smokey Mountains National Park. Environ Exp Bot 36:413–420CrossRefGoogle Scholar
  28. Fahn A (1990) Plant anatomy, 4th edn. Pergamon Press, Oxford, p 588Google Scholar
  29. Fahn A, Cutler DF (1992) Xerophytes. Encyclopedia of plant anatomy, 3rd edn. Gebrüder Borntraeger, BerlinGoogle Scholar
  30. Ferdinand JA, Fredericksen TS, Kouterick KB, Skelly JM (2000) Leaf morphology and ozone sensitivity of two open pollinated genotypes of black cherry (Prunus serotina) seedlings. Environ Pollut 108:297–302PubMedCrossRefGoogle Scholar
  31. Ferris R, Nijs I, Behaeghe T, Impens I (1996) Elevated CO2 and temperature have different effects on leaf anatomy of perennial ryegrass in spring and summer. Ann Bot 78:489–497CrossRefGoogle Scholar
  32. Gerosa G, Marzuolib R, Bussottic F, Pancrazic M, Dentid AB (2003) Ozone Sensitivity of Fagus sylvatica and Fraxinus excelsior young trees in relation to leaf structure and foliar ozone uptake. Environ Pollut 125:91–98PubMedCrossRefGoogle Scholar
  33. Ghorbanli M, Bakhshi khaniki G, Bakand Z (2008) Air pollution effects on fresh and dry weight, amount of proline, number of stomata, trichome and epidermal cells in Nerium oleander and Robinia pseudoacacia in Tehran city. Pajouhesh-va-Sazandegi 77:28–34 (in Farsi with English abstract)Google Scholar
  34. Gostin IN (2009) Air pollution effects on the leaf structure of some Fabaceae species. Not Bot Hort Agrobot Cluj 37:57–63Google Scholar
  35. Gratani L, Crescente MF, Petruzzi M (2000) Relationship between leaf life-span and photosynthetic activity of Quercus ilex in polluted urban areas (Rome). Environ Pollut 110:19–28PubMedCrossRefGoogle Scholar
  36. Gregoriou K, Pontikis K, Vemmos S (2007) Effects of reduced irradiance on leaf morphology, photosynthesis capacity, and fruit yield in olive (Olea europaea L.). Photosynthetica 45(2):172–181CrossRefGoogle Scholar
  37. Hao G-Y, Sack L, Wang A-Y, Cao K-F, Goldstein G (2010) Differentiation of leaf water flux and drought tolerance traits in hemiepiphytic and non-hemiepiphytic Ficus tree species. Funct Ecol 24(4):731–740CrossRefGoogle Scholar
  38. Haworth M, McElwain J (2008) Hot, dry, wet, cold or toxic? Revisiting the ecological significance of leaf and cuticular micromorphology. Palaeogeogr Palaeoclim palaeoecol 262:79–90CrossRefGoogle Scholar
  39. He XY, Fu SL, Chen W, Zhao TH, Xu S, Tuba Z (2007) Changes in effects of ozone exposure on growth, photosynthesis, and respiration of Ginkgo biloba in Shenyang urban area. Photosynthetica 45:555–561CrossRefGoogle Scholar
  40. Health RL (1994) Possible mechanisms for the inhibition of photosynthesis by ozone. Photosynth Res 39:439–451CrossRefGoogle Scholar
  41. Heath RL (1980) Initial events in injury to plants by air pollutants. Annu Rev Plant Physiol 31:395–431CrossRefGoogle Scholar
  42. Heber U, Kaiser W, Luwe M, Kindermann G, Veljovic-Javonovic S, Yin Z, Pfanz H, Slovik S (1995) Air pollution, photosynthesis and forest decline: interactions and consequences. In: Schulze ED, Caldwell MM (eds) Ecophysiology of photosynthesis. Springer, Berlin, pp 279–296Google Scholar
  43. Heggestad HE, Middleton JT (1959) Ozone in high concentrations as cause of tobacco leaf injury. Science 129:208–210PubMedCrossRefGoogle Scholar
  44. Hetherington AM, Woodward FI (2003) The role of stomata in sensing and driving environmental change. Nature 424:901–908PubMedCrossRefGoogle Scholar
  45. Huttunen S, Laine K (1983) Effects of air-borne pollutants on the surface wax structure of Pinus silvestris needles. Annu Bot fenn 20:79–86Google Scholar
  46. Ilkun GM (1971) Gazoustoichyvost’ rastenii. Kiev, p 240Google Scholar
  47. Ilkun GM (1978) Zagriazniteli atmosfery i rasteniya (Pollution of atmosphere and plants). Naukova dumka, Kiev, (in Russian) p 245Google Scholar
  48. Iqbal MZ (1985) Cuticular and anatomical studies of white clover leaves from clean and air-polluted areas. Pollut Res 4:59–61Google Scholar
  49. Jahan S, Iqbal MZ (1992) Morphological and anatomical studies of leaves of different plants affected by motor vehicles exhaust. Islam Acad Sci 5:21–23Google Scholar
  50. Kaji M, Yoneyama T, Tostuka T, Iwaki H (1980) Absorption of atmospheric transfer of the nitrogen through the plants. In: Studies on the effects of air pollutants on plants and mechanisms of phytotoxicity. Res Rep Nat Inst Environ Stud Jpn 11:51–58Google Scholar
  51. Kardel F, Wuyts K, Babanezhad M, Vitharana UWA, Wuytack T, Potters G, Samson R (2010) Assessing urban habitat quality based on specific leaf area and stomatal characteristics of Plantago lanceolata L. Environ Pollut 158:788–794PubMedCrossRefGoogle Scholar
  52. Kulagin Z (1968) Ogazousto chivosti drevesnykh rasteni kak ekologicheskaia problema. V sb.: Rasti-tel’nost’i promyshlennye zagriazneniai, Okhrana prirody na Urale, Vyp. 5, Svredlovsk, p 25Google Scholar
  53. Kulkarni M, Schneider B, Raveh E, Tel-Zur N (2010) Leaf anatomical characteristics and physiological responses to short-term drought in Ziziphus mauritiana (Lamk.). Sci Hortic 124:316–322CrossRefGoogle Scholar
  54. Kulshreshtha K, Srivastava K, Ahmad KJ (1994) Effect of automobile exhaust pollution on leaf surface structures of Calotropis procera L. and Nerium indicum L. Feddes Repert 105:185–189CrossRefGoogle Scholar
  55. Larcher W (2003) Physiological plant ecology: ecophysiology and stress physiology of functional groups, 4th edn. Springer, Berlin, pp 437–450Google Scholar
  56. Letchamo W, Gosselin A (1996) Transpiration, essential oil glands, epicuticular wax and morphology of Thymus vulgaris are influenced by light intensity and water supply. J Hortic Sci 71:123–134Google Scholar
  57. Luomala E-M, Laitinen K, Sutinen S, Kellomaki S, Vapaavuori E (2005) Stomatadensity, anatomy and nutrient concentrations of Scots pine needles are affected by elevated CO2 and temperature. Plant Cell Environ 28:733–749CrossRefGoogle Scholar
  58. Manninen S, Thiec D, Rose C, Nourrison G, Rad nai F, Garrec JP, Huttunen S (1999) Pigment concentrations and ratios of Aleppo pine seedlings exposed to ozone. Water Air Soil Pollut 116:333–338CrossRefGoogle Scholar
  59. Mayo JM, Legge AH, Yeung EC, Krupa SV, Bogner JC (1992) The effects of sulphur gas and elemental sulphur dust deposition on Pinus contorta × Pinus banksiana: cell walls and water relations. Environ Pollut 76:43–50PubMedCrossRefGoogle Scholar
  60. Medri ME, Lieras E (1979) Ecofisiologia de plantas da Amozonia. 2- Anatomia foliar e ecofisiologia de Bertollethia excelsa Humb. & Bonpl. (Castanha-do-Para)- Lecythidaceae. Acta Amaz 9(1):15–23Google Scholar
  61. Mirhaji T, Jalili A, Jafari M, Akbarzadeh M, Farzaneh Z (2001) Ecological Comparision of Artemisia species in Semnan province. Pajouhesh-va-Sazandegi 52:95–102 (in Farsi with English abstract)Google Scholar
  62. Muller O, Oguchi R, Hirose T, Werger MJA, Hikosake K (2009) The leaf anatomy of a broad-laved evergreen allows an increase in leaf nitrogen content in winter. Physiol Plant 136:299–309PubMedCrossRefGoogle Scholar
  63. Nikolaevski VS (1963) O pokazateliakh gazousto chivosti drevesnykh rasteni. INTA Biologii UFAN, Vyp. 31, Svredlovsk, p 74Google Scholar
  64. Ninova D (1970) Izsledvaniia vurkhu anatomichnite pokazateli za dimoustoichivost pri niakoi du rves-ni rasteniia. Gorskostopanska nauka, p 7Google Scholar
  65. O’Toole JC, Cruz RT (1983) Genotypic variation in epicuticular wax of rice. Crop Sci 23:392–400CrossRefGoogle Scholar
  66. O’Toole JC, Cruz RT, Seiber JN (1979) Epicuticular wax and cuticular resistance in rice. Physiol Plant 47:239–241CrossRefGoogle Scholar
  67. Poorkhabbaz A (2007) The influence of air pollution on Plane (Platanus orientalis L.). Cuvillier Verlag, p 110Google Scholar
  68. Reich PB (1987) Quantifying plant response to ozone: a unifying theory. Tree Physiol 3(1):63–92PubMedGoogle Scholar
  69. Reig-Armiñana J, Calatayud V, Cervero′ J, Garcia-Breijo FJ, Ibars A, Sanz MJ (2004) Effects of ozone on the foliar histology of the mastic plant (Pistacia lentiscus L.). Environ Pollut 132:321–331PubMedCrossRefGoogle Scholar
  70. Reiling K, Davison AW (2006) Effects of ozone on stomatal conductance and photosynthesis in populations of Plantago major L. New Phytol 129:587–594CrossRefGoogle Scholar
  71. Richards BL, Middleton JT, Hewitt WB (1958) Air pollution with relation to agronomic crops: V. oxidant stipple of grape. Agron j 50:559–561CrossRefGoogle Scholar
  72. Sabeti H (1987) Botany, general anatomy of plants. Tehran university press, Tehran, p 492Google Scholar
  73. Samdur MY, Manivel P, Jain VK, Chikani BM, Gor HK, Desai S (2003) Genotypic differences and water-deficit induced enhancement in epicuticular wax load in peanut. Crop Sci 43:1294–1299CrossRefGoogle Scholar
  74. Sharma GK, Butler J (1975) Environmental pollution: leaf cuticular patterns in Trifolium pratense L. Ann Bot 39:1087–1090Google Scholar
  75. Shields LM (1950) Leaf xeromorphy as related to physiological and structural influents. Bot Rev 16:399–447CrossRefGoogle Scholar
  76. Silva LC, Azevedo AA, Silva EAM, Oliva MA (2005) Effects of simulated acid rain on the growth and anatomy of five Brazilian tree species. Aust J Bot 53:789–796CrossRefGoogle Scholar
  77. Soikkeli S (1981) Comparison of cytological injuries in conifer needles from several polluted industrial environments in inland. Ann Bot Fenni 18:47–61Google Scholar
  78. Treshow M, Anderson FK (1989) Effects of sulphur dioxide and heavy metals. In: Treshow M, Anderson FK (eds) Plant stress from air pollution. John Wiley, Chichester, pp 44–60Google Scholar
  79. Tripathi A, Tripathi DS, Prakash V (1999) Phytomonitoring and NOx pollution around silver refineries. Environ Int 25:403–410CrossRefGoogle Scholar
  80. Uddin MN, Marshall DR (1988) Variation in epicuticular wax content in wheat. Euphytica 38:3–9CrossRefGoogle Scholar
  81. Verma RB, Mahmooduzzafar TOS, Iqbal M (2006) Foliar response of Ipomea pestigridis L. to coal-smoke pollution. Turk J Bot 30:413–417Google Scholar
  82. Volenikova M, Ticha I (2001) Insertion profiles in stomatal density and sizes in Nicotiana tabacum L. plantlets. Biol Plant 44(2):161–165CrossRefGoogle Scholar
  83. Winner WE, Mooney HA, Goldstein RA (1985) Sulphur dioxide and vegetation: physiology, ecology and policy issues. Stanford University press, Stanford, p 593Google Scholar
  84. Winner WE, Lefohn AS, Cotter IS, Greitner CS, Nellessen J, McEvoy LR, Olson RL, Atkinson CJ, Moore LD (1989) Plant responses to elevational gradients of ozone exposures in Virginia. Proc Natl Acad Sci 86:8828–8832PubMedCrossRefGoogle Scholar
  85. Zhang JY, Broeckling CD, Blanca EB, Sledge MK, Summer LW, Wang ZY (2005) Overexpression of WXP1, a putative Medicago truncatula AP2 domain-containing transcription factor gene, increases cuticular wax accumulation and enhances drought tolerance in transgenic alfalfa (Medicago sativa). Plant J 42:689–707PubMedCrossRefGoogle Scholar
  86. Zobel A, Nighswander JE (1991) Accumulation of phenolic compounds in the necrotic areas of Austria and red pine needles after spraying with sulphuric acid: a possible bioindicator of air pollution. N Phytol 117:565–574CrossRefGoogle Scholar
  87. Zouzoulas D, Koutroubas SD, Vassilioua G, Vardavakis E (2009) Effects of ozone fumigation on cotton (Gossypium hirsutum L.) morphology, anatomy, physiology, yield and qualitative characteristics of fibers. Environ Exp Bot 67:293–303CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • Farahnaz Rashidi
    • 1
  • Adel Jalili
    • 2
  • Sasan Babaie Kafaki
    • 1
  • Khosro Sagheb-Talebi
    • 2
  • John Hodgson
    • 3
  1. 1.Department of Forestry, Science and Research BranchIslamic Azad UniversityTehranIran
  2. 2.Research Institute of Forest and RangelandsTehranIran
  3. 3.Department of ArchaeologyThe University of SheffieldSheffieldUK

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