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Stomata Polymorphism in Leaves of Apple Trees (Malus domestica Borkh.) Growing under Mountain and Plain Conditions

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Abstract

Stomata polymorphism in leaves of apple trees (Malus domestica) growing under mountain and plain conditions has been studied using scanning electron microscopy. The leaves of this species were hypostomatic with anomocytic stomata and radially diverging cuticular folds combined into bundles (cuticular bundles), the number of which usually corresponded to the number of epidermal cells surrounding the stomata. The average size of stomata increased linearly as the number of cuticular bundles increased. Under favorable conditions (600-m altitude above sea level), a high density of rounded stomata was observed. Stress conditions, such as high temperatures and droughts on the plain (300-m altitude) or high insolation and temperature drops in the mountains (1200-m altitude), provided the same effect on the micromorphology of the leaf surface, while the effect of altitude was manifested in the reduction of the size of epidermal cells.

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REFERENCES

  1. Blanke, M.M., Höfer, M., and Pring, R.J., Stomata and structure of tetraploid apple leaves cultured in vitro, Ann. Bot., 1994, vol. 73, pp. 651–654.

    Article  Google Scholar 

  2. Chkhubianishvili, E.I., Chanishvili, Sh.Sh., Kacharava, N.F., and Badridze, G.Sh., Structural and functional features of the leaves of meadow plants in the high mountains of the Lesser Caucasus, Fiziol. Biokhim. Kult. Rast., 2009, vol. 41, no. 2, pp. 132–139.

    Google Scholar 

  3. Elias, P., Stomata density and size of apple trees growing in irrigated and non irrigated conditions, Biol. Bratislava, 1995, vol. 50, pp. 115–118.

    Google Scholar 

  4. Franks, P.J. and Beerling, D.J., Maximum leaf conductance driven by CO2 effects on stomatal size and density over geologic time, Proc. Nat. Acad. Sci. U. S. A., 2009, vol. 106, pp. 10343–10347.

    Article  CAS  Google Scholar 

  5. Franks, P.J. and Farquhar, G.D., The mechanical diversity of stomata and its significance in gas-exchange control, Plant Physiol., 2007, vol. 143, pp. 78–87.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Franks, P.J., Franks, P.J., Drake, P.L., and Beerling, D.J., Plasticity in maximum stomatal conductance constrained by negative correlation between stomatal size and density: an analysis using Eucalyptus globulus,Plant, Cell Environ., 2009, vol. 32, pp. 1737–1748.

    Article  Google Scholar 

  7. Frohnmeyer, H. and Staiger, D., Ultraviolet-B radiation-mediated responses in plants. Balancing damage and protection, Plant Physiol., 2003, vol. 133, pp. 1420–1428.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Ganeva, T. and Uzunova, K., Comparative leaf epidermis study in species of genus Malus Mill. (Rosaceae), Bot. Serbica, 2010, vol. 34, pp. 45–49.

    Google Scholar 

  9. Giday, H., Kjaeк, K.H., Fanourakis, D., and Ottosen, C.O., Smaller stomata require less severe leaf drying to close: a case study in Rosa hydrida,J. Plant Physiol., 2013, vol. 170, pp. 1309–1316.

    Article  CAS  PubMed  Google Scholar 

  10. Gou, X., Gou, X., Chen, F., Yang, M., Li, J., Peng, J., and Jin, L., Climatic response of thick leaf spruce (Picea crassifolia) tree-ring width at different elevations over Qilian Mountains, northwestern China, J. Arid Environ., 2005, vol. 61, pp. 513–524.

    Article  Google Scholar 

  11. Hetherington, A.M. and Woodward, F.I., The role of stomata in sensing and driving environmental change, Nature, 2003, vol. 424, pp. 901–908.

    Article  CAS  PubMed  Google Scholar 

  12. Kessler, M., Siorak, Y., Wunderlich, M., and Wegner, C., Patterns of morphological leaf traits among pteridophytes along humidity and temperature gradients in the Bolivian Andes, Funct. Plant Biol., 2007, vol. 34, pp. 963–971.

    Article  PubMed  Google Scholar 

  13. Kofidis, G., Bosabalidis, A.M., and Moustakas, M., Contemporary seasonal and altitudinal variations of leaf structural features in oregano (Origanum vulgare L.), Ann. Bot., 2003, vol. 92, pp. 635–645.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Körner, C., Bannister, P., and Mark, A.F., Altitudinal variation in stomatal conductance, nitrogen content and leaf anatomy in different plant life forms in New Zealand, Oecologia, 1986, vol. 69, pp. 577–588.

    Article  PubMed  Google Scholar 

  15. Kouwenberg, L., Kürschner, W.M., and McElwain, J.C., Stomatal frequency change over altitudinal gradients: prospects for paleoaltimetry, Rev. Mineral. Geochem., 2007, vol. 66, pp. 215–241.

    Article  CAS  Google Scholar 

  16. Ma, Z.S., Jia, Y.Y., Wang, Y.H., and Xuan, L.F., Observation of leaf stomata shapes and distribution of large and small stomatas of peach (Prunus persica L.)[J], J. Agricult. Univ. Hebei, 2008, vol. 6, p. 018.

  17. Miroslavov, E.A., Structural adaptations of plants to cold climate, Bot. Zh., 1994, vol. 79, no. 2, pp. 20–26.

    Google Scholar 

  18. Miroslavov, E.A. and Kravkina, E.M., Comparative anatomy of the leaf of plants growing in mountains at different elevations, Bot. Zh., 1990, vol. 75, no. 3, pp. 368–375.

    Google Scholar 

  19. Mizutani, M. and Kanaoka, M.M., Environmental sensing and morphological plasticity in plants, in Seminars in Cell and Developmental Biology, New York: Academic, 2017, vol. 83, pp. 69–77.

    Google Scholar 

  20. Motyleva, S.M. and Kuznetsov, M.N., Micromorphology of leaves of triploid apple varieties immune to scab, Sovrem. Sadovodstvo, 2010, no. 1, pp. 72–78.

  21. Nawkar, G.M., Maibam, P., Park, J.H., Sahi, V.P., Lee, S.Y., and Kang, C.H., UV-induced cell death in plants, Int. J. Mol. Sci., 2013, vol. 14, pp. 1608–1628.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Pautov, A.A., Zakonomernosti filomorfogeneza vegetativnykh organov rastenii (Patterns of Phylomorphogenesis of Vegetative Organs of Plants), St. Petersburg: St.-Peterb. Gos. Univ., 2009a.

  23. Pautov, A.A., The role of morphogenetic correlations in the occurrence of heterostomatity, Bot. Zh., 2009b, vol. 94, no. 6, pp. 785–792.

    Google Scholar 

  24. Pautov, A.A., Location of microrelief folds on the side cells of stomata of Hydrangea macrophylla (Thunb.) Ser. (Hydrangeaceae), Vestn. S.-Peterb. Gos. Univ., Ser. 3: Biol., 2011, no. 2, pp. 39–44.

  25. Pautov, A.A., Sapach, Yu.O., Ivanova, O.V., and Krylova, E.G., Microrelief of the surface of leaves of flowering plants: stomatal rings and protrusions, Bot. Zh., 2014, vol. 99, no. 6, pp. 625–640.

    Article  Google Scholar 

  26. Pautov, A.A., Vasil’eva, V.A., and Krylova, E.G., Stomata polymophism in the epidermis of the leaf of Exbucklandia populnea (Hamamelidaceae) and its possible significance, Bot. Zh., 2015, vol. 100, no. 6, pp. 540–549.

    Article  Google Scholar 

  27. Royer, D.L., Stomatal density and stomatal index as indicators of paleoatmospheric CO2 concentration, Rev. Palaeobot. Palynol., 2001, vol. 114, pp. 1–28.

    Article  PubMed  Google Scholar 

  28. Šantrůček, J., Vráblová, M., Šimková, M., Hronková, M., Drtinová, M., Květoň, J., and Neuwithová, J., Stomatal and pavement cell density linked to leaf internal CO2 concentration, Ann. Bot., 2014, vol. 114, pp. 191–202.

    Article  PubMed  PubMed Central  Google Scholar 

  29. Seber, J., Lineinyi regressionnyi analiz (Linear Regression Analysis), Moscow: Mir, 1980.

  30. Shidakov, R.S., Sortiment yabloni i sovershenstvovanie ego putem selektsii v predgor’yakh Severnogo Kavkaza (Assortment of Apple Trees and Its Improvement by Selection in the Foothills of the North Caucasus), Nal’chik: El’brus, 1991.

  31. Shidakov, R.S. and Shidakova, A.S., Economic assessment of apple varieties and elites in agrolandscapes in different ecological zones of the North Caucasus, Usp. Sovrem. Estestvoznan., 2006, no. 11, pp. 12–15.

  32. Stenström, A., Jónsdóttir, I.S., and Augner, M., Genetic and environmental effects on morphology in clonal sedges in the Eurasian Arctic, Am. J. Bot., 2002, vol. 89, pp. 1410–1421.

    Article  PubMed  Google Scholar 

  33. Suntsova, L.N. and Inshakov, E.M., Woody plants under conditions of technogenic environment of Krasnoyarsk, Khvoinye Boreal.Zony, 2007, vol. 24, no. 1, pp. 95–99.

    Google Scholar 

  34. Suslov, F.P., Gippenreiter, E.B., and Kholodov, Zh.K., Sportivnaya trenirovka v usloviyakh srednegor’ya (Sports Training in the Midlands), Moscow: RGAFK, 1999.

  35. Vasilevskaya, V.K., Formirovanie lista zasukhoustoichivykh rastenii (Formation of the Leaf of Draught-Tolerant Plants), Ashkhabad: Akad. Nauk Turkmen. SSR, 1954.

  36. Warabieda, W., Olszak, R.W., and Dyki, B., Morphological and anatomical characters of apple leaves associated with cultivar susceptibility to spider mite infestation, Acta Agrobot., 1997, vol. 50, pp. 53–64.

    Article  Google Scholar 

  37. Wild, A. and Wolf, G., The effect of different light intensities on the frequency and size of stomata, the size of cells, the number, size and chlorophyll content of chloroplasts in the mesophyll and the guard cells during the ontogeny of primary leaves of Sinapis alba,Z. Pflanzenphysiol., 1980, vol. 97, pp. 325–342.

    Article  CAS  Google Scholar 

  38. Yang, X., Yang, Y., Ji, C., Feng, T., Shi, Y., Lin, L., and He, J.S., Large-scale patterns of stomatal traits in Tibetan and Mongolian grassland species, Basic Appl. Ecol., 2014, vol. 15, pp. 122–132.

    Article  Google Scholar 

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Correspondence to A. V. Babosha.

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The authors declare that they have no conflict of interest. This article does not contain any studies involving animals or human participants performed by any of the authors.

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Babosha, A.V., Kumachova, T.K., Ryabchenko, A.S. et al. Stomata Polymorphism in Leaves of Apple Trees (Malus domestica Borkh.) Growing under Mountain and Plain Conditions. Biol Bull Russ Acad Sci 47, 352–363 (2020). https://doi.org/10.1134/S1062359020040032

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  • DOI: https://doi.org/10.1134/S1062359020040032

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