Abstract
Periderm of the leaves of two Agathis species was studied. Agathis leaves are long-lived and remain alive for more than 25 years. Periderm occurs regularly and can be initiated in the epidermis, mesophyll, phloem parenchyma of the leaf veins and in the ground tissue of the petiole. Periderm lies on the surface, is located in the mesophyll or splits it. Periderm structure is either typical, consisting of phellogen, multilayered phellem and phelloderm or disordered. Agathis leaves are able to form true wound periderm, which has been shown experimentally. We believe that at least some of the factors inducing periderm initiation are identical both in leaves and in stems. Mechanical tension in the tissues and cell deformation plays an essential role in the periderm initiation. Leaf tissues isolated due to the suberinization process may function as a storage site for the substances not involved in the plant metabolism or excluded from it. Periderm gives an opportunity to keep such substances away from functional tissues, which is important for evergreen plants with long-lived leaves.
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References
Achor DS, Albrigo LG, McCoy CW (1991) Developmental anatomy of lesions on ‘Sunburst’ mandarin leaves initiated by citrus rust mite feeding. J Am Soc Hortic Sci 116:663–668
Albrigo LG, McCoy CW (1974) Characteristic injury by citrus rust mite to orange leaves and fruit. Proc Fla State Hortic Soc 87:48–55
Arbicheva AI, Pautov AA, Voitsekhovskaya OV (2012) Age-related changes of photosynthesis rate and assimilates export in Agathis brownii Lem. (Araucariaceae) perennial leaves. Vestnik St. Petersb Univ Ser 3 Biol 4:20–26
Arduin M, Kraus JE (1995) Anatomia e ontogenia de galhas foliares de Piptadenia gonoacantha (Fabales, Mimosaceae). Bol Bot Univ São Paulo 14:109–130. https://doi.org/10.11606/issn.2316-9052.v14i0p109-130
Ash J (1985) Growth rings and longevity of Agathis vitiensis (Seemann) Benth. & Hook. f. ex Drake in Fiji. Aust J Bot 33:81–88. https://doi.org/10.1071/BT9850081
Baas P (1975) Vegetative anatomy and the affinities of Aquifoliaceae, Sphenostemon, Phelline, and Oncotheca. Blumea 22:311–407
Balge RJ, Struckmeyer BE, Beck GE (1969) Occurrence, severity and nature of oedema in Pelargonium hortorum Ait. J Am Soc Hortic Sci 94:181–183
Biggs AR, Stobbs LW (1986) Fine structure of the suberized cell walls in the boundary zone and necrophylactic periderm in wounded peach bark. Can J Bot 64:1606–1610
Brundrett MC, Kendrick B, Peterson CA (1991) Efficient lipid staining in plant material with Sudan Red 7B or Fluorol Yellow 088 in polyethylene glycol-glycerol. Biotech Histochem 66:111–116
Cambie RC, Coddington JM, Stone MJ, Tanaka N, Li YH, Arigayo S (1989) Diterpenoids of the wood of Agathis vitiensis. Phytochemistry 28:1675–1679. https://doi.org/10.1016/S0031-9422(00)97823-3
Carlquist S (1962) Ontogeny and comparative anatomy of thorns of Hawaiian Lobeliaceae. Am J Bot 49:413–419. https://doi.org/10.2307/2439083
Chin S-W, Lutz SM, Wen J, Potter D (2013) The bitter and the sweet: inference of homology and evolution of leaf glands in Prunus (Rosaceae) through anatomy, micromorphology, and ancestral-character state reconstruction. Int J Plant Sci 174:27–46. https://doi.org/10.1086/668219
Chitanava GU (1975) Anatomical structure of leaves and lentils on them in three species of Eucalyptus (Myrtaceae). Bot Zh SSSR 60:535–541
Craver JK (2014) The effects of UVB radiation on intumescence development and the characterization of lesions from physiological disorders on ornamental sweet potato (Ipomoea batatas), tomato (Solanum lycopersicum), and interspecific geranium (Pelargonium spp.). In: Department of Horticulture, Forestry and Recreation Resources, College of Agriculture. Kansas State University, Manhattan, p 99
Dallimore W, Jackson AB (1966) A handbook of the Coniferae and Ginkgoaceae, 4th edn. Edward Arnold, London
Elliott JH (1937) The development of the vascular system in evergreen leaves more than one year old. Ann Bot (n.s.) 1:107–127. https://doi.org/10.1093/oxfordjournals.aob.a083450
Evans LS, Bromberg A (2010) Characterization of cork warts and aerenchyma in leaves of Rhizophora mangle and Rhizophora racemosa. J Torrey Bot Soc 137:30–38. https://doi.org/10.3159/09-ra-024.1
Evans LS, Okawa Y, Searcy DG (2005) Anatomy and morphology of red mangrove (Rhizophora mangle) plants in relation to internal airflow. J Torrey Bot Soc 132:537–550. https://doi.org/10.3159/1095-5674(2005)132[537:AAMORM]2.0.CO;2
Evans LS, Leon MFd, Sai E (2008) Anatomy and morphology of Rhizophora stylosa in relation to internal airflow and Attim’s plant architecture. J Torrey Bot Soc 135:114–125. https://doi.org/10.3159/07-RA-027R.1
Evans LS, Testo ZM, Cerutti JA (2009) Characterization of internal airflow within tissues of mangrove species from Australia: leaf pressurization processes. J Torrey Bot Soc 136:70–83. https://doi.org/10.3159/08-RA-078R1.1
Evert RF, Eichhorn SE (2006) Esau’s plant anatomy: meristems, cells, and tissues of the plant body: their structure, function, and development, 3rd edn. Wiley-Interscience, Hoboken
Fahn A (1982) Plant anatomy, 3rd edn. Pergamon Press, Oxford
Farooqui P (1982) Cork-warts in Eucalyptus species. Proc Indian Acad Sci (Plant Sci) 91:289–295. https://doi.org/10.1007/BF03053354
Foster AS (1928) Salient features of the problem of bud-scale morphology. Biol Rev 3:123–164. https://doi.org/10.1111/j.1469-185X.1928.tb00853.x
Gardner RO (1975) Vanillin-hydrochloric acid as a histochemical test for tannin. Stain Technol 50:315–317. https://doi.org/10.3109/10520297509117081
Guimarães AR, Andreata RHP, Costa CG (2011) Stem and leaf morphoanatomy of two atlantic forest species of Smilax Linnaeus. Rev de Biol Neotropical 8:1–14. https://doi.org/10.5216/rbn.v8i1.13680
Hamada FA, Hamed AI, Sheded MG, Shaheen ASM (2010) Macro, micro-morphological and bioactivity aspects of naturalized exotic Solanum diphyllum L. Al-Azhar Bull Sci 21:175–206
Ibrahim L, Spackman VMT, Cobb AH (2001) An investigation of wound healing in sugar beet roots using light and fluorescence microscopy. Ann Bot 88:313–320. https://doi.org/10.1006/anbo.2001.1461
Joffily A, Cardoso Vieira R (2010) Cork-warts on the leaf epidermis of four genera of Celastroidea-Celastraceae. Flora 205:313–318. https://doi.org/10.1016/j.flora.2009.12.014
Korn RW, Fredrick GW (1973) Development of d-type stomata in the leaves of Ilex crenata var. convexa. Ann Bot 37:647–656. https://doi.org/10.1093/oxfordjournals.aob.a084731
Kraus JE, Arduin M, Venturelli M (2002) Anatomy and ontogenesis of hymenopteran leaf galls of Struthanthus vulgaris Mart. (Loranthaceae). Rev Braz Bot 25:449–458. https://doi.org/10.1590/S0100-84042002012000009
Krishnan HB, Franceschi VR (1988) Anatomy of some leaf galls of Rosa woodsii (Rosaceae). Am J Bot 75:369–376. https://doi.org/10.2307/2443984
Libbert E (1973) Lehrbuch der Pflanzenphysiologie. Gustav Fischer, Jena
Lipchinsky A (2015) Morphomechanics of Plants. In: Beloussov LV (ed) Morphomechanics of development. Springer, Cham, pp 157–190. https://doi.org/10.1007/978-3-319-13990-6_5
Mabberley DJ (2002) The Agathis brownii case (Araucariaceae). Telopea 9:743–754. https://doi.org/10.7751/telopea20024012
Metcalfe CR, Chalk L (1950) Anatomy of the dicotyledons. Clarendon Press, Oxford
Meyen SV (1987) Fundamentals of palaeobotany. Chapman and Hall, New York
Mirabet V, Das P, Boudaoud A, Hamant O (2011) The role of mechanical forces in plant morphogenesis. Annu Rev Plant Biol 62:365–385. https://doi.org/10.1146/annurev-arplant-042110-103852
Morris LL, Mann LK (1955) Wound healing, keeping quality, and compositional changes during curing and storage of sweet potatoes. Hilgardia 24:142–183. https://doi.org/10.3733/hilg.v24n07p143
Morrow RC, Wheeler RM (1997) Plant physiological disorders. In: Langhans RW, Tibbitts TW (eds) Plant growth chamber handbook. Iowa State University of Science and Technology, Ames, pp 133–141
Nautiyal DD, Singh S, Pant DD (1976) Epidermal structure and ontogeny of stomata in Gnetum gnemon, G. montanum and G. ula. Phytomorphology 26:282–296
Neish PG, Drinnan AN, Ladiges PY (1995) Anatomy of leaf-margin lenticels in Eucalyptus denticulata and three other eucalypts. Aust J Bot 43:211–221. https://doi.org/10.1071/BT9950211
Oladele FA, Fawole MO, Bhat RB (1985) Leaf anatomy of Parkia clappertoniana Keay. (Mimosaceae). Korean J Bot 28:21–28
Pagoda IO, Pautov AA, Zelenskaya MS, Vlasov DY (2015) Cork warts on leaves of Gnetum L. (Gnetaceae) and its phylloplane fungi. Int J Bot 11:10–20. https://doi.org/10.3923/ijb.2015.10.20
Pinkard E, Gill W, Mohammed C (2006) Physiology and anatomy of lenticel-like structures on leaves of Eucalyptus nitens and Eucalyptus globulus seedlings. Tree Physiol 26:989–999. https://doi.org/10.1093/treephys/26.8.989
Reynolds ES (1963) The use of lead citrate at high PH as an electron-opaque stain in electron microscopy. J Cell Biol 17:208–212. https://doi.org/10.1083/jcb.17.1.208
Robinson S, Burian A, Couturier E, Landrein B, Louveaux M, Neumann ED, Peaucelle A, Weber A, Nakayama N (2013) Mechanical control of morphogenesis at the shoot apex. J Exp Bot 64:4729–4744. https://doi.org/10.1093/jxb/ert199
Salema R (1967) On the occurrence of periderm in the leaves of Welwitschia mirabilis. Can J Bot 45:1469–1471. https://doi.org/10.1139/b67-150
Sampathkumar A, Yan A, Krupinski P, Meyerowitz EM (2014) Physical forces regulate plant development and morphogenesis. Curr Biol 24:R475–R483. https://doi.org/10.1016/j.cub.2014.03.014
Santos LDT, Thadeo M, Iarema L, Meira RMSA, Ferreira FA (2008) Foliar anatomy and histochemistry in seven species of Eucalyptus. Rev Árvore 32:769–779. https://doi.org/10.1590/S0100-67622008000400019
Sinnott EW (1960) Plant morphogenesis. McGraw-Hill Book Co., New York
Stace CA (1965) Cuticle studies as an aid to plant taxonomy. Bull Br Mus (Nat Hist) Bot 4:1–78
Stace CA (1966) The use of epidermal characters in phylogenetic considerations. New Phytol 65:304–318. https://doi.org/10.1111/j.1469-8137.1966.tb06366.x
Strucktneyer BE, Riker AJ (1951) Wound periderm formation in white-pine trees resistant to blister rust. Phytopathology 41:276–281
WCSP (2017) World Checklist of Selected Plant Families. Facilitated by the Royal Botanic Gardens, Kew. http://apps.kew.org/wcsp/namedetail.do?name_id=4510. Accessed 2 Feb 2017
Whitmore TC (1980) A monograph of Agathis. Plant Syst Evol 135:41–69. https://doi.org/10.1007/BF00983006
Acknowledgements
This study was supported by the Russian Foundation for Basic Research (Grant 17-04-01213A to AAP). The study was carried out using laboratory facilities of the Research Resource Center for molecular and cell technologies and Resource Center ‘Chromas’ of St Petersburg State University Research park, as well as the Center for Collective Use ‘Cellular and Molecular Methods for Studying Plants and Fungi’ at the Komarov Botanical Institute of the Russian Academy of Sciences. We thank Irina Korshunova, curator of the Komarov Botanical Gardens for providing plant material of the studied species.
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Arbicheva, A.I., Pautov, A.A. Leaf periderm supports longevity and functionality of crown leaves in Agathis species (Araucariaceae). Braz. J. Bot 41, 155–165 (2018). https://doi.org/10.1007/s40415-017-0429-5
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DOI: https://doi.org/10.1007/s40415-017-0429-5