Leaf periderm supports longevity and functionality of crown leaves in Agathis species (Araucariaceae)

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

  1. 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

    Google Scholar 

  2. Albrigo LG, McCoy CW (1974) Characteristic injury by citrus rust mite to orange leaves and fruit. Proc Fla State Hortic Soc 87:48–55

    Google Scholar 

  3. 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

    Google Scholar 

  4. 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

    Google Scholar 

  5. 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

    Article  Google Scholar 

  6. Baas P (1975) Vegetative anatomy and the affinities of Aquifoliaceae, Sphenostemon, Phelline, and Oncotheca. Blumea 22:311–407

    Google Scholar 

  7. 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

    Google Scholar 

  8. 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

    Article  Google Scholar 

  9. 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

    CAS  Article  PubMed  Google Scholar 

  10. 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

    CAS  Article  Google Scholar 

  11. Carlquist S (1962) Ontogeny and comparative anatomy of thorns of Hawaiian Lobeliaceae. Am J Bot 49:413–419. https://doi.org/10.2307/2439083

    Article  Google Scholar 

  12. 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

    Article  Google Scholar 

  13. Chitanava GU (1975) Anatomical structure of leaves and lentils on them in three species of Eucalyptus (Myrtaceae). Bot Zh SSSR 60:535–541

    Google Scholar 

  14. 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

  15. Dallimore W, Jackson AB (1966) A handbook of the Coniferae and Ginkgoaceae, 4th edn. Edward Arnold, London

    Google Scholar 

  16. 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

    Article  Google Scholar 

  17. 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

    Article  Google Scholar 

  18. 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

    Article  Google Scholar 

  19. 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

    Article  Google Scholar 

  20. 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

    Article  Google Scholar 

  21. 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

    Book  Google Scholar 

  22. Fahn A (1982) Plant anatomy, 3rd edn. Pergamon Press, Oxford

    Google Scholar 

  23. Farooqui P (1982) Cork-warts in Eucalyptus species. Proc Indian Acad Sci (Plant Sci) 91:289–295. https://doi.org/10.1007/BF03053354

    Google Scholar 

  24. 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

    Article  Google Scholar 

  25. Gardner RO (1975) Vanillin-hydrochloric acid as a histochemical test for tannin. Stain Technol 50:315–317. https://doi.org/10.3109/10520297509117081

    CAS  Article  PubMed  Google Scholar 

  26. 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

    Google Scholar 

  27. 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

    Google Scholar 

  28. 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

    Article  Google Scholar 

  29. 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

    Article  Google Scholar 

  30. 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

    Article  Google Scholar 

  31. 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

    Article  Google Scholar 

  32. 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

    Article  Google Scholar 

  33. Libbert E (1973) Lehrbuch der Pflanzenphysiologie. Gustav Fischer, Jena

    Google Scholar 

  34. 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

    Google Scholar 

  35. Mabberley DJ (2002) The Agathis brownii case (Araucariaceae). Telopea 9:743–754. https://doi.org/10.7751/telopea20024012

    Article  Google Scholar 

  36. Metcalfe CR, Chalk L (1950) Anatomy of the dicotyledons. Clarendon Press, Oxford

    Google Scholar 

  37. Meyen SV (1987) Fundamentals of palaeobotany. Chapman and Hall, New York

    Book  Google Scholar 

  38. 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

    CAS  Article  PubMed  Google Scholar 

  39. 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

    Article  Google Scholar 

  40. 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

    Google Scholar 

  41. 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

    Google Scholar 

  42. 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

    Article  Google Scholar 

  43. Oladele FA, Fawole MO, Bhat RB (1985) Leaf anatomy of Parkia clappertoniana Keay. (Mimosaceae). Korean J Bot 28:21–28

    Google Scholar 

  44. 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

    Article  Google Scholar 

  45. 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

    CAS  Article  PubMed  Google Scholar 

  46. 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

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  47. 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

    CAS  Article  PubMed  Google Scholar 

  48. 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

    Article  Google Scholar 

  49. 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

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  50. 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

    Article  Google Scholar 

  51. Sinnott EW (1960) Plant morphogenesis. McGraw-Hill Book Co., New York

    Book  Google Scholar 

  52. Stace CA (1965) Cuticle studies as an aid to plant taxonomy. Bull Br Mus (Nat Hist) Bot 4:1–78

    Google Scholar 

  53. 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

    Article  Google Scholar 

  54. Strucktneyer BE, Riker AJ (1951) Wound periderm formation in white-pine trees resistant to blister rust. Phytopathology 41:276–281

    Google Scholar 

  55. 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

  56. Whitmore TC (1980) A monograph of Agathis. Plant Syst Evol 135:41–69. https://doi.org/10.1007/BF00983006

    Article  Google Scholar 

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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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Correspondence to Alisa I. Arbicheva.

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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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Keywords

  • Anatomy
  • Deformations
  • Lenticel
  • Metabolism
  • Suberinization