, Volume 245, Issue 1, pp 207–220 | Cite as

The role of peltate scales in desiccation tolerance of Pleopeltis polypodioides

  • Susan P. John
  • Karl H. HasensteinEmail author
Original Article


Main conclusion

The extreme drought tolerance of the resurrection fern is in part the result of the dorsal scales that assist in water distribution and controlled desiccation.

We studied the effect of peltate scales on water uptake and loss of the desiccation-tolerant epiphytic fern Pleopeltis polypodioides using optical and FTIR microscopy and staining with calcofluor, solophenyl flavine7GFE, and Ruthenium Red. We provide information on structure, property, and function of the scales by measuring water uptake and dehydration, contact angles, and metabolic activity. Peltate scales mainly contain cellulose, xylogalactans, and pectin. Water is absorbed from the center of scales, and the overlapping arrangement of scales facilitates surface spreading of water. Intact fronds hydrated fully within 5 h of imbibition of the apical pinna, without scales water uptake stopped after 1 h. Hydration rates via rhizomes followed a longer time course but also improved in the presence of scales. Fronds with and without scales lost half of their water content in 15 or 4 h, respectively. The overall metabolism of rapidly dehydrated fronds was significantly reduced compared with slowly dehydrated fronds. Thus, water management and metabolism of Pleopeltis are dependent on surface properties determined by peltate scales.


Resurrection fern Water uptake Dehydration FTIR microscopy Metabolism 



Solophenyl flavine


Fourier transform infrared spectroscopy


Ruthenium red



We thank Dr. T. Pesacreta for providing solophenyl flavine 7GFE 500 and Dr. O. Kizilkaya for his help with FTIR spectroscopy. This research was partially supported by NASA grants NNX10AP91G and NNX13AN05A.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

425_2016_2631_MOESM1_ESM.docx (1.2 mb)
Supplementary material 1 (DOCX 1195 kb)

Online Resource Video S1 Spreading of calcofluor solution on the dorsal surface of P. polypodioides. During the first 30 min of imbibition, the dye spreads from the apical pinnae towards rachis and the stipe. During the course of spreading, the dye strongly bounds to the peltate scales. Images were taken at 1 min intervals for 30 min (MP4 2471 kb)

Online Resource Video S2 Uptake of water through the central disc of the scale. Images were taken at 2 s intervals (MP4 960 kb)

Online Resource Video S3 Water movement underneath the scales and uptake via stalk of scale. Images that were taken at 2 s intervals (MP4 1129 kb)


  1. Alpert P, Oliver M (2002) Drying without dying. In: Black M, Pritchard H (eds) Desiccation and survival in plants. CAB International, Wallingford, pp 3–43CrossRefGoogle Scholar
  2. Anderson C, Carroll A, Akhmetova L, Somerville C (2010) Real-time imaging of cellulose reorientation during cell wall expansion in Arabidopsis roots. Plant Physiol 152:787–796CrossRefPubMedCentralPubMedGoogle Scholar
  3. Bartels D (2005) Desiccation tolerance studied in the resurrection plant Craterostigma plantagineum. Integr Comp Biol 45:696–701CrossRefPubMedGoogle Scholar
  4. Benzing D (1976) Bromeliad trichomes: structure, function, and ecological significance. Selbyana 1:330–348Google Scholar
  5. Benzing DH, Henderson K, Kessel B, Sulak J (1976) The absorptive capacities of bromeliad trichomes. Am J Bot 63:1009–1014CrossRefGoogle Scholar
  6. Blancaflor E, Hasenstein K (1993) Organization of cortical microtubules in graviresponding maize roots. Planta 191:231–237PubMedGoogle Scholar
  7. Boom A, Sinninge Damsté JS, de Leeuw JW (2005) Cutan, a common aliphatic biopolymer in cuticles of drought-adapted plants. Org Geochem 36:595–601CrossRefGoogle Scholar
  8. Burkhardt J, Basi S, Pariyar S, Hunsche M (2012) Stomatal penetration by aqueous solutions—an update involving leaf surface particles. New Phytol 196:774–787CrossRefPubMedGoogle Scholar
  9. Camargo M, Marenco R (2011) Density, size and distribution of stomata in 35 rainforest tree species in Central Amazonia. Acta Amazonica 41:205–211CrossRefGoogle Scholar
  10. Cruz de Carvalho R, Catalá M, Marques da Silva J, Branquinho C, Barreno E (2012) The impact of dehydration rate on the production and cellular location of reactive oxygen species in an aquatic moss. Ann Bot 110:1007–1016CrossRefPubMedCentralPubMedGoogle Scholar
  11. Dybing C, Currier H (1961) Foliar penetration by chemicals. Plant Physiol 36:169–174CrossRefPubMedCentralPubMedGoogle Scholar
  12. Ensikat H, Ditsche-Kuru P, Neinhuis C, Barthlott W (2011) Superhydrophobicity in perfection: the outstanding properties of the lotus leaf. Beilstein J Nanotechnol 2:152–161CrossRefPubMedCentralPubMedGoogle Scholar
  13. Farooq M, Hussain M, Wahid A, Siddique K (2012) Drought stress in plants: an overview. In: Aroca R (ed) Plant responses to drought stress. Springer, Berlin Heidelberg, pp 1–33CrossRefGoogle Scholar
  14. Farrant J, Lehner A, Cooper K, Wiswedel S (2009) Desiccation tolerance in the vegetative tissues of the fern Mohria caffrorum is seasonally regulated. Plant J 57:65–79CrossRefPubMedGoogle Scholar
  15. Fernández V, Eichert T (2009) Uptake of hydrophilic solutes through plant leaves: current state of knowledge and perspectives of foliar fertilization. Crit Rev Plant Sci 28:36–68CrossRefGoogle Scholar
  16. Fernández V, Sancho-Knapik D, Paula Guzmán, Javier Peguero-Pina J, Gil L, Karabourniotis G, Khayet M, Fasseas C, Alejandro Heredia-Guerrero J, Antonio Heredia, Eustaquio G-P (2014) Wettability, polarity, and water absorption of holm oak leaves: effect of leaf side and age. Plant Physiol 166:168–180CrossRefPubMedCentralPubMedGoogle Scholar
  17. Frisch H (1991) Fundamentals of membrane transport. Polym J 23:445–456CrossRefGoogle Scholar
  18. Gaff D (1977) Desiccation tolerant vascular plants of Southern Africa. Oceologia (Berl.) 31:95–109CrossRefGoogle Scholar
  19. Georgieva K, Doncheva S, Mihailova G, Petkova S (2012) Response of sun- and shade-adapted plants of Haberlea rhodopensis to desiccation. Plant Growth Regul 67:121–132CrossRefGoogle Scholar
  20. Guzman-Delgado P, Graca J, Cabral V, Gil L, Fernandez V (2016) The presence of cutan limits the interpretation of cuticular chemistry and structure: Ficus elastica leaf as an example. Physiol Plant 157:205–220CrossRefPubMedGoogle Scholar
  21. Haberlandt G (1914) The dermal system in physiological plant anatomy. MacMillan, LondonGoogle Scholar
  22. Harholt J, Suttangkakul A, Scheller H (2010) Biosynthesis of pectin. Plant Physiol 153:384–395CrossRefPubMedCentralPubMedGoogle Scholar
  23. Hauser M (2014) Molecular basis of natural variation and environmental control of trichome patterning. Front Plant Sci 5:1–7CrossRefGoogle Scholar
  24. Helseth L, Fischer T (2005) Physical mechanisms of rehydration in Polypodium polypodioides, a resurrection plant. Phys Rev E Stat Nonlinear Soft Matter Phys 71:061903CrossRefGoogle Scholar
  25. Heredia-Guerrero JA, Benitez JJ, Dominguez E, Bayer IS, Cingolani R, Athanassiou A, Heredia A (2014) Infrared and Raman spectroscopic features of plant cuticles: a review. Front Plant Sci 5:305CrossRefPubMedCentralPubMedGoogle Scholar
  26. Johnson D (1921) Polypodium vulgare as an epiphyte. Bot Gaz 72:237–244CrossRefGoogle Scholar
  27. Kappen L, Valladares F (2007) Opportunistic growth and desiccation tolerance: the ecological success of poikilohydrous autotrophs. In: Pugnaire F, Valladares F (eds) Handbook of functional plant ecology. Marcel Dekker, New York, pp 10–80Google Scholar
  28. Kerstiens G (1996) Cuticular water permeability and its physiological significance. J Exp Bot 47:1813–1832CrossRefGoogle Scholar
  29. Koch K, Bhushan B, Barthlott W (2009) Multifunctional surface structures of plants: an inspiration for biomimetics. Prog Mater Sci 54:137–178CrossRefGoogle Scholar
  30. Larson D (1981) Differential wetting in some lichens and mosses: the role of morphology. Bryologist 84:1–15CrossRefGoogle Scholar
  31. Layton B, Boyd M, Tripepi MS, Bitonti BM, Dollahon MNR, Balsamo RA (2010) Dehydration-induced expression of a 31-kDa dehydrin in Polypodium polypodioides (Polypodiaceae) may enable large, reversible deformation of cell walls. Am J Bot 97:535–544CrossRefPubMedGoogle Scholar
  32. Lewis A, Harnden V, Tyree M (1994) Collapse of water-stress emboli in the tracheids of Thuja occidentalis L. Plant Physiol 106:1639–1646CrossRefPubMedCentralPubMedGoogle Scholar
  33. Limm E, Simonin KA, Bothman AG, Dawson TE (2009) Foliar water uptake: a common water acquisition strategy for plants of the redwood forest. Oceologia 161:449–459CrossRefGoogle Scholar
  34. McCleery E (1907) Stellate hairs and peltate scales of Ohio plants. Ohio Nat 7:51–56Google Scholar
  35. Müller L, Starnecker G, Winkler S (1981a) A contribution to the ecology of epiphytic ferns from southern Brazil. I. Water absorbing trichomes. Flora 171:55–63Google Scholar
  36. Müller L, Starnecker G, Winkler S (1981b) Zur Ökologie epiphytischer Farne in Südbrasilien—I. Saugschuppen. Flora 171:55–63Google Scholar
  37. O’Brien J, Wilson I, Orton T, Pognan F (2000) Investigation of the alamar blue (resazurin) fluorescent dye for the assessment of mammalian cell cytotoxicity. Eur J Biochem 267:5421–5426CrossRefPubMedGoogle Scholar
  38. Oliver M, Velten J, Mishler B (2005) Desiccation tolerance in bryophytes: a reflection of the primitive strategy for plant survival in dehydrating habitats? Integr Comp Biol 45:788–799CrossRefPubMedGoogle Scholar
  39. Pampurova S, Van Dijck P (2014) The desiccation tolerant secrets of Selaginella lepidophylla: what we have learned so far? Plant Physiol Biochem 80:285–290CrossRefPubMedGoogle Scholar
  40. Papini A, Tani G, Di Falco P, Brigjigna L (2010) The ultrastructure of the development of Tillandsia (Bromeliaceae) trichome. Flora 205:94–100CrossRefGoogle Scholar
  41. Pesacreta T, Hasenstein K (1999) The internal cuticle of Cirsium horridulum (Asteraceae) leaves. Am J Bot 86:923–928CrossRefPubMedGoogle Scholar
  42. Pessin L (1924) A physiological and anatomical study of the leaves of Polypodium polypodioides. Am J Bot 11:370–381CrossRefGoogle Scholar
  43. Pierce S (2007) The jeweled armor of Tillandsia—multifaceted or elongated trichomes provide photoprotection. Aliso 23:44–52CrossRefGoogle Scholar
  44. Pierce S, Maxwell K, Griffiths H, Winter K (2001) Hydrophobic trichome layers and epicuticular wax powders in Bromeliaceae. Am J Bot 88:1371–1389CrossRefPubMedGoogle Scholar
  45. Porembski S (2007) Tropical inselbergs: habitat types, adaptive strategies and diversity patterns. Rev Brasil Bot 30:579–586CrossRefGoogle Scholar
  46. Proctor M, Pence V (2002) Vegetative tissues: bryophytes, vascular resurrection plants and vegetative propagules. In: Black M, Pritchard H (eds) Desiccation and survical in plants. CAB International, Wallingford, pp 207–237CrossRefGoogle Scholar
  47. Rensburg L, Peacock J, Krüger G (1999) Boundary layer, stomatal geometry and -spacing, in relation to drought tolerance in four Nicotiana tabacum L. cultivars. South Afr J Plant Soil 16:44–49CrossRefGoogle Scholar
  48. Retamales H, Scharaschkin T (2014) A staining protocol for identifying secondary compounds in Myrtaceae. Appl Plant Sci 2:1400063CrossRefGoogle Scholar
  49. Reynolds T, Bewley J (1993) Abscisic acid enhances the ability of the desiccation-tolerant fern Polypodium virginianum to withstand drying. J Exp Bot 44:1771–1779CrossRefGoogle Scholar
  50. Riederer M, Schreiber L (2001) Protecting against water loss: analysis of the barrier properties of plant cuticles. J Exp Bot 52:2023–2032CrossRefPubMedGoogle Scholar
  51. Rui Y, Anderson C (2016) Functional analysis of cellulose and xyloglucan in the walls of stomatal guard cells of Arabidopsis. Plant Physiol 170:1398–1419PubMedCentralPubMedGoogle Scholar
  52. Rundel P (1982) Water uptake by organs other than roots. In: Lange O, Nobel P, Osmond C (eds) Encyclopedia of plant physiology. Springer, Berlin, pp 111–134Google Scholar
  53. Schneider P, Schmitt J (2011) Composition, community structure and vertical distribution of epiphytic ferns on Alsophila setosa Kaulf., in a Semideciduous Seasonal Forest, Morro Reuter, RS, Brazil. Acta Bot Bras 25:557–565CrossRefGoogle Scholar
  54. Schönherr J (2006) Characterization of aqueous pores in plant cuticles and permeation of ionic solutes. J Exp Biol 57:2471–2491Google Scholar
  55. Schönherr J, Bukovac M (1972) Penetration of stomata by liquids. Dependence on surface tension, wettability, and stomatal morphology. Plant Physiol 49:813–819CrossRefPubMedCentralPubMedGoogle Scholar
  56. Shepherd T, Griffiths D (2006) The effects of stress on plant cuticular waxes. New Phytol 171:469–499CrossRefPubMedGoogle Scholar
  57. Sperry J, Tyree M (1988) Mechanism of water stress-induced xylem embolism. Plant Physiol 88:581–587CrossRefPubMedCentralPubMedGoogle Scholar
  58. Stuart T (1968) Revival of respiration and photosynthesis in dried leaves of Polypodium polypodioides. Planta 83:185–206CrossRefPubMedGoogle Scholar
  59. Synytsya A (2003) Fourier transform Raman and infrared spectroscopy of pectins. Carbohydr Polym 54:97–106CrossRefGoogle Scholar
  60. Toldi O, Tuba Z, Scott P (2009) Vegetative desiccation tolerance: is it a goldmine for bioengineering crops? Plant Sci 176:187–199CrossRefGoogle Scholar
  61. Tsutsumi C, Kato M (2008) Morphology and evolution of epiphytic Davalliaceae scales. Botany 86:1393–1403CrossRefGoogle Scholar
  62. Varadarajan G, Gilmartin A (1987) Foliar Scales of the subfamily Pitcainioideae (Bromeliaceae). Syst Bot 12:562–571CrossRefGoogle Scholar
  63. Voytena A, Minardi B, Barufi J, Santos M, Randi Á (2014) Pleopeltis pleopeltifolia (Polypodiopsida, Polypodiaceae), a poikilochlorophyllous desiccation-tolerant fern: anatomical, biochemical and physiological responses during water stress. Aust J Bot 62:647–656CrossRefGoogle Scholar
  64. Wallace I, Anderson C (2012) Small molecule probes for plant cell wall polysaccharide imaging. Front Plant Sci 3:1–8CrossRefGoogle Scholar
  65. Wang H, Shi H, Li Y, Wang Y (2014) The effects of leaf roughness, surface free energy and work of adhesion on leaf water drop adhesion. PLoS One 9:e107062CrossRefPubMedCentralPubMedGoogle Scholar
  66. Wilson RH, Smith AC, Waldron KW (2000) The mechanical prospects and molecular dynamics of plant cell wall polysaccharides studied by fourier-transform infrared spectroscopy. Plant Physiol 124:397CrossRefPubMedCentralPubMedGoogle Scholar
  67. Zenkteler E, Jędrzejczyk I (2012) Morphology and anatomy of the rhizome of Polypodium × mantoniae Rothm. In: Gola E, Szczęśniak E (eds) Genus Polypodium L. in Poland. Polish Botanical Society, Wroclaw, pp 27–38Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  1. 1.Department of BiologyUniversity of Louisiana at LafayetteLafayetteUSA

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