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Planta

, Volume 230, Issue 1, pp 95–105 | Cite as

Two sides of a leaf blade: Blumeria graminis needs chemical cues in cuticular waxes of Lolium perenne for germination and differentiation

  • Anna Ringelmann
  • Michael Riedel
  • Markus Riederer
  • Ulrich HildebrandtEmail author
Original Article

Abstract

Plant surface characteristics were repeatedly shown to play a pivotal role in plant–pathogen interactions. The abaxial leaf surface of perennial ryegrass (Lolium perenne) is extremely glossy and wettable compared to the glaucous and more hydrophobic adaxial surface. Earlier investigations have demonstrated that the abaxial leaf surface was rarely infected by powdery mildew (Blumeria graminis), even when the adaxial surface was densely colonized. This led to the assumption that components of the abaxial epicuticular leaf wax might contribute to the observed impairment of growth and development of B. graminis conidia on abaxial surfaces of L. perenne. To re-assess this hypothesis, we analyzed abundance and chemical composition of L. perenne ab- and adaxial epicuticular wax fractions. While the adaxial epicuticular waxes were dominated by primary alcohols and esters, the abaxial fraction was mainly composed of n-alkanes and aldehydes. However, the major germination and differentiation inducing compound, the C26-aldehyde n-hexacosanal, was not present in the abaxial epicuticular waxes. Spiking of isolated abaxial epicuticular Lolium waxes with synthetically produced n-hexacosanal allowed reconstituting germination and differentiation rates of B. graminis in an in vitro germination assay using wax-coated glass slides. Hence, the absence of the C26-aldehyde from the abaxial surface in combination with a distinctly reduced surface hydrophobicity appears to be primarily responsible for the failure of normal germling development of B. graminis on the abaxial leaf surfaces of L. perenne.

Keywords

Blumeria Lolium Epicuticular wax n-Hexacosanal Pre-penetration (fungal development) 

Abbreviations

agt

Appressorial germ tube

app

Appressorium

sgt

Secondary germ tube

Notes

Acknowledgments

The authors thank Olga Frank and Nadine Geudner for excellent technical assistance, Vanessa Zabka, Tanja Gulder and Gerhard Bringmann for the synthesis of n-hexacosanal. This project was financially supported by the Deutsche Forschungsgemeinschaft (Sonderforschungsbereich 567).

References

  1. Allebone JE, Hamilton RJ (1972) Cuticular leaf waxes. III. Free and esterified acids and alcohols in Chenopodium album, Lolium perenne and Stellaria media. J Sci Food Agric 23:777–786CrossRefGoogle Scholar
  2. Allebone JE, Hamilton RJ, Knights BA, Middleditch BS, Power DM (1970) Cuticular leaf waxes Part II. Chenopodium album L. and Lolium perenne L. Chem Phys Lipids 4:37–46CrossRefGoogle Scholar
  3. Allebone JE, Hamilton RJ, Bryce TA, Kelly W (1971) Anthraquinone in plant surface waxes. Experientia 27:13–14CrossRefGoogle Scholar
  4. Apel P (1979) Leitbündeldichte und Stomatafrequenz von Gramineen-Arten mit C3-beziehungsweise C4-pathway der Photosynthese. Kulturpflanze 27:91–95CrossRefGoogle Scholar
  5. Blacklock BJ, Jaworski JG (2006) Substrate specificity of Arabidopsis 3-ketoacyl-CoA synthases. Biochem Biophys Res Commun 346:583–590PubMedCrossRefGoogle Scholar
  6. Buschhaus C, Herz H, Jetter R (2007) Chemical composition of the epicuticular and intracuticular wax layers on adaxial sides of Rosa canina leaves. Ann Bot 100:1557–1564PubMedCrossRefGoogle Scholar
  7. Carver TLW, Thomas BJ (1990) Normal germling development by Erysiphe graminis on cereal leaves freed of epicuticular wax. Plant Pathol 39:375–376Google Scholar
  8. Carver TLW, Thomas BJ, Ingerson-Morris SM, Roderick HW (1990) The role of abaxial leaf surface waxes of Lolium spp. in resistance to Erysiphe graminis. Plant Pathol 39:376–390CrossRefGoogle Scholar
  9. Carver TLW, Ingerson–Morris SM, Thomas BJ (1995) Early interactions during powdery mildew infection. Can J Bot 73:S632–S639CrossRefGoogle Scholar
  10. Carver TLW, Ingerson SM, Thomas BJ (1996) Influences of host surface features on development of Erysiphe graminis and Erysiphe pisi. In: Kerstiens G (ed) Plant cuticles. BIOS Scientific Publishers, Oxford, pp 255–266Google Scholar
  11. Dragota S, Riederer M (2007) Epicuticular wax crystals of Wollemia nobilis: morphology and chemical composition. Ann Bot 100:225–231PubMedCrossRefGoogle Scholar
  12. Ellingboe AH (1972) Genetics and physiology of primary infection by Erysiphe graminis. Phytopathology 62:401–406Google Scholar
  13. Gniwotta F, Vogg G, Gartmann V, Carver TLW, Riederer M, Jetter R (2005) What do microbes encounter at the plant surface? Chemical composition of pea leaf cuticular waxes. Plant Physiol 139:519–531PubMedCrossRefGoogle Scholar
  14. Guhling O, Kinzler C, Dreyer M, Bringmann G, Jetter R (2005) Surface composition of myrmecophilic plants: cuticular wax and glandular trichomes on leaves of Macaranga tanarius. J Chem Ecol 31:2323–2341PubMedCrossRefGoogle Scholar
  15. Hall DM, Burke W (1974) Wettability of leaves of a selection of New Zealand plants. N Z J Bot 12:283–298Google Scholar
  16. Hamilton RJ, Power DM (1969) The chemical composition of the surface wax of Lolium perenne. Phytochemistry 8:1771–1775CrossRefGoogle Scholar
  17. Holloway PJ (1969) Chemistry of leaf waxes in relation to wetting. J Sci Food Agric 20:124–128CrossRefGoogle Scholar
  18. Holloway PJ (1970) Surface factors affecting the wetting of leaves. Pest Manag Sci 1:156–163Google Scholar
  19. Iwamoto M, Takeuchi Y, Takada Y, Yamaoka N (2002) Coleoptile surface cuticle of barley is involved in survival and penetration of Blumeria graminis. Physiol Mol Plant Pathol 60:31–38CrossRefGoogle Scholar
  20. Jeffree CE (2006) The fine structure of the plant cuticle. In: Riederer M, Müller C (eds) Biology of the plant cuticle. Blackwell, Oxford, pp 11–125CrossRefGoogle Scholar
  21. Jetter R, Schäffer S (2001) Chemical composition of the Prunus laurocerasus leaf surface. Dynamic changes of the epicuticular wax film during leaf development. Plant Physiol 126:1725–1737PubMedCrossRefGoogle Scholar
  22. Jetter R, Schäffer S, Riederer M (2000) Leaf cuticular waxes are arranged in chemically and mechanically distinct layers: evidence from Prunus laurocerasus L. Plant Cell Environ 23:619–628CrossRefGoogle Scholar
  23. Joubès J, Raffaele S, Bourdenx B, Garcia C, Laroche-Traineau J, Moreau P, Domergue F, Lessire R (2008) The VLCFA elongase gene family in Arabidopsis thaliana: phylogenetic analysis, 3D modelling and expression profiling. Plant Mol Biol 67:547–566PubMedCrossRefGoogle Scholar
  24. Knoll D, Schreiber L (2000) Plant–microbe interactions: wetting of ivy (Hedera helix L.) leaf surfaces in relation to colonization by epiphytic microorganisms. Microb Ecol 41:33–42Google Scholar
  25. Koch K, Barthlott W, Koch S, Hommes A, Wandelt K, Mamdouh W, De-Feyter S, Broekmann P (2006) Structural analysis of wheat wax (Triticum aestivum, c.v. ‘Naturastar’ L.): from the molecular level to three dimensional crystals. Planta 223:258–270PubMedCrossRefGoogle Scholar
  26. Lyngkjær MF, Carver TLW (1999) Induced accessibility and inaccessibility to Blumeria graminis f.sp. hordei in barley epidermal cells attacked by a compatible isolate. Physiol Mol Plant Pathol 55:151–162CrossRefGoogle Scholar
  27. Manners JG, Hossain SMM (1963) Effects of temperature and humidity on conidial germination of Erysiphe graminis. Trans Br Mycol Soc 46:225–234CrossRefGoogle Scholar
  28. Müller C, Riederer M (2005) Plant surface properties in chemical ecology. J Chem Ecol 31:2621–2651PubMedCrossRefGoogle Scholar
  29. Niks RE, Rubiales D (2002) Potentially durable resistance mechanisms in plants to specialized fungal pathogens. Euphytica 124:201–216CrossRefGoogle Scholar
  30. Pollard A, Chibnall AC, Piper SH (1931) The wax constituents of forage grasses. I. Cocksfoot and perennial ryegrass. Biochem J 25:2111–2122PubMedGoogle Scholar
  31. Reifenrath K, Riederer M, Müller C (2005) Leaf surface wax layers of Brassicaceae lack feeding stimulants for Phaedon cochleariae. Entomol Exp Appl 115:41–50CrossRefGoogle Scholar
  32. Rommerskirchen F, Plader A, Eglington G, Chikaraishi Y, Rullkötter J (2006) Chemotaxonomic significance of distribution and stable carbon isotopic composition of long-chain alkanes and alkan-1-ols in C4 grass waxes. Org Geochem 10:1303–1332CrossRefGoogle Scholar
  33. Rostás M, Ruf D, Zabka V, Hildebrandt U (2008) Plant surface wax affects parasitoids response to host footprints. Naturwissenschaften 95:997–1002PubMedCrossRefGoogle Scholar
  34. Sant FI (1969) A comparison of the morphology and anatomy of seedling leaves of Lolium multiflorum Lam. and Lolium perenne L. Ann Bot 33:303–313Google Scholar
  35. Shelvey JD, Kozioł MJ (1986) Seasonal and SO2-induced changes in epicuticular wax of ryegrass. Phytochemistry 25:415–420CrossRefGoogle Scholar
  36. Stosch AK, Solga A, Steiner U, Oerke EC, Barthlott W, Cerman Z (2007) Efficiency of self-cleaning properties in wheat (Triticum aestivum L.). J Appl Bot Food Qual 81:49–55Google Scholar
  37. Trenkamp S, Martin W, Tietjen K (2004) Specific and differential inhibition of very-long-chain fatty acid elongases from Arabidopsis thaliana by different herbicides. Proc Natl Acad Sci USA 101:11903–11908PubMedCrossRefGoogle Scholar
  38. Tsuba M, Katagiri C, Takeuchi Y, Takada Y, Yamaoka N (2002) Chemical factors of the leaf surface involved in the morphogenesis of Blumeria graminis. Physiol Mol Plant Pathol 60:51–57CrossRefGoogle Scholar
  39. Vogg G, Fischer S, Leide J, Emmanuel E, Jetter R, Levy AA, Riederer M (2004) Tomato fruit cuticular waxes and their effects on transpiration barrier properties: functional characterization of a mutant deficient in a very-long-chain fatty acid β-ketoacyl-CoA synthase. J Exp Bot 55:1401–1410PubMedCrossRefGoogle Scholar
  40. Wen M, Buschhaus C, Jetter R (2006) Nanotubules on plant surfaces: chemical composition of epicuticular wax crystals on needles of Taxus baccata L. Phytochemistry 67:1808–1817PubMedCrossRefGoogle Scholar
  41. Wilson D (1975) Leaf growth, stomatal diffusion resistances and photosynthesis during droughting of Lolium perenne populations selected for contrasting stomatal length and frequency. Ann Appl Biol 79:67–82CrossRefGoogle Scholar
  42. Yang SL, Ellingboe AH (1972) Cuticle layer as a determining factor for the formation of mature appressoria of Erysiphe graminis on wheat and barley. Phytopathology 62:708–714CrossRefGoogle Scholar
  43. Zabka V, Stangl M, Bringmann G, Riederer M, Vogg G, Hildebrandt U (2008) Host surface properties affect pre-penetration processes in the barley powdery mildew fungus. New Phytol 177:251–263PubMedGoogle Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  • Anna Ringelmann
    • 1
  • Michael Riedel
    • 1
  • Markus Riederer
    • 1
  • Ulrich Hildebrandt
    • 1
    Email author
  1. 1.Universität WürzburgJulius-von-Sachs-Institut für BiowissenschaftenWürzburgGermany

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