biologia plantarum

International journal on Plant Life established by Bohumil Němec in 1959

Biologia plantarum 63:662-670, 2019 | DOI: 10.32615/bp.2019.134

Analysis of apple epidermis in respect to ontogenic resistance against Venturia inaequalis

I. ZAJÍCOVÁ1, E. TIHLAŘÍKOVÁ2, P. CIFROVÁ1, P. KYJAKOVÁ3, V. NEDĚLA2, J. SECHET4, L. HAVELKOVÁ1, J. KLOUTVOROVÁ5, K. SCHWARZEROVÁ1,*
1 Department of Experimental Plant Biology, Faculty of Science, Charles University, 12800 Prague, Czech Republic
2 Institute of Scientific Instruments, Czech Academy of Sciences, 61264 Brno, Czech Republic
3 Institute of Organic Chemistry and Biochemistry, Czech Academy of Sciences, 16610 Prague, Czech Republic
4 Institut Jean-Pierre Bourgin, INRA, AgroParisTech, CNRS, Université Paris-Saclay, 78000 Versailles, France
5 Research and Breeding Institute of Pomology, 50801 Holovousy, Czech Republic

In order to understand mechanisms of ontogenic resistance to apple scab, we analyzed various aspects of young and old leaves. We have introduced an apple plants cultivation system where in vitro propagated and rooting explants produce a genetically uniform population of apple (Malus domestica cv. Idared) plants. In this work, we demonstrate that apple plants produced in our cultivation system showed susceptibility to Venturia inaequalis, the cause of apple scab disease in young leaves and resistance in old leaves, which is similar to orchard situation. Our analysis shows that the cessation of epidermal cell expansion and shape formation coincided with the onset of ontogenic resistance in older leaves. Formation of specific cuticular lamellar structures did not coincide with ontogenic resistance onset. Further, chemical composition analysis of wax from young susceptible and old resistant leaves did not reveal specific compounds involved in ontogenic resistance. Differences in homogalacturonan content in cell walls in susceptible and resistant cells as well as decreased methylesterification of pectin in resistant leaves suggest that polysaccharide composition of the cell wall may play a role in mycelium growth and nutrition.

Keywords: apple scab, cell wall, cuticle, homogalacturonan, Malus domestica, pectin.

Received: September 7, 2018; Revised: December 7, 2018; Accepted: January 22, 2019; Published online: October 25, 2019  Show citation

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ZAJÍCOVÁ, I., TIHLAŘÍKOVÁ, E., CIFROVÁ, P., KYJAKOVÁ, P., NEDĚLA, V., SECHET, J., ... SCHWARZEROVÁ, K. (2019). Analysis of apple epidermis in respect to ontogenic resistance against Venturia inaequalis. Biologia plantarum63, Article 662-670. https://doi.org/10.32615/bp.2019.134
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References

  1. Aragón, W., Reina-Pinto, J.J., Serrano, M., Dominguez, E.: The intimate talk between plants and microorganisms at the leaf surface. - J. exp. Bot. 68: 5339-5350, 2017. Go to original source...
  2. Blumenkrantz, N., Asboe-Hansen, G.: New method for quantitative determination of uronic acids. - Anal. Biochem. 54: 484-489, 1973. Go to original source...
  3. Bringe, K., Schumacher, C.F.A., Schmitz-Eiberger, M., Steiner, U., Oerke, E.C.: Ontogenetic variation in chemical and physical characteristics of adaxial apple leaf surfaces. Phytochemistry 67: 161-170, 2006. Go to original source...
  4. Fernández, V., Guzmán-Delgado, P., Graça, J., Santos, S., Gil, L.: Cuticle structure in relation to chemical composition: re-assessing the prevailing model. - Front. Plant Sci. 7: 427, 2016. Go to original source...
  5. Fothergill, P.G., Ashcroft, R.: The nutritional requirements of Venturia inaequalis. - J. gen. Microbiol. 12: 387-395, 1955. Go to original source...
  6. González-Domínguez, E., Armengol, J., Rossi, V.: Biology and epidemiology of Venturia species affecting fruit crops: a review. - Front. Plant Sci. 8:1496, 2017. Go to original source...
  7. Gusberti, M., Gessler, C., Broggini, G.A.L.: RNA-seq analysis reveals candidate genes for ontogenic resistance in Malus-Venturia pathosystem. - PLoS ONE 8: e78457, 2013. Go to original source...
  8. Hocq, L., Pelloux, J., Lefebvre, V.: Connecting homogalacturonan-type pectin remodeling to acid growth. - Trends Plant Sci. 22: 20-29, 2017. Go to original source...
  9. Hongo, S., Sato, K., Yokoyama, R., Nishitani, K.: Demethylesterification of the primary wall by pectin methylesterase35 provides mechanical support to the Arabidopsis stem. - Plant Cell 24: 2624-2634, 2017. Go to original source...
  10. Jha, G., Thakur, K., Thakur, P.: The Venturia-apple pathosystem: pathogenicity mechanisms and plant defense responses. - J. Biomed. Biotechnol. 680160: 1-10, 2009. Go to original source...
  11. Kerstiens, G.: Signalling across the divide: a wider perspective of cuticular structure-function relationships. - Trends Plant Sci. 1: 125-129, 1996. Go to original source...
  12. Klavons, J.A., Bennett, R.D.: Determination of methanol using alcohol oxidase and its application to methyl ester content of pectins. - J. Agr. Food Chem. 34: 597-599,1986. Go to original source...
  13. Kollar, A.: Evidence for loss of ontogenetic resistance of apple leaves against Venturia inaequalis. Eur. J. Plant Pathol. 102: 773-778, 1996. Go to original source...
  14. Kollar, A.: Characterization of an endopolygalacturonase produced by the apple scab fungus, Venturia inaequalis. - Mycol. Res. 102: 313-319, 1998. Go to original source...
  15. Köller, W., Parker, D.M., Becker, C.M.: Role of cutinase in the penetration of apple leaves by Venturia inaequalis. Phytopathology 81: 1375-1379, 1991. Go to original source...
  16. Krupková, E., Immerzeel, P., Pauly, M., Schmülling, T., Krupkova, E., Immerzeel, P., Pauly, M., Schmulling, T.: The Tumorous shoot development2 gene of Arabidopsis encoding a putative methyltransferase is required for cell adhesion and co-ordinated plant development. - Plant J. 50: 735-750, 2007. Go to original source...
  17. Levesque-Tremblay, G., Pelloux, J., Braybrook, S.A., Müller, K.: Tuning of pectin methylesterification: consequences for cell wall biomechanics and development. - Planta 242: 791-811, 2015. Go to original source...
  18. Li, B., Xu, X.: Infection and development of apple scab (Venturia inaequalis) on old leaves. - J. Phytopathol. 150: 687-691, 2002. Go to original source...
  19. MacHardy W.E.: Apple Scab: Biology, Epidemiology, and Management. - APS Press, Sankt Paul 1996.
  20. Mouille, G., Ralet, M.C., Cavelier, C., Eland, C., Effroy, D., Hematy, K., McCartney, L., Truong, H.N., Gaudon, V., Thibault, J.F., Marchant, A., Hofte, H.: Homogalacturonan synthesis in Arabidopsis thaliana requires a Golgi-localized protein with a putative methyltransferase domain. - Plant J. 50: 605-614, 2007. Go to original source...
  21. Neděla, V., Hřib, J., Havel, L., Hudec, J., Runštuk, J.: Imaging of Norway spruce early somatic embryos with the ESEM, Cryo-SEM and laser scanning microscope. - Micron 84: 67-71, 2016a. Go to original source...
  22. Neděla, V., Hřib, J., Vooková, B.: Imaging of early conifer embryogenic tissues with the environmental scanning electron microscope. - Biol. Plant. 56: 595-598, 2012. Go to original source...
  23. Neděla, V., Tihlaříková, E., Hřib, J.: The low-temperature method for study of coniferous tissues in the environmental scanning electron microscope. - Microsc. Res. Tech. 78: 13-21, 2015. Go to original source...
  24. Neděla, V., Tihlaříková, E., Schiebertová, P., Zajícová, I., Schwarzerová, K.: Study of plant waxes using low temperature method for ESEM. - Microsc. Microanal. 22: 1180-1181, 2016b. Go to original source...
  25. Neumetzler, L., Humphrey, T., Lumba, S., Snyder, S., Yeats, T.H., Usadel, B., Vasilevski, A., Patel, J., Rose, J.K.C., Persson, S., Bonetta, D.: The FRIABLE1 gene product affects cell adhesion in Arabidopsis. PLoS ONE 7: e42914, 2012. Go to original source...
  26. Peaucelle, A., Braybrook, S.A., Le Guillou, L., Bron, E., Kuhlemeier, C., Höfte, H.: Pectin-induced changes in cell wall mechanics underlie organ initiation in Arabidopsis. - Curr. Biol. 21: 1720-1726, 2011. Go to original source...
  27. Peaucelle, A., Wightman, R., Höfte, H.: The control of growth symmetry breaking in the Arabidopsis hypocotyl. - Curr. Biol. 25: 1746-1752, 2015. Go to original source...
  28. Riederer, M., Schreiber, L.: Protecting against water loss: analysis of the barrier properties of plant cuticles. - J. exp. Bot. 52: 2023-2032, 2001. Go to original source...
  29. Serrano, M., Coluccia, F., Torres, M., L'Haridon, F., Métraux, J.P.: The cuticle and plant defense to pathogens. - Front. Plant Sci. 5: 274, 2014. Go to original source...
  30. Shepherd, T., Robertson, G.W., Griffiths, D.W., Birch, A.N.E.: Epicuticular wax composition in relation to aphid infestation and resistance in red raspberry (Rubus idaeus L.). - Phytochemistry 52: 1239-1254, 1999. Go to original source...
  31. Szymańska, R., Kruk, J.: Tocopherol content and isomers' composition in selected plant species. - Plant Physiol. Biochem. 46: 29-33, 2008. Go to original source...
  32. Townsend G.R., Heuberger J.W.: Methods for estimating losses caused by diseases in fungicidal experiments. -. Plant Dis. Rep. 27: 340-343, 1943.
  33. Vallarino, J.G., Osorio, S.: Signaling role of oligogalacturonides derived during cell wall degradation. - Plant Signal. Behav. 7: 1447-1449, 2012. Go to original source...
  34. Valsangiacomo, C., Gessler, C.: Role of the cuticular membrane in ontogenic and Vf-resistance of apple leaves against Venturia inaequalis. - Phytopathology 78: 1066, 1988. Go to original source...
  35. Valsangiacomo, C., Gessler, C.: Purification and characterization of an exopolygalacturonase produced by Venturia-inaequalis, the causal agent of apple scab. - Physiol. mol. Plant Pathol. 40: 63-77, 1992. Go to original source...
  36. Wolf, S., Greiner, S.: Growth control by cell wall pectins. - Protoplasma 249: S169-S175, 2012. Go to original source...
  37. Yeats, T.H., Rose, J.K.C.: The formation and function of plant cuticles. - Plant Physiol. 163: 5-20, 2013. Go to original source...