DIFFERENCES IN THE STRUCTURE OF FRUIT BUDS IN TWO APPLE CULTIVARS WITH PARTICULAR EMPHASIS ON FEATURES RESPONSIBLE FOR FRUIT STORABILITY AND QUALITY
Agata Konarska
University of Life Sciences in LublinAbstract
‘Jonagold’ and ‘Szampion’ are winter apple cultivars, whose fruits are suitable for long-term storage. However, fruits of these cultivars differ markedly in the type of the surface and the rate and volume of water transpiration, which is manifested in fruit quality after storage and the length of apple shelf life. A majority of factors responsible for fruit quality and storability are genetically conditioned traits that are mainly developed before fruits reach harvest maturity or still develop during the storage period. The micromorphology, anatomy, and ultrastructure of 21-day-old fruit buds of the ‘Jonagold’ and ‘Szampion’ were examined using light microscopy as well as scanning and transmission electron microscopy. The analyses were particularly focused on the traits that determine fruit firmness and storability, which contribute to long-term storage capacity. It was found that the fruit buds in both cultivars differed significantly in the number of trichome scars
and stomata on the fruit surface, the thickness of the hypodermis layer and the hypodermis cell walls, and in the content of phenolic compound deposits. At the fruit bud stage, the following features related to increased or decreased fruit firmness and storability were observed: platelet crystalline wax, cuticle microcracks, stomata and trichome scars, and presence of phenolic compounds.
Keywords:
apple fruit buds, fruit peel, micromorphology, histology and ultrastructure, cuticle and epicuticular wax, microcracks, phenol compoundsReferences
Atay E., Pirlak L., Atay A.N., 2010. Determination of fruit growth in some apple varieties. J. Agric. Sci., 16, 1–8.
Babos K., Sass P., Mohácsy P., 1984. Relationship between the peel structure and storability of apples. Acta Agron. Acad. Sci. Hung., 33, 41–50.
Bain J.M., 1961. Some morphological, anatomical, and physiological changes in the pear fruit (Pyrus communis var. Williams Bon Chrétien) during development and following harvest. Aust. J. Bot., 9, 99–123.
Bednorz L., Wojciechowicz M.K., 2009. Development of the multilayered epidermis covering fruit of Sorbus torminalis (Rosaceae). Dendrobiology, 62, 11–16.
Belding R.D., Blankenship S.M., Young E., Leidy R.B., 1998. Composition and variability of epicuticular waxes in apple cultivars. J. Amer. Soc. Hort. Sci., 123, 348–356.
Celano G., Minnocci A., Sebastiani L., D’Auria M., Xiloyannis C., 2009. Changes in the structure of the skin of kiwifruit in a relation to water. J. Hortic. Sci. Biotech., 84, 41–46.
Cieslak M., Génard M., Boudon F., Baldazzi V., Godin C., Bertin N., 2013. Integrating architecture and physiological perspectives in fruit development. Proceedings of the 7th International Conference on Functional-Structural Plant Models. 9–14 June 2013, Saariselkä, Finland, 127–130.
Cheynier V., 2005. Polyphenols in foods are more complex than often thought. Am. J. Clin. Nutr., 81, 2235–2295.
Curry E.A., 2001. Lenticel and cuticle disorders: a survey. Proceedings of the Washington Tree Fruit Postharvest Conference. 13–14 March 2001, Wenatchee, WA, USA.
Curry E.A., 2005. Ultrastructure of epicuticular wax aggregates during fruit development in apple (Malus domestica Borkh). J. Hortic. Sci. Biotech., 80, 668–676.
Curry E.A., 2009. Growth-induced microcracking and repair mechanisms of fruit cuticles. Plant Physiology. Proceedings of the SEM Annual Conference. 1–4 June 2009, Albuquereque New Mexico, USA.
Czernyszewicz E., 2007. A consumer’s look at the apple quality. Annales UMCS, sec. EEE, Horticultura, 17, 70–82.
De Bellie N., Schotte S., Soucke P., De Baerdemaeker J., 2000. Development of an automated monitoring device to quantify changes in firmness of apples during storage. Postharv. Biol. Technol., 18, 1–8.
Drogoudi P.D., Michailidis Z., Pantelidis G., 2008. Peel and flesh antioxidant content and harvest quality characteristics of seven apple cultivars. Sci. Hortic., 115, 149–153.
Faust M., Shear C.B., 1972a. Russeting of apples, an interpretive review. HortSci., 7, 233–235.
Faust M., Shear C.B., 1972b. Fine structure of the fruit surface of three apple cultivars. J. Am. Soc. Hortic. Sci., 97, 351–355.
Garry L.L., Suttill N.H., Wall K.M., Beveridge T.H., 1995. Localization of condensed tannins in apple fruit peel, pulp, and seeds. Can. J. Bot., 73, 1897–1904.
Gordon D.C., Percy K.E., Riding R.T., 1998. effects of uv-radiation on epicuticular wax production and chemical composition of four Picea species. New Phytol., 138, 441–449.
Guzmán P., Fernández V., García M.L., Khayet M., Fernández A., Gil L., 2014. Localization of polysaccharides in isolated and intact cuticles of eucalypt, poplar and pear leaves by enzymegold labelling. Plant Physiol. Biochem., 76, 1–6.
Harker F.R., Ferguson I.B., 1988. Transport of calcium across cuticles isolated from apple fruit. Sci. Hortic., 36, 205–217.
Homutová I., Blažek J., 2006. Differences In fruit skin thickness between selected apple (Malus domestica Borkh.) cultivars assessed by histological and sensory methods. Hort. Sci. (Prague), 33, 108–113.
Hőhn E., 1990. Quality of apples. Acta Hort., 285, 111–118.
Khanal B.P., Knoche M., 2014. Mechanical properties of apple skin are determined by epidermis and hypodermis. J. Am. Soc. Hortic. Sci., 139(2), 139–147.
Knoche M., Peschel S., Hinz M., Bukovac M.J., 2000. Studies on water transport through the sweet cherry fruit surface: Characterizing conductance of the cuticular membrane using pericarp segments. Planta, 212, 127–135.
Knoche M., Beyer M., Peschel S., Oparlakov B., Bukovac M.J., 2004. Changes in strain and deposition of cuticle in developing sweet cherry fruit. Physiol. Plant., 120, 667–677.
Koch K., Neinhuis C., Ensikat H.J., Barthlott W., 2004. Self assembly of epicuticular waxes on living plant surfaces imaged by atomic force microscopy (AFM). J. Exp. Bot., 55, 711–718.
Konarska A., 2012. Differences in the fruit peel structures between two apple cultivars during storage. Acta Sci. Pol., Hort. Cult., 11(2), 105–116.
Konarska A., 2013. The structure of the fruit peel in two varieties of Malus domestica Borkh. (Rosaceae) before and after storage. Protoplasma, 250, 701–714.
Kruczyńska D., 2008. Jabłonie: nowe odmiany. Hortpress Warszawa.
Lattanzio V., Di-Venere D., Linsalata V., Bertolini P., Ippolito A., Salerno M., 2001. Low temperature metabolism of apple phenolics and quiescence of Phlyctaena vagabunda. J. Agric. Food Chem., 49, 5817–5821.
Lau O.L., Lane W.D., 1998. Harvest indices, storability, and poststorage refrigeration requirements of ‘Sunrise’ apple. HortSci., 33, 302–304.
Link S.O., Drake S.R., Thiede M.E., 2004. Prediction of apple firmness from mass loss and shrinkage. J. Food Quality, 27, 13–26.
Łata B., Trampczyńska A., Paczesna J., 2009. Cultivar variation in apple peel and whole fruit phenolic composition. Sci. Hortic., 121, 176–181.
Maguire K.M., Lang A., Banks N.H., Hall A., Hopcroft D., Benneti R., 1999. Relationship between water vapour permeance of apples and micro-cracking of the cuticle, Postharv. Biol. Technol., 17, 89–96.
Maguire K.M., Banks N.H., Lang A., Gordon I.L., 2000. Harvest date, cultivar, orchard and tree effects on water vapour permeance in apples. J. Am. Soc. Hort. Sci., 125, 100–104.
Mehrabani L.V., Hassanpouraghdam M.B., 2012. Developmental variation of phenolic compounds in fruit tissue of two apple cultivars. Acta Sci. Pol., Technol. Aliment., 11(3), 259–264.
Miller A.N., Walsh C.S., Cohen C.D., 1987. Measurement of indole-3-acetic acid in peach fruits (Prunus persica L. Batsch cv Redhaven) during development. Plant Physiol., 84, 491–494.
Miller R.H., 1984. The multiple epidermis-cuticle complex of Medlar fruit Mespilus germanica L. (Rosaceae). Ann. Bot., 53, 779–792.
Müller I., 2005. Relationship between preharvest soybean oil application and postharvest behavior apples. Dissertation, Washington State University.
Pieniążek S.A., 2000. Sadownictwo. PWRiL Warszawa.
Reed D.W., 1982. Wax alteration and extraction Turing electron microscopy preparation of leaf cuticles. In: The plant cuticle. Cultler, D.F., Alvin K.L., Price C.E., eds. Academic Press, London.
Rejman A., 1994. Pomologia. PWRiL Warszawa.
Reynolds E.S., 1963. The use of lead citrate at high pH as an electron-opaque stain for electron microscopy. J. Cell Biol., 17, 208–212.
Riederer M., Schreiber L., 1995. Waxes – the transport barriers of plant cuticles. In: Waxes: Chemistry, molecular biology and functions, Hamilton R.J (ed.). The Oily Press, Scotland, 131–156.
Roy S., Conway W.S., Watada A.E., Sams C.E., Erbe E.F., Wergin W.P., 1994. Heat treatment affects epicuticular wax structure and postharvest calcium uptake in ‘Golden Delicious’ apples. Hort. Sci., 29, 1056–1058.
Solovchenko A., Schmitz-Eiberger M.J., 2003. Significance of skin flavonoids for UV-B-protection in apple fruits. Exp. Bot., 54, 1977–1984.
Spurr A.R., 1969. A low-viscosity epoxy resin embedding medium for electron microscopy. J. Ultra. Res., 26, 31–43.
Veraverbake E.A., van Bruaene N., van Oostveldt P., Nicolaï B.M., 2001a. Non destructive analysis of the wax layer off apple (Malus domestica Borkh.) by means of confocal laser scanning microscopy. Planta, 213, 525–533.
Veraverbake E.A., Lammertyn J., Saevels S., Nicolaï B.M., 2001b. Changes in chemical wax composition of three different apple (Malus domestica Borkh.) cultivars during storage. Postharv. Biol. Technol., 23, 197–208.
Veraverbake E.A., Verboven P., van Oostveldt P., Nicolaï B.M., 2003a. Prediction of moisture loss across the cuticle of apple (Malus sylvestris subsp. Mitis (Wallr.)) during storage: part 1. Model development and determination of diffusion coefficients, Postharv. Biol. Technol., 30, 75–88.
Veraverbeke E.A., Verboven P., van Oostveldt P., Nicolaï B.M., 2003b. Prediction of moisture loss across the cuticle of apple (Malus sylvestris subsp. Mitis (Wallr.)) during storage: part 2. Model simulations and practical applications. Postharv. Biol. Technol., 30, 89–97.
Verboven P., Nemeth A., Abera M.K., Bongaers E., Daelemans D., Estrade P., Herremans E., Hertog M., Saeys W., Vanstreels E., Verlinden B., Leitner M., Nicolaï B., 2013. Optical coherence tomography visualizes microstructure of apple peel. Postharv. Biol. Technol., 78, 123–132.
Westwood M.N., 1995. Temperate zone pomology: Physiology and culture. (Third Edition). Timber Press, Oregon.
Zamorskyi V., 2007. The role of the anatomical structure of apple fruits as fresh cut produce. Acta Hort., 746, 509–512.
Babos K., Sass P., Mohácsy P., 1984. Relationship between the peel structure and storability of apples. Acta Agron. Acad. Sci. Hung., 33, 41–50.
Bain J.M., 1961. Some morphological, anatomical, and physiological changes in the pear fruit (Pyrus communis var. Williams Bon Chrétien) during development and following harvest. Aust. J. Bot., 9, 99–123.
Bednorz L., Wojciechowicz M.K., 2009. Development of the multilayered epidermis covering fruit of Sorbus torminalis (Rosaceae). Dendrobiology, 62, 11–16.
Belding R.D., Blankenship S.M., Young E., Leidy R.B., 1998. Composition and variability of epicuticular waxes in apple cultivars. J. Amer. Soc. Hort. Sci., 123, 348–356.
Celano G., Minnocci A., Sebastiani L., D’Auria M., Xiloyannis C., 2009. Changes in the structure of the skin of kiwifruit in a relation to water. J. Hortic. Sci. Biotech., 84, 41–46.
Cieslak M., Génard M., Boudon F., Baldazzi V., Godin C., Bertin N., 2013. Integrating architecture and physiological perspectives in fruit development. Proceedings of the 7th International Conference on Functional-Structural Plant Models. 9–14 June 2013, Saariselkä, Finland, 127–130.
Cheynier V., 2005. Polyphenols in foods are more complex than often thought. Am. J. Clin. Nutr., 81, 2235–2295.
Curry E.A., 2001. Lenticel and cuticle disorders: a survey. Proceedings of the Washington Tree Fruit Postharvest Conference. 13–14 March 2001, Wenatchee, WA, USA.
Curry E.A., 2005. Ultrastructure of epicuticular wax aggregates during fruit development in apple (Malus domestica Borkh). J. Hortic. Sci. Biotech., 80, 668–676.
Curry E.A., 2009. Growth-induced microcracking and repair mechanisms of fruit cuticles. Plant Physiology. Proceedings of the SEM Annual Conference. 1–4 June 2009, Albuquereque New Mexico, USA.
Czernyszewicz E., 2007. A consumer’s look at the apple quality. Annales UMCS, sec. EEE, Horticultura, 17, 70–82.
De Bellie N., Schotte S., Soucke P., De Baerdemaeker J., 2000. Development of an automated monitoring device to quantify changes in firmness of apples during storage. Postharv. Biol. Technol., 18, 1–8.
Drogoudi P.D., Michailidis Z., Pantelidis G., 2008. Peel and flesh antioxidant content and harvest quality characteristics of seven apple cultivars. Sci. Hortic., 115, 149–153.
Faust M., Shear C.B., 1972a. Russeting of apples, an interpretive review. HortSci., 7, 233–235.
Faust M., Shear C.B., 1972b. Fine structure of the fruit surface of three apple cultivars. J. Am. Soc. Hortic. Sci., 97, 351–355.
Garry L.L., Suttill N.H., Wall K.M., Beveridge T.H., 1995. Localization of condensed tannins in apple fruit peel, pulp, and seeds. Can. J. Bot., 73, 1897–1904.
Gordon D.C., Percy K.E., Riding R.T., 1998. effects of uv-radiation on epicuticular wax production and chemical composition of four Picea species. New Phytol., 138, 441–449.
Guzmán P., Fernández V., García M.L., Khayet M., Fernández A., Gil L., 2014. Localization of polysaccharides in isolated and intact cuticles of eucalypt, poplar and pear leaves by enzymegold labelling. Plant Physiol. Biochem., 76, 1–6.
Harker F.R., Ferguson I.B., 1988. Transport of calcium across cuticles isolated from apple fruit. Sci. Hortic., 36, 205–217.
Homutová I., Blažek J., 2006. Differences In fruit skin thickness between selected apple (Malus domestica Borkh.) cultivars assessed by histological and sensory methods. Hort. Sci. (Prague), 33, 108–113.
Hőhn E., 1990. Quality of apples. Acta Hort., 285, 111–118.
Khanal B.P., Knoche M., 2014. Mechanical properties of apple skin are determined by epidermis and hypodermis. J. Am. Soc. Hortic. Sci., 139(2), 139–147.
Knoche M., Peschel S., Hinz M., Bukovac M.J., 2000. Studies on water transport through the sweet cherry fruit surface: Characterizing conductance of the cuticular membrane using pericarp segments. Planta, 212, 127–135.
Knoche M., Beyer M., Peschel S., Oparlakov B., Bukovac M.J., 2004. Changes in strain and deposition of cuticle in developing sweet cherry fruit. Physiol. Plant., 120, 667–677.
Koch K., Neinhuis C., Ensikat H.J., Barthlott W., 2004. Self assembly of epicuticular waxes on living plant surfaces imaged by atomic force microscopy (AFM). J. Exp. Bot., 55, 711–718.
Konarska A., 2012. Differences in the fruit peel structures between two apple cultivars during storage. Acta Sci. Pol., Hort. Cult., 11(2), 105–116.
Konarska A., 2013. The structure of the fruit peel in two varieties of Malus domestica Borkh. (Rosaceae) before and after storage. Protoplasma, 250, 701–714.
Kruczyńska D., 2008. Jabłonie: nowe odmiany. Hortpress Warszawa.
Lattanzio V., Di-Venere D., Linsalata V., Bertolini P., Ippolito A., Salerno M., 2001. Low temperature metabolism of apple phenolics and quiescence of Phlyctaena vagabunda. J. Agric. Food Chem., 49, 5817–5821.
Lau O.L., Lane W.D., 1998. Harvest indices, storability, and poststorage refrigeration requirements of ‘Sunrise’ apple. HortSci., 33, 302–304.
Link S.O., Drake S.R., Thiede M.E., 2004. Prediction of apple firmness from mass loss and shrinkage. J. Food Quality, 27, 13–26.
Łata B., Trampczyńska A., Paczesna J., 2009. Cultivar variation in apple peel and whole fruit phenolic composition. Sci. Hortic., 121, 176–181.
Maguire K.M., Lang A., Banks N.H., Hall A., Hopcroft D., Benneti R., 1999. Relationship between water vapour permeance of apples and micro-cracking of the cuticle, Postharv. Biol. Technol., 17, 89–96.
Maguire K.M., Banks N.H., Lang A., Gordon I.L., 2000. Harvest date, cultivar, orchard and tree effects on water vapour permeance in apples. J. Am. Soc. Hort. Sci., 125, 100–104.
Mehrabani L.V., Hassanpouraghdam M.B., 2012. Developmental variation of phenolic compounds in fruit tissue of two apple cultivars. Acta Sci. Pol., Technol. Aliment., 11(3), 259–264.
Miller A.N., Walsh C.S., Cohen C.D., 1987. Measurement of indole-3-acetic acid in peach fruits (Prunus persica L. Batsch cv Redhaven) during development. Plant Physiol., 84, 491–494.
Miller R.H., 1984. The multiple epidermis-cuticle complex of Medlar fruit Mespilus germanica L. (Rosaceae). Ann. Bot., 53, 779–792.
Müller I., 2005. Relationship between preharvest soybean oil application and postharvest behavior apples. Dissertation, Washington State University.
Pieniążek S.A., 2000. Sadownictwo. PWRiL Warszawa.
Reed D.W., 1982. Wax alteration and extraction Turing electron microscopy preparation of leaf cuticles. In: The plant cuticle. Cultler, D.F., Alvin K.L., Price C.E., eds. Academic Press, London.
Rejman A., 1994. Pomologia. PWRiL Warszawa.
Reynolds E.S., 1963. The use of lead citrate at high pH as an electron-opaque stain for electron microscopy. J. Cell Biol., 17, 208–212.
Riederer M., Schreiber L., 1995. Waxes – the transport barriers of plant cuticles. In: Waxes: Chemistry, molecular biology and functions, Hamilton R.J (ed.). The Oily Press, Scotland, 131–156.
Roy S., Conway W.S., Watada A.E., Sams C.E., Erbe E.F., Wergin W.P., 1994. Heat treatment affects epicuticular wax structure and postharvest calcium uptake in ‘Golden Delicious’ apples. Hort. Sci., 29, 1056–1058.
Solovchenko A., Schmitz-Eiberger M.J., 2003. Significance of skin flavonoids for UV-B-protection in apple fruits. Exp. Bot., 54, 1977–1984.
Spurr A.R., 1969. A low-viscosity epoxy resin embedding medium for electron microscopy. J. Ultra. Res., 26, 31–43.
Veraverbake E.A., van Bruaene N., van Oostveldt P., Nicolaï B.M., 2001a. Non destructive analysis of the wax layer off apple (Malus domestica Borkh.) by means of confocal laser scanning microscopy. Planta, 213, 525–533.
Veraverbake E.A., Lammertyn J., Saevels S., Nicolaï B.M., 2001b. Changes in chemical wax composition of three different apple (Malus domestica Borkh.) cultivars during storage. Postharv. Biol. Technol., 23, 197–208.
Veraverbake E.A., Verboven P., van Oostveldt P., Nicolaï B.M., 2003a. Prediction of moisture loss across the cuticle of apple (Malus sylvestris subsp. Mitis (Wallr.)) during storage: part 1. Model development and determination of diffusion coefficients, Postharv. Biol. Technol., 30, 75–88.
Veraverbeke E.A., Verboven P., van Oostveldt P., Nicolaï B.M., 2003b. Prediction of moisture loss across the cuticle of apple (Malus sylvestris subsp. Mitis (Wallr.)) during storage: part 2. Model simulations and practical applications. Postharv. Biol. Technol., 30, 89–97.
Verboven P., Nemeth A., Abera M.K., Bongaers E., Daelemans D., Estrade P., Herremans E., Hertog M., Saeys W., Vanstreels E., Verlinden B., Leitner M., Nicolaï B., 2013. Optical coherence tomography visualizes microstructure of apple peel. Postharv. Biol. Technol., 78, 123–132.
Westwood M.N., 1995. Temperate zone pomology: Physiology and culture. (Third Edition). Timber Press, Oregon.
Zamorskyi V., 2007. The role of the anatomical structure of apple fruits as fresh cut produce. Acta Hort., 746, 509–512.
Agata Konarska
University of Life Sciences in Lublin
University of Life Sciences in Lublin
License
Articles are made available under the conditions CC BY 4.0 (until 2020 under the conditions CC BY-NC-ND 4.0).
Submission of the paper implies that it has not been published previously, that it is not under consideration for publication elsewhere.
The author signs a statement of the originality of the work, the contribution of individuals, and source of funding.
