Growth strains cause vascular browning and cavities in ´Nicoter´ apples

Research output: Contribution to journalArticleResearchpeer review

Authors

  • Eckhard Grimm
  • Merle Peters
  • Julian Kaltenbach
  • Chu Zhang
  • Moritz Knoche
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Original languageEnglish
Article numbere0289013
JournalPLOS ONE
Volume18
Issue number7
Publication statusPublished - 20 Jul 2023

Abstract

‘Nicoter’ apples (Malus × domestica Borkh.) occasionally develop a disorder referred to as vascular browning. Symptomatic fruit are perceived as being of low quality. The objective was to identify the mechanistic basis of this disorder. The frequency of symptomatic ‘Nicoter’ apples differed between growing sites and increased with delayed harvest. Typical symptoms are tissue browning and cavities in the ray parenchyma of the calyx region, and occasionally also of the stem end. Cavity size is positively correlated with the extent of tissue browning. Cavities were oriented radially in the direction of the bisecting line between the radii connecting the calyx/pedicel axis to the sepal and petal bundles. Microscopy revealed cell wall fragments in the cavities indicating physical rupture of cell walls. Immunolabelling of cell wall epitopes offered no evidence for separation of cells along cell walls. The growth pattern in ‘Nicoter’ is similar to that in its parents ‘Gala’ and ‘Braeburn’. Allometric analyses revealed no differences in growth in fruit length among the three cultivars. However, the allometric analyses of growth in diameter revealed a marked increase in the distance between the surface of the calyx cavity and the vascular bundle in ‘Nicoter’, that was absent in ‘Braeburn’ and ‘Gala’. This increase displaced the petal bundles in the ray parenchyma outwards and subjected the tissue between the petal and sepal bundles to tangential strain. Rupture of cells results in tissue browning and cavity formation. A timely harvest is a practicable countermeasure for decreasing the incidence of vascular browning.

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Growth strains cause vascular browning and cavities in ´Nicoter´ apples. / Grimm, Eckhard; Peters, Merle; Kaltenbach, Julian et al.
In: PLOS ONE, Vol. 18, No. 7 , e0289013, 20.07.2023.

Research output: Contribution to journalArticleResearchpeer review

Grimm, E, Peters, M, Kaltenbach, J, Zhang, C & Knoche, M 2023, 'Growth strains cause vascular browning and cavities in ´Nicoter´ apples', PLOS ONE, vol. 18, no. 7 , e0289013. https://doi.org/10.1371/journal.pone.0289013
Grimm, E., Peters, M., Kaltenbach, J., Zhang, C., & Knoche, M. (2023). Growth strains cause vascular browning and cavities in ´Nicoter´ apples. PLOS ONE, 18(7 ), Article e0289013. https://doi.org/10.1371/journal.pone.0289013
Grimm E, Peters M, Kaltenbach J, Zhang C, Knoche M. Growth strains cause vascular browning and cavities in ´Nicoter´ apples. PLOS ONE. 2023 Jul 20;18(7 ):e0289013. doi: 10.1371/journal.pone.0289013
Grimm, Eckhard ; Peters, Merle ; Kaltenbach, Julian et al. / Growth strains cause vascular browning and cavities in ´Nicoter´ apples. In: PLOS ONE. 2023 ; Vol. 18, No. 7 .
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title = "Growth strains cause vascular browning and cavities in ´Nicoter´ apples",
abstract = "{\textquoteleft}Nicoter{\textquoteright} apples (Malus × domestica Borkh.) occasionally develop a disorder referred to as vascular browning. Symptomatic fruit are perceived as being of low quality. The objective was to identify the mechanistic basis of this disorder. The frequency of symptomatic {\textquoteleft}Nicoter{\textquoteright} apples differed between growing sites and increased with delayed harvest. Typical symptoms are tissue browning and cavities in the ray parenchyma of the calyx region, and occasionally also of the stem end. Cavity size is positively correlated with the extent of tissue browning. Cavities were oriented radially in the direction of the bisecting line between the radii connecting the calyx/pedicel axis to the sepal and petal bundles. Microscopy revealed cell wall fragments in the cavities indicating physical rupture of cell walls. Immunolabelling of cell wall epitopes offered no evidence for separation of cells along cell walls. The growth pattern in {\textquoteleft}Nicoter{\textquoteright} is similar to that in its parents {\textquoteleft}Gala{\textquoteright} and {\textquoteleft}Braeburn{\textquoteright}. Allometric analyses revealed no differences in growth in fruit length among the three cultivars. However, the allometric analyses of growth in diameter revealed a marked increase in the distance between the surface of the calyx cavity and the vascular bundle in {\textquoteleft}Nicoter{\textquoteright}, that was absent in {\textquoteleft}Braeburn{\textquoteright} and {\textquoteleft}Gala{\textquoteright}. This increase displaced the petal bundles in the ray parenchyma outwards and subjected the tissue between the petal and sepal bundles to tangential strain. Rupture of cells results in tissue browning and cavity formation. A timely harvest is a practicable countermeasure for decreasing the incidence of vascular browning.",
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note = "Funding Information: We thank Dr. Paul Knox, University of Leeds, UK for helpful comments on technical aspects of immunolabeling of cell walls in fleshy fruit and the generous gift of antibodies. We thank Dr. Alexander Lang for useful comments on an earlier version of this manuscript and Heike, Karl Walter and Martin Br{\"u}ggenwirth for the gift of fruit. ",
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AU - Grimm, Eckhard

AU - Peters, Merle

AU - Kaltenbach, Julian

AU - Zhang, Chu

AU - Knoche, Moritz

N1 - Funding Information: We thank Dr. Paul Knox, University of Leeds, UK for helpful comments on technical aspects of immunolabeling of cell walls in fleshy fruit and the generous gift of antibodies. We thank Dr. Alexander Lang for useful comments on an earlier version of this manuscript and Heike, Karl Walter and Martin Brüggenwirth for the gift of fruit.

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N2 - ‘Nicoter’ apples (Malus × domestica Borkh.) occasionally develop a disorder referred to as vascular browning. Symptomatic fruit are perceived as being of low quality. The objective was to identify the mechanistic basis of this disorder. The frequency of symptomatic ‘Nicoter’ apples differed between growing sites and increased with delayed harvest. Typical symptoms are tissue browning and cavities in the ray parenchyma of the calyx region, and occasionally also of the stem end. Cavity size is positively correlated with the extent of tissue browning. Cavities were oriented radially in the direction of the bisecting line between the radii connecting the calyx/pedicel axis to the sepal and petal bundles. Microscopy revealed cell wall fragments in the cavities indicating physical rupture of cell walls. Immunolabelling of cell wall epitopes offered no evidence for separation of cells along cell walls. The growth pattern in ‘Nicoter’ is similar to that in its parents ‘Gala’ and ‘Braeburn’. Allometric analyses revealed no differences in growth in fruit length among the three cultivars. However, the allometric analyses of growth in diameter revealed a marked increase in the distance between the surface of the calyx cavity and the vascular bundle in ‘Nicoter’, that was absent in ‘Braeburn’ and ‘Gala’. This increase displaced the petal bundles in the ray parenchyma outwards and subjected the tissue between the petal and sepal bundles to tangential strain. Rupture of cells results in tissue browning and cavity formation. A timely harvest is a practicable countermeasure for decreasing the incidence of vascular browning.

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