Constitutive expression of apple endo-POLYGALACTURONASE1 in fruit induces early maturation, alters skin structure and accelerates softening

verfasst von: Kularajathevan Gunaseelan, Roswitha Schröder, Ria Rebstock, Annu S. Ninan, Cecilia Deng, Bishnu P. Khanal, Laurie Favre, Sumathi Tomes, Monica A. Dragulescu, Erin M. O'Donoghue, Ian C. Hallett, Robert J. Schaffer, Moritz Knoche, David A. Brummell, Ross G. Atkinson
Abstract: During fruit ripening, polygalacturonases (PGs) are key contributors to the softening process in many species. Apple is a crisp fruit that normally exhibits only minor changes to cell walls and limited fruit softening. Here, we explore the effects of PG overexpression during fruit development using transgenic apple lines overexpressing the ripening-related endo-POLYGALACTURONASE1 gene. MdPG1-overexpressing (PGox) fruit displayed early maturation/ripening with black seeds, conversion of starch to sugars and ethylene production occurring by 80 days after pollination (DAP). PGox fruit exhibited a striking, white-skinned phenotype that was evident from 60 DAP and most likely resulted from increased air spaces and separation of cells in the hypodermis due to degradation of the middle lamellae. Irregularities in the integrity of the epidermis and cuticle were also observed. By 120 DAP, PGox fruit cracked and showed lenticel-associated russeting. Increased cuticular permeability was associated with microcracks in the cuticle around lenticels and was correlated with reduced cortical firmness at all time points and extensive post-harvest water loss from the fruit, resulting in premature shrivelling. Transcriptomic analysis suggested that early maturation was associated with upregulation of genes involved in stress responses, and overexpression of MdPG1 also altered the expression of genes involved in cell wall metabolism (e.g. β-galactosidase, MD15G1221000) and ethylene biosynthesis (e.g. ACC synthase, MD14G1111500). The results show that upregulation of PG not only has dramatic effects on the structure of the fruit outer cell layers, indirectly affecting water status and turgor, but also has unexpected consequences for fruit development.
Organisationseinheit(en): Institut für Gartenbauliche Produktionssysteme
Externe Organisation(en): New Zealand Institute for Plant & Food Research Limited (Plant & Food Research)
Typ: Artikel
Journal: Plant Journal
Band: 117
Seiten: 1413-1431
Anzahl der Seiten: 19
ISSN: 0960-7412
Publikationsdatum: 26.02.2024
Publikationsstatus: Veröffentlicht
Peer-reviewed: Ja
ASJC Scopus Sachgebiete: Genetik, Pflanzenkunde, Zellbiologie
Elektronische Version(en): https://doi.org/10.1111/tpj.16571 (Zugang: Offen)

BibTeX

@article{8be064915f6f4cdb95be79a39ae1b25f,
title = "Constitutive expression of apple endo-POLYGALACTURONASE1 in fruit induces early maturation, alters skin structure and accelerates softening",
abstract = "During fruit ripening, polygalacturonases (PGs) are key contributors to the softening process in many species. Apple is a crisp fruit that normally exhibits only minor changes to cell walls and limited fruit softening. Here, we explore the effects of PG overexpression during fruit development using transgenic apple lines overexpressing the ripening-related endo-POLYGALACTURONASE1 gene. MdPG1-overexpressing (PGox) fruit displayed early maturation/ripening with black seeds, conversion of starch to sugars and ethylene production occurring by 80 days after pollination (DAP). PGox fruit exhibited a striking, white-skinned phenotype that was evident from 60 DAP and most likely resulted from increased air spaces and separation of cells in the hypodermis due to degradation of the middle lamellae. Irregularities in the integrity of the epidermis and cuticle were also observed. By 120 DAP, PGox fruit cracked and showed lenticel-associated russeting. Increased cuticular permeability was associated with microcracks in the cuticle around lenticels and was correlated with reduced cortical firmness at all time points and extensive post-harvest water loss from the fruit, resulting in premature shrivelling. Transcriptomic analysis suggested that early maturation was associated with upregulation of genes involved in stress responses, and overexpression of MdPG1 also altered the expression of genes involved in cell wall metabolism (e.g. β-galactosidase, MD15G1221000) and ethylene biosynthesis (e.g. ACC synthase, MD14G1111500). The results show that upregulation of PG not only has dramatic effects on the structure of the fruit outer cell layers, indirectly affecting water status and turgor, but also has unexpected consequences for fruit development.",
keywords = "cell separation, cell wall, Malus domestica, pectin, transcriptomic analysis, transpiration",
author = "Kularajathevan Gunaseelan and Roswitha Schr{\"o}der and Ria Rebstock and Ninan, {Annu S.} and Cecilia Deng and Khanal, {Bishnu P.} and Laurie Favre and Sumathi Tomes and Dragulescu, {Monica A.} and O'Donoghue, {Erin M.} and Hallett, {Ian C.} and Schaffer, {Robert J.} and Moritz Knoche and Brummell, {David A.} and Atkinson, {Ross G.}",
note = "Funding Information: KG obtained the physiological data. KG, RS, AN and EOD carried out biochemical, molecular and cell wall analyses. CD and LF analysed the transcriptomic data. ST and MD made and cared for the transgenic plants. BK and MK conducted transpiration assays. RR and IH undertook the immunolabelling and microscopy. RS, RJS, MK, DB and RA designed the research, analysed the data and wrote the paper. This work was funded by the New Zealand Ministry of Business, Innovation and Employment and internal Plant & Food Research funding. ",
year = "2024",
month = feb,
day = "26",
doi = "10.1111/tpj.16571",
language = "English",
volume = "117",
pages = "1413--1431",
journal = "Plant Journal",
issn = "0960-7412",
publisher = "Wiley-Blackwell Publishing Ltd",
number = "5",
}