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      Cell separation in kiwifruit without development of a specialised detachment zone

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          Abstract

          Background

          Unlike in abscission or dehiscence, fruit of kiwifruit Actinidia eriantha develop the ability for peel detachment when they are ripe and soft in the absence of a morphologically identifiable abscission zone. Two closely-related genotypes with contrasting detachment behaviour have been identified. The ‘good-peeling’ genotype has detachment with clean debonding of cells, and a peel tissue that does not tear. The ‘poor-peeling’ genotype has poor detachability, with cells that rupture upon debonding, and peel tissue that fragments easily.

          Results

          Structural studies indicated that peel detachability in both genotypes occurred in the outer pericarp beneath the hypodermis. Immunolabelling showed differences in methylesterification of pectin, where the interface of labelling coincided with the location of detachment in the good-peeling genotype, whereas in the poor-peeling genotype, no such interface existed. This zone of difference in methylesterification was enhanced by differential cell wall changes between the peel and outer pericarp tissue. Although both genotypes expressed two polygalacturonase genes, no enzyme activity was detected in the good-peeling genotype, suggesting limited pectin breakdown, keeping cell walls strong without tearing or fragmentation of the peel and flesh upon detachment. Differences in location and amounts of wall-stiffening galactan in the peel of the good-peeling genotype possibly contributed to this phenotype. Hemicellulose-acting transglycosylases were more active in the good-peeling genotype, suggesting an influence on peel flexibility by remodelling their substrates during development of detachability. High xyloglucanase activity in the peel of the good-peeling genotype may contribute by having a strengthening effect on the cellulose-xyloglucan network.

          Conclusions

          In fruit of A. eriantha, peel detachability is due to the establishment of a zone of discontinuity created by differential cell wall changes in peel and outer pericarp tissues that lead to changes in mechanical properties of the peel. During ripening, the peel becomes flexible and the cells continue to adhere strongly to each other, preventing breakage, whereas the underlying outer pericarp loses cell wall strength as softening proceeds. Together these results reveal a novel and interesting mechanism for enabling cell separation.

          Electronic supplementary material

          The online version of this article (doi:10.1186/s12870-017-1034-2) contains supplementary material, which is available to authorized users.

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          Most cited references51

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          A method for the analysis of sugars in plant cell-wall polysaccharides by gas-liquid chromatography

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            Modulation of the degree and pattern of methyl-esterification of pectic homogalacturonan in plant cell walls. Implications for pectin methyl esterase action, matrix properties, and cell adhesion.

            Homogalacturonan (HG) is a multifunctional pectic polysaccharide of the primary cell wall matrix of all land plants. HG is thought to be deposited in cell walls in a highly methyl-esterified form but can be subsequently de-esterified by wall-based pectin methyl esterases (PMEs) that have the capacity to remove methyl ester groups from HG. Plant PMEs typically occur in multigene families/isoforms, but the precise details of the functions of PMEs are far from clear. Most are thought to act in a processive or blockwise fashion resulting in domains of contiguous de-esterified galacturonic acid residues. Such de-esterified blocks of HG can be cross-linked by calcium resulting in gel formation and can contribute to intercellular adhesion. We demonstrate that, in addition to blockwise de-esterification, HG with a non-blockwise distribution of methyl esters is also an abundant feature of HG in primary plant cell walls. A partially methyl-esterified epitope of HG that is generated in greatest abundance by non-blockwise de-esterification is spatially regulated within the cell wall matrix and occurs at points of cell separation at intercellular spaces in parenchymatous tissues of pea and other angiosperms. Analysis of the properties of calcium-mediated gels formed from pectins containing HG domains with differing degrees and patterns of methyl-esterification indicated that HG with a non-blockwise pattern of methyl ester group distribution is likely to contribute distinct mechanical and porosity properties to the cell wall matrix. These findings have important implications for our understanding of both the action of pectin methyl esterases on matrix properties and mechanisms of intercellular adhesion and its loss in plants.
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              Abscission, dehiscence, and other cell separation processes.

              Cell separation is a critical process that takes place throughout the life cycle of a plant. It enables roots to emerge from germinating seeds, cotyledons, and leaves to expand, anthers to dehisce, fruit to ripen, and organs to be shed. The focus of this review is to examine how processes such as abscission and dehiscence are regulated and the ways new research strategies are helping us to understand the mechanisms involved in bringing about a reduction in cell-to-cell adhesion. The opportunities for using this information to manipulate cell separation for the benefit of agriculture and horticulture are evaluated.
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                Author and article information

                Contributors
                roneel.prakash@plantandfood.co.nz
                hallett@plantandfood.co.nz
                sallyfwong@gmail.com
                sarah.johnston@plantandfood.co.nz
                erin.odonoghue@plantandfood.co.nz
                peter.mcatee@plantandfood.co.nz
                alan.seal@plantandfood.co.nz
                ross.atkinson@plantandfood.co.nz
                rosie.schroeder@plantandfood.co.nz
                Journal
                BMC Plant Biol
                BMC Plant Biol
                BMC Plant Biology
                BioMed Central (London )
                1471-2229
                10 May 2017
                10 May 2017
                2017
                : 17
                : 86
                Affiliations
                [1 ]GRID grid.27859.31, , The New Zealand Institute for Plant & Food Research Limited (PFR), Mount Albert Research Centre, ; Private Bag 92169, Auckland, 1142 New Zealand
                [2 ]PFR, Mount Albert Research Centre, Private Bag 92169, Auckland, 1142 New Zealand
                [3 ]PFR, Hawke’s Bay Research Centre, Cnr Crosses and St George’s Roads, Havelock North, 4130 New Zealand
                [4 ]PFR, Food Industry Science Centre, Fitzherbert Science Centre, Batchelar Road, Palmerston North, 4474 New Zealand
                [5 ]PFR, Te Puke Research Centre, 412 No 1 Road RD 2, Te Puke, 3182 New Zealand
                Author information
                http://orcid.org/0000-0003-1554-2606
                Article
                1034
                10.1186/s12870-017-1034-2
                5424339
                28486974
                b8dcce87-db79-470a-a254-936efa403132
                © The Author(s). 2017

                Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

                History
                : 7 February 2017
                : 20 April 2017
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/501100003524, Ministry of Business, Innovation and Employment;
                Categories
                Research Article
                Custom metadata
                © The Author(s) 2017

                Plant science & Botany
                cell wall,detachment,kiwifruit,peeling,polygalacturonase,transglycosylase
                Plant science & Botany
                cell wall, detachment, kiwifruit, peeling, polygalacturonase, transglycosylase

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