Promotion of testa rupture during garden cress germination involves seed compartment-specific expression and activity of pectin methylesterases

Pectin methylesterase (PME) controls the methylesterification status of pectins and thereby determines the biophysical properties of plant cell walls, which are important for tissue growth and weakening processes. We demonstrate here that tissue-specific and spatiotemporal alterations in cell wall p...

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Main Authors: Scheler, Claudia, Weitbrecht, Karin, Pearce, Simon P., Hampstead, Anthony, Büttner-Mainik, Annette, Lee, Kieran J.D., Voegele, Antje, Oracz, Krystyna, Dekkers, Bas J.W., Wang, Xiaofeng, Wood, Andrew T.A., Bentsink, Leónie, King, John R., Knox, J. Paul, Holdsworth, Michael J., Müller, Kerstin, Leubner-Metzger, Gerhard
Format: Article
Published: American Society of Plant Biologists 2015
Online Access:https://eprints.nottingham.ac.uk/30253/
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author Scheler, Claudia
Weitbrecht, Karin
Pearce, Simon P.
Hampstead, Anthony
Büttner-Mainik, Annette
Lee, Kieran J.D.
Voegele, Antje
Oracz, Krystyna
Dekkers, Bas J.W.
Wang, Xiaofeng
Wood, Andrew T.A.
Bentsink, Leónie
King, John R.
Knox, J. Paul
Holdsworth, Michael J.
Müller, Kerstin
Leubner-Metzger, Gerhard
author_facet Scheler, Claudia
Weitbrecht, Karin
Pearce, Simon P.
Hampstead, Anthony
Büttner-Mainik, Annette
Lee, Kieran J.D.
Voegele, Antje
Oracz, Krystyna
Dekkers, Bas J.W.
Wang, Xiaofeng
Wood, Andrew T.A.
Bentsink, Leónie
King, John R.
Knox, J. Paul
Holdsworth, Michael J.
Müller, Kerstin
Leubner-Metzger, Gerhard
author_sort Scheler, Claudia
building Nottingham Research Data Repository
collection Online Access
description Pectin methylesterase (PME) controls the methylesterification status of pectins and thereby determines the biophysical properties of plant cell walls, which are important for tissue growth and weakening processes. We demonstrate here that tissue-specific and spatiotemporal alterations in cell wall pectin methylesterification occur during the germination of garden cress (Lepidium sativum). These cell wall changes are associated with characteristic expression patterns of PME genes and resultant enzyme activities in the key seed compartments CAP (micropylar endosperm) and RAD (radicle plus lower hypocotyl). Transcriptome and quantitative real-time reverse transcription-polymerase chain reaction analysis as well as PME enzyme activity measurements of separated seed compartments, including CAP and RAD, revealed distinct phases during germination. These were associated with hormonal and compartment-specific regulation of PME group 1, PME group 2, and PME inhibitor transcript expression and total PME activity. The regulatory patterns indicated a role for PME activity in testa rupture (TR). Consistent with a role for cell wall pectin methylesterification in TR, treatment of seeds with PME resulted in enhanced testa permeability and promoted TR. Mathematical modeling of transcript expression changes in germinating garden cress and Arabidopsis (Arabidopsis thaliana) seeds suggested that group 2 PMEs make a major contribution to the overall PME activity rather than acting as PME inhibitors. It is concluded that regulated changes in the degree of pectin methylesterification through CAP- and RAD-specific PME and PME inhibitor expression play a crucial role during Brassicaceae seed germination.
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institution University of Nottingham Malaysia Campus
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publishDate 2015
publisher American Society of Plant Biologists
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spelling nottingham-302532020-05-04T20:10:21Z https://eprints.nottingham.ac.uk/30253/ Promotion of testa rupture during garden cress germination involves seed compartment-specific expression and activity of pectin methylesterases Scheler, Claudia Weitbrecht, Karin Pearce, Simon P. Hampstead, Anthony Büttner-Mainik, Annette Lee, Kieran J.D. Voegele, Antje Oracz, Krystyna Dekkers, Bas J.W. Wang, Xiaofeng Wood, Andrew T.A. Bentsink, Leónie King, John R. Knox, J. Paul Holdsworth, Michael J. Müller, Kerstin Leubner-Metzger, Gerhard Pectin methylesterase (PME) controls the methylesterification status of pectins and thereby determines the biophysical properties of plant cell walls, which are important for tissue growth and weakening processes. We demonstrate here that tissue-specific and spatiotemporal alterations in cell wall pectin methylesterification occur during the germination of garden cress (Lepidium sativum). These cell wall changes are associated with characteristic expression patterns of PME genes and resultant enzyme activities in the key seed compartments CAP (micropylar endosperm) and RAD (radicle plus lower hypocotyl). Transcriptome and quantitative real-time reverse transcription-polymerase chain reaction analysis as well as PME enzyme activity measurements of separated seed compartments, including CAP and RAD, revealed distinct phases during germination. These were associated with hormonal and compartment-specific regulation of PME group 1, PME group 2, and PME inhibitor transcript expression and total PME activity. The regulatory patterns indicated a role for PME activity in testa rupture (TR). Consistent with a role for cell wall pectin methylesterification in TR, treatment of seeds with PME resulted in enhanced testa permeability and promoted TR. Mathematical modeling of transcript expression changes in germinating garden cress and Arabidopsis (Arabidopsis thaliana) seeds suggested that group 2 PMEs make a major contribution to the overall PME activity rather than acting as PME inhibitors. It is concluded that regulated changes in the degree of pectin methylesterification through CAP- and RAD-specific PME and PME inhibitor expression play a crucial role during Brassicaceae seed germination. American Society of Plant Biologists 2015-01 Article PeerReviewed Scheler, Claudia, Weitbrecht, Karin, Pearce, Simon P., Hampstead, Anthony, Büttner-Mainik, Annette, Lee, Kieran J.D., Voegele, Antje, Oracz, Krystyna, Dekkers, Bas J.W., Wang, Xiaofeng, Wood, Andrew T.A., Bentsink, Leónie, King, John R., Knox, J. Paul, Holdsworth, Michael J., Müller, Kerstin and Leubner-Metzger, Gerhard (2015) Promotion of testa rupture during garden cress germination involves seed compartment-specific expression and activity of pectin methylesterases. Plant Physiology, 167 (1). pp. 200-215. ISSN 0032-0889 http://www.plantphysiol.org/content/167/1/200 doi:10.​1104/​pp.​114.​247429 doi:10.​1104/​pp.​114.​247429
spellingShingle Scheler, Claudia
Weitbrecht, Karin
Pearce, Simon P.
Hampstead, Anthony
Büttner-Mainik, Annette
Lee, Kieran J.D.
Voegele, Antje
Oracz, Krystyna
Dekkers, Bas J.W.
Wang, Xiaofeng
Wood, Andrew T.A.
Bentsink, Leónie
King, John R.
Knox, J. Paul
Holdsworth, Michael J.
Müller, Kerstin
Leubner-Metzger, Gerhard
Promotion of testa rupture during garden cress germination involves seed compartment-specific expression and activity of pectin methylesterases
title Promotion of testa rupture during garden cress germination involves seed compartment-specific expression and activity of pectin methylesterases
title_full Promotion of testa rupture during garden cress germination involves seed compartment-specific expression and activity of pectin methylesterases
title_fullStr Promotion of testa rupture during garden cress germination involves seed compartment-specific expression and activity of pectin methylesterases
title_full_unstemmed Promotion of testa rupture during garden cress germination involves seed compartment-specific expression and activity of pectin methylesterases
title_short Promotion of testa rupture during garden cress germination involves seed compartment-specific expression and activity of pectin methylesterases
title_sort promotion of testa rupture during garden cress germination involves seed compartment-specific expression and activity of pectin methylesterases
url https://eprints.nottingham.ac.uk/30253/
https://eprints.nottingham.ac.uk/30253/
https://eprints.nottingham.ac.uk/30253/