The auxin-regulated CrRLK1L kinase ERULUS controls cell wall composition during root hair tip growth

Root hairs facilitate a plant’s ability to acquire soil anchorage and nutrients. Root hair growth is regulated by the plant hormone auxin and dependent on localized synthesis, secretion and modification of the root hair tip cell wall. However, the exact well wall regulators in root hairs controlled...

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Main Authors: Schoenaers, Sébastjen, Balcerowicz, Daria, Breen, Gordon, Hill, Kristine, Zdanio, Malgorzata, Mouille, Grégory, Holman, Tara J., Oh, Jaesung, Wilson, Michael H., Nikonorova, Natalia, Vu, Lam Dai, De Smet, Ive, Swarup, Ranjan, De Vos, Winnok H., Pintelon, Isabel, Adriaensen, Dirk, Grierson, Claire, Bennett, Malcolm J., Vissenberg, Kris
Format: Article
Published: Elsevier (Cell Press) 2018
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Online Access:https://eprints.nottingham.ac.uk/49905/
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author Schoenaers, Sébastjen
Balcerowicz, Daria
Breen, Gordon
Hill, Kristine
Zdanio, Malgorzata
Mouille, Grégory
Holman, Tara J.
Oh, Jaesung
Wilson, Michael H.
Nikonorova, Natalia
Vu, Lam Dai
De Smet, Ive
Swarup, Ranjan
De Vos, Winnok H.
Pintelon, Isabel
Adriaensen, Dirk
Grierson, Claire
Bennett, Malcolm J.
Vissenberg, Kris
author_facet Schoenaers, Sébastjen
Balcerowicz, Daria
Breen, Gordon
Hill, Kristine
Zdanio, Malgorzata
Mouille, Grégory
Holman, Tara J.
Oh, Jaesung
Wilson, Michael H.
Nikonorova, Natalia
Vu, Lam Dai
De Smet, Ive
Swarup, Ranjan
De Vos, Winnok H.
Pintelon, Isabel
Adriaensen, Dirk
Grierson, Claire
Bennett, Malcolm J.
Vissenberg, Kris
author_sort Schoenaers, Sébastjen
building Nottingham Research Data Repository
collection Online Access
description Root hairs facilitate a plant’s ability to acquire soil anchorage and nutrients. Root hair growth is regulated by the plant hormone auxin and dependent on localized synthesis, secretion and modification of the root hair tip cell wall. However, the exact well wall regulators in root hairs controlled by auxin have yet to be determined. In this study, we describe the characterization of ERULUS (ERU), an auxin-induced Arabidopsis receptor-like kinase whose expression is directly regulated by ARF7 and ARF19 transcription factors. ERU belongs to the Catharanthus roseus RECEPTOR-LIKE KINASE 1-LIKE (CrRLK1L) subfamily of putative cell wall sensor proteins. Imaging of a fluorescent fusion protein revealed that ERU is localized to the apical root hair plasma membrane. ERU regulates cell wall composition in root hairs and modulates pectin dynamics through negative control of pectin methylesterase (PME) activity. Mutant eru (-/-) root hairs accumulate de-esterified homogalacturonan and exhibit aberrant pectin Ca²⁺ binding site oscillations and increased PME activity. Up to 80% of the eru root hair phenotype is rescued by pharmacological supplementation with a PME inhibiting catechin extract. ERU transcription is altered in specific cell wall-related root hair mutants, suggesting it is a target for feedback regulation. Loss of ERU alters the phosphorylation status of FERONIA and H⁺-ATPases 1/2, regulators of apoplastic pH. Furthermore, H⁺-ATPases 1/2 and ERU are differentially phosphorylated in response to auxin. We conclude that ERULUS is a key auxin-controlled regulator of cell wall composition and pectin dynamics during root hair tip growth.
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spelling nottingham-499052020-05-04T19:33:21Z https://eprints.nottingham.ac.uk/49905/ The auxin-regulated CrRLK1L kinase ERULUS controls cell wall composition during root hair tip growth Schoenaers, Sébastjen Balcerowicz, Daria Breen, Gordon Hill, Kristine Zdanio, Malgorzata Mouille, Grégory Holman, Tara J. Oh, Jaesung Wilson, Michael H. Nikonorova, Natalia Vu, Lam Dai De Smet, Ive Swarup, Ranjan De Vos, Winnok H. Pintelon, Isabel Adriaensen, Dirk Grierson, Claire Bennett, Malcolm J. Vissenberg, Kris Root hairs facilitate a plant’s ability to acquire soil anchorage and nutrients. Root hair growth is regulated by the plant hormone auxin and dependent on localized synthesis, secretion and modification of the root hair tip cell wall. However, the exact well wall regulators in root hairs controlled by auxin have yet to be determined. In this study, we describe the characterization of ERULUS (ERU), an auxin-induced Arabidopsis receptor-like kinase whose expression is directly regulated by ARF7 and ARF19 transcription factors. ERU belongs to the Catharanthus roseus RECEPTOR-LIKE KINASE 1-LIKE (CrRLK1L) subfamily of putative cell wall sensor proteins. Imaging of a fluorescent fusion protein revealed that ERU is localized to the apical root hair plasma membrane. ERU regulates cell wall composition in root hairs and modulates pectin dynamics through negative control of pectin methylesterase (PME) activity. Mutant eru (-/-) root hairs accumulate de-esterified homogalacturonan and exhibit aberrant pectin Ca²⁺ binding site oscillations and increased PME activity. Up to 80% of the eru root hair phenotype is rescued by pharmacological supplementation with a PME inhibiting catechin extract. ERU transcription is altered in specific cell wall-related root hair mutants, suggesting it is a target for feedback regulation. Loss of ERU alters the phosphorylation status of FERONIA and H⁺-ATPases 1/2, regulators of apoplastic pH. Furthermore, H⁺-ATPases 1/2 and ERU are differentially phosphorylated in response to auxin. We conclude that ERULUS is a key auxin-controlled regulator of cell wall composition and pectin dynamics during root hair tip growth. Elsevier (Cell Press) 2018-02-22 Article PeerReviewed Schoenaers, Sébastjen, Balcerowicz, Daria, Breen, Gordon, Hill, Kristine, Zdanio, Malgorzata, Mouille, Grégory, Holman, Tara J., Oh, Jaesung, Wilson, Michael H., Nikonorova, Natalia, Vu, Lam Dai, De Smet, Ive, Swarup, Ranjan, De Vos, Winnok H., Pintelon, Isabel, Adriaensen, Dirk, Grierson, Claire, Bennett, Malcolm J. and Vissenberg, Kris (2018) The auxin-regulated CrRLK1L kinase ERULUS controls cell wall composition during root hair tip growth. Current Biology, 28 (5). pp. 722-732. ISSN 1879-0445 auxin kinase root hair cell wall pectin tip growth Arabidopsis CrRLK1L AUXIN RESPONSE FACTOR FERONIA AHA2 https://www.sciencedirect.com/science/article/pii/S0960982218300836 doi:10.1016/j.cub.2018.01.050 doi:10.1016/j.cub.2018.01.050
spellingShingle auxin
kinase
root hair
cell wall
pectin
tip growth
Arabidopsis
CrRLK1L
AUXIN RESPONSE FACTOR
FERONIA
AHA2
Schoenaers, Sébastjen
Balcerowicz, Daria
Breen, Gordon
Hill, Kristine
Zdanio, Malgorzata
Mouille, Grégory
Holman, Tara J.
Oh, Jaesung
Wilson, Michael H.
Nikonorova, Natalia
Vu, Lam Dai
De Smet, Ive
Swarup, Ranjan
De Vos, Winnok H.
Pintelon, Isabel
Adriaensen, Dirk
Grierson, Claire
Bennett, Malcolm J.
Vissenberg, Kris
The auxin-regulated CrRLK1L kinase ERULUS controls cell wall composition during root hair tip growth
title The auxin-regulated CrRLK1L kinase ERULUS controls cell wall composition during root hair tip growth
title_full The auxin-regulated CrRLK1L kinase ERULUS controls cell wall composition during root hair tip growth
title_fullStr The auxin-regulated CrRLK1L kinase ERULUS controls cell wall composition during root hair tip growth
title_full_unstemmed The auxin-regulated CrRLK1L kinase ERULUS controls cell wall composition during root hair tip growth
title_short The auxin-regulated CrRLK1L kinase ERULUS controls cell wall composition during root hair tip growth
title_sort auxin-regulated crrlk1l kinase erulus controls cell wall composition during root hair tip growth
topic auxin
kinase
root hair
cell wall
pectin
tip growth
Arabidopsis
CrRLK1L
AUXIN RESPONSE FACTOR
FERONIA
AHA2
url https://eprints.nottingham.ac.uk/49905/
https://eprints.nottingham.ac.uk/49905/
https://eprints.nottingham.ac.uk/49905/