The Auxin-Regulated CrRLK1L Kinase ERULUS Controls Cell Wall Composition during Root Hair Tip Growth

Sébastjen Schoenaers; Daria Balcerowicz; Gordon Breen; Kristine Hill; Malgorzata Zdanio; Grégory Mouille; Tara J. Holman; Jaesung Oh; Michael H. Wilson; Natalia Nikonorova; Lam Dai Vu; Ive De Smet; Ranjan Swarup; Winnok H. De Vos; Isabel Pintelon; Dirk Adriaensen; Claire Grierson; Malcolm J. Bennett; Kris Vissenberg

doi:10.1016/j.cub.2018.01.050

The Auxin-Regulated CrRLK1L Kinase ERULUS Controls Cell Wall Composition during Root Hair Tip Growth

Sébastjen Schoenaers, Daria Balcerowicz, Gordon Breen, Kristine Hill, Malgorzata Zdanio, Grégory Mouille, Tara J. Holman, Jaesung Oh, Michael H. Wilson, Natalia Nikonorova, Lam Dai Vu, Ive De Smet, Ranjan Swarup, Winnok H. De Vos, Isabel Pintelon, Dirk Adriaensen, Claire Grierson, Malcolm J. Bennett, Kris Vissenberg^*

^*Corresponding author for this work

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Abstract

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 cell 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 that 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. Root hair growth increases root surface area for nutrient uptake. Schoenaers et al. report that auxin regulates the receptor-like kinase ERULUS, which localizes to the apical root hair plasma membrane, where it controls cell wall composition through pectin methylesterases and phosphorylation of cell-elongation regulators FERONIA and H⁺-ATPase 1/2.

Original language	English
Pages (from-to)	722-732.e6
Number of pages	11
Journal	Current Biology
Volume	28
Issue number	5
Early online date	22 Feb 2018
DOIs	https://doi.org/10.1016/j.cub.2018.01.050
Publication status	Published - 5 Mar 2018

Keywords

Arabidopsis
auxin
AUXIN RESPONSE FACTOR
cell wall
CrRLK1L
FERONIA
kinase
pectin
root hair
tip growth

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Accepted author manuscript, 8.5 MBLicence: CC BY-NC-ND

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Schoenaers, S., Balcerowicz, D., Breen, G., Hill, K., Zdanio, M., Mouille, G., Holman, T. J., Oh, J., Wilson, M. H., Nikonorova, N., Vu, L. D., De Smet, I., Swarup, R., De Vos, W. H., Pintelon, I., Adriaensen, D., Grierson, C., Bennett, M. J., & Vissenberg, K. (2018). The Auxin-Regulated CrRLK1L Kinase ERULUS Controls Cell Wall Composition during Root Hair Tip Growth. Current Biology, 28(5), 722-732.e6. https://doi.org/10.1016/j.cub.2018.01.050

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title = "The Auxin-Regulated CrRLK1L Kinase ERULUS Controls Cell Wall Composition during Root Hair Tip Growth",

abstract = "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 cell 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 that 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. Root hair growth increases root surface area for nutrient uptake. Schoenaers et al. report that auxin regulates the receptor-like kinase ERULUS, which localizes to the apical root hair plasma membrane, where it controls cell wall composition through pectin methylesterases and phosphorylation of cell-elongation regulators FERONIA and H+-ATPase 1/2.",

keywords = "Arabidopsis, auxin, AUXIN RESPONSE FACTOR, cell wall, CrRLK1L, FERONIA, kinase, pectin, root hair, tip growth",

author = "S{\'e}bastjen Schoenaers and Daria Balcerowicz and Gordon Breen and Kristine Hill and Malgorzata Zdanio and Gr{\'e}gory Mouille and Holman, {Tara J.} and Jaesung Oh and Wilson, {Michael H.} and Natalia Nikonorova and Vu, {Lam Dai} and {De Smet}, Ive and Ranjan Swarup and {De Vos}, {Winnok H.} and Isabel Pintelon and Dirk Adriaensen and Claire Grierson and Bennett, {Malcolm J.} and Kris Vissenberg",

year = "2018",

month = mar,

day = "5",

doi = "10.1016/j.cub.2018.01.050",

language = "English",

volume = "28",

pages = "722--732.e6",

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Schoenaers, S, Balcerowicz, D, Breen, G, Hill, K, Zdanio, M, Mouille, G, Holman, TJ, Oh, J, Wilson, MH, Nikonorova, N, Vu, LD, De Smet, I, Swarup, R, De Vos, WH, Pintelon, I, Adriaensen, D, Grierson, C, Bennett, MJ & Vissenberg, K 2018, 'The Auxin-Regulated CrRLK1L Kinase ERULUS Controls Cell Wall Composition during Root Hair Tip Growth', Current Biology, vol. 28, no. 5, pp. 722-732.e6. https://doi.org/10.1016/j.cub.2018.01.050

TY - JOUR

T1 - The Auxin-Regulated CrRLK1L Kinase ERULUS Controls Cell Wall Composition during Root Hair Tip Growth

AU - Schoenaers, Sébastjen

AU - Balcerowicz, Daria

AU - Breen, Gordon

AU - Hill, Kristine

AU - Zdanio, Malgorzata

AU - Mouille, Grégory

AU - Holman, Tara J.

AU - Oh, Jaesung

AU - Wilson, Michael H.

AU - Nikonorova, Natalia

AU - Vu, Lam Dai

AU - De Smet, Ive

AU - Swarup, Ranjan

AU - De Vos, Winnok H.

AU - Pintelon, Isabel

AU - Adriaensen, Dirk

AU - Grierson, Claire

AU - Bennett, Malcolm J.

AU - Vissenberg, Kris

PY - 2018/3/5

Y1 - 2018/3/5

N2 - 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 cell 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 that 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. Root hair growth increases root surface area for nutrient uptake. Schoenaers et al. report that auxin regulates the receptor-like kinase ERULUS, which localizes to the apical root hair plasma membrane, where it controls cell wall composition through pectin methylesterases and phosphorylation of cell-elongation regulators FERONIA and H+-ATPase 1/2.

AB - 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 cell 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 that 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. Root hair growth increases root surface area for nutrient uptake. Schoenaers et al. report that auxin regulates the receptor-like kinase ERULUS, which localizes to the apical root hair plasma membrane, where it controls cell wall composition through pectin methylesterases and phosphorylation of cell-elongation regulators FERONIA and H+-ATPase 1/2.

KW - Arabidopsis

KW - auxin

KW - AUXIN RESPONSE FACTOR

KW - cell wall

KW - CrRLK1L

KW - FERONIA

KW - kinase

KW - pectin

KW - root hair

KW - tip growth

UR - http://www.scopus.com/inward/record.url?scp=85042351401&partnerID=8YFLogxK

U2 - 10.1016/j.cub.2018.01.050

DO - 10.1016/j.cub.2018.01.050

M3 - Article (Academic Journal)

C2 - 29478854

AN - SCOPUS:85042351401

SN - 0960-9822

VL - 28

SP - 722-732.e6

JO - Current Biology

JF - Current Biology

IS - 5

ER -

The Auxin-Regulated CrRLK1L Kinase ERULUS Controls Cell Wall Composition during Root Hair Tip Growth

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The Auxin-Regulated CrRLK1L Kinase ERULUS Controls Cell Wall Composition during Root Hair Tip Growth

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