Cell surface receptor kinase FERONIA linked to nutrient sensor TORC signaling controls root hair growth at low temperature linked to low nitrate in Arabidopsis thaliana

Javier Martínez Pacheco; Limei Song; Lenka Kuběnová; Miroslav Ovečka; Victoria Berdion Gabarain; Juan Manuel Peralta; Tomás Urzúa Lehuedé; Miguel Angel Ibeas; Martiniano M. Ricardi; Sirui Zhu; Yanan Shen; Mikhail Schepetilnikov; Lyubov A. Ryabova; José M. Alvarez; Rodrigo A. Gutierrez; Guido Grossmann; Jozef Šamaj; Feng Yu; José M. Estevez

doi:10.1111/nph.18723

Cell surface receptor kinase FERONIA linked to nutrient sensor TORC signaling controls root hair growth at low temperature linked to low nitrate in Arabidopsis thaliana

Javier Martínez Pacheco, Limei Song, Lenka Kuběnová, Miroslav Ovečka, Victoria Berdion Gabarain, Juan Manuel Peralta, Tomás Urzúa Lehuedé, Miguel Angel Ibeas, Martiniano M. Ricardi, Sirui Zhu, Yanan Shen, Mikhail Schepetilnikov, Lyubov A. Ryabova, José M. Alvarez, Rodrigo A. Gutierrez, Guido Grossmann, Jozef Šamaj, Feng Yu, José M. Estevez

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12 Citations (Scopus)

Abstract

Root hairs (RH) are excellent model systems for studying cell size and polarity since they elongate several hundred-fold their original size. Their tip growth is determined both by intrinsic and environmental signals. Although nutrient availability and temperature are key factors for a sustained plant growth, the molecular mechanisms underlying their sensing and downstream signaling pathways remain unclear. We use genetics to address the roles of the cell surface receptor kinase FERONIA (FER) and the nutrient sensing TOR Complex 1 (TORC) in RH growth. We identified that low temperature (10°C) triggers a strong RH elongation response in Arabidopsis thaliana involving FER and TORC. We found that FER is required to perceive limited nutrient availability caused by low temperature. FERONIA interacts with and activates TORC-downstream components to trigger RH growth. In addition, the small GTPase Rho of plants 2 (ROP2) is also involved in this RH growth response linking FER and TOR. We also found that limited nitrogen nutrient availability can mimic the RH growth response at 10°C in a NRT1.1-dependent manner. These results uncover a molecular mechanism by which a central hub composed by FER-ROP2-TORC is involved in the control of RH elongation under low temperature and nitrogen deficiency.

Original language	English
Pages (from-to)	169-185
Number of pages	17
Journal	New Phytologist
Volume	238
Issue number	1
DOIs	https://doi.org/10.1111/nph.18723
Publication status	Published - Apr 2023

Keywords

Arabidopsis
cell surface
FERONIA
low temperature
nitrogen
root hairs
ROP2
TOR kinase

ASJC Scopus subject areas

Physiology
Plant Science

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10.1111/nph.18723

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Pacheco, J. M., Song, L., Kuběnová, L., Ovečka, M., Berdion Gabarain, V., Peralta, J. M., Lehuedé, T. U., Ibeas, M. A., Ricardi, M. M., Zhu, S., Shen, Y., Schepetilnikov, M., Ryabova, L. A., Alvarez, J. M., Gutierrez, R. A., Grossmann, G., Šamaj, J., Yu, F., & Estevez, J. M. (2023). Cell surface receptor kinase FERONIA linked to nutrient sensor TORC signaling controls root hair growth at low temperature linked to low nitrate in Arabidopsis thaliana. New Phytologist, 238(1), 169-185. https://doi.org/10.1111/nph.18723

@article{262f3445708348b18f2a00d8dd9ec2f4,

title = "Cell surface receptor kinase FERONIA linked to nutrient sensor TORC signaling controls root hair growth at low temperature linked to low nitrate in Arabidopsis thaliana",

abstract = "Root hairs (RH) are excellent model systems for studying cell size and polarity since they elongate several hundred-fold their original size. Their tip growth is determined both by intrinsic and environmental signals. Although nutrient availability and temperature are key factors for a sustained plant growth, the molecular mechanisms underlying their sensing and downstream signaling pathways remain unclear. We use genetics to address the roles of the cell surface receptor kinase FERONIA (FER) and the nutrient sensing TOR Complex 1 (TORC) in RH growth. We identified that low temperature (10°C) triggers a strong RH elongation response in Arabidopsis thaliana involving FER and TORC. We found that FER is required to perceive limited nutrient availability caused by low temperature. FERONIA interacts with and activates TORC-downstream components to trigger RH growth. In addition, the small GTPase Rho of plants 2 (ROP2) is also involved in this RH growth response linking FER and TOR. We also found that limited nitrogen nutrient availability can mimic the RH growth response at 10°C in a NRT1.1-dependent manner. These results uncover a molecular mechanism by which a central hub composed by FER-ROP2-TORC is involved in the control of RH elongation under low temperature and nitrogen deficiency.",

keywords = "Arabidopsis, cell surface, FERONIA, low temperature, nitrogen, root hairs, ROP2, TOR kinase",

author = "Pacheco, {Javier Mart{\'i}nez} and Limei Song and Lenka Kub{\v e}nov{\'a} and Miroslav Ove{\v c}ka and {Berdion Gabarain}, Victoria and Peralta, {Juan Manuel} and Lehued{\'e}, {Tom{\'a}s Urz{\'u}a} and Ibeas, {Miguel Angel} and Ricardi, {Martiniano M.} and Sirui Zhu and Yanan Shen and Mikhail Schepetilnikov and Ryabova, {Lyubov A.} and Alvarez, {Jos{\'e} M.} and Gutierrez, {Rodrigo A.} and Guido Grossmann and Jozef {\v S}amaj and Feng Yu and Estevez, {Jos{\'e} M.}",

note = "Publisher Copyright: {\textcopyright} 2023 The Authors. New Phytologist {\textcopyright} 2023 New Phytologist Foundation.",

year = "2023",

month = apr,

doi = "10.1111/nph.18723",

language = "English",

volume = "238",

pages = "169--185",

journal = "New Phytologist",

issn = "0028-646X",

publisher = "Wiley-Blackwell",

number = "1",

}

Pacheco, JM, Song, L, Kuběnová, L, Ovečka, M, Berdion Gabarain, V, Peralta, JM, Lehuedé, TU, Ibeas, MA, Ricardi, MM, Zhu, S, Shen, Y, Schepetilnikov, M, Ryabova, LA, Alvarez, JM, Gutierrez, RA, Grossmann, G, Šamaj, J, Yu, F & Estevez, JM 2023, 'Cell surface receptor kinase FERONIA linked to nutrient sensor TORC signaling controls root hair growth at low temperature linked to low nitrate in Arabidopsis thaliana', New Phytologist, vol. 238, no. 1, pp. 169-185. https://doi.org/10.1111/nph.18723

TY - JOUR

T1 - Cell surface receptor kinase FERONIA linked to nutrient sensor TORC signaling controls root hair growth at low temperature linked to low nitrate in Arabidopsis thaliana

AU - Pacheco, Javier Martínez

AU - Song, Limei

AU - Kuběnová, Lenka

AU - Ovečka, Miroslav

AU - Berdion Gabarain, Victoria

AU - Peralta, Juan Manuel

AU - Lehuedé, Tomás Urzúa

AU - Ibeas, Miguel Angel

AU - Ricardi, Martiniano M.

AU - Zhu, Sirui

AU - Shen, Yanan

AU - Schepetilnikov, Mikhail

AU - Ryabova, Lyubov A.

AU - Alvarez, José M.

AU - Gutierrez, Rodrigo A.

AU - Grossmann, Guido

AU - Šamaj, Jozef

AU - Yu, Feng

AU - Estevez, José M.

PY - 2023/4

Y1 - 2023/4

N2 - Root hairs (RH) are excellent model systems for studying cell size and polarity since they elongate several hundred-fold their original size. Their tip growth is determined both by intrinsic and environmental signals. Although nutrient availability and temperature are key factors for a sustained plant growth, the molecular mechanisms underlying their sensing and downstream signaling pathways remain unclear. We use genetics to address the roles of the cell surface receptor kinase FERONIA (FER) and the nutrient sensing TOR Complex 1 (TORC) in RH growth. We identified that low temperature (10°C) triggers a strong RH elongation response in Arabidopsis thaliana involving FER and TORC. We found that FER is required to perceive limited nutrient availability caused by low temperature. FERONIA interacts with and activates TORC-downstream components to trigger RH growth. In addition, the small GTPase Rho of plants 2 (ROP2) is also involved in this RH growth response linking FER and TOR. We also found that limited nitrogen nutrient availability can mimic the RH growth response at 10°C in a NRT1.1-dependent manner. These results uncover a molecular mechanism by which a central hub composed by FER-ROP2-TORC is involved in the control of RH elongation under low temperature and nitrogen deficiency.

AB - Root hairs (RH) are excellent model systems for studying cell size and polarity since they elongate several hundred-fold their original size. Their tip growth is determined both by intrinsic and environmental signals. Although nutrient availability and temperature are key factors for a sustained plant growth, the molecular mechanisms underlying their sensing and downstream signaling pathways remain unclear. We use genetics to address the roles of the cell surface receptor kinase FERONIA (FER) and the nutrient sensing TOR Complex 1 (TORC) in RH growth. We identified that low temperature (10°C) triggers a strong RH elongation response in Arabidopsis thaliana involving FER and TORC. We found that FER is required to perceive limited nutrient availability caused by low temperature. FERONIA interacts with and activates TORC-downstream components to trigger RH growth. In addition, the small GTPase Rho of plants 2 (ROP2) is also involved in this RH growth response linking FER and TOR. We also found that limited nitrogen nutrient availability can mimic the RH growth response at 10°C in a NRT1.1-dependent manner. These results uncover a molecular mechanism by which a central hub composed by FER-ROP2-TORC is involved in the control of RH elongation under low temperature and nitrogen deficiency.

KW - Arabidopsis

KW - cell surface

KW - FERONIA

KW - low temperature

KW - nitrogen

KW - root hairs

KW - ROP2

KW - TOR kinase

UR - http://www.scopus.com/inward/record.url?scp=85147358996&partnerID=8YFLogxK

U2 - 10.1111/nph.18723

DO - 10.1111/nph.18723

M3 - Article

AN - SCOPUS:85147358996

SN - 0028-646X

VL - 238

SP - 169

EP - 185

JO - New Phytologist

JF - New Phytologist

IS - 1

ER -

Cell surface receptor kinase FERONIA linked to nutrient sensor TORC signaling controls root hair growth at low temperature linked to low nitrate in Arabidopsis thaliana

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