Root branching under high salinity requires auxin-independent modulation of LATERAL ORGAN BOUNDARY DOMAIN 16 function

Yanxia Zhang; Yiyun Li; Thijs de Zeeuw; Kilian Duijts; Dorota Kawa; Jasper Lamers; Kristina S Munzert; Hongfei Li; Yutao Zou; A Jessica Meyer; Jinxuan Yan; Francel Verstappen; Yixuan Wang; Tom Gijsberts; Jielin Wang; Nora Gigli-Bisceglia; Timo Engelsdorf; Aalt D J van Dijk; Christa Testerink

doi:10.1093/plcell/koad317

Root branching under high salinity requires auxin-independent modulation of LATERAL ORGAN BOUNDARY DOMAIN 16 function

Yanxia Zhang^*, Yiyun Li, Thijs de Zeeuw, Kilian Duijts, Dorota Kawa, Jasper Lamers, Kristina S Munzert, Hongfei Li, Yutao Zou, A Jessica Meyer, Jinxuan Yan, Francel Verstappen, Yixuan Wang, Tom Gijsberts, Jielin Wang, Nora Gigli-Bisceglia, Timo Engelsdorf, Aalt D J van Dijk, Christa Testerink

^*Corresponding author for this work

Research output: Contribution to journal › Article › Academic › peer-review

Abstract

Salinity stress constrains lateral root (LR) growth and severely affects plant growth. Auxin signaling regulates LR formation, but the molecular mechanism by which salinity affects root auxin signaling and whether salt induces other pathways that regulate LR development remains unknown. In Arabidopsis thaliana, the auxin-regulated transcription factor LATERAL ORGAN BOUNDARY DOMAIN 16 (LBD16) is an essential player in LR development under control conditions. Here, we show that under high-salt conditions, an alternative pathway regulates LBD16 expression. Salt represses auxin signaling but, in parallel, activates ZINC FINGER OF ARABIDOPSIS THALIANA 6 (ZAT6), a transcriptional activator of LBD16. ZAT6 activates LBD16 expression, thus contributing to downstream cell wall remodeling and promoting LR development under high-salt conditions. Our study thus shows that the integration of auxin-dependent repressive and salt-activated auxin-independent pathways converging on LBD16 modulates root branching under high-salt conditions.

Original language	English
Pages (from-to)	899-918
Number of pages	20
Journal	The Plant Cell
Volume	36
Issue number	4
DOIs	https://doi.org/10.1093/plcell/koad317
Publication status	Published - 29 Mar 2024
Externally published	Yes

Bibliographical note

Publisher Copyright:
© The Author(s) 2023. Published by Oxford University Press on behalf of American Society of Plant Biologists.

Funding

This work was supported by the European Research Council (ERC; grant agreement 724321); Dutch Research Council (NWO) Vici (Grant VI.C.192.033) and NWO-ENW KLEIN (OCENW.KLEIN.421) grants; Netherlands Organisation for Health Research and Development (ZonMW) Enabling Technologies Hotels programme—early career scientists projects (Grant No. 435004012); and a China Scholarship Council (CSC)—Sino-Dutch Bilateral Exchange Scholarship (CF 13731).

Funders	Funder number
European Research Council
ZonMw	435004012
NWO-ENW	OCENW.KLEIN.421
Nederlandse Organisatie voor Wetenschappelijk Onderzoek	VI.C.192.033
Horizon 2020 Framework Programme	724321
China Scholarship Council	CF 13731

Keywords

Arabidopsis Proteins/genetics
Arabidopsis/metabolism
Gene Expression Regulation, Plant
Indoleacetic Acids/metabolism
Plant Roots/metabolism
Salinity

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10.1093/plcell/koad317Licence: CC BY

Cite this

Zhang, Y., Li, Y., de Zeeuw, T., Duijts, K., Kawa, D., Lamers, J., Munzert, K. S., Li, H., Zou, Y., Meyer, A. J., Yan, J., Verstappen, F., Wang, Y., Gijsberts, T., Wang, J., Gigli-Bisceglia, N., Engelsdorf, T., van Dijk, A. D. J., & Testerink, C. (2024). Root branching under high salinity requires auxin-independent modulation of LATERAL ORGAN BOUNDARY DOMAIN 16 function. The Plant Cell, 36(4), 899-918. https://doi.org/10.1093/plcell/koad317

@article{f0f5dc27aad64f7ca335242ff1a16727,

title = "Root branching under high salinity requires auxin-independent modulation of LATERAL ORGAN BOUNDARY DOMAIN 16 function",

abstract = "Salinity stress constrains lateral root (LR) growth and severely affects plant growth. Auxin signaling regulates LR formation, but the molecular mechanism by which salinity affects root auxin signaling and whether salt induces other pathways that regulate LR development remains unknown. In Arabidopsis thaliana, the auxin-regulated transcription factor LATERAL ORGAN BOUNDARY DOMAIN 16 (LBD16) is an essential player in LR development under control conditions. Here, we show that under high-salt conditions, an alternative pathway regulates LBD16 expression. Salt represses auxin signaling but, in parallel, activates ZINC FINGER OF ARABIDOPSIS THALIANA 6 (ZAT6), a transcriptional activator of LBD16. ZAT6 activates LBD16 expression, thus contributing to downstream cell wall remodeling and promoting LR development under high-salt conditions. Our study thus shows that the integration of auxin-dependent repressive and salt-activated auxin-independent pathways converging on LBD16 modulates root branching under high-salt conditions.",

keywords = "Arabidopsis Proteins/genetics, Arabidopsis/metabolism, Gene Expression Regulation, Plant, Indoleacetic Acids/metabolism, Plant Roots/metabolism, Salinity",

author = "Yanxia Zhang and Yiyun Li and {de Zeeuw}, Thijs and Kilian Duijts and Dorota Kawa and Jasper Lamers and Munzert, {Kristina S} and Hongfei Li and Yutao Zou and Meyer, {A Jessica} and Jinxuan Yan and Francel Verstappen and Yixuan Wang and Tom Gijsberts and Jielin Wang and Nora Gigli-Bisceglia and Timo Engelsdorf and {van Dijk}, {Aalt D J} and Christa Testerink",

note = "Publisher Copyright: {\textcopyright} The Author(s) 2023. Published by Oxford University Press on behalf of American Society of Plant Biologists.",

year = "2024",

month = mar,

day = "29",

doi = "10.1093/plcell/koad317",

language = "English",

volume = "36",

pages = "899--918",

journal = "The Plant Cell",

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Zhang, Y, Li, Y, de Zeeuw, T, Duijts, K, Kawa, D, Lamers, J, Munzert, KS, Li, H, Zou, Y, Meyer, AJ, Yan, J, Verstappen, F, Wang, Y, Gijsberts, T, Wang, J, Gigli-Bisceglia, N, Engelsdorf, T, van Dijk, ADJ & Testerink, C 2024, 'Root branching under high salinity requires auxin-independent modulation of LATERAL ORGAN BOUNDARY DOMAIN 16 function', The Plant Cell, vol. 36, no. 4, pp. 899-918. https://doi.org/10.1093/plcell/koad317

TY - JOUR

T1 - Root branching under high salinity requires auxin-independent modulation of LATERAL ORGAN BOUNDARY DOMAIN 16 function

AU - Zhang, Yanxia

AU - Li, Yiyun

AU - de Zeeuw, Thijs

AU - Duijts, Kilian

AU - Kawa, Dorota

AU - Lamers, Jasper

AU - Munzert, Kristina S

AU - Li, Hongfei

AU - Zou, Yutao

AU - Meyer, A Jessica

AU - Yan, Jinxuan

AU - Verstappen, Francel

AU - Wang, Yixuan

AU - Gijsberts, Tom

AU - Wang, Jielin

AU - Gigli-Bisceglia, Nora

AU - Engelsdorf, Timo

AU - van Dijk, Aalt D J

AU - Testerink, Christa

PY - 2024/3/29

Y1 - 2024/3/29

N2 - Salinity stress constrains lateral root (LR) growth and severely affects plant growth. Auxin signaling regulates LR formation, but the molecular mechanism by which salinity affects root auxin signaling and whether salt induces other pathways that regulate LR development remains unknown. In Arabidopsis thaliana, the auxin-regulated transcription factor LATERAL ORGAN BOUNDARY DOMAIN 16 (LBD16) is an essential player in LR development under control conditions. Here, we show that under high-salt conditions, an alternative pathway regulates LBD16 expression. Salt represses auxin signaling but, in parallel, activates ZINC FINGER OF ARABIDOPSIS THALIANA 6 (ZAT6), a transcriptional activator of LBD16. ZAT6 activates LBD16 expression, thus contributing to downstream cell wall remodeling and promoting LR development under high-salt conditions. Our study thus shows that the integration of auxin-dependent repressive and salt-activated auxin-independent pathways converging on LBD16 modulates root branching under high-salt conditions.

AB - Salinity stress constrains lateral root (LR) growth and severely affects plant growth. Auxin signaling regulates LR formation, but the molecular mechanism by which salinity affects root auxin signaling and whether salt induces other pathways that regulate LR development remains unknown. In Arabidopsis thaliana, the auxin-regulated transcription factor LATERAL ORGAN BOUNDARY DOMAIN 16 (LBD16) is an essential player in LR development under control conditions. Here, we show that under high-salt conditions, an alternative pathway regulates LBD16 expression. Salt represses auxin signaling but, in parallel, activates ZINC FINGER OF ARABIDOPSIS THALIANA 6 (ZAT6), a transcriptional activator of LBD16. ZAT6 activates LBD16 expression, thus contributing to downstream cell wall remodeling and promoting LR development under high-salt conditions. Our study thus shows that the integration of auxin-dependent repressive and salt-activated auxin-independent pathways converging on LBD16 modulates root branching under high-salt conditions.

KW - Arabidopsis Proteins/genetics

KW - Arabidopsis/metabolism

KW - Gene Expression Regulation, Plant

KW - Indoleacetic Acids/metabolism

KW - Plant Roots/metabolism

KW - Salinity

UR - http://www.scopus.com/inward/record.url?scp=85189374243&partnerID=8YFLogxK

U2 - 10.1093/plcell/koad317

DO - 10.1093/plcell/koad317

M3 - Article

C2 - 38142228

SN - 1040-4651

VL - 36

SP - 899

EP - 918

JO - The Plant Cell

JF - The Plant Cell

IS - 4

ER -

Root branching under high salinity requires auxin-independent modulation of LATERAL ORGAN BOUNDARY DOMAIN 16 function

Abstract

Bibliographical note

Funding

Keywords

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