ZINC FINGER PROTEIN2 suppresses funiculus lignification to ensure seed loading efficiency in Arabidopsis

Pui Man Low; Que Kong; Leonard Blaschek; Zhiming Ma; Peng Ken Lim; Yuzhou Yang; Trisha Quek; Cuithbert J.R. Lim; Sanjay K. Singh; Christoph Crocoll; Ellen Engquist; Jakob S. Thorsen; Sitakanta Pattanaik; Wan Ting Tee; Marek Mutwil; Yansong Miao; Ling Yuan; Deyang Xu; Staffan Persson; Wei Ma

doi:10.1016/j.devcel.2025.01.021

ZINC FINGER PROTEIN2 suppresses funiculus lignification to ensure seed loading efficiency in Arabidopsis

Pui Man Low, Que Kong, Leonard Blaschek, Zhiming Ma, Peng Ken Lim, Yuzhou Yang, Trisha Quek, Cuithbert J.R. Lim, Sanjay K. Singh, Christoph Crocoll, Ellen Engquist, Jakob S. Thorsen, Sitakanta Pattanaik, Wan Ting Tee, Marek Mutwil, Yansong Miao, Ling Yuan, Deyang Xu, Staffan Persson, Wei Ma

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

1 Scopus citations

Abstract

The plant funiculus anchors the developing seed to the placenta within the inner dorsal pod strands of the silique wall and directly transports nutrients to the seeds. The lignified vasculature critically supports nutrient transport through the funiculus. However, molecular mechanisms underlying lignified secondary cell wall (SCW) biosynthesis in the funiculus remain elusive. Here, we show that the transcription factor ZINC FINGER PROTEIN2 (ZFP2) represses SCW formation in the cortex cells that surround the vasculature. This function is essential for efficient nutrient loading into the seeds. Notably, ZFP2 directly acts on the SCW transcription factor NAC SECONDARY WALL THICKENING PROMOTING FACTOR1 (NST1) to repress cortex cell lignification, providing a mechanism of how SCW biosynthesis is restricted to the vasculature of the funiculus to ensure proper seed loading in Arabidopsis.

Original language	English
Pages (from-to)	1719-1729.e6
Journal	Developmental Cell
Volume	60
Issue number	12
DOIs	https://doi.org/10.1016/j.devcel.2025.01.021
State	Published - Jun 23 2025

Bibliographical note

Publisher Copyright:
© 2025 Elsevier Inc.

Funding

We thank Dr. Hao Yu (National University of Singapore) for the seeds of N. benthamiana expressing H2B-RFP, Dr. Lisha Shen (Temasek Life Sciences Laboratory), and Dr. Chengxiang Li (Sichuan University) for suggestions on the ChIP-qPCR assay. This work was supported by the Ministry of Education (MOE) of Singapore Tier 2 (grant nos. MOE-T2EP30123-0001 and MOE-T2EP30220-0011 and to W.M.), MOE of Singapore Tier 1 (grant no. RG32/23 to W.M.), Villum Investigator (grant no. 25915 to S.P.), DNRF Chair (grant no. DNRF155 to S.P.), Novo Nordisk Laureate (grant no. NNF19OC0056076 to S.P.), Novo Nordisk Emerging Investigator (grant no. NNF20OC0060564 to S.P.), Novo Nordisk Data Science (grant no. NNF0068884 to S.P.), Independent Research Fund Denmark (grant no. 2102-00258B to D.X.), Innovation Fund Denmark (grant no. 3141-00040B to D.X.), Novo Nordisk Foundation (grant no. NNF23OC0085289 to D.X.), MOE of Singapore Tier 2 (grant no. MOE-T2EP30122-0021 to Y.M.), Singapore National Research Foundation Investigatorship (grant no. NRF-NRFI08-2022-0012 to Y.M.), and MOE of Singapore Tier 2 (grant no. MOE-T2EP30122-0017 to M.M.). L.B. is supported by the EMBO postdoctoral fellowship ALTF 37-2022 .

Funders	Funder number
Ministry of Education China
Michigan State University
National University Hospital, Singapore
Sichuan University, Chengdu, Sichuan
MOE of Singapore	RG32/23, 25915
Novo Nordisk Laureate	NNF19OC0056076
Danmarks Grundforskningsfond	DNRF155
Danmarks Grundforskningsfond
Novo Nordisk Fonden	NNF23OC0085289, MOE-T2EP30122-0021
Novo Nordisk Fonden
Ministry of Education - Singapore	MOE-T2EP30123-0001, MOE-T2EP30220-0011
Ministry of Education - Singapore
Independent Research Fund Denmark	2102-00258B
Innovationsfonden	3141-00040B
Innovationsfonden
Novo Nordisk A/S	NNF20OC0060564
Novo Nordisk A/S
European Molecular Biology Organization	ALTF 37-2022
European Molecular Biology Organization
National Research Foundation Singapore	NRF-NRFI08-2022-0012, MOE-T2EP30122-0017
National Research Foundation Singapore
Novo Nordisk Data Science	NNF0068884

Keywords

Arabidopsis
ZINC FINGER PROTEIN2
funiculus
secondary cell wall biosynthesis
transcription factor
transcriptional repression

ASJC Scopus subject areas

Molecular Biology
General Biochemistry, Genetics and Molecular Biology
Developmental Biology
Cell Biology

Access to Document

10.1016/j.devcel.2025.01.021

Cite this

Low, P. M., Kong, Q., Blaschek, L., Ma, Z., Lim, P. K., Yang, Y., Quek, T., Lim, C. J. R., Singh, S. K., Crocoll, C., Engquist, E., Thorsen, J. S., Pattanaik, S., Tee, W. T., Mutwil, M., Miao, Y., Yuan, L., Xu, D., Persson, S., & Ma, W. (2025). ZINC FINGER PROTEIN2 suppresses funiculus lignification to ensure seed loading efficiency in Arabidopsis. Developmental Cell, 60(12), 1719-1729.e6. https://doi.org/10.1016/j.devcel.2025.01.021

@article{407bd4da226843b2acf117302b6dd25e,

title = "ZINC FINGER PROTEIN2 suppresses funiculus lignification to ensure seed loading efficiency in Arabidopsis",

abstract = "The plant funiculus anchors the developing seed to the placenta within the inner dorsal pod strands of the silique wall and directly transports nutrients to the seeds. The lignified vasculature critically supports nutrient transport through the funiculus. However, molecular mechanisms underlying lignified secondary cell wall (SCW) biosynthesis in the funiculus remain elusive. Here, we show that the transcription factor ZINC FINGER PROTEIN2 (ZFP2) represses SCW formation in the cortex cells that surround the vasculature. This function is essential for efficient nutrient loading into the seeds. Notably, ZFP2 directly acts on the SCW transcription factor NAC SECONDARY WALL THICKENING PROMOTING FACTOR1 (NST1) to repress cortex cell lignification, providing a mechanism of how SCW biosynthesis is restricted to the vasculature of the funiculus to ensure proper seed loading in Arabidopsis.",

keywords = "Arabidopsis, ZINC FINGER PROTEIN2, funiculus, secondary cell wall biosynthesis, transcription factor, transcriptional repression",

author = "Low, \{Pui Man\} and Que Kong and Leonard Blaschek and Zhiming Ma and Lim, \{Peng Ken\} and Yuzhou Yang and Trisha Quek and Lim, \{Cuithbert J.R.\} and Singh, \{Sanjay K.\} and Christoph Crocoll and Ellen Engquist and Thorsen, \{Jakob S.\} and Sitakanta Pattanaik and Tee, \{Wan Ting\} and Marek Mutwil and Yansong Miao and Ling Yuan and Deyang Xu and Staffan Persson and Wei Ma",

note = "Publisher Copyright: {\textcopyright} 2025 Elsevier Inc.",

year = "2025",

month = jun,

day = "23",

doi = "10.1016/j.devcel.2025.01.021",

language = "English",

volume = "60",

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Low, PM, Kong, Q, Blaschek, L, Ma, Z, Lim, PK, Yang, Y, Quek, T, Lim, CJR, Singh, SK, Crocoll, C, Engquist, E, Thorsen, JS, Pattanaik, S, Tee, WT, Mutwil, M, Miao, Y, Yuan, L, Xu, D, Persson, S & Ma, W 2025, 'ZINC FINGER PROTEIN2 suppresses funiculus lignification to ensure seed loading efficiency in Arabidopsis', Developmental Cell, vol. 60, no. 12, pp. 1719-1729.e6. https://doi.org/10.1016/j.devcel.2025.01.021

TY - JOUR

T1 - ZINC FINGER PROTEIN2 suppresses funiculus lignification to ensure seed loading efficiency in Arabidopsis

AU - Low, Pui Man

AU - Kong, Que

AU - Blaschek, Leonard

AU - Ma, Zhiming

AU - Lim, Peng Ken

AU - Yang, Yuzhou

AU - Quek, Trisha

AU - Lim, Cuithbert J.R.

AU - Singh, Sanjay K.

AU - Crocoll, Christoph

AU - Engquist, Ellen

AU - Thorsen, Jakob S.

AU - Pattanaik, Sitakanta

AU - Tee, Wan Ting

AU - Mutwil, Marek

AU - Miao, Yansong

AU - Yuan, Ling

AU - Xu, Deyang

AU - Persson, Staffan

AU - Ma, Wei

PY - 2025/6/23

Y1 - 2025/6/23

N2 - The plant funiculus anchors the developing seed to the placenta within the inner dorsal pod strands of the silique wall and directly transports nutrients to the seeds. The lignified vasculature critically supports nutrient transport through the funiculus. However, molecular mechanisms underlying lignified secondary cell wall (SCW) biosynthesis in the funiculus remain elusive. Here, we show that the transcription factor ZINC FINGER PROTEIN2 (ZFP2) represses SCW formation in the cortex cells that surround the vasculature. This function is essential for efficient nutrient loading into the seeds. Notably, ZFP2 directly acts on the SCW transcription factor NAC SECONDARY WALL THICKENING PROMOTING FACTOR1 (NST1) to repress cortex cell lignification, providing a mechanism of how SCW biosynthesis is restricted to the vasculature of the funiculus to ensure proper seed loading in Arabidopsis.

AB - The plant funiculus anchors the developing seed to the placenta within the inner dorsal pod strands of the silique wall and directly transports nutrients to the seeds. The lignified vasculature critically supports nutrient transport through the funiculus. However, molecular mechanisms underlying lignified secondary cell wall (SCW) biosynthesis in the funiculus remain elusive. Here, we show that the transcription factor ZINC FINGER PROTEIN2 (ZFP2) represses SCW formation in the cortex cells that surround the vasculature. This function is essential for efficient nutrient loading into the seeds. Notably, ZFP2 directly acts on the SCW transcription factor NAC SECONDARY WALL THICKENING PROMOTING FACTOR1 (NST1) to repress cortex cell lignification, providing a mechanism of how SCW biosynthesis is restricted to the vasculature of the funiculus to ensure proper seed loading in Arabidopsis.

KW - Arabidopsis

KW - ZINC FINGER PROTEIN2

KW - funiculus

KW - secondary cell wall biosynthesis

KW - transcription factor

KW - transcriptional repression

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UR - https://www.scopus.com/inward/citedby.url?scp=105000778799&partnerID=8YFLogxK

U2 - 10.1016/j.devcel.2025.01.021

DO - 10.1016/j.devcel.2025.01.021

M3 - Article

C2 - 39999844

AN - SCOPUS:105000778799

SN - 1534-5807

VL - 60

SP - 1719-1729.e6

JO - Developmental Cell

JF - Developmental Cell

IS - 12

ER -

ZINC FINGER PROTEIN2 suppresses funiculus lignification to ensure seed loading efficiency in Arabidopsis

Abstract

Bibliographical note

Funding

Keywords

ASJC Scopus subject areas

Access to Document

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