Teosinte branched1/cycloidea/ proliferating cell factor4 interacts with wrinkled1 to mediate seed oil biosynthesis

Que Kong; Sanjay K. Singh; Jenny J. Mantyla; Sitakanta Pattanaik; Liang Guo; Ling Yuan; Christoph Benning; Wei Ma

doi:10.1104/pp.20.00547

Teosinte branched1/cycloidea/ proliferating cell factor4 interacts with wrinkled1 to mediate seed oil biosynthesis

Que Kong, Sanjay K. Singh, Jenny J. Mantyla, Sitakanta Pattanaik, Liang Guo, Ling Yuan, Christoph Benning, Wei Ma

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

20 Scopus citations

Abstract

Cross-family transcription factor (TF) interactions play critical roles in the regulation of plant developmental and metabolic pathways. WRINKLED1 (WRI1) is a key TF governing oil biosynthesis in plants. However, little is known about WRI1-interacting factors and their roles in oil biosynthesis. We screened a TF library using Arabidopsis (Arabidopsis thaliana) WRI1 (AtWRI1) as bait in yeast two-hybrid assays and identified three TEOSINTE BRANCHED1/CYCLOIDEA/PROLIFERATING CELL FACTOR (TCP) family TFs, namely TCP4, TCP10, and TCP24, as AtWRI1-interacting partners. The physical interaction between AtWRI1 and TCPs was further validated using bimolecular fluorescence complementation assays. TCPs play important roles in various plant developmental processes; however, their involvement in fatty acid biosynthesis was not previously known. Coexpression of TCP4, but not TCP10 or TCP24, with AtWRI1 reduced AtWRI1-mediated oil biosynthesis in Nicotiana benthamiana leaves. Transcriptomic analysis in transgenic Arabidopsis plants with enhanced TCP4 activity engineered by expressing rTCP4 (i.e. miR319-resistant TCP4) revealed that AtWRI1 target genes were significantly repressed. TCP4 expression is strongly correlated with AtWRI1 during embryo development. A tcp4 loss-of-function mutant, the jaw-D mutant with a strong reduction of TCP4 expression, and a tcp2 tcp4 tcp10 triple mutant accumulated more seed oil than wild-type Arabidopsis. In addition, TCP4 repressed the AtWRI1-mediated transactivation of the promoters of fatty acid biosynthetic genes. Collectively, our findings suggest that TCP4 represses fatty acid biosynthetic gene expression through interaction with AtWRI1, leading to a reduction of AtWRI1-mediated seed oil accumulation.

Original language	English
Pages (from-to)	658-665
Number of pages	8
Journal	Plant Physiology
Volume	184
Issue number	2
DOIs	https://doi.org/10.1104/pp.20.00547
State	Published - Oct 2020

Bibliographical note

Funding Information:
1This work was supported by a Department of Energy-Great Lakes Bioenergy Research Center Cooperative Agreement (grant no. DE– FC02–07ER64494 to C.B.), the Harold R. Burton Endowed Professorship (to L.Y.), a Nanyang Technological University Startup Grant (to W.M.), and the Ministry of Education of Singapore Tier 1 (grant no. 2018–T1–002–019 to W.M.). 2Author for contact: weima@ntu.edu.sg. 3Senior author.

Publisher Copyright:
© 2020 American Society of Plant Biologists. All rights reserved.

ASJC Scopus subject areas

Physiology
Genetics
Plant Science

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title = "Teosinte branched1/cycloidea/ proliferating cell factor4 interacts with wrinkled1 to mediate seed oil biosynthesis",

abstract = "Cross-family transcription factor (TF) interactions play critical roles in the regulation of plant developmental and metabolic pathways. WRINKLED1 (WRI1) is a key TF governing oil biosynthesis in plants. However, little is known about WRI1-interacting factors and their roles in oil biosynthesis. We screened a TF library using Arabidopsis (Arabidopsis thaliana) WRI1 (AtWRI1) as bait in yeast two-hybrid assays and identified three TEOSINTE BRANCHED1/CYCLOIDEA/PROLIFERATING CELL FACTOR (TCP) family TFs, namely TCP4, TCP10, and TCP24, as AtWRI1-interacting partners. The physical interaction between AtWRI1 and TCPs was further validated using bimolecular fluorescence complementation assays. TCPs play important roles in various plant developmental processes; however, their involvement in fatty acid biosynthesis was not previously known. Coexpression of TCP4, but not TCP10 or TCP24, with AtWRI1 reduced AtWRI1-mediated oil biosynthesis in Nicotiana benthamiana leaves. Transcriptomic analysis in transgenic Arabidopsis plants with enhanced TCP4 activity engineered by expressing rTCP4 (i.e. miR319-resistant TCP4) revealed that AtWRI1 target genes were significantly repressed. TCP4 expression is strongly correlated with AtWRI1 during embryo development. A tcp4 loss-of-function mutant, the jaw-D mutant with a strong reduction of TCP4 expression, and a tcp2 tcp4 tcp10 triple mutant accumulated more seed oil than wild-type Arabidopsis. In addition, TCP4 repressed the AtWRI1-mediated transactivation of the promoters of fatty acid biosynthetic genes. Collectively, our findings suggest that TCP4 represses fatty acid biosynthetic gene expression through interaction with AtWRI1, leading to a reduction of AtWRI1-mediated seed oil accumulation.",

author = "Que Kong and Singh, {Sanjay K.} and Mantyla, {Jenny J.} and Sitakanta Pattanaik and Liang Guo and Ling Yuan and Christoph Benning and Wei Ma",

note = "Funding Information: 1This work was supported by a Department of Energy-Great Lakes Bioenergy Research Center Cooperative Agreement (grant no. DE– FC02–07ER64494 to C.B.), the Harold R. Burton Endowed Professorship (to L.Y.), a Nanyang Technological University Startup Grant (to W.M.), and the Ministry of Education of Singapore Tier 1 (grant no. 2018–T1–002–019 to W.M.). 2Author for contact: weima@ntu.edu.sg. 3Senior author. Publisher Copyright: {\textcopyright} 2020 American Society of Plant Biologists. All rights reserved.",

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doi = "10.1104/pp.20.00547",

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AU - Kong, Que

AU - Singh, Sanjay K.

AU - Mantyla, Jenny J.

AU - Pattanaik, Sitakanta

AU - Guo, Liang

AU - Yuan, Ling

AU - Benning, Christoph

AU - Ma, Wei

N1 - Funding Information: 1This work was supported by a Department of Energy-Great Lakes Bioenergy Research Center Cooperative Agreement (grant no. DE– FC02–07ER64494 to C.B.), the Harold R. Burton Endowed Professorship (to L.Y.), a Nanyang Technological University Startup Grant (to W.M.), and the Ministry of Education of Singapore Tier 1 (grant no. 2018–T1–002–019 to W.M.). 2Author for contact: weima@ntu.edu.sg. 3Senior author. Publisher Copyright: © 2020 American Society of Plant Biologists. All rights reserved.

PY - 2020/10

Y1 - 2020/10

N2 - Cross-family transcription factor (TF) interactions play critical roles in the regulation of plant developmental and metabolic pathways. WRINKLED1 (WRI1) is a key TF governing oil biosynthesis in plants. However, little is known about WRI1-interacting factors and their roles in oil biosynthesis. We screened a TF library using Arabidopsis (Arabidopsis thaliana) WRI1 (AtWRI1) as bait in yeast two-hybrid assays and identified three TEOSINTE BRANCHED1/CYCLOIDEA/PROLIFERATING CELL FACTOR (TCP) family TFs, namely TCP4, TCP10, and TCP24, as AtWRI1-interacting partners. The physical interaction between AtWRI1 and TCPs was further validated using bimolecular fluorescence complementation assays. TCPs play important roles in various plant developmental processes; however, their involvement in fatty acid biosynthesis was not previously known. Coexpression of TCP4, but not TCP10 or TCP24, with AtWRI1 reduced AtWRI1-mediated oil biosynthesis in Nicotiana benthamiana leaves. Transcriptomic analysis in transgenic Arabidopsis plants with enhanced TCP4 activity engineered by expressing rTCP4 (i.e. miR319-resistant TCP4) revealed that AtWRI1 target genes were significantly repressed. TCP4 expression is strongly correlated with AtWRI1 during embryo development. A tcp4 loss-of-function mutant, the jaw-D mutant with a strong reduction of TCP4 expression, and a tcp2 tcp4 tcp10 triple mutant accumulated more seed oil than wild-type Arabidopsis. In addition, TCP4 repressed the AtWRI1-mediated transactivation of the promoters of fatty acid biosynthetic genes. Collectively, our findings suggest that TCP4 represses fatty acid biosynthetic gene expression through interaction with AtWRI1, leading to a reduction of AtWRI1-mediated seed oil accumulation.

AB - Cross-family transcription factor (TF) interactions play critical roles in the regulation of plant developmental and metabolic pathways. WRINKLED1 (WRI1) is a key TF governing oil biosynthesis in plants. However, little is known about WRI1-interacting factors and their roles in oil biosynthesis. We screened a TF library using Arabidopsis (Arabidopsis thaliana) WRI1 (AtWRI1) as bait in yeast two-hybrid assays and identified three TEOSINTE BRANCHED1/CYCLOIDEA/PROLIFERATING CELL FACTOR (TCP) family TFs, namely TCP4, TCP10, and TCP24, as AtWRI1-interacting partners. The physical interaction between AtWRI1 and TCPs was further validated using bimolecular fluorescence complementation assays. TCPs play important roles in various plant developmental processes; however, their involvement in fatty acid biosynthesis was not previously known. Coexpression of TCP4, but not TCP10 or TCP24, with AtWRI1 reduced AtWRI1-mediated oil biosynthesis in Nicotiana benthamiana leaves. Transcriptomic analysis in transgenic Arabidopsis plants with enhanced TCP4 activity engineered by expressing rTCP4 (i.e. miR319-resistant TCP4) revealed that AtWRI1 target genes were significantly repressed. TCP4 expression is strongly correlated with AtWRI1 during embryo development. A tcp4 loss-of-function mutant, the jaw-D mutant with a strong reduction of TCP4 expression, and a tcp2 tcp4 tcp10 triple mutant accumulated more seed oil than wild-type Arabidopsis. In addition, TCP4 repressed the AtWRI1-mediated transactivation of the promoters of fatty acid biosynthetic genes. Collectively, our findings suggest that TCP4 represses fatty acid biosynthetic gene expression through interaction with AtWRI1, leading to a reduction of AtWRI1-mediated seed oil accumulation.

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Teosinte branched1/cycloidea/ proliferating cell factor4 interacts with wrinkled1 to mediate seed oil biosynthesis

Abstract

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