Role of a ZF-HD Transcription Factor in miR157-Mediated Feed-Forward Regulatory Module That Determines Plant Architecture in <i>Arabidopsis</i>

In plants, vegetative and reproductive development are associated with agronomically important traits that contribute to grain yield and biomass. Zinc finger homeodomain (ZF-HD) transcription factors (TFs) constitute a relatively small gene family that has been studied in several model plants, inclu...

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Main Authors: Young Koung Lee, Sunita Kumari, Andrew Olson, Felix Hauser, Doreen Ware
Format: Article
Language:English
Published: MDPI AG 2022-08-01
Series:International Journal of Molecular Sciences
Subjects:
Online Access:https://www.mdpi.com/1422-0067/23/15/8665
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author Young Koung Lee
Sunita Kumari
Andrew Olson
Felix Hauser
Doreen Ware
author_facet Young Koung Lee
Sunita Kumari
Andrew Olson
Felix Hauser
Doreen Ware
author_sort Young Koung Lee
collection DOAJ
description In plants, vegetative and reproductive development are associated with agronomically important traits that contribute to grain yield and biomass. Zinc finger homeodomain (ZF-HD) transcription factors (TFs) constitute a relatively small gene family that has been studied in several model plants, including <i>Arabidopsis thaliana</i> L. and <i>Oryza sativa</i> L. The ZF-HD family members play important roles in plant growth and development, but their contribution to the regulation of plant architecture remains largely unknown due to their functional redundancy. To understand the gene regulatory network controlled by ZF-HD TFs, we analyzed multiple loss-of-function mutants of ZF-HD TFs in <i>Arabidopsis</i> that exhibited morphological abnormalities in branching and flowering architecture. We found that ZF-HD TFs, especially HB34, negatively regulate the expression of miR157 and positively regulate SQUAMOSA PROMOTER BINDING–LIKE 10 (<i>SPL10</i>), a target of miR157. Genome-wide chromatin immunoprecipitation sequencing (ChIP-Seq) analysis revealed that <i>miR157D</i> and <i>SPL10</i> are direct targets of HB34, creating a feed-forward loop that constitutes a robust miRNA regulatory module. Network motif analysis contains overrepresented coherent type IV feedforward motifs in the amiR zf-HD and <i>hbq</i> mutant background. This finding indicates that miRNA-mediated ZF-HD feedforward modules modify branching and inflorescence architecture in <i>Arabidopsis</i>. Taken together, these findings reveal a guiding role of ZF-HD TFs in the regulatory network module and demonstrate its role in plant architecture in <i>Arabidopsis</i>.
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spelling doaj.art-2545e71b26444b2e8c6ed37eb9783c402023-11-30T22:30:08ZengMDPI AGInternational Journal of Molecular Sciences1661-65961422-00672022-08-012315866510.3390/ijms23158665Role of a ZF-HD Transcription Factor in miR157-Mediated Feed-Forward Regulatory Module That Determines Plant Architecture in <i>Arabidopsis</i>Young Koung Lee0Sunita Kumari1Andrew Olson2Felix Hauser3Doreen Ware4Cold Spring Harbor Laboratory, 1 Bungtown Road, Cold Spring Harbor, NY 11724, USACold Spring Harbor Laboratory, 1 Bungtown Road, Cold Spring Harbor, NY 11724, USACold Spring Harbor Laboratory, 1 Bungtown Road, Cold Spring Harbor, NY 11724, USADivision of Biological Sciences, University of California–San Diego, La Jolla, CA 92093, USACold Spring Harbor Laboratory, 1 Bungtown Road, Cold Spring Harbor, NY 11724, USAIn plants, vegetative and reproductive development are associated with agronomically important traits that contribute to grain yield and biomass. Zinc finger homeodomain (ZF-HD) transcription factors (TFs) constitute a relatively small gene family that has been studied in several model plants, including <i>Arabidopsis thaliana</i> L. and <i>Oryza sativa</i> L. The ZF-HD family members play important roles in plant growth and development, but their contribution to the regulation of plant architecture remains largely unknown due to their functional redundancy. To understand the gene regulatory network controlled by ZF-HD TFs, we analyzed multiple loss-of-function mutants of ZF-HD TFs in <i>Arabidopsis</i> that exhibited morphological abnormalities in branching and flowering architecture. We found that ZF-HD TFs, especially HB34, negatively regulate the expression of miR157 and positively regulate SQUAMOSA PROMOTER BINDING–LIKE 10 (<i>SPL10</i>), a target of miR157. Genome-wide chromatin immunoprecipitation sequencing (ChIP-Seq) analysis revealed that <i>miR157D</i> and <i>SPL10</i> are direct targets of HB34, creating a feed-forward loop that constitutes a robust miRNA regulatory module. Network motif analysis contains overrepresented coherent type IV feedforward motifs in the amiR zf-HD and <i>hbq</i> mutant background. This finding indicates that miRNA-mediated ZF-HD feedforward modules modify branching and inflorescence architecture in <i>Arabidopsis</i>. Taken together, these findings reveal a guiding role of ZF-HD TFs in the regulatory network module and demonstrate its role in plant architecture in <i>Arabidopsis</i>.https://www.mdpi.com/1422-0067/23/15/8665ChIP-Seqfeed-forward loop (FFL)gene regulatory network (GRN)HB34miRNAnext-generation sequencing
spellingShingle Young Koung Lee
Sunita Kumari
Andrew Olson
Felix Hauser
Doreen Ware
Role of a ZF-HD Transcription Factor in miR157-Mediated Feed-Forward Regulatory Module That Determines Plant Architecture in <i>Arabidopsis</i>
International Journal of Molecular Sciences
ChIP-Seq
feed-forward loop (FFL)
gene regulatory network (GRN)
HB34
miRNA
next-generation sequencing
title Role of a ZF-HD Transcription Factor in miR157-Mediated Feed-Forward Regulatory Module That Determines Plant Architecture in <i>Arabidopsis</i>
title_full Role of a ZF-HD Transcription Factor in miR157-Mediated Feed-Forward Regulatory Module That Determines Plant Architecture in <i>Arabidopsis</i>
title_fullStr Role of a ZF-HD Transcription Factor in miR157-Mediated Feed-Forward Regulatory Module That Determines Plant Architecture in <i>Arabidopsis</i>
title_full_unstemmed Role of a ZF-HD Transcription Factor in miR157-Mediated Feed-Forward Regulatory Module That Determines Plant Architecture in <i>Arabidopsis</i>
title_short Role of a ZF-HD Transcription Factor in miR157-Mediated Feed-Forward Regulatory Module That Determines Plant Architecture in <i>Arabidopsis</i>
title_sort role of a zf hd transcription factor in mir157 mediated feed forward regulatory module that determines plant architecture in i arabidopsis i
topic ChIP-Seq
feed-forward loop (FFL)
gene regulatory network (GRN)
HB34
miRNA
next-generation sequencing
url https://www.mdpi.com/1422-0067/23/15/8665
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