PIF7 controls leaf cell proliferation through an AN3 substitution repression mechanism

Ejaz Hussain; Andrés Romanowski; Karen J. Halliday

doi:10.1073/pnas.2115682119

PIF7 controls leaf cell proliferation through an AN3 substitution repression mechanism

Ejaz Hussain, Andrés Romanowski, Karen J. Halliday

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

Abstract

Plants are agile, plastic organisms able to adapt to everchanging circumstances. Responding to far-red (FR) wavelengths from nearby vegetation, shade-intolerant species elicit the adaptive shade-avoidance syndrome (SAS), characterized by elongated petioles, leaf hyponasty, and smaller leaves. We utilized end-of-day FR (EODFR) treatments to interrogate molecular processes that underlie the SAS leaf response. Genetic analysis established that PHYTOCHROME-INTERACTING FACTOR 7 (PIF7) is required for EODFR-mediated constraint of leaf blade cell division, while EODFR messenger RNA sequencing data identified ANGUSTIFOLIA3 (AN3) as a potential PIF7 target. We show that PIF7 can suppress AN3 transcription by directly interacting with and sequestering AN3. We also establish that PIF7 and AN3 impose antagonistic control of gene expression via common cis-acting promoter motifs in several cell-cycle regulator genes. EODFR triggers the molecular substitution of AN3 to PIF7 at G-box/PBE-box promoter regions and a switch from promotion to repression of gene expression.

Original language	English
Article number	e2115682119
Pages (from-to)	1-11
Number of pages	11
Journal	Proceedings of the National Academy of Sciences
Volume	119
Issue number	5
DOIs	https://doi.org/10.1073/pnas.2115682119
Publication status	Published - 1 Feb 2022
Externally published	Yes

Bibliographical note

Funding Information:
ACKNOWLEDGMENTS. We thank Prof. Dirk Inzé for providing us with the 35S::AN3-GSyellow line, Prof. Gorou Horiguchi for an3-4 seeds, Prof. Jeong Hoe Kim for grf1-3;grf3-1;grf5-2, grf1-3;grf3-1; grf4-1;grf5-2 seeds, and Prof. Joanne Chory and Dr. Elena Monte for 35S::PIF7-Flash line. We would like to thank Prof. Enamul Huq, Dr. Beatriz Orosa, Dr. Imtiyaz Yaseen, Dr. Gabriela Toledo-Ortiz and Dr. Michael Skelly for advice on molecular assays, and also M. E. Goya for her help with BioRender. E.H. was funded by the Punjab Educational Endowment Fund PEEF/CMMS/2016/203. This work was supported by United Kingdom Research and Innovation, Biotechnology, and Biological Sciences Research Council Grants BB/M025551/1 and BB/ N005147/1 awarded to K.J.H.

Publisher Copyright:
© 2022 National Academy of Sciences. All rights reserved.

Keywords

AN3
Cell proliferation
EODFR
Leaf development
PIF7

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Cite this

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title = "PIF7 controls leaf cell proliferation through an AN3 substitution repression mechanism",

abstract = "Plants are agile, plastic organisms able to adapt to everchanging circumstances. Responding to far-red (FR) wavelengths from nearby vegetation, shade-intolerant species elicit the adaptive shade-avoidance syndrome (SAS), characterized by elongated petioles, leaf hyponasty, and smaller leaves. We utilized end-of-day FR (EODFR) treatments to interrogate molecular processes that underlie the SAS leaf response. Genetic analysis established that PHYTOCHROME-INTERACTING FACTOR 7 (PIF7) is required for EODFR-mediated constraint of leaf blade cell division, while EODFR messenger RNA sequencing data identified ANGUSTIFOLIA3 (AN3) as a potential PIF7 target. We show that PIF7 can suppress AN3 transcription by directly interacting with and sequestering AN3. We also establish that PIF7 and AN3 impose antagonistic control of gene expression via common cis-acting promoter motifs in several cell-cycle regulator genes. EODFR triggers the molecular substitution of AN3 to PIF7 at G-box/PBE-box promoter regions and a switch from promotion to repression of gene expression.",

keywords = "AN3, Cell proliferation, EODFR, Leaf development, PIF7",

author = "Ejaz Hussain and Andr{\'e}s Romanowski and Halliday, {Karen J.}",

note = "Funding Information: ACKNOWLEDGMENTS. We thank Prof. Dirk Inz{\'e} for providing us with the 35S::AN3-GSyellow line, Prof. Gorou Horiguchi for an3-4 seeds, Prof. Jeong Hoe Kim for grf1-3;grf3-1;grf5-2, grf1-3;grf3-1; grf4-1;grf5-2 seeds, and Prof. Joanne Chory and Dr. Elena Monte for 35S::PIF7-Flash line. We would like to thank Prof. Enamul Huq, Dr. Beatriz Orosa, Dr. Imtiyaz Yaseen, Dr. Gabriela Toledo-Ortiz and Dr. Michael Skelly for advice on molecular assays, and also M. E. Goya for her help with BioRender. E.H. was funded by the Punjab Educational Endowment Fund PEEF/CMMS/2016/203. This work was supported by United Kingdom Research and Innovation, Biotechnology, and Biological Sciences Research Council Grants BB/M025551/1 and BB/ N005147/1 awarded to K.J.H. Publisher Copyright: {\textcopyright} 2022 National Academy of Sciences. All rights reserved.",

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doi = "10.1073/pnas.2115682119",

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AU - Romanowski, Andrés

AU - Halliday, Karen J.

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N2 - Plants are agile, plastic organisms able to adapt to everchanging circumstances. Responding to far-red (FR) wavelengths from nearby vegetation, shade-intolerant species elicit the adaptive shade-avoidance syndrome (SAS), characterized by elongated petioles, leaf hyponasty, and smaller leaves. We utilized end-of-day FR (EODFR) treatments to interrogate molecular processes that underlie the SAS leaf response. Genetic analysis established that PHYTOCHROME-INTERACTING FACTOR 7 (PIF7) is required for EODFR-mediated constraint of leaf blade cell division, while EODFR messenger RNA sequencing data identified ANGUSTIFOLIA3 (AN3) as a potential PIF7 target. We show that PIF7 can suppress AN3 transcription by directly interacting with and sequestering AN3. We also establish that PIF7 and AN3 impose antagonistic control of gene expression via common cis-acting promoter motifs in several cell-cycle regulator genes. EODFR triggers the molecular substitution of AN3 to PIF7 at G-box/PBE-box promoter regions and a switch from promotion to repression of gene expression.

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DO - 10.1073/pnas.2115682119

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JO - Proceedings of the National Academy of Sciences

JF - Proceedings of the National Academy of Sciences

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M1 - e2115682119

ER -

PIF7 controls leaf cell proliferation through an AN3 substitution repression mechanism

Abstract

Bibliographical note

Keywords

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