Phytochrome A elevates plant circadian clock components to suppress shade avoidance in deep canopy shade

Donald P Fraser; Paige E Panter; Ashutosh Sharma; Bhavana Sharma; Antony N Dodd; Keara A Franklin

doi:10.1073/pnas.2108176118

Phytochrome A elevates plant circadian clock components to suppress shade avoidance in deep canopy shade

Donald P Fraser, Paige E Panter, Ashutosh Sharma, Bhavana Sharma, Antony N Dodd^*, Keara A Franklin^*

^*Corresponding author for this work

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Abstract

Shade-avoiding plants can detect the presence of neighboring vegetation and evoke escape responses before canopy cover limits photosynthesis. Rapid stem elongation facilitates light foraging and enables plants to overtop competitors. A major regulator of this response is the phytochrome B (phyB) photoreceptor, which becomes inactivated in light environments with a low ratio of red to far-red light (low R:FR), characteristic of vegetational shade. Although shade avoidance can provide plants with a competitive advantage in fast-growing stands, excessive
stem elongation can be detrimental to plant survival. As such, plants have evolved multiple feedback mechanisms to attenuate shade avoidance signaling. The very low R:FR and reduced levels of photosynthetically active radiation (PAR) present in deep canopy shade can, together, trigger phytochrome A (phyA) signaling, inhibiting shade avoidance and promoting plant survival when resources are severely limited. The molecular mechanisms underlying this response have not been fully elucidated. Here, we show that Arabidopsis thaliana phyA elevates early evening expression of the central circadian clock components TIMING OF CAB
EXPRESSION 1 (TOC1), PSEUDO RESPONSE REGULATOR 7 (PRR7), EARLY FLOWERING 3 (ELF3) and ELF4 in photocycles of low R:FR and low PAR. These collectively
suppress stem elongation, antagonising shade avoidance in deep canopy shade.

Original language	English
Article number	e2108176118
Number of pages	9
Journal	Proceedings of the National Academy of Sciences of the United States of America
Volume	118
Issue number	27
DOIs	https://doi.org/10.1073/pnas.2108176118
Publication status	Published - 6 Jul 2021

Bibliographical note

Funding Information:
ACKNOWLEDGMENTS. We thank Elena Monte (Centre for Research in Agricultural Genomics, Barcelona, Spain) for the donation of toc1-101 seed, Stacey Harmer (University of California, Davis, CA) for the donation of rve8-1 seed, Rob McClung (Dartmouth College, Hanover, NH) for prr5-3 and prr7-3 mutants, Takeshi Mizuno for prr5-11/7-11 mutants, and Anthony Hall (Earlham Institute, Norwich, United Kingdom) for the donation of transgenic lines containing CCA1::LUC and TOC1::LUC. This work was funded by Biotechnology and Biological Sciences Research Council (BBSRC) Grants BB/ L01369X, BB/M008711/1, BB/R002045/1, and GEN BB/P013511/1, the Bristol Centre for Agricultural Innovation, and The Leverhulme Trust Grant RPG-2018-216.

Funding Information:
We thank Elena Monte (Centre for Research in Agricultural Genomics, Barcelona, Spain) for the donation of toc1-101 seed, Stacey Harmer (University of California, Davis, CA) for the donation of rve8-1 seed, Rob McClung (Dartmouth College, Hanover, NH) for prr5-3 and prr7-3 mutants, Takeshi Mizuno for prr5-11/7-11 mutants, and Anthony Hall (Earlham Institute, Norwich, United Kingdom) for the donation of transgenic lines containing CCA1::LUC and TOC1::LUC. This work was funded by Biotechnology and Biological Sciences Research Council (BBSRC) Grants BB/ L01369X, BB/M008711/1, BB/R002045/1, and GEN BB/P013511/1, the Bristol Centre for Agricultural Innovation, and The Leverhulme Trust Grant RPG-2018-216.

Publisher Copyright:
© 2021 National Academy of Sciences. All rights reserved.

Keywords

Phytochrome A
circadian clock
deep shade

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title = "Phytochrome A elevates plant circadian clock components to suppress shade avoidance in deep canopy shade",

abstract = "Shade-avoiding plants can detect the presence of neighboring vegetation and evoke escape responses before canopy cover limits photosynthesis. Rapid stem elongation facilitates light foraging and enables plants to overtop competitors. A major regulator of this response is the phytochrome B (phyB) photoreceptor, which becomes inactivated in light environments with a low ratio of red to far-red light (low R:FR), characteristic of vegetational shade. Although shade avoidance can provide plants with a competitive advantage in fast-growing stands, excessive stem elongation can be detrimental to plant survival. As such, plants have evolved multiple feedback mechanisms to attenuate shade avoidance signaling. The very low R:FR and reduced levels of photosynthetically active radiation (PAR) present in deep canopy shade can, together, trigger phytochrome A (phyA) signaling, inhibiting shade avoidance and promoting plant survival when resources are severely limited. The molecular mechanisms underlying this response have not been fully elucidated. Here, we show that Arabidopsis thaliana phyA elevates early evening expression of the central circadian clock components TIMING OF CAB EXPRESSION 1 (TOC1), PSEUDO RESPONSE REGULATOR 7 (PRR7), EARLY FLOWERING 3 (ELF3) and ELF4 in photocycles of low R:FR and low PAR. These collectively suppress stem elongation, antagonising shade avoidance in deep canopy shade.",

keywords = "Phytochrome A, circadian clock, deep shade",

author = "Fraser, {Donald P} and Panter, {Paige E} and Ashutosh Sharma and Bhavana Sharma and Dodd, {Antony N} and Franklin, {Keara A}",

note = "Funding Information: ACKNOWLEDGMENTS. We thank Elena Monte (Centre for Research in Agricultural Genomics, Barcelona, Spain) for the donation of toc1-101 seed, Stacey Harmer (University of California, Davis, CA) for the donation of rve8-1 seed, Rob McClung (Dartmouth College, Hanover, NH) for prr5-3 and prr7-3 mutants, Takeshi Mizuno for prr5-11/7-11 mutants, and Anthony Hall (Earlham Institute, Norwich, United Kingdom) for the donation of transgenic lines containing CCA1::LUC and TOC1::LUC. This work was funded by Biotechnology and Biological Sciences Research Council (BBSRC) Grants BB/ L01369X, BB/M008711/1, BB/R002045/1, and GEN BB/P013511/1, the Bristol Centre for Agricultural Innovation, and The Leverhulme Trust Grant RPG-2018-216. Funding Information: We thank Elena Monte (Centre for Research in Agricultural Genomics, Barcelona, Spain) for the donation of toc1-101 seed, Stacey Harmer (University of California, Davis, CA) for the donation of rve8-1 seed, Rob McClung (Dartmouth College, Hanover, NH) for prr5-3 and prr7-3 mutants, Takeshi Mizuno for prr5-11/7-11 mutants, and Anthony Hall (Earlham Institute, Norwich, United Kingdom) for the donation of transgenic lines containing CCA1::LUC and TOC1::LUC. This work was funded by Biotechnology and Biological Sciences Research Council (BBSRC) Grants BB/ L01369X, BB/M008711/1, BB/R002045/1, and GEN BB/P013511/1, the Bristol Centre for Agricultural Innovation, and The Leverhulme Trust Grant RPG-2018-216. Publisher Copyright: {\textcopyright} 2021 National Academy of Sciences. All rights reserved.",

year = "2021",

month = jul,

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doi = "10.1073/pnas.2108176118",

language = "English",

volume = "118",

journal = "Proceedings of the National Academy of Sciences of the United States of America",

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Phytochrome A elevates plant circadian clock components to suppress shade avoidance in deep canopy shade. / Fraser, Donald P; Panter, Paige E; Sharma, Ashutosh et al.
In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 118, No. 27, e2108176118, 06.07.2021.

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

TY - JOUR

T1 - Phytochrome A elevates plant circadian clock components to suppress shade avoidance in deep canopy shade

AU - Fraser, Donald P

AU - Panter, Paige E

AU - Sharma, Ashutosh

AU - Sharma, Bhavana

AU - Dodd, Antony N

AU - Franklin, Keara A

N1 - Funding Information: ACKNOWLEDGMENTS. We thank Elena Monte (Centre for Research in Agricultural Genomics, Barcelona, Spain) for the donation of toc1-101 seed, Stacey Harmer (University of California, Davis, CA) for the donation of rve8-1 seed, Rob McClung (Dartmouth College, Hanover, NH) for prr5-3 and prr7-3 mutants, Takeshi Mizuno for prr5-11/7-11 mutants, and Anthony Hall (Earlham Institute, Norwich, United Kingdom) for the donation of transgenic lines containing CCA1::LUC and TOC1::LUC. This work was funded by Biotechnology and Biological Sciences Research Council (BBSRC) Grants BB/ L01369X, BB/M008711/1, BB/R002045/1, and GEN BB/P013511/1, the Bristol Centre for Agricultural Innovation, and The Leverhulme Trust Grant RPG-2018-216. Funding Information: We thank Elena Monte (Centre for Research in Agricultural Genomics, Barcelona, Spain) for the donation of toc1-101 seed, Stacey Harmer (University of California, Davis, CA) for the donation of rve8-1 seed, Rob McClung (Dartmouth College, Hanover, NH) for prr5-3 and prr7-3 mutants, Takeshi Mizuno for prr5-11/7-11 mutants, and Anthony Hall (Earlham Institute, Norwich, United Kingdom) for the donation of transgenic lines containing CCA1::LUC and TOC1::LUC. This work was funded by Biotechnology and Biological Sciences Research Council (BBSRC) Grants BB/ L01369X, BB/M008711/1, BB/R002045/1, and GEN BB/P013511/1, the Bristol Centre for Agricultural Innovation, and The Leverhulme Trust Grant RPG-2018-216. Publisher Copyright: © 2021 National Academy of Sciences. All rights reserved.

PY - 2021/7/6

Y1 - 2021/7/6

N2 - Shade-avoiding plants can detect the presence of neighboring vegetation and evoke escape responses before canopy cover limits photosynthesis. Rapid stem elongation facilitates light foraging and enables plants to overtop competitors. A major regulator of this response is the phytochrome B (phyB) photoreceptor, which becomes inactivated in light environments with a low ratio of red to far-red light (low R:FR), characteristic of vegetational shade. Although shade avoidance can provide plants with a competitive advantage in fast-growing stands, excessive stem elongation can be detrimental to plant survival. As such, plants have evolved multiple feedback mechanisms to attenuate shade avoidance signaling. The very low R:FR and reduced levels of photosynthetically active radiation (PAR) present in deep canopy shade can, together, trigger phytochrome A (phyA) signaling, inhibiting shade avoidance and promoting plant survival when resources are severely limited. The molecular mechanisms underlying this response have not been fully elucidated. Here, we show that Arabidopsis thaliana phyA elevates early evening expression of the central circadian clock components TIMING OF CAB EXPRESSION 1 (TOC1), PSEUDO RESPONSE REGULATOR 7 (PRR7), EARLY FLOWERING 3 (ELF3) and ELF4 in photocycles of low R:FR and low PAR. These collectively suppress stem elongation, antagonising shade avoidance in deep canopy shade.

AB - Shade-avoiding plants can detect the presence of neighboring vegetation and evoke escape responses before canopy cover limits photosynthesis. Rapid stem elongation facilitates light foraging and enables plants to overtop competitors. A major regulator of this response is the phytochrome B (phyB) photoreceptor, which becomes inactivated in light environments with a low ratio of red to far-red light (low R:FR), characteristic of vegetational shade. Although shade avoidance can provide plants with a competitive advantage in fast-growing stands, excessive stem elongation can be detrimental to plant survival. As such, plants have evolved multiple feedback mechanisms to attenuate shade avoidance signaling. The very low R:FR and reduced levels of photosynthetically active radiation (PAR) present in deep canopy shade can, together, trigger phytochrome A (phyA) signaling, inhibiting shade avoidance and promoting plant survival when resources are severely limited. The molecular mechanisms underlying this response have not been fully elucidated. Here, we show that Arabidopsis thaliana phyA elevates early evening expression of the central circadian clock components TIMING OF CAB EXPRESSION 1 (TOC1), PSEUDO RESPONSE REGULATOR 7 (PRR7), EARLY FLOWERING 3 (ELF3) and ELF4 in photocycles of low R:FR and low PAR. These collectively suppress stem elongation, antagonising shade avoidance in deep canopy shade.

KW - Phytochrome A

KW - circadian clock

KW - deep shade

U2 - 10.1073/pnas.2108176118

DO - 10.1073/pnas.2108176118

M3 - Article (Academic Journal)

C2 - 34187900

SN - 0027-8424

VL - 118

JO - Proceedings of the National Academy of Sciences of the United States of America

JF - Proceedings of the National Academy of Sciences of the United States of America

IS - 27

M1 - e2108176118

ER -

Phytochrome A elevates plant circadian clock components to suppress shade avoidance in deep canopy shade

Abstract

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Keywords

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