The VIL gene CRAWLING ELEPHANT controls maturation and differentiation in tomato via polycomb silencing

Ido Shwartz; Chen Yahav; Neta Kovetz; Matan Levy; Alon Israeli; Maya Bar; Katherine L. Duval; Ellen G. Krall; Naama Teboul; José M. Jiménez-Gómez; Roger B. Deal; Naomi Ori

doi:10.1371/journal.pgen.1009633

The VIL gene CRAWLING ELEPHANT controls maturation and differentiation in tomato via polycomb silencing

Ido Shwartz, Chen Yahav, Neta Kovetz, Matan Levy, Alon Israeli, Maya Bar, Katherine L. Duval, Ellen G. Krall, Naama Teboul, José M. Jiménez-Gómez, Roger B. Deal^*, Naomi Ori^*

^*Corresponding author for this work

Institute of Plant Sciences and Genetics in Agriculture

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

Abstract

VERNALIZATION INSENSITIVE 3-LIKE (VIL) proteins are PHD-finger proteins that recruit the repressor complex Polycomb Repressive Complex 2 (PRC2) to the promoters of target genes. Most known VIL targets are flowering repressor genes. Here, we show that the tomato VIL gene CRAWLING ELEPHANT (CREL) promotes differentiation throughout plant development by facilitating the trimethylation of Histone H3 on lysine 27 (H3K27me3). We identified the crel mutant in a screen for suppressors of the simple-leaf phenotype of entire (e), a mutant in the AUX/IAA gene ENTIRE/SlIAA9, involved in compound-leaf development in tomato. crel mutants have increased leaf complexity, and suppress the ectopic blade growth of e mutants. In addition, crel mutants are late flowering, and have delayed and aberrant stem, root and flower development. Consistent with a role for CREL in recruiting PRC2, crel mutants show drastically reduced H3K27me3 enrichment at approximately half of the 14,789 sites enriched in wild-type plants, along with upregulation of many underlying genes. Interestingly, this reduction in H3K27me3 across the genome in crel is also associated with gains in H3K27me3 at a smaller number of sites that normally have modest levels of the mark in wild-type plants, suggesting that PRC2 activity is no longer limiting in the absence of CREL. Our results uncover a wide role for CREL in plant and organ differentiation in tomato and suggest that CREL is required for targeting PRC2 activity to, and thus silencing, a specific subset of polycomb targets.

Original language	American English
Article number	e1009633
Journal	PLoS Genetics
Volume	18
Issue number	3
DOIs	https://doi.org/10.1371/journal.pgen.1009633
State	Published - 7 Mar 2022

Bibliographical note

Funding Information:
This work was supported by grants from the United States – Israel Binational Science Foundation (BSF, 2015093) to N.O and R.B.D., German-Israel Project Cooperation Foundation (OR309/1-1;FE552/12-1) to N.O. and J.M.J.-and from the U.S. – Israel Binational Agricultural Research and Development Fund (IS4531-12(c) and IS5103-18R) and the Israel Science Foundation (grants number 2407-18 and 248-19) to NO. AI thanks the Azrieli Foundation for the award of an Azrieli fellowship. E.G.K. was supported by NIH training grant 5T32GM008490. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. We thank Yuval Eshed, Alon Samach and Dani Zamir for plant material and fruitful discussions and suggestions; Michael Lach for technical help, members of the Ori lab for continuous discussions and help; Revital Bronstein, Yuval Eshed and Zach Lippman for sharing the tomato mapping marker set.

Publisher Copyright:
Copyright: © 2022 Shwartz et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Keywords

Drosophila Proteins/metabolism
Histones/genetics
Lycopersicon esculentum/genetics
Polycomb Repressive Complex 2/genetics
Polycomb-Group Proteins/genetics

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

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10.1371/journal.pgen.1009633

Cite this

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title = "The VIL gene CRAWLING ELEPHANT controls maturation and differentiation in tomato via polycomb silencing",

abstract = "VERNALIZATION INSENSITIVE 3-LIKE (VIL) proteins are PHD-finger proteins that recruit the repressor complex Polycomb Repressive Complex 2 (PRC2) to the promoters of target genes. Most known VIL targets are flowering repressor genes. Here, we show that the tomato VIL gene CRAWLING ELEPHANT (CREL) promotes differentiation throughout plant development by facilitating the trimethylation of Histone H3 on lysine 27 (H3K27me3). We identified the crel mutant in a screen for suppressors of the simple-leaf phenotype of entire (e), a mutant in the AUX/IAA gene ENTIRE/SlIAA9, involved in compound-leaf development in tomato. crel mutants have increased leaf complexity, and suppress the ectopic blade growth of e mutants. In addition, crel mutants are late flowering, and have delayed and aberrant stem, root and flower development. Consistent with a role for CREL in recruiting PRC2, crel mutants show drastically reduced H3K27me3 enrichment at approximately half of the 14,789 sites enriched in wild-type plants, along with upregulation of many underlying genes. Interestingly, this reduction in H3K27me3 across the genome in crel is also associated with gains in H3K27me3 at a smaller number of sites that normally have modest levels of the mark in wild-type plants, suggesting that PRC2 activity is no longer limiting in the absence of CREL. Our results uncover a wide role for CREL in plant and organ differentiation in tomato and suggest that CREL is required for targeting PRC2 activity to, and thus silencing, a specific subset of polycomb targets.",

keywords = "Drosophila Proteins/metabolism, Histones/genetics, Lycopersicon esculentum/genetics, Polycomb Repressive Complex 2/genetics, Polycomb-Group Proteins/genetics",

author = "Ido Shwartz and Chen Yahav and Neta Kovetz and Matan Levy and Alon Israeli and Maya Bar and Duval, {Katherine L.} and Krall, {Ellen G.} and Naama Teboul and Jim{\'e}nez-G{\'o}mez, {Jos{\'e} M.} and Deal, {Roger B.} and Naomi Ori",

note = "Funding Information: This work was supported by grants from the United States – Israel Binational Science Foundation (BSF, 2015093) to N.O and R.B.D., German-Israel Project Cooperation Foundation (OR309/1-1;FE552/12-1) to N.O. and J.M.J.-and from the U.S. – Israel Binational Agricultural Research and Development Fund (IS4531-12(c) and IS5103-18R) and the Israel Science Foundation (grants number 2407-18 and 248-19) to NO. AI thanks the Azrieli Foundation for the award of an Azrieli fellowship. E.G.K. was supported by NIH training grant 5T32GM008490. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. We thank Yuval Eshed, Alon Samach and Dani Zamir for plant material and fruitful discussions and suggestions; Michael Lach for technical help, members of the Ori lab for continuous discussions and help; Revital Bronstein, Yuval Eshed and Zach Lippman for sharing the tomato mapping marker set. Publisher Copyright: Copyright: {\textcopyright} 2022 Shwartz et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.",

year = "2022",

month = mar,

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doi = "10.1371/journal.pgen.1009633",

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T1 - The VIL gene CRAWLING ELEPHANT controls maturation and differentiation in tomato via polycomb silencing

AU - Shwartz, Ido

AU - Yahav, Chen

AU - Kovetz, Neta

AU - Levy, Matan

AU - Israeli, Alon

AU - Bar, Maya

AU - Duval, Katherine L.

AU - Krall, Ellen G.

AU - Teboul, Naama

AU - Jiménez-Gómez, José M.

AU - Deal, Roger B.

AU - Ori, Naomi

N1 - Funding Information: This work was supported by grants from the United States – Israel Binational Science Foundation (BSF, 2015093) to N.O and R.B.D., German-Israel Project Cooperation Foundation (OR309/1-1;FE552/12-1) to N.O. and J.M.J.-and from the U.S. – Israel Binational Agricultural Research and Development Fund (IS4531-12(c) and IS5103-18R) and the Israel Science Foundation (grants number 2407-18 and 248-19) to NO. AI thanks the Azrieli Foundation for the award of an Azrieli fellowship. E.G.K. was supported by NIH training grant 5T32GM008490. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. We thank Yuval Eshed, Alon Samach and Dani Zamir for plant material and fruitful discussions and suggestions; Michael Lach for technical help, members of the Ori lab for continuous discussions and help; Revital Bronstein, Yuval Eshed and Zach Lippman for sharing the tomato mapping marker set. Publisher Copyright: Copyright: © 2022 Shwartz et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

PY - 2022/3/7

Y1 - 2022/3/7

N2 - VERNALIZATION INSENSITIVE 3-LIKE (VIL) proteins are PHD-finger proteins that recruit the repressor complex Polycomb Repressive Complex 2 (PRC2) to the promoters of target genes. Most known VIL targets are flowering repressor genes. Here, we show that the tomato VIL gene CRAWLING ELEPHANT (CREL) promotes differentiation throughout plant development by facilitating the trimethylation of Histone H3 on lysine 27 (H3K27me3). We identified the crel mutant in a screen for suppressors of the simple-leaf phenotype of entire (e), a mutant in the AUX/IAA gene ENTIRE/SlIAA9, involved in compound-leaf development in tomato. crel mutants have increased leaf complexity, and suppress the ectopic blade growth of e mutants. In addition, crel mutants are late flowering, and have delayed and aberrant stem, root and flower development. Consistent with a role for CREL in recruiting PRC2, crel mutants show drastically reduced H3K27me3 enrichment at approximately half of the 14,789 sites enriched in wild-type plants, along with upregulation of many underlying genes. Interestingly, this reduction in H3K27me3 across the genome in crel is also associated with gains in H3K27me3 at a smaller number of sites that normally have modest levels of the mark in wild-type plants, suggesting that PRC2 activity is no longer limiting in the absence of CREL. Our results uncover a wide role for CREL in plant and organ differentiation in tomato and suggest that CREL is required for targeting PRC2 activity to, and thus silencing, a specific subset of polycomb targets.

AB - VERNALIZATION INSENSITIVE 3-LIKE (VIL) proteins are PHD-finger proteins that recruit the repressor complex Polycomb Repressive Complex 2 (PRC2) to the promoters of target genes. Most known VIL targets are flowering repressor genes. Here, we show that the tomato VIL gene CRAWLING ELEPHANT (CREL) promotes differentiation throughout plant development by facilitating the trimethylation of Histone H3 on lysine 27 (H3K27me3). We identified the crel mutant in a screen for suppressors of the simple-leaf phenotype of entire (e), a mutant in the AUX/IAA gene ENTIRE/SlIAA9, involved in compound-leaf development in tomato. crel mutants have increased leaf complexity, and suppress the ectopic blade growth of e mutants. In addition, crel mutants are late flowering, and have delayed and aberrant stem, root and flower development. Consistent with a role for CREL in recruiting PRC2, crel mutants show drastically reduced H3K27me3 enrichment at approximately half of the 14,789 sites enriched in wild-type plants, along with upregulation of many underlying genes. Interestingly, this reduction in H3K27me3 across the genome in crel is also associated with gains in H3K27me3 at a smaller number of sites that normally have modest levels of the mark in wild-type plants, suggesting that PRC2 activity is no longer limiting in the absence of CREL. Our results uncover a wide role for CREL in plant and organ differentiation in tomato and suggest that CREL is required for targeting PRC2 activity to, and thus silencing, a specific subset of polycomb targets.

KW - Drosophila Proteins/metabolism

KW - Histones/genetics

KW - Lycopersicon esculentum/genetics

KW - Polycomb Repressive Complex 2/genetics

KW - Polycomb-Group Proteins/genetics

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DO - 10.1371/journal.pgen.1009633

M3 - Article

C2 - 35255095

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SN - 1553-7390

VL - 18

JO - PLoS Genetics

JF - PLoS Genetics

IS - 3

M1 - e1009633

ER -

The VIL gene CRAWLING ELEPHANT controls maturation and differentiation in tomato via polycomb silencing

Abstract

Bibliographical note

Keywords

UN SDGs

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