Conserved pleiotropy of an ancient plant homeobox gene uncovered by cis-regulatory dissection

Anat Hendelman; Sophia Zebell; Daniel Rodriguez-Leal; Noah Dukler; Gina Robitaille; Xuelin Wu; Jamie Kostyun; Lior Tal; Peipei Wang; Madelaine E. Bartlett; Yuval Eshed; Idan Efroni; Zachary B. Lippman

doi:10.1016/j.cell.2021.02.001

Conserved pleiotropy of an ancient plant homeobox gene uncovered by cis-regulatory dissection

Anat Hendelman, Sophia Zebell, Daniel Rodriguez-Leal, Noah Dukler, Gina Robitaille, Xuelin Wu, Jamie Kostyun, Lior Tal, Peipei Wang, Madelaine E. Bartlett, Yuval Eshed, Idan Efroni^*, Zachary B. Lippman^*

^*Corresponding author for this work

Institute of Plant Sciences and Genetics in Agriculture

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

68 Scopus citations

Abstract

Functional

Original language	American English
Pages (from-to)	1724-1739.e16
Journal	Cell
Volume	184
Issue number	7
DOIs	https://doi.org/10.1016/j.cell.2021.02.001
State	Published - 1 Apr 2021

Bibliographical note

Funding Information:
We thank members of the Lippman laboratory for valuable comments and discussions. We thank J. Kim and A. Krainer for technical support. We thank L. Randall, A. Horowitz Doyle, P. Keen, K. Swartwood, M. Tjahjadi, and J. Van Eck for performing tomato and groundcherry transformations. We thank T. Mulligan, K. Schlecht, A. Krainer, and S. Qiao for assistance with plant care. We thank M. Karaca from Inari Agriculture for assistance with ATAC-seq (prior to September 2018). We thank B. Usadel, S. Strickler, and L. Mueller for sharing the S. lycopersicoides genome assembly and annotation sequences. We thank D. Jackson for comments on the manuscript. This research was supported by the Howard Hughes Medical Institute and grant support from the BARD (United States-Israel Binational Agricultural Research and Development Fund, IS-5120-18C ) to Y.E. and Z.B.L. and the Vaadia-BARD Postdoctoral Fellowship (award no. FL-542-16 ) to A.H., the Howard Hughes Medical Institute International Scholar Grant ( 55008730 ) and Israel Science Foundation ( ISF966/17 ) to I.E., and the National Science Foundation Plant Genome Research Program (grant no. IOS-1546837 ) to M.E.B. and Z.B.L.

Funding Information:
We thank members of the Lippman laboratory for valuable comments and discussions. We thank J. Kim and A. Krainer for technical support. We thank L. Randall, A. Horowitz Doyle, P. Keen, K. Swartwood, M. Tjahjadi, and J. Van Eck for performing tomato and groundcherry transformations. We thank T. Mulligan, K. Schlecht, A. Krainer, and S. Qiao for assistance with plant care. We thank M. Karaca from Inari Agriculture for assistance with ATAC-seq (prior to September 2018). We thank B. Usadel, S. Strickler, and L. Mueller for sharing the S. lycopersicoides genome assembly and annotation sequences. We thank D. Jackson for comments on the manuscript. This research was supported by the Howard Hughes Medical Institute and grant support from the BARD (United States-Israel Binational Agricultural Research and Development Fund, IS-5120-18C) to Y.E. and Z.B.L. and the Vaadia-BARD Postdoctoral Fellowship (award no. FL-542-16) to A.H. the Howard Hughes Medical Institute International Scholar Grant (55008730) and Israel Science Foundation (ISF966/17) to I.E. and the National Science Foundation Plant Genome Research Program (grant no. IOS-1546837) to M.E.B. and Z.B.L. Z.B.L. conceived the project. A.H. S.Z. D.R.-L. X.W. I.E. and Z.B.L. designed and planned experiments. A.H. S.Z. D.R.-L. G.R. X.W. L.T. P.W. Y.E. I.E. and Z.B.L. performed experiments and collected data. A.H. S.Z. N.D. X.W. J.K. P.W. M.E.B. I.E. and Z.B.L. analyzed data and A.H. I.E. and Z.B.L. wrote the manuscript with input from M.E.B. and Y.E. All authors read, edited, and approved the manuscript. Z.B.L. is a consultant for and a member of the Scientific Strategy Board of Inari Agriculture, and he is also a named inventor on a number of patents and patent applications directed to related technology that have been exclusively licensed from CSHL to Inari Agriculture.

Publisher Copyright:
© 2021 Elsevier Inc.

Keywords

ATAC sequencing
Arabidopsis
Brassicaceae
Solanaceae
cis-regulatory
conserved non-coding sequences
homeobox
inflorescence
plant development
pleiotropy
tomato

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10.1016/j.cell.2021.02.001

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title = "Conserved pleiotropy of an ancient plant homeobox gene uncovered by cis-regulatory dissection",

abstract = "Functional",

keywords = "ATAC sequencing, Arabidopsis, Brassicaceae, Solanaceae, cis-regulatory, conserved non-coding sequences, homeobox, inflorescence, plant development, pleiotropy, tomato",

author = "Anat Hendelman and Sophia Zebell and Daniel Rodriguez-Leal and Noah Dukler and Gina Robitaille and Xuelin Wu and Jamie Kostyun and Lior Tal and Peipei Wang and Bartlett, {Madelaine E.} and Yuval Eshed and Idan Efroni and Lippman, {Zachary B.}",

note = "Funding Information: We thank members of the Lippman laboratory for valuable comments and discussions. We thank J. Kim and A. Krainer for technical support. We thank L. Randall, A. Horowitz Doyle, P. Keen, K. Swartwood, M. Tjahjadi, and J. Van Eck for performing tomato and groundcherry transformations. We thank T. Mulligan, K. Schlecht, A. Krainer, and S. Qiao for assistance with plant care. We thank M. Karaca from Inari Agriculture for assistance with ATAC-seq (prior to September 2018). We thank B. Usadel, S. Strickler, and L. Mueller for sharing the S. lycopersicoides genome assembly and annotation sequences. We thank D. Jackson for comments on the manuscript. This research was supported by the Howard Hughes Medical Institute and grant support from the BARD (United States-Israel Binational Agricultural Research and Development Fund, IS-5120-18C ) to Y.E. and Z.B.L. and the Vaadia-BARD Postdoctoral Fellowship (award no. FL-542-16 ) to A.H., the Howard Hughes Medical Institute International Scholar Grant ( 55008730 ) and Israel Science Foundation ( ISF966/17 ) to I.E., and the National Science Foundation Plant Genome Research Program (grant no. IOS-1546837 ) to M.E.B. and Z.B.L. Funding Information: We thank members of the Lippman laboratory for valuable comments and discussions. We thank J. Kim and A. Krainer for technical support. We thank L. Randall, A. Horowitz Doyle, P. Keen, K. Swartwood, M. Tjahjadi, and J. Van Eck for performing tomato and groundcherry transformations. We thank T. Mulligan, K. Schlecht, A. Krainer, and S. Qiao for assistance with plant care. We thank M. Karaca from Inari Agriculture for assistance with ATAC-seq (prior to September 2018). We thank B. Usadel, S. Strickler, and L. Mueller for sharing the S. lycopersicoides genome assembly and annotation sequences. We thank D. Jackson for comments on the manuscript. This research was supported by the Howard Hughes Medical Institute and grant support from the BARD (United States-Israel Binational Agricultural Research and Development Fund, IS-5120-18C) to Y.E. and Z.B.L. and the Vaadia-BARD Postdoctoral Fellowship (award no. FL-542-16) to A.H. the Howard Hughes Medical Institute International Scholar Grant (55008730) and Israel Science Foundation (ISF966/17) to I.E. and the National Science Foundation Plant Genome Research Program (grant no. IOS-1546837) to M.E.B. and Z.B.L. Z.B.L. conceived the project. A.H. S.Z. D.R.-L. X.W. I.E. and Z.B.L. designed and planned experiments. A.H. S.Z. D.R.-L. G.R. X.W. L.T. P.W. Y.E. I.E. and Z.B.L. performed experiments and collected data. A.H. S.Z. N.D. X.W. J.K. P.W. M.E.B. I.E. and Z.B.L. analyzed data and A.H. I.E. and Z.B.L. wrote the manuscript with input from M.E.B. and Y.E. All authors read, edited, and approved the manuscript. Z.B.L. is a consultant for and a member of the Scientific Strategy Board of Inari Agriculture, and he is also a named inventor on a number of patents and patent applications directed to related technology that have been exclusively licensed from CSHL to Inari Agriculture. Publisher Copyright: {\textcopyright} 2021 Elsevier Inc.",

year = "2021",

month = apr,

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doi = "10.1016/j.cell.2021.02.001",

language = "American English",

volume = "184",

pages = "1724--1739.e16",

journal = "Cell",

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TY - JOUR

T1 - Conserved pleiotropy of an ancient plant homeobox gene uncovered by cis-regulatory dissection

AU - Hendelman, Anat

AU - Zebell, Sophia

AU - Rodriguez-Leal, Daniel

AU - Dukler, Noah

AU - Robitaille, Gina

AU - Wu, Xuelin

AU - Kostyun, Jamie

AU - Tal, Lior

AU - Wang, Peipei

AU - Bartlett, Madelaine E.

AU - Eshed, Yuval

AU - Efroni, Idan

AU - Lippman, Zachary B.

N1 - Funding Information: We thank members of the Lippman laboratory for valuable comments and discussions. We thank J. Kim and A. Krainer for technical support. We thank L. Randall, A. Horowitz Doyle, P. Keen, K. Swartwood, M. Tjahjadi, and J. Van Eck for performing tomato and groundcherry transformations. We thank T. Mulligan, K. Schlecht, A. Krainer, and S. Qiao for assistance with plant care. We thank M. Karaca from Inari Agriculture for assistance with ATAC-seq (prior to September 2018). We thank B. Usadel, S. Strickler, and L. Mueller for sharing the S. lycopersicoides genome assembly and annotation sequences. We thank D. Jackson for comments on the manuscript. This research was supported by the Howard Hughes Medical Institute and grant support from the BARD (United States-Israel Binational Agricultural Research and Development Fund, IS-5120-18C ) to Y.E. and Z.B.L. and the Vaadia-BARD Postdoctoral Fellowship (award no. FL-542-16 ) to A.H., the Howard Hughes Medical Institute International Scholar Grant ( 55008730 ) and Israel Science Foundation ( ISF966/17 ) to I.E., and the National Science Foundation Plant Genome Research Program (grant no. IOS-1546837 ) to M.E.B. and Z.B.L. Funding Information: We thank members of the Lippman laboratory for valuable comments and discussions. We thank J. Kim and A. Krainer for technical support. We thank L. Randall, A. Horowitz Doyle, P. Keen, K. Swartwood, M. Tjahjadi, and J. Van Eck for performing tomato and groundcherry transformations. We thank T. Mulligan, K. Schlecht, A. Krainer, and S. Qiao for assistance with plant care. We thank M. Karaca from Inari Agriculture for assistance with ATAC-seq (prior to September 2018). We thank B. Usadel, S. Strickler, and L. Mueller for sharing the S. lycopersicoides genome assembly and annotation sequences. We thank D. Jackson for comments on the manuscript. This research was supported by the Howard Hughes Medical Institute and grant support from the BARD (United States-Israel Binational Agricultural Research and Development Fund, IS-5120-18C) to Y.E. and Z.B.L. and the Vaadia-BARD Postdoctoral Fellowship (award no. FL-542-16) to A.H. the Howard Hughes Medical Institute International Scholar Grant (55008730) and Israel Science Foundation (ISF966/17) to I.E. and the National Science Foundation Plant Genome Research Program (grant no. IOS-1546837) to M.E.B. and Z.B.L. Z.B.L. conceived the project. A.H. S.Z. D.R.-L. X.W. I.E. and Z.B.L. designed and planned experiments. A.H. S.Z. D.R.-L. G.R. X.W. L.T. P.W. Y.E. I.E. and Z.B.L. performed experiments and collected data. A.H. S.Z. N.D. X.W. J.K. P.W. M.E.B. I.E. and Z.B.L. analyzed data and A.H. I.E. and Z.B.L. wrote the manuscript with input from M.E.B. and Y.E. All authors read, edited, and approved the manuscript. Z.B.L. is a consultant for and a member of the Scientific Strategy Board of Inari Agriculture, and he is also a named inventor on a number of patents and patent applications directed to related technology that have been exclusively licensed from CSHL to Inari Agriculture. Publisher Copyright: © 2021 Elsevier Inc.

PY - 2021/4/1

Y1 - 2021/4/1

N2 - Functional

AB - Functional

KW - ATAC sequencing

KW - Arabidopsis

KW - Brassicaceae

KW - Solanaceae

KW - cis-regulatory

KW - conserved non-coding sequences

KW - homeobox

KW - inflorescence

KW - plant development

KW - pleiotropy

KW - tomato

UR - http://www.scopus.com/inward/record.url?scp=85103257271&partnerID=8YFLogxK

U2 - 10.1016/j.cell.2021.02.001

DO - 10.1016/j.cell.2021.02.001

M3 - Article

C2 - 33667348

AN - SCOPUS:85103257271

SN - 0092-8674

VL - 184

SP - 1724-1739.e16

JO - Cell

JF - Cell

IS - 7

ER -

Conserved pleiotropy of an ancient plant homeobox gene uncovered by cis-regulatory dissection

Abstract

Bibliographical note

Keywords

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