Innovation, conservation, and repurposing of gene function in root cell type development

Kaisa Kajala; Mona Gouran; Lidor Shaar-Moshe; G. Alex Mason; Joel Rodriguez-Medina; Dorota Kawa; Germain Pauluzzi; Mauricio Reynoso; Alex Canto-Pastor; Concepcion Manzano; Vincent Lau; Mariana A.S. Artur; Donnelly A. West; Sharon B. Gray; Alexander T. Borowsky; Bryshal P. Moore; Andrew I. Yao; Kevin W. Morimoto; Marko Bajic; Elide Formentin; Niba A. Nirmal; Alan Rodriguez; Asher Pasha; Roger B. Deal; Daniel J. Kliebenstein; Torgeir R. Hvidsten; Nicholas J. Provart; Neelima R. Sinha; Daniel E. Runcie; Julia Bailey-Serres; Siobhan M. Brady

doi:10.1016/j.cell.2021.04.024

Innovation, conservation, and repurposing of gene function in root cell type development

Kaisa Kajala, Mona Gouran, Lidor Shaar-Moshe, G. Alex Mason, Joel Rodriguez-Medina, Dorota Kawa, Germain Pauluzzi, Mauricio Reynoso, Alex Canto-Pastor, Concepcion Manzano, Vincent Lau, Mariana A.S. Artur, Donnelly A. West, Sharon B. Gray, Alexander T. Borowsky, Bryshal P. Moore, Andrew I. Yao, Kevin W. Morimoto, Marko Bajic, Elide FormentinNiba A. Nirmal, Alan Rodriguez, Asher Pasha, Roger B. Deal, Daniel J. Kliebenstein, Torgeir R. Hvidsten, Nicholas J. Provart, Neelima R. Sinha, Daniel E. Runcie, Julia Bailey-Serres, Siobhan M. Brady

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

Abstract

Plant species have evolved myriads of solutions, including complex cell type development and regulation, to adapt to dynamic environments. To understand this cellular diversity, we profiled tomato root cell type translatomes. Using xylem differentiation in tomato, examples of functional innovation, repurposing, and conservation of transcription factors are described, relative to the model plant Arabidopsis. Repurposing and innovation of genes are further observed within an exodermis regulatory network and illustrate its function. Comparative translatome analyses of rice, tomato, and Arabidopsis cell populations suggest increased expression conservation of root meristems compared with other homologous populations. In addition, the functions of constitutively expressed genes are more conserved than those of cell type/tissue-enriched genes. These observations suggest that higher order properties of cell type and pan-cell type regulation are evolutionarily conserved between plants and animals.

Original language	English
Pages (from-to)	3333-3348.e19
Journal	Cell
Volume	184
Issue number	12
DOIs	https://doi.org/10.1016/j.cell.2021.04.024
State	Published - 10 Jun 2021
Externally published	Yes

Bibliographical note

Publisher Copyright:
© 2021 The Author(s)

Keywords

cell types
evolution
exodermis
gene regulation
rice
root development
tomato
translatomes
xylem

ASJC Scopus subject areas

General Biochemistry, Genetics and Molecular Biology

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10.1016/j.cell.2021.04.024

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Kajala, K., Gouran, M., Shaar-Moshe, L., Mason, G. A., Rodriguez-Medina, J., Kawa, D., Pauluzzi, G., Reynoso, M., Canto-Pastor, A., Manzano, C., Lau, V., Artur, M. A. S., West, D. A., Gray, S. B., Borowsky, A. T., Moore, B. P., Yao, A. I., Morimoto, K. W., Bajic, M., ... Brady, S. M. (2021). Innovation, conservation, and repurposing of gene function in root cell type development. Cell, 184(12), 3333-3348.e19. https://doi.org/10.1016/j.cell.2021.04.024

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title = "Innovation, conservation, and repurposing of gene function in root cell type development",

abstract = "Plant species have evolved myriads of solutions, including complex cell type development and regulation, to adapt to dynamic environments. To understand this cellular diversity, we profiled tomato root cell type translatomes. Using xylem differentiation in tomato, examples of functional innovation, repurposing, and conservation of transcription factors are described, relative to the model plant Arabidopsis. Repurposing and innovation of genes are further observed within an exodermis regulatory network and illustrate its function. Comparative translatome analyses of rice, tomato, and Arabidopsis cell populations suggest increased expression conservation of root meristems compared with other homologous populations. In addition, the functions of constitutively expressed genes are more conserved than those of cell type/tissue-enriched genes. These observations suggest that higher order properties of cell type and pan-cell type regulation are evolutionarily conserved between plants and animals.",

keywords = "cell types, evolution, exodermis, gene regulation, rice, root development, tomato, translatomes, xylem",

author = "Kaisa Kajala and Mona Gouran and Lidor Shaar-Moshe and Mason, {G. Alex} and Joel Rodriguez-Medina and Dorota Kawa and Germain Pauluzzi and Mauricio Reynoso and Alex Canto-Pastor and Concepcion Manzano and Vincent Lau and Artur, {Mariana A.S.} and West, {Donnelly A.} and Gray, {Sharon B.} and Borowsky, {Alexander T.} and Moore, {Bryshal P.} and Yao, {Andrew I.} and Morimoto, {Kevin W.} and Marko Bajic and Elide Formentin and Nirmal, {Niba A.} and Alan Rodriguez and Asher Pasha and Deal, {Roger B.} and Kliebenstein, {Daniel J.} and Hvidsten, {Torgeir R.} and Provart, {Nicholas J.} and Sinha, {Neelima R.} and Runcie, {Daniel E.} and Julia Bailey-Serres and Brady, {Siobhan M.}",

note = "Publisher Copyright: {\textcopyright} 2021 The Author(s)",

year = "2021",

month = jun,

day = "10",

doi = "10.1016/j.cell.2021.04.024",

language = "English",

volume = "184",

pages = "3333--3348.e19",

journal = "Cell",

issn = "0092-8674",

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Kajala, K, Gouran, M, Shaar-Moshe, L, Mason, GA, Rodriguez-Medina, J, Kawa, D, Pauluzzi, G, Reynoso, M, Canto-Pastor, A, Manzano, C, Lau, V, Artur, MAS, West, DA, Gray, SB, Borowsky, AT, Moore, BP, Yao, AI, Morimoto, KW, Bajic, M, Formentin, E, Nirmal, NA, Rodriguez, A, Pasha, A, Deal, RB, Kliebenstein, DJ, Hvidsten, TR, Provart, NJ, Sinha, NR, Runcie, DE, Bailey-Serres, J & Brady, SM 2021, 'Innovation, conservation, and repurposing of gene function in root cell type development', Cell, vol. 184, no. 12, pp. 3333-3348.e19. https://doi.org/10.1016/j.cell.2021.04.024

TY - JOUR

T1 - Innovation, conservation, and repurposing of gene function in root cell type development

AU - Kajala, Kaisa

AU - Gouran, Mona

AU - Shaar-Moshe, Lidor

AU - Mason, G. Alex

AU - Rodriguez-Medina, Joel

AU - Kawa, Dorota

AU - Pauluzzi, Germain

AU - Reynoso, Mauricio

AU - Canto-Pastor, Alex

AU - Manzano, Concepcion

AU - Lau, Vincent

AU - Artur, Mariana A.S.

AU - West, Donnelly A.

AU - Gray, Sharon B.

AU - Borowsky, Alexander T.

AU - Moore, Bryshal P.

AU - Yao, Andrew I.

AU - Morimoto, Kevin W.

AU - Bajic, Marko

AU - Formentin, Elide

AU - Nirmal, Niba A.

AU - Rodriguez, Alan

AU - Pasha, Asher

AU - Deal, Roger B.

AU - Kliebenstein, Daniel J.

AU - Hvidsten, Torgeir R.

AU - Provart, Nicholas J.

AU - Sinha, Neelima R.

AU - Runcie, Daniel E.

AU - Bailey-Serres, Julia

AU - Brady, Siobhan M.

PY - 2021/6/10

Y1 - 2021/6/10

N2 - Plant species have evolved myriads of solutions, including complex cell type development and regulation, to adapt to dynamic environments. To understand this cellular diversity, we profiled tomato root cell type translatomes. Using xylem differentiation in tomato, examples of functional innovation, repurposing, and conservation of transcription factors are described, relative to the model plant Arabidopsis. Repurposing and innovation of genes are further observed within an exodermis regulatory network and illustrate its function. Comparative translatome analyses of rice, tomato, and Arabidopsis cell populations suggest increased expression conservation of root meristems compared with other homologous populations. In addition, the functions of constitutively expressed genes are more conserved than those of cell type/tissue-enriched genes. These observations suggest that higher order properties of cell type and pan-cell type regulation are evolutionarily conserved between plants and animals.

AB - Plant species have evolved myriads of solutions, including complex cell type development and regulation, to adapt to dynamic environments. To understand this cellular diversity, we profiled tomato root cell type translatomes. Using xylem differentiation in tomato, examples of functional innovation, repurposing, and conservation of transcription factors are described, relative to the model plant Arabidopsis. Repurposing and innovation of genes are further observed within an exodermis regulatory network and illustrate its function. Comparative translatome analyses of rice, tomato, and Arabidopsis cell populations suggest increased expression conservation of root meristems compared with other homologous populations. In addition, the functions of constitutively expressed genes are more conserved than those of cell type/tissue-enriched genes. These observations suggest that higher order properties of cell type and pan-cell type regulation are evolutionarily conserved between plants and animals.

KW - cell types

KW - evolution

KW - exodermis

KW - gene regulation

KW - rice

KW - root development

KW - tomato

KW - translatomes

KW - xylem

UR - http://www.scopus.com/inward/record.url?scp=85107420686&partnerID=8YFLogxK

U2 - 10.1016/j.cell.2021.04.024

DO - 10.1016/j.cell.2021.04.024

M3 - Article

C2 - 34010619

AN - SCOPUS:85107420686

SN - 0092-8674

VL - 184

SP - 3333-3348.e19

JO - Cell

JF - Cell

IS - 12

ER -

Innovation, conservation, and repurposing of gene function in root cell type development

Abstract

Bibliographical note

Keywords

ASJC Scopus subject areas

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