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^*

^*Corresponding author for this work

Sub Plant Ecophysiology

Research output: Contribution to journal › Article › Academic › 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
Article number	e19
Pages (from-to)	3333-3348.e19
Journal	Cell
Volume	184
Issue number	12
DOIs	https://doi.org/10.1016/j.cell.2021.04.024
Publication status	Published - 10 Jun 2021

Keywords

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

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10.1016/j.cell.2021.04.024Licence: CC BY-NC-ND

PIIS0092867421005043Final published version, 17.9 MBLicence: CC BY-NC-ND

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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. Article e19. https://doi.org/10.1016/j.cell.2021.04.024

@article{05430b92c8cd491b84e48349aa64b799,

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 = "Funding Information: We would like to thank H. Masson, R.M. Sanz, A. Gothberg, S. Vitales, J. Zheng, K. Zumstein, and B. Waring for experimental assistance; T. Demura, E. Kellogg, and K. Bubb for discussion; A. Hay for seed; and P. Benfey, N. Geldner, L. Strader, and J. Harada for manuscript critique. Funding was as follows: S.M.B. by HHMI 55108506; S.B.G. by NSF PGRP IOS-1306848; R.B.D. N.R.S. J.B.-S. and S.M.B. by NSF PGRP IOS-123824 and IOS-1856749; J.B.-S. and A.T.B. by NSF PGRP IOS-1810468; T.R.H. by the US-Norway Fulbright Foundation; K.K. by an SKR Postdoctoral Fellowship and MSCA RI Fellowship 790057; J.R.-M. by UC-MEXUS/CONACYT; A.T.B. by NSF DGE-1922642; D.J.K. by NSF MCB 1906486 and SDA NIFA Hatch CA-D-PLS-7033-H; V.L. by a Michael Smith Foreign Studies Supplement; V.L. and N.J.P. by an NSERC and OG-128; C.M. by MSCA Global Fellowship 655406; G.A.M. by NSF PGRP IOS-1907088; D.E.R. by USDA NIFA Hatch 1010469; L.S.-M. by BARD FI-570-2018; N.R.S. by NSF IOS-1558900; and B.P.M. by the PABGAP grant, funded by the UCOP/UC-HBCU Initiative. Conceptualization, K.K. L.S.-M. G.A.M. G.P. M.R. D.A.W. S.B.G. N.R.S. D.E.R. J.B.-S. and S.M.B.; data curation, K.K. L.S.-M. G.A.M. J.R.-M. D.K. G.P. M.R. A.C.-P. C.M. K.M. and M.G.; formal analysis, K.K. L.S.-M. G.A.M. M.G. J.R.-M. D.K. A.C.-P. V.L. A.T.B. D.J.K. T.R.H. N.R.S. and D.E.R.; funding acquisition, K.K. L.S.-M. G.A.M. R.B.D. N.J.P. N.R.S. J.B.-S. and S.M.B.; investigation, K.K. L.S.-M. G.A.M. M.G. J.R.-M. D.K. G.P. M.R. V.L. M.A.S.A. D.A.W. C.M. S.B.G. A.I.Y. M.B. E.F. N.A.N. A.R. A.T.B. and S.M.B.; methodology, K.K. L.S.-M. G.A.M. J.R.-M. M.G. G.P. M.R. A.T.B. M.B. D.E.R. and S.M.B.; project administration, R.B.D. N.R.S. J.B.-S. and S.M.B.; software, L.S.-M. G.A.M. J.R.-M. A.C.-P. V.L. A.T.B. T.R.H. N.J.P. and D.E.R.; supervision, K.K. L.S.-M. G.A.M. J.R.-M. C.M. R.B.D. T.R.H. N.J.P. N.R.S. D.E.R. J.B.-S. and S.M.B.; validation, K.K. L.S.-M. G.A.M. M.G. J.R.-M. D.K. G.P. M.R. C.M. K.M. A.C.-P. M.A.S.A. D.E.R. and S.M.B.; visualization, K.K. L.S.-M. G.A.M. M.G. J.R.-M. D.K. G.P. M.R. V.L. M.A.S.A. D.W. C.M. N.J.P. and S.M.B.; writing ? original draft, K.K. L.S.-M. G.A.M. M.G. J.R.-M. A.T.B. D.K. M.A.S.A. and S.M.B.; writing ? review & editing, K.K. L.S.-M. G.A.M. M.G. J.R.-M. D.K. M.R. A.C.-P. M.A.S.A. D.W. C.M. A.T.B. R.B.D. D.J.K. N.R.S. D.E.R. J.B.-S. and S.M.B. The authors declare no competing interests. One or more of the authors of this paper self-identifies as an underrepresented ethnic minority in science. One or more of the authors of this paper self-identifies as a member of the LGBTQ+ community. One or more of the authors of this paper received support from a program designed to increase minority representation in science. The author list of this paper includes contributors from the location where the research was conducted who participated in the data collection, design, analysis, and/or interpretation of the work. Funding Information: We would like to thank H. Masson, R.M. Sanz, A. Gothberg, S. Vitales, J. Zheng, K. Zumstein, and B. Waring for experimental assistance; T. Demura, E. Kellogg, and K. Bubb for discussion; A. Hay for seed; and P. Benfey, N. Geldner, L. Strader, and J. Harada for manuscript critique. Funding was as follows: S.M.B. by HHMI 55108506 ; S.B.G. by NSF PGRP IOS-1306848 ; R.B.D., N.R.S., J.B.-S., and S.M.B. by NSF PGRP IOS-123824 and IOS-1856749 ; J.B.-S. and A.T.B. by NSF PGRP IOS-1810468 ; T.R.H. by the US-Norway Fulbright Foundation ; K.K. by an SKR Postdoctoral Fellowship and MSCA RI Fellowship 790057 ; J.R.-M. by UC-MEXUS/CONACYT ; A.T.B. by NSF DGE-1922642 ; D.J.K. by NSF MCB 1906486 and SDA NIFA Hatch CA-D-PLS-7033-H ; V.L. by a Michael Smith Foreign Studies Supplement ; V.L. and N.J.P. by an NSERC and OG-128; C.M. by MSCA Global Fellowship 655406 ; G.A.M. by NSF PGRP IOS-1907088 ; D.E.R. by USDA NIFA Hatch 1010469 ; L.S.-M. by BARD FI-570-2018 ; N.R.S. by NSF IOS-1558900 ; and B.P.M. by the PABGAP grant , funded by the UCOP/UC-HBCU Initiative . 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",

publisher = "Elsevier",

number = "12",

}

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, e19, 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.

N1 - Funding Information: We would like to thank H. Masson, R.M. Sanz, A. Gothberg, S. Vitales, J. Zheng, K. Zumstein, and B. Waring for experimental assistance; T. Demura, E. Kellogg, and K. Bubb for discussion; A. Hay for seed; and P. Benfey, N. Geldner, L. Strader, and J. Harada for manuscript critique. Funding was as follows: S.M.B. by HHMI 55108506; S.B.G. by NSF PGRP IOS-1306848; R.B.D. N.R.S. J.B.-S. and S.M.B. by NSF PGRP IOS-123824 and IOS-1856749; J.B.-S. and A.T.B. by NSF PGRP IOS-1810468; T.R.H. by the US-Norway Fulbright Foundation; K.K. by an SKR Postdoctoral Fellowship and MSCA RI Fellowship 790057; J.R.-M. by UC-MEXUS/CONACYT; A.T.B. by NSF DGE-1922642; D.J.K. by NSF MCB 1906486 and SDA NIFA Hatch CA-D-PLS-7033-H; V.L. by a Michael Smith Foreign Studies Supplement; V.L. and N.J.P. by an NSERC and OG-128; C.M. by MSCA Global Fellowship 655406; G.A.M. by NSF PGRP IOS-1907088; D.E.R. by USDA NIFA Hatch 1010469; L.S.-M. by BARD FI-570-2018; N.R.S. by NSF IOS-1558900; and B.P.M. by the PABGAP grant, funded by the UCOP/UC-HBCU Initiative. Conceptualization, K.K. L.S.-M. G.A.M. G.P. M.R. D.A.W. S.B.G. N.R.S. D.E.R. J.B.-S. and S.M.B.; data curation, K.K. L.S.-M. G.A.M. J.R.-M. D.K. G.P. M.R. A.C.-P. C.M. K.M. and M.G.; formal analysis, K.K. L.S.-M. G.A.M. M.G. J.R.-M. D.K. A.C.-P. V.L. A.T.B. D.J.K. T.R.H. N.R.S. and D.E.R.; funding acquisition, K.K. L.S.-M. G.A.M. R.B.D. N.J.P. N.R.S. J.B.-S. and S.M.B.; investigation, K.K. L.S.-M. G.A.M. M.G. J.R.-M. D.K. G.P. M.R. V.L. M.A.S.A. D.A.W. C.M. S.B.G. A.I.Y. M.B. E.F. N.A.N. A.R. A.T.B. and S.M.B.; methodology, K.K. L.S.-M. G.A.M. J.R.-M. M.G. G.P. M.R. A.T.B. M.B. D.E.R. and S.M.B.; project administration, R.B.D. N.R.S. J.B.-S. and S.M.B.; software, L.S.-M. G.A.M. J.R.-M. A.C.-P. V.L. A.T.B. T.R.H. N.J.P. and D.E.R.; supervision, K.K. L.S.-M. G.A.M. J.R.-M. C.M. R.B.D. T.R.H. N.J.P. N.R.S. D.E.R. J.B.-S. and S.M.B.; validation, K.K. L.S.-M. G.A.M. M.G. J.R.-M. D.K. G.P. M.R. C.M. K.M. A.C.-P. M.A.S.A. D.E.R. and S.M.B.; visualization, K.K. L.S.-M. G.A.M. M.G. J.R.-M. D.K. G.P. M.R. V.L. M.A.S.A. D.W. C.M. N.J.P. and S.M.B.; writing ? original draft, K.K. L.S.-M. G.A.M. M.G. J.R.-M. A.T.B. D.K. M.A.S.A. and S.M.B.; writing ? review & editing, K.K. L.S.-M. G.A.M. M.G. J.R.-M. D.K. M.R. A.C.-P. M.A.S.A. D.W. C.M. A.T.B. R.B.D. D.J.K. N.R.S. D.E.R. J.B.-S. and S.M.B. The authors declare no competing interests. One or more of the authors of this paper self-identifies as an underrepresented ethnic minority in science. One or more of the authors of this paper self-identifies as a member of the LGBTQ+ community. One or more of the authors of this paper received support from a program designed to increase minority representation in science. The author list of this paper includes contributors from the location where the research was conducted who participated in the data collection, design, analysis, and/or interpretation of the work. Funding Information: We would like to thank H. Masson, R.M. Sanz, A. Gothberg, S. Vitales, J. Zheng, K. Zumstein, and B. Waring for experimental assistance; T. Demura, E. Kellogg, and K. Bubb for discussion; A. Hay for seed; and P. Benfey, N. Geldner, L. Strader, and J. Harada for manuscript critique. Funding was as follows: S.M.B. by HHMI 55108506 ; S.B.G. by NSF PGRP IOS-1306848 ; R.B.D., N.R.S., J.B.-S., and S.M.B. by NSF PGRP IOS-123824 and IOS-1856749 ; J.B.-S. and A.T.B. by NSF PGRP IOS-1810468 ; T.R.H. by the US-Norway Fulbright Foundation ; K.K. by an SKR Postdoctoral Fellowship and MSCA RI Fellowship 790057 ; J.R.-M. by UC-MEXUS/CONACYT ; A.T.B. by NSF DGE-1922642 ; D.J.K. by NSF MCB 1906486 and SDA NIFA Hatch CA-D-PLS-7033-H ; V.L. by a Michael Smith Foreign Studies Supplement ; V.L. and N.J.P. by an NSERC and OG-128; C.M. by MSCA Global Fellowship 655406 ; G.A.M. by NSF PGRP IOS-1907088 ; D.E.R. by USDA NIFA Hatch 1010469 ; L.S.-M. by BARD FI-570-2018 ; N.R.S. by NSF IOS-1558900 ; and B.P.M. by the PABGAP grant , funded by the UCOP/UC-HBCU Initiative . Publisher Copyright: © 2021 The Author(s)

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

M1 - e19

ER -

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

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