Innovation, conservation, and repurposing of gene function in root cell type development
Kajala, Kaisa; Gouran, Mona; Shaar-Moshe, Lidor; Mason, G. Alex; Rodriguez-Medina, Joel; Kawa, Dorota; Pauluzzi, Germain; Reynoso, Mauricio; Canto-Pastor, Alex; Manzano, Concepcion; Lau, Vincent; Artur, Mariana A.S.; West, Donnelly A.; Gray, Sharon B.; Borowsky, Alexander T.; Moore, Bryshal P.; Yao, Andrew I.; Morimoto, Kevin W.; Bajic, Marko; Formentin, Elide; Nirmal, Niba A.; Rodriguez, Alan; Pasha, Asher; Deal, Roger B.; Kliebenstein, Daniel J.; Hvidsten, Torgeir R.; Provart, Nicholas J.; Sinha, Neelima R.; Runcie, Daniel E.; Bailey-Serres, Julia; Brady, Siobhan M.
(2021) Cell, volume 184, issue 12, pp. 3333 - 3348.e19
(Article)
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
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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.
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Keywords: cell types, evolution, exodermis, gene regulation, rice, root development, tomato, translatomes, xylem, Biochemistry, Genetics and Molecular Biology(all)
ISSN: 0092-8674
Publisher: Cell Press
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: © 2021 The Author(s)
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