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

• Type of Material: Article
• Authors: Kaisa Kajala, University of California Davis; Mona Gouran, University of California Davis; Lidor Shaar-Moshe, University of California Davis; G. Alex Mason, University of California Davis; Joel Rodriguez-Medina, University of California Davis; Dorota Kawa, University of California Davis; Germain Pauluzzi, University of California Riverside; Mauricio Reynoso, University of California Riverside; Alex Canto-Pastor, University of California Davis; Concepcion Manzano, University of California Davis; Vincent Lau, University of Toronto; Mariana A. A. Artur, Utrecht University; Donnelly A. West, University of California Davis; Sharon B. Gray, University of California Davis; Alexander T. Borowsky, University of California Riverside; Bryshal P. Moore, Fort Valley State University; Andrew I. Yao, University of California Davis; Kevin W. Morimoto, University of California Davis; Marko Bajic, Emory University; Elide Formentin, University of California Riverside; Niba A. Nirmal, University of California Davis; Alan Rodriguez, University of California Davis; Asher Pasha, University of Toronto; Roger Deal, Emory University; Daniel J. Kliebenstein, University of California Davis; Torgeir R. Hvidsten, Norwegian University of Life Sciences; Nicholas J. Provart, University of Toronto; Neelima R. Sinha, University of California Davis; Daniel E. Runcie, University of California Davis; Julia Bailey-Serres, Utrecht University; Siobhan M. Brady, University of California Davis
• Language: English
• Date: 2021-06-10
• Publisher: Elsevier
• Publication Version: Final Published Version
• Copyright Statement: © 2021 The Author(s). Published by Elsevier Inc.
• License: Creative Commons Attribution-NonCommercial-NoDerivs 4.0 International
• Final Published Version (URL): https://doi.org/10.1016/j.cell.2021.04.024
• Title of Journal or Parent Work: Cell
• Volume: 184
• Issue: 12
• Start Page: 3333
• End Page: 3348.e19
• Grant/Funding Information: 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.
• Keywords: exodermis; xylem; translatomes; gene regulation; cell types; tomato; evolution; rice; root development
• Research Categories: Biology, Cell; Biology, Plant Physiology; Biology, Genetics

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.