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

Cell. 2021 Jun 10;184(12):3333-3348.e19. doi: 10.1016/j.cell.2021.04.024. Epub 2021 May 18.

Authors

Kaisa Kajala¹, Mona Gouran², Lidor Shaar-Moshe³, G Alex Mason³, Joel Rodriguez-Medina⁴, Dorota Kawa³, Germain Pauluzzi⁵, Mauricio Reynoso⁶, Alex Canto-Pastor³, Concepcion Manzano³, Vincent Lau⁷, Mariana A S Artur⁸, Donnelly A West⁹, Sharon B Gray³, Alexander T Borowsky⁵, Bryshal P Moore¹⁰, Andrew I Yao¹¹, Kevin W Morimoto³, Marko Bajic¹², Elide Formentin¹³, Niba A Nirmal³, Alan Rodriguez³, Asher Pasha⁷, Roger B Deal¹², Daniel J Kliebenstein¹⁴, Torgeir R Hvidsten¹⁵, Nicholas J Provart⁷, Neelima R Sinha¹⁶, Daniel E Runcie¹⁴, Julia Bailey-Serres¹⁷, Siobhan M Brady¹⁸

Affiliations

¹ Department of Plant Biology and Genome Center, University of California, Davis, Davis, CA 95616, USA; Plant Ecophysiology, Institute of Environmental Biology, Utrecht University, 3584 Utrecht, the Netherlands.
² Department of Plant Biology and Genome Center, University of California, Davis, Davis, CA 95616, USA; Plant Biology Graduate Group, University of California, Davis, Davis, CA 95616, USA.
³ Department of Plant Biology and Genome Center, University of California, Davis, Davis, CA 95616, USA.
⁴ Department of Plant Biology and Genome Center, University of California, Davis, Davis, CA 95616, USA; Integrative Genetics and Genomics Graduate Group, University of California, Davis, Davis, CA 95616, USA.
⁵ Center for Plant Cell Biology, Department of Botany and Plant Sciences, University of California, Riverside, Riverside, CA 92521, USA.
⁶ Center for Plant Cell Biology, Department of Botany and Plant Sciences, University of California, Riverside, Riverside, CA 92521, USA; IBBM, FCE-UNLP CONICET, La Plata 1900, Argentina.
⁷ Department of Cell and Systems Biology/Centre for the Analysis of Genome Evolution and Function, University of Toronto, 25 Willcocks St., Toronto, ON M5S 3B2, Canada.
⁸ Plant Ecophysiology, Institute of Environmental Biology, Utrecht University, 3584 Utrecht, the Netherlands.
⁹ Integrative Genetics and Genomics Graduate Group, University of California, Davis, Davis, CA 95616, USA; Department of Plant Biology, University of California, Davis, Davis, CA 95616, USA.
¹⁰ Fort Valley State University, Fort Valley, GA 31030, USA.
¹¹ Department of Biomedical Engineering and Genome Center, University of California, Davis, Davis, CA 95616, USA.
¹² Department of Biology, Emory University, Atlanta, GA 30322, USA.
¹³ Center for Plant Cell Biology, Department of Botany and Plant Sciences, University of California, Riverside, Riverside, CA 92521, USA; Department of Biology, University of Padova, Padova, Italy.
¹⁴ Department of Plant Sciences, University of California, Davis, Davis, CA 95616, USA.
¹⁵ Faculty of Chemistry, Biotechnology and Food Science, Norwegian University of Life Sciences, 1432 Ås, Norway.
¹⁶ Department of Plant Biology, University of California, Davis, Davis, CA 95616, USA.
¹⁷ Plant Ecophysiology, Institute of Environmental Biology, Utrecht University, 3584 Utrecht, the Netherlands; Center for Plant Cell Biology, Department of Botany and Plant Sciences, University of California, Riverside, Riverside, CA 92521, USA.
¹⁸ Department of Plant Biology and Genome Center, University of California, Davis, Davis, CA 95616, USA. Electronic address: sbrady@ucdavis.edu.

PMID: 34010619
DOI: 10.1016/j.cell.2021.04.024

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.

Publication types

Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

Arabidopsis / genetics*
Gene Expression Regulation, Plant
Gene Regulatory Networks
Genes, Plant*
Green Fluorescent Proteins / metabolism
Inventions*
Meristem / metabolism
Plant Proteins / genetics
Plant Proteins / metabolism
Plant Roots / cytology
Plant Roots / genetics*
Plant Roots / growth & development*
Promoter Regions, Genetic / genetics
Protein Biosynthesis
Solanum lycopersicum / cytology
Solanum lycopersicum / genetics*
Species Specificity
Transcription Factors / metabolism
Xylem / genetics

Substances

Plant Proteins
Transcription Factors
Green Fluorescent Proteins

Grants and funding

55108506/HHMI/Howard Hughes Medical Institute/United States