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

• Published in: Cell Vol. 184; no. 12; pp. 3333 - 3348.e19
• Main Authors: 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.
• Format: Journal Article
• Language: English
• Published: United States Elsevier Inc 10-06-2021
• Subjects: Arabidopsis - genetics; cell types; evolution; exodermis; Gene Expression Regulation, Plant; gene regulation; Gene Regulatory Networks; Genes, Plant; Green Fluorescent Proteins - metabolism; Inventions; Lycopersicon esculentum - cytology; Lycopersicon esculentum - genetics; Meristem - metabolism; Plant Proteins - genetics; Plant Proteins - metabolism; Plant Roots - cytology; Plant Roots - genetics; Plant Roots - growth & development; Promoter Regions, Genetic - genetics; Protein Biosynthesis; rice; root development; Species Specificity; tomato; Transcription Factors - metabolism; translatomes; xylem; Xylem - genetics; xylem; root development; translatomes; gene regulation; cell types; tomato; evolution; exodermis; rice
• ISSN: 0092-8674; 1097-4172
• DOI: 10.1016/j.cell.2021.04.024

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.
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•Tomato cell type-resolution translatome atlas reveals cell type function•Conservation and repurposing in gene regulation between Arabidopsis and tomato•The tomato exodermis is lignified, suberized, and enriched for nitrogen regulation•The root meristem is molecularly homologous across plant species
The integration of pan-species cell type data reveals molecular signatures across growth conditions and sheds light on novelty, conservation, and repurposing of gene function relevant to crop engineering.