Plants continuously form new organs in different developmental contexts in response to environmental cues. Underground lateral roots initiate from prepatterned cells in the main root, but cells can also bypass the root-shoot trajectory separation and generate shoot-borne roots through an unknown mechanism. We mapped tomato (Solanum lycopersicum) shoot-borne root development at single-cell resolution and showed that these roots initiate from phloem-associated cells through a unique transition state. This state requires the activity of a transcription factor that we named SHOOTBORNE ROOTLESS (SBRL). Evolutionary analysis reveals that SBRL’s function and cis regulation are conserved in angiosperms and that it arose as an ancient duplication, with paralogs controlling wound-induced and lateral root initiation. We propose that the activation of a common transition state by context-specific regulators underlies the plasticity of plant root systems.
Bibliographical noteFunding Information:
We thank T. Beeckman, Y. Eshed, Z. Lippman, and S. Savaldi-Goldstein for comments and discussions; M. De Martino for setting up the CRISPR system; I. Pri-Tal for tissue culture work; O. Roth for assistance in etiolated seedlings assay; and M. Chemla for assistance in library preparation. Funding: I.E. is supported by a Howard Hughes Medical Institute International Research Scholar grant (grant no. 55008730) and the Israeli Science Foundation (grant no. ISF966/17). A.H. is supported by National Science Foundation grant Plant Genome Research Program grant IOS-1546837 to Z.B.L. Author contributions: M.O., N.G.-Y., and I.E. conceived and designed the study and performed the experiments. C.Y. performed the shoot-borne root quantification and lateral root RNA-Seq assay. A.H. performed in situ hybridizations. E.S. performed potato transformation. I.E., N.G.-Y., and M.O. wrote the manuscript. Competing interests: The authors declare no competing interests. Data and materials availability: Raw and processed data are available at the Gene Expression Omnibus (GEO; single-cell data: GSE159055; lateral root transcriptome data: GSE159050). All other data are available in the main paper or the supplementary materials.
© 2022 American Association for the Advancement of Science. All rights reserved.
- Gene Expression Regulation, Plant
- Genes, Plant
- Genetic Loci
- Lycopersicon esculentum/genetics
- Meristem/growth & development
- Plant Proteins/genetics
- Plant Roots/cytology
- Plant Shoots/cytology
- Single-Cell Analysis
- Transcription, Genetic