Mobile PEAR transcription factors integrate positional cues to prime cambial growth

Miyashima, Shunsuke; Roszak, Pawel; Sevilem, Iris; Toyokura, Koichi; Blob, Bernhard; Heo, Jung ok; Mellor, Nathan; Help-Rinta-Rahko, Hanna; Otero, Sofia; Smet, Wouter; Boekschoten, Mark; Hooiveld, Guido; Hashimoto, Kayo; Wallner, Eva Sophie; Kondo, Yuki; Melnyk, Charles; Greb, Thomas; Nakajima, Keiji; Sozzani, Ross; Bishopp, Anthony; De Rybel, Bert; Helariutta, Yk�

Abstract

© 2019, Springer Nature Limited. Apical growth in plants initiates upon seed germination, whereas radial growth is primed only during early ontogenesis in procambium cells and activated later by the vascular cambium 1 . Although it is not known how radial growth is organized and regulated in plants, this system resembles the developmental competence observed in some animal systems, in which pre-existing patterns of developmental potential are established early on 2,3 . Here we show that in Arabidopsis the initiation of radial growth occurs around early protophloem-sieve-element cell files of the root procambial tissue. In this domain, cytokinin signalling promotes the expression of a pair of mobile transcription factors—PHLOEM EARLY DOF 1 (PEAR1) and PHLOEM EARLY DOF 2 (PEAR2)—and their four homologues (DOF6, TMO6, OBP2 and HCA2), which we collectively name PEAR proteins. The PEAR proteins form a short-range concentration gradient that peaks at protophloem sieve elements, and activates gene expression that promotes radial growth. The expression and function of PEAR proteins are antagonized by the HD-ZIP III proteins, well-known polarity transcription factors 4 —the expression of which is concentrated in the more-internal domain of radially non-dividing procambial cells by the function of auxin, and mobile miR165 and miR166 microRNAs. The PEAR proteins locally promote transcription of their inhibitory HD-ZIP III genes, and thereby establish a negative-feedback loop that forms a robust boundary that demarks the zone of cell division. Taken together, our data establish that during root procambial development there exists a network in which a module that links PEAR and HD-ZIP III transcription factors integrates spatial information of the hormonal domains and miRNA gradients to provide adjacent zones of dividing and more-quiescent cells, which forms a foundation for further radial growth.

Citation

Miyashima, S., Roszak, P., Sevilem, I., Toyokura, K., Blob, B., Heo, J. O., Mellor, N., Help-Rinta-Rahko, H., Otero, S., Smet, W., Boekschoten, M., Hooiveld, G., Hashimoto, K., Wallner, E. S., Kondo, Y., Melnyk, C., Greb, T., Nakajima, K., Sozzani, R., Bishopp, A., …Helariutta, Y. (2019). Mobile PEAR transcription factors integrate positional cues to prime cambial growth. Nature, 565(7740), 490-494. https://doi.org/10.1038/s41586-018-0839-y

• Journal Article Type: Letter
• Acceptance Date: Dec 4, 2018
• Online Publication Date: Jan 9, 2019
• Publication Date: Jan 24, 2019
• Deposit Date: Jan 7, 2019
• Publicly Available Date: Jul 10, 2019
• Journal: Nature
• Print ISSN: 0028-0836
• Electronic ISSN: 1476-4687
• Publisher: Nature Publishing Group
• Peer Reviewed: Peer Reviewed
• Volume: 565
• Issue: 7740
• Pages: 490-494
• DOI: https://doi.org/10.1038/s41586-018-0839-y
• Public URL: https://nottingham-repository.worktribe.com/output/1446939
• Publisher URL: https://www.nature.com/articles/s41586-018-0839-y?WT.feed_name=subjects_molecular-biology
• Contract Date: Jan 7, 2019