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., …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