Mobile PEAR transcription factors integrate positional cues to prime cambial growth

Shunsuke Miyashima, Pawel Roszak, Iris Sevilem, Koichi Toyokura, Bernhard Blob, Jung-ok Heo, Nathan Mellor, Hanna Help-Rinta-Rahko, Sofia Otero, Wouter Smet, Mark Boekschoten, Guido Hooiveld, Kayo Hashimoto, Ondřej Smetana, Riccardo Siligato, Eva-Sophie Wallner, Ari Pekka Mähönen, Yuki Kondo, Charles W. Melnyk, Thomas Greb, Keiji Nakajima, Rosangela Sozzani, Anthony Bishopp, Bert Rybel () and Ykä Helariutta ()
Additional contact information
Shunsuke Miyashima: University of Helsinki
Pawel Roszak: University of Helsinki
Iris Sevilem: University of Helsinki
Koichi Toyokura: University of Cambridge
Bernhard Blob: University of Cambridge
Jung-ok Heo: University of Helsinki
Nathan Mellor: University of Nottingham
Hanna Help-Rinta-Rahko: University of Helsinki
Sofia Otero: University of Cambridge
Wouter Smet: Ghent University
Mark Boekschoten: Wageningen University
Guido Hooiveld: Wageningen University
Kayo Hashimoto: Nara Institute of Science and Technology
Ondřej Smetana: University of Helsinki
Riccardo Siligato: University of Helsinki
Eva-Sophie Wallner: Heidelberg University
Ari Pekka Mähönen: University of Helsinki
Yuki Kondo: Graduate School of Science, The University of Tokyo
Charles W. Melnyk: University of Cambridge
Thomas Greb: Heidelberg University
Keiji Nakajima: Nara Institute of Science and Technology
Rosangela Sozzani: North Carolina State University
Anthony Bishopp: University of Nottingham
Bert Rybel: Ghent University
Ykä Helariutta: University of Helsinki

Nature, 2019, vol. 565, issue 7740, 490-494

Abstract: Abstract 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 cambium1. 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 on2,3. 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 factors4—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.

Date: 2019
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DOI: 10.1038/s41586-018-0839-y

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