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 & 5 others Keiji Nakajima, Rosangela Sozzani, Anthony Bishopp, Bert de Rybel, Ykä Helariutta*

*Corresponding author for this work

Research output: Contribution to journalLetterAcademicpeer-review

13 Citations (Scopus)

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.

Original languageEnglish
Pages (from-to)490-494
JournalNature
Volume565
Issue number7740
DOIs
Publication statusPublished - 24 Jan 2019

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Cues
Transcription Factors
Growth
Proteins
MicroRNAs
Cytokinins
Indoleacetic Acids
Germination
Arabidopsis
Cell Division
Mental Competency
Names
Blood Vessels
Seeds
Gene Expression
Genes

Cite this

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
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 ; Smetana, Ondřej ; Siligato, Riccardo ; Wallner, Eva Sophie ; Mähönen, Ari Pekka ; Kondo, Yuki ; Melnyk, Charles W. ; Greb, Thomas ; Nakajima, Keiji ; Sozzani, Rosangela ; Bishopp, Anthony ; de Rybel, Bert ; Helariutta, Ykä. / Mobile PEAR transcription factors integrate positional cues to prime cambial growth. In: Nature. 2019 ; Vol. 565, No. 7740. pp. 490-494.
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title = "Mobile PEAR transcription factors integrate positional cues to prime cambial growth",
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.",
author = "Shunsuke Miyashima and Pawel Roszak and Iris Sevilem and Koichi Toyokura and Bernhard Blob and Jung-Ok Heo and Nathan Mellor and Hanna Help-Rinta-Rahko and Sofia Otero and Wouter Smet and Mark Boekschoten and Guido Hooiveld and Kayo Hashimoto and Ondřej Smetana and Riccardo Siligato and Wallner, {Eva Sophie} and M{\"a}h{\"o}nen, {Ari Pekka} and Yuki Kondo and Melnyk, {Charles W.} and Thomas Greb and Keiji Nakajima and Rosangela Sozzani and Anthony Bishopp and {de Rybel}, Bert and Yk{\"a} Helariutta",
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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, Smetana, O, Siligato, R, Wallner, ES, Mähönen, AP, Kondo, Y, Melnyk, CW, Greb, T, Nakajima, K, Sozzani, R, Bishopp, A, de Rybel, B & Helariutta, Y 2019, 'Mobile PEAR transcription factors integrate positional cues to prime cambial growth', Nature, vol. 565, no. 7740, pp. 490-494. https://doi.org/10.1038/s41586-018-0839-y

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; Smetana, Ondřej; Siligato, Riccardo; Wallner, Eva Sophie; Mähönen, Ari Pekka; Kondo, Yuki; Melnyk, Charles W.; Greb, Thomas; Nakajima, Keiji; Sozzani, Rosangela; Bishopp, Anthony; de Rybel, Bert; Helariutta, Ykä.

In: Nature, Vol. 565, No. 7740, 24.01.2019, p. 490-494.

Research output: Contribution to journalLetterAcademicpeer-review

TY - JOUR

T1 - Mobile PEAR transcription factors integrate positional cues to prime cambial growth

AU - Miyashima, Shunsuke

AU - Roszak, Pawel

AU - Sevilem, Iris

AU - Toyokura, Koichi

AU - Blob, Bernhard

AU - Heo, Jung-Ok

AU - Mellor, Nathan

AU - Help-Rinta-Rahko, Hanna

AU - Otero, Sofia

AU - Smet, Wouter

AU - Boekschoten, Mark

AU - Hooiveld, Guido

AU - Hashimoto, Kayo

AU - Smetana, Ondřej

AU - Siligato, Riccardo

AU - Wallner, Eva Sophie

AU - Mähönen, Ari Pekka

AU - Kondo, Yuki

AU - Melnyk, Charles W.

AU - Greb, Thomas

AU - Nakajima, Keiji

AU - Sozzani, Rosangela

AU - Bishopp, Anthony

AU - de Rybel, Bert

AU - Helariutta, Ykä

PY - 2019/1/24

Y1 - 2019/1/24

N2 - 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.

AB - 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.

U2 - 10.1038/s41586-018-0839-y

DO - 10.1038/s41586-018-0839-y

M3 - Letter

VL - 565

SP - 490

EP - 494

JO - Nature

JF - Nature

SN - 0028-0836

IS - 7740

ER -

Miyashima S, Roszak P, Sevilem I, Toyokura K, Blob B, Heo J-O et al. Mobile PEAR transcription factors integrate positional cues to prime cambial growth. Nature. 2019 Jan 24;565(7740):490-494. https://doi.org/10.1038/s41586-018-0839-y