Cell-by-cell dissection of phloem development links a maturation gradient to cell specialization

Pawel Roszak; Jung-Ok Heo; Bernhard Blob; Koichi Toyokura; Yuki Sugiyama; Maria Angels de Luis Balaguer; Winnie W.Y. Lau; Fiona Hamey; Jacopo Cirrone; Ewelina Madej; Alida M. Bouatta; Xin Wang; Marjorie Guichard; Robertas Ursache; Hugo Tavares; Kevin Verstaen; Jos Wendrich; Charles W. Melnyk; Yoshihisa Oda; Dennis Shasha; Sebastian E. Ahnert; Yvan Saeys; Bert De Rybel; Renze Heidstra; Ben Scheres; Guido Grossmann; Ari Pekka Mähönen; Philipp Denninger; Berthold Göttgens; Rosangela Sozzani; Kenneth D. Birnbaum; Yrjö Helariutta

doi:10.1126/science.aba5531

Cell-by-cell dissection of phloem development links a maturation gradient to cell specialization

Pawel Roszak, Jung-Ok Heo, Bernhard Blob, Koichi Toyokura, Yuki Sugiyama, Maria Angels de Luis Balaguer, Winnie W.Y. Lau, Fiona Hamey, Jacopo Cirrone, Ewelina Madej, Alida M. Bouatta, Xin Wang, Marjorie Guichard, Robertas Ursache, Hugo Tavares, Kevin Verstaen, Jos Wendrich, Charles W. Melnyk, Yoshihisa Oda, Dennis ShashaSebastian E. Ahnert, Yvan Saeys, Bert De Rybel, Renze Heidstra, Ben Scheres, Guido Grossmann, Ari Pekka Mähönen, Philipp Denninger, Berthold Göttgens, Rosangela Sozzani^*, Kenneth D. Birnbaum^*, Yrjö Helariutta^*

^*Corresponding author for this work

Research output: Contribution to journal › Article › Academic › peer-review

55 Citations (Scopus)

Abstract

In the plant meristem, tissue-wide maturation gradients are coordinated with specialized cell networks to establish various developmental phases required for indeterminate growth. Here, we used single-cell transcriptomics to reconstruct the protophloem developmental trajectory from the birth of cell progenitors to terminal differentiation in the Arabidopsis thaliana root. PHLOEM EARLY DNA-BINDING-WITH-ONE-FINGER (PEAR) transcription factors mediate lineage bifurcation by activating guanosine triphosphatase signaling and prime a transcriptional differentiation program. This program is initially repressed by a meristem-wide gradient of PLETHORA transcription factors. Only the dissipation of PLETHORA gradient permits activation of the differentiation program that involves mutual inhibition of early versus late meristem regulators. Thus, for phloem development, broad maturation gradients interface with cell-type-specific transcriptional regulators to stage cellular differentiation.

Original language	English
Article number	eaba5531
Journal	Science
Volume	374
Issue number	6575
DOIs	https://doi.org/10.1126/science.aba5531
Publication status	Published - 24 Dec 2021

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https://hdl.handle.net/10138/343022

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Roszak, P., Heo, J.-O., Blob, B., Toyokura, K., Sugiyama, Y., de Luis Balaguer, M. A., Lau, W. W. Y., Hamey, F., Cirrone, J., Madej, E., Bouatta, A. M., Wang, X., Guichard, M., Ursache, R., Tavares, H., Verstaen, K., Wendrich, J., Melnyk, C. W., Oda, Y., ... Helariutta, Y. (2021). Cell-by-cell dissection of phloem development links a maturation gradient to cell specialization. Science, 374(6575), Article eaba5531. https://doi.org/10.1126/science.aba5531

@article{5e89f4d1508b4dc28745648475dca904,

title = "Cell-by-cell dissection of phloem development links a maturation gradient to cell specialization",

abstract = "In the plant meristem, tissue-wide maturation gradients are coordinated with specialized cell networks to establish various developmental phases required for indeterminate growth. Here, we used single-cell transcriptomics to reconstruct the protophloem developmental trajectory from the birth of cell progenitors to terminal differentiation in the Arabidopsis thaliana root. PHLOEM EARLY DNA-BINDING-WITH-ONE-FINGER (PEAR) transcription factors mediate lineage bifurcation by activating guanosine triphosphatase signaling and prime a transcriptional differentiation program. This program is initially repressed by a meristem-wide gradient of PLETHORA transcription factors. Only the dissipation of PLETHORA gradient permits activation of the differentiation program that involves mutual inhibition of early versus late meristem regulators. Thus, for phloem development, broad maturation gradients interface with cell-type-specific transcriptional regulators to stage cellular differentiation.",

author = "Pawel Roszak and Jung-Ok Heo and Bernhard Blob and Koichi Toyokura and Yuki Sugiyama and {de Luis Balaguer}, {Maria Angels} and Lau, {Winnie W.Y.} and Fiona Hamey and Jacopo Cirrone and Ewelina Madej and Bouatta, {Alida M.} and Xin Wang and Marjorie Guichard and Robertas Ursache and Hugo Tavares and Kevin Verstaen and Jos Wendrich and Melnyk, {Charles W.} and Yoshihisa Oda and Dennis Shasha and Ahnert, {Sebastian E.} and Yvan Saeys and {De Rybel}, Bert and Renze Heidstra and Ben Scheres and Guido Grossmann and M{\"a}h{\"o}nen, {Ari Pekka} and Philipp Denninger and Berthold G{\"o}ttgens and Rosangela Sozzani and Birnbaum, {Kenneth D.} and Yrj{\"o} Helariutta",

year = "2021",

month = dec,

day = "24",

doi = "10.1126/science.aba5531",

language = "English",

volume = "374",

journal = "Science",

issn = "0036-8075",

publisher = "American Association for the Advancement of Science",

number = "6575",

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Roszak, P, Heo, J-O, Blob, B, Toyokura, K, Sugiyama, Y, de Luis Balaguer, MA, Lau, WWY, Hamey, F, Cirrone, J, Madej, E, Bouatta, AM, Wang, X, Guichard, M, Ursache, R, Tavares, H, Verstaen, K, Wendrich, J, Melnyk, CW, Oda, Y, Shasha, D, Ahnert, SE, Saeys, Y, De Rybel, B, Heidstra, R , Scheres, B, Grossmann, G, Mähönen, AP, Denninger, P, Göttgens, B, Sozzani, R, Birnbaum, KD & Helariutta, Y 2021, 'Cell-by-cell dissection of phloem development links a maturation gradient to cell specialization', Science, vol. 374, no. 6575, eaba5531. https://doi.org/10.1126/science.aba5531

TY - JOUR

T1 - Cell-by-cell dissection of phloem development links a maturation gradient to cell specialization

AU - Roszak, Pawel

AU - Heo, Jung-Ok

AU - Blob, Bernhard

AU - Toyokura, Koichi

AU - Sugiyama, Yuki

AU - de Luis Balaguer, Maria Angels

AU - Lau, Winnie W.Y.

AU - Hamey, Fiona

AU - Cirrone, Jacopo

AU - Madej, Ewelina

AU - Bouatta, Alida M.

AU - Wang, Xin

AU - Guichard, Marjorie

AU - Ursache, Robertas

AU - Tavares, Hugo

AU - Verstaen, Kevin

AU - Wendrich, Jos

AU - Melnyk, Charles W.

AU - Oda, Yoshihisa

AU - Shasha, Dennis

AU - Ahnert, Sebastian E.

AU - Saeys, Yvan

AU - De Rybel, Bert

AU - Heidstra, Renze

AU - Scheres, Ben

AU - Grossmann, Guido

AU - Mähönen, Ari Pekka

AU - Denninger, Philipp

AU - Göttgens, Berthold

AU - Sozzani, Rosangela

AU - Birnbaum, Kenneth D.

AU - Helariutta, Yrjö

PY - 2021/12/24

Y1 - 2021/12/24

N2 - In the plant meristem, tissue-wide maturation gradients are coordinated with specialized cell networks to establish various developmental phases required for indeterminate growth. Here, we used single-cell transcriptomics to reconstruct the protophloem developmental trajectory from the birth of cell progenitors to terminal differentiation in the Arabidopsis thaliana root. PHLOEM EARLY DNA-BINDING-WITH-ONE-FINGER (PEAR) transcription factors mediate lineage bifurcation by activating guanosine triphosphatase signaling and prime a transcriptional differentiation program. This program is initially repressed by a meristem-wide gradient of PLETHORA transcription factors. Only the dissipation of PLETHORA gradient permits activation of the differentiation program that involves mutual inhibition of early versus late meristem regulators. Thus, for phloem development, broad maturation gradients interface with cell-type-specific transcriptional regulators to stage cellular differentiation.

AB - In the plant meristem, tissue-wide maturation gradients are coordinated with specialized cell networks to establish various developmental phases required for indeterminate growth. Here, we used single-cell transcriptomics to reconstruct the protophloem developmental trajectory from the birth of cell progenitors to terminal differentiation in the Arabidopsis thaliana root. PHLOEM EARLY DNA-BINDING-WITH-ONE-FINGER (PEAR) transcription factors mediate lineage bifurcation by activating guanosine triphosphatase signaling and prime a transcriptional differentiation program. This program is initially repressed by a meristem-wide gradient of PLETHORA transcription factors. Only the dissipation of PLETHORA gradient permits activation of the differentiation program that involves mutual inhibition of early versus late meristem regulators. Thus, for phloem development, broad maturation gradients interface with cell-type-specific transcriptional regulators to stage cellular differentiation.

U2 - 10.1126/science.aba5531

DO - 10.1126/science.aba5531

M3 - Article

SN - 0036-8075

VL - 374

JO - Science

JF - Science

IS - 6575

M1 - eaba5531

ER -

Cell-by-cell dissection of phloem development links a maturation gradient to cell specialization

Abstract

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