Callose Biosynthesis Regulates Symplastic Trafficking during Root Development

Anne Vatén; Jan Dettmer; Shuang Wu; York Dieter Stierhof; Shunsuke Miyashima; Shri Ram Yadav; Christina J. Roberts; Ana Campilho; Vincent Bulone; Raffael Lichtenberger; Satu Lehesranta; Ari Pekka Mähönen; Jae Yean Kim; Eija Jokitalo; Norbert Sauer; Ben Scheres; Keiji Nakajima; Annelie Carlsbecker; Kimberly L. Gallagher; Ykä Helariutta

doi:10.1016/j.devcel.2011.10.006

Callose Biosynthesis Regulates Symplastic Trafficking during Root Development

Anne Vatén, Jan Dettmer, Shuang Wu, York Dieter Stierhof, Shunsuke Miyashima, Shri Ram Yadav, Christina J. Roberts, Ana Campilho, Vincent Bulone, Raffael Lichtenberger, Satu Lehesranta, Ari Pekka Mähönen, Jae Yean Kim, Eija Jokitalo, Norbert Sauer, Ben Scheres, Keiji Nakajima, Annelie Carlsbecker, Kimberly L. Gallagher, Ykä Helariutta

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367 Citations (Scopus)

Abstract

Plant cells are connected through plasmodesmata (PD), membrane-lined channels that allow symplastic movement of molecules between cells. However, little is known about the role of PD-mediated signaling during plant morphogenesis. Here, we describe an Arabidopsis gene, CALS3/GSL12. Gain-of-function mutations in CALS3 result in increased accumulation of callose (β-1,3-glucan) at the PD, a decrease in PD aperture, defects in root development, and reduced intercellular trafficking. Enhancement of CALS3 expression during phloem development suppressed loss-of-function mutations in the phloem abundant callose synthase, CALS7 indicating that CALS3 is a bona fide callose synthase. CALS3 alleles allowed us to spatially and temporally control the PD aperture between plant tissues. Using this tool, we are able to show that movement of the transcription factor SHORT-ROOT and microRNA165 between the stele and the endodermis is PD dependent. Taken together, we conclude that regulated callose biosynthesis at PD is essential for cell signaling.

Original language	English
Pages (from-to)	1144-1155
Number of pages	12
Journal	DEVELOPMENTAL CELL
Volume	21
Issue number	6
DOIs	https://doi.org/10.1016/j.devcel.2011.10.006
Publication status	Published - 13 Dec 2011
Externally published	Yes

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Vatén, A., Dettmer, J., Wu, S., Stierhof, Y. D., Miyashima, S., Yadav, S. R., Roberts, C. J., Campilho, A., Bulone, V., Lichtenberger, R., Lehesranta, S., Mähönen, A. P., Kim, J. Y., Jokitalo, E., Sauer, N., Scheres, B., Nakajima, K., Carlsbecker, A., Gallagher, K. L., & Helariutta, Y. (2011). Callose Biosynthesis Regulates Symplastic Trafficking during Root Development. DEVELOPMENTAL CELL, 21(6), 1144-1155. https://doi.org/10.1016/j.devcel.2011.10.006

@article{02eadb028aea46d5a156853541ea778b,

title = "Callose Biosynthesis Regulates Symplastic Trafficking during Root Development",

abstract = "Plant cells are connected through plasmodesmata (PD), membrane-lined channels that allow symplastic movement of molecules between cells. However, little is known about the role of PD-mediated signaling during plant morphogenesis. Here, we describe an Arabidopsis gene, CALS3/GSL12. Gain-of-function mutations in CALS3 result in increased accumulation of callose (β-1,3-glucan) at the PD, a decrease in PD aperture, defects in root development, and reduced intercellular trafficking. Enhancement of CALS3 expression during phloem development suppressed loss-of-function mutations in the phloem abundant callose synthase, CALS7 indicating that CALS3 is a bona fide callose synthase. CALS3 alleles allowed us to spatially and temporally control the PD aperture between plant tissues. Using this tool, we are able to show that movement of the transcription factor SHORT-ROOT and microRNA165 between the stele and the endodermis is PD dependent. Taken together, we conclude that regulated callose biosynthesis at PD is essential for cell signaling.",

author = "Anne Vat{\'e}n and Jan Dettmer and Shuang Wu and Stierhof, {York Dieter} and Shunsuke Miyashima and Yadav, {Shri Ram} and Roberts, {Christina J.} and Ana Campilho and Vincent Bulone and Raffael Lichtenberger and Satu Lehesranta and M{\"a}h{\"o}nen, {Ari Pekka} and Kim, {Jae Yean} and Eija Jokitalo and Norbert Sauer and Ben Scheres and Keiji Nakajima and Annelie Carlsbecker and Gallagher, {Kimberly L.} and Yk{\"a} Helariutta",

year = "2011",

month = dec,

day = "13",

doi = "10.1016/j.devcel.2011.10.006",

language = "English",

volume = "21",

pages = "1144--1155",

journal = "DEVELOPMENTAL CELL",

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Vatén, A, Dettmer, J, Wu, S, Stierhof, YD, Miyashima, S, Yadav, SR, Roberts, CJ, Campilho, A, Bulone, V, Lichtenberger, R, Lehesranta, S, Mähönen, AP, Kim, JY, Jokitalo, E, Sauer, N, Scheres, B, Nakajima, K, Carlsbecker, A, Gallagher, KL & Helariutta, Y 2011, 'Callose Biosynthesis Regulates Symplastic Trafficking during Root Development', DEVELOPMENTAL CELL, vol. 21, no. 6, pp. 1144-1155. https://doi.org/10.1016/j.devcel.2011.10.006

TY - JOUR

T1 - Callose Biosynthesis Regulates Symplastic Trafficking during Root Development

AU - Vatén, Anne

AU - Dettmer, Jan

AU - Wu, Shuang

AU - Stierhof, York Dieter

AU - Miyashima, Shunsuke

AU - Yadav, Shri Ram

AU - Roberts, Christina J.

AU - Campilho, Ana

AU - Bulone, Vincent

AU - Lichtenberger, Raffael

AU - Lehesranta, Satu

AU - Mähönen, Ari Pekka

AU - Kim, Jae Yean

AU - Jokitalo, Eija

AU - Sauer, Norbert

AU - Scheres, Ben

AU - Nakajima, Keiji

AU - Carlsbecker, Annelie

AU - Gallagher, Kimberly L.

AU - Helariutta, Ykä

PY - 2011/12/13

Y1 - 2011/12/13

N2 - Plant cells are connected through plasmodesmata (PD), membrane-lined channels that allow symplastic movement of molecules between cells. However, little is known about the role of PD-mediated signaling during plant morphogenesis. Here, we describe an Arabidopsis gene, CALS3/GSL12. Gain-of-function mutations in CALS3 result in increased accumulation of callose (β-1,3-glucan) at the PD, a decrease in PD aperture, defects in root development, and reduced intercellular trafficking. Enhancement of CALS3 expression during phloem development suppressed loss-of-function mutations in the phloem abundant callose synthase, CALS7 indicating that CALS3 is a bona fide callose synthase. CALS3 alleles allowed us to spatially and temporally control the PD aperture between plant tissues. Using this tool, we are able to show that movement of the transcription factor SHORT-ROOT and microRNA165 between the stele and the endodermis is PD dependent. Taken together, we conclude that regulated callose biosynthesis at PD is essential for cell signaling.

AB - Plant cells are connected through plasmodesmata (PD), membrane-lined channels that allow symplastic movement of molecules between cells. However, little is known about the role of PD-mediated signaling during plant morphogenesis. Here, we describe an Arabidopsis gene, CALS3/GSL12. Gain-of-function mutations in CALS3 result in increased accumulation of callose (β-1,3-glucan) at the PD, a decrease in PD aperture, defects in root development, and reduced intercellular trafficking. Enhancement of CALS3 expression during phloem development suppressed loss-of-function mutations in the phloem abundant callose synthase, CALS7 indicating that CALS3 is a bona fide callose synthase. CALS3 alleles allowed us to spatially and temporally control the PD aperture between plant tissues. Using this tool, we are able to show that movement of the transcription factor SHORT-ROOT and microRNA165 between the stele and the endodermis is PD dependent. Taken together, we conclude that regulated callose biosynthesis at PD is essential for cell signaling.

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U2 - 10.1016/j.devcel.2011.10.006

DO - 10.1016/j.devcel.2011.10.006

M3 - Article

C2 - 22172675

AN - SCOPUS:83455229801

SN - 1534-5807

VL - 21

SP - 1144

EP - 1155

JO - DEVELOPMENTAL CELL

JF - DEVELOPMENTAL CELL

IS - 6

ER -

Callose Biosynthesis Regulates Symplastic Trafficking during Root Development

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