Regulation of leaf maturation by chromatin-mediated modulation of cytokinin responses

Idan Efroni; Soon Ki Han; Hye Jin Kim; Miin Feng Wu; Evyatar Steiner; Kenneth D. Birnbaum; Jong Chan Hong; Yuval Eshed; Doris Wagner

doi:10.1016/j.devcel.2013.01.019

Regulation of leaf maturation by chromatin-mediated modulation of cytokinin responses

Idan Efroni, Soon Ki Han, Hye Jin Kim, Miin Feng Wu, Evyatar Steiner, Kenneth D. Birnbaum, Jong Chan Hong, Yuval Eshed^*, Doris Wagner

^*Corresponding author for this work

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

188 Scopus citations

Abstract

Plant shoots display indeterminate growth, while their evolutionary decedents, the leaves, are determinate. Determinate leaf growth is conditioned by the CIN-TCP transcription factors, which promote leaf maturation and are negatively regulated by miR319 in leaf primordia. Here we show that CIN-TCPs reduce leaf sensitivity to cytokinin (CK), a phytohormone implicated in inhibition of differentiation in the shoot. We identify the SWI/SNF chromatin remodeling ATPase BRAHMA (BRM) as a genetic mediator of CIN-TCP activities and CK responses. An interactome screen further revealed that SWI/SNF complex components including BRM preferentially interacted with basic-helix-loop-helix (bHLH) transcription factors and the bHLH-related CIN-TCPs. Indeed, TCP4 and BRM interacted in planta. Both TCP4 and BRM bound the promoter of an inhibitor of CK responses, ARR16, and induced its expression. Reconstituting ARR16 levels in leaves with reduced CIN-TCP activity restored normal growth. Thus, CIN-TCP and BRM together promote determinate leaf growth by stage-specific modification of CK responses.

Original language	English
Pages (from-to)	438-445
Number of pages	8
Journal	Developmental Cell
Volume	24
Issue number	4
DOIs	https://doi.org/10.1016/j.devcel.2013.01.019
State	Published - 25 Feb 2013
Externally published	Yes

Bibliographical note

Funding Information:
We thank D. Weiss, J. Bowman, and N. Ori for comments; J. Reyes for pDBLeu-SYD; J. Pfluger for help with the interaction assays; C. Winter for statistical analyses; N. Ohad for technical advice; B. Ren and E. Shani for seeds; and J. Lohman for sharing expression datasets. This work was supported in part by a grant from the Next-Generation BioGreen 21 Program (SSAC No. 2011); the Rural Development Administration, Republic of Korea; the Basic Science Research Program through the National Research Foundation of Korea (MEST 2010-0012801 to J.C.H.); MINERVA (ISF 1294-10 to Y.E.); NIH (R01 GM64650-01 to D.W.); NSF (IOS 0849298 to D.W.); and EMBO (LTF185-2010 to I.E.).

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title = "Regulation of leaf maturation by chromatin-mediated modulation of cytokinin responses",

abstract = "Plant shoots display indeterminate growth, while their evolutionary decedents, the leaves, are determinate. Determinate leaf growth is conditioned by the CIN-TCP transcription factors, which promote leaf maturation and are negatively regulated by miR319 in leaf primordia. Here we show that CIN-TCPs reduce leaf sensitivity to cytokinin (CK), a phytohormone implicated in inhibition of differentiation in the shoot. We identify the SWI/SNF chromatin remodeling ATPase BRAHMA (BRM) as a genetic mediator of CIN-TCP activities and CK responses. An interactome screen further revealed that SWI/SNF complex components including BRM preferentially interacted with basic-helix-loop-helix (bHLH) transcription factors and the bHLH-related CIN-TCPs. Indeed, TCP4 and BRM interacted in planta. Both TCP4 and BRM bound the promoter of an inhibitor of CK responses, ARR16, and induced its expression. Reconstituting ARR16 levels in leaves with reduced CIN-TCP activity restored normal growth. Thus, CIN-TCP and BRM together promote determinate leaf growth by stage-specific modification of CK responses.",

author = "Idan Efroni and Han, {Soon Ki} and Kim, {Hye Jin} and Wu, {Miin Feng} and Evyatar Steiner and Birnbaum, {Kenneth D.} and Hong, {Jong Chan} and Yuval Eshed and Doris Wagner",

note = "Funding Information: We thank D. Weiss, J. Bowman, and N. Ori for comments; J. Reyes for pDBLeu-SYD; J. Pfluger for help with the interaction assays; C. Winter for statistical analyses; N. Ohad for technical advice; B. Ren and E. Shani for seeds; and J. Lohman for sharing expression datasets. This work was supported in part by a grant from the Next-Generation BioGreen 21 Program (SSAC No. 2011); the Rural Development Administration, Republic of Korea; the Basic Science Research Program through the National Research Foundation of Korea (MEST 2010-0012801 to J.C.H.); MINERVA (ISF 1294-10 to Y.E.); NIH (R01 GM64650-01 to D.W.); NSF (IOS 0849298 to D.W.); and EMBO (LTF185-2010 to I.E.). ",

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T1 - Regulation of leaf maturation by chromatin-mediated modulation of cytokinin responses

AU - Efroni, Idan

AU - Han, Soon Ki

AU - Kim, Hye Jin

AU - Wu, Miin Feng

AU - Steiner, Evyatar

AU - Birnbaum, Kenneth D.

AU - Hong, Jong Chan

AU - Eshed, Yuval

AU - Wagner, Doris

N1 - Funding Information: We thank D. Weiss, J. Bowman, and N. Ori for comments; J. Reyes for pDBLeu-SYD; J. Pfluger for help with the interaction assays; C. Winter for statistical analyses; N. Ohad for technical advice; B. Ren and E. Shani for seeds; and J. Lohman for sharing expression datasets. This work was supported in part by a grant from the Next-Generation BioGreen 21 Program (SSAC No. 2011); the Rural Development Administration, Republic of Korea; the Basic Science Research Program through the National Research Foundation of Korea (MEST 2010-0012801 to J.C.H.); MINERVA (ISF 1294-10 to Y.E.); NIH (R01 GM64650-01 to D.W.); NSF (IOS 0849298 to D.W.); and EMBO (LTF185-2010 to I.E.).

PY - 2013/2/25

Y1 - 2013/2/25

N2 - Plant shoots display indeterminate growth, while their evolutionary decedents, the leaves, are determinate. Determinate leaf growth is conditioned by the CIN-TCP transcription factors, which promote leaf maturation and are negatively regulated by miR319 in leaf primordia. Here we show that CIN-TCPs reduce leaf sensitivity to cytokinin (CK), a phytohormone implicated in inhibition of differentiation in the shoot. We identify the SWI/SNF chromatin remodeling ATPase BRAHMA (BRM) as a genetic mediator of CIN-TCP activities and CK responses. An interactome screen further revealed that SWI/SNF complex components including BRM preferentially interacted with basic-helix-loop-helix (bHLH) transcription factors and the bHLH-related CIN-TCPs. Indeed, TCP4 and BRM interacted in planta. Both TCP4 and BRM bound the promoter of an inhibitor of CK responses, ARR16, and induced its expression. Reconstituting ARR16 levels in leaves with reduced CIN-TCP activity restored normal growth. Thus, CIN-TCP and BRM together promote determinate leaf growth by stage-specific modification of CK responses.

AB - Plant shoots display indeterminate growth, while their evolutionary decedents, the leaves, are determinate. Determinate leaf growth is conditioned by the CIN-TCP transcription factors, which promote leaf maturation and are negatively regulated by miR319 in leaf primordia. Here we show that CIN-TCPs reduce leaf sensitivity to cytokinin (CK), a phytohormone implicated in inhibition of differentiation in the shoot. We identify the SWI/SNF chromatin remodeling ATPase BRAHMA (BRM) as a genetic mediator of CIN-TCP activities and CK responses. An interactome screen further revealed that SWI/SNF complex components including BRM preferentially interacted with basic-helix-loop-helix (bHLH) transcription factors and the bHLH-related CIN-TCPs. Indeed, TCP4 and BRM interacted in planta. Both TCP4 and BRM bound the promoter of an inhibitor of CK responses, ARR16, and induced its expression. Reconstituting ARR16 levels in leaves with reduced CIN-TCP activity restored normal growth. Thus, CIN-TCP and BRM together promote determinate leaf growth by stage-specific modification of CK responses.

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JF - Developmental Cell

IS - 4

ER -

Regulation of leaf maturation by chromatin-mediated modulation of cytokinin responses

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