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Dynamic changes in ANGUSTIFOLIA3 complex composition reveal a growth regulatory mechanism in the maize leaf

Hilde Nelissen UGent, Dominique Eeckhout UGent, Kirin Demuynck UGent, Geert Persiau UGent, Alan Walton, Michiel Van Bel UGent, Marieke Vervoort, Jasper Candaele, Jolien De Block UGent, Stijn Aesaert UGent, et al. (2015) PLANT CELL. 27(6). p.1605-1619
abstract
Most molecular processes during plant development occur with a particular spatio-temporal specificity. Thus far, it has remained technically challenging to capture dynamic protein-protein interactions within a growing organ, where the interplay between cell division and cell expansion is instrumental. Here, we combined high-resolution sampling of the growing maize (Zea mays) leaf with tandem affinity purification followed by mass spectrometry. Our results indicate that the growth-regulating SWI/SNF chromatin remodeling complex associated with ANGUSTIFOLIA3 (AN3) was conserved within growing organs and between dicots and monocots. Moreover, we were able to demonstrate the dynamics of the AN3-interacting proteins within the growing leaf, since copurified GROWTH-REGULATING FACTORs (GRFs) varied throughout the growing leaf. Indeed, GRF1, GRF6, GRF7, GRF12, GRF15, and GRF17 were significantly enriched in the division zone of the growing leaf, while GRF4 and GRF10 levels were comparable between division zone and expansion zone in the growing leaf. These dynamics were also reflected at the mRNA and protein levels, indicating tight developmental regulation of the AN3-associated chromatin remodeling complex. In addition, the phenotypes of maize plants overexpressing miRNA396a-resistant GRF1 support a model proposing that distinct associations of the chromatin remodeling complex with specific GRFs tightly regulate the transition between cell division and cell expansion. Together, our data demonstrate that advancing from static to dynamic protein-protein interaction analysis in a growing organ adds insights in how developmental switches are regulated.
Please use this url to cite or link to this publication:
author
organization
year
type
journalArticle (original)
publication status
published
subject
keyword
GRF TRANSCRIPTION FACTORS, ARABIDOPSIS-THALIANA, CELL-DIVISION, PROTEIN COMPLEXES, MICRORNA MIR396, GENE, DIFFERENTIATION, FAMILY, TANDEM AFFINITY PURIFICATION, CHROMATIN REMODELING COMPLEXES
journal title
PLANT CELL
Plant Cell
volume
27
issue
6
pages
1605 - 1619
Web of Science type
Article
Web of Science id
000357718800006
JCR category
PLANT SCIENCES
JCR impact factor
8.538 (2015)
JCR rank
4/209 (2015)
JCR quartile
1 (2015)
ISSN
1040-4651
DOI
10.1105/tpc.15.00269
project
Bioinformatics: from nucleotids to networks (N2N)
project
Biotechnology for a sustainable economy (Bio-Economy)
language
English
UGent publication?
yes
classification
A1
additional info
the last two authors contributed equally to this work
copyright statement
I have retained and own the full copyright for this publication
id
6890910
handle
http://hdl.handle.net/1854/LU-6890910
date created
2015-08-03 14:15:03
date last changed
2016-12-19 15:42:46
@article{6890910,
  abstract     = {Most molecular processes during plant development occur with a particular spatio-temporal specificity. Thus far, it has remained technically challenging to capture dynamic protein-protein interactions within a growing organ, where the interplay between cell division and cell expansion is instrumental. Here, we combined high-resolution sampling of the growing maize (Zea mays) leaf with tandem affinity purification followed by mass spectrometry. Our results indicate that the growth-regulating SWI/SNF chromatin remodeling complex associated with ANGUSTIFOLIA3 (AN3) was conserved within growing organs and between dicots and monocots. Moreover, we were able to demonstrate the dynamics of the AN3-interacting proteins within the growing leaf, since copurified GROWTH-REGULATING FACTORs (GRFs) varied throughout the growing leaf. Indeed, GRF1, GRF6, GRF7, GRF12, GRF15, and GRF17 were significantly enriched in the division zone of the growing leaf, while GRF4 and GRF10 levels were comparable between division zone and expansion zone in the growing leaf. These dynamics were also reflected at the mRNA and protein levels, indicating tight developmental regulation of the AN3-associated chromatin remodeling complex. In addition, the phenotypes of maize plants overexpressing miRNA396a-resistant GRF1 support a model proposing that distinct associations of the chromatin remodeling complex with specific GRFs tightly regulate the transition between cell division and cell expansion. Together, our data demonstrate that advancing from static to dynamic protein-protein interaction analysis in a growing organ adds insights in how developmental switches are regulated.},
  author       = {Nelissen, Hilde and Eeckhout, Dominique and Demuynck, Kirin and Persiau, Geert and Walton, Alan and Van Bel, Michiel and Vervoort, Marieke and Candaele, Jasper and De Block, Jolien and Aesaert, Stijn and Van Lijsebettens, Maria and Goormachtig, Sofie and Vandepoele, Klaas and Van Leene, Jelle and Muszynski, Michael and Gevaert, Kris and Inz{\'e}, Dirk and De Jaeger, Geert},
  issn         = {1040-4651},
  journal      = {PLANT CELL},
  keyword      = {GRF TRANSCRIPTION FACTORS,ARABIDOPSIS-THALIANA,CELL-DIVISION,PROTEIN COMPLEXES,MICRORNA MIR396,GENE,DIFFERENTIATION,FAMILY,TANDEM AFFINITY PURIFICATION,CHROMATIN REMODELING COMPLEXES},
  language     = {eng},
  number       = {6},
  pages        = {1605--1619},
  title        = {Dynamic changes in ANGUSTIFOLIA3 complex composition reveal a growth regulatory mechanism in the maize leaf},
  url          = {http://dx.doi.org/10.1105/tpc.15.00269},
  volume       = {27},
  year         = {2015},
}

Chicago
Nelissen, Hilde, Dominique Eeckhout, Kirin Demuynck, Geert Persiau, Alan Walton, Michiel Van Bel, Marieke Vervoort, et al. 2015. “Dynamic Changes in ANGUSTIFOLIA3 Complex Composition Reveal a Growth Regulatory Mechanism in the Maize Leaf.” Plant Cell 27 (6): 1605–1619.
APA
Nelissen, H., Eeckhout, D., Demuynck, K., Persiau, G., Walton, A., Van Bel, M., Vervoort, M., et al. (2015). Dynamic changes in ANGUSTIFOLIA3 complex composition reveal a growth regulatory mechanism in the maize leaf. PLANT CELL, 27(6), 1605–1619.
Vancouver
1.
Nelissen H, Eeckhout D, Demuynck K, Persiau G, Walton A, Van Bel M, et al. Dynamic changes in ANGUSTIFOLIA3 complex composition reveal a growth regulatory mechanism in the maize leaf. PLANT CELL. 2015;27(6):1605–19.
MLA
Nelissen, Hilde, Dominique Eeckhout, Kirin Demuynck, et al. “Dynamic Changes in ANGUSTIFOLIA3 Complex Composition Reveal a Growth Regulatory Mechanism in the Maize Leaf.” PLANT CELL 27.6 (2015): 1605–1619. Print.