Ubiquitylation activates a peptidase that promotes cleavage and destabilization of its activating E3 ligases and diverse growth regulatory proteins to limit cell proliferation inArabidopsis.
The characteristic shapes and sizes of organs are established by cell proliferation patterns and final cell sizes, but the underlying molecular mechanisms coordinating these are poorly understood. Here we characterize a ubiquitin-activated peptidase called DA1 that limits the duration of cell proliferation during organ growth inArabidopsis thalianaThe peptidase is activated by two RING E3 ligases, Big Brother (BB) and DA2, which are subsequently cleaved by the activated peptidase and destabilized. In the case of BB, cleavage leads to destabilization by the RING E3 ligase PROTEOLYSIS 1 (PRT1) of the N-end rule pathway. DA1 peptidase activity also cleaves the deubiquitylase UBP15, which promotes cell proliferation, and the transcription factors TEOSINTE BRANCED 1/CYCLOIDEA/PCF 15 (TCP15) and TCP22, which promote cell proliferation and repress endoreduplication. We propose that DA1 peptidase activity regulates the duration of cell proliferation and the transition to endoreduplication and differentiation during organ formation in plants by coordinating the destabilization of regulatory proteins.
John Innes Centre, Norwich NR4 7QA, United Kingdom.
Hui
H
Dong
John Innes Centre, Norwich NR4 7QA, United Kingdom.
Jack
J
Dumenil
John Innes Centre, Norwich NR4 7QA, United Kingdom.
Fu-Hao
FH
Lu
State Key Laboratory of Plant Cell and Chromosome Engineering, CAS Centre of Excellence in Molecular Plant Biology, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100101, China.
Li
L
Na
VIB-UGent Centre for Plant Systems Biology, Ghent University, 9052 Gent, Belgium.
Hannes
H
Vanhaeren
Leibniz Institute of Plant Biochemistry (IPB), D-06120 Halle, Germany.
Christin
C
Naumann
Leibniz Institute of Plant Biochemistry (IPB), D-06120 Halle, Germany.
Maria
M
Klecker
John Innes Centre, Norwich NR4 7QA, United Kingdom.
Rachel
R
Prior
John Innes Centre, Norwich NR4 7QA, United Kingdom.
Caroline
C
Smith
John Innes Centre, Norwich NR4 7QA, United Kingdom.
Neil
N
McKenzie
John Innes Centre, Norwich NR4 7QA, United Kingdom.
Gerhard
G
Saalbach
State Key Laboratory of Plant Cell and Chromosome Engineering, CAS Centre of Excellence in Molecular Plant Biology, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100101, China.
Liangliang
L
Chen
State Key Laboratory of Plant Cell and Chromosome Engineering, CAS Centre of Excellence in Molecular Plant Biology, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100101, China.
Tian
T
Xia
VIB-UGent Centre for Plant Systems Biology, Ghent University, 9052 Gent, Belgium.
Nathalie
N
Gonzalez
John Innes Centre, Norwich NR4 7QA, United Kingdom.
Mathilde
M
Seguela
VIB-UGent Centre for Plant Systems Biology, Ghent University, 9052 Gent, Belgium.
Dirk
D
Inze
Leibniz Institute of Plant Biochemistry (IPB), D-06120 Halle, Germany.
Nico
N
Dissmeyer
State Key Laboratory of Plant Cell and Chromosome Engineering, CAS Centre of Excellence in Molecular Plant Biology, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100101, China.
Yunhai
Y
Li
John Innes Centre, Norwich NR4 7QA, United Kingdom.
Michael W
MW
Bevan
D017360:Arabidopsis / Q000201:enzymology* / Q000235:genetics / Q000254:growth & development*; D029681:Arabidopsis Proteins / Q000235:genetics / Q000378:metabolism*; D049109:Cell Proliferation; D004789:Enzyme Activation; D060588:LIM Domain Proteins / Q000235:genetics / Q000378:metabolism*; D055550:Protein Stability; D044767:Ubiquitin-Protein Ligases / Q000378:metabolism*; D054875:Ubiquitination
D029681:Arabidopsis Proteins; C529975:DA1 protein, Arabidopsis; D060588:LIM Domain Proteins; D044767:Ubiquitin-Protein Ligases
Arabidopsis; N-end rule-mediated degradation; organ size; ubiquitin-activated peptidase; ubiquitylation