title: A plant U-box protein, PUB4, regulates asymmetric cell division and cell proliferation in the root meristem.
abstract: The root meristem (RM) is a fundamental structure that is responsible for postembryonic root growth. The RM contains the quiescent center (QC), stem cells and frequently dividing meristematic cells, in which the timing and the frequency of cell division are tightly regulated. In Arabidopsis thaliana, several gain-of-function analyses have demonstrated that peptide ligands of the Clavata3 (CLV3)/embryo surrounding region-related (CLE) family are important for maintaining RM size. Here, we demonstrate that a plant U-box E3 ubiquitin ligase, PUB4, is a novel downstream component of CLV3/CLE signaling in the RM. Mutations in PUB4 reduced the inhibitory effect of exogenous CLV3/CLE peptide on root cell proliferation and columella stem cell maintenance. Moreover, pub4 mutants grown without exogenous CLV3/CLE peptide exhibited characteristic phenotypes in the RM, such as enhanced root growth, increased number of cortex/endodermis stem cells and decreased number of columella layers. Our phenotypic and gene expression analyses indicated that PUB4 promotes expression of a cell cycle regulatory gene, CYCD6;1, and regulates formative periclinal asymmetric cell divisions in endodermis and cortex/endodermis initial daughters. These data suggest that PUB4 functions as a global regulator of cell proliferation and the timing of asymmetric cell division that are important for final root architecture.
authors.affiliation: RIKEN Center for Sustainable Resource Science, Tsurumi, Yokohama 230-0045, Japan.
authors.forename: Atsuko
authors.initials: A
authors.lastname: Kinoshita
authors.affiliation: Molecular Genetics, Department of Biology, Utrecht University, Utrecht 3584 CH, The Netherlands Laboratory of Biochemistry, Wageningen University, Dreijenlaan 3, Wageningen 6703HA, The Netherlands.
authors.forename: Colette A
authors.initials: CA
authors.lastname: ten Hove
authors.affiliation: Graduate School of Science and Technology, Kumamoto University, Kumamoto 860-8555, Japan.
authors.forename: Ryo
authors.initials: R
authors.lastname: Tabata
authors.affiliation: Department of Biology and Institute for Genome Science and Policy Center for Systems Biology, Duke University, Durham, NC 27708, USA.
authors.forename: Masashi
authors.initials: M
authors.lastname: Yamada
authors.affiliation: Graduate School of Science and Technology, Kumamoto University, Kumamoto 860-8555, Japan.
authors.forename: Noriko
authors.initials: N
authors.lastname: Shimizu
authors.affiliation: Graduate School of Science and Technology, Kumamoto University, Kumamoto 860-8555, Japan.
authors.forename: Takashi
authors.initials: T
authors.lastname: Ishida
authors.affiliation: Functional Genomics Facility, National Institute for Basic Biology, Okazaki 444-8585, Japan.
authors.forename: Katsushi
authors.initials: K
authors.lastname: Yamaguchi
authors.affiliation: Functional Genomics Facility, National Institute for Basic Biology, Okazaki 444-8585, Japan School of Life Science, The Graduate University for Advanced Studies, Okazaki 444-8585, Japan.
authors.forename: Shuji
authors.initials: S
authors.lastname: Shigenobu
authors.affiliation: RIKEN Center for Sustainable Resource Science, Tsurumi, Yokohama 230-0045, Japan.
authors.forename: Yumiko
authors.initials: Y
authors.lastname: Takebayashi
authors.affiliation: RIKEN BioResource Center, 3-1-1 Koyadai, Tsukuba, Ibaraki 305-0074, Japan.
authors.forename: Satoshi
authors.initials: S
authors.lastname: Iuchi
authors.affiliation: RIKEN BioResource Center, 3-1-1 Koyadai, Tsukuba, Ibaraki 305-0074, Japan.
authors.forename: Masatomo
authors.initials: M
authors.lastname: Kobayashi
authors.affiliation: Graduate School of Biological Sciences, NAIST, Ikoma 630-0192, Japan.
authors.forename: Tetsuya
authors.initials: T
authors.lastname: Kurata
authors.affiliation: Graduate School of Biosphere Sciences, Hiroshima University, Higashi-Hiroshima 739-8528, Japan.
authors.forename: Takuji
authors.initials: T
authors.lastname: Wada
authors.affiliation: RIKEN Center for Sustainable Resource Science, Tsurumi, Yokohama 230-0045, Japan.
authors.forename: Mitsunori
authors.initials: M
authors.lastname: Seo
authors.affiliation: School of Life Science, The Graduate University for Advanced Studies, Okazaki 444-8585, Japan Division of Evolutionary Biology, National Institute for Basic Biology, Okazaki 444-8585, Japan.
authors.forename: Mitsuyasu
authors.initials: M
authors.lastname: Hasebe
authors.affiliation: Molecular Genetics, Department of Biology, Utrecht University, Utrecht 3584 CH, The Netherlands Plant Developmental Biology, Wageningen University, Droevendaalsesteeg 1, Wageningen 6700AP, The Netherlands.
authors.forename: Ikram
authors.initials: I
authors.lastname: Blilou
authors.affiliation: Department of Biological Sciences, Graduate School of Science, University of Tokyo, Hongo 7-3-1, Bunkyo-ku, Tokyo 113-0033, Japan.
authors.forename: Hiroo
authors.initials: H
authors.lastname: Fukuda
authors.affiliation: Molecular Genetics, Department of Biology, Utrecht University, Utrecht 3584 CH, The Netherlands Plant Developmental Biology, Wageningen University, Droevendaalsesteeg 1, Wageningen 6700AP, The Netherlands.
authors.forename: Ben
authors.initials: B
authors.lastname: Scheres
authors.affiliation: Molecular Genetics, Department of Biology, Utrecht University, Utrecht 3584 CH, The Netherlands Plant Developmental Biology, Wageningen University, Droevendaalsesteeg 1, Wageningen 6700AP, The Netherlands.
authors.forename: Renze
authors.initials: R
authors.lastname: Heidstra
authors.affiliation: RIKEN Center for Sustainable Resource Science, Tsurumi, Yokohama 230-0045, Japan.
authors.forename: Yuji
authors.initials: Y
authors.lastname: Kamiya
authors.affiliation: Graduate School of Science and Technology, Kumamoto University, Kumamoto 860-8555, Japan sawa@sci.kumamoto-u.ac.jp.
authors.forename: Shinichiro
authors.initials: S
authors.lastname: Sawa
mesh_terms: D017360:Arabidopsis / Q000235:genetics / Q000254:growth & development*; D029681:Arabidopsis Proteins / Q000235:genetics / Q000378:metabolism*; D060049:Asymmetric Cell Division / Q000235:genetics / Q000502:physiology*; D018797:Cell Cycle Proteins / Q000378:metabolism; D049109:Cell Proliferation / Q000235:genetics / Q000502:physiology*; D003001:Cloning, Molecular; D016213:Cyclins / Q000378:metabolism; D020869:Gene Expression Profiling; D018506:Gene Expression Regulation, Plant / Q000235:genetics*; D018519:Meristem / Q000166:cytology*; D018613:Microscopy, Confocal; D030821:Plants, Genetically Modified; D015398:Signal Transduction / Q000235:genetics / Q000502:physiology*; D020798:Two-Hybrid System Techniques; D044767:Ubiquitin-Protein Ligases / Q000235:genetics / Q000378:metabolism*
chemical_list: C118167:AT2G27250 protein, Arabidopsis; D029681:Arabidopsis Proteins; C000596070:CYCD6;1 protein, Arabidopsis; D018797:Cell Cycle Proteins; D016213:Cyclins; D044767:Ubiquitin-Protein Ligases; C000596069:PUB4 protein, Arabidopsis
keywords: Arabidopsis development; Asymmetric cell division; Cell proliferation; Root meristem