Abstract
The signal transduction pathways that control cytokinesis in plants are largely uncharacterized. Here, we provide genetic evidence that mitogen-activated protein kinase kinase kinases (MAPKKKs) play a role in the control of plant cell division. Using a reverse-genetic approach, we isolated plants carrying knockout alleles of the Arabidopsis MAPKKK genes ANP1, ANP2, and ANP3. The resulting single-mutant plants displayed no obvious abnormal phenotypes; two of the three double-mutant combinations displayed defects in cell division and growth; and the triple-mutant combination was not transmitted through either male or female gametes. The molecular and structural phenotypes displayed by the double mutants support a model in which the ANP family of MAPKKKs positively regulates cell division and growth and may negatively regulate stress responses.
MeSH Terms
Abscisic Acid/pharmacology
Alleles
Arabidopsis/enzymology,genetics,growth & development
Brassinosteroids
Cell Division/genetics
Cholestanols/pharmacology
Cytokinins/pharmacology
Ethylenes/pharmacology
Gene Expression Regulation, Plant/drug effects
Genetic Complementation Test
Gibberellins/pharmacology
Hypocotyl/drug effects,growth & development,ultrastructure
Indoleacetic Acids/pharmacology
MAP Kinase Kinase Kinases/genetics,metabolism
Microscopy, Electron
Multigene Family
Mutation
Phenotype
Plant Epidermis/drug effects,growth & development,ultrastructure
Plant Growth Regulators/pharmacology
Plant Stems/drug effects,growth & development,ultrastructure
Plants, Genetically Modified
Signal Transduction/genetics
Steroids, Heterocyclic/pharmacology
Chemicals
Brassinosteroids
Cholestanols
Cytokinins
Ethylenes
Gibberellins
Indoleacetic Acids
Plant Growth Regulators
Steroids, Heterocyclic
Abscisic Acid
ethylene
ANP1 kinase
MAP Kinase Kinase Kinases
brassinolide
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Krysan Patrick J
Biotechnology Center, University of Wisconsin-Madison, 425 Henry Mall, Madison, Wisconsin 53706, USA. fpat@biotech.wisc.edu
Jester Peter J
Gottwald Jennifer R
Sussman Michael R
References (29)
29 references, click to expand
-
Plant MAP kinase kinase kinases structure, classification and evolution.
Gene. 1999 Jun 11;233(1-2):1-11
PMID: 10375615
-
Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana.
Plant J. 1998 Dec;16(6):735-43
PMID: 10069079
-
The KEULE gene is involved in cytokinesis in Arabidopsis.
Mol Gen Genet. 1996 Dec 13;253(3):267-77
PMID: 9003313
-
Activation tagging of the floral inducer FT.
Science. 1999 Dec 3;286(5446):1962-5
PMID: 10583961
-
T-DNA as an insertional mutagen in Arabidopsis.
Plant Cell. 1999 Dec;11(12):2283-90
PMID: 10590158
-
Plant organ size control: AINTEGUMENTA regulates growth and cell numbers during organogenesis.
Proc Natl Acad Sci U S A. 2000 Jan 18;97(2):942-7
PMID: 10639184
-
Functional analysis of oxidative stress-activated mitogen-activated protein kinase cascade in plants.
Proc Natl Acad Sci U S A. 2000 Mar 14;97(6):2940-5
PMID: 10717008
-
The Arabidopsis KNOLLE and KEULE genes interact to promote vesicle fusion during cytokinesis.
Curr Biol. 2000 Nov 2;10(21):1371-4
PMID: 11084337
-
Genetic dissection of cytokinesis.
Plant Mol Biol. 2000 Aug;43(5-6):719-33
PMID: 11089872
-
Characterization of a cytokinesis defective (cyd1) mutant of Arabidopsis.
J Exp Bot. 1999 Sep;50(338):1437-46
PMID: 11543207
-
Negative regulation of defense responses in plants by a conserved MAPKK kinase.
Proc Natl Acad Sci U S A. 2001 Jan 2;98(1):373-8
PMID: 11114160
-
The NPK1 mitogen-activated protein kinase kinase kinase is a regulator of cell-plate formation in plant cytokinesis.
Genes Dev. 2001 Feb 1;15(3):352-63
PMID: 11159915
-
The cytokinesis gene KEULE encodes a Sec1 protein that binds the syntaxin KNOLLE.
J Cell Biol. 2001 Feb 5;152(3):531-43
PMID: 11157980
-
Plant mitogen-activated protein kinase cascades: Negative regulatory roles turn out positive.
Proc Natl Acad Sci U S A. 2001 Jan 30;98(3):784-6
PMID: 11158543
-
Plant cytokinesis. Exploring the links.
Plant Physiol. 2001 Jun;126(2):509-16
PMID: 11402182
-
Plant mitogen-activated protein kinase signaling cascades.
Curr Opin Plant Biol. 2001 Oct;4(5):392-400
PMID: 11597496
-
CTR1, a negative regulator of the ethylene response pathway in Arabidopsis, encodes a member of the raf family of protein kinases.
Cell. 1993 Feb 12;72(3):427-41
PMID: 8431946
-
NPK1, a tobacco gene that encodes a protein with a domain homologous to yeast BCK1, STE11, and Byr2 protein kinases.
Mol Cell Biol. 1993 Aug;13(8):4745-52
PMID: 8336712
-
Cytokinesis in the Arabidopsis embryo involves the syntaxin-related KNOLLE gene product.
Cell. 1996 Jan 12;84(1):61-71
PMID: 8548827
-
Identification of transferred DNA insertions within Arabidopsis genes involved in signal transduction and ion transport.
Proc Natl Acad Sci U S A. 1996 Jul 23;93(15):8145-50
PMID: 8755618
-
TSO1 functions in cell division during Arabidopsis flower development.
Development. 1997 Feb;124(3):665-72
PMID: 9043081
-
Possible involvement of differential splicing in regulation of the activity of Arabidopsis ANP1 that is related to mitogen-activated protein kinase kinase kinases (MAPKKKs).
Plant J. 1997 Jul;12(1):39-48
PMID: 9263451
-
Molecular analysis of cellulose biosynthesis in Arabidopsis.
Science. 1998 Jan 30;279(5351):717-20
PMID: 9445479
-
The expression pattern of the gene for NPK1 protein kinase related to mitogen-activated protein kinase kinase kinase (MAPKKK) in a tobacco plant: correlation with cell proliferation.
Plant Cell Physiol. 1998 Jul;39(7):690-700
PMID: 9729893
-
A plasma membrane-bound putative endo-1,4-beta-D-glucanase is required for normal wall assembly and cell elongation in Arabidopsis.
EMBO J. 1998 Oct 1;17(19):5563-76
PMID: 9755157
-
Suppression of auxin signal transduction by a MAPK cascade in higher plants.
Nature. 1998 Oct 15;395(6703):716-20
PMID: 9790195
-
MAP kinase pathways in the yeast Saccharomyces cerevisiae.
Microbiol Mol Biol Rev. 1998 Dec;62(4):1264-300
PMID: 9841672
-
A MAP kinase is activated late in plant mitosis and becomes localized to the plane of cell division.
Plant Cell. 1999 Jan;11(1):101-13
PMID: 9878635
-
Mitogen-activated protein kinase: conservation of a three-kinase module from yeast to human.
Physiol Rev. 1999 Jan;79(1):143-80
PMID: 9922370