Endoreduplication mediated by the anaphase-promoting complex activator CCS52A is required for symbiotic cell differentiation in Medicago truncatula nodules.
In Medicago nodules, endoreduplication cycles and ploidy-dependent cell enlargement occur during the differentiation of bacteroid-containing nitrogen-fixing symbiotic cells. These events are accompanied by the expression of ccs52A, a plant ortholog of the yeast and animal cdh1/srw1/fzr genes, acting as a substrate-specific activator of the anaphase-promoting complex (APC) ubiquitin ligase. Because CCS52A is involved in the transition of mitotic cycles to endoreduplication cycles, we investigated the importance of somatic endoploidy and the role of the M. truncatula ccs52A gene in symbiotic cell differentiation. Transcription analysis and ccs52A promoter-driven beta-glucuronidase activity in transgenic plants showed that ccs52A was dispensable for the mitotic cycles and nodule primordium formation, whereas it was induced before nodule differentiation. The CCS52A protein was present in the nucleus of endoreduplication-competent cells, indicating that it may activate APC constitutively during the endoreduplication cycles. Downregulation of ccs52A in transgenic M. truncatula plants drastically affected nodule development, resulting in lower ploidy, reduced cell size, inefficient invasion, and the maturation of symbiotic cells, accompanied by early senescence and finally the death of both the bacterium and plant cells. Thus, ccs52A expression is essential for the formation of large highly polyploid symbiotic cells, and endoreduplication is an integral part of normal nodule development.
Vinardell
Jose Maria
JM
Institut des Sciences du Végétal, Centre National de la Recherche Scientifique Unité Propre de Recherche 2355, 91198 Gif-sur-Yvette, France.
Fedorova
Elena
E
Cebolla
Angel
A
Kevei
Zoltan
Z
Horvath
Gabor
G
Kelemen
Zsolt
Z
Tarayre
Sylvie
S
Roudier
François
F
Mergaert
Peter
P
Kondorosi
Adam
A
Kondorosi
Eva
E
D064173:Anaphase-Promoting Complex-Cyclosome; D017209:Apoptosis / Q000502:physiology; D018797:Cell Cycle Proteins / Q000235:genetics / Q000378:metabolism; D002454:Cell Differentiation / Q000235:genetics* / Q000502:physiology; D002455:Cell Division / Q000235:genetics / Q000502:physiology; D018507:Gene Expression Regulation, Developmental; D018506:Gene Expression Regulation, Plant; D005966:Glucuronidase / Q000235:genetics / Q000378:metabolism; D029902:Medicago / Q000235:genetics* / Q000382:microbiology / Q000648:ultrastructure; D008854:Microscopy, Electron; D009586:Nitrogen Fixation / Q000235:genetics / Q000502:physiology; D010940:Plant Proteins / Q000235:genetics* / Q000378:metabolism; D030821:Plants, Genetically Modified; D011123:Polyploidy; D016962:Sinorhizobium meliloti / Q000254:growth & development / Q000648:ultrastructure; D013559:Symbiosis / Q000235:genetics* / Q000502:physiology; D043743:Ubiquitin-Protein Ligase Complexes / Q000235:genetics* / Q000378:metabolism; D044767:Ubiquitin-Protein Ligases / Q000235:genetics / Q000378:metabolism
D018797:Cell Cycle Proteins; D010940:Plant Proteins; D043743:Ubiquitin-Protein Ligase Complexes; D064173:Anaphase-Promoting Complex-Cyclosome; D044767:Ubiquitin-Protein Ligases; D005966:Glucuronidase