Endoreduplication mediated by the anaphase-promoting complex activator CCS52A is required for symbiotic cell differentiation in Medicago truncatula nodules

Jose Maria Vinardell, Elena Fedorova, Angel Cebolla, Zoltan Kevei, G. Horváth, Zsolt Kelemen, Sylvie Tarayre, François Roudier, Peter Mergaert, Adam Kondorosi, É. Kondorosi

Research output: Contribution to journalArticle

127 Citations (Scopus)

Abstract

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 β-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.

Original languageEnglish
Pages (from-to)2093-2105
Number of pages13
JournalPlant Cell
Volume15
Issue number9
DOIs
Publication statusPublished - Sep 1 2003

Fingerprint

Endoreduplication
Medicago truncatula
Anaphase-Promoting Complex-Cyclosome
endopolyploidy
cell differentiation
Cell Differentiation
Genes
Glucuronidase
Transcription
Ligases
Ubiquitin
Yeast
Ploidies
Bacteria
Animals
Nitrogen
cells
ploidy
Cell Enlargement
Substrates

ASJC Scopus subject areas

  • Plant Science
  • Biochemistry, Genetics and Molecular Biology(all)
  • Biochemistry
  • Cell Biology

Cite this

Endoreduplication mediated by the anaphase-promoting complex activator CCS52A is required for symbiotic cell differentiation in Medicago truncatula nodules. / Vinardell, Jose Maria; Fedorova, Elena; Cebolla, Angel; Kevei, Zoltan; Horváth, G.; Kelemen, Zsolt; Tarayre, Sylvie; Roudier, François; Mergaert, Peter; Kondorosi, Adam; Kondorosi, É.

In: Plant Cell, Vol. 15, No. 9, 01.09.2003, p. 2093-2105.

Research output: Contribution to journalArticle

Vinardell, JM, Fedorova, E, Cebolla, A, Kevei, Z, Horváth, G, Kelemen, Z, Tarayre, S, Roudier, F, Mergaert, P, Kondorosi, A & Kondorosi, É 2003, 'Endoreduplication mediated by the anaphase-promoting complex activator CCS52A is required for symbiotic cell differentiation in Medicago truncatula nodules', Plant Cell, vol. 15, no. 9, pp. 2093-2105. https://doi.org/10.1105/tpc.014373
Vinardell, Jose Maria ; Fedorova, Elena ; Cebolla, Angel ; Kevei, Zoltan ; Horváth, G. ; Kelemen, Zsolt ; Tarayre, Sylvie ; Roudier, François ; Mergaert, Peter ; Kondorosi, Adam ; Kondorosi, É. / Endoreduplication mediated by the anaphase-promoting complex activator CCS52A is required for symbiotic cell differentiation in Medicago truncatula nodules. In: Plant Cell. 2003 ; Vol. 15, No. 9. pp. 2093-2105.
@article{afa26a1631d74322b098626ce9dd07c8,
title = "Endoreduplication mediated by the anaphase-promoting complex activator CCS52A is required for symbiotic cell differentiation in Medicago truncatula nodules",
abstract = "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 β-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.",
author = "Vinardell, {Jose Maria} and Elena Fedorova and Angel Cebolla and Zoltan Kevei and G. Horv{\'a}th and Zsolt Kelemen and Sylvie Tarayre and Fran{\cc}ois Roudier and Peter Mergaert and Adam Kondorosi and {\'E}. Kondorosi",
year = "2003",
month = "9",
day = "1",
doi = "10.1105/tpc.014373",
language = "English",
volume = "15",
pages = "2093--2105",
journal = "Plant Cell",
issn = "1040-4651",
publisher = "American Society of Plant Biologists",
number = "9",

}

TY - JOUR

T1 - Endoreduplication mediated by the anaphase-promoting complex activator CCS52A is required for symbiotic cell differentiation in Medicago truncatula nodules

AU - Vinardell, Jose Maria

AU - Fedorova, Elena

AU - Cebolla, Angel

AU - Kevei, Zoltan

AU - Horváth, G.

AU - Kelemen, Zsolt

AU - Tarayre, Sylvie

AU - Roudier, François

AU - Mergaert, Peter

AU - Kondorosi, Adam

AU - Kondorosi, É.

PY - 2003/9/1

Y1 - 2003/9/1

N2 - 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 β-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.

AB - 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 β-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.

UR - http://www.scopus.com/inward/record.url?scp=0141564565&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=0141564565&partnerID=8YFLogxK

U2 - 10.1105/tpc.014373

DO - 10.1105/tpc.014373

M3 - Article

VL - 15

SP - 2093

EP - 2105

JO - Plant Cell

JF - Plant Cell

SN - 1040-4651

IS - 9

ER -