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IPD3 Controls the Formation of Nitrogen-Fixing Symbiosomes in Pea and Medicago Spp.

November 2011 , Volume 24 , Number  11
Pages  1,333 - 1,344

Evgenia Ovchinnikova,1,2 Etienne-Pascal Journet,3,4 Mireille Chabaud,3,4 Viviane Cosson,5 Pascal Ratet,5 Gerard Duc,6 Elena Fedorova,1 Wei Liu,1 Rik Op den Camp,1 Vladimir Zhukov,2 Igor Tikhonovich,2 Alexey Borisov,2 Ton Bisseling,1,7 and Erik Limpens1

1Department of Molecular Biology, Wageningen University, Droevendaalsesteeg 1, 6708 PB, Wageningen, The Netherlands; 2All-Russia Research Institute for Agricultural Microbiology, Laboratory of Genetics of Plant-Microbe Interactions, Podbelsky chaussee 3, 196608, Pushkin 8, St. Petersburg, Russia; 3INRA, Laboratoire des Interactions Plantes-Microorganismes (LIPM), UMR441, F-31326 Castanet-Tolosan, France; 4CNRS, LIPM, UMR 2594, F-31326 Castanet-Tolosan, France; 5Institut des Sciences du Végétal, UPR2355, CNRS, Avenue de la Terrasse, 91198, Gif sur Yvette, France; 6Unité Mixte de Recherche en Génétique et Ecophysiologie des Légumineuses, UMR INRA 102, BP 86510, F-21065 Dijon, France; 7King Saud University, P.O. BOX 2454, Riyadh 11451, Kingdom of Saudi Arabia

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Accepted 28 June 2011.

A successful nitrogen-fixing symbiosis requires the accommodation of rhizobial bacteria as new organelle-like structures, called symbiosomes, inside the cells of their legume hosts. Two legume mutants that are most strongly impaired in their ability to form symbiosomes are sym1/TE7 in Medicago truncatula and sym33 in Pisum sativum. We have cloned both MtSYM1 and PsSYM33 and show that both encode the recently identified interacting protein of DMI3 (IPD3), an ortholog of Lotus japonicus (Lotus) CYCLOPS. IPD3 and CYCLOPS were shown to interact with DMI3/CCaMK, which encodes a calcium- and calmodulin-dependent kinase that is an essential component of the common symbiotic signaling pathway for both rhizobial and mycorrhizal symbioses. Our data reveal a novel, key role for IPD3 in symbiosome formation and development. We show that MtIPD3 participates in but is not essential for infection thread formation and that MtIPD3 also affects DMI3-induced spontaneous nodule formation upstream of cytokinin signaling. Further, MtIPD3 appears to be required for the expression of a nodule-specific remorin, which controls proper infection thread growth and is essential for symbiosome formation.

© 2011 The American Phytopathological Society