The independent acquisition of plant root nitrogen-fixing symbiosis in Fabids recruited the same genetic pathway for nodule organogenesis

PLoS One. 2013 May 31;8(5):e64515. doi: 10.1371/journal.pone.0064515. Print 2013.

Abstract

Only species belonging to the Fabid clade, limited to four classes and ten families of Angiosperms, are able to form nitrogen-fixing root nodule symbioses (RNS) with soil bacteria. This concerns plants of the legume family (Fabaceae) and Parasponia (Cannabaceae) associated with the Gram-negative proteobacteria collectively called rhizobia and actinorhizal plants associated with the Gram-positive actinomycetes of the genus Frankia. Calcium and calmodulin-dependent protein kinase (CCaMK) is a key component of the common signaling pathway leading to both rhizobial and arbuscular mycorrhizal symbioses (AM) and plays a central role in cross-signaling between root nodule organogenesis and infection processes. Here, we show that CCaMK is also needed for successful actinorhiza formation and interaction with AM fungi in the actinorhizal tree Casuarina glauca and is also able to restore both nodulation and AM symbioses in a Medicago truncatula ccamk mutant. Besides, we expressed auto-active CgCCaMK lacking the auto-inhibitory/CaM domain in two actinorhizal species: C. glauca (Casuarinaceae), which develops an intracellular infection pathway, and Discaria trinervis (Rhamnaceae) which is characterized by an ancestral intercellular infection mechanism. In both species, we found induction of nodulation independent of Frankia similar to response to the activation of CCaMK in the rhizobia-legume symbiosis and conclude that the regulation of actinorhiza organogenesis is conserved regardless of the infection mode. It has been suggested that rhizobial and actinorhizal symbioses originated from a common ancestor with several independent evolutionary origins. Our findings are consistent with the recruitment of a similar genetic pathway governing rhizobial and Frankia nodule organogenesis.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acid Sequence
  • Bacterial Proteins / genetics*
  • Bacterial Proteins / metabolism
  • Biological Evolution
  • Calcium-Calmodulin-Dependent Protein Kinase Kinase / genetics*
  • Calcium-Calmodulin-Dependent Protein Kinase Kinase / metabolism
  • Cannabaceae / enzymology
  • Cannabaceae / genetics*
  • Fabaceae / enzymology
  • Fabaceae / genetics*
  • Frankia / enzymology
  • Frankia / genetics*
  • Gene Expression
  • Genetic Complementation Test
  • Molecular Sequence Data
  • Mutation
  • Mycorrhizae / enzymology
  • Mycorrhizae / genetics*
  • Nitrogen Fixation / physiology
  • Plant Proteins / genetics*
  • Plant Proteins / metabolism
  • Plant Root Nodulation / physiology
  • Rhizobium / enzymology
  • Rhizobium / genetics*
  • Signal Transduction
  • Symbiosis
  • Transduction, Genetic

Substances

  • Bacterial Proteins
  • Plant Proteins
  • Calcium-Calmodulin-Dependent Protein Kinase Kinase

Associated data

  • GENBANK/HF952923
  • GENBANK/HF952924

Grants and funding

Financial support was provided by IRD, grants from Agence Nationale de la Recherche Projects NewNod and SESAM (AN-06-BLAN-0095 and 2010 BLAN 1708 01), University of Quilmes and ECOS-SUD (A07B02). F.M.B. was funded by the European Union (Averroes program). M.N.V. was funded by the Department of Biotechnology, Ministry of Science and Technology, Government of India. L.I. was funded by the IRD Department of Capacity-Building for Southern Scientific Communities (IRD-DPF) and the Argentinean National Research Council (CONICET). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.