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Journal of Molecular Evolution

, Volume 86, Issue 8, pp 554–565 | Cite as

The Ammonium Channel NOD26 is the Evolutionary Innovation that Drives the Emergence, Consolidation, and Dissemination of Nitrogen-Fixing Symbiosis in Angiosperms

  • Romina Frare
  • Nicolás Ayub
  • Karina Alleva
  • Gabriela Soto
Original Article

Abstract

Increasing evidence indicates that N-fixing symbiosis has evolved several times in the N-fixing clade of angiosperms and that this evolution is driven by a single evolutionary innovation. However, the genetics of this ancestral predisposition to N-fixing symbiosis remains unclear. A natural candidate for such molecular innovation is the ammonium channel NOD26, the main protein component of the symbiosome membrane, which facilitates the plant uptake of the nitrogen fixed by symbiotic bacteria. Here, in concordance with the emergence of N-fixing symbiosis in angiosperms but not in ancestral plants, phylogenetic analysis showed that NOD26 belongs to an angiosperm-exclusive subgroup of aquaporins. Integrated genomic, phylogenetic, and gene expression analyses supported NOD26 occurrence in the N-fixing clade, the increase in the NOD26 copy number by block and tandem duplications in legumes, and the low-copy number or even the loss of NOD26 in non-legume species of the N-fixing clade, which correlated with the possibility to lose N-fixing symbiosis in legume and non-legume lineages. Metabolic reconstructions showed that retention of NOD26 in N-fixing precursor could represent an adaptive mechanism to bypass energy crisis during anaerobic stress by ammonium detoxification. Finally, we discuss the potential use of NOD26 to transfer N-fixation to non-N-fixing crops as cereals.

Keywords

Ammonium Channel Preadaptation Anaerobic Symbiosis Evolution 

Notes

Acknowledgements

This work was supported by Grant PICT-2015-0090 provided to Gabriela Soto.

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Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Instituto de Genética Ewald A. Favret (IGEAF)Buenos AiresArgentina
  2. 2.Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET)Buenos AiresArgentina
  3. 3.Instituto de Química y Fisicoquímica Biológica (IQUIFIB)Buenos AiresArgentina

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