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

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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.

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References

  • Abascal F, Irisarri I, Zardoya R (2014) Diversity and evolution of membrane intrinsic proteins. Biochim Biophys Acta 1840:1468

    Article  CAS  Google Scholar 

  • Allegre A, Silvestre J, Morard P, Kallerhoff J, Pinelli E (2004) Nitrate reductase regulation in tomato roots by exogenous nitrate: a possible role in tolerance to long-term root anoxia. J Exp Bot 55:2625

    Article  CAS  Google Scholar 

  • Azad AK, Yoshikawa N, Ishikawa T, Sawa Y, Shibata H (2012) Substitution of a single amino acid residue in the aromatic/arginine selectivity filter alters the transport profiles of tonoplast aquaporin homologs. Biochim Biophys Acta 1818:1

    Article  CAS  Google Scholar 

  • Benedito VA, Torres-Jerez I, Murray JD, Andriankaja A, Allen S, Kakar K, Wandrey M, Verdier J, Zuber H, Ott T, Moreau S, Niebel A, Frickey T, Weiller G, He J, Dai X, Zhao PX, Tang Y, Udvardi MK (2008) A gene expression atlas of the model legume Medicago truncatula. Plant J 55:504

    Article  CAS  Google Scholar 

  • Bertioli DJ, Moretzsohn MC, Madsen LH, Sandal N, Leal-Bertioli SC, Guimaraes PM, Hougaard BK, Fredslund J, Schauser L, Nielsen AM, Sato S, Tabata S, Cannon SB, Stougaard J (2009) An analysis of synteny of Arachis with Lotus and Medicago sheds new light on the structure, stability and evolution of legume genomes. BMC Genom 10:45

    Article  Google Scholar 

  • Bobik C, Meilhoc E, Batut J (2006) FixJ: a major regulator of the oxygen limitation response and late symbiotic functions of Sinorhizobium meliloti. J Bacteriol 188:4890

    Article  CAS  Google Scholar 

  • Campanella JJ, Bitincka L, Smalley J (2003) MatGAT: an application that generates similarity/identity matrices using protein or DNA sequences. BMC Bioinform 4:29

    Article  Google Scholar 

  • Choi WG, Roberts DM (2007) Arabidopsis NIP2;1, a major intrinsic protein transporter of lactic acid induced by anoxic stress. J Biol Chem 282:24209

    Article  CAS  Google Scholar 

  • Chopra R, Burow G, Farmer A, Mudge J, Simpson CE, Burow MD (2014) Comparisons of de novo transcriptome assemblers in diploid and polyploid species using peanut (Arachis spp.) RNA-Seq data. PLoS ONE 9:e115055

    Article  Google Scholar 

  • Cleland C, Xa E (2002) Methodological and epistemic differences between historical science and experimental science*. Philos Sci 69:447

    Article  Google Scholar 

  • Di Giorgio JA, Bienert GP, Ayub ND, Yaneff A, Barberini ML, Mecchia MA, Amodeo G, Soto GC, Muschietti JP (2016) Pollen-specific aquaporins NIP4;1 and NIP4;2 are required for pollen development and pollination in Arabidopsis thaliana. Plant Cell 28:1053

    Article  Google Scholar 

  • Doyle JJ (2011) Phylogenetic perspectives on the origins of nodulation. Mol Plant Microbe Interact 24:1289

    Article  CAS  Google Scholar 

  • Doyle JJ (2016) Chasing unicorns: nodulation origins and the paradox of novelty. Am J Bot 103:1865

    Article  Google Scholar 

  • Esteban R, Ariz I, Cruz C, Moran JF (2016) Review: mechanisms of ammonium toxicity and the quest for tolerance. Plant Sci 248:92

    Article  CAS  Google Scholar 

  • Felle HH (2005) pH regulation in anoxic plants. Ann Bot 96:519

    Article  CAS  Google Scholar 

  • Fortin MG, Morrison NA, Verma DP (1987) Nodulin-26, a peribacteroid membrane nodulin is expressed independently of the development of the peribacteroid compartment. Nucleic Acids Res 15:813

    Article  CAS  Google Scholar 

  • Galardini M, Pini F, Bazzicalupo M, Biondi EG, Mengoni A (2013) Replicon-dependent bacterial genome evolution: the case of Sinorhizobium meliloti. Genome Biol Evol 5:542

    Article  Google Scholar 

  • Geurts R, Xiao TT, Reinhold-Hurek B (2016) What does it take to evolve a nitrogen-fixing endosymbiosis? Trends Plant Sci 21:199

    Article  CAS  Google Scholar 

  • Griesmann M, Chang Y, Liu X, Song Y, Haberer G, Crook MB, Billault-Penneteau B, Lauressergues D, Keller J, Imanishi L, Roswanjaya YP, Kohlen W, Pujic P, Battenberg K, Alloisio N, Liang Y, Hilhorst H, Salgado MG, Hocher V, Gherbi H, Svistoonoff S, Doyle JJ, He S, Xu Y, Xu S, Qu J, Gao Q, Fang X, Fu Y, Normand P, Berry AM, Wall LG, Ane JM, Pawlowski K, Xu X, Yang H, Spannagl M, Mayer KFX, Wong GK, Parniske M, Delaux PM, Cheng S (2018) Phylogenomics reveals multiple losses of nitrogen-fixing root nodule symbiosis. Science https://doi.org/10.1126/science.aat1743

    Article  PubMed  Google Scholar 

  • Haskett TL, Terpolilli JJ, Bekuma A, O’Hara GW, Sullivan JT, Wang P, Ronson CW, Ramsay JP (2016) Assembly and transfer of tripartite integrative and conjugative genetic elements. Proc Natl Acad Sci USA 113:12268

    Article  CAS  Google Scholar 

  • Hwang JH, Ellingson SR, Roberts DM (2010) Ammonia permeability of the soybean nodulin 26 channel. FEBS Lett 584:4339

    Article  CAS  Google Scholar 

  • Jones KM, Kobayashi H, Davies BW, Taga ME, Walker GC (2007) How rhizobial symbionts invade plants: the Sinorhizobium–Medicago model. Nat Rev Microbiol 5:619–633

    Article  CAS  Google Scholar 

  • Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, Buxton S, Cooper A, Markowitz S, Duran C, Thierer T, Ashton B, Meintjes P, Drummond A (2012) Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28:1647

    Article  Google Scholar 

  • Krenc D, Song J, Almasalmeh A, Wu B, Beitz E (2014) The arginine-facing amino acid residue of the rat aquaporin 1 constriction determines solute selectivity according to its size and lipophilicity. Mol Membr Biol 31:228

    Article  CAS  Google Scholar 

  • Lavin M, Herendeen PS, Wojciechowski MF (2005) Evolutionary rates analysis of Leguminosae implicates a rapid diversification of lineages during the tertiary. Syst Biol 54:575

    Article  Google Scholar 

  • Libault M, Farmer A, Brechenmacher L, Drnevich J, Langley RJ, Bilgin DD, Radwan O, Neece DJ, Clough SJ, May GD, Stacey G (2010) Complete transcriptome of the soybean root hair cell, a single-cell model, and its alteration in response to Bradyrhizobium japonicum infection. Plant Physiol 152:541

    Article  CAS  Google Scholar 

  • O’Rourke JA, Iniguez LP, Fu F, Bucciarelli B, Miller SS, Jackson SA, McClean PE, Li J, Dai X, Zhao PX, Hernandez G, Vance CP (2014) An RNA-Seq based gene expression atlas of the common bean. BMC Genom 15:866

    Article  Google Scholar 

  • Ott T, van Dongen JT, Gunther C, Krusell L, Desbrosses G, Vigeolas H, Bock V, Czechowski T, Geigenberger P, Udvardi MK (2005) Symbiotic leghemoglobins are crucial for nitrogen fixation in legume root nodules but not for general plant growth and development. Curr Biol 15:531

    Article  CAS  Google Scholar 

  • Oyserman BO, Moya F, Lawson CE, Garcia AL, Vogt M, Heffernen M, Noguera DR, McMahon KD (2016) Ancestral genome reconstruction identifies the evolutionary basis for trait acquisition in polyphosphate accumulating bacteria. ISME J 10:2931

    Article  Google Scholar 

  • Perez Di Giorgio J, Soto G, Alleva K, Jozefkowicz C, Amodeo G, Muschietti JP, Ayub ND (2014) Prediction of aquaporin function by integrating evolutionary and functional analyses. J Membr Biol 247:107

    Article  CAS  Google Scholar 

  • Schmutz J, Cannon SB, Schlueter J, Ma J, Mitros T, Nelson W, Hyten DL, Song Q, Thelen JJ, Cheng J, Xu D, Hellsten U, May GD, Yu Y, Sakurai T, Umezawa T, Bhattacharyya MK, Sandhu D, Valliyodan B, Lindquist E, Peto M, Grant D, Shu S, Goodstein D, Barry K, Futrell-Griggs M, Abernathy B, Du J, Tian Z, Zhu L, Gill N, Joshi T, Libault M, Sethuraman A, Zhang XC, Shinozaki K, Nguyen HT, Wing RA, Cregan P, Specht J, Grimwood J, Rokhsar D, Stacey G, Shoemaker RC, Jackson SA (2010) Genome sequence of the palaeopolyploid soybean. Nature 463:178

    Article  CAS  Google Scholar 

  • Shingaki-Wells R, Millar AH, Whelan J, Narsai R (2014) What happens to plant mitochondria under low oxygen? An omics review of the responses to low oxygen and reoxygenation. Plant Cell Environ 37:2260

    CAS  PubMed  Google Scholar 

  • Shubin N, Tabin C, Carroll S (2009) Deep homology and the origins of evolutionary novelty. Nature 457:818

    Article  CAS  Google Scholar 

  • Soltis DE, Soltis PS, Morgan DR, Swensen SM, Mullin BC, Dowd JM, Martin PG (1995) Chloroplast gene sequence data suggest a single origin of the predisposition for symbiotic nitrogen fixation in angiosperms. Proc Natl Acad Sci USA 92:2647

    Article  CAS  Google Scholar 

  • Svistoonoff S, Benabdoun FM, Nambiar-Veetil M, Imanishi L, Vaissayre V, Cesari S, Diagne N, Hocher V, de Billy F, Bonneau J, Wall L, Ykhlef N, Rosenberg C, Bogusz D, Franche C, Gherbi H (2013) The independent acquisition of plant root nitrogen-fixing symbiosis in Fabids recruited the same genetic pathway for nodule organogenesis. PLoS ONE 8:e64515

    Article  CAS  Google Scholar 

  • van Velzen R, Holmer R, Bu F, Rutten L, van Zeijl A, Liu W, Santuari L, Cao Q, Sharma T, Shen D, Roswanjaya Y, Wardhani TAK, Kalhor MS, Jansen J, van den Hoogen J, Gungor B, Hartog M, Hontelez J, Verver J, Yang WC, Schijlen E, Repin R, Schilthuizen M, Schranz ME, Heidstra R, Miyata K, Fedorova E, Kohlen W, Bisseling T, Smit S, Geurts R (2018) Comparative genomics of the nonlegume Parasponia reveals insights into evolution of nitrogen-fixing rhizobium symbioses. Proc Natl Acad Sci USA 115:E4700

    Article  Google Scholar 

  • Verdier J, Torres-Jerez I, Wang M, Andriankaja A, Allen SN, He J, Tang Y, Murray JD, Udvardi MK (2013) Establishment of the Lotus japonicus Gene Expression Atlas (LjGEA) and its use to explore legume seed maturation. Plant J 74:351

    Article  CAS  Google Scholar 

  • Werner GD, Cornwell WK, Sprent JI, Kattge J, Kiers ET (2014) A single evolutionary innovation drives the deep evolution of symbiotic N2-fixation in angiosperms. Nat Commun 5:4087

    Article  CAS  Google Scholar 

  • Williams JH (2008) Novelties of the flowering plant pollen tube underlie diversification of a key life history stage. Proc Natl Acad Sci USA 105:11259

    Article  CAS  Google Scholar 

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Acknowledgements

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

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Authors and Affiliations

  1. Instituto de Genética Ewald A. Favret (IGEAF), De los Reseros S/N, Castelar C25(1712), Buenos Aires, Argentina

    Romina Frare, Nicolás Ayub, Karina Alleva & Gabriela Soto

  2. Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Buenos Aires, Argentina

    Romina Frare, Nicolás Ayub & Gabriela Soto

  3. Instituto de Química y Fisicoquímica Biológica (IQUIFIB), Buenos Aires, Argentina

    Karina Alleva

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  1. Romina Frare
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  2. Nicolás Ayub
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  3. Karina Alleva
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  4. Gabriela Soto
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Correspondence to Gabriela Soto.

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Frare, R., Ayub, N., Alleva, K. et al. The Ammonium Channel NOD26 is the Evolutionary Innovation that Drives the Emergence, Consolidation, and Dissemination of Nitrogen-Fixing Symbiosis in Angiosperms. J Mol Evol 86, 554–565 (2018). https://doi.org/10.1007/s00239-018-9867-3

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  • DOI: https://doi.org/10.1007/s00239-018-9867-3

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