The N-metabolites of roots and actinorhizal nodules from Alnus glutinosa and Datisca glomerata: can D. glomerata change N-transport forms when nodulated?
- 166 Downloads
To gain more insight in nitrogen metabolism in actinorhizal nodules, a comparison between the N metabolite profiles in roots vs. nodules was initiated for one host plant from the best-examined order of actinorhizal plants, Fagales, A. glutinosa (Betulaceae), a temperate tree, and one host plant from the Cucurbitales order, Datisca glomerata (Datiscaceae). For both symbioses, the symbiotic transcriptomes have been published and can be used to assess the expression of genes representing specific metabolic pathways in nodules. The amino acid profiles of roots in this study suggest that A. glutinosa transported aspartate, glutamate and citrulline in the xylem, a combination of nitrogenous solutes not published previously for this species. The amino acid profiles of D. glomerata roots depended on whether the plants were nodulated or grown on nitrate; roots of nodulated plants contained increased amounts of arginine. Although bacterial transcriptome data showed no symbiotic auxotrophy for branched chain amino acids (leucine, isoleucine, valine) in either symbiosis, D. glomerata nodules contained comparatively high levels of these amino acids. This might represent a response to osmotic stress.
KeywordsActinorhiza Frankia Nitrogen-fixation Arginine Gamma-aminobutyrate (GABA) Citrulline
We would like to thank Peter Litfors for taking care of the plants in Stockholm and Pascale Fournier for A. glutinosa growth experiments and harvesting of roots and nodules. This work was funded by grants from the Swedish Research Council Formas (229-2005-679) and the Carl Tryggers Foundation to KP, by a grant from the French ANR (Sesam ANR-10-BLAN-1708 and BugsInACell ANR-13-BSV7-0013-03), to PN, and by USDA CA-D* PLS-2173-H to AMB.
- Carro L, Pujic P, Alloisio N, Fournier P, Boubakri H, Hay AE, Poly F, François P, Hocher V, Mergaert P, Balmand S, Rey M, Heddi A, Normand P (2015) Alnus peptides modify membrane porosity and induce the release of nitrogen-rich metabolites from nitrogen-fixing Frankia. ISME J 9:1723–1733CrossRefPubMedPubMedCentralGoogle Scholar
- Hoagland DR, Arnon DT (1938) The water-culture method for growing plants without soil, California Agriculture Experiment Station Circular 347. University of CA, BerkeleyGoogle Scholar
- Hocher V, Alloisio N, Auguy F, Fournier P, Doumas P, Pujic P, Gherbi H, Queiroux C, Da Silva C, Wincker P, Normand P, Bogusz D (2011) Transcriptomics of actinorhizal symbioses reveals homologs of the whole common symbiotic signaling cascade. Plant Physiol 156:700–711CrossRefPubMedPubMedCentralGoogle Scholar
- Hosie AHF, Allaway D, Galloway CS, Dunsby HA, Poole PS (2002) Rhizobium leguminosarum has a second general amino acid permease with unusually broad substrate specificity and high similarity to branched-chain amino acid transporters (Bra/LIV) of the ABC family. J Bacteriol 184:4071–4080CrossRefPubMedPubMedCentralGoogle Scholar
- Karp PD, Paley SM, Krummenacker M, Latendresse M, Dale JM, Lee TJ, Kaipa P, Gilham F, Spaulding A, Popescu L, Altman T, Paulsen I, Keseler IM, Caspi R (2010) Pathway tools version 13.0: integrated software for pathway/genome informatics and systems biology. Brief Bioinform 11:40–79CrossRefPubMedGoogle Scholar
- Normand P, Lapierre P, Tisa LS, Gogarten JP, Alloisio N, Bagnarol E, Bassi CA, Berry AM, Bickhart DM, Choisne N, Couloux A, Cournoyer B, Cruveiller S, Daubin V, Demange N, Francino MP, Goltsman E, Huang Y, Kopp OR, Labarre L, Lapidus A, Lavire C, Marechal J, Martinez M, Mastronunzio JE, Mullin BC, Niemann J, Pujic P, Rawnsley T, Rouy Z, Schenowitz C, Sellstedt A, Tavares F, Tomkins JP, Vallenet D, Valverde C, Wall LG, Wang Y, Medigue C, Benson DR (2007) Genome characteristics of facultatively symbiotic Frankia sp. strains reflect host range and host plant biogeography. Genome Res 17:7–15CrossRefPubMedPubMedCentralGoogle Scholar
- Persson T, Benson DR, Normand P, Vanden Heuvel B, Pujic P, Chertkov O, Teshima H, Bruce BC, Detter C, Tapia R, Han S, Han J, Woyke T, Pitluck S, Pennacchio L, Nolan M, Ivanova N, Pati A, Land ML, Pawlowski K, Berry AM (2011) The genome of Candidatus Frankia datiscae Dg1, the uncultured microsymbiont from nitrogen-fixing root nodules of the dicot Datisca glomerata. J Bacteriol 193:7017–7018CrossRefPubMedPubMedCentralGoogle Scholar
- Persson T, Battenberg K, Demina IV, Vigil-Stenman T, Vanden Heuvel B, Pujic P, Facciotti MT, Wilbanks EG, O’Brien A, Fournier P, Cruz Hernandez MA, Mendoz Herrera A, Médigue C, Normand P, Pawlowski K, Berry AM (2015) Candidatus Frankia datiscae Dg1, the actinobacterial microsymbiont of Datisca glomerata, expresses the canonical nod genes nodABC in symbiosis with its host plant. PLoS One 10:e0127630CrossRefPubMedPubMedCentralGoogle Scholar
- Sen A, Daubin V, Abrouk D, Gifford I, Berry AM, Normand P (2014) Phylogeny of the class Actinobacteria revisited in the light of complete genomes. The orders ‘Frankiales’ and Micrococcales should be split into coherent entities: proposal of Frankiales ord. nov., Geodermatophilales ord. nov., Acidothermales ord. nov. and Nakamurellales ord. nov. Int J Syst Evol Microbiol 64:3821–3832CrossRefPubMedGoogle Scholar
- Simonet P, Navarro E, Rouvier C, Reddell P, Zimpfer J, Dawson J, Dommergues Y, Bardin R, Combarro P, Hamelin J, Domenach A-M, Gourbière F, Prin Y, Normand P (1999) Co-evolution between Frankia populations and host plants in the family Casuarinaceae and consequent patterns of global dispersal. Environ Microbiol 1:525–535CrossRefPubMedGoogle Scholar
- Snedden WA, Fromm H (1999) Regulation of the γ-aminobutyrate-synthesizing enzyme, glutamate decarboxylase, by calcium–calmodulin: a mechanism for rapid activation in response to stress. In: Lerner HR (ed) Plant responses to environmental stresses: from phytohormones to genome reorganization. Marcel Dekker, New York, pp. 549–574Google Scholar