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Symbiosis

, Volume 78, Issue 2, pp 149–162 | Cite as

A first glimpse at genes important to the Azolla–Nostoc symbiosis

  • Ariana N. EilyEmail author
  • Kathleen M. Pryer
  • Fay-Wei Li
Article

Abstract

Azolla is a small genus of diminutive aquatic ferns with a surprisingly vast potential to benefit the environment and agriculture, as well as to provide insight into the evolution of plant-cyanobacterial symbioses. This capability is derived from the unique relationship Azolla spp. have with their obligate, nitrogen-fixing cyanobacterial symbiont, Nostoc azollae, that resides in their leaves. Although previous work has specified the importance of the exchange of ammonium and sucrose metabolites between these two partners, we have yet to determine the underlying molecular mechanisms that make this symbiosis so successful. The newly sequenced and annotated reference genome of Azolla filiculoides has allowed us to investigate gene expression profiles of A. filiculoides—both with and without its obligate cyanobiont, N. azollae—revealing genes potentially essential to the Azolla-Nostoc symbiosis. We observed the absence of differentially expressed glutamine synthetase (GS) and glutamate synthase (GOGAT) genes, leading to questions about how A. filiculoides regulates the machinery it uses for nitrogen assimilation. Ushering A. filiculoides into the era of transcriptomics sets the stage to truly begin to understand the uniqueness of the Azolla-Nostoc symbiosis.

Keywords

Ferns Nitrogen-assimilation Nitrogen-fixation RNA-sequencing Symbiosis 

Notes

Acknowledgements

The authors thank Kathryn Picard, Karla Sosa, Layne Huiet, Tzu-Tong Kao, Deb Greene, the two anonymous reviewers, and the editor of Symbiosis for their support and feedback on the earlier versions of this manuscript. We are also grateful to Henriette Schluepmann for sending us whole plants of Azolla filiculoides, Eric Monson for expertise in data visualization, David Corcoran for consultation on the transcription factor enrichment analysis, Joseph Jackson and Daniel Higginbotham for computational troubleshooting, and Daniele Armaleo for help and resources with qPCR. The first author is especially grateful to these funding sources: National Science Foundation Graduate Research Fellowship Program, Sigma Xi grant-in-aid of research, Duke Biology grant-in-aid of research, and the Botanical Society of America for conferring the Edgar T. Wherry award to the first author’s presentation of this as a contributed paper in the Pteridological section of Botany 2018. This paper is part of a doctoral dissertation completed at Duke University by ANE under the direction of KMP.

Compliance with ethical standards

Conflict of interest

Authors ANE, F.-W.L., and KMP declare that they have no conflicts of interest.

Supplementary material

13199_2019_599_Fig7_ESM.png (1.2 mb)
Online Resource 1

Confocal fluorescent microscopy images of wild-type A. filiculoides (a) and cyanobiont-free A. filiculoides (b) to show absence of cyanobiont at 200x magnification (PNG 1258 kb)

13199_2019_599_MOESM1_ESM.eps (8.6 mb)
High resolution image (EPS 8846 kb)
13199_2019_599_MOESM2_ESM.xlsx (41 kb)
Online Resource 2 Up-regulated putative symbiosis genes. Gene IDs for each up-regulated putative symbiosis gene with their respective annotations and significance values for their mean log2-fold change gene expression. GO distinctions: molecular function (MF), biological processes (BP), and cellular compartment (CC) (XLSX 41 kb)
13199_2019_599_MOESM3_ESM.xlsx (38 kb)
Online Resource 3 Down-regulated putative symbiosis genes. Gene IDs for each down-regulated putative symbiosis gene with their respective annotations and significance values for their mean log2-fold change gene expression. GO distinctions: molecular function (MF), biological processes (BP), and cellular compartment (CC) (XLSX 38 kb)
13199_2019_599_MOESM4_ESM.docx (17 kb)
Online Resource 4 Glutamine synthetase amino-acid sequence alignment for Azolla filiculoides and Medicago truncatula. The nitrated tyrosine 167 of MtGS1is indicated in bold, blue font; as is the phosphorylated serine 97 of MtGS2. The additional tyrosine residues that are present in MtGS1, and are not in MtGS2 are also highlighted in blue and bold font. The conserved domains are indicated in bold and highlighted with gray boxes. The N-terminal transit peptide and C-terminal extension unique to GS2 is indicated in bold. For brevity, the gene sequence names for A. filiculoides are only provided to the first three digits after the “g” (DOCX 17 kb)
13199_2019_599_MOESM5_ESM.xlsx (30 kb)
Online Resource 5 Post-translational modification prediction results for the glutamine synthetase (GS) amino acid sequences in A. filiculoides. Results list the confidence scores as predicted by the ModPred server (XLSX 29 kb)
13199_2019_599_MOESM6_ESM.xlsx (1017 kb)
Online Resource 6 Post-translational modification prediction results for the glutamate synthase (GOGAT) amino acid sequences in A. filiculoides. Results list the confidence scores as predicted by the ModPred server (XLSX 1016 kb)
13199_2019_599_MOESM7_ESM.xlsx (19 kb)
Online Resource 7 Putative symbiosis gene ontology results. Gene ontology categories resulting from modified goatools output. This includes the regulation of the category (up- or down-regulated), information on the GO category and hierarchy levels, the number of genes and gene IDs per category, and the p value (XLSX 18 kb)

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© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.Department of BiologyDuke UniversityDurhamUSA
  2. 2.Boyce Thompson Institute & Plant Biology SectionCornell UniversityIthacaUSA

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