Plastid genome structure and phylogenomics of Nymphaeales: conserved gene order and new insights into relationships

Abstract

The plastid genomes of early-diverging angiosperms were among the first land plant plastomes investigated. Despite their importance to understanding angiosperm evolution, no investigation has so far compared gene content or gene synteny of these plastid genomes with a focus on the Nymphaeales. Here, we report an evaluation and comparison of gene content, gene synteny and inverted repeat length for a set of 15 plastid genomes of early-diverging angiosperms. Seven plastid genomes of the Nymphaeales were newly sequenced for this investigation. We compare gene order and inverted repeat (IR) length across all genomes, review the gene annotations of previously published genomes, generate a multi-gene alignment of 77 plastid-encoded genes and reconstruct the phylogenetic relationships of the taxa under study. Our results show that gene content and synteny are highly conserved across early-diverging angiosperms: All species analyzed display complete gene synteny when accounting for expansions and contractions of the IRs. This conservation was initially obscured by ambiguous and potentially incorrect gene annotations in previously published genomes. We also report the presence of intact open reading frames across all taxa analyzed. The multi-gene phylogeny displays maximum support for the families Cabombaceae and Hydatellaceae, but no support for a clade of all Nymphaeaceae. It further indicates that the genus Victoria is embedded within Nymphaea. Plastid genomes of Trithuria were found to deviate by numerous substitutions and length changes in the IRs. Phylogenetic analyses further indicate that a previously published plastome named Nymphaea mexicana falls into a clade of N. odorata and should be re-evaluated.

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Acknowledgements

The authors would like to thank Virginia Duwe of the Botanischer Garten und Botanisches Museum Berlin and Bettina Giesicke of the Freie Universität Berlin for assistance with DNA extractions. The authors also thank Susan Mbedi of the Berlin Center for Genomics in Biodiversity Research for assistance with Illumina library preparations. Moreover, the authors would like to thank the gardeners of the Botanischer Garten und Botanisches Museum Berlin for cultivating the water lily living collection in the greenhouses that provided the specimens of the taxa under study. Finally, the authors would like to acknowledge the high-performance computing service of the ZEDAT of the Freie Universität Berlin for providing allocations of computing time. This investigation was supported by a start-up grant (Initiativmittel der Forschungskommission) of the Freie Universität Berlin to MG.

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Handling editor: Marcus Koch.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Online Resource 1

Species name, taxonomic position, place of publication, GenBank accession number and other associated information for each of the 15 plastid genomes analyzed. (PDF 95 kb)

Online Resource 2

Overview of read number, mean read length, coverage depth, contig number, contig length and other assembly statistics of plastid genomes that were newly-generated for this investigation. (PDF 82 kb)

Online Resource 3

Circular plastome maps of Nymphaea alba (KU234277), Barclaya longifolia (KY284156), Nymphaea ampla (KU189255), Nymphaea jamesoniana (NC_031826), Victoria cruziana (KY001813), Brasenia schreberi (NC_031343) and Cabomba caroliniana (KT705317). (PDF 1194 kb)

Online Resource 4

Individual partitions and their best-fitting nucleotide substitution models of the four data partitioning strategies. (PDF 88 kb)

Online Resource 5

Alignment of the hypothetical gene ycf15 across the study taxa. (PDF 8906 kb)

Online Resource 6

Alignment of hypothetical gene ycf68 across the study taxa. (PDF 9564 kb)

Online Resource 7

Alignment of the open reading frame orf42 across the study taxa. (PDF 311 kb)

Online Resource 8

Alignment of the open reading frame orf56 across the study taxa. (PDF 225 kb)

Online Resource 9

Best ML trees inferred from the multi-gene dataset of 77 plastid-encoded genes under four different data partitioning strategies. (PDF 733 kb)

Information on Electronic Supplementary Material

Information on Electronic Supplementary Material

Online Resource 1. Species name, taxonomic position, place of publication, GenBank accession number and other associated information for each of the 15 plastid genomes analyzed.

Online Resource 2. Overview of read number, mean read length, coverage depth, contig number, contig length and other assembly statistics of plastid genomes that were newly-generated for this investigation.

Online Resource 3. Circular plastome maps of Nymphaea alba (KU234277), Barclaya longifolia (KY284156), Nymphaea ampla (KU189255), Nymphaea jamesoniana (NC_031826), Victoria cruziana (KY001813), Brasenia schreberi (NC_031343) and Cabomba caroliniana (KT705317).

Online Resource 4. Individual partitions and their best-fitting nucleotide substitution models of the four data partitioning strategies.

Online Resource 5. Alignment of the hypothetical gene ycf15 across the study taxa.

Online Resource 6. Alignment of hypothetical gene ycf68 across the study taxa.

Online Resource 7. Alignment of the open reading frame orf42 across the study taxa.

Online Resource 8. Alignment of the open reading frame orf56 across the study taxa.

Online Resource 9. Best ML trees inferred from the multi-gene dataset of 77 plastid-encoded genes under four different data partitioning strategies.

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Gruenstaeudl, M., Nauheimer, L. & Borsch, T. Plastid genome structure and phylogenomics of Nymphaeales: conserved gene order and new insights into relationships. Plant Syst Evol 303, 1251–1270 (2017). https://doi.org/10.1007/s00606-017-1436-5

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Keywords

  • Early-diverging angiosperms
  • Gene annotations
  • Gene order
  • Inverted repeats
  • Nymphaeales
  • Plastid genome