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Caught in action: fine-scale plastome evolution in the parasitic plants of Cuscuta section Ceratophorae (Convolvulaceae)

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A Correction to this article was published on 24 September 2019

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Abstract

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An exhaustive analysis of a group of closely related parasitic plants shows a predominantly gradual reduction in plastid genome composition and provides the most reduced plastomes in the genus Cuscuta.

Abstract

Parasitic plants have a diminished to completely absent reliance on photosynthesis, and are characterized by sweeping morphological, physiological, and genomic changes. The plastid genome (plastome) is highly conserved in autotrophic plants but is often reduced in parasites, and provides a useful system for documenting the genomic effects of a loss of photosynthesis. Previous studies have shown a substantial degree of heterogeneity in plastome length and composition across the species of the genus Cuscuta. Specifically, species in Cuscuta sect. Ceratophorae were suspected to exhibit even more dynamic plastome evolution than the rest of the genus. This complex of eight closely related species was exhaustively sampled here, and one accession per species was sequenced via a high-throughput approach. Complete plastid genomes were assembled and annotated for each of these species and were found to be 61–87 kbp in length, representing a 45–60% reduction relative to autotrophic Convolvulaceae. The most reduced plastomes on this spectrum have lost the bulk of their photosynthetic genes and are the first fully holoparasitic plastomes described for Cuscuta. The fine-scale nature of the system introduced here allowed us to phylogenetically triangulate the locations of gene loss and pseudogenization events precisely, and to construct a step-by-step model of plastome evolution in these plants. This model reveals an intense burst of gene loss along the branch leading to the most reduced plastomes, and a few idiosyncratic changes elsewhere, allowing us to conclude that the tempo of plastid evolution in sect. Ceratophorae is a blend of gradual and punctuated mode.

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Change history

  • 24 September 2019

    Regrettably, an in-text citation wasn’t listed in the reference section of the above mentioned publication. The citation reads Schneider et al. (2018) and the correct reference is published here.

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Acknowledgements

Special thanks to Eleazer Carranza, Mihai Costea, Ignacio Garcia Ruiz, Marc Johnson, and Tom Van Devender for tissue collections crucial to this project. We are also grateful to two anonymous reviewers for their valuable comments that have improved the quality of the manuscript. This work was supported by the Natural Sciences and Engineering Research Council of Canada (Grant No. 326439); the Canada Foundation for Innovation (Grant No. 12810); and Ontario Research Funds, all to S.S.

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Authors

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AB and SS conceived the research conducted here. SS obtained plant tissue and extracted DNA. AB prepared samples for high-throughput sequencing and performed plastome assemblies and annotations. Analyses were conducted by both AB and SS. AB produced the first draft of the manuscript. Both authors have read and approved the final version of the manuscript.

Corresponding author

Correspondence to Arjan Banerjee.

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Supplementary material 1 (DOCX 371 kb)

11103_2019_884_MOESM2_ESM.eps

Supplementary material 2 (EPS 56 kb) Fig. S1 Whole-plastome alignment for the species assembled from Cuscuta section Ceratophorae

11103_2019_884_MOESM3_ESM.eps

Supplementary material 3 (EPS 287 kb) Fig. S2 dN vs. dS branch lengths for four additional genes from Cuscuta section Ceratophorae plastomes

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Banerjee, A., Stefanović, S. Caught in action: fine-scale plastome evolution in the parasitic plants of Cuscuta section Ceratophorae (Convolvulaceae). Plant Mol Biol 100, 621–634 (2019). https://doi.org/10.1007/s11103-019-00884-0

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  • DOI: https://doi.org/10.1007/s11103-019-00884-0

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