Understanding the evolution of holoparasitic plants: the complete plastid genome of the holoparasite Cytinus hypocistis (Cytinaceae) - PubMed (original) (raw)

Understanding the evolution of holoparasitic plants: the complete plastid genome of the holoparasite Cytinus hypocistis (Cytinaceae)

Cristina Roquet et al. Ann Bot. 2016.

Abstract

Background and Aims Plant plastid genomes are highly conserved in size, gene content and structure; however, parasitic plants are a noticeable exception to this evolutionary stability. Although the evolution of parasites could help to better understand plastome evolution in general, complete plastomes of parasites have been sequenced only for some lineages so far. Here we contribute to filling this gap by providing and analysing the complete plastome sequence of Cytinus hypocistis, the first parasite sequenced for Malvales and a species suspected to have an extremely small genome. Methods We sequenced and assembled de novo the plastid genome of Cytinus hypocistis using a shotgun approach on genomic DNA. Phylogenomic analyses based on coding regions were performed on Malvidae. For each coding region present in Cytinus, we tested for relaxation or intensification of selective pressures in the Cytinus lineage compared with autotrophic Malvales. Key Results Cytinus hypocistis has an extremely divergent genome that is among the smallest sequenced to date (19·4 kb), with only 23 genes and no inverted repeat regions. Phylogenomic analysis confirmed the position of Cytinus within Malvales. All coding regions of Cytinus plastome presented very high substitution rates compared with non-parasitic Malvales. Conclusions Some regions were inferred to be under relaxed negative selection in Cytinus, suggesting that further plastome reduction is occurring due to relaxed purifying selection associated with the loss of photosynthetic activity. On the other hand, increased selection intensity and strong positive selection were detected for rpl22 in the Cytinus lineage, which might indicate an evolutionary role in the host-parasite arms race, a point that needs further research.

Keywords: Chloroplast genome; Cytinaceae; Cytinus hypocistis; Malvales; mycoheterotroph; parasite; plastome evolution; selective pressure.

© The Author 2016. Published by Oxford University Press on behalf of the Annals of Botany Company. All rights reserved. For Permissions, please email: journals.permissions@oup.com.

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Figures

<sc>Fig</sc>. 1.

Fig. 1.

Number of unique plastid genes in each functional group of parasite and mycoheterotroph species and their closest autotrophic relative for which the whole plastome has been sequenced (Ptilidium: Forrest et al., 2011; Piper: Cai et al., 2006; Phalaenopsis: Chang et al., 2006; Dioscorea: Hansen et al., 2007; Carludovica: Lam et al., 2015; Vitis: Jansen et al., 2006; Ipomoea: McNeal et al., 2007; Lindenbergia: Wicke et al., 2013; Theobroma: Kane et al., 2012; all references concerning parasitic species are cited in the main text). The species are grouped by the family to which they belong (indicated in grey capital letters). The family of the autotrophic relative is indicated in lower-case letters when it belongs to a different family.

<sc>Fig</sc>. 2.

Fig. 2.

Chloroplast gene phylogeny of Malvidae: phylogram of the maximum likelihood tree determined by RAxML with 200 independent searches. Numbers associated with branches indicate bootstrap support values obtained with 1000 replicates; unnumbered branches had 100 % support. Scale indicates substitutions per site. Collapsed monophyletic clades correspond to five Oenothera, 20 Gossypium and 31 Eucalyptus species. The inserted image shows Cytinus hypocistis parasitizing a Cistus sp. (Stromboli, Aeolian Islands; © Cristina Roquet).

<sc>Fig</sc>. 3.

Fig. 3.

Chloroplast genome map of Cytinus hypocistis showing annotated genes. The grey circle indicates the GC content and the line marks the 50 % threshold. Ψ indicates pseudogenes and * indicates genes that might be pseudogenes.

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References

    1. Achaz G, Boyer F, Rocha EPC, Viari A, Coissac E. 2007. Repseek, a tool to retrieve approximate repeats from large DNA sequences. Bioinformatics 23: 119–121. - PubMed
    1. Barbrook AC, Howe CJ, Purton S. 2006. Why are plastid genomes retained in non-photosynthetic organisms? Trends in Plant Science 11: 101–108. - PubMed
    1. Barkman TJ, McNeal JR, Lim S-H, et al. 2007. Mitochondrial DNA suggests at least 11 origins of parasitism in angiosperms and reveals genomic chimerism in parasitic plants. BMC Evolutionary Biology 7: 248. - PMC - PubMed
    1. Barrett CF, Davis JI. 2012. The plastid genome of the mycoheterotrophic Corallorhiza striata (Orchidaceae) is in the relatively early stages of degradation. American Journal of Botany 99: 1513–1523. - PubMed
    1. Barrett CF, Freudenstein JV, Li J, et al. 2014. Investigating the path of plastid genome degradation in an early-transitional clade of heterotrophic orchids, and implications for heterotrophic angiosperms. Molecular Biology and Evolution 31: 3095–3112. - PubMed

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