Plastome Evolution in Hemiparasitic Mistletoes

Abstract

Santalales is an order of plants consisting almost entirely of parasites. Some, such as Osyris, are facultative root parasites whereas others, such as Viscum, are obligate stem parasitic mistletoes. Here, we report the complete plastome sequences of one species of Osyris and three species of Viscum, and we investigate the evolutionary aspects of structural changes and changes in gene content in relation to parasitism. Compared with typical angiosperms plastomes, the four Santalales plastomes are all reduced in size (10-22% compared with Vitis), and they have experienced rearrangements, mostly but not exclusively in the border areas of the inverted repeats. Additionally, a number of protein-coding genes (matK, infA, ccsA, rpl33, and all 11 ndh genes) as well as two transfer RNA genes (trnG-UCC and trnV-UAC) have been pseudogenized or completely lost. Most of the remaining plastid genes have a significantly changed selection pattern compared with other dicots, and the relaxed selection of photosynthesis genes is noteworthy. Although gene loss obviously reduces plastome size, intergenic regions were also shortened. As plastome modifications are generally most prominent in Viscum, they are most likely correlated with the increased nutritional dependence on the host compared with Osyris.

Keywords: Viscum; gene loss; hemiparasite; intergenic regions; pseudogenes; selection; structural rearrangements.

Fig. 1.—

The three species of Viscum studied. (A) Viscum album with white, ripe fruits. (B) Viscum crassulae growing on Portulacaria afra. (C) Flowering V. minimum emerging from the stem of the succulent Euphorbia mammillaris.

Fig. 2.—

Circular map of the plastome of V. minimum. Genes shown outside the outer circle are transcribed clockwise and those inside are transcribed counterclockwise. Pseudogenes are marked by ψ. Drawing made using OGDRAW v.1.2 (Lohse et al. 2013).

Fig. 3.—

Proportions of palindromic and forward repeat DNA in plastomes of Vitis and four species of Santalales. Numbers above columns indicate the repeat density, for example, 1/1,000 means that a repeat occurs every 1,000 bp.

Fig. 4.—

Phylogeny of the Santalales taxa studied here, based on maximum-likelihood analysis of the IR region, showing the progressive degeneration of the ndhB gene. Open bars symbolize minor indels (<15 bp), black bars symbolize major deletions (>50 bp). ψ indicates pseudogenization.