Understanding plastome evolution in Hemiparasitic Santalales: Complete chloroplast genomes of three species, Dendrotrophe varians, Helixanthera parasitica, and Macrosolen cochinchinensis

Abstract

Santalales is a large order, with over 2200 species, most of which are root or aerial (stem) hemiparasites. In this study, we report the newly assembled chloroplast genome of Dendrotrophe varians (140,666 bp) in the family Amphorogynaceae and the cp genomes of Helixanthera parasitica (124,881 bp) and Macrosolen cochinchinensis (122,986 bp), both in the family Loranthaceae. We compared the cp genomes of 11 Santalales including eight currently available cp genomes. Santalales cp genomes are slightly or not reduced in size (119-147 kb), similar to other hemiparasitic species, when compared with typical angiosperm cp genomes (120-170 kb). In a phylogeny examining gene content, the NADH dehydrogenase gene group is the only one among eight functional gene groups that lost complete functionally in all examined Santalales. This supports the idea that the functional loss of ndh genes is the initial stage in the evolution of the plastome of parasitic plants, but the loss has occurred independently multiple times in angiosperms, while they are not found in some parasites. This suggests that the functional loss of ndh genes is not essential for the transition from autotroph to parasite. We additionally examined the correlation between gene content and type of parasitism (obligate/facultative and stem/root parasites) of all hemiparasitic species in which cp genomes have been reported to date. Correlation was not found in any types of parasitism.

Fig 1. Maximum likelihood tree resulting from the 58 concatenated protein-coding genes common to 14 representative taxa.

The BI tree had identical topology with the ML tree. The GTR+I+G model was selected based on Modeltest. The bootstrap support values of the ML tree and the posterior probabilities of the BI tree at all nodes are 100% and 1.00, respectively, except for one node marked by an asterisk, which has a value of 99% and probability of 1.00. ψ, pseudogene; †, partial gene sequence.

Fig 2. Comparison of the SSC-IR and LSC-IR boundary regions across 11 Santalales species.

Fig 3. Comparison of the cp genome gene content of 16 hemiparasitic plants published to date with one autotrophic plant and two Cuscuta species, based on Funk, H. T., et al. (2007), McNeal, J. R., et al. (2007), Wicke, S., et al. (2013), Petersen, G., et al. (2015), Rossetto, M., et al. (2015), Fan, W., et al. (2016), Su, H. -J. and J. -M. Hu (2016), Wicke, S., et al. (2016), Li, Y., et al. (2017) and Yang, G. -S., et al. (2017).

In the case of Striga hemonthica, pseudogene presence was not confirmed in a previous paper. Black/gray/white boxes indicate each gene present and are considered functional/pseudogene or fragment of gene present/gene absent. AU, autotroph; HE, hemiparasite; HO, holoparasite; O, obligate parasite; F, facultative parasite; S, stem parasite; R, root parasite.