Comparative Plastome Analysis of Root- and Stem-Feeding Parasites of Santalales Untangle the Footprints of Feeding Mode and Lifestyle Transitions

Abstract

In plants, parasitism triggers the reductive evolution of plastid genomes (plastomes). To disentangle the molecular evolutionary associations between feeding on other plants below- or aboveground and general transitions from facultative to obligate parasitism, we analyzed 34 complete plastomes of autotrophic, root- and stem-feeding hemiparasitic, and holoparasitic Santalales. We observed inexplicable losses of housekeeping genes and tRNAs in hemiparasites and dramatic genomic reconfiguration in holoparasitic Balanophoraceae, whose plastomes have exceptionally low GC contents. Genomic changes are related primarily to the evolution of hemi- or holoparasitism, whereas the transition from a root- to a stem-feeding mode plays no major role. In contrast, the rate of molecular evolution accelerates in a stepwise manner from autotrophs to root- and then stem-feeding parasites. Already the ancestral transition to root-parasitism coincides with a relaxation of selection in plastomes. Another significant selectional shift in plastid genes occurs as stem-feeders evolve, suggesting that this derived form coincides with trophic specialization despite the retention of photosynthetic capacity. Parasitic Santalales fill a gap in our understanding of parasitism-associated plastome degeneration. We reveal that lifestyle-genome associations unfold interdependently over trophic specialization and feeding mode transitions, where holoparasitic Balanophoraceae provide a system for exploring the functional realms of plastomes.

Genomic comparison of non-photosynthetic plants from the family Balanophoraceae with their photosynthetic relatives

“…It was previously shown that plastid genomes of Balanophoraceae are very AT-rich, with AT contents of currently sequenced genomes being in the range of 86.8%-88.4% (Su et al, 2019; Schelkunov, Nuraliev & Logacheva, 2019; Chen et al, 2020a). This makes them the most AT-rich of any plant genomes, and one of the most AT-rich among all genomes.…”

“…Information about the plastid gene content in Rhopalocnemis phalloides and Balanophora fungosa was obtained from the papers that described their plastid genomes (Schelkunov, Nuraliev & Logacheva, 2019; Chen et al, 2020a). The plastid genome sequences of Daenikera sp.…”

“…and Dendropemon caribaeus are still unknown. However, given the similar gene content in the plastid genome of photosynthetic Santalales (Chen et al, 2020a), it is reasonable to assume that the plastid gene content in Daenikera sp. and Dendropemon caribaeus is approximately the same.…”

“…One of them states that the genome length is 158,163 bp, while the other tells about a 125,050 bp-long genome. Given that the gene content in the second genome highly differs from gene contents in other photosynthetic Santalales (Chen et al, 2020a), we suppose that the second genome either contains assembly mistakes or belongs to some other species, misidentified as Malania oleifera . Therefore, as the true plastid genome of Malania oleifera we consider the longer one.…”

“…Among the most unusual plastid genomes currently known to scientists are plastid genomes of non-photosynthetic plants from the family Balanophoraceae (Su et al, 2019; Schelkunov, Nuraliev & Logacheva, 2019; Chen et al, 2020a). The family Balanophoraceae comprises several dozen species that inhabit tropical and subtropical areas and feed by attaching to roots of different plants and sucking nutrients from them.…”