Invited Review Beyond parasitic convergence: unravelling the evolution of the organellar genomes in holoparasites

Abstract

Background: The molecular evolution of organellar genomes in angiosperms has been studied extensively, with some lineages, such as parasitic ones, displaying unique characteristics. Parasitism has emerged 12 times independently in angiosperm evolution. Holoparasitism is the most severe form of parasitism, and is found in ~10 % of parasitic angiosperms. Although a few holoparasitic species have been examined at the molecular level, most reports involve plastomes instead of mitogenomes. Parasitic plants establish vascular connections with their hosts through haustoria to obtain water and nutrients, which facilitates the exchange of genetic information, making them more susceptible to horizontal gene transfer (HGT). HGT is more prevalent in the mitochondria than in the chloroplast or nuclear compartments.

Scope: This review summarizes current knowledge on the plastid and mitochondrial genomes of holoparasitic angiosperms, compares the genomic features across the different lineages, and discusses their convergent evolutionary trajectories and distinctive features. We focused on Balanophoraceae (Santalales), which exhibits extraordinary traits in both their organelles.

Conclusions: Apart from morphological similarities, plastid genomes of holoparasitic plants also display other convergent features, such as rampant gene loss, biased nucleotide composition and accelerated evolutionary rates. In addition, the plastomes of Balanophoraceae have extremely low GC and gene content, and two unexpected changes in the genetic code. Limited data on the mitochondrial genomes of holoparasitic plants preclude thorough comparisons. Nonetheless, no obvious genomic features distinguish them from the mitochondria of free-living angiosperms, except for a higher incidence of HGT. HGT appears to be predominant in holoparasitic angiosperms with a long-lasting endophytic stage. Among the Balanophoraceae, mitochondrial genomes exhibit disparate evolutionary paths with notable levels of heteroplasmy in Rhopalocnemis and unprecedented levels of HGT in Lophophytum. Despite their differences, these Balanophoraceae share a multichromosomal mitogenome, a feature also found in a few free-living angiosperms.

Keywords: Cuscuta; Lophophytum mirabile; Ombrophytum subterraneum; Rhopalocnemis phalloides; Balanophoraceae; Rafflesiaceae; Santalales; horizontal gene transfer; mitochondria; non-photosynthetic plastid.

Fig. 1.

Phylogeny of angiosperms depicting parasitic lineages. Red branches depict lineages including parasitic plants. Families that contain holoparasitic plants are in boldface. The availability of organellar genomic resources of holoparasites is indicated by a schematic plastid or mitochondrion. A pie chart next to the parasitic lineages shows the proportion of hemi- and holoparasitic taxa. The phylogeny follows Angiosperm Phylogeny Group IV (2016) classification and the phylogeny of Santalales is based on Nickrent (2020).

Fig. 2.

Phylogeny and features of Balanophoraceae. Maximum-likelihood phylogenetic tree based on a concatenated alignment of nuclear (rDNA operon) and mitochondrial (matR) sequences. No molecular data are available for Ditepalanthus, Lathrophytum or Chlamydophytum. Thick and thin branches indicate strongly or weakly supported relationships with bootstrap support values above or below 90 %, respectively. Details of the phylogenetic analysis are shown in Supplementary Data Figure S1. The availability of organellar genomic resources of holoparasites is indicated by a schematic plastid (in yellow) or mitochondrion (in orange). The geographical distribution and number of species was taken from https://powo.science.kew.org/.

Fig. 3.

Lophophytum pyramidale. (A) Map of the plastome with the main features shown in the centre. (B) Inflorescences of L. pyramidale growing in the province of Misiones (Argentina). Yellow and whitish flowers are male and female, respectively. (C) Transmission electron micrograph of an ovarian cell. The arrow points to the non-photosynthetic plastid. (D) Light micrograph of a cell from the female flower stained with iodine. Arrowheads depict starch granules.

Fig. 4.

Rhopalocnemis phalloides. (A) Photo of an inflorescence of R. phalloides, courtesy of Runxian Yu. (B) Map of a mitochondrial chromosome of R. phalloides, depicting the conserved region (in orange) shared across chromosomes, which includes a region that can fold into a stem loop and is considered the origin of replication. Genes are shown in blue.

Fig. 5.

Lophophytum mirabile. (A) Inflorescence of L. mirabile growing in Jujuy (Argentina). Only the staminate flowers emerged above the soil level; female flowers are located below them. (B) Diagram of the internal membrane of the mitochondria with the five OXPHOS complexes of L. mirabile depicting the subunits coloured according to their phylogenetic origin and the genome in which the genes are located. Figure modified from Gatica-Soria et al. (2022). (C) Proportion of each of the mitochondrial chromosomes of L. mirabile with similarity (>80 %) to the mitogenomes of mimosoids, the actual host plant Anadenanthera colubrina, or to the close relatives Ombrophytum subterraneum and Rhopalocnemis phalloides.