The First Plastid Genome of the Holoparasitic Genus Prosopanche (Hydnoraceae)

Abstract

Plastomes of parasitic and mycoheterotrophic plants show different degrees of reduction depending on the plants’ level of heterotrophy and host dependence in comparison to photoautotrophic sister species, and the amount of time since heterotrophic dependence was established. In all but the most recent heterotrophic lineages, this reduction involves substantial decrease in genome size and gene content and sometimes alterations of genome structure. Here, we present the first plastid genome of the holoparasitic genus Prosopanche, which shows clear signs of functionality. The plastome of Prosopanche americana has a length of 28,191 bp and contains only 24 unique genes, i.e., 14 ribosomal protein genes, four ribosomal RNA genes, five genes coding for tRNAs and three genes with other or unknown function (accD, ycf1, ycf2). The inverted repeat has been lost. Despite the split of Prosopanche and Hydnora about 54 MYA ago, the level of genome reduction is strikingly congruent between the two holoparasites although highly dissimilar nucleotide sequences are observed. Our results lead to two possible evolutionary scenarios that will be tested in the future with a larger sampling: 1) a Hydnoraceae plastome, similar to those of Hydnora and Prosopanche today, existed already in the most recent common ancestor and has not changed much with respect to gene content and structure, or 2) the genome similarities we observe today are the result of two independent evolutionary trajectories leading to almost the same endpoint. The first hypothesis would be most parsimonious whereas the second would point to taxon dependent essential gene sets for plants released from photosynthetic constraints.

Genome-wide macroevolutionary signatures of key innovations in butterflies colonizing new host plants

“…We obtained four chloroplast genes (matK, rbcl, trnL and trnL-trnF) and one nuclear marker (ITS) for 247 species of perianth-bearing Piperales (~49% of the total species diversity 130 ) and six outgroups from perianth-less Piperales. We could not include the two genera Hydnora and Prosopanche (Hydnoraceae) because available genetic data do not overlap those of perianth-bearing Piperales 126,128,131,132 . We applied the same analytical procedure that we did for Papilionidae.…”

Understanding the Ethnobotany, Chemistry, Pharmacology, and Distribution of Genus Hydnora (Aristolochiaceae)

“…However, a recent study grouped the Hydnoraceae family as a sister group to the Winteraceae family ( Drimys granadensis ) because of the long branching problem [ 45 ]. Another study indicated that the Hydnoraceae family formed a monophyletic clade with a low bootstrap support value of 13%, which cannot justify the grouping of Hydnoraceae [ 3 ]. To date, only H. visseri and H. abyssinica complete genomes have been studied in this genus (5, Mkala et al in press).…”

“…They are native and distributed in arid and semi-arid parts of Africa and Asia. This family contains two genera; Hydnora and Prosopanche , named among the oldest parasitic lineages [ 1 , 2 , 3 ]. Prosopanche is naturally found in Central America and South America, whereas Hydnora is indigenous to Africa, Madagascar, and the Arabian Peninsula [ 2 , 3 , 4 ].…”

Plant Organelle DNA Maintenance

“…The plastome of such plant species provides an excellent tool to study the loss of organelle genetic material to the nucleus while they shift from the autotrophic to the heterotrophic mode. Jost et al [8] sequenced the plastome of a holoparasitic plant species, Prosopanche americana, which has only 24 housekeeping genes and has lost the inverted repeats (IR) that are thought to stabilize the genome. The genetic machinery of P. americana shows an incredibly high degree of bias towards "AT"-rich codons, with >90% of the plastome sequence containing "A" and "T" nucleotides.…”