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.
Highlights
The plastid chromosome encodes essential genes for major photosynthesis related functions and is mostly considered highly conserved with respect to gene order and gene content [1] as well as its organization as quadripartite structure consisting of two single copy regions separated by two copies of an inverted repeat [2,3]
Genes involved in photosynthesis show signatures of relaxed functional constraints and eventually become pseudogenized and lost, often starting with ndh genes [16,18]
Following the initial losses is a relaxation of purifying selection in genes related to photosynthesis and genes involved in the translation and transcription machinery
Summary
The plastid chromosome encodes essential genes for major photosynthesis related functions and is mostly considered highly conserved with respect to gene order and gene content [1] as well as its organization as quadripartite structure consisting of two single copy regions separated by two copies of an inverted repeat [2,3]. The plastomes of parasitic plants are a prime subject to study the possibilities and changes of otherwise highly conserved genomic structures that can occur when organellar genomes are released from selective constraints [4,5]. Plants 2020, 9, 306 mutational rates has been reported within individual lineages and the speed and extent of degradation seem lineage-specific [3] Despite those lineage-specific differences, an underlying pattern can be found that plants follow as they transition from autotrophic to heterotrophic lifestyle. It is apparent that often gene order and plastome structure such as the quadripartite nature (large single copy region LSC, small single copy region SSC and inverted repeats IR) are retained in different parasitic plastomes
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