Plastome Reduction in the Only Parasitic Gymnosperm Parasitaxus Is Due to Losses of Photosynthesis but Not Housekeeping Genes and Apparently Involves the Secondary Gain of a Large Inverted Repeat

Abstract

Plastid genomes (plastomes) of parasitic plants undergo dramatic reductions as the need for photosynthesis relaxes. Here, we report the plastome of the only known heterotrophic gymnosperm Parasitaxus usta (Podocarpaceae). With 68 unique genes, of which 33 encode proteins, 31 tRNAs, and four rRNAs in a plastome of 85.3-kb length, Parasitaxus has both the smallest and the functionally least capable plastid genome of gymnosperms. Although the heterotroph retains chlorophyll, all genes for photosynthesis are physically or functionally lost, making photosynthetic energy gain impossible. The pseudogenization of the three plastome-encoded light-independent chlorophyll biosynthesis genes chlB, chlL, and chlN implies that Parasitaxus relies on either only the light-dependent chlorophyll biosynthesis pathway or another regulation system. Nesting within a group of gymnosperms known for the absence of the large inverted repeat regions (IRs), another unusual feature of the Parasitaxus plastome is the existence of a 9,256-bp long IR. Its short length and a gene composition that completely differs from those of IR-containing gymnosperms together suggest a regain of this critical, plastome structure-stabilizing feature. In sum, our findings highlight the particular path of lifestyle-associated reductive plastome evolution, where structural features might provide additional cues of a continued selection for plastome maintenance.

Keywords: Parasitaxus; gene loss; mycoheterotrophy; parasitism; plastome.

Fig. 1.

—Plastome structure of Parasitaxus in comparison with its autotrophic relatives. (A) Linear plastome maps with coverage assessment for the newly sequenced Parasitaxus and Manoao, drawn to scale. The heterotroph is shown without its IR, which allowed estimating coverage (see supplementary fig. S1, Supplementary Material online, for a full map). One copy of the IRs is highlighted by a red bar. Full-color boxes with labeled gene names highlight coding sequences by gene class, as summarized to the right. Gray text and gene boxes in Parasitaxus indicate pseudogenes (Ψ). Read depth is scaled by species with the maximum coverage value indicated at the y axis. (B) The distribution of five selection (ω-) regimes within Podocarpaceae is highlighted in the phylogenetic tree, which was inferred by ML from 33 commonly present protein-coding genes. Each branch color represents a distinguished ω-class, as indicated at the bottom. Whole-plastome alignments show distinct LCBs as large colored blocks in the upper chromosome drawing per species. Changes in strandedness of LCBs are implied by their illustrations below or above the chromosome bars, and horizontal lines between different species indicate changes of synteny. Sequence conservation within LCBs is indicated by the heights of small bars. The bottom plots per species illustrate the gene distribution in the plastome, where white boxes correspond to protein genes, red to rRNA, and green to tRNA. All plastomes are drawn to scale.

Fig. 2.

—Plastid coding capacities of Parasitaxus and other heterotrophic land plants. The presence and absence of plastid genes across all currently studied plastomes of heterotrophic plants compiled by Wicke and Naumann (2018) and all data published since (full list of included data: supplementary table S4, Supplementary Material online) is depicted for all plastid gene classes. Not included here are the chl genes, which have been lost ancestrally in angiosperms, unrelated to heterotrophy (Wicke et al. 2011). Parasitaxus is highlighted in blue. Offwhite and light gray indicate the presence of specific genes as intact or pseudogene, whereas the absence of a gene from a plastome is marked in dark gray. Heterotrophic plant species are sorted by decreasing plastome size (from top to bottom).