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

Qu XJ, Fan SJ, Wicke S, Yi TS

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 gymnospermParasitaxus usta(Podocarpaceae). With 68 unique genes, of which 33 encode proteins, 31 tRNAs, and four rRNAs in a plastome of 85.3 kb length,Parasitaxushas both the smallest as well as 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 geneschlB,chlL, andchlNimplies thatParasitaxusrelies 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 theParasitaxusplastome 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 re-gain 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.