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.

Xiao-Jian Qu,Shou-Jin Fan,Susann Wicke,Ting-Shuang Yi,Daniel Sloan

doi:10.1093/gbe/evz187

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.

Highlights

The plastid’s principal function in photosynthesis is reflected in its semiautonomous genome that encodes many components for the photosynthetic machinery (Palmer 1985; Wicke et al 2011)
The pseudogenization of the three plastomeencoded 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 9,256bp long IR

Summary

Introduction

The plastid’s principal function in photosynthesis is reflected in its semiautonomous genome (plastome) that encodes many components for the photosynthetic machinery (Palmer 1985; Wicke et al 2011). The presence of fungal hyphae at the parasite–host junction, the direct plant–plant connection, and carbon isotope ratios indicative of additional nutrient uptake from a fungus suggest that Parasitaxus “presents a unique physiological chimera” of haustorial parasites and mycoheterotrophic plants We sequenced, assembled, and annotated the complete plastomes of Parasitaxus usta and its photosynthetic relative Manoao colensoi. It was the aim of our study to infer whether the heterotrophic mode of Parasitaxus follows the predicted course of heterotrophy-associated plastome reduction that is characteristic of nonphotosynthetic land plants. We focused our analyses on changes of the plastid coding capacity of Parasitaxus and found that its degree of physical and functional reduction, as well as its structural evolution, is exceptionally different from those of other heterotrophs

Materials and Methods

Results and Discussion

Literature Cited