Mycoheterotrophic Epirixanthes (Polygalaceae) has a typical angiosperm mitogenome but unorthodox plastid genomes.

G Petersen,O Seberg,H Æ Pedersen,V K Y Lam,S W Graham,A Zervas,V S F T Merckx,H Darby

doi:10.1093/aob/mcz114

Abstract

Background and AimsFully mycoheterotrophic plants derive carbon and other nutrients from root-associated fungi and have lost the ability to photosynthesize. While mycoheterotroph plastomes are often degraded compared with green plants, the effect of this unusual symbiosis on mitochondrial genome evolution is unknown. By providing the first complete organelle genome data from Polygalaceae, one of only three eudicot families that developed mycoheterotrophy, we explore how both organellar genomes evolved after loss of photosynthesis.MethodsWe sequenced and assembled four complete plastid genomes and a mitochondrial genome from species of Polygalaceae, focusing on non-photosynthetic Epirixanthes. We compared these genomes with those of other mycoheterotroph and parasitic plant lineages, and assessed whether organelle genes in Epirixanthes experienced relaxed or intensified selection compared with autotrophic relatives.Key ResultsPlastomes of two species of Epirixanthes have become substantially degraded compared with that of autotrophic Polygala. Although the lack of photosynthesis is presumably homologous in the genus, the surveyed Epirixanthes species have marked differences in terms of plastome size, structural rearrangements, gene content and substitution rates. Remarkably, both apparently replaced a canonical plastid inverted repeat with large directly repeated sequences. The mitogenome of E. elongata incorporated a considerable number of fossilized plastid genes, by intracellular transfer from an ancestor with a less degraded plastome. Both plastid and mitochondrial genes in E. elongata have increased substitution rates, but the plastid genes of E. pallida do not. Despite this, both species have similar selection patterns operating on plastid housekeeping genes.ConclusionsPlastome evolution largely fits with patterns of gene degradation seen in other heterotrophic plants, but includes highly unusual directly duplicated regions. The causes of rate elevation in the sequenced Epirixanthes mitogenome and of rate differences in plastomes of related mycoheterotrophic species are not currently understood.

Highlights

Mycoheterotrophic plants are specialized to take up carbohydrates from root-associated mycorrhizal or saprophytic fungi, thereby reducing their dependency on photosynthesis for carbon fixation
A third relocation and inversion implied by the Mauve alignment (Fig. 3) is an artefact caused by the removal of the inverted repeats (IRs)-A region prior to aligning the genomes and the differences between the borders of the small single copy (SSC) region and the IR of P. arillata and Cercis
The differences in plastome degradation between E. pallida and E. elongata evolved after their divergence from their achlorophyllous most recent common ancestor, and this illustrates that different evolutionary trajectories after a common loss of photosynthesis may lead to pronounced differences in plastome reduction, similar to other clades with multiple heterotrophic taxa (e.g. Corsiaceae, Mennes et al, 2015a; Orobanchaceae, Wicke et al, 2013)

Summary

Introduction

Mycoheterotrophic plants are specialized to take up carbohydrates from root-associated mycorrhizal or saprophytic fungi, thereby reducing their dependency on photosynthesis for carbon fixation. Mycoheterotrophy has evolved repeatedly in angiosperms and, while some lineages exhibit only initial stages of heterotrophy, others are fully heterotrophic and photosynthesis has been lost completely (Graham et al, 2017). A reduced dependency on photosynthesis is shared between mycoheterotrophic plants and parasitic plants, and a number of studies have described the consequential degradation of the plastid genome (plastome) in both cases (reviewed in Krause, 2011; Wicke et al, 2011; Graham et al, 2017; Wicke and Naumann, 2018). A more inclusive model accounting for several aspects of plastome changes, including structural changes and substitution by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited

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