Plastid phylogenomics reveals evolutionary relationships in the mycoheterotrophic orchid genus Dipodium and provides insights into plastid gene degeneration

Stephanie Goedderz; Mark A Clements; Stephen J Bent; James A Nicholls; Vidushi S Patel; Darren M Crayn; Philipp M Schlüter; Katharina Nargar

doi:10.3389/fpls.2024.1388537

Plastid phylogenomics reveals evolutionary relationships in the mycoheterotrophic orchid genus Dipodium and provides insights into plastid gene degeneration

Front Plant Sci. 2024 Jun 13:15:1388537. doi: 10.3389/fpls.2024.1388537. eCollection 2024.

Authors

Stephanie Goedderz^{1

2}, Mark A Clements³, Stephen J Bent⁴, James A Nicholls⁵, Vidushi S Patel⁶, Darren M Crayn¹, Philipp M Schlüter², Katharina Nargar^{1

6}

Affiliations

¹ Australian Tropical Herbarium, James Cook University, Cairns, QLD, Australia.
² Department of Plant Evolutionary Biology, Institute of Biology, University of Hohenheim, Stuttgart, Germany.
³ Centre for Australian National Biodiversity Research (joint venture between Parks Australia and CSIRO), Canberra, ACT, Australia.
⁴ Data61, Commonwealth Industrial and Scientific Research Organisation (CSIRO), Brisbane, QLD, Australia.
⁵ Australian National Insect Collection, Commonwealth Industrial and Scientific Research Organisation (CSIRO), Canberra, ACT, Australia.
⁶ National Research Collections Australia, Commonwealth Industrial and Scientific Research Organisation (CSIRO), Canberra, ACT, Australia.

Abstract

The orchid genus Dipodium R.Br. (Epidendroideae) comprises leafy autotrophic and leafless mycoheterotrophic species, with the latter confined to sect. Dipodium. This study examined plastome degeneration in Dipodium in a phylogenomic and temporal context. Whole plastomes were reconstructed and annotated for 24 Dipodium samples representing 14 species and two putatively new species, encompassing over 80% of species diversity in sect. Dipodium. Phylogenomic analysis based on 68 plastid loci including a broad outgroup sampling across Orchidaceae found that sect. Leopardanthus is the sister lineage to sect. Dipodium. Dipodium ensifolium, the only leafy autotrophic species in sect. Dipodium, was found to be a sister to all leafless, mycoheterotrophic species, supporting a single evolutionary origin of mycoheterotrophy in the genus. Divergence-time estimations found that Dipodium arose ca. 33.3 Ma near the lower boundary of the Oligocene and that crown diversification commenced in the late Miocene, ca. 11.3 Ma. Mycoheterotrophy in the genus was estimated to have evolved in the late Miocene, ca. 7.3 Ma, in sect. Dipodium. The comparative assessment of plastome structure and gene degradation in Dipodium revealed that plastid ndh genes were pseudogenised or physically lost in all Dipodium species, including in leafy autotrophic species of both Dipodium sections. Levels of plastid ndh gene degradation were found to vary among species as well as within species, providing evidence of relaxed selection for retention of the NADH dehydrogenase complex within the genus. Dipodium exhibits an early stage of plastid genome degradation, as all species were found to have retained a full set of functional photosynthesis-related genes and housekeeping genes. This study provides important insights into plastid genome degradation along the transition from autotrophy to mycoheterotrophy in a phylogenomic and temporal context.

Keywords: Dipodium; divergence-time estimation; gene degradation; mycoheterotrophy; phylogenetics; plastome.

Grants and funding

The author(s) declare financial support was received for the research, authorship, and/or publication of this article. This study was supported by the Australian Biological Resources Study (Dept. of Agriculture, Water and the Environment, Australian Government NTRGP BBR210–34) and the Australian Orchid Foundation (AOF325.18; AOF357.23). SG received a research grant from the Australian Tropical Herbarium.