Plastome Evolution in Saxifragaceae and Multiple Plastid Capture Events Involving Heuchera and Tiarella.

Lu-Xian Liu,Douglas E Soltis,Fu-De Shang,Pan Li,Shen-Yi Wang,Ying-Xue Du,Ryan A Folk

doi:10.3389/fpls.2020.00361

Abstract

Saxifragaceae, a family of over 600 species and approximately 30 genera of herbaceous perennials, is well-known for intergeneric hybridization. Of the main lineages in this family, the Heuchera group represents a valuable model for the analysis of plastid capture and its impact on phylogeny reconstruction. In this study, we investigated plastome evolution across the family, reconstructed the phylogeny of the Heuchera group and examined putative plastid capture between Heuchera and Tiarella. Seven species (11 individuals) representing Tiarella, as well as Mitella and Heuchera, were selected for genome skimming. We assembled the plastomes, and then compared these to six others published for Saxifragaceae; the plastomes were found to be highly similar in overall size, structure, gene order and content. Moreover, ycf15 was lost due to pseudogenization and rpl2 lost its only intron for all the analyzed plastomes. Comparative plastome analysis revealed that size variations of the plastomes are purely ascribed to the length differences of LSC, SSC, and IRs regions. Using nuclear ITS + ETS and the complete plastome, we fully resolved the species relationships of Tiarella, finding that the genus is monophyletic and the Asian species is most closely related to the western North American species. However, the position of the Heuchera species was highly incongruent between nuclear and plastid data. Comparisons of nuclear and plastid phylogenies revealed that multiple plastid capture events have occurred between Heuchera and Tiarella, through putative ancient hybridization. Moreover, we developed numerous molecular markers for Tiarella (e.g., plastid hotspot and polymorphic nuclear SSRs), which will be useful for future studies on the population genetics and phylogeography of this disjunct genus.

Highlights

In the past, studies have relied heavily on organellar markers for inferring phylogenetic relationships
After filtering by quality with average Phred score < 30, the average length of remaining paired-end reads ranged from 100.43 bp (T. polyphylla-NPKB) to 135.53 bp (H. villosa), and
Incomplete lineage sorting may likewise be excluded for the following reasons: (1) the plastid DNA in the Heuchera group is haploid and maternally inherited (Soltis et al, 1990), and the effective population size of plastid loci is generally one-quarter of that of nuclear loci (Birky et al, 1983), which means stochastic lineage sorting of an organelle locus is four times faster than that of a nuclear locus (Moore, 1995); and (2) previous application of a coalescent method on the Heuchera group demonstrated that incomplete lineage sorting alone does not adequately explain the plastid phylogeny of this group (Folk et al, 2017)

Summary

Introduction

Studies have relied heavily on organellar markers for inferring phylogenetic relationships. Chloroplast and mitochondrial genes often show markedly different phylogenetic patterns from nuclear markers (Rieseberg and Soltis, 1991; Toews and Brelsford, 2012). Various factors, including convergent evolution, lineage sorting, hybridization and Plastid Genome Evolution in Saxifragaceae introgression, may cause phylogenetic incongruence between nuclear and plastid DNA (e.g., Soltis and Kuzoff, 1995; McKinnon et al, 2001; Acosta and Premoli, 2010). One extreme result of hybridization is plastid capture, in which the cytoplasm of one species is replaced by that of another species through inter-species hybridization and subsequent backcrossing, yielding a plant with a novel combination of nuclear and plastid genomes (Rieseberg and Soltis, 1991). Plastid capture has been reported across numerous plant lineages (Okuyama et al, 2005; Fehrer et al, 2007; Acosta and Premoli, 2010; Gurushidze et al, 2010; Mir et al, 2010)

Methods

Discussion

Conclusion