Phylogeny and evolution of Asparagaceae subfamily Nolinoideae: new insights from plastid phylogenomics

Abstract

Background and aims Asparagaceae subfamily Nolinoideae is an economically important plant group, however, the deep relationships and evolutionary history of the lineage remains poorly understood. Based on a large data set including 37 newly sequenced samples and publicly available plastomes, this study aims to better resolve the inter-tribal relationships of Nolinoideae, and to rigorously examine the tribe level monophyly of Convallarieae, Ophiopogoneae, and Polygonateae. Methods Maximum likelihood (ML) and Bayesian inference (BI) methods were employed to infer phylogenetic relationships of Nolinoideae at the genus level and above. The diversification history of Nolinoideae was explored using molecular dating. Key results Both ML and BI analyses identically recovered five clades within Nolinoideae, respectively corresponding to Dracaeneae + Rusceae, Polygonateae + Theropogon, Ophiopogoneae, Nolineae, and Convallarieae excluding Theropogon, and most deep nodes were well supported. As Theropogon was embedded in Polygonateae, the plastome phylogeny failed to resolve Convallarieae and Polygonateae as reciprocally monophyletic. Divergence time estimation showed that the origins of most Nolinoideae genera were dated to the Miocene and Pliocene. The youthfulness of Nolinoideae genera is well-represented in the three herbaceous tribes (Convallarieae, Ophiopogoneae, and Polygonateae) chiefly distributed in the temperate areas of the Northern Hemisphere, as the median stem ages of all the 14 genera currently belonging to them were estimated less than 12.37 Ma. Conclusions This study recovered a robust backbone phylogeny, providing new insights for better understanding the evolution and classification of Nolinoideae. Compared with the deep relationships recovered by a previous study based on transcriptomic data, our data suggest that ancient hybridization or incomplete lineage sorting may have occurred in the early diversification of Nolinoideae. Our findings will provide important reference for further study of the evolutionary complexity of Nolinoideae using nuclear genomic data. The recent origin of these herbaceous genera currently belonging to Convallarieae, Ophiopogoneae, and Polygonateae provides new evidence to support the hypothesis that the global expansion of temperate habitats caused by the climate cooling over the past 15 Ma may have dramatically driven lineage diversification and speciation in the Northern Hemisphere temperate flora.

Comprehensive Comparative Analyses of Aspidistra Chloroplast Genomes: Insights into Interspecific Plastid Diversity and Phylogeny

“…The monophyly of Aspidistra was well supported with 100% BS (Figure 6). In our results, the sister genus of Aspidistra was Tupistra, a finding similar to those of previous studies based on the plastid genome (containing four Aspidistra species) [29] and transcriptome data (with one Aspidistra species) [47]. Within the Aspidistra, the first branching clade was A. erecta, representing a group with distinguishable vegetative morphology (erect stem) [10,48].…”

“…The remaining Nolinoideae species are divided into two clades: one (BS = 100%) containing the tribe Convallarieae; and the other (BS = 100%) encompassing the tribes Ophiopogoneae, Nolineae, and Polygonateae. The phylogenetic relationships among these six tribes were consistent with the Nolinoideae phylogeny from plastid phylogenomics [29]. The monophyly of Aspidistra was well supported with 100% BS (Figure 6).…”

“…The complete chloroplast genome has been frequently employed in resolving the phylogenetic relationships of plants across various classification levels [3,29,[43][44][45][46]. This study used 40 Asparagaceae species (including 36 species for the subfamily Nolinoideae; see Section 4.4) to construct the ML tree based on plastid genomes.…”

“…With the development of high-throughput sequencing technologies, plastid genomes (plastomes) and genome-wide nuclear sequence data of numerous plant species have been sequenced and applied in phylogenetic studies. As for the Asparagaceae, cp genomes of over 200 species have been reported (data from CGIR (Chloroplast Genome Information Resource)) [26][27][28][29]. Although four plastomes of Aspidistra species are available (accessed on 1 August 2023) in the National Center for Biotechnology Information (NCBI), there is still a lack of information regarding the plastid phylogenomics of the genus.…”

Historical biogeography and evolutionary diversification of Lilium (Liliaceae): New insights from plastome phylogenomics

“…Theoretically, phylogenetic reconstruction based on the uniparentally inherited plastome DNA sequences recovers only the maternal (or in some cases the paternal) relationships of a certain plant lineage, compared with the relatively integrated evolutionary schemes recovered by analysis of the biparentally inherited nuclear genome-scale data. Even so, with the widespread application of plastomes in phylogenetic studies, numerous historically difficult issues in plant phylogenetics have been satisfactorily addressed ( Jansen et al., 2007 ; Moore et al., 2007 , 2010 ; Parks et al., 2009 ; Huang et al., 2016 ; Carlsen et al., 2018 ; Li et al., 2019 ; Yang et al., 2019 ; Ji et al., 2021 , 2023 ), indicating that plastomes are as important as nuclear genome data sets and will continue to play an indispensable role in plant phylogenetics.…”