The rapid radiation of Bomarea (Alstroemeriaceae: Liliales), driven by the rise of the Andes.

Geological events such as mountain uplift affect how, when, and where species diversify, but measuring those effects is a longstanding challenge. Andean orogeny impacted the evolution of regional biota by creating barriers to gene flow, opening new habitats, and changing local climate. B⁢o⁢m⁢a⁢r⁢e⁢a (Alstroemeriaceae) are tropical plants with (often) small, isolated ranges; in total, B⁢o⁢m⁢a⁢r⁢e⁢a species occur from central Mexico to central Chile. This genus appears to have evolved rapidly and quite recently, and rapid radiations are often challenging to resolve with traditional phylogenetic inference. In this study, we apply phylogenomics-with hundreds of loci, gene-tree-based data curation, and a multispecies-coalescent approach-to infer the phylogeny of B⁢o⁢m⁢a⁢r⁢e⁢a. We use this phylogeny to untangle the potential drivers of diversification and biogeographic history. In particular, we test if Andean orogeny contributed to the diversification of B⁢o⁢m⁢a⁢r⁢e⁢a. We find that B⁢o⁢m⁢a⁢r⁢e⁢a originated in the central Andes during the mid-Miocene, then spread north, following the trajectory of mountain uplift. Furthermore, Andean lineages diversified faster than non-Andean relatives. B⁢o⁢m⁢a⁢r⁢e⁢a thus demonstrates that-at least in some cases-geological change rather than environmental stability has driven high species diversity in a tropical biodiversity hotspot. These results also demonstrate the utility (and danger) of genome-scale data for making macroevolutionary inferences.

The complete chloroplast genome of a shrub species, Smilax glabra (Smilacaceae) from Guangdong, China.

Smilax glabra is a perennial woody scandent shrub, of which the dried aerial tuber has been used as Chinese medicine. Here, we sequenced S. glabra and assembled its complete chloroplast (cp) genome. The genome is 157,889 bp in length and has a typical quadripartite structure. We annotated 131 genes, of which 84 were protein-coding genes, 37 were tRNAs and 8 were rRNA genes. Phylogenetic analysis of this genome with 26 representatives Liliales fully resolved S. glabra in a clade with S. china. The phylogenetic tree we constructed is largely consistent with recently published phylogenetic trees using both complete chloroplast genomes and marker gene sequences.

Phylogeny, Age, and Evolution of Tribe Lilieae (Liliaceae) Based on Whole Plastid Genomes.

Tribe Lilieae, encompassing Lilium, Notholirion, Cardiocrinum, and Fritillaria, includes economically important crops with a horticultural and medicinal value. It is considered to be a core lineage of Liliaceae, but phylogenetic relationships within it, and the timing of the origin of individual clades, remain incompletely resolved. To address these issues, we reconstructed the evolutionary history of the tribe. We sequenced 45 Liliaceae plastomes and combined them with publicly available data (for a total of 139 plastomes) to explore the systematics, origin, divergence, and evolution of Lilieae. Our taxon sampling covers all ten sections of Lilium, all Cardiocrinum species, three Notholirion species, and major phylogenetic clades of Fritillaria. Our phylogenetic analysis confirms the monophyly of major sections/subgenera of Lilium and Fritillaria with strong support. We dated the origin of Lilieae to the Eocene, with genera and species radiations inferred to have occurred in the Miocene. The reconstruction of the ancestral area implies that Lilieae may have originated from the Qinghai-Tibet Plateau (QTP): the Himalayas and Hengduan Mountains and uplifting of the QTP likely promoted divergence within the tribe. Ancestral-state reconstructions of the bulb component number (including bulblets and scales) show a strong correlation with the genus-level phylogenetic diversity in Lilieae. They also predict that the most recent common ancestor of Lilieae had bulbs with numerous bulblets. Based on these observations, we predicted that climatic oscillations associated with the QTP uplift played an important role in the evolution of the Lilieae bulb. Our findings provide a well-supported picture of evolutionary relationships and a useful framework for understanding the pathway of bulb evolution within Lilieae, contributing to a better understanding of the evolutionary history of lilies.

Implications of plastome evolution in the true lilies (monocot order Liliales).

The families of the monocot order Liliales exhibit highly contrasting characteristic of photosynthetic and mycoheterotrophic life histories. Although previous phylogenetic and morphological studies of Liliales have been conducted, they have not examined molecular evolution associated with this contrasting phenomenon. Here, we conduct the first comparative plastome study of all ten families of Liliales using 29 newly sequenced plastid genomes analyzed together with previously published data. We also present a phylogenetic analysis for Liliales of 78 plastid genes combined with 22 genes from all three genomes (nuclear 18S rDNA and phyC; 17 plastid genes; and mitochondrial matR, atpA, and cob). Within the newly generated phylogenetic tree of Liliales, we evaluate the ancestral state changes of selected morphological traits in the order. There are no significant differences in plastid genome features among species that show divergent characteristics correlated with family circumscriptions. However, the results clearly differentiate between photosynthetic and mycoheterotrophic taxa of Liliales in terms of genome structure, and gene content and order. The newly sequenced plastid genomes and combined three-genome data revealed Smilacaceae as sister to Liliaceae instead of Philesiaceae and Ripogonaceae. Additionally, we propose a revised familial classification system of Liliales that consists of nine families, considering Ripogonaceae a synonym of Philesiaceae. The ancestral state reconstruction indicated synapomorphies for each family of Liliales, except Liliaceae, Melanthiaceae and Colchicaceae. A taxonomic key for all nine families of Liliales is also provided.

A Dynamic Tandem Repeat in Monocotyledons Inferred from a Comparative Analysis of Chloroplast Genomes in Melanthiaceae.

Chloroplast genomes (cpDNA) are highly valuable resources for evolutionary studies of angiosperms, since they are highly conserved, are small in size, and play critical roles in plants. Slipped-strand mispairing (SSM) was assumed to be a mechanism for generating repeat units in cpDNA. However, research on the employment of different small repeated sequences through SSM events, which may induce the accumulation of distinct types of repeats within the same region in cpDNA, has not been documented. Here, we sequenced two chloroplast genomes from the endemic species Heloniopsis tubiflora (Korea) and Xerophyllum tenax (USA) to cover the gap between molecular data and explore "hot spots" for genomic events in Melanthiaceae. Comparative analysis of 23 complete cpDNA sequences revealed that there were different stages of deletion in the rps16 region across the Melanthiaceae. Based on the partial or complete loss of rps16 gene in cpDNA, we have firstly reported potential molecular markers for recognizing two sections (Veratrum and Fuscoveratrum) of Veratrum. Melathiaceae exhibits a significant change in the junction between large single copy and inverted repeat regions, ranging from trnH_GUG to a part of rps3. Our results show an accumulation of tandem repeats in the rpl23-ycf2 regions of cpDNAs. Small conserved sequences exist and flank tandem repeats in further observation of this region across most of the examined taxa of Liliales. Therefore, we propose three scenarios in which different small repeated sequences were used during SSM events to generate newly distinct types of repeats. Occasionally, prior to the SSM process, point mutation event and double strand break repair occurred and induced the formation of initial repeat units which are indispensable in the SSM process. SSM may have likely occurred more frequently for short repeats than for long repeat sequences in tribe Parideae (Melanthiaceae, Liliales). Collectively, these findings add new evidence of dynamic results from SSM in chloroplast genomes which can be useful for further evolutionary studies in angiosperms. Additionally, genomics events in cpDNA are potential resources for mining molecular markers in Liliales.

A few-gene plastid phylogenetic framework for mycoheterotrophic monocots.

PREMISE OF THE STUDY: Few-gene studies with broad taxon sampling have provided major insights into phylogeny and underpin plant classification. However, they have typically excluded heterotrophic plants because of loss, pseudogenization, or rapid evolution of plastid genes. Here we performed a phylogenetic survey of three commonly retained plastid genes to assess their utility in placing mycoheterotrophs. METHODS: We surveyed accD, clpP, and matK for 34 taxa from seven monocot families that include full mycoheterotrophs and a broad sampling of photosynthetic taxa. After screening for weak contaminants, we conducted phylogenetic analyses and characterized among-lineage rate variation. KEY RESULTS: Likelihood analyses strongly supported local placements of fully mycoheterotrophic taxa for Corsiaceae, Iridaceae, Orchidaceae, and Petrosaviaceae, in positions consistent with other studies. Depression of likelihood bootstrap support values near mycoheterotrophic clades was alleviated when each mycoheterotrophic family was considered separately. Triuridaceae (Sciaphila) monophyly was recovered in a partitioned likelihood analysis, and the family then placed as sister to Cyclanthaceae-Pandanaceae. Burmanniaceae placed in Dioscoreales with weak to strong support depending on analysis details, and we inferred a plastid-based phylogeny for the family. Thismiaceae species may retain a plastid genome, based on accD retention. The inferred position of Thismiaceae is unstable, but was close to Taccaceae (Dioscoreales) in some analyses. CONCLUSIONS: Long branches/elevated substitution rates, missing genes, and occasional contaminants are challenges for plastid-based phylogenetic inference with full mycoheterotrophs. However, most mycoheterotrophs can be readily integrated into the broad picture of plant phylogeny using several plastid genes and broad taxonomic sampling.

A trnI_CAU triplication event in the complete chloroplast genome of Paris verticillata M.Bieb. (Melanthiaceae, Liliales).

The chloroplast is an essential plant organelle responsible for photosynthesis. Gene duplication, relocation, and loss in the chloroplast genome (cpDNA) are useful for exploring the evolution and phylogeny of plant species. In this study, the complete chloroplast genome of Paris verticillata was sequenced using the 454 sequencing system and Sanger sequencing method to trace the evolutionary pattern in the tribe Parideae of the family Melanthiaceae (Liliales). The circular double-stranded cpDNA of P. verticillata (157,379 bp) consists of two inverted repeat regions each of 28,373 bp, a large single copy of 82,726 bp, and a small single copy of 17,907 bp. Gene content and order are generally similar to the previously reported cpDNA sequences within the order Liliales. However, we found that trnI_CAU was triplicated in P. verticillata. In addition, cemA is suspected to be a pseudogene due to the presence of internal stop codons created by poly(A) insertion and single small CA repeats. Such changes were not found in previously examined cpDNAs of the Melanthiaceae or other families of the Liliales, suggesting that such features are unique to the tribe Parideae of Melanthiaceae. The characteristics of P. verticillata cpDNA will provide useful information for uncovering the evolution within Paris and for further research of plastid genome evolution and phylogenetic studies in Liliales.

Leaf fossils of Luzuriaga and a monocot flower with in situ pollen of Liliacidites contortus Mildenh. & Bannister sp. nov. (Alstroemeriaceae) from the Early Miocene.

PREMISE OF THE STUDY: The Foulden Maar lake sediments in Otago, South Island, New Zealand, date to the earliest Miocene and provide an important picture of the diversity of the Australasian biota, paleoecology, and climate at a time when New Zealand had a smaller land area than today. The diverse rainforest contains many taxa now restricted to Australia, New Caledonia, or South America. The presence of Luzuriaga-like fossils in these deposits is important for understanding Alstroemeriaceae evolution and the biogeography of genera shared between New Zealand and South America. METHODS: Leaves and a flower with in situ pollen that resemble extant Luzuriaga are described and placed phylogenetically. Geographic range information and a molecular clock model for the Alstroemeriaceae were used to investigate possible biogeographic scenarios and the influence of the new fossil on inferred divergence times. KEY RESULTS: Luzuriaga peterbannisteri Conran, Bannister, Mildenh., & D.E.Lee sp. nov. represents the first macrofossil record for Alstroemeriaceae. An associated Luzuriaga-like flower with in situ fossil pollen of Liliacidites contortus Mildenh. & Bannister sp. nov. is also described. The biogeographic analysis suggests that there have been several dispersal events across the Southern Ocean for the genus, with the fossil representing a now-extinct New Zealand lineage. CONCLUSIONS: Luzuriaga was present in Early Miocene New Zealand, indicating a long paleogeographic history for the genus, and L. peterbannisteri strengthens biogeographic connections between South America and Australasia during the Oligocene and earliest Miocene.

A universe of dwarfs and giants: genome size and chromosome evolution in the monocot family Melanthiaceae.

• Since the occurrence of giant genomes in angiosperms is restricted to just a few lineages, identifying where shifts towards genome obesity have occurred is essential for understanding the evolutionary mechanisms triggering this process. • Genome sizes were assessed using flow cytometry in 79 species and new chromosome numbers were obtained. Phylogenetically based statistical methods were applied to infer ancestral character reconstructions of chromosome numbers and nuclear DNA contents. • Melanthiaceae are the most diverse family in terms of genome size, with C-values ranging more than 230-fold. Our data confirmed that giant genomes are restricted to tribe Parideae, with most extant species in the family characterized by small genomes. Ancestral genome size reconstruction revealed that the most recent common ancestor (MRCA) for the family had a relatively small genome (1C = 5.37 pg). Chromosome losses and polyploidy are recovered as the main evolutionary mechanisms generating chromosome number change. • Genome evolution in Melanthiaceae has been characterized by a trend towards genome size reduction, with just one episode of dramatic DNA accumulation in Parideae. Such extreme contrasting profiles of genome size evolution illustrate the key role of transposable elements and chromosome rearrangements in driving the evolution of plant genomes.

Comparative genomics of four Liliales families inferred from the complete chloroplast genome sequence of Veratrum patulum O. Loes. (Melanthiaceae).

The sequence of the chloroplast genome, which is inherited maternally, contains useful information for many scientific fields such as plant systematics, biogeography and biotechnology because its characteristics are highly conserved among species. There is an increase in chloroplast genomes of angiosperms that have been sequenced in recent years. In this study, the nucleotide sequence of the chloroplast genome (cpDNA) of Veratrum patulum Loes. (Melanthiaceae, Liliales) was analyzed completely. The circular double-stranded DNA of 153,699 bp consists of two inverted repeat (IR) regions of 26,360 bp each, a large single copy of 83,372 bp, and a small single copy of 17,607 bp. This plastome contains 81 protein-coding genes, 30 distinct tRNA and four genes of rRNA. In addition, there are six hypothetical coding regions (ycf1, ycf2, ycf3, ycf4, ycf15 and ycf68) and two open reading frames (ORF42 and ORF56), which are also found in the chloroplast genomes of the other species. The gene orders and gene contents of the V. patulum plastid genome are similar to that of Smilax china, Lilium longiflorum and Alstroemeria aurea, members of the Smilacaceae, Liliaceae and Alstroemeriaceae (Liliales), respectively. However, the loss rps16 exon 2 in V. patulum results in the difference in the large single copy regions in comparison with other species. The base substitution rate is quite similar among genes of these species. Additionally, the base substitution rate of inverted repeat region was smaller than that of single copy regions in all observed species of Liliales. The IR regions were expanded to trnH_GUG in V. patulum, a part of rps19 in L. longiflorum and A. aurea, and whole sequence of rps19 in S. china. Furthermore, the IGS lengths of rbcL-accD-psaI region were variable among Liliales species, suggesting that this region might be a hotspot of indel events and the informative site for phylogenetic studies in Liliales. In general, the whole chloroplast genome of V. patulum, a potential medicinal plant, will contribute to research on the genetic applications of this genus.