Early diversification and karyotype evolution of flowering plants

Abstract

Flowering plants (angiosperms) dominate our planet and sustain all life on Earth. However, evolutionary relationships among the angiosperm lineages that diverged early – Amborellales, Nymphaeales, Austrobaileyales and Mesangiospermae, which further comprises monocots and other four clades – have remained highly disputed likely because of their rapid diversification promoted by an ancestral polyploidization event. Here, we present high-quality chromosomal-level genome assemblies of two species – star anise (Illicium verum: 12.5 Gb with a large size) in the Austrobaileyales and calamus (Acorus gramineus) representing the sister lineage to all other extant monocots. These two genomes filled the final gaps of all genomic representatives for major angiosperm lineages. Our phylogenetic analyses of collinear genes support Amborellales and Nymphaeales as sister lineages and they, together with Austrobaileyales and monocots are successively sister to other Mesangiospermae clades. Based on chromosome-like synteny blocks shared between extant genomes, we constructed the ancestral angiosperm karyotype to be x=16. We independently established evolutionary relationships for all sampled species based on shared polyploidizations and chromosomal fusions from the common ancestral karyotype. This phylogenetic relationship is congruent with that from collinear genes, especially the finding that Amborellales and Nymphaeales shared a rare chromosomal fusion not seen in other angiosperms. These results advance our understanding and shed new lights on early diversification and karyotype evolution of flowering plants.

Genome‐scale angiosperm phylogenies based on nuclear, plastome, and mitochondrial datasets

“…Therefore, the presence of paralogous genes arising from WGD might also make it difficult to accurately extract true nuclear “orthologous genes” for phylogenetic reconstruction (Xiong et al, 2022). The assumed nuclear “orthologous” genes from different species with independent WGD events might have arisen from the random retention of one copy from the duplicated pair, making them “paralogous” rather than “orthologous.” One possible solution to this issue is to avoid using traditional methods to extract nuclear “orthologous” genes and instead to identify all “colinear and paralogous” genes from chromosome‐level high‐quality de novo genomes for phylogenetic analysis (Sun et al, 2022; Xiong et al, 2022). In addition, examining changes in genomic structure or karyotypic evolution may be useful for independently examining the phylogenetic relationships of disputed lineages in angiosperms (Sun et al, 2022).…”

“…One possible solution to this issue is to avoid using traditional methods to extract nuclear "orthologous" genes and instead to identify all "colinear and paralogous" genes from chromosome-level high-quality de novo genomes for phylogenetic analysis (Sun et al, 2022;Xiong et al, 2022). In addition, examining changes in genomic structure or karyotypic evolution may be useful for independently examining the phylogenetic relationships of disputed lineages in angiosperms (Sun et al, 2022).…”

“…Polyploidizations or whole‐genome duplications (WGDs) are very common in plants (Jiao et al, 2011). It is likely that the species selected to represent the same unit during different analyses may have different polyploidization histories, which may lead to the misidentification of orthologs due to recent WGD(s) (Sun et al, 2022). Horizontal gene transfer, which is likely to occur for both plastomes and mitochondrial genomes (Albert et al, 2013), may also lead to phylogenetic inconsistencies between phylogenies based on different genomes.…”

“…Phylogenetic reconstructions of these different genome‐scale datasets and further topological comparisons may help to prevent the discrepancies arising from the selection of different species. In addition, the use of orthologous or single‐copy nuclear sequences from de novo genomes is more accurate compared with transcriptome data and/or TSCD because duplicated colinear genes could easily be identified in well assembled genomes (Sun et al, 2022).…”

Subgenome phasing for complex allopolyploidy: case-based benchmarking and recommendations

“…Subgenome-aware phylogeny, a phylogenetic methodology based on a comprehensive gene set derived from the subgenomes of a polyploid, can offer a more robust and insightful framework than phylogenetic approaches at the gene or syntenic block level for deciphering the origin and evolutionary trajectories of polyploids. This subgenome-aware phylogenetic approach has been used to probe the evolutionary history, including diversification and polyploidization processes, not only in early angiosperms [ 10 , 11 ] but also in recently formed allopolyploids and interspecific hybrids, including those found in cereals [ 12 ], trees [ 13 ], fruits [ 14 ], vegetables [ 15 ], herbs [ 16 ] and fish [ 17 ]. A vital step in these studies is the phasing of a polyploid’s subgenomes, which involves sorting the subgenomes according to their parental origin with the highest possible precision.…”