The soursop genome and comparative genomics of basal angiosperms provide new insights on evolutionary incongruence

Abstract

Deep relationships and the sequence of divergence among major lineages of angiosperms (magnoliids, monocots and eudicots) remain ambiguous and differ depending on analytical approaches and datasets used.Complete genomes potentially provide opportunities to resolve these uncertainties, but two recently published magnoliid genomes instead deliver further conflicting signals. To disentangle key angiosperm relationships, we report a high-quality draft genome for the soursop (Annona muricata, Annonaceae). We reconstructed phylogenomic trees and show that the soursop represents a genomic mosaic supporting different histories, with scaffolds almost exclusively supporting single topologies. However, coalescent methods and a majority of genes support magnoliids as sister to monocots and eudicots, where previous whole genome-based studies remained inconclusive. This result is clear and consistent with recent studies using plastomes. The soursop genome highlights the need for more early diverging angiosperm genomes and critical assessment of the suitability of such genomes for inferring evolutionary history. 36 37 38 39 40 41 42 43 44 45 46 47 2 successive reductions in the number of whorls of both the perianth and the androecium. In both cases, disparate reductions may have paved the way for the evolution of clade specific features of genomes and flower morphology in contemporary clades. Since the publication of the first plant genome, that of Arabidopsis thaliana (Initiative 2000), there has been a steady increase in the number of sequenced eudicot and monocot genomes. However, with the exception of the iconic Amborella trichopoda, basal angiosperm diversity represented by the ancient lineages of Nymphaeales, Austrobaileyales, Chloranthales, and magnoliids has largely been overlooked. After eudicots and monocots, Magnoliidae are the most diverse clade of angiosperms (Massoni et al. 2014) with 9,000-10,000 species in four orders (Canellales, Piperales, Laurales and Magnoliales). However, despite this diversity and economic value (e.g. avocado, black pepper, cinnamon, soursop), only two genomes have been

The genome of Magnolia biondii Pamp. provides insights into the evolution of Magnoliales and biosynthesis of terpenoids

“…Specifically, magnoliids are resolved as sister to eudicots, with relatively strong support 11 , which is consistent with the results of a phylotranscriptomic analysis of 92 streptophytes 13 and 20 representative angiosperms 14 . Alternatively, magnoliids are resolved as sister to eudicots and monocots, with weak support [8][9][10]12 , which is in agreement with the large-scale plastome phylogenomic analysis of land plants, Viridiplantae, and angiosperms [15][16][17] . As phylogenetic inferences rely heavily on the sampling of lineages and genes, as well as analytical methods 5 , these controversial taxonomic placements of magnoliids relative to monocots and eudicots need to be further examined with more genomic data from magnoliids.…”

“…This WGD event might have occurred shortly before the split of the Magnoliales and Laurales, as was indicated in a recent study on the genome evolution of Litsea 89 . However, this hypothesis needs to be further examined in light of other results, such as the absence of a WGD event in Magnoliales Annona muricata 10 .…”

“…After the early divergence of angiosperms (Amborellales, Austrobaileyales, and Nymphaeales), the rapid radiation of five lineages of mesangiosperms (magnoliids, Chloranthaceae, Ceratophyllum, monocots, and eudicots) occurred within a very short time frame of < 5MYA 6 , leading to unresolved/ controversial phylogenetic relationships among some lineages of mesangiosperms 5 . To date, of the 323 genome sequences available for angiosperm species 7 , mostly those of plants with agronomic value, genomes are available for only five magnoliids: black pepper 8 , avocado 9 , soursop 10 , stout camphor tree 11 , and Liriodendron chinense 12 . Phylogenomic analyses based on these genomic data have led to controversial taxonomic placements of magnoliids.…”

The draft mitochondrial genome of Magnolia biondii and mitochondrial phylogenomics of angiosperms

“…However, some deep nodes, such as the phylogenetic divergence order of Nymphaeales and Amborellales, the relationship among the five mesangiosperm lineages, were not well resolved in the current analysis. Extended samplings of more representatives of the early angiosperms and the comparison of mt phylogeny with those of the plastid [36,37], nuclear [34,72], morphology, and non-molecular data would be essential to confidently revolve the phylogenetic relationships of magnoliids relative to monocots and eudicots.…”

The Soursop Genome (Annona muricata L., Annonaceae)

“…avocado, black pepper, cinnamon, soursop), only two genomes have been published to date (Chaw et al 2019;Chen et al 2019). Contrary to expectations, comparative genomic analyzes did not resolve the still unclear relationships of magnoliids with the rest of angiosperms (Strijk et al 2019b). Results strongly disagreed on the position of magnoliids, supporting either a sister relationship to eudicots and monocots (Chen et al 2019), or to eudicots alone (Chaw et al 2019).…”