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

Abstract

Magnolia biondii Pamp. (Magnoliaceae, magnoliids) is a phylogenetically, economically, and medicinally important ornamental tree species widely grown and cultivated in the north-temperate regions of China. Determining the genome sequence of M. biondii would help resolve the phylogenetic uncertainty of magnoliids and improve the understanding of individual trait evolution within the Magnolia genus. We assembled a chromosome-level reference genome of M. biondii using ~67, ~175, and ~154 Gb of raw DNA sequences generated via Pacific Biosciences single-molecule real-time sequencing, 10X Genomics Chromium, and Hi-C scaffolding strategies, respectively. The final genome assembly was ~2.22 Gb, with a contig N50 value of 269.11 kb and a BUSCO complete gene percentage of 91.90%. Approximately 89.17% of the genome was organized into 19 chromosomes, resulting in a scaffold N50 of 92.86 Mb. The genome contained 47,547 protein-coding genes, accounting for 23.47% of the genome length, whereas 66.48% of the genome length consisted of repetitive elements. We confirmed a WGD event that occurred very close to the time of the split between the Magnoliales and Laurales. Functional enrichment of the Magnolia-specific and expanded gene families highlighted genes involved in the biosynthesis of secondary metabolites, plant–pathogen interactions, and responses to stimuli, which may improve the ecological fitness and biological adaptability of the lineage. Phylogenomic analyses revealed a sister relationship of magnoliids and Chloranthaceae, which are sister to a clade comprising monocots and eudicots. The genome sequence of M. biondii could lead to trait improvement, germplasm conservation, and evolutionary studies on the rapid radiation of early angiosperms.

The chromosome-scale genome of Magnolia officinalis provides insight into the evolutionary position of magnoliids

“…Thus, these indicated that all four magnoliid species experienced a λ multiplication event about 120 million years ago. This point was consistent with previously sequenced genomes of M. biondii , L. chinense , C. kanehirae, and L. cubeba ( Chaw et al., 2019 ; Chen et al., 2019 , 2020b ; Dong et al., 2021 ). While the Ks values of one-to-one orthologs analysis of M. officinalis with L. chinense , C. kanehirae and L. cubeba were 0.13, 0.75, and 0.76, respectively.…”

“…Based on the phylogenetic tree constructed by 365 single-copy genes, we found that the magnoliids were as sister groups to the eudicots and monocots. Together with the two genomes of Magnoliaceae ( M. biondii and L. chinense ) previously published, our phylogenomic analyses all indicated that magnoliids were independent of monocots and eudicots, which was consistent with the results observed in previous studies ( Chen et al., 2019 , 2020a ; Dong et al., 2021 ; Hu et al., 2019 ; Rendón-Anaya et al., 2019 ).

Figure 4 The Phylogenetic tree including 14 species was constructed based on 365 single-copy genes The WGD shared between the Magnoliales and Laurales is indicated with a red star, and the purple box indicated that an extra recent WGD event was experienced in the Laurales.

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“…In recent years, whole-genome sequencing has been widely performed in a number of magnoliid species, including Magnolia biondii , Liriodendron chinense , Cinnamomum kanehirae , Piper nigrum etc., which provides a certain support for the analyzing of the developmental relationship of angiosperms ( Chaw et al., 2019 ; Chen et al., 2019 ; Dong et al., 2021 ; Hu et al., 2019 ). The position of magnoliids in plant evolution and taxonomy belongs to a relatively primitive class group, and there has long been considerable disagreement over the phylogenetic status of the phylogenetic position of the eudicots, monocots, and magnoliids ( Chen et al., 2020a ; Lv et al., 2020 ).…”

“…Notably, the M. officinalis genome contains 1.37 Gb of repetitive elements, reaching an amazing ratio of 81.44% ( Table S6 ), which was the highest proportion of sequenced repetitive sequences in magnoliids, compared with M. biondii (∼66.48% in a 2,252.5 Mb genome) ( Dong et al., 2021 ), C. kanehirae (∼48% in a 730.7 Mb genome) ( Chaw et al., 2019 ), L. chinense (∼62% in a 1742.4 Mb genome) ( Chen et al., 2019 ), P. bournei (∼68.51% in a 989.19 Mb genome) ( Chen et al., 2020a ), and P. nigrum (∼54.85% in a 761.74 Mb genome) ( Hu et al., 2019 ). Among these repetitive elements of M. officinalis , class I retrotransposons were the majority, with the LTR/Gypsy, LTR/Copia and LARDs classes accounting for 27.53%, 21.11% and 23.90% of the genome, respectively.…”

“…The position of magnoliids in plant evolution and taxonomy belongs to a relatively primitive class group, and there has long been considerable disagreement over the phylogenetic status of the phylogenetic position of the eudicots, monocots, and magnoliids ( Chen et al., 2020a ; Lv et al., 2020 ). For instance, the phylogenetic analysis of M. biondii , L. chinense , P. nigrum , Persea americana, and Phoebe bournei supported that the magnoliids were a sister clade of the eudicots and monocots ( Chen et al., 2019 , 2020a ; Dong et al., 2021 ; Hu et al., 2019 ; Rendón-Anaya et al., 2019 ), whereas some other genomic studies on C. kanehirae , Litsea cubeba and Chimonanthus praecox , C. salicifolius recognized that magnoliids were a sister clade of eudicots ( Chaw et al., 2019 ; Chen et al., 2020b ; Lv et al., 2020 ; Shang et al., 2020 ). In addition, a phylogenetic summary including the ANA-grade angiosperms, eudicots, magnoliids, monocots, and a gymnosperm and timescale of 115 plant species (44 genomes and 71 transcriptomes) were summarized by Zhang et al.…”