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.2023 Jan;113(2):262-276.
doi: 10.1111/tpj.16044. Epub 2022 Dec 10.

The genome of the king protea, Protea cynaroides

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The genome of the king protea, Protea cynaroides

Jiyang Chang et al. Plant J.2023 Jan.

Abstract

The king protea (Protea cynaroides), an early-diverging eudicot, is the most iconic species from the Megadiverse Cape Floristic Region, and the national flower of South Africa. Perhaps best known for its iconic flower head, Protea is a key genus for the South African horticulture industry and cut-flower market. Ecologically, the genus and the family Proteaceae are important models for radiation and adaptation, particularly to soils with limited phosphorus bio-availability. Here, we present a high-quality chromosome-scale assembly of the P. cynaroides genome as the first representative of the fynbos biome. We reveal an ancestral whole-genome duplication event that occurred in the Proteaceae around the late Cretaceous that preceded the divergence of all crown groups within the family and its extant diversity in all Southern continents. The relatively stable genome structure of P. cynaroides is invaluable for comparative studies and for unveiling paleopolyploidy in other groups, such as the distantly related sister group Ranunculales. Comparative genomics in sequenced genomes of the Proteales shows loss of key arbuscular mycorrhizal symbiosis genes likely ancestral to the family, and possibly the order. The P. cynaroides genome empowers new research in plant diversification, horticulture and adaptation, particularly to nutrient-poor soils.

Keywords: Protea cynaroides; comparative genomics; early-divergent eudicot; genome annotation; genome assembly.

© 2022 The Authors. The Plant Journal published by Society for Experimental Biology and John Wiley & Sons Ltd.

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Conflict of interest statement

The authors declare that they have no conflicts of interest associated with this work.

Figures

Figure 1
Figure 1
Genome assembly features ofProtea. (a) Hi‐C interaction heatmap of the assembledProtea cynaroides genome. (b) The landscape ofP. cynaroides genome assembly. Bar plots (from innermost outwards) show DNA transposable elements (TEs), Copia, Gypsy, gene density per 300 kb and chromosomes. Ribbons connect inter‐chromosomal syntenic regions. (c) Gypsy and Copia content comparison of six early‐diverging eudicot plants.
Figure 2
Figure 2
The whole‐genome duplication (WGD) event in Proteaceae. (a)Ks distributions for anchor pairs (retained paralogs from the WGD event) withinProtea cynaroides,Macadamia integrifolia andTelopea speciosissima genome, and for orthologs ofP. cynaroides and related species. (b) Inferred phylogenetic tree with 176 single‐copy genes in 17 species except forPapaver somniferum andPapaver setigerum identified by OrthoFinder. Timing of Proteaceae WGD was estimated in this study, and previously reported whole‐genome triplication (WGT)/WGD events are superimposed on the tree. (c) Intergenomic co‐linearity amongP. cynaroides,Vitis vinifera andM. integrifolia. (d) Absolute dating of theP. cynaroides WGD event. The age distribution was obtained by phylogenomic dating ofP. cynaroides paralogs. The solid black line represents the Kernel Density Estimation (KDE) of the dated paralogs, while the vertical dashed black line represents its peak at 67.9 MYA, which was used as the consensus WGD age estimate. The gray lines represent density estimates from 2500 bootstrap replicates, and the vertical black dotted lines represent the corresponding 90% confidence interval (CI) for the WGD age estimate, 59.267–76.85 MYA (see Experimental Procedures section). The histogram shows the raw distribution of dated paralogs.
Figure 3
Figure 3
Intergenomic comparisons between Protea and early‐diverging eudicots. Synteny betweenProtea cynaroides and three early‐Eudicot species (Nelumbo nucifera,Aquilegia oxysepala andCorydalis tomentella), as well as three poppies (Papaver rhoeas,Papaver somniferum andPapaver setigerum), respectively. A clear 2:2 syntenic relationship betweenP. cynaroides and these three early‐Eudicot species from different families can be observed. Meanwhile, a clear 2:2 synteny relationships betweenP. cynaroides andPa. rhoeas, 2:4 synteny relationships betweenP. cynaroides andPa. somniferum, and 2:8 synteny relationships betweenP. cynaroides andP. setigerum can be identified.
Figure 4
Figure 4
MADS‐box genes inProtea cynaroides andMacadamia integrifolia. (a) The phylogenetic tree of type II MADS‐box genes inP. cynaroides,M. integrifolia,Arabidopsis thaliana andOryza sativa. (b) The syntenic relationships of MADS‐box genes inP. cynaroides andM. integrifolia. Genes in yellow are MADS‐box genes; lines link the genes in the syntenic blocks, derived from the whole‐genome duplication (WGD) event. (c) Gene expression patterns of type II MADS‐box genes from various organs inP. cynaroides.
Figure 5
Figure 5
Loss of arbuscular mycorrhizal (AM)‐conserved genes in the order Proteales. Homologs of common symbiotic pathway (CSP) genes are present in both host (H) and non‐host species. In contrast, homologs of ‘AM‐conserved’ genes were lost in known non‐hosts (Lupinus albus andArabidopsis thaliana) as well as in the Proteales species indicated here. Boxes indicate presence, with gray indicating presence based on previous studies. Lines indicate absence. Genes indicated by a transparent red box are considered ‘conserved’ genes based on available literature (Delaux et al., 2014).
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