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. 2013 Aug;25(8):2813-30.
doi: 10.1105/tpc.113.113480. Epub 2013 Aug 27.

The Tarenaya hassleriana genome provides insight into reproductive trait and genome evolution of crucifers

Shifeng Cheng  1 , Erik van den Bergh, Peng Zeng, Xiao Zhong, Jiajia Xu, Xin Liu, Johannes Hofberger, Suzanne de Bruijn, Amey S Bhide, Canan Kuelahoglu, Chao Bian, Jing Chen, Guangyi Fan, Kerstin Kaufmann, Jocelyn C Hall, Annette Becker, Andrea Bräutigam, Andreas P M Weber, Chengcheng Shi, Zhijun Zheng, Wujiao Li, Mingju Lv, Yimin Tao, Junyi Wang, Hongfeng Zou, Zhiwu Quan, Julian M Hibberd, Gengyun Zhang, Xin-Guang Zhu, Xun Xu, M Eric Schranz
Affiliations

The Tarenaya hassleriana genome provides insight into reproductive trait and genome evolution of crucifers

Shifeng Cheng et al. Plant Cell. 2013 Aug.

Abstract

The Brassicaceae, including Arabidopsis thaliana and Brassica crops, is unmatched among plants in its wealth of genomic and functional molecular data and has long served as a model for understanding gene, genome, and trait evolution. However, genome information from a phylogenetic outgroup that is essential for inferring directionality of evolutionary change has been lacking. We therefore sequenced the genome of the spider flower (Tarenaya hassleriana) from the Brassicaceae sister family, the Cleomaceae. By comparative analysis of the two lineages, we show that genome evolution following ancient polyploidy and gene duplication events affect reproductively important traits. We found an ancient genome triplication in Tarenaya (Th-α) that is independent of the Brassicaceae-specific duplication (At-α) and nested Brassica (Br-α) triplication. To showcase the potential of sister lineage genome analysis, we investigated the state of floral developmental genes and show Brassica retains twice as many floral MADS (for minichromosome maintenance1, AGAMOUS, DEFICIENS and serum response factor) genes as Tarenaya that likely contribute to morphological diversity in Brassica. We also performed synteny analysis of gene families that confer self-incompatibility in Brassicaceae and found that the critical serine receptor kinase receptor gene is derived from a lineage-specific tandem duplication. The T. hassleriana genome will facilitate future research toward elucidating the evolutionary history of Brassicaceae genomes.

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Figures

Figure 1.
Figure 1.
Venn Diagram Illustrating the Shared and Unique Gene Families from T. hassleriana (Cleomaceae), A. thaliana, A. lyrata, and B. rapa (Brassicaceae). In total, we predicted 28,917 well-supported gene models for T. hassleriana, of which 22,482 could be placed into one of the 14,505 gene families. A total of 87.5% of gene families found in Tarenaya were present in all three Brassicaceae species and 7.4% in one or two Brassicaceae species, and only 5% of gene families were unique to Tarenaya with many of these associated genome-specific retrotransposons. Thus, comparative functional and evolutionary analysis of well-characterized Arabidopsis and Brassicaceae genes is feasible using Tarenaya as an outgroup.
Figure 2.
Figure 2.
Relative Timing of the Polyploidy Events and Lineage Splitting Based on Divergence of Fourfold Degenerate Sites (4DTv) for Duplicated Genes within A. thaliana, B. rapa, and T. hassleriana and Orthologous Genes between A. thaliana and T. hassleriana. All plots detect broad overlapping peaks between 0.5 and 1.0, representing shared older polyploidy events (At-β, At-γ, ε, and ζ). The divergence of the Brassicaceae-Cleomaceae lineages is seen by the differentiation of Arabidopsis and Tarenaya homologs at the peak centered at ∼0.35 (highlighted by red star). The divergence between paralogs from the At-α duplication event occurred slightly after the lineage splitting and is detected by the peaks centered at ∼0.3 for both Arabidopsis and Brassica. The At-α peak is lacking from Tarenaya, proving At-α is Brassicaceae specific. Nearly overlapping distributions between 0.15 and 0.25 were detected for Brassica and Tarenaya, representing the independent Br-α and Th-α ancient hexaploidy events, respectively.
Figure 3.
Figure 3.
Homologous Genome Blocks within and between Genomes for Cleomaceae and Brassicaceae. The largest 20 (plus additional two smaller scaffolds) color-coded superscaffolds of T. hassleriana are taken as the reference, such that any region homologous to the 22 scaffolds is colored accordingly. A, Self-alignment of Tarenaya superscaffolds, with the inner circle showing links of syntenic blocks. Over 47% of the genome is found in three copies, supporting the conclusion that it experienced an ancient hexaploidy event (Th-α = triplication). Rings within a genome (inner gray bars) and blocks homologous to Tarenaya (outer color-coded bars) for completed Brassicaceae genomes: B, A. thaliana; C, A. lyrata; and D, B. rapa. The inner gray bars show a clear pattern related to the ancient polyploidy events of the Brassicaceae (At-α = duplication) and nested Brassica-specific lineage (Br-α = triplication). The color-coded outer rings of homology relative to Tarenaya show a complex pattern due to the independent polyploidy events between families. The two small insets illustrate examples of the three Tarenaya to two Arabidopsis to six Brassica genome equivalents due to ancient polyploidy events.
Figure 4.
Figure 4.
Phylogenetic Tree of Type-II MADS Box Transcription Factor Genes Involved in Floral Organ Specification. The alignment used to create this tree is available in the online materials (see Supplemental Data Set 2 online). The major floral MADS box genes cluster into five groups corresponding to the five main functional types (AP1-like genes, shown in yellow; AP3/PI-like genes, B-type shown in blue; AG-like genes shown in gray; STK-like genes shown in red; and SEP-like genes in green) according to the ABC(DE) model of floral development. Species included are A. thaliana (At), grape (Vitis vinifera, Vv), tomato (Solanum lycopersicum, Sl), poplar (Populus trichocarpa, Pt), B. rapa (Br), and T. hassleriana (Th). Tarenaya genes are indicated in red. The colored squares (duplication events) and circles (triplication events) placed on nodes represent gene lineage expansion(s) that can be associated with particular ancient polyploid events: Th-α, At-α, Br-α, At-β, At-γ, ε, T (identified by tomato genome sequencing), and Pt-α (identified by poplar genome sequencing). Type-II MADS box genes are often retained after ancient polyploidy events. From the tree above, we calculated a 27.3% syntelog (homolog generated by a polyploidy event) retention after At-α, 27.3% syntelog retention after Th-α, and a much higher (67.8%) syntelog retention after Br-α, despite the fact that Th-α and Br-α triplications are of approximately the same age. The Tarenaya B-class genes show unusual patterns in that the AP3 homologs (Ch02920 and Th02921) represent a recent tandem duplication, which is rare for floral MADS box genes, and there are two copies of PI homologs that are likely due to At-β with one lineage being lost in Brassicaceae. Shown is a maximum likelihood tree with 1000 replicate bootstrap values, of which the branches with a bootstrap value of >80 are presented, visualized topology only.
Figure 5.
Figure 5.
Collinearity Analysis of B-Class Type II MADS Box Gene (AP3 and PI) Homologs Reveals Unusual Patterns of Gene Loss, Lineage-Specific Transpositions, and Local Tandem Duplications. The placement of ancient polyploid events giving rise to gene duplicates is shown on appropriate nodes (At-β, At-α, Br-α, and Th-α). For the AP3 group genes in Brassicaceae (shown by red bars), there is only a single locus retained in A. thaliana and A. lyrata and two retained Brassica syntelogs derived from Br-α. Collinear homoeologous regions derived from At-α are detectable in Brassicaceae genomes; however, the AP3 syntelogs were lost (regions highlighted in red boxes). T. hassleriana has an unusual tandem duplication of AP3 genes in one of two homoeologous regions derived from Th-α. The AP3 genes and the neighboring Forkhead gene (EMB1967) are the only genes syntenic to the AP3 Brassicaceae region (see Supplemental Figure 25 online). The Cleomaceae AP3 region is syntenic with AP3 regions of all other eudicot genomes analyzed (see Supplemental Figure 23 online). Thus, we conclude that there was a lineage-specific transposition of AP3 and the neighboring Forkhead locus in the Brassicaceae. There is only a single copy of PI genes (red bars) in A. thaliana and A. lyrata and all three Br-α derived syntelogs in Brassicaceae. There is no detectable homoeologous region in Brassicaceae derived from At-α. In Tarenaya, we detected one syntenic PI gene and region to the Brassicaceae, but also a second region that is syntenic to other eudicots (see Supplemental Figure 24 online). We conclude that these two Tarenaya PI genes were generated due to the At-β ancient duplication event with the subsequent transposition of one locus into the region collinear between Brassicaceae and Cleomaceae and loss of the nontransposed locus from only the Brassicaceae lineage. The differences in genomic context and gene expression (see Supplemental Figure 27 online) may contribute to shifts in floral morphology and symmetry between families.
Figure 6.
Figure 6.
Synteny and Protein Domain Analysis of the Brassicaceae SI-Like Regions with Cleomaceae and Inference of the Ancestral Genomic Region. All regions presented here are drawn in more detail (including genetic coordinates) in Supplemental Figure 28 online. Genes are marked by block arrows and color coded according to their protein domain composition as listed in the legend. In the case of pseudogenes, the block arrows have a dashed border. To find protein domain composition in pseudogenes, the longest open reading frame was translated in silico (see Methods). Gene orientation is shown by block arrows pointing left for gene orientation toward the 5′ end and pointing right for gene orientation toward the 3′end. The At-α duplication and the Br-α and Th-α triplications have been marked on the tree with an orange box (At-α) and yellow and purple circles (Br-α and Th-α, respectively). Each branch corresponds to a subgenome resulting from such a polyploid event. Theoretically, B. rapa should have six subgenomes, but only the regions showing synteny are listed here for clarity. The bottom branch represents a hypothetical layout of this genome region in the common ancestor of these species before the At-α, Br-α, and Th-α polyploid events. From our results, we conclude that an ARK3-like gene underwent a Brassicaceae-specific tandem gene duplication generating the key SI receptor SRK.
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