Extensive characterization of 28 complete chloroplast genomes of Hydrangea species: A perspective view of their organization and phylogenetic and evolutionary relationships

Abstract

The tribe Hydrangeeae displays a unique, distinctive disjunct distribution encompassing East Asia, North America and Hawaii. Despite its complex trait variations and polyphyletic nature, comprehensive phylogenomic and biogeographical studies on this tribe have been lacking. To address this gap, we sequenced and characterized 28 plastomes of Hydrangeeae. Our study highlights the highly conserved nature of Hydrangeaceae chloroplast (cp) genomes in terms of gene content and arrangement. Notably, synapomorphic characteristics of tandem repeats in the conserved domain of accD were observed in the Macrophyllae, Chinenses, and Dichroa sections within the Hydrangeeae tribe. Additionally, we found lower expression of accD in these sections using structure prediction and quantitative real-time PCR analysis. Phylogenomic analyses revealed the subdivision of the Hydrangeeae tribe into two clades with robust support values. Consistent with polyphyletic relationships, sect. Broussaisia was identified as the basal group in the tribe Hydrangeeae. Our study also provides insights into the phylogenetic relationships of Hydrangea petiolaris in the Jeju and Ulleung Island populations, suggesting the need for further studies with more samples and molecular data. Divergence time estimation and biogeographical analyses suggested that the common ancestors of the tribe Hydrangeeae likely originated from North America and East Asia during the Paleocene period via the Bering Land Bridge, potentially facilitating migration within the tribe between these regions. In conclusion, this study enhances our understanding of the evolutionary history and biogeography of the tribe Hydrangeeae, shedding light on the dispersal patterns and origins of this intriguing plant group with its unique disjunct distribution.

Graphical Abstract

Highlights

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  The architecture and gene functions of 28 newly sequenced Hydrangeaceae chloroplast genomes were revealed.

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  Hydrangea clade II possessed synapomorphic characteristics of 18-bp tandem repeats in the conserved domain of accD.

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  Phylogenomic analyses revealed the subdivision of the tribe Hydrangeeae into two clades with robust support values.

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  Explored phylogenetic links of Hydrangea petiolaris in Jeju and Ulleung Island populations for evolutionary insights.

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  Divergent analysis showed Hydrangeeae tribe likely originated in East Asia, North America, during Paleocene via Bering Land Bridge.