Pangenomic study of water caltrop — structural variations play a role in speciation and asymmetric subgenome evolution

Rice, maize, and wheat provide more than half of the calories consumed by humans. The decrease in crop diversity poses a significant risk to global food security. Therefore, the utilization of orphan crops has become an effective approach to address food security crises. Nevertheless, in the face of rapid urban and rural modernization and the intensification of agricultural practices, the availability of wild and cultivated orphan crops is dwindling, with a noticeable disparity in their collection, preservation, and application of modern breeding techniques. Water caltrop (Trapa spp.) is a kind of typical orphan crop, which has been consciously collected and domesticated as early as the Neolithic period. During the Tang and Song Dynasties, after further artificial selection, more than 20 varieties, e.g. ‘Wuling’, ‘Nanhuling’, were cultivated. With the development of genomic technologies, pangenome research has become an essential approach for comprehensively understanding the mechanisms underlying agronomic trait. In October 2023, a research paper entitled ‘Pangenome of water caltrop reveals structural variations and asymmetric subgenome divergence after allopolyploidization’ was published in the Horticulture Research by Dr. Yingxiong Qiu’s research team from the Wuhan Botanical Garden, Chinese Academy of Sciences.

The annual herbaceous and aquatic genus Trapa L. (Lythraceae), has traditionally been divided into two species, i.e. T. natans L. with diploid (2n = 2x = 48, AA) and tetraploid (2n = 4x = 96, AABB) cytotypes, and diploid T. incisa Sieb. and Zucc. (2n = 2x = 48, BB). Cultivated water caltrop was derived from the diploid T. natans with larger fruit size (Figure 1). In this study, the authors generated two chromosome-level genome assemblies of diploid T. natans and T. incisa. In conjunction with four previously published (sub)genomes of Trapa, a gene-based pangenome was constructed. The results show that core, dispensable, and private gene clusters accounted for 48.05%, 28.92% and 23.03% of all gene clusters, respectively (Figure 2). Besides, to precisely identify the potential presence-absence variations (PAVs) that may contribute to reproductive isolation and phenotypic divergence between T. incisa and diploid T. natans, the authors also constructed a graph-based pangenome based on 211,598 non-redundant PAVs among the six (sub)genomes. A total of 40,453 PAVs were found completely differentiated between A- and B-lineages, involving 2,570 genes. Gene ontology enrichment analysis showed that these genes were mainly enriched in organ development process, organic substance metabolic process and response to stimulus. Transcriptomic analysis further revealed that most of those genes were differentially expressed between T. incisa and diploid T. natans, indicating these genes likely play a crucial role in phenotypic differentiation and reproductive isolation between the two diploid species. Additionally, based on comparative genome analysis and pan transposable element (TE) analyses, the authors found that allotetraploid T. natans underwent asymmetric subgenome divergence, with the B-subgenome being more dominant than the A-subgenome. Multiple factors, including PAVs, asymmetrical amplification of TEs, homeologous exchanges (HEs), and homeolog expression divergence, together affected genome evolution after polyploidization (Figure 3). In conclusion, the pangenome of Trapa affords a platform for a thorough exploration of genomic variation of Trapa species, thereby promoting a better understanding of the evolutionary and functional genomics of this currently underutilized crop variation.

Ph. D. students Xinyi Zhang and Yang Chen (Currently working at Ningbo Academy of Agricultural Sciences) from Zhejiang University/Wuhan Botanical Garden, Chinese Academy of Sciences are the co-first authors of the paper. Prof. Yingxiong Qiu from Wuhan Botanical Garden and Prof. Zhaisheng Zheng from Jinhua Academy of Agricultural Sciences are the co-corresponding authors. Associate Prof. Yuanyuan Chen from Wuhan Botanical Garden participated in this work. Prof. Yongfeng Zhou from Shenzhen Institute of Genomics, Chinese Academy of Agricultural Sciences, provided valuable suggestions for this project. This work was supported by the collaborative program of Chinese Academy of Agricultural Sciences (CAAS)-Jinhua Academy of Agricultural Sciences, funded by Jinhua City of Zhejiang Province, and the Research Grant from Wuhan Botanic Garden (E1559901).

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References

Authors

Xinyi Zhang^1,2,†, Yang Chen^1,2,†, Lingyun Wang³, Ye Yuan⁴, Mingya Fang³, Lin Shi³, Ruisen Lu⁵, Hans Peter Comes⁶, Yazhen Ma², Yuanyuan Chen², Guizhou Huang⁷, Yongfeng Zhou⁷, Zhaisheng Zheng^3,*, Yingxiong Qiu^2,*

Affiliations

¹Systematic and Evolutionary Botany and Biodiversity Laboratory, College of Life Sciences, Zhejiang University, Hangzhou 310058, Zhejiang, China

²CAS Key Laboratory of Plant Germplasm Enhancement and Specialty Agriculture, Wuhan Botanical Garden, Chinese Academy of Sciences, Wuhan 430074, Hubei, China

³Provincial Key Laboratory of Characteristic Aquatic Vegetable Breeding and Cultivation, Jinhua Academy of Agricultural Sciences (Zhejiang Institute of Agricultural Machinery), Jinhua 321000, Zhejiang, China

⁴Jiaxing Academy of Agricultural Sciences, Jiaxing 314016, Zhejiang, China

⁵Institute of Botany, Jiangsu Province and Chinese Academy of Sciences, Nanjing 210014, Jiangsu, China

⁶Department of Environment & Biodiversity, Salzburg University, Salzburg 5020, Austria

⁷State Key Laboratory of Tropical Crop Breeding, Shenzhen Branch, Guangdong Laboratory of Lingnan Modern Agriculture; Key Laboratory of Synthetic Biology, Ministry of Agriculture and Rural Affairs, Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences, Shenzhen 518124, Guangdong, China

About Yingxiong Qiu

Dr. Qiu is currently a full professor of Wuhan Botanical Garden, Chinese Academy of Sciences. His current research interests include plant systematics and evolution, conservation biology, as well as enhancement and utilization of plant germplasm resources. He is a member of the editorial board of BMC Plant Biology, Plant Systematics and Evolution, Journal of Systematics and Evolution, Plant Diversity, Biodiversity. Dr. Qiu has published more than 100 peer-reviewed papers in journals, including Nat. Commun., New Phytol., Plant Biotechnol., The Plant J., Mol. Ecol., Evol. Appl., Mol. Phylogenet. Evol., J. Biogeogr., Mol. Ecol. Resour., Ann. Bot., BMC Plant Biol., Taxon, and Am. J. Bot. He is the recipient of the second prize of the Natural Science Award of the Ministry of Education (2017) and Zhejiang Province (2008, 2015).