Haplotype‐resolved genomes of octoploid species in Phyllanthaceae family reveal a critical role for polyploidization and hybridization in speciation

Author:

Li Fangping123,Hou Zhuangwei14,Xu Shiqiang1,Han Danlu5,Li Bin1,Hu Haifei6,Liu Jieying2,Cai Shike1,Gan Zhenpeng2,Gu Yan1,Zhang Xiufeng2,Zhou Xiaofan2ORCID,Wang Shaokui2,Zhao Junliang6,Mei Yu1,Zhang Jisen7ORCID,Wang Zefu3,Wang Jihua1ORCID

Affiliation:

1. Guangdong Provincial Key Laboratory of Crops Genetics and Improvement Crop Research Institute, Guangdong Academy of Agriculture Sciences Guangzhou 510640 China

2. Guangdong Provincial Key Laboratory of Plant Molecular Breeding, State Key Laboratory for Conservation and Utilization of Subtropical Agro‐Bioresources South China Agricultural University Guangzhou 510642 China

3. Co‐Innovation Center for Sustainable Forestry in Southern China, College of Ecology and Environment Nanjing Forestry University Nanjing 210037 China

4. Shenzhen Branch, Guangdong Laboratory for Lingnan Modern Agriculture, Genome Analysis Laboratory of the Ministry of Agriculture Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences Shenzhen Guangdong China

5. Guangdong Provincial Key Laboratory of Biotechnology for Plant Development, School of Life Science South China Normal University 510631 Guangzhou China

6. Rice Research Institute & Guangdong Key Laboratory of New Technology in Rice Breeding & Guangdong Rice Engineering Laboratory Guangdong Academy of Agricultural Sciences Guangzhou 510640 China

7. State Key Lab for Conservation and Utilization of Subtropical Agric‐Biological Resources Guangxi University Nanning 530005 China

Abstract

SUMMARYThe Phyllanthaceae family comprises a diverse range of plants with medicinal, edible, and ornamental value, extensively cultivated worldwide. Polyploid species commonly occur in Phyllanthaceae. Due to the rather complex genomes and evolutionary histories, their speciation process has been still lacking in research. In this study, we generated chromosome‐scale haplotype‐resolved genomes of two octoploid species (Phyllanthus emblica and Sauropus spatulifolius) in Phyllanthaceae family. Combined with our previously reported one tetraploid (Sauropus androgynus) and one diploid species (Phyllanthus cochinchinensis) from the same family, we explored their speciation history. The three polyploid species were all identified as allopolyploids with subgenome A/B. Each of their two distinct subgenome groups from various species was uncovered to independently share a common diploid ancestor (Ancestor‐AA and Ancestor‐BB). Via different evolutionary routes, comprising various scenarios of bifurcating divergence, allopolyploidization (hybrid polyploidization), and autopolyploidization, they finally evolved to the current tetraploid S. androgynus, and octoploid S. spatulifolius and P. emblica, respectively. We further discuss the variations in copy number of alleles and the potential impacts within the two octoploids. In addition, we also investigated the fluctuation of metabolites with medical values and identified the key factor in its biosynthesis process in octoploids species. Our study reconstructed the evolutionary history of these Phyllanthaceae species, highlighting the critical roles of polyploidization and hybridization in their speciation processes. The high‐quality genomes of the two octoploid species provide valuable genomic resources for further research of evolution and functional genomics.

Publisher

Wiley

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