Haplotype‐resolved genome assembly of Populus tremula × P. alba reveals aspen‐specific megabase satellite DNA

• Published in: The Plant journal : for cell and molecular biology 2023-11, Vol.116 (4), p.1003-1017
• Main Authors: Zhou, Ran, Jenkins, Jerry W, Zeng, Yibing, Shu, Shengqiang, Jang, Hosung, Harding, Scott A., Williams, Melissa, Plott, Christopher, Barry, Kerrie W., Koriabine, Maxim, Amirebrahimi, Mojgan, Talag, Jayson, Rajasekar, Shanmugam, Grimwood, Jane, Schmitz, Robert J., Dawe, R. Kelly, Schmutz, Jeremy, Tsai, Chung‐Jui
• Format: Article
• Language: English
• Subjects: Arrays; Biotechnology; Centromeres; Chromosomes; Deoxyribonucleic acid; DNA; Genetic transformation; Genomes; Genomics; Haplotypes; Interspecific hybridization; Knobs; Nucleotide sequence; Populus tremula; Satellite DNA; Telomeres
• ISSN: 0960-7412; 1365-313X
• DOI: 10.1111/tpj.16454

Populus species play a foundational role in diverse ecosystems and are important renewable feedstocks for bioenergy and bioproducts. Hybrid aspen Populus tremula × P. alba INRA 717‐1B4 is a widely used transformation model in tree functional genomics and biotechnology research. As an outcrossing interspecific hybrid, its genome is riddled with sequence polymorphisms which present a challenge for sequence‐sensitive analyses. Here we report a telomere‐to‐telomere genome for this hybrid aspen with two chromosome‐scale, haplotype‐resolved assemblies. We performed a comprehensive analysis of the repetitive landscape and identified both tandem repeat array‐based and array‐less centromeres. Unexpectedly, the most abundant satellite repeats in both haplotypes lie outside of the centromeres, consist of a 147 bp monomer PtaM147, frequently span >1 megabases, and form heterochromatic knobs. PtaM147 repeats are detected exclusively in aspens (section Populus ) but PtaM147‐like sequences occur in LTR‐retrotransposons of closely related species, suggesting their origin from the retrotransposons. The genomic resource generated for this transformation model genotype has greatly improved the design and analysis of genome editing experiments that are highly sensitive to sequence polymorphisms. The work should motivate future hypothesis‐driven research to probe into the function of the abundant and aspen‐specific PtaM147 satellite DNA. High‐quality, chromosome‐scale haplotype assemblies are needed for exploring not only gene‐rich but also gene‐poor genome regions of any outcrossing species for functional, population, ecological, and evolutionary research. We generated telomere‐to‐telomere, haplotype‐resolved assemblies for hybrid aspen 717 used in transgenic research. We exemplified the value of the genome with the discovery of an abundant class of tandem repeat arrays that differentiates aspen from closely related Populus species.