<p>The genetic basis for the adaptive advantages of polyploids over their diploid relatives remains poorly understood. To address this knowledge gap, we generate a haplotype-resolved autotetraploid alfalfa (<i>Medicago sativa</i> subsp. <i>sativa</i>) genome and construct a super-pangenome from 13 genomes across seven <i>Medicago</i> taxa. We discover substantial gene content variation in alfalfa, with only 20.1% of genes present on all four haplotypes. Within this group, 53.3% are core genes conserved across the <i>Medicago</i> genus, which we term ‘tetra-copy core genes’. We find these genes are significantly enriched in climate-adaptation-associated genes (1.60-fold) and stress-responsive differentially expressed genes (1.61-fold). Paradoxically, they also carry a high genetic burden, with 80.1% of deleterious variants located in coding regions. Indeed, overexpressing a representative tetra-copy core gene, the glycine decarboxylase (<i>MsGDC</i>), improves both biomass and nitrogen use efficiency, despite its high genetic burden. Our study reveals the trade-off between adaptation and evolutionary constraints mediated by tetra-copy core genes, facilitating polyploid genetics and alfalfa breeding.</p>

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Medicago super-pangenome reveals adaptive advantages and evolutionary constraints in autotetraploid alfalfa

  • Fan Zhang,
  • Chunxue Wei,
  • Xiaoya Shi,
  • Shuo Cao,
  • Xiaodong Xu,
  • Zhiyao Ma,
  • Yanling Peng,
  • Rida Arshad,
  • Hui Xue,
  • Zhen Zhang,
  • Wei Zhang,
  • Yanshuai Xu,
  • Yang Dong,
  • Lianzhu Zhou,
  • Xuejing Cao,
  • Mengrui Du,
  • Xu Wang,
  • Zhiwu Zhang,
  • Ruicai Long,
  • Junmei Kang,
  • Yongfeng Zhou,
  • Qingchuan Yang

摘要

The genetic basis for the adaptive advantages of polyploids over their diploid relatives remains poorly understood. To address this knowledge gap, we generate a haplotype-resolved autotetraploid alfalfa (Medicago sativa subsp. sativa) genome and construct a super-pangenome from 13 genomes across seven Medicago taxa. We discover substantial gene content variation in alfalfa, with only 20.1% of genes present on all four haplotypes. Within this group, 53.3% are core genes conserved across the Medicago genus, which we term ‘tetra-copy core genes’. We find these genes are significantly enriched in climate-adaptation-associated genes (1.60-fold) and stress-responsive differentially expressed genes (1.61-fold). Paradoxically, they also carry a high genetic burden, with 80.1% of deleterious variants located in coding regions. Indeed, overexpressing a representative tetra-copy core gene, the glycine decarboxylase (MsGDC), improves both biomass and nitrogen use efficiency, despite its high genetic burden. Our study reveals the trade-off between adaptation and evolutionary constraints mediated by tetra-copy core genes, facilitating polyploid genetics and alfalfa breeding.