Background <p>The Polygonaceae family comprises approximately 1,200 species of pharmacological, economic, and ecological importance, including medicinal genera such as <i>Rheum</i>, <i>Polygonum</i>, and <i>Fagopyrum</i>, which produce bioactive anthraquinones, stilbenes, and flavonoids. Despite their therapeutic importance, comprehensive analyses of chloroplast genomes across this family remain limited. Chloroplast genomes provide valuable molecular markers for evolutionary studies, phylogenetic reconstruction, and quality control of herbal medicines.</p> Results <p>This study comprehensively analyzed chloroplast genomes across 48 Polygonaceae species, focusing on genome architecture, gene content, codon usage patterns, selection pressures, simple sequence repeats (SSRs), and phylogenetic relationships. All chloroplast genomes exhibited conserved quadripartite structures, with genome sizes ranging from 155,838 − 179,064&#xa0;bp and GC contents ranging from 36.59 to 38.22%, demonstrating AT enrichment and a consistent bias toward A/U-ending codons. RSCU analysis revealed six universally optimal codons (AGA, GAU, GCU, UAU, UCU, and UUA) conserved across the family. ENC values (46.36–48.28) indicated weak overall codon bias; however, ENC-GC3 plots, neutrality, and PR2 analyses confirmed that natural selection, rather than mutational pressure, predominantly shaped synonymous codon usage. Ka/Ks analysis revealed that 89.1% of gene pairs were under strong purifying selection, with photosystem-related genes the most conserved. A total of 4,593 SSR loci were identified, predominantly mononucleotide repeats concentrated in intergenic regions. Collinearity analyses demonstrated high structural conservation within genera, with coding regions more conserved than noncoding sequences. Phylogenetic reconstruction delineated major lineages and suggested that subfamily-specific codon usage patterns correlate with ecological adaptation.</p> Conclusions <p>This study provides comprehensive insights into chloroplast genome evolution in Polygonaceae, highlighting the predominant role of natural selection in codon usage bias and identifying conserved genomic features, SSR resources, and phylogenetic relationships. These findings establish a foundation for molecular marker development, quality control of medicinal species, and evolutionary investigations of this pharmacologically important plant family.</p>

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Integrative chloroplast genomics of Polygonaceae: evolutionary dynamics, codon optimization, and phylogenetic resolution

  • Haodi Wang,
  • Zishuo Wang,
  • Zhuofan Liu,
  • Guy Smagghe,
  • Xiaoyan Zhao,
  • Dong Li,
  • Yunpeng Gai

摘要

Background

The Polygonaceae family comprises approximately 1,200 species of pharmacological, economic, and ecological importance, including medicinal genera such as Rheum, Polygonum, and Fagopyrum, which produce bioactive anthraquinones, stilbenes, and flavonoids. Despite their therapeutic importance, comprehensive analyses of chloroplast genomes across this family remain limited. Chloroplast genomes provide valuable molecular markers for evolutionary studies, phylogenetic reconstruction, and quality control of herbal medicines.

Results

This study comprehensively analyzed chloroplast genomes across 48 Polygonaceae species, focusing on genome architecture, gene content, codon usage patterns, selection pressures, simple sequence repeats (SSRs), and phylogenetic relationships. All chloroplast genomes exhibited conserved quadripartite structures, with genome sizes ranging from 155,838 − 179,064 bp and GC contents ranging from 36.59 to 38.22%, demonstrating AT enrichment and a consistent bias toward A/U-ending codons. RSCU analysis revealed six universally optimal codons (AGA, GAU, GCU, UAU, UCU, and UUA) conserved across the family. ENC values (46.36–48.28) indicated weak overall codon bias; however, ENC-GC3 plots, neutrality, and PR2 analyses confirmed that natural selection, rather than mutational pressure, predominantly shaped synonymous codon usage. Ka/Ks analysis revealed that 89.1% of gene pairs were under strong purifying selection, with photosystem-related genes the most conserved. A total of 4,593 SSR loci were identified, predominantly mononucleotide repeats concentrated in intergenic regions. Collinearity analyses demonstrated high structural conservation within genera, with coding regions more conserved than noncoding sequences. Phylogenetic reconstruction delineated major lineages and suggested that subfamily-specific codon usage patterns correlate with ecological adaptation.

Conclusions

This study provides comprehensive insights into chloroplast genome evolution in Polygonaceae, highlighting the predominant role of natural selection in codon usage bias and identifying conserved genomic features, SSR resources, and phylogenetic relationships. These findings establish a foundation for molecular marker development, quality control of medicinal species, and evolutionary investigations of this pharmacologically important plant family.