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<p>C<sub>4</sub> photosynthesis possess complex traits associated with high efficiencies in light, nitrogen and water utilization. To investigate the coupling of carbon and nitrogen stoichiometry within the systematic metabolism along the evolutionary path from C<sub>3</sub> to C<sub>4</sub> photosynthesis, we applied the nuclear magnetic resonance (NMR)-based metabolomics and advanced lipidomic approaches to profile 38 metabolites and 246 lipids in leaves of representative C<sub>3</sub> ancestral, C<sub>3</sub>–C<sub>4</sub> intermediate, and C<sub>4</sub> species in the genus <i>Flaveria</i>. Our results revealed that progressive changes in metabolic profiles associated with amino acids/amines, organic acids, choline/its derivatives, and phospholipids along the C<sub>3</sub> to C<sub>4</sub> transition, implicating these pathways in cellular responses functionally oriented toward protein synthesis and degradation, tricarboxylic acid (TCA) cycle activity, and oxidative stress. In contrast, the metabolism related to carbohydrate and lipid biosynthesis exhibited a declining trend from C<sub>3</sub> to C<sub>4</sub> species. Among C<sub>3</sub>–C<sub>4</sub> intermediates, the type II <i>F. ramosissima</i> displayed a unique metabolic profile, combining characteristics of both C<sub>3</sub> species (elevated carbohydrate levels) and C<sub>4</sub> species (elevated amino acid and organic acid levels)<i>.</i> Taking together, these comprehensive metabolic phenotypes delineate distinct biochemical signatures associated with photosynthetic types in <i>Flaveria</i>, providing novel insights into the metabolic reprogramming underpinning C<sub>4</sub> photosynthetic evolution.</p>

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Quantitative metabolic and lipidomic landscapes reveal the molecular phenotype of C4 evolution in genus Flaveria

  • 期刊论文

  • 出版模式：

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  • 发表日期：

    2026年5月13日

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  • Yanpeng An,
  • Wenjuan Qian,
  • Ming-Ju Amy Lyu,
  • Yuxuan Zhu,
  • Qingxia Huang,
  • Qi Wang,
  • Xinguang Zhu,
  • Huiru Tang,
  • Hongyan Yao

摘要

C4 photosynthesis possess complex traits associated with high efficiencies in light, nitrogen and water utilization. To investigate the coupling of carbon and nitrogen stoichiometry within the systematic metabolism along the evolutionary path from C3 to C4 photosynthesis, we applied the nuclear magnetic resonance (NMR)-based metabolomics and advanced lipidomic approaches to profile 38 metabolites and 246 lipids in leaves of representative C3 ancestral, C3–C4 intermediate, and C4 species in the genus Flaveria. Our results revealed that progressive changes in metabolic profiles associated with amino acids/amines, organic acids, choline/its derivatives, and phospholipids along the C3 to C4 transition, implicating these pathways in cellular responses functionally oriented toward protein synthesis and degradation, tricarboxylic acid (TCA) cycle activity, and oxidative stress. In contrast, the metabolism related to carbohydrate and lipid biosynthesis exhibited a declining trend from C3 to C4 species. Among C3–C4 intermediates, the type II F. ramosissima displayed a unique metabolic profile, combining characteristics of both C3 species (elevated carbohydrate levels) and C4 species (elevated amino acid and organic acid levels). Taking together, these comprehensive metabolic phenotypes delineate distinct biochemical signatures associated with photosynthetic types in Flaveria, providing novel insights into the metabolic reprogramming underpinning C4 photosynthetic evolution.