Chenopodiaceae s.s.(Amaranthaceae s.l.)contains the largest number of C4 species among eudicots.Despite this,plastome evolution within this family has been investigated in only a few species.Here,we analyzed 119 pl...Chenopodiaceae s.s.(Amaranthaceae s.l.)contains the largest number of C4 species among eudicots.Despite this,plastome evolution within this family has been investigated in only a few species.Here,we analyzed 119 plastomes from 115 species,including 78 newly sequenced plastomes,representing all subfamilies and most C4 lineages of Chenopodiaceae s.s.Plastome structural variants,rearrangements,and codon usage bias were compared across subfamilies and photosynthetic types.Multiple phylogenetic approaches were employed to reconstruct the evolutionary relationships within Chenopodiaceae s.s.,and Bayesian divergence time estimation was performed.Various Mk models for discrete character evolution were tested to investigate the evolution of C4 photosynthesis,and stochastic character mapping simulations were used to reconstruct shifts in photosynthetic pathways through time.Several plastome structural variants and rearrangements were identified,but associations with photosynthetic types were observed only in the subfamily Suaedoideae.Codon usage bias analysis revealed significant bias exclusively in C4 species,suggesting enhanced translational efficiency and accuracy as an adaptation to environmental conditions.We inferred multiple independent origins of the C4 pathway,with the oldest lineages—Bienertia(Suaedoideae)and Caroxyleae(Salsoloideae)—dating to approximately 34 and 32 million years ago(Ma),respectively,during the Oligocene.A marked increase in the number of C4 lineages occurred between 20 and 15 Ma.Declining atmospheric CO2 concentrations,combined with genetic,ecological,and environmental factors,likely promoted the expansion of C4 photosynthesis until recently.Finally,we identified five new hypervariable regions that will be valuable for phylogenetic and DNA barcoding applications in Chenopodiaceae s.s.展开更多
基金supported by the Xinjiang Uygur Autonomous Region Science Foundation(No.2025D01E58)the Tianshan Talent Training Program(No.2023TSYCCX0090)+6 种基金the Shanghai Cooperation Organization Partnership and International Technology Cooperation Plan of Science and Technology Projects(No.2022E01033)the National Natural Science Foundation of China(No.31970354)and the CAS President's International Fellowship Initiative(PIFI)(Nos.2024VBA0015,2024VBC0006)supported by the"National Biodiversity Future Center-NBFC"under the National Recovery and Resilience Plan(NRRP),Mission 4 Component 2 Investment 1.4—Call for tender No.3138 of December 16,2021,rectified by Decree No.3175 of December 18,2021 of the Italian Ministry of University and Research,funded by the European Union-Next Generation EUProject code CN_00000033,Concession Decree No.1034 of June 17,2022 adopted by the Italian Ministry of University and Research,CUP H43C22000530001Project title"NationalBiodiversity Future Center—NBFC."The study of APS was conducted under the state assignment of Lomonosov Moscow State University.
摘要Chenopodiaceae s.s.(Amaranthaceae s.l.)contains the largest number of C4 species among eudicots.Despite this,plastome evolution within this family has been investigated in only a few species.Here,we analyzed 119 plastomes from 115 species,including 78 newly sequenced plastomes,representing all subfamilies and most C4 lineages of Chenopodiaceae s.s.Plastome structural variants,rearrangements,and codon usage bias were compared across subfamilies and photosynthetic types.Multiple phylogenetic approaches were employed to reconstruct the evolutionary relationships within Chenopodiaceae s.s.,and Bayesian divergence time estimation was performed.Various Mk models for discrete character evolution were tested to investigate the evolution of C4 photosynthesis,and stochastic character mapping simulations were used to reconstruct shifts in photosynthetic pathways through time.Several plastome structural variants and rearrangements were identified,but associations with photosynthetic types were observed only in the subfamily Suaedoideae.Codon usage bias analysis revealed significant bias exclusively in C4 species,suggesting enhanced translational efficiency and accuracy as an adaptation to environmental conditions.We inferred multiple independent origins of the C4 pathway,with the oldest lineages—Bienertia(Suaedoideae)and Caroxyleae(Salsoloideae)—dating to approximately 34 and 32 million years ago(Ma),respectively,during the Oligocene.A marked increase in the number of C4 lineages occurred between 20 and 15 Ma.Declining atmospheric CO2 concentrations,combined with genetic,ecological,and environmental factors,likely promoted the expansion of C4 photosynthesis until recently.Finally,we identified five new hypervariable regions that will be valuable for phylogenetic and DNA barcoding applications in Chenopodiaceae s.s.