Organelle genomes of two Scaevola species, S. taccada and S. hainanensis, provide new insights into evolutionary divergence between Scaevola and its related species

Chloroplast and mitochondrial genomes harbor crucial information that can be utilized for elucidating plant evolution and environmental adaptation. The organellar genomic characteristics of Goodeniaceae, a sister family to Asteraceae, remain unexplored. Here, using a combination of short-read and lo...

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Main Authors: Danni Meng, Tianxin Lu, Meng He, Yuze Ren, Mumei Fu, Yuxiao Zhang, Peifeng Yang, Xinyu Lin, Yong Yang, Ying Zhang, Yuchen Yang, Xiang Jin
Format: Article
Language:English
Published: Frontiers Media S.A. 2025-04-01
Series:Frontiers in Plant Science
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Online Access:https://www.frontiersin.org/articles/10.3389/fpls.2025.1587750/full
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author Danni Meng
Danni Meng
Tianxin Lu
Tianxin Lu
Tianxin Lu
Meng He
Meng He
Yuze Ren
Yuze Ren
Mumei Fu
Mumei Fu
Yuxiao Zhang
Yuxiao Zhang
Peifeng Yang
Peifeng Yang
Xinyu Lin
Xinyu Lin
Yong Yang
Yong Yang
Ying Zhang
Yuchen Yang
Xiang Jin
Xiang Jin
author_facet Danni Meng
Danni Meng
Tianxin Lu
Tianxin Lu
Tianxin Lu
Meng He
Meng He
Yuze Ren
Yuze Ren
Mumei Fu
Mumei Fu
Yuxiao Zhang
Yuxiao Zhang
Peifeng Yang
Peifeng Yang
Xinyu Lin
Xinyu Lin
Yong Yang
Yong Yang
Ying Zhang
Yuchen Yang
Xiang Jin
Xiang Jin
author_sort Danni Meng
collection DOAJ
description Chloroplast and mitochondrial genomes harbor crucial information that can be utilized for elucidating plant evolution and environmental adaptation. The organellar genomic characteristics of Goodeniaceae, a sister family to Asteraceae, remain unexplored. Here, using a combination of short-read and long-read sequencing technologies, we successfully assembled the complete organellar genomes of two Goodeniaceae species native to China, Scaevola taccada and S. hainanensis. Chloroplast genome collinearity analysis revealed that Scaevola expanded its genome length through inverted repeat expansion and large single copy fragment duplication, resulting in 181,022 bp (S. taccada) and 182,726 bp (S. hainanensis), ~30 kb increase compared to its related species. Mitochondrial genomes of two Scaevola species exhibit multi-ring topology, forming dual mitochondrial chromosomes of 314,251 bp (S. taccada) and 276,175 bp (S. hainanensis). Sequence variation analysis demonstrated substantial chloroplast sequence divergence (Pi = 0.45) and an increase in gene copy number within the genus. Relative synonymous codon usage (RSCU) analysis revealed that Scaevola chloroplast has a higher bias for A/U-ending codons than mitochondria, with chloroplasts RSCU values ranging from 0.32 to 1.94, whereas mitochondrial RSCU values ranging from 0.38 to 1.62. Phylogenetic analyses support the monophyly of the Asteraceae-Goodeniaceae sister group, whereas the extended evolutionary branches of Scaevola, coupled with mitochondrial collinearity analysis, indicate rapid organellar genome evolution of Scaevola. Organellar-nuclear horizontal gene transfer analysis identified specific increased in the copy numbers of photosynthesis-related genes and chloroplast-nuclear transfer events in S. taccada. Our study not only provides insights for understanding environmental adaptation mechanisms of coastal plants, but also contributes to elucidating organellar genome evolution in Scaevola and Goodeniaceae.
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spelling doaj-art-216a28dade864862a0e3666e8962053d2025-08-20T02:12:35ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2025-04-011610.3389/fpls.2025.15877501587750Organelle genomes of two Scaevola species, S. taccada and S. hainanensis, provide new insights into evolutionary divergence between Scaevola and its related speciesDanni Meng0Danni Meng1Tianxin Lu2Tianxin Lu3Tianxin Lu4Meng He5Meng He6Yuze Ren7Yuze Ren8Mumei Fu9Mumei Fu10Yuxiao Zhang11Yuxiao Zhang12Peifeng Yang13Peifeng Yang14Xinyu Lin15Xinyu Lin16Yong Yang17Yong Yang18Ying Zhang19Yuchen Yang20Xiang Jin21Xiang Jin22Ministry of Education Key Laboratory for Ecology of Tropical Islands, Key Laboratory of Tropical Animal and Plant Ecology of Hainan Province, College of Life Sciences, Hainan Normal University, Haikou, ChinaHainan Observation and Research Station of Dongzhaigang Mangrove Wetland Ecosystem, Hainan Normal University, Haikou, ChinaMinistry of Education Key Laboratory for Ecology of Tropical Islands, Key Laboratory of Tropical Animal and Plant Ecology of Hainan Province, College of Life Sciences, Hainan Normal University, Haikou, ChinaHainan Observation and Research Station of Dongzhaigang Mangrove Wetland Ecosystem, Hainan Normal University, Haikou, ChinaKey Laboratory of Xinjiang Phytomedicine Resource and Utilization of Ministry of Education, Key Laboratory of Oasis Town and Mountain-Basin System Ecology of Xinjiang Production and Construction Corps, College of Life Sciences, Shihezi University, Shihezi, ChinaMinistry of Education Key Laboratory for Ecology of Tropical Islands, Key Laboratory of Tropical Animal and Plant Ecology of Hainan Province, College of Life Sciences, Hainan Normal University, Haikou, ChinaHainan Observation and Research Station of Dongzhaigang Mangrove Wetland Ecosystem, Hainan Normal University, Haikou, ChinaMinistry of Education Key Laboratory for Ecology of Tropical Islands, Key Laboratory of Tropical Animal and Plant Ecology of Hainan Province, College of Life Sciences, Hainan Normal University, Haikou, ChinaHainan Observation and Research Station of Dongzhaigang Mangrove Wetland Ecosystem, Hainan Normal University, Haikou, ChinaMinistry of Education Key Laboratory for Ecology of Tropical Islands, Key Laboratory of Tropical Animal and Plant Ecology of Hainan Province, College of Life Sciences, Hainan Normal University, Haikou, ChinaHainan Observation and Research Station of Dongzhaigang Mangrove Wetland Ecosystem, Hainan Normal University, Haikou, ChinaMinistry of Education Key Laboratory for Ecology of Tropical Islands, Key Laboratory of Tropical Animal and Plant Ecology of Hainan Province, College of Life Sciences, Hainan Normal University, Haikou, ChinaHainan Observation and Research Station of Dongzhaigang Mangrove Wetland Ecosystem, Hainan Normal University, Haikou, ChinaMinistry of Education Key Laboratory for Ecology of Tropical Islands, Key Laboratory of Tropical Animal and Plant Ecology of Hainan Province, College of Life Sciences, Hainan Normal University, Haikou, ChinaHainan Observation and Research Station of Dongzhaigang Mangrove Wetland Ecosystem, Hainan Normal University, Haikou, ChinaMinistry of Education Key Laboratory for Ecology of Tropical Islands, Key Laboratory of Tropical Animal and Plant Ecology of Hainan Province, College of Life Sciences, Hainan Normal University, Haikou, ChinaHainan Observation and Research Station of Dongzhaigang Mangrove Wetland Ecosystem, Hainan Normal University, Haikou, ChinaMinistry of Education Key Laboratory for Ecology of Tropical Islands, Key Laboratory of Tropical Animal and Plant Ecology of Hainan Province, College of Life Sciences, Hainan Normal University, Haikou, ChinaHainan Observation and Research Station of Dongzhaigang Mangrove Wetland Ecosystem, Hainan Normal University, Haikou, ChinaEngineering and Technological Research in Protection and Utilization of Mangrove Rare and Endangered Species, Lingnan Normal University, Zhanjiang, ChinaState Key Laboratory of Biocontrol, School of Ecology, Sun Yat-sen University, Shenzhen, ChinaMinistry of Education Key Laboratory for Ecology of Tropical Islands, Key Laboratory of Tropical Animal and Plant Ecology of Hainan Province, College of Life Sciences, Hainan Normal University, Haikou, ChinaHainan Observation and Research Station of Dongzhaigang Mangrove Wetland Ecosystem, Hainan Normal University, Haikou, ChinaChloroplast and mitochondrial genomes harbor crucial information that can be utilized for elucidating plant evolution and environmental adaptation. The organellar genomic characteristics of Goodeniaceae, a sister family to Asteraceae, remain unexplored. Here, using a combination of short-read and long-read sequencing technologies, we successfully assembled the complete organellar genomes of two Goodeniaceae species native to China, Scaevola taccada and S. hainanensis. Chloroplast genome collinearity analysis revealed that Scaevola expanded its genome length through inverted repeat expansion and large single copy fragment duplication, resulting in 181,022 bp (S. taccada) and 182,726 bp (S. hainanensis), ~30 kb increase compared to its related species. Mitochondrial genomes of two Scaevola species exhibit multi-ring topology, forming dual mitochondrial chromosomes of 314,251 bp (S. taccada) and 276,175 bp (S. hainanensis). Sequence variation analysis demonstrated substantial chloroplast sequence divergence (Pi = 0.45) and an increase in gene copy number within the genus. Relative synonymous codon usage (RSCU) analysis revealed that Scaevola chloroplast has a higher bias for A/U-ending codons than mitochondria, with chloroplasts RSCU values ranging from 0.32 to 1.94, whereas mitochondrial RSCU values ranging from 0.38 to 1.62. Phylogenetic analyses support the monophyly of the Asteraceae-Goodeniaceae sister group, whereas the extended evolutionary branches of Scaevola, coupled with mitochondrial collinearity analysis, indicate rapid organellar genome evolution of Scaevola. Organellar-nuclear horizontal gene transfer analysis identified specific increased in the copy numbers of photosynthesis-related genes and chloroplast-nuclear transfer events in S. taccada. Our study not only provides insights for understanding environmental adaptation mechanisms of coastal plants, but also contributes to elucidating organellar genome evolution in Scaevola and Goodeniaceae.https://www.frontiersin.org/articles/10.3389/fpls.2025.1587750/fullorganelle genomesScaevolaGoodeniaceaeAsteraceaeevolutionary divergence
spellingShingle Danni Meng
Danni Meng
Tianxin Lu
Tianxin Lu
Tianxin Lu
Meng He
Meng He
Yuze Ren
Yuze Ren
Mumei Fu
Mumei Fu
Yuxiao Zhang
Yuxiao Zhang
Peifeng Yang
Peifeng Yang
Xinyu Lin
Xinyu Lin
Yong Yang
Yong Yang
Ying Zhang
Yuchen Yang
Xiang Jin
Xiang Jin
Organelle genomes of two Scaevola species, S. taccada and S. hainanensis, provide new insights into evolutionary divergence between Scaevola and its related species
Frontiers in Plant Science
organelle genomes
Scaevola
Goodeniaceae
Asteraceae
evolutionary divergence
title Organelle genomes of two Scaevola species, S. taccada and S. hainanensis, provide new insights into evolutionary divergence between Scaevola and its related species
title_full Organelle genomes of two Scaevola species, S. taccada and S. hainanensis, provide new insights into evolutionary divergence between Scaevola and its related species
title_fullStr Organelle genomes of two Scaevola species, S. taccada and S. hainanensis, provide new insights into evolutionary divergence between Scaevola and its related species
title_full_unstemmed Organelle genomes of two Scaevola species, S. taccada and S. hainanensis, provide new insights into evolutionary divergence between Scaevola and its related species
title_short Organelle genomes of two Scaevola species, S. taccada and S. hainanensis, provide new insights into evolutionary divergence between Scaevola and its related species
title_sort organelle genomes of two scaevola species s taccada and s hainanensis provide new insights into evolutionary divergence between scaevola and its related species
topic organelle genomes
Scaevola
Goodeniaceae
Asteraceae
evolutionary divergence
url https://www.frontiersin.org/articles/10.3389/fpls.2025.1587750/full
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