Chloroplast Pan-Genomes and Comparative Transcriptomics Reveal Genetic Variation and Temperature Adaptation in the Cucumber
Although whole genome sequencing, genetic variation mapping, and pan-genome studies have been done on a large group of cucumber nuclear genomes, organelle genome information is largely unclear. As an important component of the organelle genome, the chloroplast genome is highly conserved, which makes...
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MDPI AG
2023-05-01
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| Series: | International Journal of Molecular Sciences |
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| author | Lei Xia Han Wang Xiaokun Zhao Hesbon Ochieng Obel Xiaqing Yu Qunfeng Lou Jinfeng Chen Chunyan Cheng |
| author_facet | Lei Xia Han Wang Xiaokun Zhao Hesbon Ochieng Obel Xiaqing Yu Qunfeng Lou Jinfeng Chen Chunyan Cheng |
| author_sort | Lei Xia |
| collection | DOAJ |
| description | Although whole genome sequencing, genetic variation mapping, and pan-genome studies have been done on a large group of cucumber nuclear genomes, organelle genome information is largely unclear. As an important component of the organelle genome, the chloroplast genome is highly conserved, which makes it a useful tool for studying plant phylogeny, crop domestication, and species adaptation. Here, we have constructed the first cucumber chloroplast pan-genome based on 121 cucumber germplasms, and investigated the genetic variations of the cucumber chloroplast genome through comparative genomic, phylogenetic, haplotype, and population genetic structure analysis. Meanwhile, we explored the changes in expression of cucumber chloroplast genes under high- and low-temperature stimulation via transcriptome analysis. As a result, a total of 50 complete chloroplast genomes were successfully assembled from 121 cucumber resequencing data, ranging in size from 156,616–157,641 bp. The 50 cucumber chloroplast genomes have typical quadripartite structures, consisting of a large single copy (LSC, 86,339–86,883 bp), a small single copy (SSC, 18,069–18,363 bp), and two inverted repeats (IRs, 25,166–25,797 bp). Comparative genomic, haplotype, and population genetic structure results showed that there is more genetic variation in Indian ecotype cucumbers compared to other cucumber cultivars, which means that many genetic resources remain to be explored in Indian ecotype cucumbers. Phylogenetic analysis showed that the 50 cucumber germplasms could be classified into 3 types: East Asian, Eurasian + Indian, and Xishuangbanna + Indian. The transcriptomic analysis showed that <i>matK</i> were significantly up-regulated under high- and low-temperature stresses, further demonstrating that cucumber chloroplasts respond to temperature adversity by regulating lipid metabolism and ribosome metabolism. Further, <i>accD</i> has higher editing efficiency under high-temperature stress, which may contribute to the heat tolerance. These studies provide useful insight into genetic variation in the chloroplast genome, and established the foundation for exploring the mechanisms of temperature-stimulated chloroplast adaptation. |
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| language | English |
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| spelling | doaj.art-c41aa9c75cbc4415af1ead2b3fdf1e7f2023-11-18T01:44:37ZengMDPI AGInternational Journal of Molecular Sciences1661-65961422-00672023-05-012410894310.3390/ijms24108943Chloroplast Pan-Genomes and Comparative Transcriptomics Reveal Genetic Variation and Temperature Adaptation in the CucumberLei Xia0Han Wang1Xiaokun Zhao2Hesbon Ochieng Obel3Xiaqing Yu4Qunfeng Lou5Jinfeng Chen6Chunyan Cheng7National Key Laboratory of Crop Genetics & Germplasm Enhancement and Utilization, College of Horticulture, Nanjing Agricultural University, Nanjing 210095, ChinaNational Key Laboratory of Crop Genetics & Germplasm Enhancement and Utilization, College of Horticulture, Nanjing Agricultural University, Nanjing 210095, ChinaNational Key Laboratory of Crop Genetics & Germplasm Enhancement and Utilization, College of Horticulture, Nanjing Agricultural University, Nanjing 210095, ChinaNational Key Laboratory of Crop Genetics & Germplasm Enhancement and Utilization, College of Horticulture, Nanjing Agricultural University, Nanjing 210095, ChinaNational Key Laboratory of Crop Genetics & Germplasm Enhancement and Utilization, College of Horticulture, Nanjing Agricultural University, Nanjing 210095, ChinaNational Key Laboratory of Crop Genetics & Germplasm Enhancement and Utilization, College of Horticulture, Nanjing Agricultural University, Nanjing 210095, ChinaNational Key Laboratory of Crop Genetics & Germplasm Enhancement and Utilization, College of Horticulture, Nanjing Agricultural University, Nanjing 210095, ChinaNational Key Laboratory of Crop Genetics & Germplasm Enhancement and Utilization, College of Horticulture, Nanjing Agricultural University, Nanjing 210095, ChinaAlthough whole genome sequencing, genetic variation mapping, and pan-genome studies have been done on a large group of cucumber nuclear genomes, organelle genome information is largely unclear. As an important component of the organelle genome, the chloroplast genome is highly conserved, which makes it a useful tool for studying plant phylogeny, crop domestication, and species adaptation. Here, we have constructed the first cucumber chloroplast pan-genome based on 121 cucumber germplasms, and investigated the genetic variations of the cucumber chloroplast genome through comparative genomic, phylogenetic, haplotype, and population genetic structure analysis. Meanwhile, we explored the changes in expression of cucumber chloroplast genes under high- and low-temperature stimulation via transcriptome analysis. As a result, a total of 50 complete chloroplast genomes were successfully assembled from 121 cucumber resequencing data, ranging in size from 156,616–157,641 bp. The 50 cucumber chloroplast genomes have typical quadripartite structures, consisting of a large single copy (LSC, 86,339–86,883 bp), a small single copy (SSC, 18,069–18,363 bp), and two inverted repeats (IRs, 25,166–25,797 bp). Comparative genomic, haplotype, and population genetic structure results showed that there is more genetic variation in Indian ecotype cucumbers compared to other cucumber cultivars, which means that many genetic resources remain to be explored in Indian ecotype cucumbers. Phylogenetic analysis showed that the 50 cucumber germplasms could be classified into 3 types: East Asian, Eurasian + Indian, and Xishuangbanna + Indian. The transcriptomic analysis showed that <i>matK</i> were significantly up-regulated under high- and low-temperature stresses, further demonstrating that cucumber chloroplasts respond to temperature adversity by regulating lipid metabolism and ribosome metabolism. Further, <i>accD</i> has higher editing efficiency under high-temperature stress, which may contribute to the heat tolerance. These studies provide useful insight into genetic variation in the chloroplast genome, and established the foundation for exploring the mechanisms of temperature-stimulated chloroplast adaptation.https://www.mdpi.com/1422-0067/24/10/8943chloroplast pan-genomecucumbergenetic variationRNA editing efficiencytemperature adversity |
| spellingShingle | Lei Xia Han Wang Xiaokun Zhao Hesbon Ochieng Obel Xiaqing Yu Qunfeng Lou Jinfeng Chen Chunyan Cheng Chloroplast Pan-Genomes and Comparative Transcriptomics Reveal Genetic Variation and Temperature Adaptation in the Cucumber International Journal of Molecular Sciences chloroplast pan-genome cucumber genetic variation RNA editing efficiency temperature adversity |
| title | Chloroplast Pan-Genomes and Comparative Transcriptomics Reveal Genetic Variation and Temperature Adaptation in the Cucumber |
| title_full | Chloroplast Pan-Genomes and Comparative Transcriptomics Reveal Genetic Variation and Temperature Adaptation in the Cucumber |
| title_fullStr | Chloroplast Pan-Genomes and Comparative Transcriptomics Reveal Genetic Variation and Temperature Adaptation in the Cucumber |
| title_full_unstemmed | Chloroplast Pan-Genomes and Comparative Transcriptomics Reveal Genetic Variation and Temperature Adaptation in the Cucumber |
| title_short | Chloroplast Pan-Genomes and Comparative Transcriptomics Reveal Genetic Variation and Temperature Adaptation in the Cucumber |
| title_sort | chloroplast pan genomes and comparative transcriptomics reveal genetic variation and temperature adaptation in the cucumber |
| topic | chloroplast pan-genome cucumber genetic variation RNA editing efficiency temperature adversity |
| url | https://www.mdpi.com/1422-0067/24/10/8943 |
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