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. 2023 Dec 1;23(1):608.
doi: 10.1186/s12870-023-04634-9.

GC heterogeneity reveals sequence-structures evolution of angiosperm ITS2

Yubo Liu #  1   2 , Nan Liang #  1   3 , Qing Xian  1 , Wei Zhang  4
Affiliations

GC heterogeneity reveals sequence-structures evolution of angiosperm ITS2

Yubo Liu et al. BMC Plant Biol. .

Abstract

Background: Despite GC variation constitutes a fundamental element of genome and species diversity, the precise mechanisms driving it remain unclear. The abundant sequence data available for the ITS2, a commonly employed phylogenetic marker in plants, offers an exceptional resource for exploring the GC variation across angiosperms.

Results: A comprehensive selection of 8666 species, comprising 165 genera, 63 families, and 30 orders were used for the analyses. The alignment of ITS2 sequence-structures and partitioning of secondary structures into paired and unpaired regions were performed using 4SALE. Substitution rates and frequencies among GC base-pairs in the paired regions of ITS2 were calculated using RNA-specific models in the PHASE package. The results showed that the distribution of ITS2 GC contents on the angiosperm phylogeny was heterogeneous, but their increase was generally associated with ITS2 sequence homogenization, thereby supporting the occurrence of GC-biased gene conversion (gBGC) during the concerted evolution of ITS2. Additionally, the GC content in the paired regions of the ITS2 secondary structure was significantly higher than that of the unpaired regions, indicating the selection of GC for thermodynamic stability. Furthermore, the RNA substitution models demonstrated that base-pair transformations favored both the elevation and fixation of GC in the paired regions, providing further support for gBGC.

Conclusions: Our findings highlight the significance of secondary structure in GC investigation, which demonstrate that both gBGC and structure-based selection are influential factors driving angiosperm ITS2 GC content.

Keywords: GC-biased gene conversion; ITS2 content; Secondary structure; Thermodynamic stability.

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Conflict of interest statement

The authors declare that they have no competing interests.

Figures

Fig. 1
Fig. 1
Variation of ITS2 GC content across the 165 angiosperm phylogeny. The three dotted-line circles outside the circular tree represent the GC content intervals, in which the GC boxplots are added behind their generic names. The phylogeny was constructed by using the NCBI taxonomy, which is based on the APG system. The main orders are highlighted with color blocks. The mean ITS2 GC content of each order is indicated by a pink line, and the width of the line represents the 95% confidence interval
Fig. 2
Fig. 2
Distribution and variation of ITS2 GC contents among angiosperms. A Histogram of ITS2 GC contents across 165 sampled genera showing a normal distribution. B a scatter plot illustrating the correlation between ITS2 GC contents and the GC contents at the third codon position of the expressed sequence tags (EST-GC3) among 107 representative genera of Eudicots, Poaceae and the non-Poaceae monocots. Each data point represents the average GC value of a genus
Fig. 3
Fig. 3
GC distribution in ITS2 secondary structure. A An example of the ITS2 consensus secondary structure from genus Aegilops (family Poaceae). The four stems are labelled I–IV. The characteristic bulge in stem II, and the UGGU in stem III that are common to nearly all angiosperms, are indicated in red. Degree of conservation over the entire sequences is displayed using color grades ranging from green (conservative) to red (variable). B ITS2 sequence logo of the genus Aegilops is used to visualize the base composition in different sequence-structure partitions. The overall height of the letter stack in each position indicates the sequence conservation (measured in bits), while the height of letter within the stack represents the relative frequency of the bases at that position. C The statistics of GC contents and G-C base pair frequency in ITS2 sequence-structure partitions among the 165 investigated genera
Fig. 4
Fig. 4
Correlations between the current and the equilibrium GC content (frequency) among 165 ITS2 sequence structures. Each data point represents the average GC value or G-C frequency of a genus
Fig. 5
Fig. 5
Correlations between the average number of nucleotide differences (K) and GC content (G-C frequency) among 165 ITS2 sequence-structure matrices. Each data point represents the average GC value or G-C frequency for a single genus. The regression line was calculated using Pearson’s correlation, with the error bands represent 95% confidence intervals based on a binomial model. A Comparison of the GC content and the K value for the entire ITS2 sequence. B Comparison of the GC content and the K value for the ITS2 paired regions. C Comparison of the G-C frequency and the K value for the ITS2 paired regions. D Comparison of the GC content and the K value for the ITS2 unpaired regions
Fig. 6
Fig. 6
Comparison of base-pair transformations to GC and AU in ITS2 transition-rate matrices using the best-fit RNA substitution models. The transition rate for each matrix was normalized to an average substitution rate of 1.0. A-D Base-pair transformations derived from the initial states of 142 ITS2 transition-rate matrices, A,B The relative rates of the six possible transformations to GC and AU, respectively. C Comparison of the total formation rates for GC and AU base pairs. D Scatter plot showing the frequency-mutability relationship of formation rates for GC and AU base pairs, indicating an increased fixation of GC with GC enrichment. E-H base-pair transformations derived from the equilibrium states of 46 ITS2 transition-rate matrices. E,F The relative rates of the six possible transformations to GC and AU, respectively. G Comparison of the total formation rates for GC and AU base pairs. H Scatter plot illustrating the frequency-mutability relationship of formation rates for GC and AU base pairs, indicating an increased fixation of GC with GC enrichment
Fig. 7
Fig. 7
Mismatch base-pair transformation in meiotic recombination. A A schematic representation of gene conversion during meiotic recombination. The double-strand always break during meiosis, and a heteroduplex formed when the single-stranded DNA invades the homologous sequence, enabling the repair of up to four possible mismatches by altering one side of the nucleotides. B,C Comparison of mismatch base-pair transformations in both (B) initial and (C) equilibrium states reveals a GC-biased gene conversion
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References

    1. Sriaporn C, Campbell KA, Van Kranendonk MJ, Handley KM. Genomic adaptations enabling Acidithiobacillus distribution across wide-ranging hot spring temperatures and pHs. Microbiome. 2021;9:135. doi: 10.1186/s40168-021-01090-1. - DOI - PMC - PubMed
    1. Hu EZ, Lan XR, Liu ZL, Gao J, Niu DK. A positive correlation between GC content and growth temperature in prokaryotes. BMC Genomics. 2022;23:1–17. doi: 10.1186/s12864-022-08353-7. - DOI - PMC - PubMed
    1. Smarda P, Bures P, Horova L, Leitch IJ, Mucina L, Pacini E, et al. Ecological and evolutionary significance of genomic GC content diversity in monocots. Proc Natl Acad Sci USA. 2014;111:E4096–102. doi: 10.1073/pnas.1321152111. - DOI - PMC - PubMed
    1. Bernardi G, Olofsson B, Filipski J, Zerial M, Salinas J, Cuny G, et al. The mosaic genome of warm-blooded vertebrates. Science. 1985;228:953–8. doi: 10.1126/science.4001930. - DOI - PubMed
    1. Costantini M, Cammarano R, Bernardi G. The evolution of isochore patterns in vertebrate genomes. BMC Genomics. 2009;10:146. doi: 10.1186/1471-2164-10-146. - DOI - PMC - PubMed

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