Construction of Ancestral Chromosomes in Gymnosperms and the Application in Comparative Genomic Analysis

Abstract

Chromosome rearrangements during plant evolution can lead to alterations in genome structure and gene function, thereby influencing species adaptation and evolutionary processes. Gymnosperms, as an ancient group of plants, offer valuable insights into the morphological, physiological, and ecological characteristics of early terrestrial flora. The reconstruction of ancestral karyotypes in gymnosperms may provide critical clues for understanding their evolutionary history. In this study, we inferred the ancestral gymnosperm karyotype (AGK), which comprises 12 chromosomes, and conducted a collinearity analysis with existing gymnosperm genomes. Our findings indicate that chromosome numbers have remained remarkably stable throughout the evolution of gymnosperms. For species with multiplied chromosome numbers, such as gnetophytes, weak collinearities with the AGK were observed. Comparisons between the AGK and gnetophyte genomes revealed a biased pattern regarding retained duplication blocks. Furthermore, our analysis of transposable elements in Welwitschia mirabilis identified enriched regions containing LINE-1 retrotransposons within the syntenic blocks. Syntenic analysis between the AGK and angiosperms also demonstrated a biased distribution across chromosomes. These results provide a fundamental resource for further characterization of chromosomal evolution in gymnosperms.

Keywords: LINE-1; ancestral karyotype; chromosome stability; collinearity; gymnosperm.

Figure 1

Inference of the ancestral chromosomes in gymnosperms. Collinearity blocks between pairs of gymnosperm species were identified to construct proto-chromosomes of AGK1 to AGK12, such as (A) AGK1, AGK2, and AGK10 from G. biloba (Gbil) vs. P. tabulaeformis (Ptab). (B) AGK11, AGK6, and AGK12 from G. biloba (Gbil) vs. C. panzhihuaensis (Cpan). (C) AGK5 from G. biloba (Gbil) vs. C. panzhihuaensis (Cpan) and P. tabulaeformis (Ptab). (D) AGK8 from G. biloba (Gbil) vs. C. panzhihuaensis (Cpan) and P. tabulaeformis (Ptab). (E) AGK9 from G. biloba (Gbil) vs. C. panzhihuaensis (Cpan) and T. grandis (Tgra). AGK3, AGK4, and AGK7 from G. biloba (Gbil) vs. M. glyptostroboides (Mgly) (F) and P. tabulaeformis (Ptab) (G). AGK1 to AGK12: the inferred gymnosperm proto-chromosomes were color-coded with 12 distinct colors to differentiate the chromosomes (SteelBlue, ForestGreen, GoldEnrod, OrangeRed, Crimson, DarkOrchid, Tan, IndianRed, OliveDrab, DarkTurquoise, LightSteelBlue, and SlateGray). Numbers with circular symbols represented ancestral chromosomes, and boxes of dotted lines were used to represent blocks involved in the construction of ancestral chromosomes.

Figure 2

Karyotype projection of 10 extant gymnosperms based on AGK. The colors of the 12 proto-chromosomes are the same as in Figure 1. Whole-genome duplication events are represented by a red pentagram. The karyotypes of ancestral chromosomes in modern plant genomes are shown at the branches. The numbers of genes and chromosomes are exhibited for each species.

Figure 3

Synteny analysis of AGK and genomes of gymnosperm species. (A): Syntenic plot illustrating the relationship between AGK and various gymnosperms with differing chromosome numbers. The gray lines show collinear blocks. (B–E): Karyotype projection of four species genomes based on AGK, including T. grandis (B), T. yunnanensis (C), W. mirabilis (D), and G. montanum (E). Boxes with black dashed lines represent syntenic blocks that may have resulted from whole-genome duplication events. The colors of the 12 proto-chromosomes are the same as in Figure 1.

Figure 4

Distribution statistics of evolutionarily conserved syntenic blocks in the genomes of S. sempervirens (Ssem), G. montanum (Gmon), and W. mirabilis (Wmir) across the arms of the AGK chromosome.

Figure 5

Comparative analysis of W. mirabilis and P. tabuliformis within the conserved syntenic block on AGK7R, AGK9R, AGK11R, and AGK12L. (A) Collinearity analysis of W. mirabilis and P. tabuliformis in the conserved syntenic block on AGK7R, AGK9R, AGK11R, and AGK12L. Orange font represents the chromosomes of the species, purple font represents the chromosome arms of AGK, and black font represents the position of the block on the chromosome. (B) Transposable element statistics of W. mirabilis and P. tabuliformis in the conserved syntenic block on AGK7R, AGK9R, AGK11R, and AGK12L.

Figure 6

Distribution statistics of the synteny blocks on the arms of the AGK chromosome in A. trichopoda (A), N. colorata (B), P. trichocarpa (C), V. vinifera (D), O. sativa (E), and Z. mays (F), respectively. Blue bars represent the expected numbers of synteny blocks calculated according to the lengths of chromosomes, and red bars represent the actual number of synteny blocks presented on the chromosome arms.