The chromosome-level genome of the submerged plant Cryptocoryne crispatula provides insights into the terrestrial-freshwater transition in Araceae

Abstract

Plant terrestrialization (i.e. the transition to a terrestrial environment) is a significant evolutionary event that has been intensively studied. While certain plant lineages, particularly in angiosperms, have re-adapted to freshwater habitats after colonizing terrene, however, the molecular mechanism of the terrestrial-freshwater (T-F) transition remains limited. Here, the basal monocot Araceae was selected as the study object to explore the T-F transition adaptation mechanism by comparative genomic analysis. Our findings revealed that the substitution rates significantly increased in the lineage of freshwater Araceae, which may promote their adaptation to the freshwater habitat. Additionally, 20 gene sets across all four freshwater species displayed signs of positive selection contributing to tissue development and defense responses in freshwater plants. Comparative synteny analysis showed that genes specific to submerged plants were enriched in cellular respiration and photosynthesis. In contrast, floating plants were involved in regulating gene expression, suggesting that gene and genome duplications may provide the original material for plants to adapt to the freshwater environment. Our study provides valuable insights into the genomic aspects of the transition from terrestrial to aquatic environments in Araceae, laying the groundwork for future research in the angiosperm.

Keywords: Cryptocoryne crispatula; adaptation; genomic synteny; mutation rates; terrestrial–freshwater transition.

Figure 1.

An overview of genomic features Cryptocoryne crispatula genome. (a) Chromosome length; (b) GC content; (c) gene density; (d) repeat coverage; (e) LTR-Gypsy density; (g) LTR-Copia density; (g) syntenic blocks. The window size used in the circles was 200 kb.

Figure 2.

Gene family analysis. (A) Phylogenetic tree showing divergence times and the evolution of gene families in freshwater Araceae. The estimated divergence times (million years ago, Mya) are shown at each node. Expansion and contraction of gene families are denoted as numbers with green and red, respectively. (B) Bar plot showing gene number identified by OrthorFinder. Unassigned genes: a gene that has not been assigned any orthogroup, i.e. singleton genes that have no orthologs in other species and no copy genes within a species. (C) Venn diagram showing the expanded gene families among four freshwater plants. (D) Venn diagram showing the contracted gene families among four freshwater plants.

Figure 3.

Comparative analysis of evolutionary rates between freshwater and terrestrial plants. (A) A maximum-likelihood tree was inferred using IQ-TREE, with A. tatarinowii as an outgroup. The number on the branch represents the branch length information. (B) We applied the free-ratio model to calculate dN, dS, and dN/dS separately for each species. The dotted line of the box plot means the average value. P-value is from Wilcoxon signed ranks test (***P < 0.001).

Figure 4.

Hierarchical clustering of synteny genes in Araceae. (A) 16,147 synteny network clusters were identified in seven Araceae plants. (B) 70 freshwater plant-specific synteny clusters were identified in seven species. (C) 784 submerged plant-specific synteny clusters and 479 floating plant-specific synteny were identified in seven species, respectively. (D) Significantly enriched biological process top 25 GO terms of specific synteny clusters in submerged plant genomes. (E) Top 20 of KEGG enrichment of specific synteny clusters in submerged plant genomes. (F) Significantly enriched biological process top 25 GO terms of specific synteny clusters in floating plant genomes. (G) Top 20 of KEGG enrichment of specific synteny clusters in floating plant genomes.