The Malvaceae family is economically significant, comprising 243 genera and 4225 identified species, including cotton (Gossypium spp.), cacao (Theobroma spp.), and durian (Durio spp.) (Wang et al., 2020). The family consists of nine subfamilies, the Sterculioideae, Malvoideae, Brownlowioideae, Grewioideae, Bombacoideae, Byttnerioideae, Tilioideae, Helicteroideae, and Dombeyoideae (Group et al., 2016). In the last decade, several genomes have been assembled for Malvaceae species, including jute (Islam et al., 2017; Zhang et al., 2021), Theobroma cacao (Argout et al., 2011, 2017), cotton (Wen et al., 2023), Durio zibethinus (Teh et al., 2017), Bombax ceiba (Gao et al., 2018), and Ceiba pentandra (Shao et al., 2024). However, the genomes of the Sterculioideae remain unsequenced, and the genomic-level evolutionary relationships of the Sterculioideae with other subfamilies remain unclear.

Species within the Malvaceae family show a wide range of genome sizes, from 234 Mb to 2676 Mb (Yang et al., 2022), an 11-fold difference at the extremes. Genome size variation may be attributed to polyploidization (Gerstein and Otto, 2009), which can generate diverse phenotypic innovations within populations and potentially drive long-term evolutionary paths (Otto and Whitton, 2000). Amplification of transposable elements (TEs) is also a significant influence on genome size (Wendel et al., 2016; Neale et al., 2017). Indeed, TEs may explain large differences in genome size among species that share a polyploidization event, as documented in studies on flowering plants (Bennetzen, 2002), conifers (Nystedt et al., 2013), and salamanders (Nowoshilow et al., 2018). Recently, the “accordion” model has been proposed which integrates the correlation between the expansion of genomic DNA via repeat elements and its reduction through their deletion, particularly of long terminal repeat retrotransposons (LTR-RTs), which are class I TEs (Kidwell, 2002). This model has been applied to the study of genome size variation mechanisms in squamates (Pasquesi et al., 2018), birds, and mammals (Kapusta et al., 2017). However, research on the relationship between polyploidization events, TE content, DNA variation, and genome size changes has not yet been conducted in the Malvaceae family. Consequently, the evolutionary mechanisms underlying genome size in this plant family remain unclear.

Firmiana, a genus in the Sterculioideae subfamily, comprises 12–18 species globally (Chen et al., 2015), with 9 species found in China, five of which are endemic with restricted distribution ranges (Lu and Luo, 2022). Among these species, F. hainanensis holds the southernmost distribution (Fig. 1A), exclusively inhabiting the mountainous areas of central and southern Hainan. The species is of considerable economic and medicinal value; it serves as raw material for papermaking, ropes, and furniture and contains anti-cancer active factors, syringic aldehyde, and scopoletin. F. hainanensis has maintained a long-standing status as a globally vulnerable species, categorized as Near Threatened (The IUCN Red List of Threatened Species) and as a second-class protected plant in China (Information System of Chinese Rare and Endangered Plants, ISCREP). Furthermore, nearly all other species of the Firmiana genus are officially listed as second-class protected plants in China. However, genome resources for this genus are extremely limited.

Here, we present a chromosome-scale genome assembly for F. hainanensis based on PacBio HiFi and Hi-C data. We further performed comparative analyses of the F. hainanensis genome and those of eight other species, covering six subfamilies, enhancing our understanding of the evolutionary relationships within the Malvaceae. Additionally, we conducted a comprehensive identification and comparison of polyploidy events. We infer that F. hainanensis underwent a species-specific whole-genome duplication (WGD) event following the γ event. Using the published ancestral karyotype with 11 proto-chromosomes (Sun et al., 2024), we reconstructed the evolutionary trajectory of F. hainanensis chromosomes and found that fissions and fusions may have been crucial drivers of chromosome number variation. Next, we explored the evolutionary mechanisms of genome size in Malvaceae, focusing on polyploidization events, TE content, and DNA variation and species-specific TE subfamily proliferation. We found the quantitative abundance of Tekay transposable elements, part of the Gypsy family, to differ significantly between large and small genomes. Finally, through comparative genomic analyses, gene family expansion and contraction analyses, and gene mining, we extended our awareness of the genetic foundations of cell wall biosynthesis and wood density in Malvaceae species.