Genome Sequencing of the Endangered Kingdonia uniflora (Circaeasteraceae, Ranunculales) Reveals Potential Mechanisms of Evolutionary Specialization

Abstract

Kingdonia uniflora, an alpine herb, has an extremely narrow distribution and represents a model for studying evolutionary mechanisms of species that have adapted to undisturbed environments for evolutionarily long periods of time. We assembled a 1,004.7-Mb draft genome (encoding 43,301 genes) of K. uniflora and found significant overrepresentation in gene families associated with DNA repair, underrepresentation in gene families associated with stress response, and loss of most plastid ndh genes. During the evolutionary process, the overrepresentation of gene families involved in DNA repair could help asexual K. uniflora reduce the accumulation of deleterious mutations, while reducing genetic diversity, which is important in responding to environment fluctuations. The underrepresentation of gene families related to stress response and functional loss of ndh genes could be due to lack or loss of ability to respond to environmental changes caused by long-term adaptation to a relatively stable ecological environment.

Lineage‐specific plastid degradation in subtribe Gentianinae (Gentianaceae)

“…The ndh complex is essential for electron cycling around photosystem I under heat‐stressed conditions, but is less important under cold‐stressed conditions (Wang et al., 2006). In addition, the loss of ndh genes in the plastome is also assumed to be related to dry and light‐intensive habitats in Selaginella (Xu et al., 2018; Zhang et al., 2019), or similar habitats in Kingdonia (Sun et al., 2020). In contrast, it remains challenging to identify an associated habitat characteristic explaining gene losses in Gentiana .…”

Genomic insights into adaptation to heterogeneous environments for the ancient relictual Circaeaster agrestis (Circaeasteraceae, Ranunculales)

“…Our molecular dating based on plastome sequences suggested an early Eocene origin of C . agrestis , which is in accord with previous estimates (Ruiz‐Sanchez et al ., 2012) and recent results from nuclear data (Sun et al ., 2020). The diversification of C .…”

“…A recent study charactering the genome of Kingdonia uniflora (sister to C. agrestis) calculated the nucleotide substitution rate of 1.4 9 10 À9 per site per year (Sun et al, 2020), which is comparatively lower than an estimate of Arabidopsis thaliana (7.0 9 10 À9 ) (Ossowski et al, 2010) and indirect estimates based on the divergence between monocots and dicots (5.8-8.1 9 10 À9 ) (Wolfe et al, 1987). The low nucleotide substitution rate may contribute to low speciation rate (Webster et al, 2003), a possible reason for the paucity of species in the family and the low morphological diversity of C. agrestis and K. uniflora.…”

On the Edge of Dispensability, the Chloroplast ndh Genes

“…However, extensive research using plant species lacking ndh genes is required to confirm the selective advantages provided by the Ndh complex. In this line of research, Sun et al [79] reported intense variability and loss of ndh genes in the critically endangered Kingdonia uniflora. Similarly, Folk et al [80] found intense pseudogenization and loss of ndh genes in the semi-aquatic plant Saniculiphyllum guangxiense, which contrasts with the strong conservatism of the plastid genes in other Saxifragales.…”

“…Angiosperms that have lost plastid ndh genes survive in mild and moderate stress environments or adopt a heterotrophic or carnivorous metabolism that compensates for their low or absent photosynthetic efficiency. Variable environments along the scale time of biological evolution place Angiosperms without ndh at permanent risk of extinction, as may be occurring with the endangered Kingdonia uniflora [79]. Consequently, phylogenetic analyses indicate that Angiosperm species lacking plastid ndh genes lost them recently (typically less than 10 Mya).…”