Strong plastid degradation is consistent within section Chondrophyllae, the most speciose lineage of Gentiana

Abstract

Recovering phylogenetic relationships in lineages experiencing intense diversification has always been a persistent challenge in evolutionary studies, including in Gentiana section Chondrophyllae sensu lato (s.l.). Indeed, this subcosmopolitan taxon encompasses more than 180 mostly annual species distributed around the world. We sequenced and assembled 22 new plastomes representing 21 species in section Chondrophyllae s.l. In addition to previously released plastome data, our study includes all main lineages within the section. We reconstructed their phylogenetic relationships based on protein‐coding genes and recombinant DNA (rDNA) cistron sequences, and then investigated plastome structural evolution as well as divergence time. Despite an admittedly humble species cover overall, we recovered a well‐supported phylogenetic tree based on plastome data, and found significant discordance between phylogenetic relationships and taxonomic treatments. Our results show that G. capitata and G. leucomelaena diverged early within the section, which is then further divided into two clades. The divergence time estimation showed that section Chondrophyllae s.l. evolved in the second half of the Oligocene. We found that section Chondrophyllae s.l. had the smallest average plastome size (128 KB) in tribe Gentianeae (Gentianaceae), with frequent gene and sequence losses such as the ndh complex and its flanking regions. In addition, we detected both expansion and contraction of the inverted repeat (IR) regions. Our study suggests that plastome degradation parallels the diversification of this group, and illustrates the strong discordance between phylogenetic relationships and taxonomic treatments, which now need to be carefully revised.

Cryptic diversity and rampant hybridization in annual gentians on the Qinghai-Tibet Plateau revealed by population genomic analysis

“…Growing evidence from both population genetics and phylogenetics suggests that hybridization might be more pervasive than previously believed in this species-rich genus Gentiana , which has received increased attention. Hybridization was observed in nearly every taxon examined, for example, ancient hybridization in the sections Ciminalis ( Christe et al., 2014 ), Cruciata ( Fu et al., 2021a ), and Chondrophyllae ( Chen et al., 2021 ; Fu et al., 2022c ), and recent hybridization in the sections Cruciata ( Hu et al., 2016 ), Kudoa ( Fu et al., 2020 , 2022a ), and Isomeria ( Sun et al., 2022 ). Compared with rapidly growing cases of hybridization within the genus, reports of ancient hybridization among genera or lineages are scarce.…”

“…is the only section that is globally distributed, which has 182 species and accounts for 51.7% of all Gentiana species ( Ho and Liu, 2001 ; Favre et al., 2020 ). This section has experienced rapid evolution ( Yuan and Küpfer, 1997 ) and presented extremely long branches in the phylogenetic trees ( Favre et al., 2020 ; Chen et al., 2021 ; Fu et al., 2021b , 2022c ). However, the reasons underlying the rich diversity in this section are yet unclear.…”

“…Additionally, section Chondrophyllae s.l. is a well-supported monophyletic group, but the intra-sectional relationship is ambiguous as a result of rich cyto-nuclear conflicts ( Chen et al., 2021 ; Fu et al., 2022c ). Therefore, hybridization is assumed to be rampant in this section and has been essential in the assembly of biodiversity, although there is little direct evidence.…”

The dynamic history of plastome structure across aquatic subclass Alismatidae

“…1 ). Therefore, it seems reasonable to assume that the loss/pseudogenization of ndh genes is associated with the IR extraction/expansion, as has been suggested in Gentianaceae [ 22 ], Orobanchaceae [ 16 ], and Polygonaceae [ 19 ].…”

“…As well, SVs in plastomes may be associated with IR expansion/contraction, which in turn affects the plastome size [ 9 ]. The studies of Fu et al [ 22 , 23 ] revealed frequent gene loss (i.e., ndh complex) and plastome degradation in the genus Gentiana , which was suggested to parallel the diversification in this group. In Alismatidae, Ross et al [ 24 ] found that the independent loss of the ndh complex in three families (Hydrocharitaceae, Cymodoceaceae, and Posidoniaceae) of Alismatidae may be associated with changes in plastome sizes [e.g., Thalassia hemprichii (loss of ndh complex; 178,261 bp) vs. Zostera marina (keep ndh complex; 143,877 bp)].…”