The distinct plastid genome structure of Maackia fauriei (Fabaceae: Papilionoideae) and its systematic implications for genistoids and tribe Sophoreae

Abstract

Traditionally, the tribe Sophoreae sensu lato has been considered a basal but also heterogeneous taxonomic group of the papilionoid legumes. Phylogenetic studies have placed Sophoreae sensu stricto (s.s.) as a member of the core genistoids. The recently suggested new circumscription of this tribe involved the removal of traditional members and the inclusion of Euchresteae and Thermopsideae. Nonetheless, definitions and inter- and intra-taxonomic issues of Sophoreae remain unclear. Within the field of legume systematics, the molecular characteristics of a plastid genome (plastome) have an important role in helping to define taxonomic groups. Here, we examined the plastome of Maackia fauriei, belonging to Sophoreae s.s., to elucidate the molecular characteristics of Sophoreae. Its gene contents are similar to the plastomes of other typical legumes. Putative pseudogene rps16 of Maackia and Lupinus species imply independent functional gene loss from the genistoids. Our overall examination of that loss among legumes suggests that it is common among all major clades of Papilionoideae. The M. fauriei plastome has a novel 24-kb inversion in its large single copy region, as well as previously recognized 50-kb and 36-kb inversions. The 36-kb inversion is shared by the core genistoids. The 24-kb inversion is present in the eight genera belonging to three tribes: Euchresteae, Sophoreae s.s., and Thermopsideae. The phylogenetic distribution of this 24-kb inversion strongly supports the monophyly of members of Sophoreae s.s. with Euchresteae and Thermopsideae. Hence, it can be used as a putative synapomorphic characteristic for the newly circumscribed Sophoreae, including Euchresteae and Thermopsideae. However, plastome conformation suggests a slightly narrower taxonomic group because of heterogeneous results from Bolusanthus and Dicraeopetalum. The phylogenetic analysis, based on plastome sequences from 43 legumes, represents well our understanding of legume systematics while resolving the genistoid clade as a sister group to an Old World clade. It also demonstrates the value that plastomes are powerful marker for systematic studies of basal papilionoid legumes.

New Insights Into the Plastome Evolution of the Millettioid/Phaseoloid Clade (Papilionoideae, Leguminosae)

“…Of note, the IV-D is a synapomorphy of one subclade of the tribes Phaseoleae and core-Millettieae, which is congruent with their closely related evolutionary relationships. Consistent with some previous studies (Martin et al, 2014;Dugas et al, 2015;Choi and Choi, 2017), our results suggest that significant plastome structural rearrangements such as inversion may provide useful information about phylogenetic relationships. However, some previous studies have suggested caution in using inversions in phylogenetic analysis.…”

“…Most members of papilionoids, with the exception of a few early diverging lineages, share a 50-kb inversion in the LSC (Doyle et al, 1996). Previous studies have reported multiple inversions of 23, 24, or 36-kb in the Genistoid clade (Martin et al, 2014;Choi and Choi, 2017;Feng et al, 2017;Keller et al, 2017), a 39kb inversion in Robinia (Schwarz et al, 2015), and a large 78-kb inversion in the subtribe Phaseolinae of tribe Phaseoleae (Bruneau et al, 1990). However, only a few studies have examined PSV in the Millettioid/Phaseoloid clade (hereafter referred as the MP clade), one of the most species-rich clades within subfamily Papilionoideae.…”

“…The plastome structure of autotrophic plants is usually conserved (Kim and Jansen, 2005;Lin et al, 2015). However, significant structural variations including IR loss, IR contraction/expansion, inversion, pseudogenization, gene duplication, and gene loss have been reported in some gymnosperms (Wu and Chaw, 2016) and angiosperm families such as Campanulaceae (Cosner et al, 1997;Haberle et al, 2008), Geraniaceae (Chumley et al, 2006;Guisinger et al, 2011;Weng et al, 2014), Oleaceae (Lee et al, 2007), Petrosaviaceae (Logacheva et al, 2014), and Leguminosae (Lavin et al, 1990;Wojciechowski, 2003;Luo et al, 2016;Choi and Choi, 2017;Wang et al, 2017).…”

“…Some species of Leguminosae, especially those of the subfamily Papilionoideae, have acquired significant plastome structural variations (PSVs) during their evolution. These PSVs includes loss of IR (e.g., Lavin et al, 1990;Doyle et al, 1996), gene or plastome segment inversion (Choi and Choi, 2017), IR expansion, and/or contraction (Choi and Choi, 2017), and gene loss (Jansen et al, 2007;Sabir et al, 2014;Asaf et al, 2017). Most members of papilionoids, with the exception of a few early diverging lineages, share a 50-kb inversion in the LSC (Doyle et al, 1996).…”

The Intertwined Chloroplast and Nuclear Genome Coevolution in Plants

“…Chloroplast genome structure and gene order are also highly affected by inversions. Many inversions have been described in the literature, especially in legumes, with, for instance, fragments of 50 kb in the Papilionoideae [38], 36 kb in the Genistoids [39]; 29 kb in Sophoreae [40] or 7 kb in Tylosema esculentum [41]. Multiple inversions have also been found in Geraniaceae, Campanulaceae (more than 40 inversions detected), and other lineages [25,42,43].…”