Molecular systematics of the tribe Prismatomerideae (Rubiaceae) and its taxonomic consequences, with notes on the importance of the inflorescence morphology for species‐group recognition in Rennellia

Abstract

Tropical Asia is one of the centers of species diversity of flowering plants, in particular the coffee family (Rubiaceae). Prismatomerideae (the Psychotrieae alliance, subfamily Rubioideae) are a mostly Southeast Asian tribe encompassing four genera of shrubs and small trees (monospecific Gentingia and Motleyia, Prismatomeris with 16 spp., Rennellia with 4-5 spp.). We conducted molecular phylogenetic analyses of this group based on the nuclear and plastid sequence data from six markers and using Bayesian inference. The main goal was to produce a robust phylogeny of the tribe, which was subsequently used to (1) reassess its monophyly and phylogenetic position within the Psychotrieae alliance; (2) rigorously test the monophyly of Prismatomeris and Rennellia;(3) assess the phylogenetic relationships between the genera; and (4) evaluate the phylogenetic value of the inflorescence type currently used for species recognition in Rennellia. Motleyia was not sequenced due to the lack of material, and therefore its affinity with the other genera was assessed based on morphology. The tribe was supported as monophyletic and resolved as sister to the (Gaertnereae (Mitchelleae-Morindeae)) clade. The monophyly of Prismatomeris sensu Johansson was strongly supported, but we argue for the merging of the monospecific genus Motleyia into Prismatomeris based on their strong morphological similarities coupled with the paraphyly of Prismatomeris with respect to Motleyia. Rennellia was strongly supported as paraphyletic with respect to Gentingia. We propose the transfer of the monospecific genus Gentingia to Rennellia, also consistent with their strong morphological resemblance. Prismatomerideae were resolved in two major sister lineages, the Prismatomeris and Rennellia clades, corresponding to our broadly delimited Prismatomeris and Rennellia. Three well-supported and morphologically distinct subclades were identified within Rennellia s.l., of which one was represented by Rennellia subsessilis, with sessile and reduced umbel-like inflorescences bearing two to four flowers. The other two subclades have compound spike-like (or sub-raceme-like) and raceme-like inflorescences, an important distinction in species-group recognition. We conclude that inflorescence type shows a strong phylogenetic signal and is, therefore, a reliable feature for recognizing groups of species in Rennellia. Additional taxonomic characters are, however, needed for teasing apart closely related species with the same inflorescence types. Subsequent to our taxonomic revision, the tribe Prismatomerideae comprises two genera: Prismatomeris and Rennellia. One and two new combinations, respectively, are presented, bringing the total number of species in the tribe to 25, of which 17 are in Prismatomeris and 8 in Rennellia. A new species key to Rennellia s.l. is presented.

Phylogeny and classification of the coffee family (Rubiaceae, Gentianales): Overview and outlook

“…Sister to the Mitchelleae‐Morindeae clade within the Psychotrieae alliance based on mitochondrial genomic data, as well as nuclear genomic data (Rydin & al., 2017; Antonelli & al., 2021; Thureborn & al., 2022), and to Mitchelleae‐Morindeae + Gaertnereae based on plastid data (e.g., Rydin & al., 2009b; Wikström & al., 2015; Razafimandimbison & al., 2017, 2021; Thureborn & al., 2024b). Note that there is cytonuclear discord regarding the position of Gaertnereae (see above and Thureborn & al., 2024b).…”

“…Johansson (1987a,b,c, 1989), Johansson & Wong (1988), Igersheim & Robbrecht (1994), Jalaluddin & Bruhl (2008), and Razafimandimbison & al. (2008, 2017, 2021).…”

“…The members of the Asian tribe Prismatomerideae were historically associated with the tribe Morindeae (e.g., Robbrecht, 1988) mainly due to the occurrence of syncarps (compound fruits, Igersheim & Robbrecht, 1994) as a result of a congenital fusion of ovaries of adjacent flowers borne in a head‐like receptacle (e.g., Razafimandimbison & al., 2021). It was Ruan (1988) who described the tribe Prismatomerideae to accommodate its type genus Prismatomeris .…”

“…The monophyly of the tribe is supported by molecular data (e.g., Razafimandimbison & al., 2008; Thureborn & al., 2022), and its generic limits have recently been assessed by Razafimandimbison & al. (2021). This group of plants is characterized by the combination of its terminal inflorescences, placentae attached to middle of the septum, sessile ovules, large seeds, frequently with blue endosperm, and excavation filled with parenchyma‐like, possibly placental tissue (Igersheim & Robbrecht, 1994).…”

A target enrichment probe set for resolving phylogenetic relationships in the coffee family, Rubiaceae

“…This variation has inspired multiple studies to understand patterns of trait evolution (Bremer and Eriksson, 1992 ; Ferrero et al, 2012 ; Razafimandimbison et al, 2014 ; Ehrendorfer et al, 2019 ), and the family has been used as a model to characterize angiosperm macroevolution (Antonelli et al, 2009 ). While many phylogenetic studies have been performed for different clades in Rubiaceae (Löfstrand et al, 2019 ; Borges et al, 2021 ; Razafimandimbison et al, 2021 ; Amenu et al, 2022 ), as well for the entire family (Bremer and Eriksson, 2009 ), these have mostly relied on a few loci. Only a handful of studies have used genomic‐scale phylogenetic data to resolve relationships within Rubiaceae, with most of these using the Angiosperms353 data (Antonelli et al, 2021 ; Canales et al, 2022 ; Thureborn et al, 2022 ) and another using microarray technology (Prata et al, 2018 ).…”