Plastomes from tribe Plantagineae (Plantaginaceae) reveal infrageneric structural synapormorphies and localized hypermutation for Plantago and functional loss of ndh genes from Littorella

[Display omitted] •We generated 25 plastomes representing all Plantagineae genera (Aragoa, Littorella, Plantago) and Plantago subgenera, and compared them with 32 additional plastome sequences from Plantaginaceae.•Our plastid phylogenomic analysis established that Aragoa is sister to Littorella + Plantago, and Plantago subgenera Bougueria + Psyllium are sister to subgenera Coronopus + Plantago.•Plastomes from subgenera Coronopus and Plantago exhibit substantial genomic change, including increased size and repetitiveness, expansions and inversions of the inverted repeat, and gene-specific substitution rates.•The Littorella plastome has lost functional copies of ndh genes, which likely results from its amphibious lifestyle or partial use of Crassulacean acid metabolism (CAM) photosynthesis. Tribe Plantagineae (Plantaginaceae) comprises ~ 270 species in three currently recognized genera (Aragoa, Littorella, Plantago), of which Plantago is most speciose. Plantago plastomes exhibit several atypical features including large inversions, expansions of the inverted repeat, increased repetitiveness, intron losses, and gene-specific increases in substitution rate, but the prevalence of these plastid features among species and subgenera is unknown. To assess phylogenetic relationships and plastomic evolutionary dynamics among Plantagineae genera and Plantago subgenera, we generated 25 complete plastome sequences and compared them with existing plastome sequences from Plantaginaceae. Using whole plastome and partitioned alignments, our phylogenomic analyses provided strong support for relationships among major Plantagineae lineages. General plastid features—including size, GC content, intron content, and indels—provided additional support that reinforced major Plantagineae subdivisions. Plastomes from Plantago subgenera Plantago and Coronopus have synapomorphic expansions and inversions affecting the size and gene order of the inverted repeats, and particular genes near the inversion breakpoints exhibit accelerated nucleotide substitution rates, suggesting localized hypermutation associated with rearrangements. The Littorella plastome lacks functional copies of ndh genes, which may be related to an amphibious lifestyle and partial reliance on CAM photosynthesis.