The chicken or the egg? Plastome evolution and an independent loss of the inverted repeat in papilionoid legumes

Abstract

Summary The plastid genome (plastome), while surprisingly constant in gene order and content across most photosynthetic angiosperms, exhibits variability in several unrelated lineages. During the diversification history of the legume family Fabaceae, plastomes have undergone many rearrangements, including inversions, expansion, contraction and loss of the typical inverted repeat (IR), gene loss and repeat accumulation in both shared and independent events. While legume plastomes have been the subject of study for some time, most work has focused on agricultural species in the IR‐lacking clade (IRLC) and the plant model Medicago truncatula. The subfamily Papilionoideae, which contains virtually all of the agricultural legume species, also comprises most of the plastome variation detected thus far in the family. In this study three non‐papilioniods were included among 34 newly sequenced legume plastomes, along with 33 publicly available sequences, to assess plastome structural evolution in the subfamily. In an effort to examine plastome variation across the subfamily, approximately 20% of the sampling represents the IRLC with the remainder selected to represent the early‐branching papilionoid clades. A number of IR‐related and repeat‐mediated changes were identified and examined in a phylogenetic context. Recombination between direct repeats associated with ycf2 resulted in intraindividual plastome heteroplasmy. Although loss of the IR has not been reported in legumes outside of the IRLC, one genistoid taxon was found to completely lack the typical plastome IR. The role of the IR and non‐IR repeats in the progression of plastome change is discussed.

Highly Resolved Papilionoid Legume Phylogeny Based on Plastid Phylogenomics

“…The 50 kb-inversion was long considered an unequivocal molecular synapomorphy for this clade, but recently at least three species of Sesbania Adans. were shown to have completely reverted the 50-kb sequence, resulting in essentially the same gene order as found in the earliest-diverging papilionoids ( Lee et al, 2021 ).…”

“…To avoid introducing non-orthologous sequences during the rearrangements, non-genic edges of LCBs were deleted. The intergenic regions that coincide with the end points of the 50-kb inversion and an adjacent gene encoding rps16 , pseudogenized in many papilionoids ( Schwarz et al, 2015 ; Choi and Choi, 2017 ; Lee et al, 2021 ), were deleted from all taxa. Complete plastomes were aligned by MAFFT v7.450 ( Katoh and Standley, 2013 ) in Geneious Prime 2021.0.3 4 using default options.…”

“…The family provides a wide diversity of secondary metabolites (alkaloids, flavonoids, lignans, tannins, terpenoids, benzofuranoids, and non-proteinogenic amino acids such as canavanine; Bisby et al, 1994 ; Kursar et al, 2009 ; Wink, 2013 ). The family is also an excellent model to reveal the patterns and processes of plastome structural evolution, since its taxa have undergone several dramatic rearrangements involving inversions of large blocks of sequence, contraction, loss, and regain of the inverted repeat (IR), gene/intron loss and repeat accumulation (e.g., Palmer et al, 1987 ; Lavin et al, 1990 ; Doyle et al, 1996 ; Jansen et al, 2008 ; Martin et al, 2014 ; Schwarz et al, 2015 ; Choi and Choi, 2017 ; Choi et al, 2019 ; Zhang et al, 2020 ; Charboneau et al, 2021 ; Lee et al, 2021 ). One of the most striking examples is a 50-kb inversion situated in the plastome large single-copy region (LSC) that is shared by the vast majority of subfamily Papilionoideae (papilionoids) ( Doyle et al, 1996 ; Pennington et al, 2001 ; Wojciechowski et al, 2004 ; Cardoso et al, 2012a ; LPWG et al, 2013 ).…”

Chloroplast Phylogenomic Analyses Reveal a Maternal Hybridization Event Leading to the Formation of Cultivated Peanuts

“…To take an extreme example, the IR region is completely lost in Erodium L'Herit. and some papilionoid legumes (Blazier et al, 2016;Lee et al, 2021). Angiosperm plastomes generally encode 110-130 genes, which include approximately 80 protein coding genes, 30 transfer RNA genes, and four ribosomal RNA genes (Daniell et al, 2016).…”

The complete chloroplast genome of the threatened Napa False Indigo Amorpha californica var. napensis Jeps. 1925 (Fabaceae) from Northern California, USA

“…The following accessions with references were used for the phylogenetic anlaysis: Amorpha roemeriana MW628937 , Centrolobium microchaete MW628956, Ctenodon histrix MW628943, Geoffroea spinosa MW628955, Grazielodendron riodocensis MW628957, Poiretia bahiana MW628942, Zornia myriadena MW628944 (Lee et al. 2021 ); Amorpha fruticosa NC_047310, Dialium schlechteri MN709806, Petalostylis labicheoides NC_047335, Smithia erubescens NC_047390, Tipuana tipu NC_047321, Zornia diphylla MN709887 (Zhang, Wang, et al. 2020 ); Pterocarpus marsupium MT249113, Pterocarpus pedatus MT249114, Pterocarpus santalinus MT249117 (Hong et al.…”