Mimosoid legume plastome evolution: IR expansion, tandem repeat expansions and accelerated rate of evolution in clpP

Abstract

The Leguminosae has emerged as a model for studying angiosperm plastome evolution because of its striking diversity of structural rearrangements and sequence variation. However, most of what is known about legume plastomes comes from few genera representing a subset of lineages in subfamily Papilionoideae. We investigate plastome evolution in subfamily Mimosoideae based on two newly sequenced plastomes (Inga and Leucaena) and two recently published plastomes (Acacia and Prosopis), and discuss the results in the context of other legume and rosid plastid genomes. Mimosoid plastomes have a typical angiosperm gene content and general organization as well as a generally slow rate of protein coding gene evolution, but they are the largest known among legumes. The increased length results from tandem repeat expansions and an unusual 13 kb IR-SSC boundary shift in Acacia and Inga. Mimosoid plastomes harbor additional interesting features, including loss of clpP intron1 in Inga, accelerated rates of evolution in clpP for Acacia and Inga, and dN/dS ratios consistent with neutral and positive selection for several genes. These new plastomes and results provide important resources for legume comparative genomics, plant breeding, and plastid genetic engineering, while shedding further light on the complexity of plastome evolution in legumes and angiosperms.

Positive Selection in Rapidly Evolving Plastid–Nuclear Enzyme Complexes

“…In numerous angiosperm lineages, a subset of plastid genes, including clpP1 and accD, display accelerated evolutionary rates, but the causes of this recurring phenomenon have remained unclear (Jansen et al 2007;Erixon and Oxelman 2008;Greiner et al 2008b;Guisinger et al 2008Guisinger et al , 2010Guisinger et al , 2011Straub et al 2011;Sloan et al 2012aSloan et al , 2014aBarnard-Kubow et al 2014;Weng et al 2014;Dugas et al 2015;Williams et al 2015;Blazier et al 2016;Zhang et al 2016). We investigated the nuclear genes that contribute to the multisubunit complexes that include ClpP1 and AccD, and incorporated population genetic and structural data to distinguish between relaxed purifying selection and positive selection as drivers of elevated d N /d S values.…”

“…Within angiosperms, most plastid genomes are highly conserved in sequence and structure (Jansen et al 2007;Wicke et al 2011), but multiple independent lineages have experienced accelerated rates of aa substitution in similar subsets of nonphotosynthetic genes (Jansen et al 2007;Erixon and Oxelman 2008;Greiner et al 2008b;Guisinger et al 2008Guisinger et al , 2010Guisinger et al , 2011Straub et al 2011;Sloan et al 2012aSloan et al , 2014aBarnard-Kubow et al 2014;Weng et al 2014;Dugas et al 2015;Williams et al 2015;Zhang et al 2016). Several mechanisms have been hypothesized to explain these repeated accelerations including positive selection, reduced effective population size (N e ), altered DNA repair, changes in gene expression, and pseudogenization following gene transfer to the nucleus (see above citations).…”

Comparative DNA sequence analyses of Pyramimonas parkeae (Prasinophyceae) chloroplast genomes

“…The boundary shifts in Eucommia ulmoides were hypothesized to be the result of genome rearrangement, whereas the shifts in the legumes were accompanied by the presence of an increased number of tandem repeats in the genome (Dugas et al. , Wang et al. ).…”

“…Comparative plastome studies in embryophyte families showed that boundaries between the IR and single copy regions are not static, but rather have been subjected to dynamic and random processes that allow the conservative expansion and contraction of IR regions. Movement of IR boundaries is likely to be unique for each species, and hypothesized to reflect relationship among embryophyte families (Zhu et al 2015, Wang et al 2016) and contribute to the expansion of the genome (Dugas et al 2015, Zhu et al 2016.…”

“…Extreme cases included (i) the medicinal plant Eucommia ulmoides, where the IR was expanded by 5 kb in comparison to other angiosperms, and (ii) the legumes Acacia and Inga, where the IR was expanded by 13 kb. The boundary shifts in Eucommia ulmoides were hypothesized to be the result of genome rearrangement, whereas the shifts in the legumes were accompanied by the presence of an increased number of tandem repeats in the genome (Dugas et al 2015, Wang et al 2016.…”