The Linum usitatissimum L. plastome reveals atypical structural evolution, new editing sites, and the phylogenetic position of Linaceae within Malpighiales

Abstract

The plastome of Linum usitatissimum was completely sequenced allowing analyses of evolution of genome structure, RNA editing sites, molecular markers, and indicating the position of Linaceae within Malpighiales. Flax (Linum usitatissimum L.) is an economically important crop used as food, feed, and industrial feedstock. It belongs to the Linaceae family, which is noted by high morphological and ecological diversity. Here, we reported the complete sequence of flax plastome, the first species within Linaceae family to have the plastome sequenced, assembled and characterized in detail. The plastome of flax is a circular DNA molecule of 156,721 bp with a typical quadripartite structure including two IRs of 31,990 bp separating the LSC of 81,767 bp and the SSC of 10,974 bp. It shows two expansion events from IRB to LSC and from IRB to SSC, and a contraction event in the IRA-LSC junction, which changed significantly the size and the gene content of LSC, SSC and IRs. We identified 109 unique genes and 2 pseudogenes (rpl23 and ndhF). The plastome lost the conserved introns of clpP gene and the complete sequence of rps16 gene. The clpP, ycf1, and ycf2 genes show high nucleotide and aminoacid divergence, but they still possibly retain the functionality. Moreover, we also identified 176 SSRs, 20 tandem repeats, and 39 dispersed repeats. We predicted in 18 genes a total of 53 RNA editing sites of which 32 were not found before in other species. The phylogenetic inference based on 63 plastid protein-coding genes of 38 taxa supports three major clades within Malpighiales order. One of these clades has flax (Linaceae) sister to Chrysobalanaceae family, differing from earlier studies that included Linaceae into the euphorbioid clade.

Complete chloroplast genomes of 14 mangroves: phylogenetic and genomic comparative analyses

“…We found that Euphorbiaceae constituted a single branch, while Rhizophoraceae (including four mangroves: Bruguiera sexangular , Kandelia obovata , Rhizophora stylosa , Ceriops tagal ) is neighboring Erythroxylaceae and Clusiaceae, and Linaceae is a sister to Chrysobalanaceae and Malpighiaceae. This relationship is supported by a very recent study [22]. Finally, our phylogenetic tree supported the sister relationship between the mangrove Pongamia pinnata included order Fabales and Rosales, Cucurbitales and Fagales.…”

“…In summary, the Ka/Ks values here provide comparative results for detection of selective pressure in mangrove chloroplasts. The genes that involve photosynthesis and energy metabolism for chloroplasts are conserved with very low Ka/Ks ratio, and this kind of evolutionary pattern has been generally observed in other plant chloroplasts [22,32]. The potential positive selection or relax pressure of ycf1 , rpl23 , rps7 , rpl36 , petL , psaI were also detected in mangroves, indicating their fast evolve rate and divergence in different species in spite of its ambiguous function in chloroplast genomes.…”

“…We speculate that relaxed neutral selection (Ka/Ks value around 1.0) and potential positive selection (Ka/Ks value greater than 1.0) of rpl23 , rpl36 , and rps7 in various species here reflects the highly diverse environments and adaptions of plants (Table S4). For gene ycf1 , it is one of the largest genes in chloroplast genome and usually has two functional copies [22,25], or one of the two copies was evolved to be a pseudogene in some plants [19,31–33] as well as in 11 mangroves ( Avicennia marina , Xylocarpus moluccensis , Hibiscus tiliaceus , Excoecaria agallocha , Bruguiera sexangula , Kandelia obovata , Rhizophora stylosa , Ceriops tagal , Sonneratia ovata , Pemphis acidula , Laguncularia racemose ). In this study, most species in Malpighiales including one mangrove Excoecaria agallocha , have ycf1 Ka/Ks values around or greater than 1.0, while about 0.4 in Malvales, Myrtales and Sapindales, and about 0.6 in Fabales and Lamiales, showing the diverse evolve rates in different species (Table S4, Figure 4).…”

Passifloraplastome sequencing reveals widespread genomic rearrangements

“…Plastomes from these two families are collinear with the ancestral angiosperm organization and Salicaceae has experienced a few gene losses (Ueda et al, 2007(Ueda et al, , 2008. A recent report of the plastome sequence of the Malpighiales genus Linum usitatissimum (Linaceae, de Santana Lopes et al, 2017) identified two pseudogenes, the loss of rps16 and a single inversion. A single inversion in the LSC was also detected in the Hevea brasiliensis (Euphorbiaceae) plastome (Tangphatsornruang et al, 2011).…”

The complete plastome of macaw palm [Acrocomia aculeata (Jacq.) Lodd. ex Mart.] and extensive molecular analyses of the evolution of plastid genes in Arecaceae

“…Plastome sequences are also of great importance to understand evolutionary events in plants based on the knowledge of gene content, recombination events, loss of genes, gene transfer to the nucleus and genome rearrangements (Vieira et al 2016b;Bock 2017;Lopes et al 2017;Park et al 2017;Ruhlman et al 2017), as well as for plastid transformation aiming basic research (Rogalski et al 2006(Rogalski et al , 2008Alkatib et al 2012) and biotechnological applications (Daniell et al 2016;Zhang et al 2017) since the complete sequence of plastome is a prerequisite to choose target intergenic regions for insertion of transgenes and development of transplastomic plants (Daniell et al 2016;Fuentes et al 2017). The plastid transformation has been used efficiently for metabolic engineering (Daniell et al 2016;Fuentes et al 2017) and it is a viable alternative to manipulate plastid fatty acid biosynthesis (Rogalski and Carrer 2011) given that several efficient protocols of plant regeneration based on somatic embryogenesis are available for macaw palm (Moura et al 2009;Luis and Scherwinski-Pereira 2014;Padilha et al 2015).…”