The evolutionary fate of rpl32 and rps16 losses in the Euphorbia schimperi (Euphorbiaceae) plastome

Abstract

Gene transfers from mitochondria and plastids to the nucleus are an important process in the evolution of the eukaryotic cell. Plastid (pt) gene losses have been documented in multiple angiosperm lineages and are often associated with functional transfers to the nucleus or substitutions by duplicated nuclear genes targeted to both the plastid and mitochondrion. The plastid genome sequence of Euphorbia schimperi was assembled and three major genomic changes were detected, the complete loss of rpl32 and pseudogenization of rps16 and infA. The nuclear transcriptome of E. schimperi was sequenced to investigate the transfer/substitution of the rpl32 and rps16 genes to the nucleus. Transfer of plastid-encoded rpl32 to the nucleus was identified previously in three families of Malpighiales, Rhizophoraceae, Salicaceae and Passifloraceae. An E. schimperi transcript of pt SOD-1-RPL32 confirmed that the transfer in Euphorbiaceae is similar to other Malpighiales indicating that it occurred early in the divergence of the order. Ribosomal protein S16 (rps16) is encoded in the plastome in most angiosperms but not in Salicaceae and Passifloraceae. Substitution of the E. schimperi pt rps16 was likely due to a duplication of nuclear-encoded mitochondrial-targeted rps16 resulting in copies dually targeted to the mitochondrion and plastid. Sequences of RPS16-1 and RPS16-2 in the three families of Malpighiales (Salicaceae, Passifloraceae and Euphorbiaceae) have high sequence identity suggesting that the substitution event dates to the early divergence within Malpighiales.

Plastome Evolution in the Hyperdiverse Genus Euphorbia (Euphorbiaceae) Using Phylogenomic and Comparative Analyses: Large-Scale Expansion and Contraction of the Inverted Repeat Region

“…Comparative plastome analyses based on a taxon sampling representing the four major lineages of Euphorbia reveal a wide range of plastome size, rearrangements, gene losses/pseudogenizations, and duplications, suggesting that organelle evolution in the genus is far more complex than first thought ( Alqahtani and Jansen, 2021 ). Plastomes are frequently treated as highly conserved among angiosperm, especially at genera and infrageneric levels ( Wicke et al, 2011 ; Ruhlman and Jansen, 2014 ), including previous plastome comparative analyses of Euphorbia based on four species ( Khan et al, 2020 ).…”

“…This gene loss has also been documented in Salicaceae of Malpighiales ( Ueda et al, 2007 ). On the other hand, the evolutionary fate of infA , rpl32 , and rps16 loss in the plastome was investigated and discussed, setting Euphorbia schimperi as an example ( Alqahtani and Jansen, 2021 ). The loss of ycf15 in E. schlechtendalii and E. neogillettii , accompanied by large-scale IR expansion/contraction, was possibly associated with the IR boundary shift, as evidenced in Caprifoliaceae ( He et al, 2017 ).…”

“…Euphorbia species have been used in different aspects of human’s activities, due to their highly ornamental and aesthetic values ( Berry and Riina, 2007 ), their important roles in traditional medicine ( Ernst et al, 2015 , 2019 ), their usages in pharmaceutical industries ( Shi et al, 2008 ), as well as being promising biofuel sources ( Patan et al, 2018 ). Although, plastome sequences of Euphorbia have been sporadically reported in recent years ( Horvath et al, 2018 ; Zhang et al, 2019 ; Jiang et al, 2020 ; Khan et al, 2020 ; Alqahtani and Jansen, 2021 ), a comprehensive comparative plastome analysis has not been considered until now.…”

Comparative Chloroplast Genomics in Phyllanthaceae Species

“…Many mutational events are reported in the chloroplast genome, including substitutions, insertiondeletions (InDels), repeats, and inversions [23][24][25]. The deletion of certain genes from the chloroplast genome or their transfer to nuclear genomes has also been reported in several plant lineages, including the species of the order Malpighiales to which the family Phyllanthaceae belongs [20,26,27]. The chloroplast genome evolves slowly and lacks the meiotic recombination of the nuclear genome, where homologous chromosomes exchange segments [28].…”

Chloroplast Genome of Phyllanthus Emblica and Leptopus Cordifolius: Comparative Analysis and Phylogenetic within Family Phyllanthaceae

“…Many mutational events are reported in chloroplast genomes, including substitutions, insertion-deletions (InDels), repeats, and inversion [21][22][23]. The deletion of certain genes from the chloroplast genome or their transfer to nuclear genomes are also reported in several plant lineages, including the species of order Malpighiales to which family Phyllanthaceae belong [16,24,25]. The chloroplast genome is slowly evolving and lacks the meiotic recombination that is seen in the nuclear genome where homologous chromosomes exchange segments [26].…”