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

Aldanah A Alqahtani,Robert K Jansen

doi:10.1038/s41598-021-86820-z

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.

Highlights

Plastids evolved from endosymbiosis of a cyanobacterium[1]
A novel transit peptide that was acquired by exon shuffling of unknown nuclear-encoded plastid gene has been identified in Ranunculaceae (Thalictrum and Aquilegia)[12]
The Euphorbia schimperi plastome had a length of 159,462 base pairs with a pair of inverted repeats (IR) of 26,629 bp, which separate the large single copy (LSC, 88,904 bp) and small single copy (SSC, 17,300 bp) regions (Fig. S1, accession number MT900567)

Summary

Introduction

Plastids evolved from endosymbiosis of a cyanobacterium[1]. Since the primary and secondary endosymbiotic events a tremendous number of genes have transferred to the nucleus of the host cell or have been lost entirely from the plastid genome (plastome)[2]. The missing plastid genes carry out important roles and their fate has been explained by two possible mechanisms that have been verified by experimental and/or bioinformatic approaches They have been either transferred to the nuclear genome such as rpl[32], rpl[22], rps[7], rpoA and infA4, 10–12, 14, 26, 27, 29, substituted by a dual targeted nuclear-encoded mitochondrial gene such as rps[16] in Medicago truncatula (Fabaceae), Populus alba (Salicaceae) and Passifloraceae[14, 22], or substituted by a nuclear-encoded mitochondrial gene such as accD in grasses[30], rpl[23] in spinach and Geranium (Geraniaceae)[31, 32] and rpl[20] in Passifloraceae[14]. In Populus alba and Medicago truncatula, the RPS16 nuclear copy has gained targeting information within its mature protein without having a N-terminal extension s equence[22]

Methods

Results

Discussion

Conclusion