Rapid sequence evolution is associated with genetic incompatibilities in the plastid Clp complex

• Published in: Plant molecular biology Vol. 108; no. 3; pp. 277 - 287
• Main Authors: Abdel-Ghany, Salah E., LaManna, Lisa M., Harroun, Haleakala T., Maliga, Pal, Sloan, Daniel B.
• Format: Journal Article
• Language: English
• Published: Dordrecht Springer Netherlands 01.02.2022; Springer; Springer Nature B.V
• Subjects: Amino Acid Sequence; Amino acid substitution; Amino acids; Angiosperms; Biochemistry; Biomedical and Life Sciences; Clp protein; Conserved Sequence; Divergence; Epistasis; Evolution; Genetic aspects; Genetic engineering; Genetic Markers; Genetic transformation; Genomes; Genomics; Homeostasis; Life Sciences; Nicotiana - genetics; Nicotiana - metabolism; Nicotiana tabacum; Phylogeny; Plant Pathology; Plant Proteins - chemistry; Plant Proteins - genetics; Plant Proteins - metabolism; Plant Sciences; Plants, Genetically Modified; Plastids - genetics; Proteins; Silene; Species; Cytonuclear coevolution; Epistasis; Plastome editing; Silene; Nicotiana; clpP
• ISSN: 0167-4412; 1573-5028
• DOI: 10.1007/s11103-022-01241-4

Key message Replacing the native clpP1 gene in the Nicotiana plastid genome with homologs from different donor species showed that the extent of genetic incompatibilities depended on the rate of sequence evolution. The plastid caseinolytic protease (Clp) complex plays essential roles in maintaining protein homeostasis and comprises both plastid-encoded and nuclear-encoded subunits. Despite the Clp complex being retained across green plants with highly conserved protein sequences in most species, examples of extremely accelerated amino acid substitution rates have been identified in numerous angiosperms. The causes of these accelerations have been the subject of extensive speculation but still remain unclear. To distinguish among prevailing hypotheses and begin to understand the functional consequences of rapid sequence divergence in Clp subunits, we used plastome transformation to replace the native clpP1 gene in tobacco ( Nicotiana tabacum ) with counterparts from another angiosperm genus ( Silene ) that exhibits a wide range in rates of Clp protein sequence evolution. We found that antibiotic-mediated selection could drive a transgenic clpP1 replacement from a slowly evolving donor species ( S. latifolia ) to homoplasmy but that clpP1 copies from Silene species with accelerated evolutionary rates remained heteroplasmic, meaning that they could not functionally replace the essential tobacco clpP1 gene. These results suggest that observed cases of rapid Clp sequence evolution are a source of epistatic incompatibilities that must be ameliorated by coevolutionary responses between plastid and nuclear subunits.