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

Salah E. Abdel-Ghany, Lisa M. LaManna, Haleakala T. Harroun, Pal Maliga, Daniel B. Sloan

Research output: Contribution to journalArticlepeer-review

Abstract

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. Abstract: 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.

Original languageAmerican English
Pages (from-to)277-287
Number of pages11
JournalPlant Molecular Biology
Volume108
Issue number3
DOIs
StatePublished - Feb 2022

ASJC Scopus subject areas

  • Genetics
  • Agronomy and Crop Science
  • Plant Science

Keywords

  • Cytonuclear coevolution
  • Epistasis
  • Nicotiana
  • Plastome editing
  • Silene
  • clpP

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