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

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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.

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Data availability

Data are included as supplementary material, and transformation constructs are available via Addgene accessions 173,794–173,797.

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Acknowledgements

We thank Alissa Williams and two anonymous reviewers for comments on an earlier version of this manuscript and Zora Svab, Amber Torres and Matheus Fernandes Gyorfy for lab assistance. This work was supported by a Grant from the National Science Foundation (MCB-1733227).

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National Science Foundation (MCB-1733227).

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Authors and Affiliations

  1. Department of Biology, Colorado State University, Fort Collins, CO, 80523, USA

    Salah E. Abdel-Ghany, Haleakala T. Harroun & Daniel B. Sloan

  2. Waksman Institute of Microbiology, Rutgers University, Piscataway, NJ, 08854, USA

    Lisa M. LaManna & Pal Maliga

  3. Department of Plant Biology, Rutgers University, New Brunswick, NJ, 08901, USA

    Pal Maliga

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  1. Salah E. Abdel-Ghany
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  2. Lisa M. LaManna
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  3. Haleakala T. Harroun
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  4. Pal Maliga
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Contributions

Conceptualization: DBS; Experimental Design: SEAG, PM, DBS; Data Generation: SEAG, LMLM, HTH; Writing—original draft preparation: DBS; Writing—review and editing: SEAG, PM.

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Correspondence to Salah E. Abdel-Ghany or Daniel B. Sloan.

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Abdel-Ghany, S.E., LaManna, L.M., Harroun, H.T. et al. Rapid sequence evolution is associated with genetic incompatibilities in the plastid Clp complex. Plant Mol Biol 108, 277–287 (2022). https://doi.org/10.1007/s11103-022-01241-4

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