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Tightly constrained genome reduction and relaxation of purifying selection during secondary plastid endosymbiosis

Kavitha Uthanumallian, View ORCID ProfileCintia Iha, Sonja I. Repetti, View ORCID ProfileCheong Xin Chan, Debashish Bhattacharya, Sebastian Duchene, Heroen Verbruggen
doi: https://doi.org/10.1101/2021.05.27.446077
Kavitha Uthanumallian
1School of BioSciences, University of Melbourne, Melbourne, Australia
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  • For correspondence: kavitha.uthanumallian@student.unimelb.edu.au
Cintia Iha
1School of BioSciences, University of Melbourne, Melbourne, Australia
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Sonja I. Repetti
1School of BioSciences, University of Melbourne, Melbourne, Australia
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Cheong Xin Chan
2Australian Centre for Ecogenomics, School of Chemistry and Molecular Biosciences, The University of Queensland, Brisbane, Queensland 4072, Australia
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Debashish Bhattacharya
3Department of Biochemistry and Microbiology, Rutgers University, New Brunswick, New Jersey, 08901 USA
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Sebastian Duchene
4Dept. of Microbiology and Immunology, Peter Doherty Institute for Infection and Immunity, University of Melbourne, Melbourne, Australia
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Heroen Verbruggen
1School of BioSciences, University of Melbourne, Melbourne, Australia
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Abstract

Endosymbiosis, the establishment of a former free-living prokaryotic or eukaryotic cell as an organelle inside a host cell, can dramatically alter the genomic architecture of the endosymbiont. Plastids, the light harvesting organelles of photosynthetic eukaryotes, are excellent models to study this phenomenon because plastid origin has occurred multiple times in evolution. Here, we investigate the genomic signature of molecular processes acting through secondary plastid endosymbiosis – the origination of a new plastid from a free-living eukaryotic alga. We used phylogenetic comparative methods to study gene loss and changes in selective regimes on plastid genomes, focusing on the green lineage that has given rise to three independent lineages with secondary plastids (euglenophytes, chlorarachniophytes, Lepidodinium). Our results show an overall increase in gene loss associated with secondary endosymbiosis, but this loss is tightly constrained by retention of genes essential for plastid function. The data show that secondary plastids have experienced temporary relaxation of purifying selection during secondary endosymbiosis. However, this process is tightly constrained as well, with selection relaxed only relative to the background in primary plastids, but purifying selection remaining strong in absolute terms even during the endosymbiosis events. Selection intensity rebounds to pre-endosymbiosis levels following endosymbiosis events, demonstrating the changes in selection efficiency during different phases of secondary plastid origin. Independent endosymbiosis events in the euglenophytes, chlorarachniophytes, and Lepidodinium differ in their degree of relaxation of selection, highlighting the different evolutionary contexts of these events. This study reveals the selection-drift interplay during secondary endosymbiosis, and evolutionary parallels during the process of organelle origination.

Competing Interest Statement

The authors have declared no competing interest.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-ND 4.0 International license.
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Posted May 29, 2021.
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Tightly constrained genome reduction and relaxation of purifying selection during secondary plastid endosymbiosis
Kavitha Uthanumallian, Cintia Iha, Sonja I. Repetti, Cheong Xin Chan, Debashish Bhattacharya, Sebastian Duchene, Heroen Verbruggen
bioRxiv 2021.05.27.446077; doi: https://doi.org/10.1101/2021.05.27.446077
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Tightly constrained genome reduction and relaxation of purifying selection during secondary plastid endosymbiosis
Kavitha Uthanumallian, Cintia Iha, Sonja I. Repetti, Cheong Xin Chan, Debashish Bhattacharya, Sebastian Duchene, Heroen Verbruggen
bioRxiv 2021.05.27.446077; doi: https://doi.org/10.1101/2021.05.27.446077

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