Genome-Wide Insights Into the Organelle Translocation of Photosynthetic NDH-1 Genes During Evolution

Translocation of chloroplast-located genes to mitochondria or nucleus is considered to be a safety strategy that impedes mutation of photosynthetic genes and maintains their household function during evolution. The organelle translocation strategy is also developed in photosynthetic NDH-1 (pNDH-1) g...

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Main Authors: Jie Yu, Zhaoxing Ran, Jingsong Zhang, Lanzhen Wei, Weimin Ma
Format: Article
Language:English
Published: Frontiers Media S.A. 2022-07-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2022.956578/full
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author Jie Yu
Zhaoxing Ran
Jingsong Zhang
Lanzhen Wei
Weimin Ma
author_facet Jie Yu
Zhaoxing Ran
Jingsong Zhang
Lanzhen Wei
Weimin Ma
author_sort Jie Yu
collection DOAJ
description Translocation of chloroplast-located genes to mitochondria or nucleus is considered to be a safety strategy that impedes mutation of photosynthetic genes and maintains their household function during evolution. The organelle translocation strategy is also developed in photosynthetic NDH-1 (pNDH-1) genes but its understanding is still far from complete. Here, we found that the mutation rate of the conserved pNDH-1 genes was gradually reduced but their selection pressure was maintained at a high level during evolution from cyanobacteria to angiosperm. By contrast, oxygenic photosynthesis-specific (OPS) pNDH-1 genes had an opposite trend, explaining the reason why they were transferred from the reactive oxygen species (ROS)-enriched chloroplast to the ROS-barren nucleus. Further, genome-wide sequence analysis supported the possibility that all conserved pNDH-1 genes lost in chloroplast genomes of Chlorophyceae and Pinaceae were transferred to the ROS-less mitochondrial genome as deduced from their truncated pNDH-1 gene fragments. Collectively, we propose that the organelle translocation strategy of pNDH-1 genes during evolution is necessary to maintain the function of the pNDH-1 complex as an important antioxidant mechanism for efficient photosynthesis.
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spelling doaj.art-ede1c2a583bc4d808aa290b9d593ffb02022-12-22T00:56:31ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2022-07-011310.3389/fmicb.2022.956578956578Genome-Wide Insights Into the Organelle Translocation of Photosynthetic NDH-1 Genes During EvolutionJie YuZhaoxing RanJingsong ZhangLanzhen WeiWeimin MaTranslocation of chloroplast-located genes to mitochondria or nucleus is considered to be a safety strategy that impedes mutation of photosynthetic genes and maintains their household function during evolution. The organelle translocation strategy is also developed in photosynthetic NDH-1 (pNDH-1) genes but its understanding is still far from complete. Here, we found that the mutation rate of the conserved pNDH-1 genes was gradually reduced but their selection pressure was maintained at a high level during evolution from cyanobacteria to angiosperm. By contrast, oxygenic photosynthesis-specific (OPS) pNDH-1 genes had an opposite trend, explaining the reason why they were transferred from the reactive oxygen species (ROS)-enriched chloroplast to the ROS-barren nucleus. Further, genome-wide sequence analysis supported the possibility that all conserved pNDH-1 genes lost in chloroplast genomes of Chlorophyceae and Pinaceae were transferred to the ROS-less mitochondrial genome as deduced from their truncated pNDH-1 gene fragments. Collectively, we propose that the organelle translocation strategy of pNDH-1 genes during evolution is necessary to maintain the function of the pNDH-1 complex as an important antioxidant mechanism for efficient photosynthesis.https://www.frontiersin.org/articles/10.3389/fmicb.2022.956578/fullorganelle translocationphotosynthetic NDH-1mitochondrial NDH-1evolutionary eventsplant evolution
spellingShingle Jie Yu
Zhaoxing Ran
Jingsong Zhang
Lanzhen Wei
Weimin Ma
Genome-Wide Insights Into the Organelle Translocation of Photosynthetic NDH-1 Genes During Evolution
Frontiers in Microbiology
organelle translocation
photosynthetic NDH-1
mitochondrial NDH-1
evolutionary events
plant evolution
title Genome-Wide Insights Into the Organelle Translocation of Photosynthetic NDH-1 Genes During Evolution
title_full Genome-Wide Insights Into the Organelle Translocation of Photosynthetic NDH-1 Genes During Evolution
title_fullStr Genome-Wide Insights Into the Organelle Translocation of Photosynthetic NDH-1 Genes During Evolution
title_full_unstemmed Genome-Wide Insights Into the Organelle Translocation of Photosynthetic NDH-1 Genes During Evolution
title_short Genome-Wide Insights Into the Organelle Translocation of Photosynthetic NDH-1 Genes During Evolution
title_sort genome wide insights into the organelle translocation of photosynthetic ndh 1 genes during evolution
topic organelle translocation
photosynthetic NDH-1
mitochondrial NDH-1
evolutionary events
plant evolution
url https://www.frontiersin.org/articles/10.3389/fmicb.2022.956578/full
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AT jingsongzhang genomewideinsightsintotheorganelletranslocationofphotosyntheticndh1genesduringevolution
AT lanzhenwei genomewideinsightsintotheorganelletranslocationofphotosyntheticndh1genesduringevolution
AT weiminma genomewideinsightsintotheorganelletranslocationofphotosyntheticndh1genesduringevolution