The economics of organellar gene loss and endosymbiotic gene transfer

Abstract Background The endosymbiosis of the bacterial progenitors of the mitochondrion and the chloroplast are landmark events in the evolution of life on Earth. While both organelles have retained substantial proteomic and biochemical complexity, this complexity is not reflected in the content of their genomes. Instead, the organellar genomes encode fewer than 5% of the genes found in living relatives of their ancestors. While many of the 95% of missing organellar genes have been discarded, others have been transferred to the host nuclear genome through a process known as endosymbiotic gene transfer. Results Here, we demonstrate that the difference in the per-cell copy number of the organellar and nuclear genomes presents an energetic incentive to the cell to either delete organellar genes or transfer them to the nuclear genome. We show that, for the majority of transferred organellar genes, the energy saved by nuclear transfer exceeds the costs incurred from importing the encoded protein into the organelle where it can provide its function. Finally, we show that the net energy saved by endosymbiotic gene transfer can constitute an appreciable proportion of total cellular energy budgets and is therefore sufficient to impart a selectable advantage to the cell. Conclusion Thus, reduced cellular cost and improved energy efficiency likely played a role in the reductive evolution of mitochondrial and chloroplast genomes and the transfer of organellar genes to the nuclear genome.

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The economics of endosymbiotic gene transfer and the evolution of organellar genomes

10.1101/2020.10.01.322487 ◽

2020 ◽

Cited By ~ 1

Author(s):

Steven Kelly

Keyword(s):

Gene Transfer ◽

Host Cell ◽

Protein Import ◽

Nuclear Genome ◽

Selective Advantage ◽

Endosymbiotic Gene Transfer ◽

Organellar Genomes ◽

Evolution Of Life ◽

A Cell ◽

Life On Earth

AbstractThe endosymbiosis of the bacterial progenitors of mitochondrion and the chloroplast are landmark events in the evolution of life on earth. While both organelles have retained substantial proteomic and biochemical complexity, this complexity is not reflected in the content of their genomes. Instead, the organellar genomes encode fewer than 5% of genes found in living relatives of their ancestors. While some of the 95% of missing organellar genes have been discarded, many have been transferred to the host nuclear genome through a process known as endosymbiotic gene transfer. Here we demonstrate that the energy liberated or consumed by a cell as a result of endosymbiotic gene transfer can be sufficient to provide a selectable advantage for retention or nuclear-transfer of organellar genes in eukaryotic cells. We further demonstrate that for realistic estimates of protein abundances, organellar protein import costs, host cell sizes, and cellular investment in organelles that it is energetically favourable to transfer the majority of organellar genes to the nuclear genome. Moreover, we show that the selective advantage of such transfers is sufficiently large to enable such events to rapidly reach fixation. Thus, endosymbiotic gene transfer can be advantageous in the absence of any additional benefit to the host cell, providing new insight into the processes that have shaped eukaryotic genome evolution.One sentence summaryThe high copy number of organellar genomes renders endosymbiotic gene transfer energetically favourable for the vast majority of organellar genes.

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Horizontal gene transfer from extinct and extant lineages: biological innovation and the coral of life

Philosophical Transactions of the Royal Society B Biological Sciences ◽

10.1098/rstb.2009.0033 ◽

2009 ◽

Vol 364 (1527) ◽

pp. 2229-2239 ◽

Cited By ~ 49

Author(s):

Gregory P. Fournier ◽

Jinling Huang ◽

J. Peter Gogarten

Keyword(s):

Gene Transfer ◽

Horizontal Gene Transfer ◽

Evolutionary History ◽

Phylogenetic Reconstruction ◽

Gene Trees ◽

Individual Gene ◽

Evolution Of Life ◽

Domains Of Life ◽

Life On Earth ◽

Simple Tree

Horizontal gene transfer (HGT) is often considered to be a source of error in phylogenetic reconstruction, causing individual gene trees within an organismal lineage to be incongruent, obfuscating the ‘true’ evolutionary history. However, when identified as such, HGTs between divergent organismal lineages are useful, phylogenetically informative characters that can provide insight into evolutionary history. Here, we discuss several distinct HGT events involving all three domains of life, illustrating the selective advantages that can be conveyed via HGT, and the utility of HGT in aiding phylogenetic reconstruction and in dating the relative sequence of speciation events. We also discuss the role of HGT from extinct lineages, and its impact on our understanding of the evolution of life on Earth. Organismal phylogeny needs to incorporate reticulations; a simple tree does not provide an accurate depiction of the processes that have shaped life's history.

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Intergenomic gene transfer in diploid and allopolyploid Gossypium

BMC Plant Biology ◽

10.1186/s12870-019-2041-2 ◽

2019 ◽

Vol 19 (1) ◽

Author(s):

Nan Zhao ◽

Corrinne E. Grover ◽

Zhiwen Chen ◽

Jonathan F. Wendel ◽

Jinping Hua

Keyword(s):

Gene Transfer ◽

Mitochondrial Genome ◽

Chloroplast Dna ◽

Nuclear Genome ◽

Plant Evolution ◽

Trna Genes ◽

Organellar Genomes ◽

Plastid Genomes ◽

Cotton Species ◽

Chloroplast Trna Genes

Abstract Background Intergenomic gene transfer (IGT) between nuclear and organellar genomes is a common phenomenon during plant evolution. Gossypium is a useful model to evaluate the genomic consequences of IGT for both diploid and polyploid species. Here, we explore IGT among nuclear, mitochondrial, and plastid genomes of four cotton species, including two allopolyploids and their model diploid progenitors (genome donors, G. arboreum: A2 and G. raimondii: D5). Results Extensive IGT events exist for both diploid and allotetraploid cotton (Gossypium) species, with the nuclear genome being the predominant recipient of transferred DNA followed by the mitochondrial genome. The nuclear genome has integrated 100 times more foreign sequences than the mitochondrial genome has in total length. In the nucleus, the integrated length of chloroplast DNA (cpDNA) was between 1.87 times (in diploids) to nearly four times (in allopolyploids) greater than that of mitochondrial DNA (mtDNA). In the mitochondrion, the length of nuclear DNA (nuDNA) was typically three times than that of cpDNA. Gossypium mitochondrial genomes integrated three nuclear retrotransposons and eight chloroplast tRNA genes, and incorporated chloroplast DNA prior to divergence between the diploids and allopolyploid formation. For mitochondrial chloroplast-tRNA genes, there were 2-6 bp conserved microhomologies flanking their insertion sites across distantly related genera, which increased to 10 bp microhomologies for the four cotton species studied. For organellar DNA sequences, there are source hotspots, e.g., the atp6-trnW intergenic region in the mitochondrion and the inverted repeat region in the chloroplast. Organellar DNAs in the nucleus were rarely expressed, and at low levels. Surprisingly, there was asymmetry in the survivorship of ancestral insertions following allopolyploidy, with most numts (nuclear mitochondrial insertions) decaying or being lost whereas most nupts (nuclear plastidial insertions) were retained. Conclusions This study characterized and compared intracellular transfer among nuclear and organellar genomes within two cultivated allopolyploids and their ancestral diploid cotton species. A striking asymmetry in the fate of IGTs in allopolyploid cotton was discovered, with numts being preferentially lost relative to nupts. Our results connect intergenomic gene transfer with allotetraploidy and provide new insight into intracellular genome evolution.

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Faculty Opinions recommendation of Origins and evolution of the recA/RAD51 gene family: evidence for ancient gene duplication and endosymbiotic gene transfer.

Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature ◽

10.3410/f.1033431.386704 ◽

2006 ◽

Author(s):

Guenter Theissen

Keyword(s):

Gene Transfer ◽

Gene Duplication ◽

Gene Family ◽

Endosymbiotic Gene Transfer ◽

Rad51 Gene ◽

Ancient Gene ◽

Ancient Gene Duplication

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Organellar Introns in Fungi, Algae, and Plants

Cells ◽

10.3390/cells10082001 ◽

2021 ◽

Vol 10 (8) ◽

pp. 2001

Author(s):

Jigeesha Mukhopadhyay ◽

Georg Hausner

Keyword(s):

Gene Expression ◽

Ribosomal Proteins ◽

Heterologous Gene Expression ◽

Group I Introns ◽

Group Ii Introns ◽

Homing Endonucleases ◽

Organellar Genomes ◽

Chloroplast Genomes ◽

Group I ◽

Group Ii

Introns are ubiquitous in eukaryotic genomes and have long been considered as ‘junk RNA’ but the huge energy expenditure in their transcription, removal, and degradation indicate that they may have functional significance and can offer evolutionary advantages. In fungi, plants and algae introns make a significant contribution to the size of the organellar genomes. Organellar introns are classified as catalytic self-splicing introns that can be categorized as either Group I or Group II introns. There are some biases, with Group I introns being more frequently encountered in fungal mitochondrial genomes, whereas among plants Group II introns dominate within the mitochondrial and chloroplast genomes. Organellar introns can encode a variety of proteins, such as maturases, homing endonucleases, reverse transcriptases, and, in some cases, ribosomal proteins, along with other novel open reading frames. Although organellar introns are viewed to be ribozymes, they do interact with various intron- or nuclear genome-encoded protein factors that assist in the intron RNA to fold into competent splicing structures, or facilitate the turn-over of intron RNAs to prevent reverse splicing. Organellar introns are also known to be involved in non-canonical splicing, such as backsplicing and trans-splicing which can result in novel splicing products or, in some instances, compensate for the fragmentation of genes by recombination events. In organellar genomes, Group I and II introns may exist in nested intronic arrangements, such as introns within introns, referred to as twintrons, where splicing of the external intron may be dependent on splicing of the internal intron. These nested or complex introns, with two or three-component intron modules, are being explored as platforms for alternative splicing and their possible function as molecular switches for modulating gene expression which could be potentially applied towards heterologous gene expression. This review explores recent findings on organellar Group I and II introns, focusing on splicing and mobility mechanisms aided by associated intron/nuclear encoded proteins and their potential roles in organellar gene expression and cross talk between nuclear and organellar genomes. Potential application for these types of elements in biotechnology are also discussed.

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Horizontal Gene Transfer Involving Chloroplasts

International Journal of Molecular Sciences ◽

10.3390/ijms22094484 ◽

2021 ◽

Vol 22 (9) ◽

pp. 4484

Author(s):

Ewa Filip ◽

Lidia Skuza

Keyword(s):

Gene Transfer ◽

Horizontal Gene Transfer ◽

Driving Force ◽

Genetic Material ◽

Adaptive Significance ◽

Chloroplast Genomes ◽

Organelle Genomes ◽

Number Of Genes ◽

Cellular Compartments

Horizontal gene transfer (HGT)- is defined as the acquisition of genetic material from another organism. However, recent findings indicate a possible role of HGT in the acquisition of traits with adaptive significance, suggesting that HGT is an important driving force in the evolution of eukaryotes as well as prokaryotes. It has been noted that, in eukaryotes, HGT is more prevalent than originally thought. Mitochondria and chloroplasts lost a large number of genes after their respective endosymbiotic events occurred. Even after this major content loss, organelle genomes still continue to lose their own genes. Many of these are subsequently acquired by intracellular gene transfer from the original plastid. The aim of our review was to elucidate the role of chloroplasts in the transfer of genes. This review also explores gene transfer involving mitochondrial and nuclear genomes, though recent studies indicate that chloroplast genomes are far more active in HGT as compared to these other two DNA-containing cellular compartments.

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Origin of the Eukaryotic Cell

Molecular Frontiers Journal ◽

10.1142/s2529732517400120 ◽

2017 ◽

Vol 01 (02) ◽

pp. 108-120 ◽

Cited By ~ 2

Author(s):

Nick Lane

Keyword(s):

Protein Synthesis ◽

Host Cell ◽

Genome Size ◽

Energy Savings ◽

Nuclear Genome ◽

Eukaryotic Cell ◽

Eukaryotic Cells ◽

Bacterial Genomes ◽

Complex Cells ◽

Life On Earth

All complex life on Earth is composed of ‘eukaryotic’ cells. Eukaryotes arose just once in 4 billion years, via an endosymbiosis — bacteria entered a simple host cell, evolving into mitochondria, the ‘powerhouses’ of complex cells. Mitochondria lost most of their genes, retaining only those needed for respiration, giving eukaryotes ‘multi-bacterial’ power without the costs of maintaining thousands of complete bacterial genomes. These energy savings supported a substantial expansion in nuclear genome size, and far more protein synthesis from each gene.

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Comparative analysis of chloroplast genomes of cultivars and wild species of sweetpotato (Ipomoea batatas [L.] Lam)

BMC Genomics ◽

10.1186/s12864-021-07544-y ◽

2021 ◽

Vol 22 (1) ◽

Author(s):

Shizhuo Xiao ◽

Pan Xu ◽

Yitong Deng ◽

Xibin Dai ◽

Lukuan Zhao ◽

...

Keyword(s):

Comparative Analysis ◽

Genetic Structure ◽

Chloroplast Genome ◽

Wild Species ◽

Ipomoea Batatas ◽

Nuclear Genome ◽

Ipomoea Trifida ◽

Chloroplast Markers ◽

Chloroplast Genomes ◽

Chloroplast Dna Markers

Abstract Background Sweetpotato (Ipomoea batatas [L.] Lam.) is an important food crop. However, the genetic information of the nuclear genome of this species is difficult to determine accurately because of its large genome and complex genetic background. This drawback has limited studies on the origin, evolution, genetic diversity and other relevant studies on sweetpotato. Results The chloroplast genomes of 107 sweetpotato cultivars were sequenced, assembled and annotated. The resulting chloroplast genomes were comparatively analysed with the published chloroplast genomes of wild species of sweetpotato. High similarity and certain specificity were found among the chloroplast genomes of Ipomoea spp. Phylogenetic analysis could clearly distinguish wild species from cultivars. Ipomoea trifida and Ipomoea tabascana showed the closest relationship with the cultivars, and different haplotypes of ycf1 could be used to distinguish the cultivars from their wild relatives. The genetic structure was analyzed using variations in the chloroplast genome. Compared with traditional nuclear markers, the chloroplast markers designed based on the InDels on the chloroplast genome showed significant advantages. Conclusions Comparative analysis of chloroplast genomes of 107 cultivars and several wild species of sweetpotato was performed to help analyze the evolution, genetic structure and the development of chloroplast DNA markers of sweetpotato.

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Evolution of the chloroplast genome and polymorphic ITS regions in Allium subg. Melanocrommyum

Genome ◽

10.1139/g98-123 ◽

1999 ◽

Vol 42 (2) ◽

pp. 237-247 ◽

Cited By ~ 24

Author(s):

Ted HM Mes ◽

Reinhard M Fritsch ◽

Sven Pollner ◽

Konrad Bachmann

Keyword(s):

Concerted Evolution ◽

Morphological Evolution ◽

Restriction Analysis ◽

Nuclear Genome ◽

Restriction Enzymes ◽

Border Region ◽

Chloroplast Genomes ◽

Central Asian ◽

Its Regions ◽

Chloroplast Haplotypes

Relationships based on PCR-RFLPs of non-coding regions of cpDNA indicate that some of the largest subgenera of the genus Allium and five of the largest sections of the Central Asian subg. Melanocrommyum are artificial. Internested synapomorphic mutations without homoplasy were found only in the chloroplast genomes of plants of subg. Melanocrommyum that occur in the border region of Tajikistan, Uzbekistan, Afghanistan, and Kyrgyzstan. Eighteen of 49 plants surveyed were polymorphic for their ITS regions. Even plants that had identical chloroplast genomes were polymorphic for nuclear ribosomal regions. These individuals had markedly different frequencies of ITS variants that were detected with various restriction enzymes. The geographic partitioning of chloroplast haplotypes and the fact that the ITS variants could not be ordered hierarchically can readily be envisioned to result from gene flow. Processes such as concerted evolution and parallel morphological evolution may also be partly responsible for the disconcordance of mutations in the chloroplast and nuclear genome. However, the chimeric nature of the nuclear ribosomal regions indicates that concerted evolution is not the dominating process in Allium subg. Melanocrommyum.Key words: polymorphic, phylogeny, restriction analysis.

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