DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Kingdom-Wide Analysis of Fungal Protein-Coding and tRNA Genes Reveals Conserved Patterns of Adaptive Evolution

Journal Article · · Molecular Biology and Evolution
ORCiD logo [1];  [2]; ORCiD logo [3]
  1. Univ. of California, Merced, CA (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
  2. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
  3. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States); Univ. of California, Berkeley, CA (United States)

Protein-coding genes evolved codon usage bias due to the combined but uneven effects of adaptive and nonadaptive influences. Studies in model fungi agree on codon usage bias as an adaptation for fine-tuning gene expression levels; however, such knowledge is lacking for most other fungi. Our comparative genomics analysis of over 450 species supports codon usage and transfer RNAs (tRNAs) as coadapted for translation speed and this is most likely a realization of convergent evolution. Rather than drift, phylogenetic reconstruction inferred adaptive radiation as the best explanation for the variation of interspecific codon usage bias. Although the phylogenetic signals for individual codon and tRNAs frequencies are lower than expected by genetic drift, we found remarkable conservation of highly expressed genes being codon optimized for translation by the most abundant tRNAs, especially by inosine-modified tRNAs. As an application, we present a sequence-to-expression neural network that uses codons to reliably predict highly expressed transcripts. The kingdom Fungi, with over a million species, includes many key players in various ecosystems and good targets for biotechnology. Collectively, our results have implications for better understanding the evolutionary success of fungi, as well as informing the biosynthetic manipulation of fungal genes.

Research Organization:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Organization:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
Grant/Contract Number:
AC02-05CH11231
OSTI ID:
1891484
Journal Information:
Molecular Biology and Evolution, Journal Name: Molecular Biology and Evolution Journal Issue: 2 Vol. 39; ISSN 0737-4038
Publisher:
Oxford University PressCopyright Statement
Country of Publication:
United States
Language:
English

References (84)

Correlation between the abundance of yeast transfer RNAs and the occurrence of the respective codons in protein genes journal July 1982
The ‘effective number of codons’ used in a gene journal March 1990
tRNA gene number and codon usage in the C. elegans genome are co-adapted for optimal translation of highly expressed genes journal July 2000
Biased gene conversion: implications for genome and sex evolution journal June 2003
A Role for Codon Order in Translation Dynamics journal April 2010
An Evolutionarily Conserved Mechanism for Controlling the Efficiency of Protein Translation journal April 2010
A Role for tRNA Modifications in Genome Structure and Codon Usage journal March 2012
Codon Optimality Is a Major Determinant of mRNA Stability journal March 2015
Adjacent Codons Act in Concert to Modulate Translation Efficiency in Yeast journal July 2016
The Fungi journal September 2009
An overview on data representation learning: From traditional feature learning to recent deep learning journal December 2016
Resolution of deep divergence of club fungi (phylum Basidiomycota) journal December 2019
The importance of sourcing enzymes from non-conventional fungi for metabolic engineering and biomass breakdown journal November 2017
tRNomics: Analysis of tRNA genes from 50 genomes of Eukarya, Archaea, and Bacteria reveals anticodon-sparing strategies and domain-specific features journal October 2002
Inferring the historical patterns of biological evolution journal October 1999
Reconstructing the early evolution of Fungi using a six-gene phylogeny journal October 2006
A-to-I editing of coding and non-coding RNAs by ADARs journal December 2015
Superwobbling facilitates translation with reduced tRNA sets journal January 2008
Evolutionary conservation of codon optimality reveals hidden signatures of cotranslational folding journal December 2012
Studying fungal pathogens of humans and fungal infections: fungal diversity and diversity of approaches journal April 2019
Translation of non-standard codon nucleotides reveals minimal requirements for codon-anticodon interactions journal November 2018
Tempo and timing of ecological trait divergence in bird speciation journal June 2018
Megaphylogeny resolves global patterns of mushroom evolution journal March 2019
Leveraging single-cell genomics to expand the fungal tree of life journal October 2018
Utilization of selenocysteine in early-branching fungal phyla journal February 2019
Codon usage between genomes is constrained by genome-wide mutational processes journal February 2004
The adaptive radiation of lichen-forming Teloschistaceae is associated with sunscreening pigments and a bark-to-rock substrate shift journal August 2015
Apicomplexa -specific tRip facilitates import of exogenous tRNAs into malaria parasites journal April 2016
Codon usage is an important determinant of gene expression levels largely through its effects on transcription journal September 2016
Codon usage of highly expressed genes affects proteome-wide translation efficiency journal May 2018
Genome-wide role of codon usage on transcription and identification of potential regulators journal February 2021
Phylogenetic Signal, Evolutionary Process, and Rate journal August 2008
Codon adaptation to tRNAs with Inosine modification at position 34 is widespread among Eukaryotes and present in two Bacterial phyla journal September 2017
Phylogenies and the Comparative Method journal January 1985
Phylogenetic Comparative Analysis: A Modeling Approach for Adaptive Evolution journal December 2004
Seeing the Forest for the Trees: The Limitations of Phylogenies in Comparative Biology journal June 2011
Picante: R tools for integrating phylogenies and ecology journal April 2010
geiger v2.0: an expanded suite of methods for fitting macroevolutionary models to phylogenetic trees journal April 2014
Learned protein embeddings for machine learning journal June 2018
Genome-wide location of yeast RNA polymerase III transcription machinery journal September 2003
The Codon Usage of Lowly Expressed Genes Is Subject to Natural Selection journal April 2018
The selection-mutation-drift theory of synonymous codon usage. journal November 1991
Coevolution of Codon Usage and tRNA Genes Leads to Alternative Stable States of Biased Codon Usage journal August 2008
Estimating Translational Selection in Eukaryotic Genomes journal November 2008
Translationally Optimal Codons Associate with Structurally Sensitive Sites in Proteins journal April 2009
Elucidation of Codon Usage Signatures across the Domains of Life journal May 2019
Codon usage in yeast: cluster analysis clearly differentiates highly and lowly expressed genes journal January 1986
The codon adaptation index-a measure of directional synonymous codon usage bias, and its potential applications journal January 1987
ARAGORN, a program to detect tRNA genes and tmRNA genes in nucleotide sequences journal January 2004
MycoCosm portal: gearing up for 1000 fungal genomes journal December 2013
Environmental shaping of codon usage and functional adaptation across microbial communities journal August 2013
GtRNAdb 2.0: an expanded database of transfer RNA genes identified in complete and draft genomes journal December 2015
Procedures for the Analysis of Comparative Data Using Phylogenetically Independent Contrasts journal March 1992
The Evolution of Defense Mechanisms Correlate with the Explosive Diversification of Autodigesting Coprinellus Mushrooms (Agaricales, Fungi) journal January 2012
Forces that influence the evolution of codon bias journal April 2010
Phylogenetic signal in primate behaviour, ecology and life history journal May 2013
Two new graphical methods for mapping trait evolution on phylogenies journal June 2013
Is the switch to an ectomycorrhizal state an evolutionary key innovation in mushroom-forming fungi? A case study in the Tricholomatineae (Agaricales): DIVERSIFICATION OF ECTOMYCORRHIZAL FUNGI journal November 2016
Testing for Phylogenetic Signal in Comparative Data: Behavioral Traits are more Labile journal April 2003
Using phylogenetics to detect pollinator‐mediated floral evolution journal May 2010
Convergence, Adaptation, and Constraint journal April 2011
phytools: an R package for phylogenetic comparative biology (and other things): phytools: R package journal December 2011
Genome sequencing provides insight into the reproductive biology, nutritional mode and ploidy of the fern pathogen Mixia osmundae journal December 2013
First evidence of mutualism between ancient plant lineages (Haplomitriopsida liverworts) and Mucoromycotina fungi and its response to simulated Palaeozoic changes in atmospheric CO 2 journal September 2014
The Fungal Tree of Life: from Molecular Systematics to Genome-Scale Phylogenies journal October 2017
Repertoires of tRNAs: The Couplers of Genomics and Proteomics journal October 2018
Early Diverging Fungi: Diversity and Impact at the Dawn of Terrestrial Life journal September 2017
Selection on Codon Bias journal December 2008
Evolutionary dynamics of eukaryotic selenoproteomes: large selenoproteomes may associate with aquatic life and small with terrestrial life journal January 2007
Variation in global codon usage bias among prokaryotic organisms is associated with their lifestyles journal January 2011
What defines an adaptive radiation? Macroevolutionary diversification dynamics of an exceptionally species-rich continental lizard radiation journal August 2015
Orthologs, turn-over, and remolding of tRNAs in primates and fruit flies journal August 2016
Horseshoes in multidimensional scaling and local kernel methods journal September 2008
Computational identification of the selenocysteine tRNA (tRNASec) in genomes journal February 2017
Ten quick tips for effective dimensionality reduction journal June 2019
Variation and selection on codon usage bias across an entire subphylum journal July 2019
A General Model of Codon Bias Due to GC Mutational Bias journal October 2010
Effects of Codon Distributions and tRNA Competition on Protein Translation journal August 2008
Beneficial Services of Arbuscular Mycorrhizal Fungi – From Ecology to Application journal September 2018
Codon adaptation to tRNAs with Inosine modification at position 34 is widespread among Eukaryotes and present in two Bacterial phyla dataset January 2017
Orthologs, turn-over, and remolding of tRNAs in primates and fruit flies collection January 2016
Variation and selection on codon usage bias across an entire subphylum collection January 2019
The Major Features of Evolution book December 1953
Codon optimization underpins generalist parasitism in fungi journal February 2017