myTAI: evolutionary transcriptomics with R

Drost, Hajk-Georg; Gabel, Alexander; Liu, Jialin; Quint, Marcel; Große, Ivo

doi:10.1093/bioinformatics/btx835

Cited by 49 publications

(56 citation statements)

References 13 publications

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“…The whole procedure of obtaining TdNI, TdSI, PdNI and PdSI was made in R package orthologr V0.3.0.9000. The statistical analysis for TAI, PAI, TdNI, TdSI, PdNI, PdSI, TCBI, PCBI was calculated using the R package myTAI V0.9.0 78 .…”

Section: Methodsmentioning

confidence: 99%

Embryo-like features in developingBacillus subtilisbiofilms

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Opasic

Koska

et al. 2020

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34Correspondence between evolution and development has been discussed for more than 35 two centuries 1 . Recent work reveals that phylogeny-ontogeny correlations are indeed 36 present in developmental transcriptomes of eukaryotic clades with complex 37 multicellularity 2-10 . Nevertheless, it has been largely ignored that the pervasive presence 38 of phylogeny-ontogeny correlations is a hallmark of development in eukaryotes 6,10-12 . This 39 perspective opens a possibility to look for similar parallelisms in biological settings where 40 developmental logic and multicellular complexity are more obscure [13][14][15][16] . For instance, it 41 has been increasingly recognized that multicellular behaviour underlies biofilm formation 42 in bacteria 13,14,[17][18][19] . However, it remains unclear whether bacterial biofilm growth shares 43 some basic principles with development in complex eukaryotes [14][15][16]18,20 . Here we show that 44 the ontogeny of growing Bacillus subtilis biofilms recapitulates phylogeny at the 45 expression level. Using time-resolved transcriptome and proteome profiles, we found that 46 biofilm ontogeny correlates with the evolutionary measures, in a way that evolutionary 47 younger and more diverged genes were increasingly expressed towards later timepoints 48 of biofilm growth. Molecular and morphological signatures also revealed that biofilm 49 growth is highly regulated and organized into discrete ontogenetic stages, analogous to 50 those of eukaryotic embryos 11,21 . Together, this suggests that biofilm formation in Bacillus 51 is a bona fide developmental process comparable to organismal development in animals, 52 plants and fungi. Given that most cells on Earth reside in the form of biofilms 22 and that 53 biofilms represent the oldest known fossils 23 , we anticipate that the widely-adopted vision 54 of the first life as a single-cell and free-living organism needs rethinking. 55 56 Multicellular behaviour is wide-spread in bacteria and it was proposed that they should be 57 considered multicellular organisms 13 . However, this idea has not been generally adopted likely 58 3 due to the widespread laboratory use of domesticated bacterial models selected against 59 multicellular behaviours, the long tradition of viewing early diverging groups as simple, and 60 the lack of evidence for system-level commonalities between bacteria and multicellular 61 eukaryotes 15,16,18,24 . Recently developed phylo-transcriptomic tools for tracking evolutionary 62 signatures in animal development 2-4 were also successfully applied in the analysis of 63 developmental processes in plants and fungi 5,6,10 . Although development evolved 64 independently in these three major branches of eukaryotic diversity 12 , their ontogenies showed 65 similar phylogeny-ontogeny correlations indicating that possibly all eukaryotic developmental 66 programs have an evolutionary imprint. Transferability of the phylo-transcriptomic tools across 67 clades and likely universal patterns of phylogeny-ontogeny correlations in e...

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Section: Methodsmentioning

confidence: 99%

Embryo-like features in developingBacillus subtilisbiofilms

Futo

Opasic

Koska

et al. 2020

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“…BLASTs (NCBI BLAST+) against this library of genomes with maize and again with sorghum 547 peptides. TAI was calculated using variance-stabilized RPKM gene expression values with 548 myTAI (Drost et al, 2018). For gene models with multiple predicted peptides, TAI was 549 calculated with the most conserved phylostrata assigned to that locus.…”

Section: Evolutionary Expression Analysis 542mentioning

confidence: 99%

“…Needleman-Wunsch algorithm and then codon aligned with PAL2NAL before calculating 554 substitution rates and separating into equal deciles. TDI was calculated using variance-555 stabilized RPKM gene expression values with myTAI (Drost et al, 2018). For gene models with 556 multiple predicted peptides, TAI was calculated with the most conserved codon divergence 557 strata assigned to that locus.…”

Section: Evolutionary Expression Analysis 542mentioning

confidence: 99%

“…We combined 210 phylostratigraphy, where the ancestry of maize peptides was inferred by protein BLASTs 211 against a representative set of 216 plant, animal, and bacterial genomes with our developmental 212 transcriptomes to produce a transcriptional age index, TAI(Arendsee et al, 2019; Drost et al, 213 2018;Quint et al, 2012). In parallel, we determined the conservation of maize or sorghum 214 codons by calculating Ka/Ks in reciprocal best-BLAST-hits against the Setaria italica genome in 215 a codon divergence stratigraphy approach to determine a transcriptional divergence index or 216 TDI(Drost et al, 2018;Quint et al, 2012). Across maize tassel development, TAI and TDI 217 fluctuated significantly, with an increased contribution of anciently-conserved genes during high 218 floral meristem abundance detected by both phylostratigraphy and codon divergence 219 stratigraphy (ZM4;Figure 6C).…”

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Reconstructing the transcriptional ontogeny of maize and sorghum supports an inverse hourglass model of inflorescence development

Leiboff

Hake

2019

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Assembling meaningful comparisons between species is a major limitation in studying the evolution of organismal form. To understand development in maize and sorghum, closely-related species with architecturally distinct inflorescences, we collected RNAseq profiles encompassing inflorescence body plan specification in both species. We reconstructed molecular ontogenies from 40 B73 maize tassels and 47 BT×623 sorghum panicles and separated them into transcriptional stages. To discover new markers of inflorescence development, we used random forest machine learning to determine stage by RNAseq. We used two descriptions of transcriptional conservation to identify hourglass-like developmental stages. Despite short evolutionary ancestry of 12 million years, we found maize and sorghum inflorescences are most different during their hourglass-like stages of development, following an ‘inverse-hourglass’ model of development. We discuss if agricultural selection may account for the rapid divergence signatures in these species and the observed separation of evolutionary pressure and developmental reprogramming.HighlightsTranscript dynamics identify maize tassel and sorghum panicle developmental stagesRandom forest predicts developmental age by gene expression, providing molecular markers and an in silico staging applicationMaize and sorghum inflorescences are most similar when committing stem cells to a determinant fateExpression conservation identifies hourglass-like stage, but transcriptomes diverge, similar to ‘inverse hourglass’ observations in cross-phyla animal embryo comparisons

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“…Finally, the 95% confidence interval is defined as the range from quantile 2.5% to quantile 97.5% of the 10,000 transcriptome indexes. This approach was integrated into myTAI (Drost et al 2017), a R package for evolutionary transcriptome index analysis.…”

Section: Confidence Interval Analysismentioning

confidence: 99%

Developmental constraints on genome evolution in four bilaterian model species

Liu

Robinson‐Rechavi

2017

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Developmental constraints on genome evolution have been suggested to follow either an early conservation model or an "hourglass" model. Both models agree that late development strongly diverges between species, but debate on which developmental period is the most conserved. Here, based on a modified "Transcriptome Age Index" approach, i.e. weighting parameters by expression level, we analyzed the constraints acting on three evolutionary traits of protein coding genes (strength of purifying selection on protein sequences, phyletic age, and duplicability) in four species: nematode worm C. elegans, fly D. melanogaster, zebrafish D. rerio, and mouse M.musculus. In general, we found that both models can be supported by different genomic properties. The evolution of phyletic age and of duplicability follow an early conservation model in all species, but sequence evolution follows different models in different species: an early conservation model in fly, and an hourglass model in both zebrafish and mouse. Further analyses indicate that stronger purifying selection on sequences in early development of fly and during the morphological 'phylotypic' period of zebrafish and mouse are driven by temporal pleiotropy of these genes. In addition, we report evidence that expression in late development is enriched with retrogenes, which usually lack efficient regulatory elements. This implies that expression in late development could facilitate transcription of new genes, and provide opportunities for acquisition of function. Finally, in nematode, we suggest that dosage imbalance could be one of the main factors that cause depleted expression of high duplicability genes in early development.

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myTAI: evolutionary transcriptomics with R

Cited by 49 publications

References 13 publications

Embryo-like features in developingBacillus subtilisbiofilms

Embryo-like features in developingBacillus subtilisbiofilms

Reconstructing the transcriptional ontogeny of maize and sorghum supports an inverse hourglass model of inflorescence development

Developmental constraints on genome evolution in four bilaterian model species

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