Rapid evolution of protein diversity by de novo origination in Oryza

Zhang, Li; Ren, Yan; Yang, Tao; Li, Guangwei; Chen, Jianhai; Gschwend, Andrea R.; Yu, Yeisoo; Hou, Guixue; Zi, Jian; Zhou, Ruo; Wen, Bo; Zhang, Jianwei; Chougule, Kapeel; Wang, Muhua; Copetti, Dario; Peng, Zhiyu; Chen, Feng; Zhang, Yong; Ouyang, Yidan; Wing, Rod A.; Liu, Siqi; Long, Manyuan

doi:10.1038/s41559-019-0822-5

Cited by 130 publications

(193 citation statements)

References 102 publications

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“…These results indicate that, although MIR might be functional in all Oryza species, its role is not central, and can be changed or lost in specific lineages. This corroborates the idea that newly evolved genes might not be central in regulatory networks/metabolism, and therefore might be lost/changed more easily (Tautz and Domazet-Loso 2011;Zhang, et al 2019). Moreover, based on gene expression data, we have shown that MIR genes are likely to have a conserved function in Oryza within the subset of AA genome species, where it is found, regulating responses to low Fe.…”

supporting

confidence: 86%

“…Strikingly, we found distant similarities between a MIR-based hidden markov model and sequences derived from an exon inside Raffinose Synthase Family genes, spread throughout the monocot lineages ( Figure 6). These results indicate that Raffinose Synthase genes might have been the source of genetic material for MIR origin, although in an indirect path: the exons of Raffinose Synthase genes generated the sequences P present in chromosome 6 (and in chromosome 4 after a duplication event), which in turn were the sources of functional MIR de novo origination (Tautz and Domazet-Loso 2011;Zhang, et al 2019).…”

Section: A Model For Mir Originationmentioning

confidence: 94%

“…Thus, genes unique to certain species or lineages can be important for modulating existent pathways, rather than necessary for its function. The Oryza genus, which recently had several genomes sequenced (Stein, et al 2018), is especially attractive for identifying gene families for genes considered orphans based on previous analyses of the rice genome (Zhang, et al 2019).…”

Section: Mir Is Not An Orphan But Rather a Lineage-restricted Genementioning

confidence: 99%

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The Mitochondrial Iron Regulated (MIR) gene is Oryza genus-specific and evolved before the speciation of major AA-genome lineages

Wairich

et al. 2019

Preprint

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Rice (Oryza sativa L.) is both a model species and an economically relevant crop. The Oryza genus comprises 25 species, which constitute a genetic reservoir for cultivated rice breeding. Genomic data is available for several Oryza species, making it a good model for genetics and evolution within closely related species. The Mitochondrial Iron Regulated (MIR) gene was previously implicated in O. sativa Fe deficiency response, and was considered an orphan gene present only in rice. Here we show that MIR is also found in other Oryza species that belong to the AA genome group. We characterized the evolutionary pattern of MIR genes within the Oryza genus. Our data suggest that MIR originated de novo from non-coding sequences present only in AA genome species, but these sequences in turn are derived from an exon fragment of Raffinose Synthase genes, present in several groups of monocots. We also show that all species that have a putative functional MIR conserve their regulation by Fe deficiency, with the exception of Oryza barthii. In O. barthii, the MIR coding sequence was translocated to a different chromosomal position and separated from its regulatory region, which led to a lack of Fe deficiency responsiveness. Moreover, we show that MIR co-expression subnetwork cluster in O. sativa is responsive to Fe deficiency, evidencing the importance of the newly originated gene in Fe uptake. This work establishes that MIR is not an orphan gene as previously proposed, but a de novo originated gene within the Oryza genus. We also showed that MIR is undergoing genomic changes in at least one species (O. barthii), which can impact its role in Fe deficiency. P

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supporting

confidence: 86%

Section: A Model For Mir Originationmentioning

confidence: 94%

Section: Mir Is Not An Orphan But Rather a Lineage-restricted Genementioning

confidence: 99%

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The Mitochondrial Iron Regulated (MIR) gene is Oryza genus-specific and evolved before the speciation of major AA-genome lineages

Wairich

et al. 2019

Preprint

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“…In keeping with rigorous best practices 1,22,23 , young de novo ORFs were identified based on a combination of inter-specific sequence similarity searches (phylostratigraphy) and syntenic alignments. Similarly, ORFs encoding useful protein products were identified stringently based on multiple lines of evidence 1,8,24,25 : inter-specific conservation, translation signatures, length, and evidence of intra-specific purifying selection at the codon level. We classified annotated S. cerevisiae ORFs into two categories: emerging ORFs, which appear to have arisen de novo and to lack a useful protein product; and established ORFs, which encode a useful protein product irrespective of whether they emerged de novo or not ( Fig.…”

Section: Resultsmentioning

confidence: 99%

De novo emergence of adaptive membrane proteins from thymine-rich genomic sequences

et al. 2020

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Recent evidence demonstrates that novel protein-coding genes can arise de novo from nongenic loci. This evolutionary innovation is thought to be facilitated by the pervasive translation of non-genic transcripts, which exposes a reservoir of variable polypeptides to natural selection. Here, we systematically characterize how these de novo emerging coding sequences impact fitness in budding yeast. Disruption of emerging sequences is generally inconsequential for fitness in the laboratory and in natural populations. Overexpression of emerging sequences, however, is enriched in adaptive fitness effects compared to overexpression of established genes. We find that adaptive emerging sequences tend to encode putative transmembrane domains, and that thymine-rich intergenic regions harbor a widespread potential to produce transmembrane domains. These findings, together with in-depth examination of the de novo emerging YBR196C-A locus, suggest a novel evolutionary model whereby adaptive transmembrane polypeptides emerge de novo from thymine-rich nongenic regions and subsequently accumulate changes molded by natural selection.

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“…For protein-coding genes, the essential prerequisites of this process are the formation of an open reading frame (ORF), together with the transcription and translation of that ORF. Because much of the genome is transcribed (Kapranov, et al 2007; Neme and Tautz 2016) and many lineage-specific transcripts containing ORFs show evidence of translation (Wilson and Masel 2011; Ingolia, et al 2014; Ruiz-Orera, et al 2014; Prabh and Rödelsperger 2016; Ruiz-Orera, et al 2018; Schmitz, et al 2018; Ruiz-Orera and Alba 2019; Zhang, et al 2019), the de novo evolution of new protein-coding genes is also a likely contributor to the growth of gene regulatory networks.…”

Section: Introductionmentioning

confidence: 99%

Enhancers facilitate the birth of de novo genes and their integration into regulatory networks

Majic

Payne

2019

Preprint

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6Regulatory networks control the spatiotemporal gene expression patterns that give rise to and define 7 the individual cell types of multicellular organisms. In eumetazoa, distal regulatory elements called 8 enhancers play a key role in determining the structure of such networks, particularly the wiring diagram 9 of "who regulates whom." Mutations that affect enhancer activity can therefore rewire regulatory 10 networks, potentially causing changes in gene expression that are adaptive. Here, we use whole-tissue 11 and single-cell transcriptomic and chromatin accessibility data from mouse to show that enhancers play 12 an additional role in the evolution of regulatory networks: They facilitate network growth by creating 13 transcriptionally active regions of open chromatin that are conducive to de novo gene evolution.14 Specifically, our comparative transcriptomic analysis with three other mammalian species shows that 15 young, mouse-specific intergenic open reading frames are preferentially located near enhancers, 16 whereas older open reading frames are not. Mouse-specific intergenic open reading frames that are 17 proximal to enhancers are more highly and stably transcribed than those that are not proximal to 18 enhancers or promoters, and they are transcribed in a limited diversity of cellular contexts. Furthermore, 19 we report several instances of mouse-specific intergenic open reading frames that are proximal to 20 promoters that show evidence of being repurposed enhancers. We also show that open reading frames 21 gradually acquire specific interactions with enhancers over macro-evolutionary timescales, helping 22 integrate new genes into existing regulatory networks. Taken together, our results highlight a dual role 23 of enhancers in expanding and rewiring gene regulatory networks. 24 25 26 57 al. 2019), the de novo evolution of new protein-coding genes is also a likely contributor to the growth 58 of gene regulatory networks. 59An important question concerning de novo genes is how they integrate into existing regulatory 60 networks, and what role enhancers may play in this process. It has been hypothesized that enhancer 61 acquisition allows new genes to expand their breadth of expression, providing opportunities to acquire 62 3 new functions in different cellular contexts (Tautz and Domazet-Loso 2011). Enhancers may therefore 63 help new genes integrate into existing regulatory networks via edge formation and rewiring. Less 64 appreciated is the role enhancers may play in the origin of de novo genes (Wu and Sharp 2013), and 65 thus in the growth of gene regulatory networks. The physical proximity between active enhancers and 66 their target genes (Levine, et al. 2014) -facilitated by DNA looping -creates a transcriptionally 67 permissive environment that is engaged with RNA polymerase II, which may lead to the transcription 68 of DNA near the enhancer, or to the transcription of the enhancer itself, producing so-called enhancer 69 RNA (De Santa, et al. 2010; Kim, et al. 2010; Li, et al. 2016; Haberle an...

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Rapid evolution of protein diversity by de novo origination in Oryza

Cited by 130 publications

References 102 publications

The Mitochondrial Iron Regulated (MIR) gene is Oryza genus-specific and evolved before the speciation of major AA-genome lineages

The Mitochondrial Iron Regulated (MIR) gene is Oryza genus-specific and evolved before the speciation of major AA-genome lineages

De novo emergence of adaptive membrane proteins from thymine-rich genomic sequences

Enhancers facilitate the birth of de novo genes and their integration into regulatory networks

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