Genetics of alternative splicing evolution during sunflower domestication

Smith, Chris C. R.; Tittes, Silas; Mendieta, J. Paul; Collier-zans, Erin C. E.; Rowe, Heather C.; Rieseberg, Loren H.; Kane, Nolan C.

doi:10.1073/pnas.1803361115

Cited by 42 publications

(54 citation statements)

References 41 publications

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“…While introns do add noncoding length to genes, thus incurring costs during cell division and transcription, they offer the potential benefit of alternative splicing, contributing valuable flexibility in gene expression and regulation (Dibb, 1993;Jo & Choi, 2015;Lynch et al, 2006;Smith et al, 2018). Alternative splicing may in fact confer greater genetic flexibility to the mitochondrial genomes of plants and fungi compared to those of the relatively intron-poor bilateral animals (Dibb, 1993;Jo & Choi, 2015;Kazan, 2003;Keren, Lev-Maor, & Ast, 2010;Lynch et al, 2006).…”

Section: Discussionmentioning

confidence: 99%

Genome streamlining via complete loss of introns has occurred multiple times in lichenized fungal mitochondria

Pogoda

Keepers

Nadiadi

et al. 2019

Ecology and Evolution

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Reductions in genome size and complexity are a hallmark of obligate symbioses. The mitochondrial genome displays clear examples of these reductions, with the ancestral alpha‐proteobacterial genome size and gene number having been reduced by orders of magnitude in most descendent modern mitochondrial genomes. Here, we examine patterns of mitochondrial evolution specifically looking at intron size, number, and position across 58 species from 21 genera of lichenized Ascomycete fungi, representing a broad range of fungal diversity and niches. Our results show that the cox1 gene always contained the highest number of introns out of all the mitochondrial protein‐coding genes, that high intron sequence similarity (>90%) can be maintained between different genera, and that lichens have undergone at least two instances of complete, genome‐wide intron loss consistent with evidence for genome streamlining via loss of parasitic, noncoding DNA, in Phlyctis boliviensis and Graphis lineola . Notably, however, lichenized fungi have not only undergone intron loss but in some instances have expanded considerably in size due to intron proliferation (e.g., Alectoria fallacina and Parmotrema neotropicum ), even between closely related sister species (e.g., Cladonia ). These results shed light on the highly dynamic mitochondrial evolution that is occurring in lichens and suggest that these obligate symbiotic organisms are in some cases undergoing recent, broad‐scale genome streamlining via loss of protein‐coding genes as well as noncoding, parasitic DNA elements.

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Section: Discussionmentioning

confidence: 99%

Genome streamlining via complete loss of introns has occurred multiple times in lichenized fungal mitochondria

Pogoda

Keepers

Nadiadi

et al. 2019

Ecology and Evolution

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“…Most studies on gene expression focus on expression abundance (the number of transcripts for a whole gene). However, alternative splicing resulting in the difference of transcript proportions can also contribute to adaptation (Barbosa-Morais et al 2012; Gamazon and Stranger 2014; Smith et al 2018). Therefore, understanding the transcriptomic basis of parallel phenotypic evolution requires studies of both expression abundance and alternative splicing, although the latter aspect has rarely been studied.…”

Section: Introductionmentioning

confidence: 99%

Parallel and Population-specific Gene Regulatory Evolution in Cold-Adapted Fly Populations

Huang

Lack

Hoppel

et al. 2019

Preprint

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17Changes in gene regulation at multiple levels may comprise an important share of the molecular 18 changes underlying adaptive evolution in nature. However, few studies have assayed within-and 19 between-population variation in gene regulatory traits at a transcriptomic scale, and therefore 20 inferences about the characteristics of adaptive regulatory changes have been elusive. Here, we assess 21 quantitative trait differentiation in gene expression levels and alternative splicing (intron usage) 22 between three closely-related pairs of natural populations of Drosophila melanogaster from contrasting 23 thermal environments that reflect three separate instances of cold tolerance evolution. The cold-24 adapted populations were known to show population genetic evidence for parallel evolution at the 25 SNP level, and here we find significant although somewhat limited evidence for parallel expression 26 evolution between them, and less evidence for parallel splicing evolution. We find that genes with 27 mitochondrial functions are particularly enriched among candidates for adaptive expression 28 evolution. We also develop a method to estimate cis-versus trans-encoded contributions to 29 expression or splicing differences that does not rely on the presence of fixed differences between 30 parental strains. Applying this method, we infer important roles of both cis-and trans-regulation 31 among our putatively adaptive expression and splicing differences. The apparent contributions of cis-32 versus trans-regulation to adaptive evolution vary substantially among population pairs, with an 33 Ethiopian pair showing pervasive trans-effects, suggesting that basic characteristics of regulatory 34 evolution may depend on biological context. These findings expand our knowledge of adaptive gene 35 regulatory evolution and our ability to make inferences about this important and widespread process.36 37 50 The level of parallelism for gene expression abundance changes varies across study systems. In some 51 taxa and natural conditions, significantly more genes show parallel changes (repeatedly up-or down-52 regulated in one ecotype relative to the other among independent population pairs) than anti-53 directional changes (Zhao et al. 2015; Hart et al. 2018; Kitano et al. 2018; McGirr and Martin.54 2018). However, some other cases did not show significant parallel patterns, or they even show anti-55 parallel patterns (Derome et al. 2006; Lai et al. 2008; Hanson et al. 2017). The varying degree of 56 parallelism may partly be explained by the level of divergence among ancestors: more closely related 57 ancestors are expected to show a higher degree of parallel genetic evolution underlie similar 58 phenotypic evolution (Conte et al. 2012; Rosenblum et al. 2014). 59 60 Furthermore, gene expression evolution can be caused by the same or different molecular 61 underpinnings. Because of the difficulties of mapping expression QTL, a first step is to classify the 62 expression evolution into two regulatory classes. Cis-regulatory change...

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“…More recently, other authors [ 43 ] analyzing transcriptomes of wild and domesticated sunflowers have identified differential splicing divergence related to domestication, especially through intron retention. Differential splicing has been related to genes involved in functions related to seed development.…”

Section: Introductionmentioning

confidence: 99%

Specific LTR-Retrotransposons Show Copy Number Variations between Wild and Cultivated Sunflowers

Mascagni

Vangelisti

Giordani

et al. 2018

Genes

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The relationship between variation of the repetitive component of the genome and domestication in plant species is not fully understood. In previous work, variations in the abundance and proximity to genes of long terminal repeats (LTR)-retrotransposons of sunflower (Helianthus annuus L.) were investigated by Illumina DNA sequencingtocompare cultivars and wild accessions. In this study, we annotated and characterized 22 specific retrotransposon families whose abundance varies between domesticated and wild genotypes. These families mostly belonged to the Chromovirus lineage of the Gypsy superfamily and were distributed overall chromosomes. They were also analyzed in respect to their proximity to genes. Genes close to retrotransposon were classified according to biochemical pathways, and differences between domesticated and wild genotypes are shown. These data suggest that structural variations related to retrotransposons might have occurred to produce phenotypic variation between wild and domesticated genotypes, possibly by affecting the expression of genes that lie close to inserted or deleted retrotransposons and belong to specific biochemical pathways as those involved in plant stress responses.

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Genetics of alternative splicing evolution during sunflower domestication

Cited by 42 publications

References 41 publications

Genome streamlining via complete loss of introns has occurred multiple times in lichenized fungal mitochondria

Genome streamlining via complete loss of introns has occurred multiple times in lichenized fungal mitochondria

Parallel and Population-specific Gene Regulatory Evolution in Cold-Adapted Fly Populations

Specific LTR-Retrotransposons Show Copy Number Variations between Wild and Cultivated Sunflowers

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