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Gene-expression novelty in allopolyploid cotton: a proteomic perspective.

ABSTRACT: Allopolyploidization is accompanied by changes in gene expression that are thought to contribute to phenotypic diversification. Here we describe global changes in the single-celled cotton fiber proteome of two natural allopolyploid species (Gossypium hirsutum and G. barbadense) and living models of their diploid parents using two different proteomic approaches. In total, 1323 two-dimensional gel electrophoresis spots and 1652 identified proteins by isobaric tags for relative and absolute quantitation were quantitatively profiled during fiber elongation. Between allopolyploids and their diploid A- and D-genome progenitors, amounts of differential expression ranged from 4.4 to 12.8%. Over 80% of the allopolyploid proteome was additively expressed with respect to progenitor diploids. Interestingly, the fiber proteome of G. hirsutum resembles the parental A-genome more closely, where long, spinable fiber first evolved, than does the fiber proteome of G. barbadense. More protein expression patterns were A-dominant than D-dominant in G. hirsutum, but in G. barbadense, the direction of expression-level dominance switched from the D-genome to the A-genome during fiber development. Comparison of developmental changes between the two allopolyploid species revealed a high level of proteomic differentiation despite their shared ancestry, relatively recent evolutionary divergence, and similar gross morphology. These results suggest that the two allopolyploid species have achieved superficially similar modern fiber phenotypes through different evolutionary routes at the proteome level. We also detected homeolog-specific expression for 1001 proteins and present a novel approach to infer the relationship between homeolog-specific and duplicate expression patterns. Our study provides a proteomic perspective on understanding evolutionary consequences of allopolyploidization, showing how protein expression has been altered by polyploidization and subsequently has diversified among species.

SUBMITTER: Hu G

PROVIDER: S-EPMC4423384 | biostudies-literature | 2015 May

REPOSITORIES: biostudies-literature

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Gene-expression novelty in allopolyploid cotton: a proteomic perspective.

Hu Guanjing G Koh Jin J Yoo Mi-Jeong MJ Chen Sixue S Wendel Jonathan F JF

Genetics 20150302 1

Allopolyploidization is accompanied by changes in gene expression that are thought to contribute to phenotypic diversification. Here we describe global changes in the single-celled cotton fiber proteome of two natural allopolyploid species (Gossypium hirsutum and G. barbadense) and living models of their diploid parents using two different proteomic approaches. In total, 1323 two-dimensional gel electrophoresis spots and 1652 identified proteins by isobaric tags for relative and absolute quantit ...[more]

PMID: 25735302

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Project description:BackgroundModern allotetraploid cotton contains an "A" and "D" genome from an ancestral polyploidy event that occurred approximately 1-2 million years ago. Diploid A- and D-genome species can be compared to the A- and D-genomes found within these allotetraploids to make evolutionary inferences about polyploidy. In this paper we present a comprehensive EST assembly derived from diploid and model allotetraploid cottons and demonstrate several evolutionary inferences regarding genic evolution that can be drawn from these data.ResultsWe generated a set of cotton expressed sequence tags (ESTs), comprising approximately 4.4 million Sanger and next-generation (454) transcripts supplemented by approximately 152 million Illumina reads from diploid and allotetraploid cottons. From the EST alignments we inferred 259,192 genome-specific single nucleotide polymorphisms (SNPs). Molecular evolutionary analyses of protein-coding regions demonstrate that the rate of nucleotide substitution has increased among both allotetraploid genomes relative to the diploids, and that the ratio of nonsynonymous to synonymous substitutions has increased in one of the two polyploid lineages we sampled. We also use these SNPs to show that a surprisingly high percentage of duplicate genes (~7 %) show a signature of non-independent evolution in the allotetraploid nucleus, having experienced one or more episodes of nonreciprocal homoeologous recombination (NRHR).ConclusionsIn this study we characterize the functional and mutational properties of the cotton transcriptome, produce a large genome-specific SNP database, and detect illegitimate genetic exchanges between duplicate genomes sharing a common allotetraploid nucleus. Our findings have important implications for our understanding of the consequences of polyploidy and duplicate gene evolution. We demonstrate that cotton genes have experienced an increased rate of molecular evolution following duplication by polyploidy, and that polyploidy has enabled considerable levels of nonreciprocal exchange between homoeologous genes.

Project description:Background and aimsAllopolyploidization is a widespread phenomenon known to generate novel phenotypes by merging evolutionarily distinct parental genomes and regulatory networks in a single nucleus. The objective of this study was to investigate the transcriptional regulation associated with phenotypic novelty in coffee beans of the allotetraploid Coffea arabica.MethodsA genome-wide comparative transcriptomic analysis was performed in C. arabica and its two diploid progenitors, C. canephora and C. eugenioides. Gene expression patterns and homeologue expression were studied on seeds at five different maturation stages. The involvement of homeologue expression bias (HEB) in specific traits was addressed both by functional enrichment analyses and by the study of gene expression in the caffeine and chlorogenic acid biosynthesis pathways.Key resultsExpression-level dominance in C. arabica seed was observed for most of the genes differentially expressed between the species. Approximately a third of the genes analysed showed HEB. This proportion increased during seed maturation but the biases remained equally distributed between the sub-genomes. The relative expression levels of homeologues remained relatively constant during maturation and were correlated with those estimated in leaves of C. arabica and interspecific hybrids between C. canephora and C. eugenioides. Functional enrichment analyses performed on genes exhibiting HEB enabled the identification of processes potentially associated with physiological traits. The expression profiles of the genes involved in caffeine biosynthesis mirror the differences observed in the caffeine content of mature seeds of C. arabica and its parental species.ConclusionsNeither of the two sub-genomes is globally preferentially expressed in C. arabica seeds, and homeologues appear to be co-regulated by shared trans-regulatory mechanisms. The observed HEBs are thought to be a legacy of gene expression differences inherited from diploid progenitor species. Pre-existing functional divergences between parental species appear to play an important role in controlling the phenotype of C. arabica seeds.

Project description:How allopolyploids are able not only to cope but profit from their condition is a question that remains elusive, but is of great importance within the context of successful allopolyploid evolution. One outstanding example of successful allopolyploidy is the endemic Iberian cyprinid Squalius alburnoides. Previously, based on the evaluation of a few genes, it was reported that the transcription levels between diploid and triploid S. alburnoides were similar. If this phenomenon occurs on a full genomic scale, a wide functional ''diploidization'' could be related to the success of these polyploids. We generated RNA-seq data from whole juvenile fish and from adult livers, to perform the first comparative quantitative transcriptomic analysis between diploid and triploid individuals of a vertebrate allopolyploid. Together with an assay to estimate relative expression per cell, it was possible to infer the relative sizes of transcriptomes. This showed that diploid and triploid S. alburnoides hybrids have similar liver transcriptome sizes. This in turn made it valid to directly compare the S. alburnoides RNA-seq transcript data sets and obtain a profile of dosage responses across the S. alburnoides transcriptome. We found that 64% of transcripts in juveniles' samples and 44% in liver samples differed less than twofold between diploid and triploid hybrids (similar expression). Yet, respectively 29% and 15% of transcripts presented accurate dosage compensation (PAA/PA expression ratio of 1 instead of 1.5). Therefore, an exact functional diploidization of the triploid genome does not occur, but a significant down regulation of gene expression in triploids was observed. However, for those genes with similar expression levels between diploids and triploids, expression is not globally strictly proportional to gene dosage nor is it set to a perfect diploid level. This quantitative expression flexibility may be a strong contributor to overcome the genomic shock, and be an immediate evolutionary advantage of allopolyploids.

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Gene-expression novelty in allopolyploid cotton: a proteomic perspective.

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Gene-expression novelty in allopolyploid cotton: a proteomic perspective.

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