Gene Expression In Polyploids Research Articles

Evolutionary Dynamics of Chromatin Structure and Duplicate Gene Expression in Diploid and Allopolyploid Cotton.

Polyploidy is a prominent mechanism of plant speciation and adaptation, yet the mechanistic understandings of duplicated gene regulation remain elusive. Chromatin structure dynamics are suggested to govern gene regulatory control. Here, we characterized genome-wide nucleosome organization and chromatin accessibility in allotetraploid cotton, Gossypium hirsutum (AADD, 2n = 4X = 52), relative to its two diploid parents (AA or DD genome) and their synthetic diploid hybrid (AD), using DNS-seq. The larger A-genome exhibited wider average nucleosome spacing in diploids, and this intergenomic difference diminished in the allopolyploid but not hybrid. Allopolyploidization also exhibited increased accessibility at promoters genome-wide and synchronized cis-regulatory motifs between subgenomes. A prominent cis-acting control was inferred for chromatin dynamics and demonstrated by transposable element removal from promoters. Linking accessibility to gene expression patterns, we found distinct regulatory effects for hybridization and later allopolyploid stages, including nuanced establishment of homoeolog expression bias and expression level dominance. Histone gene expression and nucleosome organization are coordinated through chromatin accessibility. Our study demonstrates the capability to track high-resolution chromatin structure dynamics and reveals their role in the evolution of cis-regulatory landscapes and duplicate gene expression in polyploids, illuminating regulatory ties to subgenomic asymmetry and dominance.

Reduced chromatin accessibility underlies gene expression differences in homologous chromosome arms of diploid Aegilops tauschii and hexaploid wheat.

BackgroundPolyploidy is centrally important in the evolution and domestication of plants because it leads to major genomic changes, such as altered patterns of gene expression, which are thought to underlie the emergence of new traits. Despite the common occurrence of these globally altered patterns of gene expression in polyploids, the mechanisms involved are not well understood.ResultsUsing a precisely defined framework of highly conserved syntenic genes on hexaploid wheat chromosome 3DL and its progenitor 3 L chromosome arm of diploid Aegilops tauschii, we show that 70% of these gene pairs exhibited proportionately reduced gene expression, in which expression in the hexaploid context of the 3DL genes was ∼40% of the levels observed in diploid Ae tauschii. Several genes showed elevated expression during the later stages of grain development in wheat compared with Ae tauschii. Gene sequence and methylation differences probably accounted for only a few cases of differences in gene expression. In contrast, chromosome-wide patterns of reduced chromatin accessibility of genes in the hexaploid chromosome arm compared with its diploid progenitor were correlated with both reduced gene expression and the imposition of new patterns of gene expression.ConclusionsOur pilot-scale analyses show that chromatin compaction may orchestrate reduced gene expression levels in the hexaploid chromosome arm of wheat compared to its diploid progenitor chromosome arm.

Histone Modifications Define Expression Bias of Homoeologous Genomes in Allotetraploid Cotton.

Histone modifications regulate gene expression in eukaryotes, but their roles in gene expression changes in interspecific hybrids or allotetraploids are poorly understood. Histone modifications can be mapped by immunostaining of metaphase chromosomes at the single cell level and/or by chromatin immunoprecipitation-sequencing (ChIP-seq) for analyzing individual genes. Here, we comparatively analyzed immunostained metaphase chromosomes and ChIP-seq of individual genes, which revealed a chromatin basis for biased homoeologous gene expression in polyploids. We examined H3K4me3 density and transcriptome maps in root-tip cells of allotetraploid cotton (Gossypium hirsutum). The overall H3K4me3 levels were relatively equal between A and D chromosomes, which were consistent with equal numbers of expressed genes between the two subgenomes. However, intensities per chromosomal area were nearly twice as high in the D homeologs as in the A homeologs. Consistent with the cytological observation, ChIP-seq analysis showed that more D homeologs with biased H3K4me3 levels than A homeologs with biased modifications correlated with the greater number of the genes with D-biased expression than that with A-biased expression in most homeologous chromosome pairs. Two chromosomes displayed different expression levels compared with other chromosomes, which correlate with known translocations and may affect the local chromatin structure and expression levels for the genes involved. This example of genome-wide histone modifications that determine expression bias of homeologous genes in allopolyploids provides a molecular basis for the evolution and domestication of polyploid species, including many important crops.

Nonadditive gene expression in polyploids.

Allopolyploidy involves hybridization and duplication of divergent parental genomes and provides new avenues for gene expression. The expression levels of duplicated genes in polyploids can show deviation from parental additivity (the arithmetic average of the parental expression levels). Nonadditive expression has been widely observed in diverse polyploids and comprises at least three possible scenarios: (a) The total gene expression level in a polyploid is similar to that of one of its parents (expression-level dominance); (b) total gene expression is lower or higher than in both parents (transgressive expression); and (c) the relative contribution of the parental copies (homeologs) to the total gene expression is unequal (homeolog expression bias). Several factors may result in expression nonadditivity in polyploids, including maternal-paternal influence, gene dosage balance, cis- and/or trans-regulatory networks, and epigenetic regulation. As our understanding of nonadditive gene expression in polyploids remains limited, a new generation of investigators should explore additional phenomena (i.e., alternative splicing) and use other high-throughput "omics" technologies to measure the impact of nonadditive expression on phenotype, proteome, and metabolome.

Insights into the evolution of duplicate gene expression in polyploids fromGossypiumThis paper is one of a selection of papers published in the Special Issue on Systematics Research.

Polyploidy is a prominent mechanism of speciation in plants that can lead to novel phenotypes. Polyploidy is characterized by novel genetic and genomic consequences that provide raw material for morphological evolution. Polyploids often exhibit changes in genome organization and gene expression compared with their diploid progenitors. The five allopolyploid cotton (Gossypium) species and newly created cotton neopolyploids have been developed as a useful group for studies of duplicated gene expression in polyploids. Here I review recent studies on the evolution of duplicate gene expression in polyploid cotton. In addition I present new expression data from cotton neopolyploids that address the effects on expression of adding a third genome in an allohexaploid, and that provide insights into fine scale organ-specific silencing. Substantial changes in gene expression have occurred in homoeologous genes (gene pairs duplicated by polyploidy), including organ-specific gene silencing and subfunctionalization. Many of the changes in gene expression have occurred on an evolutionary timescale, whereas others occur immediately after genome merger and within a few generations. Abiotic stress can affect the expression of homoeologous gene expression, causing expression partitioning between homoeologs. To examine the effects of interspecific hybridization, without chromosome doubling, on gene expression, interspecific hybrids have been studied. Extensive variation in allelic expression was observed upon hybridization that varied by gene, organ, and genotype. Several hypotheses have been proposed for why gene expression is altered in allopolyploids and interspecific hybrids.

A Novel Approach for Characterizing Expression Levels of Genes Duplicated by Polyploidy

Studying gene expression in polyploids is complicated by genomewide gene duplication and the problem of distinguishing transcript pools derived from each of the two homeologous genomes such as the A- and D-genomes of allotetraploid Gossypium. Short oligonucleotide probes designed to specifically target several hundred homeologous gene pairs of Gossypium were printed on custom NimbleGen microarrays. These results demonstrate that relative expression levels of homeologous genes may be measured by microarrays and that deviation from equal expression levels of homeologous loci may be common in the allotetraploid nucleus of Gossypium.

Evolutionary dynamics and preferential expression of homeologous 18S-5.8S-26S nuclear ribosomal genes in natural and artificial glycine allopolyploids.

Polyploidy is an important evolutionary process in plants, but much remains to be learned about the evolution of gene expression in polyploids. Evolution and expression of the 18S-5.8S-26S ribosomal gene family was investigated at homeologous loci in the Glycine subgenus Glycine perennial soybean polyploid complex, which consists of several diploid genomes that have formed allopolyploids in various combinations, often recurrently. A semiquantitative PCR method targeting the internal transcribed spacer (ITS) of the 18S-5.8S-26S nuclear ribosomal DNA (nrDNA) was used to survey the ratio between homeologous repeats in polyploid genomes and to test for preferential expression of homeologous nrDNA loci. Most natural polyploids possess one predominant nrDNA homeolog in their genome. Analysis of F2 segregation in an artificial cross suggested that in some plants, most or all repeats at one homeologous locus have been lost, whereas in other plants two loci remain, but both have been homogenized by concerted evolution. In most natural allopolyploids harboring a relatively balanced ratio of homeologs, one homeolog was expressed preferentially, but in the majority of plants, low levels of transcription could be detected from the other homeolog. Individuals within some tetraploid taxa varied as to which homeolog was expressed preferentially. In some plants, the degree of preferential expression also varied among tissues. Preferential expression was absent in synthetic polyploids and in some artificial diploid hybrids, suggesting that nucleolar dominance is not necessarily a direct result of hybridization or polyploidization. The establishment of preferential expression in Glycine allopolyploids appears to be either stochastic within lineages or genotype specific.

Hybrid necrosis in triticale and the expression of necrosis genes in allopolyploids

The occurrence in triticale of four different genes causing hybrid necrosis is described: Ne1 and Ne2 in the B genome of wheat and Ner1 and Ner2 in the rye genome. Hybrid necrosis develops due to dominant complementary interaction of two genes. This interaction in triticale, however, may take place not only between genes belonging to the same genome but also between genes of different genomes. In triticale, these genes can cause hybrid necrosis in four different combinations. The inheritance of the phenomenon in triticale is, therefore, more complicated than it is in wheat or rye. To avoid hybrid necrosis in triticale, attention should be paid that no necrosis genes are introduced into the primary triticale stocks from the wheat and rye parents. The expression of necrosis genes is influenced by the level of ploidy. Any additional genome - A, B, D, or R - may exert a suppressing effect on the expression of necrosis genes. Therefore, when identifying genotypes of triticale with regard to their necrosis genes, the level of ploidy has to be accounted for. Moreover, the present results illustrate that gene expression in polyploids is not only determined by interactions with other single genes but that it may also be modified by the total genotype of the respective individual.