Nonsyntenic genes drive tissue-specific dynamics of differential, nonadditive and allelic expression patterns in maize hybrids

Baldauf, Jutta A.; Marcon, Caroline; Paschold, Anja; Hochholdinger, Frank

doi:10.1104/pp.16.00262

Cited by 36 publications

(50 citation statements)

References 47 publications

(73 reference statements)

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“…C, Control; WD, water deficit stress. differential gene expression (Paschold et al, 2012;Baldauf et al, 2016). Similar genotype-associated trends of differential expression have been reported previously in these four maize genotypes on the transcriptome level (Stupar and Springer, 2006;Paschold et al, 2012;Baldauf et al, 2016) and the proteome level (Marcon et al, 2013).…”

Section: Discussionsupporting

confidence: 64%

“…differential gene expression (Paschold et al, 2012;Baldauf et al, 2016). Similar genotype-associated trends of differential expression have been reported previously in these four maize genotypes on the transcriptome level (Stupar and Springer, 2006;Paschold et al, 2012;Baldauf et al, 2016) and the proteome level (Marcon et al, 2013). Likewise, in Arabidopsis (Arabidopsis thaliana), the number of differentially expressed genes between three landraces significantly exceeded that of the corresponding reciprocal hybrids (Vuylsteke et al, 2005).…”

Section: Discussionsupporting

confidence: 57%

“…In total, 614 and 676 genes (Supplemental Table S2) under control and water deficit conditions were identified for which the expression ratio of the parental inbred lines was different from that of the reciprocal hybrids. In whole maize primary roots (Paschold et al, 2012) and root tissues (Baldauf et al, 2016), 840 and 739 genes, respectively, were reported that show allelic expression ratios in hybrids deviating from the expression ratios of the parental alleles in the inbred lines. In a pioneering study for a set of 15 maize genes, allelic expression variation was observed in response to drought stress, indicating an unequal function of the parental alleles in hybrids (Guo et al, 2004).…”

Section: Discussionmentioning

confidence: 99%

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Stability of Single-Parent Gene Expression Complementation in Maize Hybrids upon Water Deficit Stress

et al. 2016

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Heterosis is the superior performance of F1 hybrids compared with their homozygous, genetically distinct parents. In this study, we monitored the transcriptomic divergence of the maize (Zea mays) inbred lines B73 and Mo17 and their reciprocal F1 hybrid progeny in primary roots under control and water deficit conditions simulated by polyethylene glycol treatment. Single-parent expression (SPE) of genes is an extreme instance of gene expression complementation, in which genes are active in only one of two parents but are expressed in both reciprocal hybrids. In this study, 1,997 genes only expressed in B73 and 2,024 genes only expressed in Mo17 displayed SPE complementation under control and water deficit conditions. As a consequence, the number of active genes in hybrids exceeded the number of active genes in the parental inbred lines significantly independent of treatment. SPE patterns were substantially more stable to expression changes by water deficit treatment than other genotype-specific expression profiles. While, on average, 75% of all SPE patterns were not altered in response to polyethylene glycol treatment, only 17% of the remaining genotype-specific expression patterns were not changed by water deficit. Nonsyntenic genes that lack syntenic orthologs in other grass species, and thus evolved late in the grass lineage, were significantly overrepresented among SPE genes. Hence, the significant overrepresentation of nonsyntenic genes among SPE patterns and their stability under water limitation might suggest a function of these genes during the early developmental manifestation of heterosis under fluctuating environmental conditions in hybrid progeny of the inbred lines B73 and Mo17.

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Section: Discussionsupporting

confidence: 64%

Section: Discussionsupporting

confidence: 57%

Section: Discussionmentioning

confidence: 99%

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Stability of Single-Parent Gene Expression Complementation in Maize Hybrids upon Water Deficit Stress

et al. 2016

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“…Functional enrichment of genes of interest is often performed after the establishment of orthology and synteny [26, 47–50]. Synteny breaks are caused by rearrangements, the insertion of novel genes, or the presence of genes that are too diverged to establish an orthologous relationship or have undergone expansion or loss.…”

Section: Resultsmentioning

confidence: 99%

Inferring synteny between genome assemblies: a systematic evaluation

2018

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BackgroundGenome assemblies across all domains of life are being produced routinely. Initial analysis of a new genome usually includes annotation and comparative genomics. Synteny provides a framework in which conservation of homologous genes and gene order is identified between genomes of different species. The availability of human and mouse genomes paved the way for algorithm development in large-scale synteny mapping, which eventually became an integral part of comparative genomics. Synteny analysis is regularly performed on assembled sequences that are fragmented, neglecting the fact that most methods were developed using complete genomes. It is unknown to what extent draft assemblies lead to errors in such analysis.ResultsWe fragmented genome assemblies of model nematodes to various extents and conducted synteny identification and downstream analysis. We first show that synteny between species can be underestimated up to 40% and find disagreements between popular tools that infer synteny blocks. This inconsistency and further demonstration of erroneous gene ontology enrichment tests raise questions about the robustness of previous synteny analysis when gold standard genome sequences remain limited. In addition, assembly scaffolding using a reference guided approach with a closely related species may result in chimeric scaffolds with inflated assembly metrics if a true evolutionary relationship was overlooked. Annotation quality, however, has minimal effect on synteny if the assembled genome is highly contiguous.ConclusionsOur results show that a minimum N50 of 1 Mb is required for robust downstream synteny analysis, which emphasizes the importance of gold standard genomes to the science community, and should be achieved given the current progress in sequencing technology.Electronic supplementary materialThe online version of this article (10.1186/s12859-018-2026-4) contains supplementary material, which is available to authorized users.

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“…While there are some examples in the literature, and we identified a small number (<20 after accounting for false positives) of additional transcriptional fractionation events, these events are not likely to be driving substantial phenotypic variation within the species. This lack of transcriptional fractionation is consistent with previous results showing an underrepresentation of syntenic genes among differentially expressed genes and genes with non‐additive gene action (Baldauf et al ., ).…”

Section: Discussionmentioning

confidence: 97%

The limited role of differential fractionation in genome content variation and function in maize (Zea mays L.) inbred lines

et al. 2017

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SUMMARYMaize is a diverse paleotetraploid species with considerable presence/absence variation and copy number variation. One mechanism through which presence/absence variation can arise is differential fractionation. Fractionation refers to the loss of duplicate gene pairs from one of the maize subgenomes during diploidization. Differential fractionation refers to non-shared gene loss events between individuals following a whole-genome duplication event. We investigated the prevalence of presence/absence variation resulting from differential fractionation in the syntenic portion of the genome using two whole-genome de novo assemblies of the inbred lines B73 and PH207. Between these two genomes, syntenic genes were highly conserved with less than 1% of syntenic genes being subject to differential fractionation. The few variably fractionated syntenic genes that were identified are unlikely to contribute to functional phenotypic variation, as there is a significant depletion of these genes in annotated gene sets. In further comparisons of 60 diverse inbred lines, non-syntenic genes were six times more likely to be variable than syntenic genes, suggesting that comparisons among additional genome assemblies are not likely to result in the discovery of large-scale presence/absence variation among syntenic genes.

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Nonsyntenic genes drive tissue-specific dynamics of differential, nonadditive and allelic expression patterns in maize hybrids

Cited by 36 publications

References 47 publications

Stability of Single-Parent Gene Expression Complementation in Maize Hybrids upon Water Deficit Stress

Stability of Single-Parent Gene Expression Complementation in Maize Hybrids upon Water Deficit Stress

Inferring synteny between genome assemblies: a systematic evaluation

The limited role of differential fractionation in genome content variation and function in maize (Zea mays L.) inbred lines

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