Trajectories of Homoeolog-Specific Expression in Allotetraploid Tragopogon castellanus Populations of Independent Origins

Polyploidization can have a significant ecological and evolutionary impact by providing substantially more genetic material that may result in novel phenotypes upon which selection may act. While the effects of polyploidization are broadly reviewed across the plant tree of life, the reproducibility of these effects within naturally occurring, independently formed polyploids is poorly characterized. The flowering plant genus Tragopogon (Asteraceae) offers a rare glimpse into the intricacies of repeated allopolyploid formation with both nascent (< 90 years old) and more ancient (mesopolyploids) formations. Neo- and mesopolyploids in Tragopogon have formed repeatedly and have extant diploid progenitors that facilitate the comparison of genome evolution after polyploidization across a broad span of evolutionary time. Here, we examine four independently formed lineages of the mesopolyploid Tragopogon castellanus for homoeolog expression changes and fractionation after polyploidization. We show that expression changes are remarkably similar among these independently formed polyploid populations with large convergence among expressed loci, moderate convergence among loci lost, and stochastic silencing. We further compare and contrast these results for T. castellanus with two nascent Tragopogon allopolyploids. While homoeolog expression bias was balanced in both nascent polyploids and T. castellanus, the degree of additive expression was significantly different, with the mesopolyploid populations demonstrating more non-additive expression. We suggest that gene dosage and expression noise minimization may play a prominent role in regulating gene expression patterns immediately after allopolyploidization as well as deeper into time, and these patterns are conserved across independent polyploid lineages.

LCM and RNA-seq analyses revealed roles of cell cycle and translational regulation and homoeolog expression bias in cotton fiber cell initiation

Background Cotton fibers provide a powerful model for studying cell differentiation and elongation. Each cotton fiber is a singular and elongated cell derived from epidermal-layer cells of a cotton seed. Efforts to understand this dramatic developmental shift have been impeded by the difficulty of separation between fiber and epidermal cells. Results Here we employed laser-capture microdissection (LCM) to separate these cell types. RNA-seq analysis revealed transitional differences between fiber and epidermal-layer cells at 0 or 2 days post anthesis. Specifically, down-regulation of putative cell cycle genes was coupled with upregulation of ribosome biosynthesis and translation-related genes, which may suggest their respective roles in fiber cell initiation. Indeed, the amount of fibers in cultured ovules was increased by cell cycle progression inhibitor, Roscovitine, and decreased by ribosome biosynthesis inhibitor, Rbin-1. Moreover, subfunctionalization of homoeologs was pervasive in fiber and epidermal cells, with expression bias towards 10% more D than A homoeologs of cell cycle related genes and 40–50% more D than A homoeologs of ribosomal protein subunit genes. Key cell cycle regulators were predicted to be epialleles in allotetraploid cotton. MYB-transcription factor genes displayed expression divergence between fibers and ovules. Notably, many phytohormone-related genes were upregulated in ovules and down-regulated in fibers, suggesting spatial-temporal effects on fiber cell development. Conclusions Fiber cell initiation is accompanied by cell cycle arrest coupled with active ribosome biosynthesis, spatial-temporal regulation of phytohormones and MYB transcription factors, and homoeolog expression bias of cell cycle and ribosome biosynthesis genes. These valuable genomic resources and molecular insights will help develop breeding and biotechnological tools to improve cotton fiber production.

Parental legacy and regulatory novelty in Brachypodium diurnal transcriptomes accompanying their polyploidy

Polyploidy is a widespread phenomenon in eukaryotes that can lead to phenotypic novelty and has important implications for evolution and diversification. The modification of phenotypes in polyploids relative to their diploid progenitors may be associated with altered gene expression. However, it is largely unknown how interactions between duplicated genes affect their diurnal expression in allopolyploid species. In this study, we explored parental legacy and hybrid novelty in the transcriptomes of an allopolyploid species and its diploid progenitors. We compared the diurnal transcriptomes of representative Brachypodium cytotypes, including the allotetraploid Brachypodium hybridum and its diploid progenitors Brachypodium distachyon and Brachypodium stacei. We also artificially induced an autotetraploid B. distachyon. We identified patterns of homoeolog expression bias (HEB) across Brachypodium cytotypes and time-dependent gain and loss of HEB in B. hybridum. Furthermore, we established that many genes with diurnal expression experienced HEB, while their expression patterns and peak times were correlated between homoeologs in B. hybridum relative to B. distachyon and B. stacei, suggesting diurnal synchronization of homoeolog expression in B. hybridum. Our findings provide insight into the parental legacy and hybrid novelty associated with polyploidy in Brachypodium, and highlight the evolutionary consequences of diurnal transcriptional regulation that accompanied allopolyploidy.

Homoeolog expression bias and expression level dominance (ELD) in four tissues of natural allotetraploid Brassica napus

Background: Allopolyploidy is widespread in angiosperms, and they can coordinate two or more different genomes through genetic and epigenetic modifications to exhibit stronger vigor and adaptability. To explore the changes in homologous gene expression patterns in the natural allotetraploid Brassica napus (AnAnCnCn) relative to its two diploid progenitors, B. rapa (ArAr) and B. oleracea (CoCo), after approximately 7,500 years of domestication, the global gene pair expression patterns in four major tissues (stems, leaves, flowers and siliques) of these three species were analyzed using an RNA sequencing approach.Results: The results showed that the ‘transcriptomic shock’ phenomenon was alleviated in natural B. napus after approximately 7,500 years of natural domestication, and most differentially expressed genes (DEGs) in B. napus were downregulated relative to those in its two diploid progenitors. The KEGG analysis indicated that three pathways related to photosynthesis were enriched in both comparison groups (AnAnCnCn vs ArAr and AnAnCnCn vs CoCo), and these pathways were all downregulated in four tissues of B. napus. In addition, homoeolog expression bias and expression level dominance (ELD) in B. napus were thoroughly studied through analysis of expression levels of 27609 B. rapa-B. oleracea orthologous gene pairs. The overwhelming majority of gene pairs (an average of 86.7%) in B. napus maintained their expression pattern in two diploid progenitors, and approximately 78.1% of the gene pairs showed expression bias with a preference toward the A subgenome. Overall, an average of 48%, 29.7% and 22.3% homologous gene pairs exhibited additive expression, ELD and transgressive expression in B. napus, respectively. The ELD bias varies from tissue to tissue; specifically, more gene pairs in stems and siliques showed ELD-A, whereas the opposite was observed in leaves and flowers. More transgressive upregulation, rather than downregulation, was observed in gene pairs of B. napus.Conclusions: In general, these results may provide a comprehensive understanding of the changes in homologous gene expression patterns in natural B. napus after approximately 7,500 years of evolution and domestication and may enhance our understanding of allopolyploidy.

Homoeolog expression bias and expression level dominance (ELD) in four tissues of natural allotetraploid Brassica napus

Background: Allopolyploidy is widespread in angiosperms, and they can coordinate two or more different genomes through genetic and epigenetic modifications to exhibit stronger vigor and adaptability. To explore the changes in homologous gene expression patterns in the natural allotetraploid Brassica napus (AnAnCnCn) relative to its two diploid progenitors, B. rapa (ArAr) and B. oleracea (CoCo), after approximately 7,500 years of domestication, the global gene pair expression patterns in four major tissues (stems, leaves, flowers and siliques) of these three species were analyzed using an RNA sequencing approach. Results: The results showed that the ‘transcriptomic shock’ phenomenon was alleviated in natural B. napus after approximately 7,500 years of natural domestication, and most differentially expressed genes (DEGs) in B. napus were downregulated relative to those in its two diploid progenitors. The KEGG analysis indicated that three pathways related to photosynthesis were enriched in both comparison groups (AnAnCnCn vs ArAr and AnAnCnCn vs CoCo), and these pathways were all downregulated in four tissues of B. napus. In addition, homoeolog expression bias and expression level dominance (ELD) in B. napus were thoroughly studied through analysis of expression levels of 27609 B. rapa-B. oleracea orthologous gene pairs. The overwhelming majority of gene pairs (an average of 86.7%) in B. napus maintained their expression pattern in two diploid progenitors, and approximately 78.1% of the gene pairs showed expression bias with a preference toward the A subgenome. Overall, an average of 48%, 29.7% and 22.3% homologous gene pairs exhibited additive expression, ELD and transgressive expression in B. napus, respectively. The ELD bias varies from tissue to tissue; specifically, more gene pairs in stems and siliques showed ELD-A, whereas the opposite was observed in leaves and flowers. More transgressive upregulation, rather than downregulation, was observed in gene pairs of B. napus. Conclusions: In general, these results may provide a comprehensive understanding of the changes in homologous gene expression patterns in natural B. napus after approximately 7,500 years of evolution and domestication and may enhance our understanding of allopolyploidy.

Homoeolog expression bias and expression level dominance (ELD) in four tissues of natural allotetraploid Brassica napus

Background: Allopolyploidy is widespread in angiosperms, and they can coordinate two or more different genomes through genetic and epigenetic modifications to exhibit stronger vigor and adaptability. To explore the changes in homologous gene expression patterns in the natural allotetraploid Brassica napus (AnAnCnCn) relative to its two diploid progenitors, B. rapa (ArAr) and B. oleracea (CoCo), after approximately 7,500 years of domestication, the global gene pair expression patterns in four major tissues (stems, leaves, flowers and siliques) of these three species were analyzed using an RNA sequencing approach. Results: The results showed that the ‘transcriptomic shock’ phenomenon was alleviated in natural B. napus after approximately 7,500 years of natural domestication, and most differentially expressed genes (DEGs) in B. napus were downregulated relative to those in its two diploid progenitors. The KEGG analysis indicated that three pathways related to photosynthesis were enriched in both comparison groups (AnAnCnCn vs ArAr and AnAnCnCn vs CoCo), and these pathways were all downregulated in four tissues of B. napus. In addition, homoeolog expression bias and expression level dominance (ELD) in B. napus were thoroughly studied through analysis of expression levels of 27609 B. rapa-B. oleracea orthologous gene pairs. The overwhelming majority of gene pairs (an average of 86.7%) in B. napus maintained their expression pattern in two diploid progenitors, and approximately 78.1% of the gene pairs showed expression bias with a preference toward the A subgenome. Overall, an average of 48%, 29.7% and 22.3% homologous gene pairs exhibited additive expression, ELD and transgressive expression in B. napus, respectively. The ELD bias varies from tissue to tissue; specifically, more gene pairs in stems and siliques showed ELD-A, whereas the opposite was observed in leaves and flowers. More transgressive upregulation, rather than downregulation, was observed in gene pairs of B. napus. Conclusions: In general, these results may provide a comprehensive understanding of the changes in homologous gene expression patterns in natural B. napus after approximately 7,500 years of evolution and domestication and may enhance our understanding of allopolyploidy.

Homoeolog expression bias and expression level dominance (ELD) in four tissues of natural allotetraploid Brassica napus

Background: Allopolyploidy is widespread in angiosperms, and they can coordinate two or more different genomes through genetic and epigenetic modifications to exhibit stronger vigor and adaptability. To explore the changes in homologous gene expression patterns in the natural allotetraploidBrassica napus(AnAnCnCn) relative to its two diploid progenitors, B. rapa(ArAr) and B. oleracea(CoCo), after approximately 7,500 years of domestication, the global gene pair expression patterns in four major tissues (stems, leaves, flowers and siliques) of these three species were analyzed using an RNA sequencing approach. Results: The results showed that the ‘transcriptomic shock’ phenomenon was alleviated in natural B. napusafter approximately 7,500 years of natural domestication, andmost differentially expressed genes (DEGs) in B. napuswere downregulated relative to those in its two diploid progenitors. The KEGG analysis indicated that three pathways related to photosynthesis were enriched in both comparison groups (AnAnCnCnvs ArArand AnAnCnCnvs CoCo), and these pathways were all downregulated in four tissues of B. napus. In addition, the homoeolog expression bias and expression level dominance (ELD) in B. napuswere thoroughly studied through analysis of the expression levels of 27609 B. rapa-B. oleraceaorthologous gene pairs. The overwhelming majority of gene pairs (an average of 86.7%) in B. napusmaintained their expression pattern in two diploid progenitors, and approximately 78.1% of the gene pairs showed expression bias with a preference toward the A subgenome. Overall, an average of 48%, 29.7% and 22.3% homologous gene pairs exhibited additivity expression, ELD and transgressive expression inB. napus, respectively. The ELD bias varies from tissue to tissue; specifically, more gene pairs in stems and siliques showed ELD-A, whereas the opposite was observed in leaves and flowers. More transgressive upregulationexpression, rather than downregulationexpression, was observedin gene pairs of B. napus. Conclusions:In general, these results may provide a comprehensive understanding of the changes in homologous gene expression patterns in natural B. napusafter approximately 7,500 years of evolution and domestication and may enhance our understanding ofallopolyploidy.

Homoeolog expression bias and expression level dominance (ELD) in four tissues of natural allotetraploid Brassica napus

Background:Allopolyploids are widespread in angiosperms, and they can coordinate two or more different genomes through genetic and epigenetic modifications to exhibit stronger growth vigor and adaptability. To explore the changes in homologous gene expression patterns in the natural allotetraploidBrassica napus(AnAnCnCn) relative to its two diploid progenitors, B. rapa(ArAr) and B. oleracea(CoCo), after approximately7,500 years of domestication, the global gene pair expression patterns in four major tissues (stems, leaves, flowers and siliques) of these three species were analyzed using an RNA sequencing approach. Results:The results showed that the ‘transcriptomic shock’ phenomenon was alleviated in natural B. napusafter approximately7,500 years of natural domestication, andmost differentially expressed genes (DEGs) in B. napuswere downregulated relative to those in its two diploid progenitors. The KEGG analysis indicated that three pathways related to photosynthesis were enriched in both comparison groups (AnAnCnCnvs ArArand AnAnCnCnvs CoCo), and these pathways were all downregulated in four tissues of B. napus. In addition, the homoeolog expression bias and expression level dominance (ELD) inB. napuswere thoroughly studied through analysis of the expression levels of 27609 B. rapa-B. oleraceaorthologous gene pairs. The overwhelming majority of gene pairs (an average of 86.7%) in B. napusmaintained their expression pattern in two diploid progenitors, and approximately 78.1% of the gene pairs showed expression bias with a preference toward the A subgenome. Overall, an average of 48%, 29.7% and 22.3% homologous gene pairs exhibited additivity expression, ELD and transgressive expression in B. napus, respectively. The ELD bias varies from tissue to tissue; specifically, more gene pairs in stems and siliques showed ELD-A, whereas the opposite was observed in leaves and flowers. More transgressive upregulationexpression, rather than downregulationexpression,was observedin gene pairs of B. napus. Conclusions:In general, these results may provide a comprehensive understanding of the changes in homologous gene expression patterns in natural B. napusafter approximately 7,500 years of evolution and domestication and mayenhance our understanding of allopolyploids.