Insights into the Ecology and Evolution of Polyploid Plants through Network Analysis

Gallagher, Joseph P.; Grover, Corrinne E.; Hu, Guanjing; Wendel, Jonathan F.

doi:10.1111/mec.13626

Cited by 34 publications

(29 citation statements)

References 189 publications

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“…Gallagher et al . ). Molecular ecologists, however, should not lose sight of the equal importance of experimental and field studies to evaluate the evolutionary and ecological consequences of hybridization and introgression.…”

Section: Discussionmentioning

confidence: 97%

“…Genomic analyses will undoubtedly become more sophisticated in the future to provide more detailed information on the effects of hybridization (e.g. Gallagher et al 2016). Molecular ecologists, however, should not lose sight of the equal importance of experimental and field studies to evaluate the evolutionary and ecological consequences of hybridization and introgression.…”

Section: Discussionmentioning

confidence: 99%

“…Thus, while homoploid hybrid speciation is theoretically possible under some conditions (Schumer et al 2015), convincing empirical examples remain exceptionally rare. Gallagher et al (2016) review and recommend network approaches for analysing the effects of genome duplication on the ecology and evolution of polyploid plants, and particularly the novel interactions that occur among duplicated genomes that affect gene expression and patterns of divergence, recruitment and loss of duplicated genes. They demonstrate the utility of this approach by focusing on the evolution of cotton fibres in the allopolyploid Gossypium hirsutum, the species that provides most of the world's cotton.…”

Section: Hybrid Speciation and The Evolution Of Hybrid Genomesmentioning

confidence: 99%

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Genomics of hybridization and its evolutionary consequences

2016

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Hybridization and its consequences have been of longstanding interest to evolutionary biologists. Darwin (1859) included a chapter on hybrids and the expression and causes of hybrid sterility in The Origin of Species, while the main proponents of the neoDarwinian synthesis discussed the topic at varying length in the mid-1900s (Haldane 1932;Dobzhansky 1937;Stebbins 1950;Mayr 1963). Subsequently, Grant (1981) underlined the importance of hybridization to plant evolution, devoting six chapters of Plant Speciation to the topic, while Arnold (1997;2006;2015) has written three books on hybridization and its evolutionary consequences over the last 20 years. Building upon this enduring foundation, there has been an enormous expansion in the study of hybridization over the past decade. This exciting resurgence has been fuelled by advances in DNA sequencing that now enable the rapid collection of genomic data across the tree of life and the ongoing development of population genetic theory and analytical tools that facilitate the analysis and interpretation of these powerful data.

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Section: Discussionmentioning

confidence: 97%

Section: Discussionmentioning

confidence: 99%

Section: Hybrid Speciation and The Evolution Of Hybrid Genomesmentioning

confidence: 99%

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Genomics of hybridization and its evolutionary consequences

2016

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“…As recently reviewed by Gallagher et al . (), co‐expression network analysis in polyploids not only has the potential to facilitate a better understanding of the complex ‘omics’ underpinnings of phenotypic and ecological traits, but also may provide novel insight into interactions among duplicated genes and genomes. Given that previous work in allopolyploids (e.g.…”

Section: The Extended Cis–trans Framework and Expression Patterns In mentioning

confidence: 99%

Cis–trans controls and regulatory novelty accompanying allopolyploidization

Wendel

2018

New Phytologist

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Summary Allopolyploidy is a prevalent process in plants, having important physiological, ecological and evolutionary consequences. Transcriptomic responses to genomic merger and doubling have been demonstrated in many allopolyploid systems, encompassing a diversity of phenomena including homoeolog expression bias, genome dominance, expression‐level dominance and revamping of co‐expression networks. Notwithstanding the foregoing, there remains a need to develop a conceptual framework that will stimulate a deeper understanding of these diverse phenomena and their mechanistic interrelationships. Here we introduce considerations relevant to this framework with a focus on cis–trans interactions among duplicated genes and alleles in hybrids and allopolyploids. By extending classic allele‐specific expression analysis to the allopolyploid level, we distinguish the distinct effects of progenitor regulatory interactions from the novel intergenomic interactions that arise from genome merger and allopolyploidization. This perspective informs experiments designed to reveal the molecular genetic basis of gene regulatory control, and will facilitate the disentangling of genetic from epigenetic and higher‐order effects that impact gene expression. Finally, we suggest that the extended cis–trans model may help conceptually unify several presently disparate hallmarks of allopolyploid evolution, including genome‐wide expression dominance and biased fractionation, and lead to a new level of understanding of phenotypic novelty accompanying polyploidy.

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“…Comparative transcriptomics has become a widely employed and powerful tool in plant evolutionary biology. Applications are many and diverse, including evolutionary rate estimation [1][2][3], reconstruction of species relationships [3][4][5], and the elucidation of co-expression and regulatory changes in gene networks [6,7]. Next-generation sequencing has facilitated inexpensive and efficient transcriptomic profiling for species whose lack of existing genomic resources would have previously been an obstacle.…”

Section: Introductionmentioning

confidence: 99%

Homoeologous gene expression and co-expression network analyses and evolutionary inference in allopolyploids

Grover

Arick

et al. 2019

Preprint

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Biographical noteGuanjing Hu (https://orcid.org/0000-0001-8552-7394) is a researcher in evolutionary genomics, functional genomics, and whole-genome duplication (polyploidization).Corrinne E. Grover (https://orcid.org/0000-0003-3878-5459) is a researcher in evolutionary genomics, molecular Evolution, and plant Systematics and Evolution. 0000-0003-3878-5459 Mark A. Arick II (https://orcid.org/0000-0002-7207-3052) is a researcher in genomics, bioinformatics, and computational sciences.Meiling Liu (https://orcid.org/0000-0001-7953-1506) is a researcher in statistics and bioinformatics.Daniel G. Peterson (https://orcid.org/0000-0002-0274-5968) is a researcher in genomics, biocomputing, and biotechnology. Jonathan F. Wendel (https://orcid.org/0000-0003-2258-5081) is a researcher in evolutionary genomics, molecular Evolution, and plant Systematics and Evolution. ABSTRACTPolyploidy is a widespread phenomenon throughout eukaryotes. Due to the coexistence of duplicated genomes, polyploids offer unique challenges for estimating gene expression levels, which is essential for understanding the massive and various forms of transcriptomic responses accompanying polyploidy. Although previous studies have explored the bioinformatics of polyploid transcriptomic profiling, the causes and consequences of inaccurate quantification of transcripts from duplicated gene copies have not been addressed. Using transcriptomic data from the cotton genus (Gossypium) as an example, we present an analytical workflow to evaluate a variety of bioinformatic method choices at different stages of RNA-seq analysis, from homoeolog expression quantification to downstream analysis used to infer key phenomena of polyploid expression evolution. In general, GSNAP-PolyCat outperforms other quantification pipelines tested, and its derived expression dataset best represents the expected homoeolog expression and co-expression divergence. The performance of co-expression network analysis was less affected by homoeolog quantification than by network construction methods, where weighted networks outperformed binary networks. By examining the extent and consequences of homoeolog read ambiguity, we illuminate the potential artifacts that may affect our understanding of duplicate gene expression, including an over-estimation of homoeolog coregulation and the incorrect inference of subgenome asymmetry in network topology. Taken together, our work points to a set of reasonable practices that we hope are broadly applicable to the evolutionary exploration of polyploids. RNA-seq read mapping and homoeolog-specific read partitioningThe following five pipelines were each independently applied to the diploid and AD polyploid datasets.GSNAP-PolyCat. This pipeline utilizes the SNP-tolerant capabilities of GSNAP [v2016-08-16] [29] to map polyploid reads to a single diploid progenitor genome (here, G. raimondii; [30]). The SNP-tolerant feature of GSNAP permits equivocal mapping of both A-and D-diploid derived reads based on a priori SNP information. Here, we used a previousl...

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Insights into the Ecology and Evolution of Polyploid Plants through Network Analysis

Cited by 34 publications

References 189 publications

Genomics of hybridization and its evolutionary consequences

Genomics of hybridization and its evolutionary consequences

Cis–trans controls and regulatory novelty accompanying allopolyploidization

Homoeologous gene expression and co-expression network analyses and evolutionary inference in allopolyploids

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