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Patterns, mechanisms, and consequences of homoeologous exchange in allopolyploid angiosperms: a genomic and epigenomic perspective

NEW PHYTOLOGIST (2023)

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Summary: Polyploidy and subsequent ploidy reduction and genome shuffling are important driving forces in genome evolution. A study on a synthetic intergeneric hybrid (Raphanobrassica, RRCC) revealed the short-term allopolyploid genome evolution. In this hybrid, genome deletions occurred quickly while rearrangements were slow. Core and high-frequency genes tended to be retained while specific and low-frequency genes tended to be deleted. Large-fragment deletions were concentrated in the heterochromatin region, possibly resulting from chromosome breaks. Intergeneric translocations primarily involved short fragments dependent on homoeology, indicating a gene conversion origin. To accelerate genome shuffling, an efficient genome editing platform was developed for Raphanobrassica. By editing Fanconi Anemia Complementation Group M (FANCM) genes, homoeologous recombination, chromosome deletion, and secondary meiosis with additional ploidy reduction were accelerated. FANCM was found to be a checkpoint for meiosis and controller of ploidy stability. Simultaneous editing of FLIP genes allowed precise gene conversion and production of mosaic genes around the target site. This intergeneric hybrid and genome editing platform not only provide models for experimental evolution research by accelerating genome shuffling and conversion, but also enhance intergeneric genetic exchange and generate new genes, thereby accelerating plant breeding.

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Mapping of homoeologous chromosome exchanges influencing quantitative trait variation in Brassica napus

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Subgenome Dominance in an Interspecific Hybrid, Synthetic Allopolyploid, and a 140-Year-Old Naturally Established Neo-Allopolyploid Monkeyflower

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Diverse genome organization following 13 independent mesopolyploid events in Brassicaceae contrasts with convergent patterns of gene retention

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PLANT JOURNAL (2017)

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Genomic features shaping the landscape of meiotic double-strand-break hotspots in maize

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PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA (2017)

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Surviving a Genome Collision: Genomic Signatures of Allopolyploidization in the Recent Crop Species Brassica napus

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High-Resolution Mapping of Crossover Events in the Hexaploid Wheat Genome Suggests a Universal Recombination Mechanism

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Repeated Whole-Genome Duplication, Karyotype Reshuffling, and Biased Retention of Stress-Responding Genes in Buckler Mustard

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Polyploidy: Pitfalls and paths to a paradigm

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The challenge of evolving stable polyploidy: could an increase in crossover interference distance play a central role?

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Meiosis in autopolyploid and allopolyploid Arabidopsis

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CURRENT OPINION IN PLANT BIOLOGY (2016)

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CURRENT OPINION IN PLANT BIOLOGY (2016)

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Ancient WGD events as drivers of key innovations in angiosperms

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Genome evolution in the allotetraploid frog Xenopus laevis

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Gene Duplicability of Core Genes Is Highly Consistent across All Angiosperms

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Epigenome confrontation triggers immediate reprogramming of DNA methylation and transposon silencing in Arabidopsis thaliana F1 epihybrids

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PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA (2016)

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Article Genetics & Heredity

Inter-genomic DNA Exchanges and Homeologous Gene Silencing Shaped the Nascent Allopolyploid Coffee Genome (Coffea arabica L.)

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Editorial Material Plant Sciences

The wondrous cycles of polyploidy in plants

Jonathan F. Wendel

AMERICAN JOURNAL OF BOTANY (2015)

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The Molecular Biology of Meiosis in Plants

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ANNUAL REVIEW OF PLANT BIOLOGY, VOL 66 (2015)

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Effects of Crossovers Between Homeologs on Inheritance and Population Genomics in Polyploid-Derived Salmonid Fishes

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DNA Crossover Motifs Associated with Epigenetic Modifications Delineate Open Chromatin Regions in Arabidopsis

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The butterfly plant arms-race escalated by gene and genome duplications

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Hybrid origins and the earliest stages of diploidization in the highly successful recent polyploid Capsella bursa-pastoris

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PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA (2015)

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Dosage, duplication, and diploidization: clarifying the interplay of multiple models for duplicate gene evolution over time

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CURRENT OPINION IN PLANT BIOLOGY (2014)

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Extensive and Biased Intergenomic Nonreciprocal DNA Exchanges Shaped a Nascent Polyploid Genome, Gossypium (Cotton)

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Shared Subgenome Dominance Following Polyploidization Explains Grass Genome Evolutionary Plasticity from a Seven Protochromosome Ancestor with 16K Protogenes

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The widespread crucifer species Cardamine flexuosa is an allotetraploid with a conserved subgenomic structure

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The BOY NAMED SUE Quantitative Trait Locus Confers Increased Meiotic Stability to an Adapted Natural Allopolyploid of Arabidopsis

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Genome rearrangements derived from homoeologous recombination following allopolyploidy speciation in coffee

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Early allopolyploid evolution in the post-Neolithic Brassica napus oilseed genome

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An assessment of karyotype restructuring in the neoallotetraploid Tragopogon miscellus (Asteraceae)

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Arabidopsis meiotic crossover hot spots overlap with H2A. Z nucleosomes at gene promoters

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NATURE GENETICS (2013)

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Dissection of a major QTL for seed colour and fibre content in Brassica napus reveals colocalization with candidate genes for phenylpropanoid biosynthesis and flavonoid deposition

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Persistent whole-chromosome aneuploidy is generally associated with nascent allohexaploid wheat

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PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA (2013)

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The genomic landscape of meiotic crossovers and gene conversions in Arabidopsis thaliana

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ELIFE (2013)

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Ancient whole genome duplications, novelty and diversification: the WGD Radiation Lag-Time Model

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CURRENT OPINION IN PLANT BIOLOGY (2012)

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Evidence for Widespread GC-biased Gene Conversion in Eukaryotes

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Homoeolog expression bias and expression level dominance in allopolyploids

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Non-random distribution of extensive chromosome rearrangements in Brassica napus depends on genome organization

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Biased Gene Fractionation and Dominant Gene Expression among the Subgenomes of Brassica rapa

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Gene balance hypothesis: Connecting issues of dosage sensitivity across biological disciplines

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PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA (2012)

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Article Multidisciplinary Sciences

Extensive chromosomal variation in a recently formed natural allopolyploid species, Tragopogon miscellus (Asteraceae)

Michael Chester et al.

PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA (2012)

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Article Multidisciplinary Sciences

Loss of DNA methylation affects the recombination landscape in Arabidopsis

Marie Mirouze et al.

PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA (2012)

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A knockout mutation in the lignin biosynthesis gene CCR1 explains a major QTL for acid detergent lignin content in Brassica napus seeds

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THEORETICAL AND APPLIED GENETICS (2012)

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Article Biochemistry & Molecular Biology

Variation in crossover rates across a 3-Mb contig of bread wheat (Triticum aestivum) reveals the presence of a meiotic recombination hotspot

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Article Biochemistry & Molecular Biology

GC-Biased Gene Conversion and Selection Affect GC Content in the Oryza Genus (rice)

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Ancestral polyploidy in seed plants and angiosperms

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Differentiation of the maize subgenomes by genome dominance and both ancient and ongoing gene loss

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PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA (2011)

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Homoeologous shuffling and chromosome compensation maintain genome balance in resynthesized allopolyploid Brassica napus

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PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA (2011)

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Homeolog loss and expression changes in natural populations of the recently and repeatedly formed allotetraploid Tragopogon mirus (Asteraceae)

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Homoeologous recombination in allopolyploids: the polyploid ratchet

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Dating the origins of polyploidy events

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Genetic regulation of meiosis in polyploid species: new insights into an old question

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The first meiosis of resynthesized Brassica napus, a genome blender

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Centromeres Convert but Don't Cross

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AMERICAN JOURNAL OF BOTANY (2009)

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Biased Gene Conversion and the Evolution of Mammalian Genomic Landscapes

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ANNUAL REVIEW OF GENOMICS AND HUMAN GENETICS (2009)

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Article Biotechnology & Applied Microbiology

Recombination between Homoeologous Chromosomes of Lager Yeasts Leads to Loss of Function of the Hybrid GPH1 Gene

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APPLIED AND ENVIRONMENTAL MICROBIOLOGY (2009)

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GC Content and Recombination: Reassessing the Causal Effects for the Saccharomyces cerevisiae Genome

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GENETICS (2009)

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Review Genetics & Heredity

Mechanisms of change in gene copy number

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NATURE REVIEWS GENETICS (2009)

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Analysis of Gene Expression in Resynthesized Brassica napus Allopolyploids Using Arabidopsis 70mer Oligo Microarrays

Robert T. Gaeta et al.

PLOS ONE (2009)

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Mating system and recombination affect molecular evolution in four Triticeae species

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GENETICS RESEARCH (2008)

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Article Biochemistry & Molecular Biology

Genomic changes in resynthesized Brassica napus and their effect on gene expression and phenotype

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PLANT CELL (2007)

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Article Genetics & Heredity

Evolution and expression of homeologous loci in Tragopogon miscellus (Asteraceae), a recent and reciprocally formed allopolyploid

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GENETICS (2006)

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Article Agronomy

Quantitative trait loci for resistance to Sclerotinia sclerotiorum and its association with a homeologous non-reciprocal transposition in Brassica napus L.

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Identification of intergenomic recombinations in unisexual salamanders of the genus Ambystoma by genomic in situ hybridization (GISH)

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Detection of chromosomal rearrangements derived from homeologous recombination in four mapping populations of Brassica napus L.

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GENETICS (2005)

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Flowering time divergence and genomic rearrangements in resynthesized Brassica polyploids (Brassicaceae)

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Understanding mechanisms of novel gene expression in polyploids

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TRENDS IN GENETICS (2003)

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Extensive genomic duplication during early chordate evolution

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