Rapid and persistent genomic and epigenomic reconciliation during formation and evolution of Arabidopsis allopolyploids

Speciation by interspecific hybridization is rare in animals as the offspring such as mule is often sterile. In plants, hybridization between species can instantaneously generate allopolyploid species through fusing unreduced gametes or forming interspecific hybrids followed by chromosome doubling.

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Different genomes in a new allopolyploid often lead to “genome shock”, a term coined by Barbara McClintock 1, which may result in different consequences 2. In some allopolyploids such as oilseed rape (or canola, Brassica napus) and Tragopogon miscellus, they show rapid genomic reshuffling, producing aneuploids and exchanges between homoeologous chromosomes. However, in other allopolyploids such as Arabidopsis suecica, Upland cotton (Gossypium hirsutum) or Pima cotton (G. barbadense) 3, the genomes coexist relatively stable, although changes can occur at levels of gene expression and epigenetic modifications. The basis for paradoxical consequences between rapid genome reshuffling in some polyploids and genome stability in other polyploids remains unknown.

In this study, Jiang et al. 2 used Arabidopsis suecica (AATT, 2n = 4x = 26) as a model system because it has natural allotetraploid derived from A. thaliana (TT) and A. arenosa(AAAA), and it can be created in the laboratory by pollinating tetraploid A. thaliana Ler4 ecotype (TTTT, 2n = 4x = 20) with A. arenosa (AAAA, 2n = 4x = 32) pollen. These neo-allotetraploids (Allo733 and Allo738) are genetically stable and comparable with natural A. suecica. Moreover, A. arenosa is obligate outcrossing and highly heterozygous, which makes it difficult to accurately assemble its genome. Using integrated (PacBio long read and Hi-C) sequencing approaches, the team completed reference-grade sequences of A. arenosa(extracted from neo-allotetraploids) and A. suecica. The newly assembled T subgenome of neo-allotetraploids is almost identical to the published A. thaliana Ler sequence, and A subgenome is closely related to the A. arenosa sequence. Except for some translocations, rearrangements, and more gene family loss in T subgenome and more gene family gain in A subgenome, A. suecica subgenomes are conserved in gene synteny and content, as also reported in another study using natural A. suecica 4. The amount of homoeologous exchanges between two subgenomes in Allo738 is relatively small, only ~21.5 kb of the A. thaliana origin in the A subgenome and ~1.4 Mb of the A. arenosa origin in the T subgenome. Among transposable elements, LTR retrotransposons tend to be more active (younger insertion events) in the T subgenome of A. suecica than in A. thaliana species. The conserved genomic synteny between allotetraploids and related species may suggest a role for epigenetic modifications in nonadditive gene expression as observed in resynthesized and natural allopolyploids.

Indeed, these balanced genomic diversities are accompanied by pervasive convergent and concerted changes in DNA methylation and gene expression among allotetraploids. Despite a similar proportion of repetitive DNA between A. thaliana and A. arenosa, overall CG methylation levels are higher in A. arenosa than in A. thaliana. Surprisingly, in A. suecica, A subgenome has lower methylation levels in all contexts especially the CG sites than A. arenosa and convergently to the T subgenome level. This overall reduced methylation levels of A subgenome in natural A. suecicamay be related to upregulation of ROS1 (encoding DNA glycosylase/AP lyase) expression. To further analyze differentially methylated regions (DMRs) between A subgenome of A. suecica and A. arenosa, the DMRs are divided into three groups: convergent, conserved, and other DMRs. In contrast to substantially overall higher methylation levels in A. arenosa than in A. thaliana, A and T homoeologs of A. suecica have similar methylation levels. This is accompanied by dramatic reduction of CG methylation levels in A homoeologs, which convergently reaches a similar level to T homoeologs in A. suecica. Thus, two subgenomes tend to maintain similar methylation levels during allotetraploid evolution. In addition to convergent changes in DMRs, subsets of hypo DMRs induced in the F1 have been maintained after 10 or more generations in Allo733 and Allo738 and are also conserved in A. suecica. Convergent hypo CG DMR-associated genes are overrepresented in reproduction, seed development, system development, and cell cycle pathways, including genes related to mitosis and meiosis. Meiotic instability occurs often in F1 and early allotetraploids and is gradually improved in neo-allotetraploids by self-pollination. These findings suggest that demethylation and upregulation of A homoeologs of reproduction-related genes may contribute to reproductive stability during evolution of A. suecica allotetraploids 2.

For those allopolyploids that underwent rapid genomic reshuffling, it is possible that the species or strains used to form natural B. napus or wheat 8,000-10,000 years ago may become extinct. In some polyploids such as Tragopogon, parental species may be closely related to experience genomic exchanges, whereas in tetraploid and hexaploid wheat, homoeologous exchanges are inhibited by pairing homoeologous (Ph) locus 5. In Arabidopsis and cotton allotetraploids, the latter of which were formed ~1.5 million years ago, a combination of balanced genomic diversity and pervasive epigenomic modifications may stabilize subgenomes. This role of epigenomic modifications in genomic stability and gene expression may help identify epigenomic targets for gene-editing tools to modify and improve agronomic traits of polyploid crops.

References

  1. McClintock, B. The significance of responses of the genome to challenge. Science 226, 792-801 (1984).
  2. Jiang, X., Song, Q., Ye, W. & Chen, Z.J. Concerted genomic and epigenomic changes accompany stabilization of Arabidopsis allopolyploids. Nat Ecol Evol (2021).
  3. Chen, Z.J. et al. Genomic diversifications of five Gossypium allopolyploid species and their impact on cotton improvement. Nat Genet 52, 525-533 (2020).
  4. Burns, R. et al. Gradual evolution of allopolyploidy in Arabidopsis suecica. Nat Ecol Evol (2021).
  5. Griffiths, S. et al. Molecular characterization of Ph1 as a major chromosome pairing locus in polyploid wheat. Nature 439, 749-52 (2006).

Z. Jeffrey Chen

Professor, The University of Texas at Austin