New discoveries on the recurrent origins and subgenomic stability of allopolyploid plants by researchers from EPS-Huesca, China and Israel

A recent publication in the prestigious journal Molecular Biology and Evolution, entitled “Subgenomic stability of progenitor genomes during repeated allotetraploid origins of the same grass Brachypodium hybridum” presents new findings on the multiple origins and subgenomic stability of allopolyploid plants, resulting from the research developed by Pilar Catalán, researcher from the Higher Polytechnic School of Huesca and the BIFI of the University of Zaragoza, and her colleagues from China and Israel.

 

Sampling of populations of Brachypodium hybridum and its progenitor species.

 

The study uncovers a third recurrent origin of the same allotetraploid grass species Brachypodium hybridum in the eastern Mediterranean, from local ancestors of its two diploid progenitor species B. stacei and B. distachyon. The three species constitute a model system, used to decipher the evolution of polyploidy in plants, a phenomenon that affects more than 50% of current angiosperms (and all of them, if we consider that the ~280,000 flowering plants existing today are descendants of paleopolyploid ancestors). The origin of current allopolyploid plants resulted from past interspecific hybridization of two progenitor species, evolutionarily close to each other but with different genomes; the sterile interspecific hybrid was able to duplicate its two inherited genomes, thus becoming a new fertile allopolyploid species. Its inherited subgenomes currently coexist in the nucleus of the allopolyploid.

In many allopolyploid plants, the emergence of the coexistence of two (or more) different subgenomes in the same nucleus has caused profound chromosomal reorganizations and gene regulation systems, to try to compensate for the imbalance of the clash of these disparate gene systems. It has been called “polyploid genomic shock”, a term coined by Barbara McClintock in 1984. In several of these allopolyploid species, these remodelings involve exchanges of chromosomal fragments between the different subgenomes, which entail reciprocal duplications and deletions, as well as differential expressions of homeologous genes, with one subgenome becoming dominant (with overexpression of a majority of genes) and another submissive (with low or no expression of those genes), and whose consequences affect the phenotype. However, in certain allopolyploid plants the existence of these post-polyploid remodeling has not been detected.

 

 Pasture of Brachypodium hybridum annual plants

 

The generation of several reference genomes and transcriptomes of Brachypodium hybridum has allowed the authors to investigate whether or not chromosomal restructuring and remodeling of gene expression have occurred between its two progenitor subgenomes in each of the three lineages (different origins) that the plant has had throughout evolutionary time (from the most ancestral lineage ~2-1.4 million years ago, to the most recent ~130 thousand years ago). The results indicate that none of the three B. hybridum lineages show significant evidence of having undergone chromosomal rearrangements or dominance between subgenomes, supporting the high subgenomic stability of all plants of the allotetraploid species, which possibly became amphidiploid immediately after the respective interspecific hybridizations and genomic duplications. This could have been caused by the large difference between the subgenomic chromosomal karyotypes and by the balanced expression of genes in both subgenomes. B. hybridum thus becomes a model plant of allopolyploid subgenomic stability, without being affected by the disturbing effects of “polyploid genomic shock” that other allopolyploid plants present.

The work has also shown that the correct detection of chromosome exchanges between subgenomes requires comparative analysis with progenitor genomes close to the allotetraploid subgenomes, while the use of other more divergent ones gives rise to the detection of “false” genomic restructurings.

The study has been developed by the team of researchers from the University of Lanzhou (China), the Universities of Haifa and Tel-Aviv (Israel) and the EPSHU-University of Zaragoza (Spain). The research has been funded by the Second Tibetan Plateau Scientific Expedition and Research program (project 2019QZKK0502), Strategic Priority Research Program of Chinese Academy of Sciences (project XDB31010300), and International Collaboration 111 Program (project BP0719040) to Jianquian Liu and Eviatar Nevo, and by the Ministry of Science and Innovation of Spain (project PID2019-108195GB-I00), the Government of Aragon (project LMP82-21) and the Government of Aragon – European Social Fund (Bioflora research group) to Pilar Catalán.

Link to article: https://doi.org/10.1093/molbev/msad259,