Resources
We developed Arabidopsis and crop models for studying epigenetic regulation of gene expression in plant polyploids. Our research employs powerful genetics in Arabidopsis and crop plants such as allotetraploid cotton. Using Arabidopsis suecica as the model system, we uncovered concerted genomic and epigenomic changes accompany inheritance and stabilization of Arabidopsis allopolyploids. During evolution successful allopolyploids must overcome ‘genome shock’ between hybridizing species but the underlying process remains elusive. In resynthesized and natural Arabidopsis suecica (TTAA) allotetraploids derived from Arabidopsis thaliana (TT) and Arabidopsis arenosa (AA). A. suecica shows conserved gene synteny and content with more gene family gain and loss in the A and T subgenomes than respective progenitors.
These balanced genomic variations are accompanied by pervasive convergent and concerted changes in DNA methylation and gene expression among allotetraploids. These changes in DNA methylation, including small RNAs, in allotetraploids may affect gene expression and phenotypic variation, including flowering, silencing of self-incompatibility and upregulation of meiosis- and mitosis-related genes. In conclusion, concerted genomic and epigenomic changes may improve stability and adaptation during polyploid evolution.
Cotton is a powerful model for studying polyploid genome evolution, as well as cell differentiation and development. Cultivated cottons are tetraploid, meaning they have four sets of chromosomes. This polyploidy arises from the merging of two distinct diploid species, one originating from Africa (mother) and the other from the Americas (father), approximately 1.5 million years ago, producing five tetraploid cotton species. Over time, five distinct tetraploid species evolved. Of these, two were independently domesticated, namely, Upland (American) and Pima (Egyptian) cottons in the last 8,000 years, becoming the primary cotton types used today, with Upland cotton dominating global cotton production (~95%).
In an international consortium, we generated reference-grade genome of the Upland cotton in 2015. We further decoded genomes and epigenomes of all five allotetraploid cotton species in 2020 and revealed over 500 epialleles – variations that affect gene expression without altering the DNA sequence itself. These epialleles appear to be stable across the five cotton species, indicating that they are inherited through ~1 million years of evolution and tens of thousands years of domestication. The identified epialleles are linked to important domestication traits, such as seed quality, fiber characteristics, and flowering time. The latter trait, photoperiodic flowering, is particularly significant as it influences the ability to grow cotton across the globe. These genomic insights will empower efforts to manipulate genetic recombination and modify epigenetic landscapes and target genes for the improvement of cotton and other polyploid crops such as wheat and canola. Polyploidy leads to low genetic recombination, comprising bottlenecks for breeding improvement, which is related to DNA methylation and chromatin modification. Epigenetic role in genetic recombination will be further investigated. Our research highlights the importance of both genomic and epigenomic perspectives in understanding and manipulating complex crop genomes, offering pathways to improve crop yield and resilience in the face of climate challenges.
Five Selected Publications
Zhang, T., Hu, Y., Jiang, W., Fang, L., Guan, X., et al. Guo, W., Li, R., and Chen, Z. J. (2015) Sequencing of allotetraploid cotton (Gossypium hirsutum L. acc. TM-1) provides a resource for fiber improvement. Nature Biotechnology 33:531-537
Song, Q., Zhang, T., Stelly, D. M., Chen, Z. J. (2017) Epigenomic and functional analyses reveal roles for epialleles in the loss of photoperiod sensitivity during domestication of allotetraploid cottons. Genome Biology 18:99.
Chen, Z. J., Sreedasyam, A., Ando, A., Song, Q., De Santiago, L. M., et al., Stelly, D. M., Grimwood, J., Schmutz, J. (2020) Genomics of the origin, diversification and improvement of polyploid cottons. Nature Genetics 52:525–533.
Jiang, X., Song, Q., Ye, W., Chen, Z. J. (2021) Concerted genomic and epigenomic changes accompany stabilization of Arabidopsis allopolyploids. Nature Ecology & Evolution 5(10):1382-1393.
Cao, S., Chen, Z. J. (2024) Transgenerational epigenetic inheritance during plant evolution and breeding. Trends in Plant Science (DOI:10.1016/j.tplants.2024.04.007).
