Recently, the researchers at the Institute of Vegetables and Flowers has made significant progress in understanding the establishment of subgenome dominance in polyploids by synthesizing Brassica allotetraploids. Their findings challenge the existing hypothesis that transposons drive the formation of subgenome dominance. The research results, titled "The lack of negative association between TE load and subgenome dominance in synthesized Brassica allotetraploids," have been published in the prestigious international journal "Proceedings of the National Academy of Sciences (PNAS)" with an impact factor of 11.1.

Whole-genome duplication is one of the key driving forces in plant species evolution and trait evolution. It can alter the genomic composition, increase genetic diversity, modify gene dosage and function, enabling plants to have advantages in the face of biotic and abiotic stresses or intra-specific competition. It plays a significant role in species differentiation, the formation of diversity, and the domestication of crops. Polyploidy has important applications in agriculture and can be utilized to create new crop resources and improve crop quality and resistance.

Subgenome dominance is an important phenomenon in the evolutionary process of polyploidization, wherein one subgenome occupies a dominant position in the polyploid genome, characterized by stronger gene expression and fewer gene losses. Subgenome dominance play important roles in shaping genome structure and promoting the evolution of new traits and functions. Therefore, understanding the mechanisms underlying its formation has been a hot topic in the field of biology. Previous studies have found that the dominant subgenome exhibits lower transposon abundance and DNA methylation levels, suggesting a potential correlation between the formation of subgenome dominance and the differential distribution of transposon sequences among subgenomes. Researchers have hypothesized that the higher levels of transposon content and methylation in certain subgenomes result in suppressed gene expression and ultimately determine the formation of subgenome dominance.

However, the differential distribution of transposons and the formation of subgenome dominance present a classic "chicken-and-egg" dilemma: is it the methylated transposons that drive the formation of subgenome dominance, or is it subgenome dominance that leads to the accumulation and distribution of transposon differences among subgenomes? Answering this question has proven challenging in studies of ancient polyploid plants, and even in cases of artificially synthesized polyploid plant systems like monkeyflowers and cucumbers, the temporal relationship between the two factors remains elusive.

In this study, the parental materials used, Chinese cabbage and cabbage, belong to the same genus Brassica in the Brassicaceae family. They underwent an ancient polyploidization event (paleopolyploidization) approximately tens of millions of years ago. By performing distant hybridization between Chinese cabbage and cabbage, combined with embryo rescue techniques, F1 plants were obtained. These F1 plants were then subjected to colchicine treatment to induce allopolyploidy, resulting in the formation of a synthetic allotetraploid (neo-polyploidization). Subsequently, eight generations of self-pollination were carried out. In this material system, there coexist three sets of subgenomes from the ancient paleopolyploidization event and two sets of subgenomes generated from the recent neo-polyploidization event, providing a well-controlled comparative relationship.

Through transcriptomic and methylation analysis of the parental and tetraploid offspring, it was found that the three sets of subgenomes from the ancient paleopolyploidization event maintained subgenome dominance in the newly synthesized allotetraploid. Furthermore, there was a negative correlation between transposon density/methylation levels and subgenome dominance in the ancient polyploid subgenomes. However, between the two subgenomes of the neo-polyploid, although the cabbage subgenome (CC) exhibited significantly higher transposon density than the Chinese cabbage subgenome (AA), the Chinese cabbage subgenome did not demonstrate gene expression dominance over the cabbage subgenome. In other words, there was no negative correlation between transposon density and subgenome dominance observed in the neo-polyploid subgenomes.

Furthermore, it was observed that the cabbage (sub)genome in both the parental and synthetic tetraploid had higher methylation levels compared to the Chinese cabbage genome. However, in the synthetic tetraploid, there was no significant correlation between methylation levels and gene expression between the two subgenomes, suggesting that the silencing effect of methylated transposons on adjacent gene expression may vary between the parental genomes. Additionally, the analysis of a natural tetraploid rapeseed derived from the hybridization of Chinese cabbage and cabbage produced results consistent with those of the artificially synthesized tetraploid. These findings strongly indicate that differences in transposon content and methylation are not the determining factors for the formation of subgenome dominance in polyploid genomes.

In summary, this study challenges the previous understanding of the relationship between transposons and subgenome dominance. It suggests that after the parental genomes merge through polyploidization, they may continue to function separately as chimeric genomes until large-scale chromosomal rearrangements occur (re-diploidization). The decisive driving force for the formation of subgenome dominance may be associated with differences in gene transcription efficiency between different genomes. These findings provide new directions for a deeper understanding of the mechanisms underlying subgenome dominance, which is of great significance for comprehending plant polyploid evolution and creating new polyploid crop germplasms.

The co-first authors of this paper are Kang Zhang, an associate professor, Lingkui Zhang, a Ph.D. student, and Yinan Cui, a master's graduate, at the Institute of Vegetables and Flowers, Chinese Academy of Agricultural Sciences. The corresponding authors of this paper are Professor Feng Cheng, Professor Xiaowu Wang, and Professor Michael Freeling from the University of California, Berkeley. The study received funding from the State Key Laboratory of Vegetable Biobreeding, the National Natural Science Foundation of China, the Innovation Program of the Chinese Academy of Agricultural Sciences, and Key Laboratory of Biology and Genetic Improvement of Horticultural Crops, Ministry of Agriculture and Rural Affairs, China.