Department of Ecology and Genetics, Evolutionary Biology Centre and Science for Life Laboratory, Uppsala University, Uppsala, Sweden.
Department of Plant Biology, Swedish University of Agricultural Sciences, Uppsala, Sweden.
Elife. 2024 Jan 8;12:RP88398. doi: 10.7554/eLife.88398.
Allopolyploidization is a frequent evolutionary transition in plants that combines whole-genome duplication (WGD) and interspecific hybridization. The genome of an allopolyploid species results from initial interactions between parental genomes and long-term evolution. Distinguishing the contributions of these two phases is essential to understanding the evolutionary trajectory of allopolyploid species. Here, we compared phenotypic and transcriptomic changes in natural and resynthesized allotetraploids with their diploid parental species. We focused on phenotypic traits associated with the selfing syndrome and on transcription-level phenomena such as expression-level dominance (ELD), transgressive expression (TRE), and homoeolog expression bias (HEB). We found that selfing syndrome, high pollen, and seed quality in natural allotetraploids likely resulted from long-term evolution. Similarly, TRE and most down-regulated ELD were only found in natural allopolyploids. Natural allotetraploids also had more ELD toward the self-fertilizing parental species than resynthesized allotetraploids, mirroring the establishment of the selfing syndrome. However, short-term changes mattered, and 40% of the cases of ELD in natural allotetraploids were already observed in resynthesized allotetraploids. Resynthesized allotetraploids showed striking variation of HEB among chromosomes and individuals. Homoeologous synapsis was its primary source and may still be a source of genetic variation in natural allotetraploids. In conclusion, both short- and long-term mechanisms contributed to transcriptomic and phenotypic changes in natural allotetraploids. However, the initial gene expression changes were largely reshaped during long-term evolution leading to further morphological changes.
异源多倍化是植物中一种常见的进化转变，它结合了全基因组复制（WGD）和种间杂交。异源多倍体物种的基因组源自亲本基因组的初始相互作用和长期进化。区分这两个阶段的贡献对于理解异源多倍体物种的进化轨迹至关重要。在这里，我们比较了自然和人工合成的异源四倍体与其二倍体亲本物种在表型和转录组水平上的变化。我们重点关注与自交综合征相关的表型特征以及转录水平上的现象，如表达水平优势（ELD）、超越表达（TRE）和同源基因表达偏向（HEB）。我们发现，自然异源四倍体中的自交综合征、高花粉和高种子质量可能是长期进化的结果。同样，TRE 和大多数下调的 ELD 仅在自然异源多倍体中发现。自然异源四倍体对自交亲本物种的 ELD 也高于人工合成的异源四倍体，反映了自交综合征的建立。然而，短期变化也很重要，自然异源四倍体中 40%的 ELD 已经在人工合成的异源四倍体中观察到。人工合成的异源四倍体在染色体和个体之间表现出明显的 HEB 变异。同源基因联会是其主要来源，可能仍然是自然异源多倍体遗传变异的来源。总之，短期和长期机制都导致了自然异源多倍体在转录组和表型上的变化。然而，初始基因表达的变化在长期进化过程中发生了很大的重塑，导致了进一步的形态变化。
