Autopolyploidization presents a transient and potential-rich window of increased transcriptional plasticity in Arabidopsis arenosa.

Abstract

Whole-genome duplication (WGD, polyploidization) is a pervasive feature of Eukaryote evolution and often viewed as a source of evolutionary success and novelty, meaning a macromutation leading to higher fitness (i.e. "hopeful monsters"). Yet, the mechanisms behind the (occasional) success of nascent polyploids remain still elusive, especially from a transcriptomic point of view. Theory suggests that duplicated genetic networks are characterised by enhanced redundancy and higher output variation, promoting the exploration of the adaptive landscape during stressful times. Artificially synthesized neo-polyploid mutants provide an exciting system to test this, however, empirical studies comparing co-expression network patterns between natural and synthetic ploidies of the same species in an evolutionary context are lacking. Here we compare diploid, synthetic and naturally established autotetraploid populations of Arabidopsis arenosa to investigate short- versus long-term effects of polyploidy on gene expression complexity and plasticity under water deficiency stress. Transcriptomic profiling revealed that synthetic neo-tetraploids explored the broadest expression space and exhibited the highest number of stress-responsive genes. Co-expression network analyses demonstrated that the network of neo-tetraploids was fragmented into multiple highly connected modules, with stress-responsive genes preferentially acting as inter-modular "bridges". In contrast, diploids and established tetraploids exhibited lower expression variation, more modular architectures, with stress response genes embedded within well-defined modules. Moreover, synthetic tetraploids displayed the highest number of modules correlated with plant fitness proxy suggesting higher output variance resulting from the transcriptional shock. Together, our results indicate that WGD induces a transient phase of transcriptomic expansion and network disorganization that broadens the phenotypic landscape, followed by evolutionary stabilization and finally retention of some advantageous novelties in established polyploids. This supports the view of neo-polyploids as "hopeful monsters", in which short-term instability creates a window of enhanced variability and plasticity with long-term evolutionary potential. SignificanceSince the early concept of polyploids as "hopeful monsters," biologists have hypothesized that whole-genome duplication can generate novel phenotypes and facilitate adaptation to environmental challenges. Yet the mechanisms linking genome doubling to evolutionary innovation remain poorly understood. By comparing diploid, synthetic autotetraploid, and naturally established autotetraploid populations of Arabidopsis arenosa, we show that newly formed polyploids undergo a transient phase of expanded transcriptomic variation and extensive regulatory network rewiring. In contrast, established polyploids exhibit a more stable and modular network architecture. Our results provide empirical support for a long-standing evolutionary hypothesis, showing how genome duplication can temporarily broaden the range of possible phenotypes before subsequent stabilization through evolution.