Cryptic variation fuels plant phenotypic change through hierarchical epistasis

Area of Science:

• Genetics
• Evolutionary Biology
• Plant Biology

Background:

• Cryptic genetic variants are thought to fuel evolutionary change through interactions.
• Pan-genomics reveals extensive variation in regulatory regions and networks.
• Studying cryptic variation's role in phenotypic diversification is challenging.

Purpose of the Study:

• To investigate how cryptic genetic variants and gene regulatory networks influence phenotypic evolution.
• To explore the role of paralogous gene pairs and their interactions in shaping complex traits.
• To understand the mechanisms underlying phenotypic buffering and rapid evolutionary change.

Main Methods:

• Identified cis-regulatory cryptic variants and trans regulators in tomato paralogous genes.
• Constructed a gene regulatory network controlling inflorescence architecture.
• Generated 216 genotypes by combining coding and cis-regulatory mutations across four network genes.
• Quantified inflorescence branching in over 35,000 individuals.
• Analyzed genotype-phenotype data using a hierarchical epistasis model.

Main Results:

• Discovered dose-dependent interactions within paralogue pairs that enhance branching.
• Revealed synergistic effects from accumulating mutations within paralogue pairs.
• Identified antagonistic interactions between paralogue pairs, where mutations in one pair buffered effects in another.
• Demonstrated how gene regulatory network architecture and paralogue diversification shape phenotypic space.

Conclusions:

• Gene regulatory network structure and complex dosage effects from paralogue diversification are key drivers of phenotypic variation.
• These mechanisms allow for both stable, buffered phenotypes and rapid, significant phenotypic shifts.
• The study provides insights into the evolutionary potential stored within cryptic genetic variation.