RT Journal Article
SR Electronic
T1 The role of non-additive gene action on gene expression variation in plant domestication
JF bioRxiv
FD Cold Spring Harbor Laboratory
SP 2022.10.13.511672
DO 10.1101/2022.10.13.511672
A1 Erik Díaz-Valenzuela
A1 Daniel Hernández-Ríos
A1 Angélica Cibrián-Jaramillo
YR 2022
UL http://biorxiv.org/content/early/2022/11/30/2022.10.13.511672.abstract
AB Background Plant domestication is a remarkable example of rapid phenotypic transformation of polygenic traits such as organ size. Evidence from a handful of study cases suggests this transformation is due to gene regulatory changes that result in non-additive phenotypes. Employing data from published genetic crosses, we estimated the role of non-additive gene action in the modulation of transcriptional landscapes in three domesticated plants: maize, sunflower, and chili pepper. Using A. thaliana, we assessed the correlation between gene regulatory network (GRN) connectivity properties, transcript abundance variation, and gene action. Finally, we investigated the propagation of non-additive gene action in GRNs.Results We compared crosses between domesticated plants and their wild relatives to a set of control crosses that included a pair of subspecies evolving under natural selection and a set of inbred lines evolving under domestication. We found abundance differences on a higher portion of transcripts in crosses between domesticated-wild plants relative to the control crosses. These transcripts showed non-additive gene action more often in crosses of domesticated-wild plants than in our control crosses. This pattern was strong for genes associated with cell cycle and cell fate determination, which control organ size. We found weak but significant negative correlations between the number of targets of trans-acting genes (Out-degree) and both the magnitude of transcript abundance differences a well as the absolute degree of dominance. Likewise, we found that the number of regulators that control a gene’s expression (In-degree) is weakly but negatively correlated with the magnitude of transcript abundance differences. We observed that dominant-recessive gene action is highly propagable through GRNs. Finally, we found that transgressive gene action is driven by trans-acting regulators showing additive gene action.Conclusions Our study highlights the role of non-additive gene action on modulating domestication-related traits such as organ size via regulatory divergence. We propose that GRNs are shaped by regulatory changes at genes with modest connectivity, which reduces the effects of antagonistic pleiotropy. Finally, we provide empirical evidence of the propagation of non-additive gene action in GRNs, which suggests a transcriptional epistatic model for the control of polygenic traits such as organ size.Competing Interest StatementThe authors have declared no competing interest.APCAnaphase-promoting complexCDC22Cell division cycle 20.2CDKD1cyclin-dependent kinase D1DEDifferentially expressedELF3Early flowering proteinESEffect sizeFCFold changeFDRFalse discovery rateGOGene ontologyGRNGene regulatory networkNGSNext generation sequencingPKLPickle remodeling factorTORTarget of rapamycinZWIP2Zink finger protein WIP2