Abstract
A fundamental question in biology is how gene expression is regulated to give rise to a phenotype. However, transcriptional variability is rarely considered although it could influence the relationship between genotype and phenotype. It is known in unicellular organisms that gene expression is often noisy rather than uniform, and this has been proposed to be beneficial when environmental conditions are unpredictable. However, little is known about inter‐individual transcriptional variability in multicellular organisms. Using transcriptomic approaches, we analysed gene expression variability between individual Arabidopsis thaliana plants growing in identical conditions over a 24‐h time course. We identified hundreds of genes that exhibit high inter‐individual variability and found that many are involved in environmental responses, with different classes of genes variable between the day and night. We also identified factors that might facilitate gene expression variability, such as gene length, the number of transcription factors regulating the genes and the chromatin environment. These results shed new light on the impact of transcriptional variability in gene expression regulation in plants.
Highlights
Gene expression in individual cells is often noisy and dynamic
BZIP transcription factors (TF) regulate multiple processes including pathogen defence, light and stress signalling, seed maturation and flower development (Jakoby et al, 2002). These are in agreement with the enriched Gene Ontology (GO) identified for highly variable genes (HVGs), involved in responses to the environment as well as biotic and abiotic stresses. These results show that HVGs are enriched for genes involved in the response to environment and stress and are targeted by TF families involved in environmental responses, while LVGs are enriched in DNA, RNA and protein metabolism
The results are broadly the same as the ones obtained on all HVGs and LVGs. These results indicate that HVGs are characterised by a more compacted chromatin environment, as further supported by the fact that the MNase signal, which indicates the level of nucleosome occupancy, is higher in the gene body and mostly at the end of the genes in HVGs compared to LVGs and random genes (Appendix Fig S7B)
Summary
Gene expression in individual cells is often noisy and dynamic. Genetically identical cells under the same environment can display widely different expression levels of key genes (Ko, 1992; Fiering et al, 2000; Martins & Locke, 2015). Noise in gene expression has been shown to have a significant impact on the design and function of genetic circuits in unicellular organisms (Elowitz et al, 2002; Eldar & Elowitz, 2010) It has been observed in multiple pathways in mammalian cells (Yin et al, 2009; Mantsoki et al, 2016; Riddle et al, 2018), in Drosophila cells (Pare et al, 2009) and between individuals in Drosophila (Lin et al, 2016). The identification of mutants in which transcriptional and/or phenotypic variability is increased indicates that variability is at least partly buffered or controlled (Rutherford & Lindquist, 1998; Queitsch et al, 2002; Raj et al, 2010; Folta et al, 2014; Schaefer et al, 2017) It is not known at a genome-wide scale to what extent gene expression can be variable during plant development or between identical plants
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