Submitted to: Plant Journal
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 5/30/2008
Publication Date: 7/4/2008
Citation: Potokina, E., Druka, A., Luo, Z., Moscou, M., Wise, R.P., Waugh, R., Kearsey, M. 2008. Tissue Dependent Limited Pleiotropy Affects Gene Expression in Barley. Plant Journal. 56(2):287-296. DOI: 10.1111/j.1365-313X.2008.03601.x. Available: http://www3.interscience.wiley.com/cgi-bin/fulltext/120696653/HTMLSTART.
Interpretive Summary: Variation in gene expression is a heritable trait and can be mapped in segregating populations using the approaches of genetical genomics. For those organisms with sequenced genomes, the approach provides an unprecedented opportunity to compare the genetic position of the gene encoding each transcript with the position of its regulator, making it possible to discriminate among control elements for thousands of genes across the genome. While non-synonymous coding mutations change the resulting protein no matter where the gene is expressed, the effects of cis-regulatory mutations could be spatially or temporally limited, for example, to a single organ or tissue even when the gene is much more widely expressed. This phenomenon is known as reduced or limited pleiotropy. In the present paper we describe the genome-wide occurrence of limited pleiotropy of cis-regulatory mutations in barley. The tissues in this analysis represent two successive ontogenetic stages of the barley plant: embryo and seedling leaves. We showed that polymorphism in cis-regulatory regions between the two parents of the population may alter gene transcription for only one of the two developmental stages, supporting reports that mutations in regulatory regions may sometimes have few or no pleiotropic consequences. Thus, instead of the question ‘how many genes are regulated in cis?’ we should ask more accurately ‘how many cis-regulatory mutations can be detected with the particular cross for a given tissue?’ Although variability in gene expression at a genome-wide scale across tissues is well known for both sequenced and unsequenced organisms, there are very few studies focusing on the tissue-specific appearance and behavior of cis-regulatory elements. The availability of such an approach has wide value in genetical analysis of crop plants and farm animals and also in complementing information available in sequenced model organisms, thus translating information from model systems to crops of significant value.
Technical Abstract: Non-synonymous coding mutations in a gene change the resulting protein no matter where it is expressed, but the effects of cis-regulatory mutations could be spatially or temporally limited, a phenomenon termed limited pleiotropy. Here we report the genome-wide occurrence of limited pleiotropy of cis-regulatory mutations in barley (Hordeum vulgare L.) using Affymetrix analysis of 22,840 genes in a population of 139 doubled haploid lines derived from a cross between the cultivars Steptoe (St) and Morex (Mx). We identified robust cis-acting expression regulators that segregate like major genes in two successive ontogenetic stages: germinating embryo tissues and seedling leaves from the embryonic axis. We show that these polymorphisms may be consistent in both tissues or cause a dramatic change in transcript abundance in one tissue but not in another. We also show that the parental allele that increases expression can vary with tissue, suggesting nucleotide polymorphism in enhancer sequences. Due to limited pleiotropy of cis-regulating mutations, the number of cis-eQTLs (expression Quantitative Trait Loci) discovered by 'genetical genomics' is strongly affected by the particular tissue or developmental stage studied. Given that limited pleiotropy is a common feature of cis-regulatory mutations in barley, we predict that the phenomenon would be relevant to developmental and/or tissue-specific interactions across wide taxonomic boundaries in plants and animals.