Transcribed microsatellite allele lengths are often correlated with gene expression in natural sunflower populations

Abstract

Microsatellites are common in genomes of most eukaryotic species. Due to their high mutability, an adaptive role for microsatellites has been considered. However, little is known concerning the contribution of microsatellites towards phenotypic variation.We used populations of the common sunflower (Helianthus annuus) at two latitudes to quantify the effect of microsatellite allele length on phenotype at the level of gene expression. We conducted a common garden experiment with seed collected from sunflower populations in Kansas and Oklahoma followed by an RNA-Seq experiment on 95 individuals. The effect of microsatellite allele length on gene expression was assessed across 3,325 microsatellites that could be consistently scored. Our study revealed 479 microsatellites at which allele length significantly correlates with gene expression (eSTRs). When irregular allele sizes not conforming to the motif length were removed, the number of eSTRs rose to 2,379. The percentage of variation in gene expression explained by eSTRs ranged from 1%-86% when controlling for population and allele-by-population interaction effects at the 479 eSTRs. Of these eSTRs, 70.4% are in untranslated regions (UTRs). A gene ontology (GO) analysis revealed that eSTRs are significantly enriched for GO terms associated with cis-and transregulatory processes. Our findings suggest that a substantial number of transcribed microsatellites can influence gene expression. K E Y W O R D S gene expression, Helianthus annuus, microsatellite, sunflower | 1705 RANATHUNGE ET Al. S U PP O RTI N G I N FO R M ATI O NAdditional supporting information may be found online in the Supporting Information section.

Microsatellites as Agents of Adaptive Change: An RNA-seq based Comparative Study of Transcriptomes from Five Helianthus Species

“…At the intra-species level, microsatellites of short motif types, specifically A and AG repeats have been implicated in gene expression divergence among common sunflower populations, which suggests that specific microsatellite motif types may be more likely to influence gene expression divergence [32]. In addition, a recent study on common sunflower populations across a narrow latitudinal range detected hundreds of transcribed microsatellites linked to gene expression variation among and within populations, which provides further evidence of the regulatory role of microsatellites at an even finer scale [27].…”

A comparative study of population genetic structure reveals patterns consistent with selection at functional microsatellites in common sunflower

“…Hence, we predicted that a significant portion of the variation in allele length at the eSTRs could be explained in relation to environmental conditions associated with latitudes. We further predicted that longer or shorter microsatellite alleles would be favored in populations located in more extreme latitudes beyond the focal populations sampled in our previous study (Ranathunge et al ., 2020). This hypothesis is consistent with the predictions of the tuning knob model which suggests that variation in microsatellite allele length can have stepwise effects on phenotypes (Kashi et al ., 1997; King et al ., 1997; Trifonov, 2004).…”

“…A total of 13 eSTRs out of 479 identified by Ranathunge et al . (2020) were selected for this study (Table 1) to assess the strength of selection acting on functional transcribed microsatellites relative to that on anonymous microsatellites that are assumed to evolve neutrally.…”

“…The eSTRs used in this study have shown significant allele length effects on gene expression in common sunflower across populations from a narrow latitudinal range between Kansas (KS) and Oklahoma (OK) (Ranathunge et al ., 2020). Given that microsatellite allele length has been linked to gene expression across a narrow latitudinal range, we hypothesized that this variation may be functional and locally adaptive.…”

Directional Decremental Abundance of (GA)9 and (GA)11 Blocks in Primate Speciation

“…This is a re ection of the highly polymorphic nature and plasticity of these genetic elements. Evolving evidence indicates crucial roles for STRs in gene expression (1)(2)(3)(4) and translation (5). A number of STRs may function as evolutionary switch codes for speciation (6,7).…”