Genetic Architecture of Natural Variation in Thermal Responses of Arabidopsis

Abstract

Wild strains of Arabidopsis (Arabidopsis thaliana) exhibit extensive natural variation in a wide variety of traits, including response to environmental changes. Ambient temperature is one of the major external factors that modulates plant growth and development. Here, we analyze the genetic architecture of natural variation in thermal responses of Arabidopsis. Exploiting wild accessions and recombinant inbred lines, we reveal extensive phenotypic variation in response to ambient temperature in distinct developmental traits such as hypocotyl elongation, root elongation, and flowering time. We show that variation in thermal response differs between traits, suggesting that the individual phenotypes do not capture all the variation associated with thermal response. Genome-wide association studies and quantitative trait locus analyses reveal that multiple rare alleles contribute to the genetic architecture of variation in thermal response. We identify at least 20 genomic regions that are associated with variation in thermal response. Further characterizations of temperature sensitivity quantitative trait loci that are shared between traits reveal a role for the blue-light receptor CRYPTOCHROME2 (CRY2) in thermosensory growth responses. We show the accession Cape Verde Islands is less sensitive to changes in ambient temperature, and through transgenic analysis, we demonstrate that allelic variation at CRY2 underlies this temperature insensitivity across several traits. Transgenic analyses suggest that the allelic effects of CRY2 on thermal response are dependent on genetic background suggestive of the presence of modifiers. In addition, our results indicate that complex light and temperature interactions, in a background-dependent manner, govern growth responses in Arabidopsis.Temperature is a critical environmental factor that has major effects on the growth, development, and distribution of plants across the globe (Fitter and Fitter, 2002;Samach and Wigge, 2005, 2013;Kotak et al., 2007;Penfield, 2008). With the predicted increase in global temperatures, and their potential impact on agricultural productivity, there are efforts to understand the genetic basis of temperature responses in plants. Traditionally, temperature effects have been studied in the context of extreme stress responses such as heat shock or cold shock (Kotak et al., 2007;Barrero-Gil and Salinas, 2013;Song et al., 2013;Storey and Storey, 2013). In recent times, there has been an interest in analyzing the response of plants to changes in their growth temperature within the nonstress range of l6°C to 27°C, as even small changes in temperature can have major impacts on plant growth and development (Wigge, 2013;Franklin et al., 2014). In this study, we refer to various phenotypic responses in plants that are attributable to small changes in ambient temperature as temperature/thermal response.A few specific phenotypic responses are often used to uncover the genetic and molecular basis of thermal response in plants. These include temperature-induced chan...

Natural variation involving deletion alleles of FRIGIDA modulate temperature‐sensitive flowering responses in Arabidopsis thaliana

“…We have recently reported the temperature sensitivity in hypocotyl elongation for several RILs including the Tsu‐0 × Col‐0 RILs in short days (Sanchez‐Bermejo et al . ). This analysis identified a region on top of chromosome 5 to be involved in the temperature sensitivity observed in hypocotyl elongation in the Tsu‐0 × Col‐0 RILs (Sanchez‐Bermejo et al .…”

“…This analysis identified a region on top of chromosome 5 to be involved in the temperature sensitivity observed in hypocotyl elongation in the Tsu‐0 × Col‐0 RILs (Sanchez‐Bermejo et al . ). The same region was found as a QTL in long days as well where the Tsu‐0 allele conferred longer hypocotyls with the effect being stronger at warmer temperatures (30 °C compared to 23 °C) (Fig.…”

“…; Sanchez‐Bermejo et al . ). We have earlier reported the thermal response in short day conditions, because the impact of temperature can be specifically analysed in short days.…”

Evolutionary adaptation to environmental stressors: a common response at the proteomic level

“…Studies investigating specific candidate mechanisms of individual environmental tolerance traits (e.g., Sørensen et al 2009;Udaka et al 2013;MacMillan et al 2015;Slotsbo et al 2016) as well as un-targeted approaches at the genetic or transcriptomic levels (Sørensen et al 2007;Chen et al 2015;Gerken et al 2015;Telonis-Scott et al 2016) have advanced the understanding of physiological tolerance mechanisms. These challenges include the lack of compliance across studies in both ectotherms and plants, due to huge effects of genetic background and the redundancy of molecular pathways, that is, the ability to attain a functional change through regulation of several different transcripts (Sarup et al 2011;Sanchez-Bermajo et al 2015). These challenges include the lack of compliance across studies in both ectotherms and plants, due to huge effects of genetic background and the redundancy of molecular pathways, that is, the ability to attain a functional change through regulation of several different transcripts (Sarup et al 2011;Sanchez-Bermajo et al 2015).…”

Genome-Wide Association Mapping and Genomic Prediction Elucidate the Genetic Architecture of Morphological Traits in Arabidopsis

“…Similar to the problem of missing heritability in human GWA studies, where individual variants cannot explain the phenotypic variation despite high heritabilities (Yang et al, 2010;Gibson, 2011;Makowsky et al, 2011), genetic variants cannot fully explain the high heritabilities in plant studies (Brachi et al, 2010;Sasaki et al, 2015). Several reasons, such as population structure (Filiault and Maloof, 2012), epistasis (Chan et al, 2011;Brachi et al, 2015;Kruijer, 2016), GxE (Sasaki et al, 2015), epigenetics (Johannes et al, 2009;Kooke et al, 2015), sample size (Korte and Farlow, 2013), heterogeneity (Atwell et al, 2010;Barboza et al, 2013), rare alleles (Salomé et al, 2011;Sanchez-Bermajo et al, 2015), and a high number of small-effect loci (Joseph et al, 2013;Verslues et al, 2014) can complicate the association between polymorphisms and phenotypes.…”