Natural Variation Identifies ICARUS1, a Universal Gene Required for Cell Proliferation and Growth at High Temperatures in Arabidopsis thaliana.

Plants are highly sensitive to environmental changes and even small variations in ambient temperature have severe consequences on their growth and development. Temperature affects multiple aspects of plant development, but the processes and mechanisms underlying thermo-sensitive growth responses are mostly unknown. Here we exploit natural variation in Arabidopsis thaliana to identify and characterize novel components and processes mediating thermo-sensitive growth responses in plants. Phenotypic screening of wild accessions identified several strains displaying pleiotropic growth defects, at cellular and organism levels, specifically at high ambient temperatures. Positional cloning and characterization of the underlying gene revealed that ICARUS1 (ICA1), which encodes a protein of the tRNAHis guanylyl transferase (Thg1) superfamily, is required for plant growth at high temperatures. Transcriptome and gene marker analyses together with DNA content measurements show that ICA1 loss-of-function results in down regulation of cell cycle associated genes at high temperatures, which is linked with a block in G2/M transition and endoreduplication. In addition, plants with mutations in ICA1 show enhanced sensitivity to DNA damage. Characterization of additional strains that carry lesions in ICA1, but display normal growth, shows that alternative splicing is likely to alleviate the deleterious effects of some natural mutations. Furthermore, analyses of worldwide and regional collections of natural accessions indicate that ICA1 loss-of-function has arisen several times independently, and that these occur at high frequency in some local populations. Overall our results suggest that ICA1-mediated-modulation of fundamental processes such as tRNAHis maturation, modify plant growth responses to temperature changes in a quantitative and reversible manner, in natural populations.

Genetic Architecture of Natural Variation in Thermal Responses of Arabidopsis.

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.