title: Natural Variation Identifies ICARUS1, a Universal Gene Required for Cell Proliferation and Growth at High Temperatures in Arabidopsis thaliana.
abstract: 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.
authors.affiliation: School of Biological Sciences, Monash University, Victoria, Australia.
authors.forename: Wangsheng
authors.initials: W
authors.lastname: Zhu
authors.affiliation: Centro Nacional de Biotecnología (CNB), Consejo Superior de Investigaciones Científicas (CSIC), Madrid, Spain.
authors.forename: Israel
authors.initials: I
authors.lastname: Ausin
authors.affiliation: School of Biological Sciences, Monash University, Victoria, Australia.
authors.forename: Andrei
authors.initials: A
authors.lastname: Seleznev
authors.affiliation: Centro Nacional de Biotecnología (CNB), Consejo Superior de Investigaciones Científicas (CSIC), Madrid, Spain.
authors.forename: Belén
authors.initials: B
authors.lastname: Méndez-Vigo
authors.affiliation: Estación Biológica de Doñana (EBD), Consejo Superior de Investigaciones Científicas (CSIC), Seville, Spain.
authors.forename: F Xavier
authors.initials: FX
authors.lastname: Picó
authors.affiliation: School of Biological Sciences, Monash University, Victoria, Australia.
authors.forename: Sridevi
authors.initials: S
authors.lastname: Sureshkumar
authors.affiliation: School of Biological Sciences, Monash University, Victoria, Australia.
authors.forename: Vignesh
authors.initials: V
authors.lastname: Sundaramoorthi
authors.affiliation: Victorian Bioinformatics Consortium, Monash University, Victoria, Australia.
authors.forename: Dieter
authors.initials: D
authors.lastname: Bulach
authors.affiliation: Victorian Bioinformatics Consortium, Monash University, Victoria, Australia.
authors.forename: David
authors.initials: D
authors.lastname: Powell
authors.affiliation: Victorian Bioinformatics Consortium, Monash University, Victoria, Australia.
authors.forename: Torsten
authors.initials: T
authors.lastname: Seemann
authors.affiliation: Centro Nacional de Biotecnología (CNB), Consejo Superior de Investigaciones Científicas (CSIC), Madrid, Spain.
authors.forename: Carlos
authors.initials: C
authors.lastname: Alonso-Blanco
authors.affiliation: School of Biological Sciences, Monash University, Victoria, Australia.
authors.forename: Sureshkumar
authors.initials: S
authors.lastname: Balasubramanian
mesh_terms: D000483:Alleles; D017398:Alternative Splicing; D017360:Arabidopsis / Q000235:genetics*; D029681:Arabidopsis Proteins / Q000235:genetics* / Q000378:metabolism; D049109:Cell Proliferation; D019295:Computational Biology; D004249:DNA Damage; D020440:Gene Duplication; D018506:Gene Expression Regulation, Plant; D005819:Genetic Markers; D014644:Genetic Variation; D006358:Hot Temperature; D008969:Molecular Sequence Data; D009154:Mutation; D009713:Nucleotidyltransferases / Q000235:genetics* / Q000378:metabolism; D018515:Plant Leaves / Q000235:genetics; D059467:Transcriptome
chemical_list: D029681:Arabidopsis Proteins; D005819:Genetic Markers; C000606969:ICA1 protein, Arabidopsis; D009713:Nucleotidyltransferases; C065307:tRNA guanylyltransferase