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

Zhu, Weiren; Ausín, Israel; Seleznev, Andrei; Méndez‐Vigo, Belén; Picó, F. Xavier; Sureshkumar, Sridevi; Sundaramoorthi, Vignesh; Bulach, Dieter; Powell, David R.; Seemann, Torsten; Alonso‐Blanco, Carlos; Balasubramanian, Sureshkumar

doi:10.1371/journal.pgen.1005085

Cited by 35 publications

(46 citation statements)

References 64 publications

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“…The plants were grown in sets of growth chambers (Percival Scientific, Canada) at 23 °C or 27 °C and 30 °C under long days (LD, 8 h dark/16 h light; 300 μ moles −1 m −2 s −1 ) for experiments or in greenhouse for bulking seeds as described previously (Zhu et al . ). Plants were watered periodically.…”

Section: Methodsmentioning

confidence: 97%

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

Sánchez-Bermejo

Balasubramanian

2016

Plant Cell & Environment

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Ambient temperature is one of the major environmental factors that modulate plant growth and development. There is extensive natural genetic variation in thermal responses of plants exemplified by the variation exhibited by the accessions of Arabidopsis thaliana. In this work we have studied the enhanced temperature response in hypocotyl elongation and flowering shown by the Tsu-0 accession in long days. Genetic mapping in the Col-0 × Tsu-0 recombinant inbred line (RIL) population identified several QTLs for thermal response including three major effect loci encompassing candidate genes FRIGIDA (FRI), FLOWERING LOCUS C (FLC) and FLOWERING LOCUS T (FT). We confirm and validate these QTLs. We show that the Tsu-0 FRI allele, which is the same as FRI-Ler is associated with late flowering but only at lower temperatures in long days. Using transgenic lines and accessions, we show that the FRI-Ler allele confers temperature-sensitive late flowering confirming a role for FRI in photoperiod-dependent thermal response. Through quantitative complementation with heterogeneous inbred families, we further show that cis-regulatory variation at FT contributes to the observed hypersensitivity of Tsu-0 to ambient temperature. Overall our results suggest that multiple loci that interact epistatically govern photoperiod-dependent thermal responses of A. thaliana.

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Section: Methodsmentioning

confidence: 97%

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

Sánchez-Bermejo

Balasubramanian

2016

Plant Cell & Environment

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“…Among these strains, Sij-4 also displays a strong temperature-dependent growth defect, in addition to the absence of temperature-induced hypocotyl elongation. Further analysis of Sij-4 revealed that allelic variation at the ICARUS1 locus, encoding a tRNA His guanylyl transferase, underlies this phenotype, indicating a role for fundamental processes in conferring variation in thermal response (Zhu et al, 2015). To decipher the genetic architecture of these accessionspecific responses, we analyzed three F2 populations derived from the relatively temperature-insensitive strains (Tsushima [Tsu-0], Meise-6, and Yeg-3) with the reference strain Columbia (Col-0), which displays relatively higher sensitivity (Supplemental Fig.…”

Section: Temperature Sensitivity In Hypocotyl Elongation Segregates Amentioning

confidence: 99%

Genetic Architecture of Natural Variation in Thermal Responses of Arabidopsis

et al. 2015

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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...

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“…LN (LN21LD, LN21SD and LNVLD for the different environments) was the sum of rosette and cauline leaves. In the 28LD environment, Don-0 and numerous RILs showed reduced survival and abnormal leaf growth caused by the temperature sensitive gene ICARUS (Zhu et al 2015). Consequently, LN could not be determined in these conditions and only 254 out of 377 RILs survived until flowering.…”

Section: Growth Conditions and Measurements Of Flowering-related Traitsmentioning

confidence: 99%

Environmental and genetic interactions reveal FLOWERING LOCUSC as a modulator of the natural variation for the plasticity of flowering in Arabidopsis

Méndez‐Vigo

Savic

Ausín

et al. 2015

Plant Cell & Environment

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The timing of flowering initiation depends strongly on the environment, a property termed as the plasticity of flowering. Such plasticity determines the adaptive potential of plants because it provides phenotypic buffer against environmental changes, and its natural variation contributes to evolutionary adaptation. We addressed the genetic mechanisms of the natural variation for this plasticity in Arabidopsis thaliana by analysing a population of recombinant inbred lines derived from Don‐0 and Ler accessions collected from distinct climates. Quantitative trait locus (QTL) mapping in four environmental conditions differing in photoperiod, vernalization treatment and ambient temperature detected the folllowing: (i) FLOWERING LOCUS C (FLC) as a large effect QTL affecting flowering time differentially in all environments; (ii) numerous QTL displaying smaller effects specifically in some conditions; and (iii) significant genetic interactions between FLC and other loci. Hence, the variation for the plasticity of flowering is determined by a combination of environmentally sensitive and specific QTL, and epistasis. Analysis of FLC from Don identified a new and more active allele likely caused by a cis‐regulatory deletion covering the non‐coding RNA COLDAIR. Further characterization of four FLC natural alleles showed different environmental and genetic interactions. Thus, FLC appears as a major modulator of the natural variation for the plasticity of flowering to multiple environmental factors.

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

Cited by 35 publications

References 64 publications

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

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

Genetic Architecture of Natural Variation in Thermal Responses of Arabidopsis

Environmental and genetic interactions reveal FLOWERING LOCUSC as a modulator of the natural variation for the plasticity of flowering in Arabidopsis

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