Abstract
Seedling establishment is inhibited on media containing high levels (∼6%) of glucose or fructose. Genetic loci that overcome the inhibition of seedling growth on high sugar have been identified using natural variation analysis and mutant selection, providing insight into sugar signaling pathways. In this study, a quantitative trait locus (QTL) analysis was performed for seedling sensitivity to high sugar in a Col/C24 F2 population of Arabidopsis thaliana. A glucose and fructose-sensing QTL, GSQ11, was mapped through selective genotyping and confirmed in near-isogenic lines in both Col and C24 backgrounds. Allelism tests and transgenic complementation showed that GSQ11 lies within the ANAC060 gene. The Col ANAC060 allele confers sugar insensitivity and was dominant over the sugar-sensitive C24 allele. Genomic and mRNA analyses showed that a single-nucleotide polymorphism (SNP) in Col ANAC060 affects the splicing patterns of ANAC060 such that 20 additional nucleotides are present in the mRNA. The insertion created a stop codon, resulting in a truncated ANAC60 protein lacking the transmembrane domain (TMD) that is present in the C24 ANAC060 protein. The absence of the TMD results in the nuclear localization of ANAC060. The short version of the ANAC060 protein is found in ∼12% of natural Arabidopsis accessions. Glucose induces GSQ11/ANAC060 expression in a process that requires abscisic acid (ABA) signaling. Chromatin immunoprecipitation-qPCR and transient expression analysis showed that ABI4 directly binds to the GSQ11/ANAC060 promoter to activate transcription. Interestingly, Col ANAC060 reduced ABA sensitivity and Glc-induced ABA accumulation, and ABI4 expression was also reduced in Col ANAC060 lines. Thus, the sugar-ABA signaling cascade induces ANAC060 expression, but the truncated Col ANAC060 protein attenuates ABA induction and ABA signaling. This negative feedback from nuclear ANAC060 on ABA signaling results in sugar insensitivity.
Highlights
Plant growth and development depends on the energy and carbon building blocks provided by soluble sugars
Mutants that are insensitive or oversensitive to different sugars have been isolated in this way, and the genes involved have been identified. Such genes function in a variety of biological processes [11,12,13,14,15,16,17,18], and it is challenging to understand how these genes participate in sugar signaling pathways. Prominent among these genes are HEXOKINASE1 (HXK1), which functions as a glucose (Glc) sensor [7], and genes involved in abscisic acid (ABA) and ethylene synthesis and signaling [11,12,17,19]
The sugarABA cascade regulates many genes involved in photosynthesis and metabolism and is antagonized by ethylene signaling via the EIN3 protein [20,21]
Summary
Plant growth and development depends on the energy and carbon building blocks provided by soluble sugars. For efficient carbon nutrient utilization, prokaryotic and eukaryotic organisms have evolved a range of sophisticated signal transduction pathways that link sugar status to growth and reproduction [1,2,3]. In plants, such sugar-sensing and -signaling systems regulate the expression of thousands of genes involved in the control of metabolic processes, growth, development and responses to the environment [4,5]. A central regulator in sugar-responsive gene expression in plants is the ABI4 gene, which encodes an ERF/
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