Fructose sensitivity is suppressed in Arabidopsis by the transcription factor ANAC089 lacking the membrane-bound domain

Abstract

In living organisms sugars not only provide energy and carbon skeletons but also act as evolutionarily conserved signaling molecules. The three major soluble sugars in plants are sucrose, glucose, and fructose. Information on plant glucose and sucrose signaling is available, but to date no fructose-specific signaling pathway has been reported. In this study, sugar repression of seedling development was used to study fructose sensitivity in the Landsberg erecta (Ler)/Cape Verde Islands (Cvi) recombinant inbred line population, and eight fructose-sensing quantitative trait loci (QTLs) (FSQ1-8) were mapped. Among them, FSQ6 was confirmed to be a fructose-specific QTL by analyzing near-isogenic lines in which Cvi genomic fragments were introgressed in the Ler background. These results indicate the existence of a fructose-specific signaling pathway in Arabidopsis. Further analysis demonstrated that the FSQ6-associated fructose-signaling pathway functions independently of the hexokinase1 (HXK1) glucose sensor. Remarkably, fructosespecific FSQ6 downstream signaling interacts with abscisic acid (ABA)-and ethylene-signaling pathways, similar to HXK1-dependent glucose signaling. The Cvi allele of FSQ6 acts as a suppressor of fructose signaling. The FSQ6 gene was identified using mapbased cloning approach, and FSQ6 was shown to encode the transcription factor gene Arabidopsis NAC (petunia No apical meristem and Arabidopsis transcription activation factor 1, 2 and Cup-shaped cotyledon 2) domain containing protein 89 (ANAC089). The Cvi allele of FSQ6/ANAC089 is a gain-of-function allele caused by a premature stop in the third exon of the gene. The truncated Cvi FSQ6/ ANAC089 protein lacks a membrane association domain that is present in ANAC089 proteins from other Arabidopsis accessions. As a result, Cvi FSQ6/ANAC089 is constitutively active as a transcription factor in the nucleus. I n plants, sugars provide the energy and carbon skeletons needed for growth and in addition act as crucial signaling molecules that affect growth, development, and response to the (a)biotic environment (1-3). Plant cells harbor sugar-sensing and -signaling systems that regulate the expression of thousands of genes and control the metabolic processes needed for growth (2-4). These sugar-response systems are known to interact with other signaling pathways, such as those for light, phytohormones, stress, and nutrients (1).The neutral sugars sucrose, glucose, and fructose are central to metabolism in plants and in other organisms as well. So far, detailed information is available only on glucose sensing, and it has been shown that the hexokinase 1 (HXK1) enzyme acts as a glucose sensor (5, 6). Sucrose-specific signaling also was demonstrated because the effect of sucrose cannot be mimicked by glucose and/or fructose (7), but so far no information on sucrosesensing systems is available. A signaling function for fructose has been proposed (8, 9), but no convincing experimental evidence on such fructose-specific signaling is available.In Arabidopsis ea...

NAC Transcription Factor SPEEDY HYPONASTIC GROWTH Regulates Flooding-Induced Leaf Movement in Arabidopsis

“…NAC TFs have been shown to be involved in many developmental and stress-related processes in plants Jensen et al, 2008;Ogo et al, 2008;Berger et al, 2009;Kim et al, 2009;Wu et al, 2009Wu et al, , 2012Balazadeh et al, 2010;Li et al, 2011;Zhong et al, 2011;Lee et al, 2012). Here, we report the biological function of SHYG, a group III NAC TF from Arabidopsis, in root flooding-induced hyponastic leaf growth.…”

“…NAC TFs typically contain a highly conserved N-terminal DNA binding domain and a divergent C-terminal part (Olsen et al, 2005). NAC TFs play important roles in various biological processes, including senescence (Guo and Gan, 2006;Kim et al, 2009;Balazadeh et al, 2010Balazadeh et al, , 2011Lee et al, 2012;Hickman et al, 2013;Rauf et al, 2013), the response to abiotic and biotic stresses Hu et al, 2006;Jensen et al, 2008;Wang et al, 2009;Wu et al, 2009;Jeong et al, 2010), leaf development (Berger et al, 2009), secondary wall biosynthesis (Zhong et al, 2010(Zhong et al, , 2011, regulation of Fru sensitivity (Li et al, 2011), regulation of iron homeostasis (Ogo et al, 2008), and others. The NAC TF VASCULAR-RELATED NAC-DOMAIN INTERACTING2 (ANAC083) integrates abscisic acid signaling with leaf senescence (Yang et al, 2011) and negatively regulates xylem vessel formation (Yamaguchi et al, 2010).…”

Arabidopsis Roots and Shoots Show Distinct Temporal Adaptation Patterns toward Nitrogen Starvation

“…In addition, sugars, especially Glc, Fru, and Suc, are important signaling molecules Rolland and Sheen, 2005;Rook et al, 2006;Li et al, 2011), and starch is a main indicator for growth (Sulpice et al, 2009). Thus, we analyzed the sugar accumulation kinetics in response to a sudden N starvation in the roots and shoots.…”

TANG1, Encoding a Symplekin_C Domain-Contained Protein, Influences Sugar Responses in Arabidopsis

“…A G-protein-coupled receptor system was also identified in sugar signaling response studies in yeast and Arabidopsis (Chen and Jones, 2004;Lemaire et al, 2004;Huang et al, 2006;Fu et al, 2014). Recently, a Fru-specific signaling pathway was also proposed by the identification of the transcription factor ANAC089 (NAC [for NAM/ ATAF1/2/CUC2) and the Fru-1,6-bisPase Fructose insensitive1 (Cho and Yoo, 2011;Li et al, 2011). Another NAC transcription factor, ANAC060, isolated by quantitative trait locus analysis, also exhibits function in sugar and ABA signaling pathways (Li et al, 2014).…”