The SLIM1 transcription factor affects sugar signaling during sulfur deficiency in Arabidopsis

Abstract

The homeostasis of major macronutrient metabolism needs to be tightly regulated, especially when the availability of one or more nutrients fluctuates in the environment. Both sulfur metabolism and glucose signaling are important processes throughout plant growth and development, as well as during stress responses. Still, very little is known about how these processes affect each other, although they are positively connected. Here, we showed that the crucial transcription factor of sulfur metabolism, SLIM1, is involved in glucose signaling during the shortage of sulfur. The germination rate of the slim1_KO mutant was severely affected by high glucose and osmotic stress. The expression of SLIM1-dependent genes in sulfur deficiency appeared to be additionally induced by the high concentration of either mannitol or glucose, but also by sucrose, which is not only the source of glucose but another signaling molecule. Additionally, SLIM1 affects PAP1 expression during sulfur deficiency by directly binding to its promoter. The lack of PAP1 induction in such conditions leads to much lower anthocyanin production. Taken together, our results indicate that SLIM1 is involved in the glucose response by modulating sulfur metabolism and directly controlling PAP1 expression in Arabidopsis during sulfur deficiency stress.

New insights into the regulation of plant metabolism by O-acetylserine: sulfate and beyond

“…SDI2 seems rather to be repressed by SLIM1 while SDI1 needs the presence of SLIM1 under sulfur-depleted conditions ( Dietzen et al , 2020 ). The promoters of the SLIM1/EIL3-regulated genes contain the known cis -elements UPE-box and TEBs ( Wawrzyńska et al , 2010 , 2022 ), and SURE elements were recently proven to bind EIL2/SLIM1( Rakpenthai et al , 2022 ). In silico and in vitro analyses of the promoter regions revealed many more putative cis -elements, indicating that further TFs are potentially able to bind to the promoter regions ( Table 3 ).…”

“…From the OAS co-expression cluster, BGLU28 , BGLU30 , and PYD also display features indicating independent sulfate deprivation and OAS signaling pathways, probably acting in parallel under sulfate-deprived growth conditions. Having a knockout SLIM1 line available ( Wawrzyńska et al , 2022 ) now provides the possibility to test this experimentally. Based on the fact that stresses other than sulfate deprivation result in OAS accumulation and the common responses of the OAS cluster genes, we have to assume that OAS signaling is distinct from sulfate deprivation signaling, though both coincide under sulfate-deprived growth conditions.…”

“…Which signals are perceived and how TFs regulate these responses is still not finally resolved ( Kopriva, 2006 ). Some progress has been achieved and suggestions provided ( Maruyama-Nakashita et al , 2006 ; Zhang et al ., 2014 ; Bielecka et al , 2015 ; Aarabi et al , 2016 ; Huang et al , 2016 ; Watanabe and Hoefgen, 2017 , 2019 ; Forzani et al , 2018 ; Rakpenthai et al , 2022 ; Wawrzyńska et al , 2022 ). In addition to these analyses, available databases allow the identification of TFs possibly involved in the OAS-driven response.…”

“…EIL3/SLIM1 is involved in the sulfate deprivation signaling pathway and is a central transcriptional regulator of plant sulfate metabolism ( Maruyama-Nakashita et al , 2006 ; Wawrzyńska et al , 2010 , 2022 ; Kawashima et al , 2011 ; Wawrzyńska and Sirko, 2014 , 2016 ; Dietzen et al , 2020 ; Rakpenthai et al , 2022 ), by controlling many sulfate deprivation response genes. EIL3/SLIM1 binds to the UPE box, the TEBS element, and the SURE element, which are present in many sulfate- and OAS-responsive genes ( Maruyama-Nakashita et al , 2005 ; Wawrzyńska et al , 2010 ; Rakpenthai et al , 2022 ).…”

Why do plants blush when they are hungry?

“…During sulphur deficiency as key TF, SLIM1 is induced in a sugar‐dependent manner (Wawrzyńska et al ., 2022). SLIM1 belongs to a small family of plant‐specific TFs, which include EIN3 and EIL1, that regulate the ethylene‐responsive gene expression.…”