Crosstalk between Two bZIP Signaling Pathways Orchestrates Salt-Induced Metabolic Reprogramming in Arabidopsis Roots

Abstract

ORCID IDs: 0000-0003-3058-7570 (A.F.); 0000-0002-7910-9118 (J.S.); 0000-0001-8122-5460 (M.J.M.); 0000-0002-6332-1712 (J.V.-C.); 0000-0002-5605-7984 (J.H.)Soil salinity increasingly causes crop losses worldwide. Although roots are the primary targets of salt stress, the signaling networks that facilitate metabolic reprogramming to induce stress tolerance are less understood than those in leaves. Here, a combination of transcriptomic and metabolic approaches was performed in salt-treated Arabidopsis thaliana roots, which revealed that the group S1 basic leucine zipper transcription factors bZIP1 and bZIP53 reprogram primary C-and N-metabolism. In particular, gluconeogenesis and amino acid catabolism are affected by these transcription factors. Importantly, bZIP1 expression reflects cellular stress and energy status in roots. In addition to the well-described abiotic stress response pathway initiated by the hormone abscisic acid (ABA) and executed by SnRK2 (Snf1-RELATED-PROTEIN-KINASE2) and AREB-like bZIP factors, we identify a structurally related ABA-independent signaling module consisting of SnRK1s and S1 bZIPs. Crosstalk between these signaling pathways recruits particular bZIP factor combinations to establish at least four distinct gene expression patterns. Understanding this signaling network provides a framework for securing future crop productivity.

Transcriptomes of eight Arabidopsis thaliana accessions reveal core conserved, genotype- and organ-specific responses to flooding stress

“…Further metabolic evidence for amino acid catabolism comes from Arabidopsis mutants defective in energy starvation signaling. In these lines, a similar suite of catabolic and gluconeogenic genes were regulated as observed here, including PPDK, and a subsequent altered metabolic profile was observed (Hartmann et al, 2015). However, it is difficult to discern metabolic fluxes from transcriptomic and metabolomic data except when start or end products of specific routes are quantified.…”

Gene Regulation and Survival under Hypoxia Requires Starch Availability and Metabolism

“…9), thus ruling out this possible link. Besides bZIP63, other bZIP genes such as bZIP1 and bZIP53 (Hartmann et al, 2015) could be involved in the regulation of anaerobic genes, a hypothesis requiring further work. The lower expression of DIN6, coding for an Asn synthase, observed in D-RAP2.12 and 35S: MA-RAP2.3 plants (Fig.…”

The SnRK1 Kinase as Central Mediator of Energy Signaling between Different Organelles

“…In these studies, it was commonly observed that the level of primary carbohydrates, Pro, and branched-chain amino acids (BCAAs) was strongly regulated by different combinations of bZIP TFs. For example, a bzip1 bzip53 double mutant was found to be affected in the coordination of BCAA catabolism under salt stress conditions, indicating a central function of these bZIPs in amino acid breakdown (Hartmann et al, 2015). Also, mutants defective in the bZIP63 TF showed increased levels of many proteinogenic amino acids, particularly under conditions of energy deprivation (Mair et al, 2015).…”

“…Particularly, the breakdown of BCAAs has recently gained more attention, leading to the conclusion that ETF/ETFQO is an essential pathway to donate electrons to the mETC and that amino acids are alternative substrates to maintain respiration under carbohydrate starvation (Cavalcanti et al, 2017). A functional link to SnRK1 via bZIP TFs has been suggested based on the observation that different bZIP TFs of the groups C and S were found to regulate amino acid breakdown, particularly Pro and BCAAs (Hanson et al, 2008;Dietrich et al, 2011;Hartmann et al, 2015). ETFQO can directly fuel electrons to the mETC and has recently been identified as direct target gene regulated by bZIP63 (Pedrotti et al, 2018), thereby providing the first functional link between SnRK1 and mitochondrial energy metabolism (Fig.…”

“…b Proteins found to be significantly (P , 5%) differentially phosphorylated in leaves between AKIN10 wild-type and knockdown plants at one or more time points within a time series along the transition into extended night (Nukarinen et al, 2016). stress, salt stress, or during dark-induced senescence (Hanson et al, 2008;Alonso et al, 2009;Weltmeier et al, 2009;Dietrich et al, 2011;Hartmann et al, 2015). In these studies, it was commonly observed that the level of primary carbohydrates, Pro, and branched-chain amino acids (BCAAs) was strongly regulated by different combinations of bZIP TFs.…”