Snf1-RELATED KINASE1-Controlled C/S₁-bZIP Signaling Activates Alternative Mitochondrial Metabolic Pathways to Ensure Plant Survival in Extended Darkness

Abstract

Sustaining energy homeostasis is of pivotal importance for all living organisms. In , evolutionarily conserved SnRK1 kinases (Snf1-RELATED KINASE1) control metabolic adaptation during low energy stress. To unravel starvation-induced transcriptional mechanisms, we performed transcriptome studies of inducible knockdown lines and found that S-basic leucine zipper transcription factors (S-bZIPs) control a defined subset of genes downstream of SnRK1. For example, S-bZIPs coordinate the expression of genes involved in branched-chain amino acid catabolism, which constitutes an alternative mitochondrial respiratory pathway that is crucial for plant survival during starvation. Molecular analyses defined S-bZIPs as SnRK1-dependent regulators that directly control transcription via binding to G-box promoter elements. Moreover, SnRK1 triggers phosphorylation of group C-bZIPs and the formation of C/S-heterodimers and, thus, the recruitment of SnRK1 directly to target promoters. Subsequently, the C/S-bZIP-SnRK1 complex interacts with the histone acetylation machinery to remodel chromatin and facilitate transcription. Taken together, this work reveals molecular mechanisms underlying how energy deprivation is transduced to reprogram gene expression, leading to metabolic adaptation upon stress.

Metabolite Regulatory Interactions Control Plant Respiratory Metabolism via Target of Rapamycin (TOR) Kinase Activation

“…Gly is the predominant amino acid substrate supplied to leaf mitochondria because of photorespiration in the light. The induced use of other amino acids as respiratory substrates under carbon starvation or senescence, in particular Ile, Leu, Val, and Lys, is well studied and has been linked to a SnRK1-bZIP signal transduction pathway and the upregulation of the ETF/ETFQO complex (Araújo et al, 2010;Cavalcanti et al, 2017;Pedrotti et al, 2018). By contrast, a connection that distinguishes Ala and Pro from most other amino acids is that they are both well known to accumulate in response to certain stresses; furthermore, this accumulation occurs at least partly in the cytosol in the case of Pro (Ketchum et al, 1991;Gagneul et al, 2007).…”

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

“…This topic is further discussed in another review of this special issue focusing on mitochondrial retrograde signals (Wagner et al, 2018). The finding that bZIP63 is a direct regulator of ETFQO and thereby affects mitochondrial electron transport (Pedrotti et al, 2018) and the identification of several differentially phosphorylated proteins in chloroplasts and mitochondria in AKIN10/11 mutants (Nukarinen et al, 2016) prompted us to screen further for target genes of those TFs, which have been identified as SnRK1 targets. In addition to the already mentioned EIN3, MYC2, IDD8, and bZIP63, we also included here Wrinkled1 (WRI1), a member of the plant-specific APE-TALA2 family, and the B3 domain TF FUSCA3 (FUS3), for both of which a direct interaction with AKIN10 has recently been shown.…”

“…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. 1).…”

An abscisic acid-responsive protein interaction network for sucrose non-fermenting related kinase1 in abiotic stress response

“…These changes were shown to promote major catabolic pathways and repress anabolic processes 14 . Similar processes were affected in conditional snrk1α1 snrk1α2 double mutants and shown to be regulated by SnRK1 phosphorylation targets, the S1-bZIP transcription factors 15,16 . SnRK1α can phosphorylate ABI5 in vitro and is itself dephosphorylated and inactivated by the PP2Cs, ABI1 and AHG3 17,18 .…”