Reciprocal regulation between nicotinamide adenine dinucleotide metabolism and abscisic acid and stress response pathways in Arabidopsis

Abstract

Nicotinamide adenine dinucleotide (NAD) is an essential coenzyme that has emerged as a central hub linking redox equilibrium and signal transduction in living organisms. The homeostasis of NAD is required for plant growth, development, and adaption to environmental cues. In this study, we isolated a chilling hypersensitive Arabidopsis thaliana mutant named qs-2 and identified the causal mutation in the gene encoding quinolinate synthase (QS) critical for NAD biosynthesis. The qs-2 mutant is also hypersensitive to salt stress and abscisic acid (ABA) but resistant to drought stress. The qs-2 mutant accumulates a reduced level of NAD and over-accumulates reactive oxygen species (ROS). The ABA-hypersensitivity of qs-2 can be rescued by supplementation of NAD precursors and by mutations in the ABA signaling components SnRK2s or RBOHF. Furthermore, ABA-induced over-accumulation of ROS in the qs-2 mutant is dependent on the SnRK2s and RBOHF. The expression of QS gene is repressed directly by ABI4, a transcription factor in the ABA response pathway. Together, our findings reveal an unexpected interplay between NAD biosynthesis and ABA and stress signaling, which is critical for our understanding of the regulation of plant growth and stress responses.

Changes in intracellular NAD status affect stomatal development in an abscisic acid‐dependent manner

“…Consistent with this hypothesis, the NAD + carrier mutants showed increased expression of NAD + salvage pathway genes. Given that the levels of NAD + itself increased in the mutant lines, and considering the important role of NAD + in redox metabolism (Noctor et al ., 2006) and in abiotic stress management (Hong et al ., 2020), we next evaluated the expression of Zinc‐Finger Protein 12 ( ZAT12 ) as an indirect transcript indicator for enhanced reactive oxygen species (ROS) production (Gadjev et al ., 2006; Mehterov et al ., 2012; Xu et al ., 2017). The expression of ZAT12 was induced in the mutant lines, most prominently at 8 days (Figure S3).…”

“…The expression of ZAT12 was induced in the mutant lines, most prominently at 8 days (Figure S3). The potential role of increased ROS generation and the activation of RBOH‐dependent stress signaling in response to deregulated NAD homeostasis deserves in depth dissection in the future (Choudhury et al ., 2017; Hong et al ., 2020).…”

“…A recent functional characterization of NDT1 and NDT2 mutants had shown reduced seed germination, a phenotype previously explained by possible enhanced ABA levels and/or signaling (de Souza Chaves et al ., 2019; Feitosa‐Araujo et al ., 2020). Furthermore, NAD(P)(H) homeostasis has previously been associated with ABA biosynthesis and signaling (Hunt and Gray, 2009a; Arias et al ., 2018; Wei et al ., 2020; Hong et al ., 2020). Taken together, these observations raised the hypothesis that altered subcellular NAD + compartmentation may trigger changes in ABA metabolism, which in turn represses entry into the stomatal lineage.…”

“…(2019) demonstrated that plants with reduced NDT1 expression displayed lower values of transpiration rate and stomatal conductance. Furthermore, a recent forward genetics study found that mutation of the QS gene of the de novo NAD biosynthesis pathway rendered plants more tolerant to drought (Hong et al ., 2020).…”

“…Furthermore, unbalanced NAD + levels have been previously linked to increased ROS production rates and oxidative stress (Chai et al ., 2006; Katoh et al ., 2006; Schippers et al ., 2008; Luo et al ., 2019). Given the upregulation of the ROS marker transcript At ZAT12 (Xu et al ., 2017) in the mutant lines (Figure S3), and the role of NAD + homeostasis in plant abiotic stress tolerance (Hong et al ., 2020; Wei et al ., 2020), we suggest that NAD + transporter mutants may be suffering from increased oxidative stress and/or deregulated RBOH‐mediated signaling.…”