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

Abstract

SUMMARY Nicotinamide adenine dinucleotide (NAD) plays a central role in redox metabolism in all domains of life. Additional roles in regulating posttranslational protein modifications and cell signaling implicate NAD as a potential integrator of central metabolism and programs regulating stress responses and development. Here we found that NAD negatively impacts stomatal development in cotyledons of Arabidopsis thaliana. Plants with reduced capacity for NAD+ transport from the cytosol into the mitochondria or the peroxisomes exhibited reduced numbers of stomatal lineage cells and reduced stomatal density. Cotyledons of plants with reduced NAD+ breakdown capacity and NAD+‐treated cotyledons also presented reduced stomatal number. Expression of stomatal lineage‐related genes was repressed in plants with reduced expression of NAD+ transporters as well as in plants treated with NAD+. Impaired NAD+ transport was further associated with an induction of abscisic acid (ABA)‐responsive genes. Inhibition of ABA synthesis rescued the stomatal phenotype in mutants deficient in intracellular NAD+ transport, whereas exogenous NAD+ feeding of aba‐2 and ost1 seedlings, impaired in ABA synthesis and ABA signaling, respectively, did not impact stomatal number, placing NAD upstream of ABA. Additionally, in vivo measurement of ABA dynamics in seedlings of an ABA‐specific optogenetic reporter − ABAleon2.1 − treated with NAD+ showed increases in ABA content suggesting that NAD+ impacts on stomatal development through ABA synthesis and signaling. Our results demonstrate that intracellular NAD+ homeostasis as set by synthesis, breakdown and transport is essential for normal stomatal development, and provide a link between central metabolism, hormone signaling and developmental plasticity.

A phytobacterial TIR domain effector manipulates NAD+ to promote virulence

“…Unlike AvrPtoB, HopAM1 and HopF2 act similarly to enhance ABA sensitivity and suppress immune responses for P. syringae virulence, but the underlying biochemical mechanism is not known (de Torres‐Zabala et al ., 2007 ; Goel et al ., 2008 ; Cao et al ., 2019 ). However, recent studies have revealed an unexpected link between NAD + and the ABA response pathway with NAD + regulation probably upstream of ABA signaling (Feitosa‐Araujo et al ., 2020 ; Hong et al ., 2020 ). While endogenous NAD + levels in plant leaves are depleted as a consequence of HopAM1 overexpression via Agrobacterium ‐mediated transformation, NAD + homeostasis is not changed significantly by T3SS‐delivered HopAM1.…”

TOR and SnRK1 fine tune SPEECHLESS transcription and protein stability to optimize stomatal development in response to exogenously supplied sugar

“…NAD(P) + was believed to be a key regulator on energy metabolism and carbon : nitrogen (C : N) balance (Takahashi et al ., 2009). A recent study reported that mutant of NAD + mitochondria transporter ndt1 − :ndt1 − and ndt2 − :ndt2 − displayed the decreased meristemoids number and stomata production (Feitosa‐Araujo et al ., 2020), suggesting the energy homeostasis plays a critical role for stomatal development. Here, we provide several lines of evidence demonstrating that sugar and TOR play the critical roles in the cell proliferation for stomatal development.…”

Genome-Wide Identification of Cotton (Gossypium spp.) Glycerol-3-Phosphate Dehydrogenase (GPDH) Family Members and the Role of GhGPDH5 in Response to Drought Stress

“…It may be linked to ABA, which plays a key role in regulating stomatal movement [ 50 , 51 , 52 ]. Recent studies have shown that the exogenous application of NAD leads to an increase in the ABA content [ 53 ]. At the same time, an increase or decrease in NAD leads to a decrease in plant stomatal number and density, suggesting that NAD may indirectly affect stomatal development by influencing ABA synthesis and signal transduction [ 54 ].…”