Nitric oxide negatively regulates AKT1-mediated potassium uptake through modulating vitamin B6 homeostasis in Arabidopsis

Abstract

Nitric oxide (NO), an active signaling molecule in plants, is involved in numerous physiological processes and adaptive responses to environmental stresses. Under high-salt conditions, plants accumulate NO quickly, and reorganize Na + and K + contents. However, the molecular connection between NO and ion homeostasis is largely unknown. Here, we report that NO lowers K + channel AKT1-mediated plant K + uptake by modulating vitamin B6 biosynthesis. In a screen for Arabidopsis NO-hypersensitive mutants, we isolated sno1 (sensitive to nitric oxide 1), which is allelic to the previously noted mutant sos4 (salt overly sensitive 4) that has impaired Na + and K + contents and overproduces pyridoxal 5′-phosphate (PLP), an active form of vitamin B6. We showed that NO increased PLP and decreased K + levels in plant. NO induced SNO1 gene expression and enzyme activity, indicating that NO-triggered PLP accumulation mainly occurs through SNO1-mediated vitamin B6 salvage biosynthetic pathway. Furthermore, we demonstrated that PLP significantly repressed the activity of K + channel AKT1 in the Xenopus oocyte system and Arabidopsis root protoplasts. Together, our results suggest that NO decreases K + absorption by promoting the synthesis of vitamin B6 PLP, which further represses the activity of K + channel AKT1 in Arabidopsis. These findings reveal a previously unidentified pivotal role of NO in modulating the homeostasis of vitamin B6 and potassium nutrition in plants, and shed light on the mechanism of NO in plant acclimation to environmental changes.genetic approach | electrophysiological studies | potassium nutrition N itric oxide (NO) acts as a crucial signaling molecule in various physiological processes in plants, such as seed germination and dormancy (1, 2), root development (3), leaf senescence (4, 5), floral transition (6), stomatal movement (7, 8), iron homeostasis (9, 10), and hormone responses (11,12). NO production is altered when plants are subjected to abiotic or biotic stresses (13,14). High salt, a major environmental factor that limits agriculture yield, induces a quick endogenous NO accumulation in plants (15,16), and triggers enhanced Na + influx and reduced K + absorption in the root (17). Both endogenously produced NO and exogenously applied NO have been proposed to enhance plant salt tolerance (18-21) by attenuating high saltinduced increases in the Na + to K + ratio. Genetic analysis showed that K + nutrition, but not Na + , plays critical role in plant salt tolerance (22). However, the molecular basis of NO effect on K + or Na + content is elusive.K + levels in plant tissues are determined by K + uptake and translocation, which are mediated by a large number of transporters and channels. In Arabidopsis, the K + channel AKT1 (23, 24) and K + transporter AtHAK5 (25) are the two major molecular entities responsible for K + absorption from the environment (26-28). AKT1 contributes to K + acquisition over a wide range of external K + concentrations (10 μM-10 mM), whereas AtHAK5 mediates limited uptake capac...

AtPep3 is a hormone-like peptide that plays a role in the salinity stress tolerance of plants

“…PLP is also recognized as a cofactor of several enzymes and can bind to ion channels and may therefore regulate Na + influx (54,55). It is possible that the regulation of Na + influx by activated AtPep3/AT13 peptide might be the basis for the observed salinity stress tolerance observed in the present study, which is opposite of the response reported in the salt overly sensitive 4 mutant (54,56,57).…”

Nitric Oxide: A Multitasked Signaling Gas in Plants

“…Furthermore, Ca 2+ in release through NAADP-, ryanodine-, and inositol-1,4,5-triphosphate-sensitive Ca 2+ channels was also shown to be activated by NO and H 2 O 2 , either by oxidation and/or nitrosylation of thiol groups present in these proteins. A genetic approach provided evidence that NO lowers K + -channel AKT1-mediated K + absorption by modulating vitamin B 6 biosynthesis, implying a role of NO in the control of high-K + content conditions in plants (Xia et al, 2014).…”

Nitric oxide induces monosaccharide accumulation through enzyme S‐nitrosylation

“…Nitric oxide (NO) is involved in many of the universal functions that orchestrate physiological and developmental processes in plants, such as floral transition (He et al 2004), root development (Pagnussat, Simontacchi, Puntarulo, & Lamattina 2002;Bai et al 2012), seed germination (Wang, Zhu, & Lang 2015), leaf senescence (Mishina, Lamb, & Zeier 2007;Du et al 2014), stomatal movement (Scuffi et al 2014;Xie et al 2014), iron homeostasis (Graziano and Lamattina 2005;Ramirez, Simontacchi, Murgia, Zabaleta, & Lamattina 2011;Xia et al 2014) and hormone crosstalk (Liu et al 2013;Sanz et al 2015). In addition to the regulatory roles of NO in these signalling events and developmental processes, NO is also responsible for at least three posttranslational modifications to target proteins by nitrosylation: Firstly, the NO moiety interacts with metalloproteins in a so-called metal nitration.…”