NUCLEAR PORE ANCHOR and EARLY IN SHORT DAYS 4 negatively regulate abscisic acid signaling by inhibiting Snf1‐related protein kinase2 activity and stability in Arabidopsis

Abstract

Abscisic acid (ABA) is a key regulator of plant responses to abiotic stresses, such as drought. Abscisic acid receptors and coreceptors perceive ABA to activate Snf1‐related protein kinase2s (SnRK2s) that phosphorylate downstream effectors, thereby activating ABA signaling and the stress response. As stress responses come with fitness penalties for plants, it is crucial to tightly control SnRK2 kinase activity to restrict ABA signaling. However, how SnRK2 kinases are inactivated remains elusive. Here, we show that NUCLEAR PORE ANCHOR (NUA), a nuclear pore complex (NPC) component, negatively regulates ABA‐mediated inhibition of seed germination and post‐germination growth, and drought tolerance in Arabidopsis thaliana. The role of NUA in response to ABA depends on SnRK2.2 and SnRK2.3 for seed germination and on SnRK2.6 for drought. NUA does not directly inhibit the phosphorylation of these SnRK2s or affects their abundance. However, the NUA‐interacting protein EARLY IN SHORT DAYS 4 (ESD4), a SUMO protease, negatively regulates ABA signaling by directly interacting with and inhibiting SnRK2 phosphorylation and protein levels. More importantly, we demonstrated that SnRK2.6 can be SUMOylated in vitro, and ESD4 inhibits its SUMOylation. Taken together, we identified NUA and ESD4 as SnRK2 kinase inhibitors that block SnRK2 activity, and reveal a mechanism whereby NUA and ESD4 negatively regulate plant responses to ABA and drought stress possibly through SUMOylation‐dependent regulation of SnRK2s.

NUA positively regulates plant immunity by coordination with ESD4 to deSUMOylate TPR1 in Arabidopsis

“…In line with the SUMO protease activity of ESD4, mutations in ESD4 lead to an increase in SUMO conjugates (Murtas et al ., 2003). nua mutants phenocopy esd4 in several phenotypic characteristics, thus, the two proteins are proposed to act in the shared pathway or complex (Xu et al ., 2007; Chang et al ., 2022). Based on these findings, we hypothesized that NUA may be involved in the regulation of TPR1 deSUMOylation through ESD4.…”

“…NUCLEAR PORE ANCHOR and ESD4 function in the same pathway to regulate plant development and ABA signaling (Xu et al ., 2007; Chang et al ., 2022). However, in contrast to the enhanced susceptibility in nua mutants, esd4 mutants display autoimmunity with elevated levels of SA and upregulated expression of PR1 gene (Villajuana‐Bonequi et al ., 2014; Huang et al ., 2022).…”

“…It would be interesting to examine whether ESD4 deSUMOylates other NPC components, and the possibility that other SUMO proteases are involved in TPR1 deSUMOylation cannot be ruled out. NUCLEAR PORE ANCHOR and ESD4 function in the same pathway to regulate plant development and ABA signaling (Xu et al, 2007;Chang et al, 2022). However, in contrast to the enhanced susceptibility in nua mutants, esd4 mutants display autoimmunity with elevated levels of SA and upregulated expression of PR1 gene (Villajuana-Bonequi et al, 2014;Huang et al, 2022).…”

How plants sense and respond to osmotic stress

“…Besides clade A PP2Cs, a clade I PP2C Drought-Induced Wilting 1 (DIW1, TaPP2C158), is also a negative regulator of both drought and ABA signaling in wheat (Wang et al, 2023a). SnRK2 activity and stability may also be repressed by SUMOylation via the SUMO protease EARLY IN SHORT DAYS 4 (ESD4) (Chang et al, 2022). The ABA-hypersensitive abi1-2abi2-2hab1-1pp2ca-1 quadruple mutant exhibited enhanced hydrotropism (Antoni et al, 2013), demonstrating that clade A PP2Cs are negative regulators of hydrotropism.…”

Tyrosylprotein sulfotransferase suppresses ABA signaling via sulfation of SnRK2.2/2.3/2.6

“…Snf1‐related kinase 2 (SnRK2) family members SnRK2.2, SnRK2.3, and SnRK2.6 are central components of abscisic acid (ABA) signaling (Yang et al, 2019; Chen et al, 2020a). SnRK2s proteins undergo various post‐translational modifications (PTMs), such as phosphorylation (Vilela et al, 2015; Takahashi et al, 2020; Pizzio and Rodriguez, 2022), dephosphorylation (Umezawa et al, 2009), ubiquitination (Cheng et al, 2017; Ali et al, 2019), S‐nitrosylation (Wang et al, 2015), glutathionylation (Ma et al, 2018), persulfidation (Chen et al, 2020b), and SUMOylation (Chang et al, 2022).…”