Enhanced Vitamin C Production Mediated by an ABA-Induced PTP-like Nucleotidase Improves Plant Drought Tolerance in Arabidopsis and Maize

Abstract

Abscisic acid (ABA) is a key phytohormone that mediates environmental stress responses. Vitamin C, or L-ascorbic acid (AsA), is the most abundant antioxidant protecting against stress damage in plants. How the ABA and AsA signaling pathways interact in stress responses remains elusive. In this study, we characterized the role of a previously unidentified gene, PTPN (PTP-like Nucleotidase) in plant drought tolerance. In Arabidopsis, (AtPTPN was expressed in multiple tissues and upregulated by ABA and drought treatments. Loss-of-function mutants of AtPTPN were hyposensitive to ABA but hypersensitive to drought stresses, whereas plants with enhanced expression of AtPTPN showed opposite phenotypes to . Overexpression of maize PTPN (ZmPTPN) promoted, while knockdown of ZmPTPN inhibited plant drought tolerance, indicating conserved and positive roles of PTPN in plant drought tolerance. We found that both AtPTPN and ZmPTPN release Pi by hydrolyzing GDP/GMP/dGMP/IMP/dIMP, and that AtPTPN positively regulated AsA production via endogenous Pi content control. Consistently, overexpression of VTC2, the rate-limiting synthetic enzyme in AsA biosynthesis, promoted AsA production and plant drought tolerance, and these effects were largely dependent on AtPTPN activity. Furthermore, we demonstrated that the heat shock transcription factor HSFA6a directly binds the AtPTPN promoter and activates AtPTPN expression. Genetic analyses showed that AtPTPN is required for HSFA6a to regulate ABA and drought responses. Taken together, our data indicate that PTPN-mediated crosstalk between the ABA signaling and AsA biosynthesis pathways positively controls plant drought tolerance.

Benefiting others and self: Production of vitamins in plants

“…Genome‐wide association studeies, which are based on natural populations, characterizes leader single nucleotide polymorphisms (SNPs) through the association between genetic variants and phenotypic variations (Flint‐Garcia et al, 2003; Xiao et al, 2017; Fang and Luo, 2019). Studies using these strategies have made advances in exploring the genetic and biochemical bases of metabolism in a large number of model plants and crops species (Gong et al, 2013; Chen et al, 2014; Zhu et al, 2018; Zeng et al, 2020). Here, we mainly discuss forward genetic studies on vitamin synthesis in plants.…”

“…The tocopherol and tocotrienol levels in plants also respond strongly to abiotic stress, and the type of stress, the stress intensity, the physiological state of plants, and the sensitivity of species to stress play important roles in the accumulation of tocopherols (Munne-Bosch, 2005;Spicher et al, 2017). In recent years, the accumulation of ascorbic acid induced by stress has been proven to be through a variety of plant hormone such as ethylene and abscisic acid (Yu et al, 2019;Zhang et al, 2020).…”

Adaptive and maladaptive expression plasticity underlying herbicide resistance in an agricultural weed

“…It was possible to annotate 41 of the 68 genes with evidence of adaptive plasticity based on homology to Arabidopsis thaliana (Table S3). Some genes were connected to stress responses, like a homolog of ATR7, which regulates abiotic stress (Sujeeth et al 2020) , a homolog of PATL1 which is important for salt and freezing tolerance (Chu et al 2018;Zhou et al 2018) , a homolog of PHT4;6 which is important for salt tolerance (Cubero et al 2009) , an ortholog of P5CDH which is important for many abiotic stress responses (Sharma and Verslues 2010;Liu et al 2015;Ren et al 2018) and a homolog of AtPTPN, which contributes to drought stress in A. thaliana (Zhang et al 2020) . However, many genes identified as having adaptive plasticity did not have homologs with obvious links to processes important for herbicide or other stress responses (Table S3).…”

The Multiple Roles of Ascorbate in the Abiotic Stress Response of Plants: Antioxidant, Cofactor, and Regulator

“…In the early stage of stress response, ABA promotes ROS production and activates ROS signaling, thereby helping plants to respond rapidly to adverse environmental conditions (Kwak et al, 2003;Liu et al, 2010;Sahu and Kar, 2018). In contrast, during the late stage of stress adaptation, ABA activates the de novo synthesis and regeneration of ASC to scavenge the accumulated ROS and thus eliminate oxidative damage, to enhance plant abiotic stress tolerance (Zhang et al, 2020). This may explain why ABA inhibits ASC synthesis and accelerates ROS accumulation in some circumstances (Jiang and Zhang, 2002;Kwak et al, 2003;Yu et al, 2019), but induces ASC synthesis and ROS scavenging in others (Jiang and Zhang, 2002;Zhang et al, 2020).…”

“…In contrast, during the late stage of stress adaptation, ABA activates the de novo synthesis and regeneration of ASC to scavenge the accumulated ROS and thus eliminate oxidative damage, to enhance plant abiotic stress tolerance (Zhang et al, 2020). This may explain why ABA inhibits ASC synthesis and accelerates ROS accumulation in some circumstances (Jiang and Zhang, 2002;Kwak et al, 2003;Yu et al, 2019), but induces ASC synthesis and ROS scavenging in others (Jiang and Zhang, 2002;Zhang et al, 2020). Therefore, we hypothesize that ASC plays a more important role in regulating plant stress signal transduction at low cellular oxidation levels, and a more critical role in scavenging ROS at high cellular oxidation levels (Figure 3).…”