ZmG6PDH1 in glucose-6-phosphate dehydrogenase family enhances cold stress tolerance in maize

Abstract

Glucose-6-phosphate dehydrogenase (G6PDH) is a key enzyme in the pentose phosphate pathway responsible for the generation of nicotinamide adenine dinucleotide phosphate (NADPH), thereby playing a central role in facilitating cellular responses to stress and maintaining redox homeostasis. This study aimed to characterize five G6PDH gene family members in maize. The classification of these ZmG6PDHs into plastidic and cytosolic isoforms was enabled by phylogenetic and transit peptide predictive analyses and confirmed by subcellular localization imaging analyses using maize mesophyll protoplasts. These ZmG6PDH genes exhibited distinctive expression patterns across tissues and developmental stages. Exposure to stressors, including cold, osmotic stress, salinity, and alkaline conditions, also significantly affected the expression and activity of the ZmG6PDHs, with particularly high expression of a cytosolic isoform (ZmG6PDH1) in response to cold stress and closely correlated with G6PDH enzymatic activity, suggesting that it may play a central role in shaping responses to cold conditions. CRISPR/Cas9-mediated knockout of ZmG6PDH1 on the B73 background led to enhanced cold stress sensitivity. Significant changes in the redox status of the NADPH, ascorbic acid (ASA), and glutathione (GSH) pools were observed after exposure of the zmg6pdh1 mutants to cold stress, with this disrupted redox balance contributing to increased production of reactive oxygen species and resultant cellular damage and death. Overall, these results highlight the importance of cytosolic ZmG6PDH1 in supporting maize resistance to cold stress, at least in part by producing NADPH that can be used by the ASA-GSH cycle to mitigate cold-induced oxidative damage.

Genome-wide diversity in lowland and highland maize landraces from southern South America: population genetics insights to assist conservation

“…Additionally, three outlier SNPs were found within genes whose expression is modified under stress conditions (Supplementary table 8A): the gene Zm00001d020497, identified as cipk28 (calcineurin B-like-interacting protein kinase28), has been observed to exhibit responses to both salt and drought stresses (Chen et al, 2013; Feng et al, 2022). Similarly, Zm00001d047587 encodes a glucose-6-phosphate dehydrogenase (G6PDH3) and has demonstrated induction under osmotic and cold stress (Li et al, 2023). Furthermore, Zm00001d025651, orthologous to the Arabidopsis poly(A)-specific ribonuclease AtPARN, is implicated in a mRNA degradation system crucial to ABA, salicylic acid, and stress responses in Arabidopsis (Nishimura et al, 2005).…”

In Silico RNAseq and Biochemical Analyses of Glucose-6-Phosphate Dehydrogenase (G6PDH) from Sweet Pepper Fruits: Involvement of Nitric Oxide (NO) in Ripening and Modulation

“…The number of G6PDH genes changes significantly among plant species. Thus, 19 G6PDH genes in strawberry (Fragaria × ananassa) [18], 9 in soybean (Glycine max) [35], 6 in Arabidopsis thaliana [8], 5 in rice (Oryza sativa), Arabidopsis tauchii, tomato (Solanum lycopersicum) [27], and maize (Zea mays) [27], and 4 G6PDH genes in rubber tree (Hevea brasiliensis) [36] and einkorn wheat (Triticum urartu) [37] have been reported. Therefore, the four CaG6PDH genes identified in this work indicate that pepper is among the species with the lowest number of G6PDH genes.…”

“…Between 10-15 exons were counted in the G6PDH genes and, in the case of the CaG6PDH3 gene (almost 24 kb length), it contained two very large introns above 6 kb each. Maize plants enclose five genes and, among them, the ZmG6PDH4 gene length is almost 18 kb with 9 exons and two large introns [27]. Strawberries have 19 G6PDH genes with 10 to 15 exons, but the largest gene which corresponds to FaG6PD14 has less than 7 kb [18].…”

“…Different studies have correlated the G6PDH activity in plants with physiological processes such as germination and development [16][17][18][19][20], but also with the mechanisms of response to numerous environmental stresses [21,22] including salinity [23][24][25], water stress [22,23], mechanical wounding, arsenic, chromium, aluminum [24], herbicides [25], low temperature [26,27], potassium deficiency or pathogens [28,29].…”