Chloroplastic SaNADP-ME4 of C(3)–C(4) Woody Desert Species Salsola laricifolia Confers Drought and Salt Stress Resistance to Arabidopsis

The NADP-malic enzyme (NADP-ME) catalyzes the reversible decarboxylation of L-malate to produce pyruvate, CO(2), and NADPH in the presence of a bivalent cation. In addition, this enzyme plays crucial roles in plant developmental and environment responses, especially for the plastidic isoform. However, this isoform is less studied in C(3)–C(4) intermediate species under drought and salt stresses than in C(3) and C(4) species. In the present study, we characterized SaNADP-ME4 from the intermediate woody desert species Salsola laricifolia. SaNADP-ME4 encoded a protein of 646 amino acids, which was found to be located in the chloroplasts based on confocal imaging. Quantitative real-time PCR analysis showed that SaNADP-ME4 was highly expressed in leaves, followed by stems and roots, and SaNADP-ME4 expression was improved and reached its maximum under the 200 mm mannitol and 100 mm NaCl treatments, respectively. Arabidopsis overexpressing SaNADP-ME4 showed increased root length and fresh weight under mannitol and salt stress conditions at the seedling stage. In the adult stage, SaNADP-ME4 could alleviate the decreased in chlorophyll contents and PSII photochemical efficiency, as well as improve the expression of superoxide dismutase, peroxidase, and pyrroline-5-carboxylate synthase genes to enhance reactive oxygen species scavenging capability and proline levels. Our results suggest that SaNADP-ME4 overexpression in Arabidopsis increases drought and salt stress resistance.