Malate-mediated CqMADS68 enhances aluminum tolerance in quinoa seedlings through interaction with CqSTOP6, CqALMT6 and CqWRKY88

Abstract

Aluminum (Al) stress in acidic soils has severe negative effects on crop productivity. In this study, the alleviating effect and related mechanism of malate on Al stress in quinoa (Chenopodium quinoa) seedlings were investigated. The findings indicated that malate alleviated the growth inhibition of quinoa seedlings under Al stress, maintained the enzymatic and nonenzymatic antioxidant systems, and aided resistance to the damage caused by excessive reactive oxygen species (ROS). Under Al stress, malate significantly increased the contents of chlorophyll and carotenoids in quinoa shoots by 103.8% and 240.7%, and significantly increased the ratios of glutathione (GSH)/oxidized glutathione (GSSG), and ascorbate (AsA)/dehydroascorbate (DHA) in roots by 59.9% and 699.2%, respectively. However, malate significantly decreased the superoxide radical (O2•-), hydrogen peroxide (H2O2), malondialdehyde (MDA) and Al contents in quinoa roots under Al stress by 32.7%, 60.9%, 63.1% and 49%, respectively. Moreover, the CqMADS family and the Al stress-responsive gene families (CqSTOP, CqALMT, and CqWRKY) were identified from the quinoa genome. Comprehensive expression profiling identified CqMADS68 as being involved in malate-mediated Al resistance. Transient overexpression of CqMADS68 increased Al tolerance in quinoa seedlings. More importantly, we found that CqMADS68 regulated the expression of CqSTOP6, CqALMT6 and CqWRKY88 and further demonstrated the interaction of CqMADS68 with CqSTOP6, CqALMT6 and CqWRKY88 by bimolecular fluorescence complementation (BIFC) experiments. Moreover, transient overexpression and physiological and biochemical analyses demonstrated that CqSTOP6, CqALMT6 and CqWRKY88 could also improve Al tolerance by maintaining the antioxidant capacity of quinoa seedlings. Taken together, these findings reveal that CqMADS68, CqSTOP6, CqALMT6 and CqWRKY88 may be important contributors to the Al tolerance regulatory network in quinoa, providing new insights into Al stress resistance.