Integrative study of subcellular distribution, chemical forms, and physiological responses for understanding manganese tolerance in the herb Macleaya cordata (papaveraceae)

Abstract

Macleaya cordata is a perennial herb, a candidate phytoremediation plant with high biomass and manganese (Mn) tolerance. To study the mechanism underlying its Mn adaptability, Mn2+ at various concentrations (0, 1000, 5000, 10000, 15000, and 20000 μM) were applied to M. cordata to investigate the subcellular distribution and chemical forms of Mn, as well as the resulting physiological and biochemical changes by pot culture experiment under natural light in a greenhouse. According to our results, Mn level in M. cordata increased with exogenous Mn concentrations; and Mn contents in different tissues exhibited a leaf > root > stem pattern. Meanwhile, biomass and the level of photosynthetic pigments increased at lower Mn concentrations but declined as Mn concentration further ascended. Subcellular distribution analysis revealed that Mn was sequestered in cell wall and vacuole; in addition, it was incorporated into pectates and protein, phosphates, and oxalates. These findings revealed a possible effective strategy for M. cordata to reduce Mn mobility and toxicity. Moreover, a continuous boost in the level of malondialdehyde was observed with Mn gradient; whereas contents of soluble proteins and proline, and the activities of superoxide dismutase and peroxidase were initially increased and then dropped. Altogether, these results indicated that most Mn was trapped in the cell wall and soluble fractions in low toxicity forms such as pectates and protein, phosphates, and oxalates. These strategies, that is functioning cooperatively with the well-coordinated antioxidant defense systems and the non-enzymatic metabolites, confer strong resistance to Mn in M. cordata.