Manganese (Mn) is an essential element for plant growth due to its participation in a series of physiological and metabolic processes. Mn is also considered a heavy metal that causes phytotoxicity when present in excess, disrupting photosynthesis and enzyme activity in plants. Thus, Mn toxicity is a major constraint limiting plant growth and production, especially in acid soils. To cope with Mn toxicity, plants have evolved a wide range of adaptive strategies to improve their growth under this stress. Mn tolerance mechanisms include activation of the antioxidant system, regulation of Mn uptake and homeostasis, and compartmentalization of Mn into subcellular compartments (e.g., vacuoles, endoplasmic reticulum, Golgi apparatus, and cell walls). In this regard, numerous genes are involved in specific pathways controlling Mn detoxification. Here, we summarize the recent advances in the mechanisms of Mn toxicity tolerance in plants and highlight the roles of genes responsible for Mn uptake, translocation, and distribution, contributing to Mn detoxification. We hope this review will provide a comprehensive understanding of the adaptive strategies of plants to Mn toxicity through gene regulation, which will aid in breeding crop varieties with Mn tolerance via genetic improvement approaches, enhancing the yield and quality of crops.

Manganese (Mn) toxicity is a major constraint limiting plant growth on acidic soils. Superior Mn tolerance in Stylosanthes spp. has been well documented, but its molecular mechanisms remain largely unknown. In this study, superior Mn tolerance in Stylosanthes guianensis was confirmed, as reflected by a high Mn toxicity threshold. Furthermore, genetic variation of Mn tolerance was evaluated using two S. guianensis genotypes, which revealed that the Fine-stem genotype had higher Mn tolerance than the TPRC2001-1 genotype, as exhibited through less reduction in dry weight under excess Mn, and accompanied by lower internal Mn concentrations. Interestingly, Mn-stimulated increases in malate concentrations and exudation rates were observed only in the Fine-stem genotype. Proteomic analysis of Fine-stem roots revealed that S. guianensis Malate Dehydrogenase1 (SgMDH1) accumulated in response to Mn toxicity. Western-blot and quantitative PCR analyses showed that Mn toxicity resulted in increased SgMDH1 accumulation only in Fine-stem roots, but not in TPRC2001-1. The function of SgMDH1-mediated malate synthesis was verified through in vitro biochemical analysis of SgMDH1 activities against oxaloacetate, as well as in vivo increased malate concentrations in yeast (Saccharomyces cerevisiae), soybean (Glycine max) hairy roots, and Arabidopsis (Arabidopsis thaliana) with SgMDH1 overexpression. Furthermore, SgMDH1 overexpression conferred Mn tolerance in Arabidopsis, which was accompanied by increased malate exudation and reduced plant Mn concentrations, suggesting that secreted malate could alleviate Mn toxicity in plants. Taken together, we conclude that the superior Mn tolerance of S. guianensis is achieved by coordination of internal and external Mn detoxification through malate synthesis and exudation, which is regulated by SgMDH1 at both transcription and protein levels.

A cell wall-localized GmPAP1-like protein is up-regulated by Pi starvation, and is involved in extracellular dNTP utilization in soybean.

As a major component of soil organic phosphorus (P), phytate-P is unavailable to plants unless hydrolysed by phytase to release inorganic phosphate. However, knowledge on natural variation in root-associated phytase activity and its underlying molecular mechanisms in plants remains fragmentary. In this study, variations in root internal and associated phytase activity were observed among 39 genotypes of Stylosanthes guianensis (Stylo), which is well adapted to acid soils. Furthermore, TPRC2001-1, the genotype with the highest root-associated phytase activity, was more capable of utilizing extracellular phytate-P than Fine-stem, the genotype with the lowest root-associated phytase activity. After protein liquid chromatography-tandem mass spectrometry analysis, a purple acid phosphatase (PAP), SgPAP23, was identified and cloned from TPRC2001-1. SgPAP23 exhibited high activity against phytate-P and was mainly localized on the plasma membrane. Furthermore, SgPAP23 overexpression resulted in significant increases of root-associated phytase activity and thus facilitated extracellular phytate-P utilization in both bean (Phaseolus vulgaris) hairy roots and Arabidopsis thaliana. The results herein support the conclusion that SgPAP23 is a primary contributor to the superior extracellular phytate-P utilization in stylo and thus is used to develop cultivars with efficient extracellular phytate-P utilization.