Dopamine improves apple replant disease resistance by regulating physiological resilience and rhizosphere microbial community structure

Apple replant disease (ARD) is a complex agricultural problem caused by multiple stressors that can lead to increased reactive oxygen species (ROS) levels and limited nutrient utilization in plants. However, existing countermeasures are insufficient to effectively address this challenge. Here, we used Malus hupehensis as a test organism to investigate the ability of the pleiotropic molecule dopamine to alleviate ARD using pot experiments. Exogenous application of 100 μmol L−1 dopamine significantly promoted the growth of apple in the replanted soil, with the relative growth rate increase of 17.44%. Our results revealed two major pathways through which dopamine regulates ARD resistance in apple plants. First, dopamine effectively reduces the level of ROS and activates the expression of genes related to nitrogen (N) transport and metabolism. Among such genes, MdNPL5, MdNRT1.1, MdNPL2, MdNRT2.5, MdNPL3, MdNRT2.4, MdNADH-GAGOT, MdFd-GAGOT were strongly regulated by dopamine. These regulatory effects promoted the uptake and utilization of soil N by plants. Second, dopamine improved physical and chemical properties, enhanced microbial community diversity, and promoted mutual cooperation between microbial communities in soil. Furthermore, dopamine altered the microbial structure of rhizosphere soil (upregulated: Clostridiales, Gaiellales, Sordariales and Mortierellales; downregulated: Micrococcales, Longimicrobiales, Hypocreales and Cystobasidiales). Notably, dopamine significantly upregulated the abundances of Gaiella and Mortierella, both of which were positively correlated with soil urease activity, soil available N content, plant growth and N uptake. Dopamine also significantly downregulated the abundance of the plant pathogen Gibberella (11.71-fold) in replant soil. Our results provide insights into the mechanisms through which dopamine promotes ARD resistance, and could promote sustainable development of the apple industry.