Mangrove plants growing in the high salt environment of coastal intertidal zones colonize a variety of microorganisms in the phyllosphere, which have potential salt-tolerant and growth-promoting effects. However, the characteristics of microbial communities in the phyllosphere of mangrove species with and without salt glands and the differences between them remain unknown, and the exploration and the agricultural utilization of functional microbial resources from the leaves of mangrove plants are insufficient. In this study, we examined six typical mangrove species to unravel the differences in the diversity and structure of phyllosphere microbial communities between mangrove species with or without salt glands. Our results showed that a combination of salt-tolerant growth-promoting strains of Pantoea stewartii A and Bacillus marisflavi Y25 (A + Y25) was constructed from the phyllosphere of mangrove plants, which demonstrated an ability to modulate osmotic substances in rice and regulate the expression of salt-resistance-associated genes. Further metagenomic analysis revealed that exogenous inoculation with A + Y25 increased the rice rhizosphere’s specific microbial taxon Chloroflexi, thereby elevating microbial community quorum sensing and ultimately enhancing ionic balance and overall microbial community function to aid salt resistance in rice. This study advances our understanding of the mutualistic and symbiotic relationships between mangrove species and their phyllosphere microbial communities. It offers a paradigm for exploring agricultural beneficial microbial resources from mangrove leaves and providing the potential for applying the salt-tolerant bacterial consortium to enhance crop adaptability in saline–alkaline land. The sources of the photos used in this figure are provided below: Avicennia marina: https://guru.sanook.com/6011/ Acanthus ilicifolius: https://tracuuduoclieu.vn/acanthus-ilicifolius-l.html Aegiceras corniculatum: https://apps.lucidcentral.org/plants_se_nsw/text/entities/aegiceras_corniculatum.html Sonneratia apetala: http://www.fpcn.net/a/shuishengzhiwu/20131109/Sonneratia_apetala.html Excoecaria agallocha: https://efloraofindia.com/2011/03/01/excoecaria-agallocha/ Kandelia candel: https://www.szhb.org/6539.html Background photo: https://www.discovery.com/nature/the-world-is-waking-up-to-the-importance-of-mangroves

Avicennia marina is a pioneer salt-tolerant plant in coastal intertidal mangroves, an efficient blue carbon ecosystem. It is of great importance to explore how salinity affects the phyllosphere and rhizosphere microbial communities of A. marina. This study showed that the microbial communities in the phyllosphere and rhizosphere of A. marina had different constitutive properties, adaptive network interactions, and potential stress-promoting functions.