Soil microorganisms buffer the reduction in plant growth and physiological performance under combined abiotic stress in the halophyte Salicornia ramosissima

The impact of multifactorial abiotic stress combinations on plant functional responses remains controversial, and general patterns of response are yet to emerge. This knowledge gap is particularly relevant for species with innate tolerance to environmental stress. Using the halophyte Salicornia ramosissima as a model species, we performed a multifactorial study with 16 experimental scenarios that included or not beneficial microorganisms in order to quantify their impact on plant growth, photosynthetic performance, osmotic adjustment and ion homeostasis. The experimental scenarios were characterized by the combination of four factors with two levels (salinity: 171 and 510 mM NaCl; water stress: yes and no; temperature min/max range: 14/25 and 18/29ºC and atmospheric CO2 concentration: 400 and 700 ppm). A plant growth-promoting rhizobacteria (PGPR) consortium was used as a proxy for positive biological interaction. The results revealed that the multifactorial stress combinations triggered unique functional responses, depending on the stress factors involved. However, there was an overall more negative impact on plant functional traits under the most extreme scenario (i.e., 510 mM NaCl + water stress + high temperature). Interestingly, the presence of PGPR was able to reverse this negative influence, although this effect was negligible under non-stressful conditions. Furthermore, the positive effect of PGPR was even magnified when coexisting with elevated atmospheric CO2 concentration. This response is associated with mitigation of the negative impacts of suboptimal factor combinations on plant growth, photosynthetic performance/efficiency, and water/nutrient homeostasis. Therefore, we conclude that the positive impact of microorganisms on halophyte tolerance in complex environmental matrices would only be determinant under extreme conditions in which plant intrinsic tolerance mechanisms would not be sufficient. Remarkably, this effect could be accentuated by increasing atmospheric CO2 concentration.