Do plant–microbe interactions support the Stress Gradient Hypothesis?

Abstract

The Stress Gradient Hypothesis (SGH), which predicts increasing ratios of facilitative:competitive interactions with increasing stress, has long been a guiding framework for conceptualizing plant-plant interactions. Recently, there has been a growing recognition of the roles of microbes in mitigating or exacerbating environmental stress for their plant hosts. As such, we might predict, based on the SGH, that beneficial microbial effects on plant performance should be positively associated with stress. Specifically, we hypothesized that support for the SGH would depend on the host plant's habitat specialization such that species that specialize in high stress habitats and thus likely coevolved with the resident microbes would exhibit stronger support for the SGH than non-specialist plant species. We further hypothesized that support for the SGH would vary with germination frequency, since boosting germination of low-frequency germinators is one effective means by which microbes can benefit plant species performance. Here, we explore whether plant-microbial interactions support the SGH using 12 plant species native to the Florida rosemary scrub. We conducted factorial experiments that manipulated the presence of microbes in nine soils collected along an elevational stress gradient, and recorded germination frequency and biomass. Microbes increased the germination frequency of four species, all of which had relatively low germination rates. Furthermore, we found support for the SGH in nearly one-half of the species examined, with soil microbes facilitating germination with increasing stress for 5 of the 12 species tested, and none of the species exhibiting the opposite trend. Support for the SGH was not predicted by either the plant hosts' habitat specialization or germination frequency. In contrast to germination, biomass results showed little support for the SGH, with four of 12 species refuting and one species supporting SGH predictions. Taken together, our study documents that interactions between the soil microbial community and plant species along a stress gradient can support the SGH, but emphasizes that these effects are life-history-stage dependent. This work also identifies a common mechanism (germination facilitation) by which microbes can benefit plant species in stressful habitats.

Host evolutionary history and ecological context modulate the adaptive potential of the microbiome

“…Stressful environments are predicted to increase the relative importance of mutualisms [26][27][28], though how often the microbiome behaves evolutionarily like a traditional mutualism remains contentious [4,5,72]. In plants, stress-adapted soil microbiomes improve germination and seedling survival in stressful environments [73,74], highlighting the importance of early life traits like we also observed for development. Second, host genotypes may vary in their ability to leverage beneficial microbes in stressful environments.…”

Response of soil microbial communities to mixed forests of European beech and conifers: Variations with site conditions

“…This ability presumably contributed to the mitigation of the detrimental effects of Douglas-fir on microorganisms at nutrient-poor / acidic sites in mixed forests. More broadly, it may explain the observed overyielding in mixed stands of beech and conifers at nutrient-poor sites, highlighting the potential role of microorganisms in the facilitation of plants under environment stress conditions (Toïgo et al, 2015; Ammer, 2019; David et al, 2020).…”

“…Chen et al, 2019), but to what extent effects of tree species composition on soil microorganisms vary with site conditions, such as nutrient status and water availability, is little known. Facilitation among plants is more pronounced in unfavorable environments according to the stress-gradient hypothesis, and such positive interspecific interactions are likely to be mediated by soil microorganisms (Defossez et al, 2011; Harpole et al, 2016; David et al, 2020). In fact, plants do not passively tolerate environmental stress, but respond in various ways to unfavorable growth conditions, such as by allocating more resources to roots than to shoots under nutrient-poor conditions (Callaway et al, 2003; Kawaletz et al, 2013; Yan et al, 2016).…”

“…Facilitation among plants is more pronounced in nutrient-poor soil according to the stress-gradient hypothesis, and such positive interspecific interactions are likely to be mediated by soil microorganisms (Defossez et al, 2011; David et al, 2020). Plants do not passively tolerate environmental stress, but respond in various ways to unfavorable growth conditions, such as by shifting the allocation of resources towards roots in nutrient-poor soil (Callaway et al, 2003; Yan et al, 2016).…”

Microbial effects on plant phenology and fitness

“…Accumulating evidence from plant-microbe systems suggests that microbial effects on phenological traits may be a key mechanism supporting these hypotheses, particularly for germination. Soil and endophytic microbes may enhance germination in nutrient-deficient soils, as observed in the Florida rosemary scrub ecosystem (David et al, 2020) and under salt stress (Piernik et al, 2017). Beneficial microbes, including pre-treatment of seeds with the best local strains (Balshor et al, 2017) could be useful to improve seed germination, a major bottleneck in large-scale ecosystem restoration plantings (Larson et al, 2015) especially for restoration or phytoremediation projects in stressful environments.…”