Introduction
Understanding the mechanisms that drive relationships between biodiversity and ecosystem function has been a major concern for ecologists and has attracted increasing attention given climate change and the loss of biodiversity . Studies to date have generally agreed that higher plant diversity contributes to increased ecosystem productivity through complementarity and selection processes , and that plant-associated microbes including plant pathogens and mycorrhizal fungi play a key role in mediating these processes . However, previous studies of the role of microbes in plant diversity-productivity relationships have generally focused on a single microbial guild of either aboveground or belowground plant microbiomes ; as a result, the interactions between microbial guilds above- and belowground and their collective effects on plant diversity-productivity relationships remain unknown. Theoretical studies have suggested that high complexity in trophic interactions could lead to varying relationships between biodiversity and ecosystem function, pointing out the necessity of considering complex plant associations with multiple microbial guilds both above- and belowground to understand the role of plant-associated microbes in determining the strength and direction of plant diversity-productivity relationships .
There is abundant empirical evidence that plant-associated microbes contribute to positive plant diversity-productivity relationships and several microbial functional groups have been implicated including plant pathogens such as foliar and soil-borne fungal pathogens, and plant-beneficial microbes including plant-growth promoting bacteria associated with leaves and roots as well as mycorrhizal fungi . The role of these microbial groups in shaping plant diversity-productivity relationships rests on a fundamental assumption that microbial impacts on plant productivity vary along gradients of plant diversity. For example, pathogens tend to reduce plant productivity at high plant conspecific density , and conspecific density is often negatively correlated with plant diversity, leading to the expectation that pathogenic effects should be weaker at higher plant diversity and thus that plant species should perform better in high-diversity communities compared to monocultures. The importance of pathogens for plant diversity and productivity has been well supported by the evidence that positive plant diversity-productivity relationships are weakened when plant pathogens are excluded and strengthened when pathogens are introduced in controlled experiments . Additionally, the diversity of plant-beneficial microbes has been observed to increase with plant diversity, which may increase the resource partitioning among plant species and promote positive diversity-productivity relationships through niche complementarity mechanisms . However, the role of plant-beneficial microbes such as arbuscular mycorrhizal fungi in shaping positive diversity-productivity relationships has not been widely supported by experimental evidence, presumably because mycorrhizal fungi are more host generalized than pathogens and their diversity and abundance do not covary with plant diversity significantly enough in experimental settings to lead to positive diversity-productivity relationships .
Plant-associated microbes can interact to determine the overall fitness of host plants, so that the impact of one microbial guild on plant diversity-productivity relationships may depend on the presence or absence of others . For instance, mycorrhizal associations improved host plant resistance during pathogen infection, leading to a more positive effect of mycorrhizal fungi on plant productivity when plant pathogens were present . Likewise, plant pathogens may cause greater reductions in productivity when host plants lack mycorrhizal associations or have a low diversity of associated beneficial bacteria . Additionally, the interplay between microbial guilds can alter the way microbial effects change with plant diversity. For example, the high pathogen pressure at high host density (and hence low diversity) may trigger strong plant association with mycorrhizal fungi, which counteract the higher pathogenic effect at lower plant diversities . Previous studies that involved introduction or removal of whole microbial communities from leaves or roots have observed positive or negative effects on plant productivity, which were interpreted as either plant pathogens or beneficial microbes . However, it remains largely unexplored whether plant pathogens and beneficial microbes can interact to mediate plant productivity and diversity-productivity relationships (Jonsson et al. 2001; Ruijven et al. 2020).
Plant leaves and roots represent two major habitats for plant-associated microbes. Both above- and belowground plant parts harbor important plant pathogenic and beneficial microbes, while differing greatly in nutrient availability and other abiotic conditions . Many plant-associated microbes are found in association with both leaves and roots; for example almost half of the bacterial taxa in the phyllosphere ofArabidopsis thaliana were also found in the A. thalianarhizosphere and soil . Additionally, the microbes in one habitat could influence the other by altering plant traits; for example, mycorrhizal associations belowground could improve plant nutrient uptake and modify plant traits such leaf chemistry which then influence the leaf microbial community . Both aboveground and belowground plant microbiomes can influence plant performance and thus may jointly mediate plant diversity-productivity relationships. However, studies to date generally have focused on either leaf- or root-associated microbes, and the interplay between plant leaf- and root-associated microbes and their collective effect on plant productivity are unclear.
To test if above- and belowground plant-associated microbes can interact to determine plant diversity-productivity relationships, we conducted a greenhouse experiment where we inoculated microbial communities collected from plant leaves and roots in the field onto plant communities of different species richness in the greenhouse. We predicted that the effect of above- and belowground microbial inoculation on plant productivity can change with plant diversity to influence plant diversity-productivity relationships. We also predicted that the effect of aboveground microbes on plant diversity-productivity relationships can be influenced by belowground microbes, resulting in a three-way interaction of plant diversity, above- and belowground microbes in determining plant productivity.