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.