Discussion
Plant interactions with microbes are a key mechanism that shapes the
relationship between plant diversity and productivity . Our results
further illustrate that plant leaf- and root-associated microbes
including plant-beneficial microbes and pathogens can interact to
determine the strength of plant diversity-productivity relationships.
Leaf microbial inoculation reduced plant productivity potentially due to
leaf pathogen infection, which is stronger in lower-diversity plant
assemblages leading to positive plant diversity-productivity
relationships. However, this leaf microbe-induced positive
diversity-productive relationship was weakened when soil microbes
including arbuscular mycorrhizal fungi were inoculated, suggesting that
the role of aboveground plant pathogens in mediating positive
diversity-productivity relationships can be compromised by
plant-beneficial microbes belowground. The interaction between leaf- and
root-associated microbes and between plant pathogens and beneficial
microbes has complicated our understanding of the influence of microbes
on ecosystem productivity, highlighting the importance of considering
both above- and belowground microbes and their collective effects in
shaping plant diversity-productivity relationships.
Plant pathogens have been proposed as a major determinant of positive
plant diversity-productivity relationships, based on the assumption that
natural enemies decrease plant productivity at high conspecific density
(low diversity) which consequently contributes to a positive plant
diversity-productivity relationship . However, previous studies have
generally focused on soil-borne fungal pathogens (but see Huang et al.
2022). In our study, we collected leaf microbial communities from plants
growing in the field, where we observed obvious symptoms of plant
disease caused by plant pathogens such as rust fungi. Inoculation of
this microbial community onto plant leaves significantly decreased plant
productivity at low plant diversity but barely at high diversity,
resulting in positive diversity-productivity relationships. The result
is consistent with a recent study conducted in a large subtropical
forest biodiversity-ecosystem function experiment, where the application
of fungicide on tree canopies eliminated positive tree species
diversity-productivity relationships . Additionally, we showed that
inoculation of leaf microbes increased the overyielding of plant biomass
(a net biodiversity effect on plant productivity), and this overyielding
results from complementarity among plant species rather than a selection
effect caused by a particular species. Indeed, the pathogenic effect can
be ‘diluted’ by plant diversity because high-diversity plant assemblages
often have low conspecific density. This diluted pathogenic effect
allows plant species to perform better in mixed communities than
monoculture, which induced interspecific complementarity and promote
positive diversity-productivity relationships .
In contrast with plant pathogens, beneficial microbes such as
mycorrhizal fungi have been suggested to promote plant productivity at
high plant diversity and thus contribute to positive
diversity-productivity relationships . This hypothesis was based on the
observation that the diversity of mycorrhizal fungi increased with plant
diversity . However, our experiment showed contrary results. Inoculation
of belowground microbes including mycorrhizal fungi had no effect on
plant diversity-productivity relationships, but when leaf inoculation
was present, these belowground microbes showed beneficial effect on
plant productivity especially at lower plant diversity, thereby
weakening the positive diversity-productivity relationship. This result
suggested that beneficial microbes can mediate diversity-productivity
relationship though their interaction with plant pathogens. This
observation is consistent with the findings of previous studies that
strong plant-mycorrhizal associations were triggered at high pathogen
pressure and promoted plant growth by defense against pathogen infection
. Therefore, our findings implied alternative roles of beneficial
microbes in mediating plant diversity-productivity relationship, that
is, beneficial microbes may counteract pathogenic effect at low plant
diversity, and thus weaken diversity-productivity relationships .
Although our findings demonstrated a significant interplay between
aboveground plant pathogens and belowground beneficial microbes in
shaping plant diversity-productivity relationships, it is important to
acknowledge that our results are based on an experiment in greenhouse
conditions. Whether these microbial effects observed in greenhouse
conditions reflect those within natural ecosystems is not clear.
Previous studies that test plant diversity effects on productivity often
manipulate plant diversity in field conditions, but microbial
transplants in the field can be challenging due to the random dispersal
of microbes through air and rain. Future studies should extend our
experiment to the field and could additionally manipulate microbial
diversity by using fungicide and bactericide in addition to inoculation
with microbes. Additionally, our experiment was limited in the number of
plant species included, due to the need to consider several different
microbial treatments; including more plant species would have greatly
increased the resources required for this experiment, but as a result
the relatively small plant diversity gradient we examined may restrict
the broad applicability of our findings to more diverse ecosystems.
Despite these caveats, our results clearly demonstrated the interaction
between above- and belowground microbes in shaping plant
diversity-productivity relationships, which can serve as a starting
point for investigating how different microbial groups can interact to
drive ecosystem functioning.
Changes in the diversity and composition of microbial communities along
plant diversity gradients is the proposed mechanism for plant-associated
microbes mediating diversity-productivity relationships . Our study
presented evidence that bacterial and fungal community composition in
soils changed with plant diversity, suggesting both soil fungi and
bacteria can play a role in affecting plant diversity-productivity
relationships . Particularly, the diversity and abundance of arbuscular
mycorrhizal fungi and potentially plant growth-promotingStreptomyces bacteria decreased with plant diversity, which may
explain the stronger positive effects of soil inoculation on plant
productivity at lower plant diversity . Additionally, the diversity and
abundance of arbuscular mycorrhizal fungi increased when leaf microbes
were inoculated, supporting the idea that the beneficial effect of soil
microbes can be triggered by potential pathogens on leaves . Identifying
the microbial taxa that drive diversity-productivity relationships and
characterizing how above- and belowground microbial communities change
along gradients of plant diversity will be essential for understanding
the influence of microbiomes on plant diversity-productivity
relationships . However, without microbial isolation and manipulation,
it’s not certain whether these microbial groups caused the observed
inoculation effect in our study. It would be intriguing for future
studies to isolate the major pathogens and beneficial microbes on leaves
and roots and inoculate these specific groups onto plant communities to
test their respective and joint effect on plant productivity.
By inoculating the entire microbial communities collected from plant
rhizosphere soil and leaves in the field onto newly germinated plants in
a greenhouse experiment, we demonstrated an overall negative effect of
plant leaf inoculum on plant productivity, implying a net pathogenic
effect of leaf microbes that promoted positive plant
diversity-productivity relationships. However, when soil microbes were
inoculated, this pathogenic effect of leaf inoculum was reduced, and the
positive plant diversity-productivity relationship was weakened. These
findings provide evidence for the interaction between aboveground
microbes and belowground microbes in shaping plant
diversity-productivity relationships in a greenhouse setting, which
paves the way for studying the role of different plant-associated
microbial groups and their interplay in mediating biodiversity-ecosystem
functioning relationships in the field and in more diverse ecosystems.