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.