Effects of long‐term mowing on leaf‐ and root‐associated bacterial community structures are linked to functional traits in 11 plant species from a temperate steppe

Abstract

Long‐term mowing can cause morphological stuntedness of plants, thus reducing grassland productivity and exacerbating grassland degradation. Although plant microbiomes can enhance plant resistance against disturbance, considerable uncertainty exists regarding how mowing and mowing‐induced plant trait plasticity affect plant microbiomes in natural grasslands. Here we examined the responses of leaf/root‐associated bacterial (LAB/RAB) communities of 11 dominant herbaceous perennials (six replicates per species) to a 17‐year mowing treatment in a temperate grassland. We also measured leaf/root physiological and morphological traits, and analysed the relationships among mowing practice, bacterial community structures and leaf/root trait parameters. We found that both leaf and root functional traits showed interspecific variations (variations across different plant species), while only the leaf traits exhibited intraspecific variation (treatment‐induced variations within plant species) between the treatments. Similarly, the LAB community structure was more sensitive to mowing but less influenced by host species identity, compared to the RAB community. The RAB community structure was primarily shaped by host species identity, while mowing was a secondary influencing factor. The different patterns of LAB and RAB communities in response to mowing could be specifically explained by the inter/intraspecific variations of the related leaf and root traits. The LAB community was strongly correlated with the leaf traits which exhibited mowing‐induced plasticity (intraspecific variation), with the correlations with nitrogen resorption efficiency and above‐ground dry weight being the greatest. The root traits were important indicators of bacterial community structure in the root compartment across the hosts, rather than between the treatments. Root tissue density showed the strongest interspecific variation, and was identified as an overwhelming driver of the RAB community. The shifts in LAB/RAB communities under mowing were largely attributed to the increased proportions of Actinobacteria. The high mowing sensitivity of the LAB community was associated with the enrichment of soil‐derived Actinobacteria in leaves under mowing. Actinobacteria were also the main keystone taxa in the bacterial community networks under mowing. Our results demonstrate that the magnitude of plant‐associated microbial community response to long‐term mowing is plant compartment and trait variation dependent, and advance our understanding of the leaf/root microbiome‐trait relationships in complex plant communities. Read the free Plain Language Summary for this article on the Journal blog.

Tolerance to land-use changes through natural modulations of the plant microbiome

“…Relocation as a strategy to avoid environmental changes might often fail because of time constraints, continued habitat shrinking, or a lacking spatial connectivity within a species’ range of dispersal (Asamoah et al, 2021; Corlett & Westcott, 2013; Gómez-Ruiz & Lacher Jr, 2019; Renton et al, 2013); likewise, the process of evolutionary adaptation to rapid alterations also takes several generations and might be too slow in most cases (Etterson & Shaw, 2001). Our data experimentally support recent findings that land-use not only affects plants and plant communities, but also the diversity and composition of plant-associated bacterial and fungal communities (Bai et al, 2023; Estendorfer et al, 2017; Gaube et al, 2021). Our data additionally demonstrate the pace and small scale of such alterations: Within three months of exposure to different land-use treatments in the small area of the common garden, surrounded by the same environment, microbial communities clearly diverged to treatment-specific compositions.…”

“…Natural modulations of plant-associated microbial communities in response to environmental stresses can represent an alternative – and faster – way for plants to cope with alterations in land-use and other components of global change (Afkhami, 2023; Allsup et al, 2023; Lau & Lennon, 2012; Trivedi et al, 2022). In fact, ecological and evolutionary microbiome responses can easily keep pace with environmental changes (Martiny et al, 2023) and land-use history, intensity, and agricultural practices have been shown to affect the diversity and composition of bacterial and fungal communities in the soil or associated with plants (Abrahao et al, 2022; Bai et al, 2023; Estendorfer et al, 2017; Gaube et al, 2021; Li et al, 2019). These rapid responses of plant-associated microbiomes may then, in turn, have positive effects on plant phenotype and performance, increasing plant species’ tolerance to changes (Friesen et al, 2011; Jiang et al, 2023).…”