Shifts in plant–microbe interactions over community succession and their effects on plant resistance to herbivores

Abstract

Soil microorganisms can influence the development of complex plant phenotypes, including resistance to herbivores. This microbiome-mediated plasticity may be particularly important for plant species that persist in environments with drastically changing herbivore pressure, for example over community succession.We established a 15-yr gradient of old-field succession to examine the herbivore resistance and rhizosphere microbial communities of Solidago altissima plants in a large-scale field experiment. To assess the functional effects of these successional microbial shifts, we inoculated S. altissima plants with microbiomes from the 2 nd , 6 th and 15 th successional years in a glasshouse and compared their herbivore resistance.The resistance of S. altissima plants to herbivores changed over succession, with concomitant shifts in the rhizosphere microbiome. Late succession microbiomes conferred the strongest herbivore resistance to S. altissima plants in a glasshouse experiment, paralleling the low levels of herbivory observed in the oldest communities in the field. While many factors change over succession and may contribute to the shifts in rhizosphere communities and herbivore resistance we observed, our results indicated that soil microbial shifts alone can alter plants' interactions with herbivores. Our findings suggest that changes in soil microbial communities over succession can play an important role in enhancing plant resistance to herbivores.

Population‐wide shifts in herbivore resistance strategies over succession

“…In addition to the plant community, the associated soil microbial community that shifts in a successional community (Hannula et al 2017) can mediate differences in resistance. In a soil microbial transplant experiment, Howard et al (2020) demonstrated that in a common garden, genotypes planted in soil inoculated with the late‐succession soil microbial community were less attractive to T. virgata adults. The combination of soil microbial effects and changes in population genetic composition may synergistically render the plant population unattractive to the insect herbivores.…”

“…Solidago altissima becomes abundant by Year 3 and remains equally abundant in the older populations (Howard et al 2018). The soil conditions change with succession but all plots follow a common trajectory of increasing soil quality over time (Howard et al 2020).…”

Soil Microbiomes From Fallow Fields Have Species-Specific Effects on Crop Growth and Pest Resistance

“…We previously found that the rhizosphere microbial communities of a native plant, tall goldenrod, Solidago altissima (Asteraceae), shift over oldfield succession in fallow maize fields, with functional effects on their resistance to herbivores. When we inoculated S. altissima with soil microbiomes from a plant community that had been left fallow for 15 years, these plants were more resistant to the specialist goldenrod leaf beetle, Trirhabda virgata , than their counterparts inoculated with early succession microbiomes, paralleling the pattern of greater herbivore resistance observed among goldenrods in late succession communities ( Howard et al., 2020 ). However, it is not known whether this microbiome-mediated resistance associated with the later oldfield succession soils is specific to the community-dominating goldenrods or could more broadly enhance the insect resistance of other plant species as well.…”

“…For example, the abundance of pathogenic fungi has been found to decrease over successional time in abandoned agricultural fields ( Hannula et al., 2017 ), suggesting that these shifts are functional and may benefit plants over succession. Our recent work also suggests that these successional shifts in microbial communities may improve plants’ resistance to herbivores ( Howard et al., 2020 ).…”

“…Leaving fields fallow and promoting the establishment of biota unimpeded by tillage and other disruptive management practices not only results in drastic changes in plant communities, but also in soil quality and soil microbiomes. Levels of soil organic matter, nutrients, and microbial biomass increase in cultivated fields that are left fallow for extended lengths of time ( Post and Kwon, 2000 ; Howard et al., 2020 ) and these successional changes in soils may affect plant growth and resistance to herbivores ( Howard et al., 2018 ). The composition of soil microbiomes is also widely known to shift over ecological succession ( Maharning et al., 2009 ), which is likely to affect the performance of the plants with which they interact.…”