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

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 2nd , 6th and 15th 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.

Impairment of chloroplast movement reduces growth and delays reproduction of Arabidopsis thaliana in natural and controlled conditions.

PREMISE: The importance of chloroplast movement for plant growth in constant, controlled light and of nonphotochemical quenching (NPQ) in variable, natural light are known. Here we concurrently investigated growth and reproduction of several Arabidopsis thaliana mutants to assess the relative importance of photoprotection via chloroplast movement and NPQ. METHODS: Plants were grown outdoors (natural conditions) or in a growth chamber with variable light and chilling temperatures (controlled conditions). Phenotypic growth and reproductive variables were determined at set times before maturity in wild-type (WT) and phot1, phot2, phot1phot2 (e.g., impaired chloroplast movement, stomatal conductance, leaf flattening), chup1 (impaired chloroplast movement), and npq1 (reduced NPQ) plants. RESULTS: Mutants were most adversely affected in natural conditions, with phot1phot2 and chup1 most severely impacted. These mutants bolted later and produced fewer leaves and siliques, less leaf biomass, and fewer secondary inflorescences than WT. In controlled conditions, leaf traits of these mutants were unaffected, but phot1phot2 bolted later and produced fewer secondary inflorescences and siliques than WT. For most variables, there were significant interactions between growth conditions and plant genotype. Many variables were correlated, but those relationships changed with growth conditions and genotype. CONCLUSIONS: Phenotypic variables at the time of the harvest were strongly affected by growth conditions and genotype. In natural conditions, phot1phot2 and chup1 mutants were most adversely affected, demonstrating the importance of chloroplast movement. In controlled conditions, only phot1phot2 was consistently affected, also emphasizing the important, pleiotropic effects of phototropins. In both conditions, NPQ was less important.

The importance of chloroplast movement, nonphotochemical quenching, and electron transport rates in light acclimation and tolerance to high light in Arabidopsis thaliana.

PREMISE: While essential for photosynthesis, excess light can damage plants. We investigated how growth light conditions affect two photoprotective strategies, chloroplast movement and nonphotochemical quenching (NPQ), as well as electron transport rates (ETR), and the relative importance of these processes in the short-term stress tolerance of Arabidopsis thaliana. METHODS: We grew wild-type (WT) and mutant plants with impaired chloroplast movement (phot1, phot2, phot1 phot2, chup1) or NPQ (npq1) at low (160 µmol photons m-2 s-1 ) or intermediate light (400 µmol photons m-2 s-1 ) before quantifying transmission changes due to chloroplast movement, NPQ, ETR, and the ability to recover from a short-term high-light treatment. RESULTS: Plants with impaired chloroplast avoidance movement (phot2, phot1 phot2, chup1) did not recover as well from a short-term high light treatment as the WT or npq1 and phot1 mutants. Plants grown at intermediate light recovered more completely from the same stress treatment regardless of their genotype and despite reduced degrees of transmission changes due to chloroplast movement. This result was due in part to all genotypes having up to a 2-fold increase in ETRmax and a slight increase in NPQmax . CONCLUSIONS: Growth light conditions affect which mechanisms are important in dealing with short-term high-light stress. The chloroplast avoidance response is important for low-light-grown plants, while increases in ETRmax and NPQmax allow plants grown at intermediate light intensities to avoid being damaged.

Eco-evolutionary processes affecting plant-herbivore interactions during early community succession.

The quality and outcome of organismal interactions are not only a function of genotypic composition of the interacting species, but also the surrounding environment. Both the strength and direction of natural selection on interacting populations vary with the community context, which itself is changed by these interactions. Here, we test for the role of interacting evolutionary and ecological processes in plant-herbivore interactions during early community succession in the tall goldenrod, Solidago altissima. We use surveys in a large-scale field experiment with repeated plots representing 6 years of early oldfield succession and reciprocal transplant common garden experiments to test for the relative importance of rapid evolution (genetic) and environmental changes (soil quality) in affecting mean plant resistance and growth phenotypes during community succession. While plant growth varied strongly with soil quality over the first 5 years of agricultural abandonment, plant secondary metabolism, and herbivore resistance varied minimally with the soil environment. Instead, mean composition and abundance of plant secondary compound bouquets differed between S. altissima plants from populations collected in communities in the first ("early") and sixth ("intermediate") years of oldfield succession, which was reflected in the feeding preference of the specialist herbivore, Trirhabda virgata, for early succession lines. Moreover, this preference was most pronounced on poorer quality, early succession soils. Overall, our data demonstrate that plant quality varies for insect herbivores during the course of early succession and this change is a combination of altered genotypic composition of the population and phenotypic plasticity in different soil environments.

The value of long-term ecological research for evolutionary insights.

Scientists must have an integrative understanding of ecology and evolution across spatial and temporal scales to predict how species will respond to global change. Although comprehensively investigating these processes in nature is challenging, the infrastructure and data from long-term ecological research networks can support cross-disciplinary investigations. We propose using these networks to advance our understanding of fundamental evolutionary processes and responses to global change. For ecologists, we outline how long-term ecological experiments can be expanded for evolutionary inquiry, and for evolutionary biologists, we illustrate how observed long-term ecological patterns may motivate new evolutionary questions. We advocate for collaborative, multi-site investigations and discuss barriers to conducting evolutionary work at network sites. Ultimately, these networks offer valuable information and opportunities to improve predictions of species' responses to global change.

Functional shifts in soil fungal communities regulate differential tree species establishment during subalpine forest succession.

Soil fungi can differentially affect plant performance and community dynamics. While fungi play key roles in driving the plant-soil feedbacks (PSFs) that promote grassland succession, it remains unclear how the fungi-mediated PSFs affect tree species establishment during forest succession. We inoculated pioneer broadleaf (Betula platyphylla and Betula albosinensis) and nonpioneer coniferous tree seedlings (Picea asperata and Abies faxoniana) with fungal-dominated rooting zone soils collected from dominant plant species of early-, mid- and late-successional stages in a subalpine forest, and compared their biomass and fungal communities. All tree species accumulated abundant pathogenic fungi in early-successional inoculated soil, which generated negative biotic feedbacks and lowered seedling biomass. High levels of soil ectomycorrhizal fungi from mid- and late-successional stages resulted in positive biotic PSFs and strongly facilitated slow-growing coniferous seedling performance to favour successional development. B. albosinensis also grew better in mid- and late-successional soils with fewer pathogenic fungi than in early-successional soil, indicating its large susceptibility to pathogen attack. In contrast, the growth of another pioneer tree, B. platyphylla, was significantly suppressed in late-successional soil and was mostly driven by saprotrophic fungi, despite the unchanged pathogenic fungal community traits between the two fast-growing species. This unexpected result suggested a host specificity-dependent mechanism involved in the different impacts of fungal pathogens on host trees. Our findings reveal a critical role of functional shifts in soil fungal communities in mediating differential PSFs of tree species across successional stages, which should be considered to improve the prediction and management of community development following forest disturbances.

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

Communities of microorganisms in the soil can affect plants' growth and interactions with aboveground herbivores. Thus, there is growing interest in utilizing soil microbiomes to improve plant performance in agriculture (e.g., for pest control), but little is known about the phenotypic responses of various crop species to different microbiomes. In this study, we inoculated four crop species from different botanical families, maize (Zea mays, Poaceae), cucumber (Cucumis sativus, Cucurbitaceae), tomato (Solanum lycopersicum, Solanaceae), and lettuce (Lactuca sativa, Asteraceae), with diverse soil microbiomes originating from actively-managed agricultural fields or fallow fields under varying stages of succession (1, 3, and 16-years post-agriculture) sourced from a large-scale field experiment. We compared the crops' responses to these different microbiomes by assessing their growth and resistance to two generalist insect pests, cabbage looper (Trichoplusia ni) and fall armyworm (Spodoptera frugiperda). These different microbiomes affected both plant growth and resistance, but the effects were species-specific. For instance, lettuce produced the largest leaves when inoculated with a 3-year fallow microbiome, the microbiome in which cucumber performed worst. Plants were generally more resistant to T. ni when inoculated with the later succession microbiomes, particularly in contrast to those treated with agricultural microbiomes. However, for tomato plants, the opposite pattern was observed with regard to S. frugiperda resistance. Collectively, these results indicate that plant responses to microbiomes are species-specific and emphasize the need to characterize the responses of taxonomically diverse plant species to different microbiomes.

Soil microbiome transfer method affects microbiome composition, including dominant microorganisms, in a novel environment.

We show that choice of soil microbiome transfer method, i.e. direct soil transfers and a common soil wash procedure, dramatically influences the microbiome that develops in a new environment, using high-throughput amplicon sequencing of 16S rRNA genes and the fungal internal transcribed spacer (ITS) region. After 3 weeks of incubation in commercial potting mix, microbiomes were most similar to the source soil when a greater volume of initial soil was transferred (5% v/v transfer), and least similar when using a soil wash. Abundant operational taxonomic units were substantially affected by transfer method, suggesting that compounds transferred from the source soil, shifts in biotic interactions, or both, play an important role in their success.