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Inoculation of crop plants with beneficial root-associated microorganisms may be a useful strategy for sustainable intensification of agriculture. In recent years, interest has grown in using rhizo...

Reduced insect pest populations found on long-term organic farms have mostly been attributed to increased biodiversity and abundance of beneficial predators, as well as to changes in plant nutrient content. However, the role of plant resistance has largely been ignored. Here, we determine whether host plant resistance mediates decreased pest populations in organic systems and identify potential underpinning mechanisms. We demonstrate that fewer numbers of leafhoppers (Circulifer tenellus) settle on tomatoes (Solanum lycopersicum) grown using organic management as compared to conventional. We present multiple lines of evidence, including rhizosphere soil microbiome sequencing, chemical analysis and transgenic approaches, to demonstrate that changes in leafhopper settling between organically and conventionally grown tomatoes are dependent on salicylic acid accumulation in plants and mediated by rhizosphere microbial communities. These results suggest that organically managed soils and microbial communities may play an unappreciated role in reducing plant attractiveness to pests by increasing plant resistance.

Perennial agroecosystems often seek to optimize productivity by breeding nutrient-efficient, disease-resistant rootstocks. In cacao (Theobroma cacao L.), however, rootstock selection has traditionally relied on locally available open pollinated populations with limited data on performance. Furthermore, rootstock associations with the rhizobiome, or rhizosphere microbiome, have been neglected. Better understanding of rootstock and scion effects on cacao-specific traits, particularly those involved in root-microbe interactions and nutrient acquisition, could contribute to more efficient rootstock selection and breeding. A rootstock-scion interaction study was conducted using three scion genotypes and eight rootstock populations under greenhouse conditions to better understand the relationships among rootstock and scion identities, soil fertility, and rhizobiome composition and the impacts of these factors on plant uptake of macro- and micronutrients. We show that rootstock genotype has a stronger influence than scion on nutrient uptake, bacterial and fungal diversity, and rhizobiome composition, and that the relative contributions of rootstock and scion genotype to foliar nutrient status are dynamic over time. Correlation analysis and stepwise regression revealed complex relationships of soil physicochemical parameters and the rhizobiome to plant nutrition and emphasized strong impacts of microbial diversity and composition on specific nutrients. Linear discriminant analysis effect size estimation identified rootstock-responsive taxa potentially related to plant nutrition. This study highlights the importance of considering root-associated microbial communities as a factor in cacao rootstock breeding and the need for further investigation into mechanisms underlying nutrient acquisition and microbial interactions in grafted plants.

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Plant–microbe interactions in the rhizosphere influence rates of organic matter mineralization and nutrient cycling that are critical to sustainable agricultural productivity. Agricultural intensification, particularly the introduction of synthetic fertilizer in the USA, altered the abundance and dominant forms of nitrogen (N), a critical plant nutrient, potentially imposing selection pressure on plant traits and plant–microbe interactions regulating N cycling and acquisition. We hypothesized that maize adaptation to synthetic N fertilization altered root functional traits and rhizosphere microbial nutrient cycling, reducing maize ability to acquire N from organic sources. Six maize genotypes released pre-fertilizer (1936, 1939, 1942) or post-fertilizer (1984, 1994, 2015) were grown in rhizoboxes containing patches of 15N-labelled clover/vetch residue. Multivariate approaches did not identify architectural traits that strongly and consistently predicted rhizosphere processes, though metrics of root morphological plasticity were linked to carbon- and N-cycling enzyme activities. Root traits, potential activities of extracellular enzymes (BG, LAP, NAG, urease), abundances of N-cycling genes (amoA, narG, nirK, nirS, nosZ) and uptake of organic N did not differ between eras of release despite substantial variation among genotypes and replicates. Thus, agricultural intensification does not appear to have impaired N cycling and acquisition from organic sources by modern maize and its rhizobiome. Improved mechanistic understanding of rhizosphere processes and their response to selective pressures will contribute greatly to rhizosphere engineering for sustainable agriculture., Synthetic nitrogen (N) fertilizers have fundamentally changed the availability of this critically important plant nutrient in agricultural systems, replacing organic sources such as compost and cover crops. Decades of plant breeding have created maize varieties that are highly productive under synthetic nitrogen fertilization, but potential trade-offs for uptake of organic nitrogen were unclear. Using a small panel of maize genotypes, we find minimal impacts of modern breeding on maize root traits, interactions between roots and associated microorganisms that regulate organic matter breakdown and transformations, and uptake of organic nitrogen from cover crops.

Subsurface drip (SSD) irrigation is becoming increasingly prevalent in drought-prone irrigated agroecosystems thanks to greater yields and irrigation water productivity (IWP) and decreased weed pressure. However, potential tradeoffs for soil health and biogeochemical cycles remain unclear, especially in organic systems that rely on soil ecosystem services and biological processes for productivity. Gains in IWP and weed control were evaluated with respect to shifts in soil biological and physicochemical parameters in an organic processing tomato (Solanum lycopersicum L.) agroecosystem. Yield, IWP, and spatial distribution of soil resources and microbial processes were measured in furrow and SSD irrigated organic processing tomato on long term organic fields. Higher IWP and lower weed density under SSD confirm known benefits, while altered distributions of inorganic N, salinity, microbial activity, and C/N cycling enzyme activities as a function of shifts in soil moisture highlight the far-reaching impacts of irrigation management on soil organic C (SOC) and N dynamics regulating resource availability. Decreased macroaggregate formation and greater unprotected C under SSD indicate that altered soil wetting patterns may reduce the C sequestration potential of irrigated land. Previously unknown tradeoffs should be integrated to develop irrigation strategies that maintain current and future sustainability and productivity of organic tomato agroecosystems.

Leguminous crops, like soybeans, often rely on biologically fixed nitrogen via their symbiosis with rhizobia rather than synthetic nitrogen inputs. However, agricultural management practices may influence the effectiveness of biological nitrogen fixation. While the ecological effects of agricultural management on rhizobia have received some attention, the evolutionary effects have been neglected in comparison. Resource mutualism theory predicts that evolutionary effects are likely, however. Both fertilization and tillage are predicted to cause the evolution of rhizobia that provide fewer growth benefits to plant hosts and fix less nitrogen. This study capitalized on an LTER (Long Term Ecological Research) experiment that manipulated agricultural management practices in a corn-soybean-wheat row crop system for 24 years to investigate whether four different management practices (conventional, no-till, low chemical input, and certified organic) cause rhizobia populations to evolve to become more or less cooperative. We found little evidence that 24 years of varying management practices affect the net growth benefits rhizobia provide to soybeans, although soybean plants inoculated with soils collected from conventional treatments tended to have lower biological nitrogen fixation rates than plants inoculated with soils from the no-till, low input, and organic management treatments. These findings suggest that rhizobia will continue to provide adequate growth benefits to leguminous crops in the future, even in intensively managed systems. This article is protected by copyright. All rights reserved.

Weed competition can severely reduce soybean (Glycine max (L.) Merr.) yields, particularly in organic systems. An efficient screening and breeding approach is needed to increase breeding progress for weed tolerance. This study sought to (i) establish a system for direct selection of competitive genotypes, (ii) evaluate genotypic differences in weed tolerance among six early-maturing genotypes and (iii) assess the contribution of selected morphological traits to weed tolerance. A direct selection system providing two different levels of weed competition through all development stages of a soybean crop was developed, using mixtures of selected crop species as sown competitors. Two resulting mixtures induced intermediate ( 50%) yield reduction, respectively. This selection system can be applied in screening and breeding programmes to facilitate breeding for weed tolerance. No significant difference in weed tolerance was detected between six soybean genotypes of maturity groups 000 to 00. Morphological traits that might influence competitive ability, for example light absorption, leaf area and lateral shoots, were assessed, and their potential for indirect selection for weed tolerance is discussed.

Maize domestication and breeding have resulted in drastic and well documented changes in aboveground traits, but belowground effects on root system functioning and rhizosphere microbial communities remain poorly understood, despite their critical importance for nutrient and water acquisition. We investigated the rhizosphere microbial community composition and structure of ten Zea mays accessions along an evolutionary transect (two teosinte, three inbred maize lines, and five modern maize hybrids) grown in nutrient depleted soil from a low input agricultural system. Microbial community analysis revealed significant differences in community composition between soil compartments (proximal vs. distal rhizosphere) and between plant genetic groups (teosinte, inbred, and modern hybrid). Only a small portion of the microbial community was differentially selected across plant genetic groups: 3.7% of prokaryotic community members and 4.9% of fungal community members were significantly associated with a specific plant genetic group. Indicator species analysis showed the greatest differentiation between modern hybrids and the other two plant genetic groups. Co-occurrence network analysis revealed that microbial co-occurrence patterns of the inbred maize lines’ rhizosphere were significantly more similar to those of the teosintes than to the modern hybrids. Our results suggest that advances in hybrid development significantly impacted rhizosphere microbial communities and network assembly.

Lower insect pest populations found on long-term organic farms have largely been attributed to increased biodiversity and abundance of beneficial predators. However, potential induction of plant defenses has largely been ignored. This study aims to determine whether host plant resistance mediates decreased pest populations in organic systems, and to identify the underpinning mechanisms. We demonstrate that greater numbers of leafhoppers (Circulifer tenellus) settle on tomatoes (Solanum lycopersicum) grown using conventional management as compared to organic. Soil microbiome sequencing, chemical analysis, and transgenic approaches, coupled with multi-model inference, suggest that changes in leafhopper settling between organically and conventionally-grown tomatoes are dependent on salicylic acid accumulation in the plant, likely mediated by rhizosphere microbial communities. These results suggest that organically-managed soils and microbial communities may play an unappreciated role in reducing plant attractiveness to pests by increasing plant resistance.

Root exploitation of soil heterogeneity and microbially mediated rhizosphere nutrient transformations play critical roles in plant resource uptake. However, how these processes change under water-saving irrigation technologies remains unclear, especially for organic systems where crops rely on soil ecological processes for plant nutrition and productivity. We conducted a field experiment and examined how water-saving subsurface drip irrigation (SDI) and concentrated organic fertilizer application altered root traits and rhizosphere processes compared to traditional furrow irrigation (FI) in an organic tomato system. We measured root distribution and morphology, the activities of C-, N-, and P-cycling enzymes in the rhizosphere, the abundance of rhizosphere microbial N-cycling genes, and root mycorrhizal colonization rate under two irrigation strategies. Tomato plants produced shorter and finer root systems with higher densities of roots around the drip line, lower activities of soil C-degrading enzymes, and shifts in the abundance of microbial N-cycling genes and mycorrhizal colonization rates in the rhizosphere of SDI plants compared to FI. SDI led to 66.4% higher irrigation water productivity than FI, but it also led to excessive vegetative growth and 28.3% lower tomato yield than FI. Our results suggest that roots and root-microbe interactions have a high potential for coordinated adaptation to water and nutrient spatial patterns to facilitate resource uptake under SDI. However, mismatches between plant needs and resource availability remain, highlighting the importance of assessing temporal dynamics of root–soil–microbe interactions to maximize their resource-mining potential for innovative irrigation systems.

Agricultural management practices affect bulk soil microbial communities and the functions they carry out, but it remains unclear how these effects extend to the rhizosphere in different agroecosystem contexts. Given close linkages between rhizosphere processes and plant nutrition and productivity, understanding how management practices impact this critical zone is of great importance to optimize plant-soil interactions for agricultural sustainability. A comparison of six paired conventional-organic processing tomato farms was conducted to investigate relationships between management, soil physicochemical parameters, and rhizosphere microbial community composition and functions. Organically managed fields were higher in soil total N and NO(3)-N, total and labile C, plant Ca, S, and Cu, and other essential nutrients, while soil pH was higher in conventionally managed fields. Differential abundance, indicator species, and random forest analyses of rhizosphere communities revealed compositional differences between organic and conventional systems and identified management-specific microbial taxa. Phylogeny-based trait prediction showed that these differences translated into more abundant pathogenesis-related gene functions in conventional systems. Structural equation modeling revealed a greater effect of soil biological communities than physicochemical parameters on plant outcomes. These results highlight the importance of rhizosphere-specific studies, as plant selection likely interacts with management in regulating microbial communities and functions that impact agricultural productivity. IMPORTANCE Agriculture relies, in part, on close linkages between plants and the microorganisms that live in association with plant roots. These rhizosphere bacteria and fungi are distinct from microbial communities found in the rest of the soil and are even more important to plant nutrient uptake and health. Evidence from field studies shows that agricultural management practices such as fertilization and tillage shape microbial communities in bulk soil, but little is known about how these practices affect the rhizosphere. We investigated how agricultural management affects plant-soil-microbe interactions by comparing soil physical and chemical properties, plant nutrients, and rhizosphere microbial communities from paired fields under organic and conventional management. Our results show that human management effects extend even to microorganisms living in close association with plant roots and highlight the importance of these bacteria and fungi to crop nutrition and productivity.

Domestication and agricultural intensification dramatically altered maize and its cultivation environment. Changes in maize genetics (G) and environmental (E) conditions increased productivity under high-synthetic-input conditions. However, novel selective pressures on the rhizobiome may have incurred undesirable tradeoffs in organic agroecosystems, where plants obtain nutrients via microbially mediated processes including mineralization of organic matter. Using twelve maize genotypes representing an evolutionary transect (teosintes, landraces, inbred parents of modern elite germplasm, and modern hybrids) and two agricultural soils with contrasting long-term management, we integrated analyses of rhizobiome community structure, potential microbe-microbe interactions, and N-cycling functional genes to better understand the impacts of maize evolution and soil management legacy on rhizobiome recruitment. We show complex shifts in rhizobiome communities during directed evolution of maize (defined as the transition from teosinte to modern hybrids), with a larger effect of domestication (teosinte to landraces) than modern breeding (inbreds to hybrids) on rhizobiome structure and greater impacts of modern breeding on potential microbe-microbe interactions. Rhizobiome structure was significantly correlated with plant nutrient composition. Furthermore, plant biomass and nutrient content were affected by G x E interactions in which teosinte and landrace genotypes had better relative performance in the organic legacy soil than inbred and modern genotypes. The abundance of six N-cycling genes of relevance for plant nutrition and N loss pathways did not significantly differ between teosinte and modern rhizospheres in either soil management legacy. These results provide insight into the potential for improving maize adaptation to organic systems and contribute to interdisciplinary efforts toward developing resource-efficient, biologically based agroecosystems.

Heightened interest in biologically-based methods of raising crop yields has driven research into beneficial microorganisms that can be used to improve crop growth and productivity. This review addresses the potential of rhizobia, vesicular-arbuscular mycorrhizae (VAM), and plant-growth-promoting rhizobacteria to improve growth of soybean (Glycine max (L.) Merr) under temperate conditions. Mechanisms of action of beneficial microorganisms and considerations for utilization at all root-zone temperatures (RZTs) are reviewed. Subsequent sections address current knowledge on the inhibition of soybean growth at low RZTs and the potential of beneficial microorganisms to alleviate low temperature stress. The three categories of beneficial microorganisms discussed differ in their modes of action and have shown potential for additive or synergistic growth promotion of soybean at all RZTs. At low RZT, pot and field studies have identified strains of rhizobia and PGPR, as well as certain phytohormones, that ameliorate the inhibitory effects of cold stress on soybean growth through a variety of mechanisms. Wider use of these treatments could aid the expansion of soybean cultivation in cold climates.

The effect of domestication and modern breeding on aboveground traits in maize (Zea mays) has been well-characterized, but the impact on root systems and the rhizosphere remain unclear. The transition from wild ecosystems to modern agriculture has focused on selecting traits that yielded the largest aboveground production with increasing levels of crop management and nutrient inputs. Root morphology, anatomy, and ecophysiological processes may have been affected by the substantial environmental and genetic shifts associated with this transition. As a result, root and rhizosphere traits that allow more efficient foraging and uptake in lower synthetic input environments might have been lost. The development of modern maize has led to a shift in microbiome community composition, but questions remain as to the dynamics and drivers of this change during maize evolution and its implications for resource acquisition and agroecosystem functioning under different management practices. Better understanding of how domestication and breeding affected root and rhizosphere microbial traits could inform breeding strategies, facilitate the sourcing of favorable alleles, and open new frontiers to improve resource use efficiency through greater integration of root development and ecophysiology with agroecosystem functioning.