Water Stress and Black Cutworm Feeding Modulate Plant Response in Maize Colonized by Metarhizium robertsii.

Plants face many environmental challenges and have evolved different strategies to defend against stress. One strategy is the establishment of mutualistic associations with endophytic microorganisms which contribute to plant defense and promote plant growth. The fungal entomopathogen Metarhizium robertsii is also an endophyte that can provide plant-protective and growth-promoting benefits to the host plant. We conducted a greenhouse experiment in which we imposed stress from deficit and excess soil moisture and feeding by larval black cutworm (BCW), Agrotis ipsilon, to maize plants that were either inoculated or not inoculated with M. robertsii (Mr). We evaluated plant growth and defense indicators to determine the effects of the interaction between Mr, maize, BCW feeding, and water stress. There was a significant effect of water treatment, but no effect of Mr treatment, on plant chlorophyl, height, and dry biomass. There was no effect of water or Mr treatment on damage caused by BCW feeding. There was a significant effect of water treatment, but not Mr treatment, on the expression of bx7 and rip2 genes and on foliar content of abscisic acid (ABA), 2,4-dihydroxy-7-methoxy-1,4-benzoxazin-3-one (DIMBOA), and gibberellin 19 (GA19), whereas GA53 was modulated by Mr treatment. Foliar content of GA19 and cis-Zeatin (cZ) was modulated by BCW feeding. In a redundancy analysis, plant phenology, plant nutrient content, and foliar DIMBOA and ABA content were most closely associated with water treatments. This study contributes toward understanding the sophisticated stress response signaling and endophytic mutualisms in crops.

Seedcorn maggot response to planting date, cover crops, and tillage in organic cropping systems.

Seedcorn maggot, Delia platura (Meigen) (Diptera: Anthomyiidae), is an economically important early-season pest of corn and soybean in the United States. Adult seedcorn maggot is attracted to decomposing plant residues for oviposition, creating potential management issues where growers typically use tillage to incorporate fertility amendments and to create a seedbed. The use of growing degree-day models to time planting dates is an important tool for effectively managing this pest, but their use has not been examined in organic crop production. Here, we report the results of experiments to determine the effects of cover crops, tillage, and relative planting date on seedcorn maggot in corn and soybean in 2 experiments: The first during the transition to organic from conventional management and the second during the 3 yr following organic certification in central Pennsylvania, United States. Overall, delaying the planting date by 1-2 wk reduced fly emergence in corn, but not in soybean in both experiments. Seedcorn maggot emergence was also consistently greater in corn than in soybean, with 6 times more flies in corn than in soy. About 15 times more seedcorn maggot flies emerged from corn in treatments in which cover crops were managed with tillage compared to treatments in which cover crops were terminated with a roller-crimper followed by no-till planting of corn. Fly emergence was negatively related to the proportion of legumes in the cover crop mixture preceding corn. These results can help inform soil, cover crop, and crop decisions for organic growers in the Mid-Atlantic United States.

Maize response to endophytic Metarhizium robertsii is altered by water stress.

To defend against damage from environmental stress, plants have evolved strategies to respond to stress efficiently. One such strategy includes forming mutualist relationships with endophytes which confer stress-alleviating plant defensive and growth promoting effects. Metarhizium robertsii is an entomopathogen and plant-protective and growth-promoting endophyte. To determine the context dependency of the relationship between M. robertsii and maize, we conducted a greenhouse experiment that imposed stress as deficit and excess soil moisture on maize plants which were inoculated or not inoculated with M. robertsii and measured plant growth and defense indicators. Maize height and endophytic root colonization by M. robertsii were positively correlated in the deficit water treatment, but not in the adequate or excess water treatments. The relative expression of ZmLOX1 in the jasmonic acid (JA) biosynthesis pathway was significantly greater in M. robertsii-inoculated than in non-inoculated plants, but water treatment had no effect. There was significant interaction between M. robertsii and water treatments on foliar concentrations of JA and jasmonoyl isoleucine (JA-ILE), suggesting that water stress impacts M. robertsii as a modulator of plant defense. Water stress, but not inoculation with M. robertsii, had a significant effect on the expression of MYB (p = 0.021) and foliar concentrations of abscisic acid (p<0.001), two signaling molecules associated with abiotic stress response. This study contributes toward understanding the highly sophisticated stress response signaling network and context dependency of endophytic mutualisms in crops.

Endophytic Metarhizium robertsii suppresses the phytopathogen, Cochliobolus heterostrophus and modulates maize defenses.

Fungi in the genus Metarhizium (Hypocreales: Clavicipitaceae) are insect-pathogens and endophytes that can benefit their host plant through growth promotion and protection against stresses. Cochliobolus heterostrophus (Drechsler) Drechsler (Pleosporales: Pleosporaceae) is an economically-significant phytopathogenic fungus that causes Southern Corn Leaf Blight (SCLB) in maize. We conducted greenhouse and lab-based experiments to determine the effects of endophytic M. robertsii J.F. Bisch., Rehner & Humber on growth and defense in maize (Zea mays L.) infected with C. heterostrophus. We inoculated maize seeds with spores of M. robertsii and, at the 3 to 4-leaf stage, the youngest true leaf of M. robertsii-treated and untreated control plants with spores of C. heterostrophus. After 96 h, we measured maize height, above-ground biomass, endophytic colonization by M. robertsii, severity of SCLB, and expression of plant defense genes and phytohormone content. We recovered M. robertsii from 74% of plants grown from treated seed. The severity of SCLB in M. robertsii-treated maize plants was lower than in plants inoculated only with C. heterostrophus. M. robertsii-treated maize inoculated or not inoculated with C. heterostrophus showed greater height and above-ground biomass compared with untreated control plants. Height and above-ground biomass of maize co-inoculated with M. robertsii and C. heterostrophus were not different from M. robertsii-treated maize. M. robertsii modulated the expression of defense genes and the phytohormone content in maize inoculated with C. heterostrophus compared with plants not inoculated with C. heterostrophus and control plants. These results suggest that endophytic M. robertsii can promote maize growth and reduce development of SCLB, possibly by induced systemic resistance mediated by modulation of phytohormones and expression of defense and growth-related genes in maize.

Cover crop mixture expression is influenced by nitrogen availability and growing degree days.

Cover crop mixtures can provide multiple ecosystem services but provisioning of these services is contingent upon the expression of component species in the mixture. From the same seed mixture, cover crop mixture expression varied greatly across farms and we hypothesized that this variation was correlated with soil inorganic nitrogen (N) concentrations and growing degree days. We measured fall and spring biomass of a standard five-species mixture of canola (Brassica napus L.), Austrian winter pea (Pisum sativum L), triticale (x Triticosecale Wittm.), red clover (Trifolium pratense L.) and crimson clover (Trifolium incarnatum L.) seeded at a research station and on 8 farms across Pennsylvania and New York in two consecutive years. At the research station, soil inorganic N (soil iN) availablity and cumulative fall growing degree days (GDD) were experimentally manipulated through fertilizer additions and planting date. Farmers seeded the standard mixture and a "farm-tuned" mixture of the same five species with component seeding rates adjusted to achieve farmer-desired services. We used Structural Equation Modeling to parse out the effects of soil iN and GDD on cover crop mixture expression. When soil iN and fall GDD were high, canola dominated the mixture, especially in the fall. Low soil iN favored legume species while a shorter growing season favored triticale. Changes in seeding rates influenced mixture composition in fall and spring but interacted with GDD to determine the final expression of the mixture. Our results show that when soil iN availability is high at the time of cover crop planting, highly competitive species can dominate mixtures which could potentially decrease services provided by other species, especially legumes. Early planting dates can exacerbate the dominance of aggressive species. Managers should choose cover crop species and seeding rates according to their soil iN and GDD to ensure the provision of desired services.

Prevalence of Early- and Late-Season Pest Damage to Corn in Cover Crop-Based Reduced-Tillage Organic Systems.

In organic agronomic cropping systems, the use of synthetic insecticides and transgenic varieties are prohibited and producers rely mainly on biological control, tillage, crop rotation, and other cultural practices to manage pests. We measured damage to organic corn (Zea mays L.) from multiple invertebrate pests, including slugs (Gastropoda: Mollusca), European corn borer (Ostrinia nubilalis Hübner), corn earworm (Helicoverpa zea Boddie), and fall armyworm (Spodoptera frugiperda Smith), early and late in the growing season in four cropping systems that varied in tillage frequency and intensity and in winter cover crop species. Specific management tactics included two cover crop mixtures preceding corn, the use of a roller-crimper or tillage to terminate cover crops preceding corn, and the establishment of interseeded cover crops after corn emergence. Prevalence of early-season damage was high, but severity of damage was very low and unrelated to corn yield. The proportion of corn plants affected by chewing pests early in the season was lower in plots in which tillage compared to a roller-crimper was used to terminate cover crops. Cropping system did not affect the numbers of late-season caterpillar pests or corn yield. Predation by natural enemies appeared to effectively maintain damage from chewing pests below yield-damaging levels. These results support the inclusion of winter and interseeded cover crops in organic agronomic crop rotations to gain environmental benefits without increasing risks of damage by insect pests.

Systemic Colonization by Metarhizium robertsii Enhances Cover Crop Growth.

Fungi in the genus Metarhizium (Hypocreales: Clavicipitaceae) are insect pathogens that can establish as endophytes and can benefit their host plant. In field experiments, we observed a positive correlation between the prevalence of M. robertsii and legume cover crops, and a negative relationship with brassicaceous cover crops and with increasing proportion of cereal rye in mixtures. Here, we report the effects of endophytic M. robertsii on three cover crop species under greenhouse conditions. We inoculated seeds of Austrian winter pea (Pisum sativum L., AWP), cereal rye (Secale cereale L.), and winter canola (Brassica napus L.) with conidia of M. robertsii to assess the effects of endophytic colonization on cover crop growth. We recovered M. robertsii from 59%, 46%, and 39% of seed-inoculated AWP, cereal rye, and canola plants, respectively. Endophytic M. robertsii significantly increased height and above-ground biomass of AWP and cereal rye but did not affect chlorophyll content of any of the cover crop species. Among inoculated plants from which we recovered M. robertsii, above-ground biomass of AWP was positively correlated with the proportion of colonized root but not leaf tissue sections. Our results suggest that winter cover crops may help to conserve Metarhizium spp. in annual cropping systems.

Soil Microarthropods and Soil Health: Intersection of Decomposition and Pest Suppression in Agroecosystems.

Two desirable functions of healthy soil are nutrient cycling and pest suppression. We review relevant literature on the contributions of soil microarthropods to soil health through their intersecting roles in decomposition and nutrient cycling and direct and indirect suppression of plant pests. Microarthropods can impact soil and plant health directly by feeding on pest organisms or serving as alternate prey for larger predatory arthropods. Indirectly, microarthropods mediate the ability of crop plants to resist or tolerate insect pests and diseases by triggering induced resistance and/or contributing to optimal nutritional balance of plants. Soil fauna, including microarthropods, are key regulators of decomposition at local scales but their role at larger scales is unresolved. Future research priorities include incorporating multi-channel omnivory into food web modeling and understanding the vulnerability of soil carbon through global climate change models.

Cover Crop Species and Management Influence Predatory Arthropods and Predation in an Organically Managed, Reduced-Tillage Cropping System.

Agricultural practices affect arthropod communities and, therefore, have the potential to influence the activities of arthropods. We evaluated the effect of cover crop species and termination timing on the activity of ground-dwelling predatory arthropods in a corn-soybean-wheat rotation in transition to organic production in Pennsylvania, United States. We compared two cover crop treatments: 1) hairy vetch (Vicia villosa Roth) planted together with triticale (×Triticosecale Wittmack) after wheat harvest, and 2) cereal rye (Secale cereale Linnaeus) planted after corn harvest. We terminated the cover crops in the spring with a roller-crimper on three dates (early, middle, and late) based on cover crop phenology and standard practices for cash crop planting in our area. We characterized the ground-dwelling arthropod community using pitfall traps and assessed relative predation using sentinel assays with live greater waxworm larvae (Galleria mellonella Fabricius). The activity density of predatory arthropods was significantly higher in the hairy vetch and triticale treatments than in cereal rye treatments. Hairy vetch and triticale favored the predator groups Araneae, Opiliones, Staphylinidae, and Carabidae. Specific taxa were associated with cover crop condition (e.g., live or dead) and termination dates. Certain variables were positively or negatively associated with the relative predation on sentinel prey, depending on cover crop treatment and stage, including the presence of predatory arthropods and various habitat measurements. Our results suggest that management of a cover crop by roller-crimper at specific times in the growing season affects predator activity density and community composition. Terminating cover crops with a roller-crimper can conserve generalist predators.

Management of Overwintering Cover Crops Influences Floral Resources and Visitation by Native Bees.

The incorporation of cover crops into annual crop rotations is one practice that is used in the Mid-Atlantic United States to manage soil fertility, suppress weeds, and control erosion. Additionally, flowering cover crops have the potential to support beneficial insect communities, such as native bees. Because of the current declines in managed honey bee colonies, the conservation of native bee communities is critical to maintaining "free" pollination services. However, native bees are negatively affected by agricultural intensification and are also in decline across North America. We conducted two experiments to assess the potential of flowering cover crops to act as a conservation resource for native bees. We evaluated the effects of cover crop diversity and fall planting date on floral resource availability and visitation by native bees for overwintering flowering cover crop species commonly used in the Mid-Atlantic region. Cover crop species, crop rotation schedule, and plant diversity significantly influenced floral resource availability. Different cover crop species not only had different blooming phenologies and winter survival responses to planting date, but attracted unique bee communities. Flower density was the primary factor influencing frequency of bee visitation across cover crop diversity and fall planting date treatments. The results from these experiments will be useful for informing recommendations on the applied use of flowering cover crops for pollinator conservation purposes.