Final report for GS22-268
Project Information
Rhizoma peanut (RP) [Arachis glabrata Benth.] is incorporated into grassland pastures, such as bahiagrass (BG) [Paspalum notatum Flüggé], to increase pasture feed quality and reduce the need for nitrogen (N) fertilizer inputs. Apart from N, phosphorus (P) is important for forage and animal nutrition. The nutrient dynamics of P is of interest because a large percent of soil P is unavailable to plants, especially in weathered soils, and P play a critical role in the contamination of water bodies. This study investigated P uptake and mobilization strategies in BG monoculture versus BG-RP mixture under low and adequate soil P level. We also identified soil microbial communities responsible for nutrient uptake both in the field and in the greenhouse. We hypothesized that in addition to soil and plant root associated microbes, RP will employ strategies that will increase soil P availability in BG-RP mixture, especially under low soil-P. Our findings showed that under low soil P, RP in BG-RP mixture has the potential to increase BG shoot biomass compared to BG monoculture. Another interesting finding was that under low soil P, RP in BG-RP mixture had greater shoot concentration of P, Fe, Mn, Zn, and Cu concentrations than BG shoots under low P, indicating that RP has higher ability to mobilize these nutrients than BG. Soil-P fractions analysis showed that NaOH- organic P occupied a larger percent (34%) of soil P. Soil microbial analysis conducted on the field showed that RP enhanced the relative abundances of fungal genera Fusarium, Gibberella, and Humicola. These fungi contribute to litter decomposition and nutrient cycling through their saprophytic lifestyle.
Hypothesis
- The integration of RP into BG system will enhance the community and functionality of both BG and RP associated microbial groups that are responsible for P solubilization and mineralization in microbial-soil interface and P exchange in plant-microbial interface.
- The enhancement of microbial mediated P cycling in hypothesis 1 will be controlled by a set of P cycling genes (Table 1), including but not limited to the genes responsible for solubilizing inorganic P (e.g., gcd and PqqABCDEF), the genes responsible for mineralizing P (e.g. PhoADN, aphA, olpA, php, glp, and app, and the genes involved in microbial-P exchange and plant uptake at the microbial-root P interface.
- Soil microbial P cycling processes (genes and enzymes release), especially the genes involved in P uptake and transport as well as P starvation genes, will be suppressed when P mineral fertilizers are applied.
Objectives
- Determine the effect of P fertilizer application on soil P pools, plant P uptake and P transfer under BG monoculture versus a BG-RP mixture.
- Identify microbial communities in the different belowground plant parts of bahiagrass (root+rhizome), rhizoma peanut (roots+ rhizome+ nodules), and in the rhizosphere, in response to forage species composition with or without mineral P fertilizer.
- Use qPCR to quantify organic P mineralization (e.g., phoC and bpp) and inorganic P dissolution (e.g., pqqC) genes in rhizosphere soil and bulk soil across forage species with and without P fertilizer.
- Profile genome expression of root microbiomes (including AMF) and root cells, with emphasis on identifying and quantifying the expression of key genes that are involved in P uptake and transport, as well as P-exchange (and P-metabolism) in the different forage systems (monoculture vs mixture) with or without mineral P fertilizer.
- Organize in-person visits with producers in North, Central, and South Florida and present our project findings to them.
Cooperators
Research
Materials and methods:
Greenhouse experiment setup: Two phases of greenhouse experiment were established to determine the microbial strategies employed by bahiagrass and rhizoma peanut for P and nutrient mobilization and uptake.
First phase: A 3x2 factorial greenhouse experiment with three forage treatments and two P levels, was conducted at the University of Florida, North Florida Research and Education Center (NFREC), Quincy, Florida from March to August 2022. Forage treatments included bahiagrass monoculture (BG), bahiagrass + “Ecoturf” rhizoma peanut (BG-RP), and bahiagrass + “Ecoturf” rhizoma peanut separated with a 30 µm fabric (BG-RPF) to prevent physical interactions of roots between both plants. The two P levels were treatments with no added P fertilizer (low P) and treatments with unlabeled P fertilizer 100 kg P2O5 ha-1 (high P). The treatments were arranged in randomized complete block design with 4 replicates.
Second phase: A second greenhouse experiment was carried out from February to June 2023. A rhizobox was designed to study in detail the microbial mechanisms involved in P and nutrient mobilization and uptake in BG-RP mixture. The treatment design was a 2x2x2 factorial design including BG-RP partitioned by 25 µm fabric and BG-RP without fabric, with or without AMF application, and two P levels were treatments with no added P fertilizer (low P) and treatments with 100 kg P2O5 ha-1 (high P). The treatments were arranged in randomized complete block design with 4 replicates.
Objective 1: Determine the distribution of applied 33P-labelled mineral P fertilizer on soil P pools, plant P uptake and P transfer under BG monoculture versus a BG-RP mixture.
Above and belowground biomasses were harvested. Bahiagrass and RP shoots in the mixtures were separated and the samples were dried in oven for 72 hours at 65ºC to measure dry biomass. The soil and aboveground samples were sent to Soil, Plant, and Water Laboratory, University of Georgia for carbon, nitrogen, phosphorus, and micronutrient analysis. Nutrient uptake for aboveground samples was also measured. Soil samples were analyzed for soil pH, total carbon (TC), total nitrogen (TN), and Mehlich-3 extractable P, K, Mg, Fe, Mn, Zn, and Cu. Soil P fractions (inorganic and organic soluble and insoluble P) were determined using the Hedley Fractionation and data were analyzed using ANOVA in R software.
Identify microbial communities and key genes involved in P transformation in bulk soil, rhizosphere, and root compartments (Objectives 2, 3, and 4).
After harvesting, pot contents (soil + roots + rhizomes) were emptied into trays and root + rhizomes for BG and root + rhizomes + nodules for RP (~2 g) were collected within 2 mins and placed in liquid N2 for DNA and RNA extraction. Root subsamples (~1.5 g) from greenhouse phase one were collected for arbuscular mycorrhizal (AM) colonization assessment. The DNA from the soil samples were extracted using DNeasy PowerSoil extraction kit, while DNA from root compartments were extracted using the cetyl trimethylammonium bromide buffer approach. Two-step PCR was carried out to produce the amplicon library, using the bacterial 16S rRNA primers (341F/806R) and ITS1F/ITS4 and NS31/AML2 for the fungal and AMF communities. The amplicon pools were sent to the Center for Genomic and Computational Biology, Duke University using Illumina MiSeq sequencer (v3 300 PE). The roots from each pot were stained and viewed under the microscope to count the AMF and their structures.
We employed metatranscriptomics for the root samples collected. Extracted root RNA samples were sent to Duke Center for Genomic and Computational Biology for sequencing using the Illumina Novaseq 6000 (2 x 150bp-PE) (Illumina Inc., San Diego, CA, USA). The computational workflow will be developed according to Liao et al. (2014) to sort the genes into bacterial and fungal rRNA, and functional genes of the root microbiome respectively and downstream analysis will be carried out in R software.
Field experiment: Three on-farm studies were conducted across Florida (North, Central, and South) as well as two other field studies at NFREC Quincy and Marianna to determine the soil microbial communities associated with integrating rhizoma peanut into bahiagrass pastures. The roles of these microbial communities in nutrient cycling in these pastures were also investigated.
SSARE_final_report_figures_tables
Greenhouse experiment:
Effects of P fertilizer levels and forage system on aboveground and belowground biomasses and nutrient concentrations
Phase 1 greenhouse experiment
At the first harvest in June and under low P, bahiagrass grown with RP with or without fabric had an average 24% greater shoot biomass than bahiagrass monoculture. However, there were no differences in shoot biomass among forage treatments under high P management (Table 1). This demonstrates that RP has the potential to increase bahiagrass growth, especially under low soil P. At the second harvest in August, shoot biomass of bahiagrass grown with RP without fabric were lower than shoot biomass of BG and BG-RPF under both, low and high P management (Table 1). Regardless of fabric separation or P management, RP in the mixture produced less shoot growth in comparison to bahiagrass (Table 1). The RP was established at the same time with bahiagrass in the mixture, which might have resulted in early competition of RP with bahiagrass and applying N fertilizer likely benefited bahiagrass growth more than RP (Shepard et al., 2022).
Although there was no forage treatment effect on belowground biomass (Table 1), higher P fertility increased belowground biomass by 55% (Table 1), demonstrating that P deficiency can inhibit root growth as has been reported in other species (Wissuwa et al., 2005; Su et al., 2022). Although there were not enough roots to examine RP response to P fertilization in phase 1 experiment, previous studies and our phase 2 data (Table 3) showed decreases in legume root dry mass with P deficiency (Bargaz et al., 2017).
There were shoot nutrient concentration responses to forage treatment. Shoot C and N were consistent across two P rates, while shoot P, Fe, Mn, Zn, and Cu varied across P rates (Table 2). Bahiagrass shoots, whether in monoculture and mixture, had greater C concentrations and in comparison, RP shoots had consistently higher N concentrations. As a result, RP shoots had lower C/N ratios than even bahiagrass-RP treatments. Regardless of species, forages under low P management also resulted in somewhat higher C values (P=0.005). Under low P fertility, RP shoots contained greater P concentrations than bahiagrass shoots under low P, but at high P, bahiagrass and RP shoots had similar P concentration. Taken together, bahiagrass shoots reported higher C/P ratios (758 to 814) than RP (251 to 256) shoots (Table 2). Considering that P mineralization and immobilization processes are reported to occur at C:P of <200:1 and > 300:1, respectively (Dubeux et al., 2006), P immobilization under bahiagrass dominated pastures is more likely than under BG-RP pastures.
Rhizoma peanut shoots had greater Fe, Mn, Zn, and Cu concentrations than bahiagrass shoots under low P, but at high soil P, bahiagrass and RP shoots were statistically similar for all micronutrient concentrations, other than Mn, where RP had lower concentrations. From these results, it may be deduced that low soil P stimulated RP plants to release more exudates able to mobilize soil P and micronutrients, as was reported in other studies (Srinivasarao et al., 2006; Mitra et al., 2020). Organic and inorganic anions released by plants to mobilize soil P can also mobilize cations that often bind P, such as Ca, Al, Fe, and Mn (Lambers et al., 2013). Compared to grasses that primarily release phytosiderophores, legumes (dicots more generally) release a suite of organic acids. Under acid mineral soils, the legume strategy appeared to be superior to the bahiagrass strategy. These results are similar to previous studies that reported legumes having a larger effect on the rhizosphere, such as greater release of organic acids and enzyme activities than grasses (Touhami et al., 2020).
Most of the nutrient uptake values followed a similar relationship to the shoot biomass data (Table 1). Bahiagrass shoot biomass was greater than RP shoot biomass, as a result bahiagrass grown as monoculture or in RP mixtures generally had a greater accumulation of shoot N, P, Mn, and Cu than RP, regardless of soil P fertility. Except for N and Fe, increasing P soil fertility led to greater shoot nutrient content.
Phase 2 greenhouse experiment:
The fabrics used in phase 1 greenhouse experiment prevented belowground growth due to the limited space in the pots used for the experiment. We conducted a phase 2 greenhouse experiment, where we designed a rhizobox (figure 2) that allowed root proliferation, while the 0.25 µm mesh fabric prevented the physical interactions of the roots of both plants. This set-up allowed us to determine the free-living and root associated microbial communities responsible for phosphorus mobilization and transfer in bahiagrass and rhizoma peanut mixture under low and high soil P levels. Our result from phase 2 greenhouse experiment showed that the BG aboveground biomass was consistently greater when there was a physical root interaction with RP compared to when fabric barriers were present (Table 3). Both plants belowground biomass were increased with both roots interactions than when fabrics were present to prevent root interactions. Rhizoma peanut shoot C, N, P, Zn, and Cu concentrations (Table 4) were lower when there was no barrier compared to barrier, indicating that bahiagrass might be competing with RP for these nutrients. This may have resulted in increased BG root and shoot biomass (Table 3).
Soil nutrients in phase 1 and 2 greenhouse experiments
There were no notable responses of Mehlich-3 nutrients to forage treatment in both greenhouse experiments. This contrasted with an increase in soil P availability reported in bahiagrass- rhizoma peanut mixtures (Sigua et al., 2014). Phosphorus fertilizer treatment resulted in a 24% increase in Mehlich-3 P concentration and a 15, 25, and 14% decrease in Mehlich-3 Mn, Zn, and Cu concentrations, respectively. Phosphorus interactions with micronutrients have been extensively studied (Murphy et al., 1981; Fageria, 2001). Phosphorus applications have been reported to decrease soil Zn diffusion rates and increase micronutrient immobilization (Fageria, 2001; Alloway, 2008).
Soil-P fractions across all treatments showed that NaOH-Po occupied a larger percent (34%) of soil P, followed by NaHCO3-Po with 25%, residual P with 15%, NaOH-Pi with 14%, NaHCO3-Pi with 11%, HCl- inorganic P with 1%, and water P with 0.7% (data not shown). The effect of forage treatment on NaHCO3-Po, HCl-P, and water P was mainly because these soil P fractions in the pots without plants were greater than pots with forages (Table 5). This might be due to There were no changes observed for inorganic and organic soil P fractions in bahiagrass-RP mixtures in comparison to bahiagrass monocultures. Phosphorus fertilizer treatment only influenced NaHCO3-Pi (P=0.014). NaHCO3-Pi was 51% greater at high P than low P (Table 5-6).
Arbuscular mycorrhizal fungal assessment
Quantification of AMF in soil using qPCR approach showed that RP soils had twice the AMF counts compared to bahiagrass soils (Figure 1B). The presence of plants played a large role in AMF abundance in soil as evident in the little or no AMF counts in pots with no plants (Figure 1B) (Li et al., 2009). In comparison, microscopic imaging of AMF colonization of the plant roots differed among forage and P treatments (Table 6; Figure 1A). Rhizoma peanut had greater arbuscular colonization than bahiagrass but only at low soil P (Figure 1A). Also at low P, bahiagrass grown in the mixture had greater vesicular colonization. The differential responses of bahiagrass and RP to arbuscular and vesicular colonization might be influenced by the low soil P environment. Rhizoma peanut requires P for N2 fixation and overall, has a greater demand for P than bahiagrass (Sigua et al., 2014). Greater arbuscules in RP might indicate an increased nutrient exchange between the plant and AMF since arbuscules are considered the site for nutrient exchange by AMF (Luginbuehl and Oldroyd, 2017).
Across all structures, AMF colonization was generally greater under high soil P fertility than low P. Others have reported a decrease in AMF colonization with P fertilizer applications (Tshewang et al., 2020). However, in this study, we found that a P application increased AMF colonization. There might be an upper soil P threshold for AM colonization, and P fertilizer application above that range might restrict AM colonization (Grant et al., 2005). This threshold may differ among plant species. Regardless of P fertilizer rate, the Mehlich-3 soil P fertility after harvest was low (15 – 17 mg P kg-1) (even for the pots without plants) based on the recommended soil-test P interpretation (<25 mg P kg-1) for agronomic crops in Florida (Mylavarapu et al., 2021), suggesting that soil P fertilizer application in this study was likely far from exceeding the threshold to inhibit mycorrhizal symbiosis. Chippano et al. (2020) showed an increase in AMF colonization in Lotus tenuis from 81.3% to 93.1% of the root length colonized when available P in soil increased from 5.0 to 12.7 mg kg–1, and AMF colonization decreased at higher soil P concentrations. Arbuscular mycorrhizal fungal associations may not be the primary strategy to acquire P at very low P availability in soil (Chippano et al., 2020). Plants may deploy other strategies that warrant further investigation. Such strategies could include manipulating root traits (Lambers et al. 2006) and release of protons that may not incur as much C cost as AM symbiosis.
Results from field experiment:
On-farm studies
The effect of incorporating RP into bahiagrass pastures in Florida on soil microbial communities responsible for nutrient cycling, especially soil bacteria depend on pasture location and growing season. Increased soil bacterial diversity in bahiagrass-RP mixtures was only evident in North Florida and during May sampling. However, the presence of RP consistently enhanced soil fungal diversity across Florida pastures during peak forage production in July (Erhunmwunse et al., 2023c). While the impact of bahiagrass RPP mixtures on some soil microbes was consistent across pastures in Florida, we found that pasture locations affected some other soil microbes. Bahiagrass-RPP mixtures promoted the relative abundance of the fungal class Nectriaceae (made up of mainly Fusarium) in north and south Florida, but not in central Florida. In north Florida, bahiagrass-RPP soils supported greater relative abundance of arbuscular mycorrhizal fungi than bahiagrass soils. However, there was no impact in central Florida. Additionally, we found a decrease in the relative abundance of arbuscular mycorrhizal fungi in bahiagrass-RPP compared to bahiagrass monocultures in south Florida (Erhunmwunse et al., 2023c; Liao and Erhunmwunse, 2024). These results demonstrate that the impact of RPP on soil microbes will not always be consistent in different pastures. Soil microbes respond to a combination of factors such as forage growth, soil chemical properties (soil pH, phosphorus, and nitrogen), environmental conditions, and animal activities. Soil pH is a major factor contributing to changes in soil microbes in bahiagrass-RPP pasture locations across Florida.
Mixtures of bahiagrass and RPP can increase soil microbial diversity. Soil fungal diversity and community are easily influenced by bahiagrass-RPP mixtures (Erhunmwunse et al., 2023a; 2023b; 2023c). However, it requires a longer establishment period of RPP into bahiagrass pastures to observe changes in soil bacterial communities (Erhunmwunse et al., 2023a). Erhunmwunse et al. (2023a; 2023b) found an increase in the relative abundance of soil fungal genera, such as Fusarium/Gibberella and Humicola responsible for N cycling and soil organic matter decomposition.
Figure 2: The relative abundance of the dominant fungal taxa that responded to forage treatments (bahia= bahiagrass monoculture; bahia-Eco= bahiagrass and Ecoturf RP mixture; bahia-Flo= bahiagrass and Florigraze RP mixture; Eco= Ecoturf RP monoculture; and Flo= Florigraze RP monoculture) in an experiment conducted at NFREC, Marianna. Lowercase letters indicate significant differences among treatments using Tukey analysis.
Objective 5
We conducted in-person visits with three forage growers/ranchers in North, Central, and South Florida and presented our project findings to them. These growers reported change in knowledge, attitudes, skills and/or awareness. They adopted the integration of rhizoma peanut as a sustainable option in their pastures. These growers mentioned the benefits such as reduction in inorganic N fertilizer and increased nutritive value of the forages for their animals. We also promoted our research to the local farming community on Perennial Peanut Field Day and growers are eager to see our research findings. They are curious to know if rhizoma peanut grown with grasses will improve P uptake and reduce P fertilizer applied to their pastures. We plan to publish extension articles to communicate our research findings to them. We exchanged contacts with some of the producers to inform them when our article is released. By improving the P fertilizer use efficiency of pasture systems, fertilizer savings will impact all regional forage and livestock producers.
References
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Su, R., Zhang, Z., Chang, C., Peng, Q., Cheng, X., Pang, J., He, H., & Lambers, H. (2022). Interactive effects of phosphorus fertilization and salinity on plant growth, phosphorus and sodium status, and tartrate exudation by roots of two alfalfa cultivars. Annals of Botany, 129(1), 53-64. https://doi.org/10.1093/aob/mcab124.
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Erhunmwunse, A. S., V. A. Guerra, J. C. Liu, C. L. Mackowiak, A. R. S. Blount, J. C. B. Dubeux Jr., and H. L. Liao. 2023a. “Soil bacterial diversity responds to long-term establishment of perennial legumes in warm-season grassland at two soil depths.” Microorganisms 11 (12): 3002. https://doi.org/10.3390/microorganisms11123002
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Educational & Outreach Activities
Participation Summary:
We have had opportunities to showcase our project in the greenhouse as well as the field experiment during field days, student tours, in-service training to students, farmers and agricultural professionals. Below are the details of the outreach activities that we have been involved in.
In-service training:
(1) We educated state and county extension agents about the need for improving phosphorus use efficiency in Florida soils using legumes and soil microbes at North Florida Beef and Forage In-service training (FBF-IST) for Florida state and county extension faculty (03/30/2023). Topic: Soil-plant interactions, Role of legumes and microbes in phosphorus mobilization in highly weathered soils, and mycotoxins in forages.
(2) On May 14, 2024, we led a Soil Health In-Service Training at NFREC, which included 8 hours of on-site training and 6 online short lectures. This training aimed to equip Extension faculty with knowledge about soil indicators and how to enhance soil health by evaluating these indicators for various cropping systems, including forage and cover cropping systems (Lead organizer: Liao; Lab participants included Ben Reimer)
Field day:
We presented a poster (legume cultivars effect on soil microbial communities (the hidden engineers) in bahiagrass system) on the 33rd perennial peanut field day, NFREC, Quincy, FL.
Tours:
- Student tour. 2022. Students in the Department of Soil Water, and Ecosystem Sciences from Gainesville and research centers in Florida. (~ 15 students were in attendance)
- Plant Sciences Council, a graduate student organization tour (~ 12 students were in attendance)
Webinars, talks and presentations:
- We organized a Microbiology class and hands-on activity lasting six hours for Cub Scouts (Wallwood Outdoor Weekend Program, Gadsden county FL) (11/19/2023). Scope:We delivered knowledge to the younger generation, focusing on environmental microbes, including beneficial soil fungi. We covered fundamental concepts such as the roles of forest decomposers, mycorrhizae, and environmental bacteria play in benefiting our environment. Instructors: Sunny Liao; Ben Reimer, Kaile Zhang, Haihua Wang; Target audience: Kindergarten to 5th grade
- Presentation at “STEM in the art” exhibition (11/29/2022) in Tallahassee. Scope: We demonstrated the benefits of perennial peanut as a forage and ornamental purpose in Florida. We taught the audience the importance of N fixing bacteria and other important microbes residing in rhizoma peanut nodules and practiced the art of culturing non-pathogenic bacteria on agar plates. Instructors: Adesuwa Erhunmwunse and Ben Reimer (PhD students). Target audience: Tallahassee community residents.
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Demonstrations at Tallahassee Science Festival (10/22/2022). Scope: Presented the role of soil microbes (mycorrhiza and rhizobia) in P cycling in agriculture. We shared handouts, used posters, and samples of rhizoma peanut as demonstration materials. Instructors: Adesuwa Erhunmwunse and Ben Reimer (PhD students), Kaile Zhang and Haihua Wang (post docs), and Vijay Verma (Biologist Scientist).
Other Educational Activities
Adesuwa Erhunmwunse (PhD student) trained a master’s student (Rachel Balster) this year on how to set up an experiment and explore molecular and microbial techniques to identify bacterial communities from the nodules of rhizoma peanut.
Project Outcomes
During this project, we developed a deeper understanding that sustainable agriculture is not a one-size-fits-all approach. Initially, we assumed that low soil phosphorus (P) would stimulate greater arbuscular mycorrhizal fungi activity and enhance P release from soil. However, our findings in the bahiagrass–rhizoma peanut system revealed that applying P fertilizer increased AMF colonization. This suggests that there may be an optimal soil P threshold for AMF colonization, beyond which fertilizer inputs could inhibit AMF activities, and that this threshold likely varies by plant species.
This experience shifted our perspective: sustainable agriculture does not mean eliminating fertilizer use but rather adopting practices that balance inputs with biological processes to improve nutrient use efficiency.
Information Products
- Changes in soil microbial diversity and community composition across bahiagrass and rhizome peanut pastures
- Soil microbes in bahiagrass and rhizoma peanut pastures
- Short-term integration of perennial peanut into bahiagrass system influence on soil microbial-mediated nitrogen cycling activities and microbial co-occurrence networks
- Soil bacterial diversity responds to long-term establishment of perennial legumes in warm-season grassland at two soil depths
- Rust disease in Florida warm season grasses