Dual Utilization of Medicinal and Aromatic Crops as Bioenergy

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Dual Utilization of Medicinal and Aromatic Crops as Bioenergy Feedstocks Valtcho D. Zheljazkov,*,† Charles Neal Stewart, Jr.,‡ Blake Joyce,‡ Holly Baxter,‡ Charles L. Cantrell,§ Tess Astatkie,¶ Ekaterina A. Jeliazkova,† and Charleson R. Poovaiah‡ †

Crop and Soil Science Department, Oregon State University, Corvallis, Oregon 97331, United States Department of Plant Sciences, University of Tennessee, Knoxville, Tennessee 37996, United States § Agricultural Research Service, United States Department of Agriculture, NPURU, University, Mississippi 38677, United States ¶ Faculty of Agriculture, Dalhousie University, 50 Pictou Road, P.O. Box 550, Truro, Nova Scotia B2N 5E3, Canada

J. Agric. Food Chem. Downloaded from pubs.acs.org by KAOHSIUNG MEDICAL UNIV on 08/19/18. For personal use only.

‡

S Supporting Information *

ABSTRACT: Dual production of biofuels and chemicals can increase the economic value of lignocellulosic bioenergy feedstocks. We compared the bioenergy potential of several essential oil (EO) crops with switchgrass (Panicum virgatum L.), a crop chosen to benchmark biomass and lignocellulosic biofuel production. The EO crops of interest were peppermint (Mentha × piperita L.), “Scotch” spearmint (Mentha × gracilis Sole), Japanese cornmint (Mentha canadensis L.), and sweet sagewort (Artemisia annua L.). We also assessed each crop for EO production in a marginal production environment in Wyoming, USA, with irrigation and nitrogen (N) rates using a split-plot experimental design. Oil content ranged from 0.31 to 0.4% for Japanese cornmint, 0.23 to 0.26% for peppermint, 0.38 to 0.5% for spearmint, and the overall mean of sweet sagewort was 0.34%. Oil yields ranged from (in kg ha−1) 34 to 165 in Japanese cornmint, 25 to 108 in peppermint, 29.3 to 126 in spearmint, and 39.7 in sweet sagewort. EO production, but not composition, was sensitive to N fertilization. The alternative bioenergy crops and switchgrass produced similar amounts of ethanol from bench-scale simultaneous saccharification and fermentation assays. Value-added incomes from the EO proceeds were estimated to be between $1055 and $5132 ha−1 from peppermint, $1309 and $5580 ha−1 from spearmint, $510 and $2460 ha−1 from Japanese cornmint, and $3613 ha−1 from sweet sagewort under Wyoming growth conditions. The advantage of the proposed crops over traditional lignocellulosic species is the production of high-value natural products in addition to lignocellulosic biofuel production. KEYWORDS: bioproducts, essential oils, ethanol, Artemisia annua, Panicum virgatum, Mentha canadensis, Mentha × piperita, Mentha × gracilis

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INTRODUCTION Why Do We Need Alternative High-Value Crops as Feedstock for Ethanol Production? Current ethanol production in the USA is mainly limited to starch-based maize grain, which is a mature production platform and unlikely to experience a major cost reduction. The net energy output-to-input ratio of maize grain to ethanol is low, 1.5:1, compared to that of lignocellulosic platforms. Ideal nextgeneration biofuel crops should have (1) high biomass potential; (2) suitability for large-scale production; (3) equal or greater value from the part of the crop not used for biofuel production compared to the commonly grown cash crops in the region; and (4) high efficiency of enzymatic or acid hydrolysis for biomass used for biofuel production. We hypothesized that some crops containing high-value natural products would be suitable alternatives to commonly used lignocellulosic feedstocks such as switchgrass. The dual production of biofuel coupled with production of high-value natural products would spread risk over commodity price constraints and other uncertainties; such crops would likely be attractive to growers as profit centers. Here we summarize the results from a 2-year study on promising high-value biofuel crops that include peppermint and spearmint as well as the new crops Japanese cornmint and © XXXX American Chemical Society

sweet sagewort. Cropping systems including these species could provide sustainable feedstock production for ethanol together with high-value natural products (biochemicals) while providing improved diversity of feedstock production. In a previous study, we investigated the possibility of using two subtropical essential oil (EO)-producing grasses, including lemongrass [Cymbopogon f lexuosus (Steud.) Wats (syn. Andropogon nardus var. flexuosus)] and palmarosa [Cymbopogon martini (Roxb.) Wats. var martinii (syn. C. martini Sapg var. motia), as dual-commodity feedstock for ethanol and EOs.1 However, lemongrass production is limited to the tropics and subtropics. Lemongrass and palmarosa are perennials but are cultivated as annuals in the U.S. South where winters include freezing temperatures.1 In a study conducted in northern Wyoming, “Native” spearmint (Mentha spicata L.), Japanese cornmint (Mentha canadensis L.), lemongrass [Cymbopogon f lexuosus (Nees ex Steud.) J.F. Watson], and common wormwood (Artemisia vulgaris L.), along with two traditional biofuel crops, maize (Zea mays L.) Received: Revised: Accepted: Published: A

March 13, 2018 June 20, 2018 July 20, 2018 July 20, 2018 DOI: 10.1021/acs.jafc.7b04594 J. Agric. Food Chem. XXXX, XXX, XXX−XXX

Article

Journal of Agricultural and Food Chemistry

production of cultivated A. annua has emerged in China, Kenya, and Vietnam. The WHO estimates stated that there is an annual need for over 2 million doses of artemisinin combination therapies (ACT) as a first line of defense against multidrug-resistant Plasmodium falciparum malaria.20 In addition, A. annua is a source of antioxidant flavonoids. Essential oil obtained from A. annua is another high-value natural product that has applications in perfumery, cosmetics, and aromatherapy. The A. annua EO possesses antioxidant, antifungal, and antibacterial properties21,22 as well as insecticidal activity.23 The dried leaves of the plant contain 1.4 to 4.0% EO, which are rich in antioxidants24 and are found to control the development of coccidian (Eimeria spp.) parasitism in chickens.25−27 Currently, Eastern Europe produces most of the A. annua EO available on the international market.28,29 We found that A. annua can selfseed in Mississippi, which allows recurrent annual production, where it appears to be readily adaptable for biomass production, growing over 2 m in height. Switchgrass (Panicum virgatum) has been widely studied as a biofuel crop in the U.S.,30 and it has been used as a control for comparison with other lignocellulosic biomass species. Reed canarygrass (Phalaris arundinacea) is a cool-season (C3) grass with significant biomass potential in diverse environments.31−33 Although reed canarygrass has shown strong potential for use as a biofuel crop, there is a concern regarding its invasiveness.34 Consequently, we excluded reed canarygrass from the current study. The long-term goal of our research is to improve economic, environmental, and agronomic sustainability of feedstock for sustainable energy production through coupling feedstock production for biofuel with the production of high-value natural products. In this two-year study, we specifically focused on determining biomass yields, biomass-scale EO content, land-area EO yield, EO composition, and ethanol production by crop species and N- and irrigation treatments.

and switchgrass (Panicum virgatum L.), were compared for biomass and ethanol yield under two contrasting types of irrigation: irrigation with either potable water or with “produced water,” a byproduct from commercial methane extraction.2 However, water is a precious commodity in Wyoming and much of the U.S. West. Also, the above studies were conducted under a single fertilizer regime. Fertilizers and water are major modifiers of crop yields and chemistry. Therefore, there is a need to evaluate new crops, including promising dual-utilization species, under various fertilizer and irrigation regimes. Essential oils (EOs) are high-value natural products that are typically extracted using steam-distillation. Steam distillation of these crops (basically a 2-h treatment of the biomass with hot steam) may overcome biomass recalcitrance described by Himmel et al.3 The steamed biomass may be more readily convertible to ethanol compared to biomass that has not received pretreatment with hot steam; hence, there may be another advantage of the EO crops as feedstock for ethanol production. Peppermint, Spearmint, Japanese Mint, and Sweet Sagewort as Alternative Feedstock for Ethanol Production. Peppermint (Mentha × piperita L.), “Scotch” spearmint (Mentha × gracilis Sole), and Japanese cornmint (M. canadensis L., synonym M. arvensis L.) are grown throughout the world for the production of EOs and for fresh or dried herbage.4,5 The EOs of these mints are used as aromatic agents in products such as chewing gum, toothpaste, and mouthwash as well as in pharmaceuticals and chemicals used in confectionaries, aromatherapy, antimicrobials, and in eco-friendly pesticides.5 The northwestern and midwestern regions of the U.S. are the major producers of peppermint and spearmint.6,7 Currently, there is no production of Japanese cornmint in the U.S., which is a major importer of the commodity. Japanese cornmint is the only commercially viable source of crystalline menthol, which is used extensively in the pharmaceutical, food, flavor, and fragrance industries.8,9 This crop produces marketable oil in addition to menthol.10−13 Previous field studies in Mississippi and in Wyoming demonstrated that Japanese cornmint can be a viable crop under a wide range of growing conditions, from the southeastern U.S. to more northern climates and higher elevations, as in northern Wyoming. These recent studies have findings congruent with those on Japanese cornmint grown in areas north of Mississippi. For example, Murray et al.14 reported good growth and composition of Japanese cornmint in Indiana (41°39′ N lat) and in Michigan (42°36′ N lat). Japanese cornmint also thrives in Bulgaria (42°08′ N lat).15−17 These studies clearly demonstrated that Japanese cornmint could be successfully grown as a perennial crop across the U.S. Interest in sweet sagewort (Artemisia annua [Asteraceae]) increased dramatically after Chinese researchers discovered antimalarial properties of this plant in 1969.18 The antimalarial activity of A. annua has been attributed to artemisinin, which was isolated from the plant in 1972.19 With an estimated 500 million people infected with malaria per year, there is tremendous interest in high-level production platforms for this antimalarial agent. According to the World Health Organization (WHO), in 2015 there were 214 million people infected with malaria and 438 000 malaria deaths.20 Currently, A. annua is the only commercial source of artemisinin, used as a natural antimalarial medicine. For that reason, large-scale

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MATERIALS AND METHODS

Field Study. Field experiments were conducted at the University of Wyoming Sheridan Research and Extension Center in the 2011 and 2012 cropping seasons for five crops species: peppermint (Mentha × piperita L.) “Black Mitcham”, “Scotch” spearmint (M. × gracilis Sole.) “Scotch”, Japanese cornmint (M. canadensis L.) “Arvensis II”, sweet sagewort (Artemisia annua L.), and switchgrass (Panicum virgatum L.) “Nebraska 28”.35 Experimental factors were N-NO3 application at four rates (0, 60, 120, and 180 kg ha−1) and irrigation at two levels (irrigated and reduced-irrigation). The species selection and N application rates were based on data from our experiments on peppermint, spearmints, Japanese cornmint,6,7,10,11,36 and the reported research on switchgrass.30,37 All plants were started at the same time. Peppermint, spearmint, Japanese cornmint, and switchgrass are perennials (and they perennate very well in conditions found in northern Wyoming and northern Mississippi). Therefore, we transplanted them once, in spring of 2011. Sweet sagewort (A. annua) was grown as an annual crop, with seedling production in a greenhouse, followed by transplanting in the field, and therefore, it was transplanted twice, in the spring of 2011 and the spring of 2012. Field Experimental Design. We used a split-plot field design, where within each of the three blocks, irrigation (irrigated and reduced irrigation) was used as the whole-plot factor because irrigation is the more difficult of the factors to randomize. The four N rates were randomly assigned to the subplots within each whole plot (irrigation level). For each of the five crop species, this design of 3 blocks, 2 levels of irrigation, and 4 N rates had 24 experimental units (subplots of size 4 × 6 m2). B

DOI: 10.1021/acs.jafc.7b04594 J. Agric. Food Chem. XXXX, XXX, XXX−XXX

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Journal of Agricultural and Food Chemistry Plant Responses and Other Measured Indices. Fresh and dry matter yields of the EO crops and switchgrass, EO content, EO profile, and biomass quality indices with respect to ethanol production were measured as response variables. The biomass production was determined at harvest; both fresh and air-dried biomass were recorded. Extraction of Essential Oil. EO content of EO crops was estimated following a steam-distillation protocol described previously.6,7,10,38 Briefly, for each crop, a sample of 500 g fresh biomass (leaves, stems, and flowers) was steam-distilled for 1 h using 2-L steam-distillation units (Hearthmagic, Rancho Santa Fe, CA). After distillation, resultant oil mass was calculated on a biomass basis. The EO composition was determined following gas-chromatography (GC) analyses described below. Gas Chromatography Flame Ionization Analysis. The chemical standards and EOs were analyzed on a Varian (Palo Alto, CA) CP-3800 GC equipped with a DB-5 column (30-m by 0.25 mm fused silica capillary column, film thickness of 0.25 mm). The following conditions were used: injector temperature, 240 °C, column temperature 60 to 120 °C at 3 °C/min followed by 120 to 240 at 20 °C/min then held at 240 °C for 5 min; carrier gas, He; injection volume, 1 μL (split on FID, split ratio 20:1). FID temperature was 300 °C. Commercial standards of (−)-carvone, (R)-(+)-limonene, (−)-menthol, (−)-menthone, and (+)-menthofuran were purchased from Fluka (Buchs, Switzerland). With five concentration points, an external standard least-squares regression was performed for quantification. All standards were used to formulate separate calibration curves using FID response data. Linearity was imposed by using response factors and regression coefficients independently. Response factors were calculated using the equation RF = DR/C, where DR was the detector response in peak area (PA) and C was the standard concentration. The chromatograms of each of the EO samples from the field experiments and the commercial mint oil samples were compared with the chromatograms from standard injections. The target peaks were confirmed by retention time. Confirmed integrated peaks were then used to determine the percentage of each chemical constituent in the EO. The RF of the target chemical constituent was used to determine the individual analyte percentage for each sample using the equation [(PA/RF)/C] × 100 = % analyte in the oil on a wt (analyte)/wt (oil) basis. Quantitative Saccharification, Ethanol Fermentation, and High Performance Liquid Chromatography Analysis. We analyzed biofuel production from biomass using bench-scale simultaneous saccharification and fermentation (SSF) methods developed by Mielenz et al.39 for soybean and subsequently adapted for switchgrass.40 In addition to several switchgrass and poplar studies, these methods were employed in a related study by our team2 to quantify ethanol production from biomass samples of various species and environmental treatments. Each biomass sample was oven-dried at 40 °C for 96 h and homogenized in a Wiley mill with a 0.8 mm screen. No pretreatment was used prior to SSF. We used 70 mL resealable fermentation vessels, with each containing 20 mL total reaction volume. The volume reactions contained 15% biomass by weight, 50 mM citrate buffer, 0.063 mg/mL streptomycin, and 1.5% (v/v) Saccharomyces cerevisiae D5A (ATCC number 200062) grown in YEPD medium to stationary phase. Accellerase 1500 (Genencor) was loaded at 15 filter paper units per gram of cellulose. Vessels were weighed and left to shake in 37 °C incubators for 2 weeks. Each vessel was weighed at 1, 2, 3, 4, 9, 12, and 15 days by piercing the rubber top with a needle and weighing. Weight loss was stoichiometrically linked to conversion of sugars to ethanol to gauge the rate of ethanol production. At the end of the 2 weeks, samples of the fermentation supernatant were centrifuged, filtered, and acidified to quantify ethanol and acetic acid content using HPLC analysis.41 Statistical Analyses. The effect of irrigation and N rate on biomass yield, ethanol (cellulose and biomass), and oil content and oil yield for each crop, and on the concentrations of carvone, limonene, and menthone for “Scotch” Spearmint; menthol, menthone, and menthofuran for Japanese cornmint and Peppermint were determined using a Split-plot design (Irrigation as the whole plot factor, and N

rate as the subplot factor) model. The model for Japanese cornmint, spearmint, and peppermint crops was modified to include growth year as a factor and the other effects of interest nested in it because the same plants were used in both years (2011 and 2012) of the experiments; they are all perennials. For the other crops in which new plants were planted in each year, combinations of the original 3 blocks and the two years were used as blocks in the split-plot design. The ANOVA was completed using the Mixed Procedure of SAS,42 and further multiple means comparison was completed when marginally significant (0.05 < p-value < 0.1) or significant (p-value < 0.05) effects were found by comparing the least-squares means of the corresponding combinations of the factors. Letter groupings for the two irrigation levels, and the 4 N rates were generated using 5% level of significance, but a 1% level of significance, instead of 5%, was used for the interaction effect of irrigation and N rate to protect overinflation of Type I experiment-wise error rate. For each model, the validity of model assumptions was verified by examining the residuals as described in Montgomery.43

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RESULTS AND DISCUSSION The average moisture content at harvest for each crop when irrigated and not-irrigated, respectively, was as follows: 72% and 70% for Japanese cornmint; 77% and 74% for spearmint; 72% and 72.7% for peppermint; 62% and 60% for sweet sagewort. Effects on Biomass Yields, Oil Content, and Oil Yield. The factors did not affect the sweet sagewort biomass yield, oil content, or yield, whereas the irrigation by N rate interaction was marginally significant (p = 0.079) on switchgrass biomass (Table 1). The overall mean sweet sagewort biomass yield was Table 1. ANOVA P-Values for Main and Interaction Effects of Irrigation (Irr) and N on Fresh Biomass of Sweet Sagewort (Artemisia annua) and Switchgrass (Panicum virgatum) Crops artemisia

switchgrass

SVa

biomass

EO content

oil yield

biomass

Irr N Irr × N

0.118 0.491 0.494

0.100 0.368 0.775

0.991 0.127 0.772

0.399 0.372 0.079b

a

SV = Source of variation. bSignificant or marginally significant effects that need multiple means comparison are shown in bold face.

11 867 kg ha−1, oil content was 0.34%, and oil yield was 39.7 kg ha−1. Irrigation within year was significant for Japanese cornmint biomass, oil content, and oil yield and for peppermint biomass (Table 2). The growth year had significant effect on all responses except for the EO content of Japanese cornmint. The N rate within a year was significant for biomass and oil yield of Japanese cornmint and spearmint, for peppermint biomass, and oil content, whereas the interaction of irrigation by N rate was significant for oil content of spearmint and marginally significant (p = 0.072) for peppermint oil yields (Table 2). Overall, switchgrass biomass yields did not increase with N rates above 60 kg ha−1 (Table 3). Reduced irrigation did not influence switchgrass biomass yields, most probably due to its deep root system. The spearmint oil content varied between 0.3 and 0.51% of fresh biomass, which is typical for the oil content for this mint species7 (Table 3). In 2011, peppermint oil yields were not affected by the N rate and were relatively low in comparison to the yields in 2012. The difference in peppermint yields between the two years was due to the fact C

DOI: 10.1021/acs.jafc.7b04594 J. Agric. Food Chem. XXXX, XXX, XXX−XXX

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Table 2. ANOVA P-Values for Effect of Year and Main and Interaction Effects of Irrigation (Irr) and N Nested in Year on Fresh Biomass, EO Content (EO), and Oil Yield of Japanese Cornmint (Mentha canadensis) cv “Arvensis II”, Spearmint (Mentha × gracilis) cv “Scotch”, and Peppermint (Mentha × piperita) cv “Black Mitcham” “Scotch” spearmint

Japanese cornmint a

peppermint

SV

biomass

EO

oil yield

biomass

EO

oil yield

biomass

EO

oil yield

year Irr(year) N(year) Irr × N(year)

0.001 0.001b 0.002 0.150

0.939 0.020 0.082 0.401

0.001 0.035 0.001 0.350

0.001 0.133 0.001 0.451

0.001 0.002 0.031 0.030

0.001 0.627 0.047 0.378

0.001 0.001 0.019 0.121

0.038 0.237 0.033 0.455

0.001 0.087 0.212 0.072

a

SV = Source of variation. bSignificant or marginally significant effects that need multiple means comparison are shown in bold face.

Table 3. Mean Switchgrass (Panicum virgatum) Fresh Biomass (kg ha−1), “Scotch” Spearmint (Mentha × gracilis) EO Content (% Oil in Fresh Biomass) in Each of 2011 and 2012, and Peppermint (M. × piperita) Oil Yield (kg ha−1) in Each of 2011 and 2012 Obtained from the Eight Combinations of Irrigation (Irr) and N Rates switchgrass

spearmint

peppermint

N (kg ha−1)

irrigation

biomass

EO 2011

EO 2012

oil 2011

oil 2012

0 60 120 180 0 60 120 180

irrigated irrigated irrigated irrigated reduced Irr reduced Irr reduced Irr reduced Irr

373ba 945ab 1517ab 1580ab 1903ab 2127a 740b 1990ab

0.383bcd 0.446ab 0.409bcd 0.421bc 0.450ab 0.421bc 0.509a 0.401bcd

0.336de 0.356cde 0.343de 0.303e 0.440ab 0.405bcd 0.360cde 0.347de

24.9d 26.2d 28.7d 29.8d 22.1d 30.9d 31.2d 34.8d

68.5c 107.8a 74.0c 95.2ab 76.5bc 70.6c 76.1bc 74.5bc

a

Within each crop, means sharing the same letter are not significantly different.

Table 4. Mean Japanese Cornmint (Mentha canadensis) cv. “Arvensis II” Fresh Biomass (kg ha−1), EO Content (EO; %), and Oil Yield (kg ha−1), “Scotch” Spearmint (M. × gracilis) Fresh Biomass (kg ha−1) and Oil Yield (kg ha−1), and Peppermint (M. × piperita) Fresh Biomass (kg ha−1) and EO Content (%) Obtained from the Two Irrigation (Irr) Levels or Four N Rates within Each of 2011 and 2012 factor levels year Irrigation irrigated reduced Irr irrigated reduced Irr N (kg ha−1) 0 60 120 180 0 60 120 180

Japanese cornmint

spearmint

biomass

EO

oil yield

2011 2011 2012 2012

11 732ca 11 676c 42 736a 30 667b

0.365ab 0.351ab 0.327b 0.387a

42.4c 40.7c 140.4a 118.7b

2011 2011 2011 2011 2012 2012 2012 2012

9502d 11 474d 11 835d 14 005d 30 491c 35 600bc 37 285b 43 430a

0.353ab 0.363ab 0.358ab 0.358ab 0.327b 0.395a 0.314b 0.391a

33.7d 40.6d 42.0d 50.1d 98.4c 139.7b 115.5c 164.6a

biomass

peppermint oil yield

biomass

EO

11 589c 12 444c 34 775a 27 245b 7189e 8259e 7873e 9384e 26 754d 30 740c 33 644b 38 831a

29.3c 35.4c 35.1c 38.3c 103.1b 116.4a 117.5a 125.8a

9303c 11 891c 13 097c 13 775c 26 309b 31 194a 32 665a 33 871a

0.258abc 0.242c 0.234c 0.235c 0.278ab 0.287a 0.228c 0.251bc

a

Factor levels whose means do not share the same letter are not significantly different.

that peppermint was transplanted in the spring of 2011, and harvested once during that year, whereas in 2012, peppermint was harvested twice. Peppermint and spearmint are usually grown as perennial crops, and it is worth noting that both mint species survived the Wyoming winters for the duration of the study. The 2012 peppermint biomass yields were comparable to the biomass yields of the same variety (“Black Mitcham”) grown in Mississippi6 (Table 3). As with spearmint and peppermint, the Japanese cornmint biomass yields in 2012 were much higher than the yields in 2011 due to the double harvests in 2012 and single harvest in

2011 (Table 4). Overall, the biomass yields in this study were similar to the biomass yields of the same cultivar grown in Mississippi.10 In 2012, the EO content was higher in reduced irrigation; however, oil and biomass yields were greater when irrigated (Table 4). Overall, the oil content and oil yields of Japanese cornmint in this study were similar to the oil content and yield of the same cultivar grown in Mississippi.10 Nitrogen rates did not significantly affect fresh biomass yields, oil content, and oil yield of Japanese cornmint in 2011, while in 2012 higher N rates resulted in greater yields, with the maximum biomass and oil yields obtained at 180 kg ha−1. D

DOI: 10.1021/acs.jafc.7b04594 J. Agric. Food Chem. XXXX, XXX, XXX−XXX

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Table 5. ANOVA P-Values for Effect of Year and Main and Interaction Effects of Irrigation (Irr) and N Nested in Year on Concentration of Carvone (%), Limonene (%), and Menthone (%) of “Scotch” Spearmint (Mentha × gracilis); Japanese Cornmint (Mentha canadensis) cv. “Arvensis II;” and Peppermint (M. × piperita) spearmint a

Japanese cornmint

peppermint

SV

carvone

limonene

menthone

menthol

menthone

menthofuran

menthol

menthone

menthofuran

year Irr(year) N(year) Irr × N(year)

0.104 0.001 0.006 0.001b

0.001 0.001 0.001 0.016

0.001 0.237 0.085 0.878

0.551 0.039 0.437 0.311

0.001 0.001 0.085 0.299

0.001 0.001 0.089 0.673

0.360 0.089 0.007 0.256

0.002 0.490 0.015 0.368

0.012 0.005 0.070 0.411

a

SV = Source of variation. bSignificant effects that need multiple means comparison are shown in bold face.

Similarly, spearmint biomass and oil yields were not affected by N rates in 2011, whereas, in 2012, the highest biomass and oil yields were obtained at the higher N application rate of 180 kg ha−1 (Table 4). In 2011, peppermint biomass yields were not affected by irrigation; however, in 2012, greater biomass yield was obtained under a complete irrigation schedule (Table 4). Also, in 2011, the peppermint biomass yield and oil content were not affected by the N application rate. However, in 2012, N application resulted in increased biomass yields relative to the unfertilized control. Peppermint oil content was higher in the 0 and 60 kg N/ha and lower in the 120 kg N/ha N rate (Table 4). Effects on Essential Oil Profile. The ANOVA p-values for the effect of growing year, and the main and interaction effects of irrigation and N nested within year on the concentrations (%) of carvone, limonene, and menthone of spearmint EO; menthol, menthone, and menthofuran of Japanese cornmint EO; and menthol, menthone, and menthofuran of peppermint EO are shown in Table 5. The effect of the factors on menthone concentration in spearmint EO was not significant, and the overall mean for menthone was 1.05%. There was a significant interaction effect of irrigation and N on carvone and limonene concentrations for spearmint EO, with ANOVA pvalues of 0.001 and 0.016, respectively. Irrigation had statistically significant effects on menthol, menthone, and menthofuran concentrations for Japanese cornmint EO, with ANOVA p-values of 0.039, 0.001, and 0.001, respectively. The effect of irrigation was also statistically significant on menthofuran concentration for peppermint EO. The N rate effect was statistically significant for menthol and menthone concentrations for peppermint EO. Mean concentrations of carvone and limonene in spearmint EO obtained from the eight combinations of irrigation and N rate within 2011 and 2012 are shown in Table 6. Carvone concentration in spearmint EO ranged from 62.2% to 66.8% in 2011 and from 51.2% to 68.8% in 2012. In 2011, N fertilizer rate and irrigation had statistically similar effects on carvone concentration, but in 2012, the carvone concentration in the spearmint EO was highest when N was applied at 120 kg ha−1 rate under reduced irrigation condition and lowest when N was applied at 120 kg ha−1 and 180 kg ha−1 rates under irrigated condition. In 2011, spearmint EO with the highest limonene concentration of 23% was obtained from plants grown under reduced irrigation condition that received N fertilizer at the rate of 180 kg ha−1. However, EO obtained from plants grown under the irrigated condition and receiving N fertilizer at the rate of either 0 or 180 kg ha−1 and EO from plants grown under reduced irrigation and receiving N fertilizer at the rate of 0 kg ha−1 contained limonene concentrations that were statistically similar to the highest limonene concentration in 2011. In the same year, spearmint EO with the lowest

Table 6. Mean Concentration of Carvone (%) and Limonene (%) from “Scotch” Spearmint (Mentha × gracilis) Obtained from Eight Combinations of Irrigation (Irr) and N Rates within 2011 and 2012 carvone

limonene

N (kg ha−1)

irrigation

2011

2012

2011

2012

0 60 120 180 0 60 120 180

irrigated irrigated irrigated irrigated reduced Irr reduced Irr reduced Irr reduced Irr

66.8aba 63.4ab 62.5b 62.2b 63.8ab 63.3b 64.7ab 64.8ab

65.9ab 65.7ab 52.3c 51.2c 64.0ab 65.8ab 68.8a 65.3ab

21.6abc 19.3d−g 20.3b−e 21.1a−d 21.5a−d 20.3b−e 19.7c−f 23.0a

18.3e−h 18.9e−h 22.1ab 22.6a 18.1fgh 16.9h 17.9fgh 17.3gh

a Within each crop, means sharing the same letter are not significantly different.

limonene concentration of 19.3% was obtained from plants grown under irrigated conditions that received N fertilizer at the rate of 60 kg ha−1. In 2012, spearmint EO with statistically similar limonene concentrations of 22.6% and 22.1% was obtained from plants grown under irrigated condition that received N fertilizer at the rate of 180 kg ha−1 and 120 kg ha−1, respectively. In the same year, limonene concentrations in EOs obtained from spearmint plants grown under the other six combinations of irrigation conditions and rate of N fertilizer were statistically similar. The mean concentrations of menthol, menthone, and menthofuran in Japanese cornmint EO; and menthofuran from peppermint EO obtained from the two Irrigations within 2011 and 2012 are shown in Table 7. Essential oil with 67% menthol, which was the lowest, was obtained in 2011 from Japanese cornmint plants grown under reduced irrigation conditions. Essential oil obtained from plants grown under Table 7. Mean Concentration of Menthol (%), Menthone (%), and Menthofuran (%) from Japanese Cornmint (Mentha canadensis) cv. “Arvensis II”; and Menthofuran (%) from Peppermint (Mentha × piperita) Obtained from Two Irrigations Levels within 2011 and 2012 Japanese cornmint Arvensis II year

irrigation

menthol

2011 2011 2012 2012

irrigated reduced Irr irrigated reduced Irr

69.2aba 67.0b 69.7a 67.5ab

menthone menthofuran 13.9a 12.2b 11.1c 9.4d

4.75d 5.29c 6.28b 6.73a

peppermint menthofuran 15.8b 16.8b 18.3a 16.5b

a

Within each column, means sharing the same letter are not significantly different.

E

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lowest amount ethanol (Table 9) even though the 2012 plants produced more cellulose than plants grown in 2011 under the same conditions (data not shown). There was no statistical difference in the content of peppermint menthol and menthone grown in 2011 and 2012 under the same conditions (Table 4, Table 8), and therefore, these terpenes would not have inhibited yeast growth to result in lower ethanol yield. Indeed, peppermint EO has been shown to induce apoptosis in Saccharomyces.44 There was an increase in the production of ethanol from sweet sagewort in the second year without a concomitant increase in cellulose content and EO yield between years. Sagewort is known to have high antioxidant capacity,24 and environmental conditions can have a significant effect on antioxidant capacity. Changes in the amount of antioxidants present in the biomass could have a protective effect on yeast thereby increasing the efficiency of the fermentation and subsequently the ethanol production. On the basis of the results from this study, the estimated ethanol production in L ha−1 would be as follows: 5932 from sweet sagewort, up to 1064 from switchgrass, 4751 to 21 713 from Japanese cornmint, 3581 to 19 415 from spearmint, and 4648 to 16 932 from peppermint (Table S1). However, switchgrass yields in this study were relatively low; it takes 3 to 4 years for switchgrass to reach its full biomass yield potential. In a review paper on switchgrass biomass yields from 39 field studies across the United States, Wullschleger et al.30 estimated mean yields of 8700 ± 4200 kg ha−1 for upland ecotypes and 12 900 ± 5900 kg ha−1 for lowland ecotypes. Therefore, if we accept mean switchgrass biomass yields of 8700 kg ha−1, then the estimated ethanol yield would be around 4349 L ha−1. Consequently, the range of ethanol yields provided by the novel biofuel crops sweet sagewort, Japanese cornmint, spearmint, and peppermint in this study would be within the range of switchgrass ethanol yields (Table S1). However, caution is advised when comparing 2-year field crop yield data; a longer duration and larger plot sizes would be recommended for an economic feasibility study. Japanese cornmint, spearmint, and peppermint are perennials, usually grown as irrigated crops from 3 to 5 years only because of weed and disease pressures; in certain circumstances, they may be grown for over 12 consecutive years. On the other hand, switchgrass can be grown for 10 or more years as nonirrigated crop in much of the eastern United States.30 Also, while weed control may be an issue in switchgrass during the establishment and first 2 years of growth,45 weed and disease control may be an issue for Japanese cornmint, spearmint, and peppermint during the entire 3 to 5 year period,17 as mint plants are not as competitive as switchgrass or sweet sagewort plants with respect to weeds. Evaluating species for double utilization is a new approach to add value to lignocellulosic feedstock production. The longterm goal of our research is to improve economic, environmental, and agronomic sustainability of feedstocks for sustainable energy production through coupling biofuel feedstock production with the production of high-value natural products with established markets. We evaluated selected crops suitable for use as lignocellulosic feedstocks for ethanol production and for the production of high-value natural products: EOs. Our study and previous reports2 demonstrated that these dual-utilization crops may have importance as supplement feedstock for ethanol production, particularly under irrigation. Such crops and systems may diversify commonly used switchgrass feedstock systems, which may be

irrigated condition in 2011 and under either irrigated or reduced irrigation conditions in 2012 had statistically similar menthol concentrations. Menthone concentration was highest in the EO obtained from Japanese cornmint plants when grown under irrigated condition in 2011 and lowest in the EO obtained from Japanese cornmint plants when grown under reduced irrigation condition in 2012. In contrast, menthofuran concentration in the EO was highest when Japanese cornmint plants were grown under reduced irrigation condition in 2012 and lowest when Japanese cornmint plants were grown under irrigated condition in 2011. In 2012 and under irrigated condition, peppermint EO had the highest and statistically different menthofuran concentration. Menthofuran concentration in peppermint EO was statistically similar for the remaining combinations of growth year and irrigation treatment. The mean concentrations of menthol and menthone in peppermint EO obtained from the four N rates within 2011 and 2012 are shown in Table 8. Peppermint EO with the Table 8. Mean Concentration of Menthol (%) and Menthone (%) from Peppermint (Mentha × piperita) Obtained from Four N Rates within 2011 and 2012 peppermint −1

year

N (kg ha )

menthol

menthone

2011 2011 2011 2011 2012 2012 2012 2012

0 60 120 180 0 60 120 180

40.8aba 40.1ab 39.8ab 36.8bc 42.3a 37.6bc 38.7bc 36.4c

13.6bc 16.3ab 19.7a 16.0abc 10.8c 13.9bc 12.0c 16.5ab

a

Within each column, means sharing the same letter are not significantly different.

highest menthol concentration of 42.3% was obtained in 2012 when plants received N fertilizer at the rate of 0 kg ha−1. Peppermint EO with the lowest menthol concentration of 36.4% was obtained in 2012 when plants received N fertilizer at the rate of 180 kg ha−1. Peppermint EO with the highest menthone concentration of 19.7% was obtained in 2011 when plants received N fertilizer at the rate of 120 kg ha−1 . This highest menthone concentration was not statistically different from the menthone concentration in peppermint EOs obtained in 2011 from plants receiving N fertilizer at the rate of 60 and 180 kg ha−1 and in 2012 from plants receiving N fertilizer at the rate of 180 kg ha −1 . Peppermint EO with the lowest menthone concentration of 10.8% was obtained in 2012 when plants received N fertilizer at the rate of 0 kg ha−1. Ethanol Production. Simultaneous saccharification and fermentation (SSF) was carried out on the biomass to estimate ethanol production for each species under the various field conditions. Mean ethanol yield on a mg/g cellulose basis in 2011 was highest from peppermint grown in reduced irrigation plots that received 180 kg ha−1 N, followed by sweet sagewort that received 180 kg N ha−1, regardless of irrigation (Table 9). In 2012, the mean SSF ethanol yield was highest from sweet sagewort that received 180 kg ha−1 N in plots of reduced irrigation. Interestingly, the peppermint grown in 2012 under reduced irrigation plots with 180 kg ha−1 N rate produced the F

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Table 9. Mean Ethanol Cellulose (mg/g) and Biomass (mg/g) Obtained from Different Crops Where Interaction between Irrigation (Irr = Irrigated, RedIrr = Reduced Irrigation) and N Nested in Year Was Significanta 2011

2012

irrigation

N (kg ha−1)

crop

cellulose

biomass

crop

cellulose

biomass

Irr Irr RedIrr RedIrr Irr Irr RedIrr RedIrr Irr Irr RedIrr RedIrr Irr Irr RedIrr RedIrr Irr Irr RedIrr RedIrr Irr Irr RedIrr RedIrr

0 180 0 180 0 180 0 180 0 180 0 180 0 180 0 180 0 180 0 180 0 180 0 180

JapC JapC JapC JapC Lemo Lemo Lemo Lemo Pepp Pepp Pepp Pepp Scot Scot Scot Scot Swee Swee Swee Swee wheat wheat wheat wheat

363eb 358e 329fg 341f 308hi 317gh 295ijk 263l 248l 261l 259l 501a 332fg 290jk 287k 408c 411c 436b 387d 450b 307hij 281k 361e 147m

90.7d 87.8de 84.0ef 80.8fg 99.0c 102.5ab 100.9bc 105.7a 57.9lm 54.1n 53.5no 64.9j 75.8h 64.8j 77.9gh 71.0i 61.5jkl 55.8mn 63.3jk 61.0kl 78.7gh 71.5i 87.1de 50.0o

JapC JapC JapC JapC Pepp Pepp Pepp Pepp Scot Scot Scot Scot Swit Swit Swit Swit Swee Swee Swee Swee

479c 328g 439d 384e 222l 307hi 193n 147p 334g 259k 211m 259k 176o 299i 312h 275j 304hi 344f 600b 693a

80.7e 62.8ij 73.6g 63.8i 62.7ij 58.2l 64.6i 61.6jk 69.9h 46.1n 60.2k 50.8m 63.9i 72.2g 77.0f 86.6d 88.7c 96.0a 92.2b 87.1cd

JapC = Japanese cornmint (M. canadensis), Lemo = LemonGrass (Cymbopogon f lexuosus), Pepp = Peppermint (M. × piperita), Scot = “Scotch” spearmint (M. × gracilis), Swit = Switchgrass (Panicum virgatum), Swee = Sweet sagewort (Artemisia annua), and wheat (Triticum aestivum L.). b Within each column, means sharing the same letter are not significantly different. a

$15 kg−1, then the potential additional income from Japanese mint would be between $510 and $2460 ha−1 based on its oil yields variation from 34 to 164 kg ha−1. The overall oil yield of A. annua was 39.7 kg ha−1, with import price from Europe being $91 kg−1.47 Therefore, the additional income from Artemisia oil would be around $3613 ha−1. However, the above prices do not include the cost of extraction of the EO, which may vary widely (10−30%) depending on the production facility. Therefore, the above discussion was provided as a guidance and not as economic analyses of coproduction. In summary, results from this study support the potential value of dual-utilization crops in the evolving biofuel industry. The N application rate was generally associated with crop yields; however, switchgrass biomass yields did not increase with N rates above 60 kg ha−1. Japanese cornmint biomass yields ranged from 9500 to 43 430 kg ha−1, with EO content of 0.31 to 0.4%, which resulted in EO yields of 34 to 165 kg ha−1, depending on the year, irrigation, and fertilizer application rates. Peppermint biomass ranged from 9300 to 33 870 kg ha−1, with oil content 0.23 to 0.26%, and oil yields of 25 to 108 kg ha−1. Spearmint biomass yields were 7190 to 33 830 kg ha−1 with oil content of 0.38 to 0.5%, and oil yields of 29.3 to 126 kg ha−1. N rate affected the concentration of EO chemical constituents, specifically carvone and limonene in spearmint, menthol, menthone, and menthofuran in Japanese cornmint, and menthone and menthofuran in peppermint. Overall, the EO chemical compositions were within the industry accepted ranges for the respective species. Japanese cornmint produced more ethanol than spearmint on a dry biomass basis suggesting that Japanese cornmint is more suitable as a lignocellulosic

grown on dryland. There are several advantages of EO crops over many other lignocellulosic species currently under investigation. Crops producing high-value natural products and preparations may foster the development of value-added products, bring new business opportunities to communities, and could be more attractive to growers. In addition, sweet sagewort can provide two natural products; EO and artemisinin, while the remaining biomass has high antioxidant capacity and may be used as feedstock for animal feed or as source for other bioactives for the nutraceutical market.21 Another advantage is that crop biomass is processed with heat (the EO is extracted by steam-distillation), which may mitigate biomass recalcitrance.3 Estimated Value of Coproduction. Overall, peppermint oil yields varied from 22 to 107 kg ha−1, spearmint oil yields were between 29.3 and 126 kg ha−1, and Japanese cornmint oil yields were from 34 to 165 kg ha−1 for different years and N rates. With recent (2016−2017) peppermint and spearmint oil prices at $45 (USD) and $48 kg−1, respectively, an additional potential farm income of $1055 to $5132 ha−1 could be generated from peppermint, while the potential income from spearmint oil would be $1309 to $5580 ha−1. The current peppermint and spearmint oil prices were taken from the USDA NASS.46 There is no current commercial production of Japanese cornmint in the U.S., although several previous studies have shown feasibility for the Midwest, Wyoming, and Mississippi.6,7,12,14 Japanese cornmint oil prices were obtained from an Indian export and import data set,47 where oil export prices varied from $15 to $25 kg−1 and import prices varied between $24 and $35 kg−1. If we take the lowest export price of G

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(5) Lawrence, B. M. Mint: The Genus Mentha; CRC Press: Boca Raton, FL, 2007; p 556. (6) Zheljazkov, V. D.; Cantrell, C.; Astatkie, T.; Ebelhar, M. W. Peppermint productivity and oil composition as a function of nitrogen, growth stage, and harvest time. Agron. J. 2010, 102 (1), 124−128. (7) Zheljazkov, V. D.; Cantrell, C. L.; Astatkie, T.; Ebelhar, M. W. Productivity, oil content and composition of two spearmint species in Mississippi. Agron. J. 2010, 102 (1), 129−133. (8) Clark, G. S. An aroma chemical profile: Menthol. Perfum. Flavor. 1998, 23, 33−46. (9) Chand, S.; Patra, N. K.; Anwar, M.; Patra, D. D. Agronomy and uses of menthol mint (Mentha arvensis) - Indian perspective. Proc. Ind. Nat. Sci. Acad. B 2004, 70, 269−297. (10) Zheljazkov, V. D.; Cantrell, C. L.; Astatkie, T. Study on Japanese cornmint in Mississippi. Agron. J. 2010, 102 (2), 696−702. (11) Zheljazkov, V. D.; Cantrell, C. L.; Astatkies, T. Yield and composition of Japanese cornmint fresh and dry material harvested successively. Agron. J. 2010, 102 (6), 1652−1656. (12) Zheljazkov, V. D.; Cantrell, C. L.; Astatkie, T.; Jeliazkova, E. Mentha canadensis L., a subtropical plant, can withstand first few fall frosts when grown in northern climate. Ind. Crops Prod. 2013, 49, 521−525. (13) Shiwakoti, S.; Sintim, H. Y.; Poudyal, S.; Bufalo, J.; Cantrell, C. L.; Astatkie, T.; Jeliazkova, E.; Ciampa, L.; Zheljazkov, V. D. Diurnal effects on Mentha canadensis oil concentration and composition at two different harvests. HortScience 2015, 50 (1), 85−89. (14) Murray, M. J.; Faas, W.; Marble, P. Chemical composition of Mentha arvensis var. piperascens and four hybrids with Mentha crispa harvested at different times in Indiana and Michigan. Crop Sci. 1972, 12, 742−745. (15) Zheljazkov, V. D.; Margina, A. Effect of increasing doses of fertilizer application on quantitative and qualitative characteristics of mint. Acta Hortic. 1996, 426, 579−592. (16) Zheljazkov, V. D.; Topalov, V.; et al. Comparison of three methods of mint propagation and their effect on the yield and fresh material and essential oil. J. Essent. Oil Res. 1996, 8, 35−45. (17) Zheljazkov, V. D.; Topalov, V.; et al. Effect of mechanical and chemical weed control on the growth, development and productivity of Mentha piperita and M. arvensis var. piperascens grown for planting material. J. Essent. Oil Res. 1996, 8, 171−176. (18) Hsu, E. The history of qing hao in the Chinese material medica. Trans. R. Soc. Trop. Med. Hyg. 2006, 100, 505−508. (19) Ferreira, J. F. S.; Laughlin, J. C.; Delabays, N.; de Magalhães, P. Cultivation and genetics of Artemisia annua L. for increased production of the antimalarial artemisinin. Plant Genet. Resour. 2005, 3 (2), 206−229. (20) World Health Organization (WHO). Malaria; WHO, 2017. http://www.who.int/gho/malaria/en/ (accessed September 2017). (21) Ferreira, J. F. S.; Zheljazkov, V. D.; Gonzalez, J. M. Artemisinin concentration and antioxidant capacity of Artemisia annua distillation byproduct. Ind. Crops Prod. 2013, 41, 294−298. (22) Juteau, F.; Masotti, V.; Bessiere, J. M.; Dherbomez, M.; Viano, J. Antibacterial and antioxidant activities of Artemisia annua essential oil. Fitoterapia 2002, 73, 532−535. (23) Tripathi, A. K.; Prajapati, V.; Aggarwal, K. K.; Khanuja, S. P. S.; Kumar, S. Repellency and toxicity of oil from Artemisia annua to certain stored-product beetles. J. Econ. Entomol. 2009, 93, 43−47. (24) Ferreira, J. F. S.; Luthria, D. L.; Sasaki, T.; Heyerick, A. Flavonoids from Artemisia annua L. as antioxidants and their potential synergism with artemisinin against malaria and cancer. Molecules 2010, 15, 3135−3170. (25) Allen, P. C.; Lydon, J.; Danforth, H. D. Effects of components of Artemisia annua on coccidia infections in chickens. Poult. Sci. 1997, 76, 1156−1163. (26) Brisibe, E. A.; Umoren, U. E.; Brisibe, F.; Magalhäes, P. M.; Ferreira, J. F. S.; Luthria, D.; Wu, X.; Prior, R. L. Nutritional characterization and antioxidant capacity of different tissues of Artemisia annua L. Food Chem. 2009, 115, 240−1246.

feedstock. Estimated ethanol production from sweet sagewort, Japanese cornmint, spearmint, and peppermint were within the range of ethanol production from switchgrass. Additional incomes from EO sales would be $1055 to $5132 ha−1 from peppermint, $1309 to $5580 ha−1 from spearmint, $510 to $2460 ha−1 from Japanese cornmint, and around $3613 from sweet sagewort, which would make these EO crops attractive to the growers. Further longer term and larger-plot research would be recommended to expand and support these findings.

■

ASSOCIATED CONTENT

S Supporting Information *

The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acs.jafc.7b04594. Estimated ethanol yield in mL ha−1 and in US gallons ha−1 for different sweet sagewort, switchgrass, Japanese cornmint “Arvensis II”, “Scotch” spearmint, and peppermint depending on treatments (PDF)

■

AUTHOR INFORMATION

Corresponding Author

*E-mail: [email protected]; Valtcho.pubs@ gmail.com. Phone: 541-737-5877. ORCID

Valtcho D. Zheljazkov: 0000-0002-3479-9653 Funding

This research was conducted with support from the SunGrant project “Development of a Production System for Emerging Feedstock with Double Utilization,” awarded to the corresponding author, Dr. Valtcho D. Jeliazkov (Zheljazkov), as well as a USDA Hatch grant to Neal Stewart. Notes

The authors declare no competing financial interest.

■

ACKNOWLEDGMENTS The authors would like to acknowledge Dan Smith at the University of Wyoming Sheridan Research and Extension Center for the technical assistance. We would also like to acknowledge Ben Wolfe from University of Tennessee, Knoxville, for the contributions to the fermentation experiments as well as Sujata Agarwal and the University of Tennessee Institute of Agriculture Genomics Hub for the high performance liquid chromatography analyses.

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REFERENCES

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