Abstract
Given the mandated increases in fuel production from alternative sources, limited high-quality production land, and predicted climate changes, identification of stress-tolerant biomass crops will be increasingly important. However, existing literature largely focuses on the responses of a small number of crops to a single source of abiotic stress. Here, we provide a much-needed review of several types of stress likely to be encountered by biomass crops on marginal lands and under future climate scenarios: drought, flooding, salinity, cold, and heat. The stress responses of 17 leading biomass crops of all growth habits (e.g., perennial grasses, short-rotation woody crops, and large trees) are summarized, and we identify several that could be considered “all purpose” for multiple stress types. Importantly, we note that some of these crops are or could become invasive in some landscapes. Therefore, growers must take care to avoid dissemination of plants or propagules outside of cultivation.
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Introduction
Production of second-generation biomass crops is growing in the USA, principally driven by the federal mandate [1] that requires novel feedstocks to offset greenhouse gas emissions from fossil fuels and minimize or avoid any negative impact on the global food supply. Thus, there has been much exploration into biomass crops that are capable of fast growth and high yields on land not suited to food production. Land that is unsuitable for traditional row crops, generally referred to as “marginal” land, may be appropriate for grazing or other uses [2], including biomass crop production. Use of marginal lands for bioenergy production could decrease land-use competition between energy and food crops and ameliorate land-use change associated with biomass crop expansion [3]. However, the fact that this land cannot economically support traditional crop production suggests it is suboptimal in some way and, therefore, may be associated with abiotic stress factors that must be overcome by any crop grown thereon. In addition, the definition of marginal land can also include land with slightly less severe abiotic stressors, potentially supporting some traditional row crops; however, even mild stress may cause those crops to perform suboptimally, causing farmers to operate at a loss, particularly if climate predictions increase the severity of abiotic stress. This paper explores abiotic stressors that may be encountered by biomass crops grown on marginal lands or under changing climate conditions and provides a breadth of options for selecting crops that can tolerate particular types of abiotic stress.
The Asia-Pacific Economic Cooperation (APEC) estimates that marginal lands make up approximately 400 million hectares across Asia, the Pacific Islands, Australia, and North America [4]. Other estimates put the global marginal land area anywhere from 1100 [5] to 6650 million hectares [2], depending on the parameters used to describe marginal (e.g., “non-favored agricultural land,” “abandoned or degraded cropland,” or arid, forested, grassland, shrubland, or savanna habitats). The potential area available in the USA for cellulosic biomass crops and low-input, high-diversity native perennial mixtures ranges from 43 to 123 million hectares [5, 6]. The differences in these estimates reflect the inconsistencies in the usage of the term “marginal land,” despite its common use in the bioenergy industry and literature [5, 7, 8]. Marginal lands are often described as degraded lands that are unfit for food production and/or of some ambiguously poor quality and are often termed unproductive [7]. Unproductive soils are characterized by unfavorable chemical and/or physical properties that limit plant growth and yield, including low water and nutrient storage capacity, high salinity, toxic elements, and poor texture [4, 9]. Further difficulties encountered in marginal landscapes include shallow soil depth due to erosion, poor drainage, low fertility, steep terrain, and unfavorable climate [2]. Despite the poor quality of marginal land and the potential problems it could present for its production, biomass is unlikely to be grown on high-quality land that is economically viable for traditional crops [7].
Climate change will exacerbate the issue of land marginalization and degradation [10, 11]. It has been predicted that negative impacts of climate change will increase over the next 25 years, with longer growing seasons (frost-free periods), increasing extreme precipitation events (both flooding and drought), fewer chilling hours, and a greater number of hot nights projected for most growing regions of the country [11]. Because these changes are projected to occur to a greater extent in certain regions of the country [11], crop production—potentially including biomass crops on marginal lands—may shift to novel regions where different stressors are present or growers may shift to different production systems. For example, to escape the predicted hot nights in the southeast, growers may shift to more northern regions where precipitation may be less frequent [11]. These changes will—and already do—directly affect the physiology and reproductive development of many crop plants, including first generation biomass crops [12, 13]. Therefore, it will be important to select the most tolerant crops suitable for future climate scenarios [14].
In this work, we review and summarize the literature on the effects of three sources of abiotic stress that may be common to marginal lands—moisture, salinity, and temperature—and identify biomass crops that display tolerance to these types of stress. Our discussion is geared toward the USA but could be applied to similar circumstances in other regions. Although most plant matter has the potential to be converted into energy, we focus on the promising non-food crops identified in the US Department of Energy’s Billion Ton Update [15] and in novel research programs that are investigating the next wave of potential biomass crops. Each of the crops in our report has been the subject of detailed study, investigating ecological, agronomic, physiological, or molecular responses to one or more stressors. Our goal is not to restate the detailed results of these studies, but instead to provide a comprehensive review of the effects of multiple stressors in the context of bioenergy production and a useful guide for growers to choose the best biomass crop for stressful growing conditions.
Moisture Stress
Framing the Issue
Water scarcity is the most limiting environmental factor to crop growth and yield [16] and is a major factor in the categorization of lands as “marginal” or unsuitable for crop production [17]. Drought is a prolonged period of time without significant precipitation, resulting in a shortage of water [18]. More frequent, severe, and longer-than-average duration of drought is predicted in the USA and globally due to changing climate conditions [11, 14, 19–21]. In addition to large-scale climatic factors, effects of drought can be exacerbated by local or regional factors including aridity, topography, or soil conditions [22]. Marginal lands are often characterized by sloped topography or eroded soils with little moisture-holding capacity [23]; therefore, the effects of drought-inducing climate changes have the potential to be stronger in these landscapes [10, 11]. For example, Lee et al. [24] observed that drought effects on biomass yield of perennial grasses varied according to topography, with greater effects at higher elevations.
Conversely, soils with poor drainage—and with the potential for flooding or waterlogging—are also typical of numerous marginal landscapes [23]. Many native Midwestern soils were poorly drained and unsuitable for annual crop production before an extensive network of tile drains were installed [23]. However, marginal land not in crop production is unlikely to have been tiled and therefore may be subject to problems associated with waterlogging in wet years or on wet sites. However, poor drainage is not only an issue in the Midwest. More than half of the freshwater wetlands in the USA have been drained or filled for agricultural use [25], and some have been or will be abandoned due to insufficient drainage [26]. Because rainfall events have become heavier and more frequent in recent years—and this trend is predicted to continue [11]—poorly drained soils can quickly become flooded or waterlogged.
Effects of Moisture Stress
Tissue expansion, dependent on cellular turgor pressure, is strongly tied to water availability, and plant growth is therefore limited by water deficits. This impacts germination, seedling growth, and stand establishment, and leads to reduced plant height, leaf area (both in size and number), and crop yield [27]. In adult plants, drought effects on shoot tissue expansion are generally more severe than in roots, which are less sensitive to water deficit stress [28]. Cellular dehydration inhibits photosynthesis under severe drought stress, resulting in reduced levels of carbon assimilation [29, 30]. Continued respiration under dry conditions can lead to a negative carbon balance in drought-affected plants [27]. This is due to the combined effects of decreased carbon assimilation overall and decreased translocation of photosynthates from leaves through phloem, which requires maintenance of cellular turgor [29]. Transpiration is inhibited in most plants under water deficit stress, due to stomatal closure and xylem cavitation, and this can lead to decreased nutrient uptake [27]. Prolonged periods of stomatal closure can also lead to heat stress (see Moisture Stress Tolerance Strategies below), as plants cannot employ transpirational cooling to reduce heat load. Reproductive structures, including both flowers and fruits, can also be severely affected by water deficit stress, due to reductions in the availability of photosynthates, inability to achieve turgor required for cellular expansion and tissue growth, and disruption in the activity of key enzymes [27]. Additional effects of water deficit have been described, but the above represent the most common impacts on plant growth and functioning.
Flooding primarily affects plants by reducing soil oxygen availability and therefore reducing root respiration [31]. Water replaces oxygen in soil pores, causing hypoxic or anoxic conditions that not only limit the diffusion of oxygen but also promotes the growth of anaerobic bacteria, which produce toxic compounds that could harm plants [29]. Many sensitive plants respond to waterlogged conditions by closing stomata, which reduces whole-plant water potential gradients and xylem transport [31, 32]. Further, waterlogged roots are unable to absorb nutrient ions, leading to nutrient deficiency symptoms in shoot tissue [29]. Similarly, the rate of photosynthate transport from leaves to roots can decrease by more than half within 30 min of flooding; this photosynthetic inhibition is not well understood, but it is thought to be linked to the toxic products of anaerobic respiration [32]. Plants sensitive to flooding are severely damaged within hours, with decreased growth, survival, and yield [29]. Plants with moderate flood tolerance are able to withstand anoxic conditions temporarily, although some can be damaged after multiple days of waterlogging. Strategies of highly flood-tolerant taxa will be discussed further below.
Moisture Stress Tolerance Strategies
True drought tolerance is the ability to grow, flower, and produce favorable yields under suboptimal water supply [27]. There are three major types of drought tolerance: drought escape, desiccation postponement or avoidance, and desiccation tolerance [29]. The life cycles of drought escapers are completed during wet seasons or while well watered [27, 29], and therefore, these plants do not necessarily possess physiological adaptations to drought stress. Desiccation postponers/avoiders maintain tissue hydration under drought conditions, while plants tolerant of desiccation perform metabolic functions even while dehydrated [29]. Several morphological, molecular, and physiological mechanisms, including alteration of root/shoot ratios, osmotic adjustment, and production of dehydrin proteins, are important in drought tolerance and are covered elsewhere in comprehensive reviews [e.g., 33–37]. While we will not detail these mechanisms here, it is important to note that plants employing the three different photosynthetic pathways (C3, C4, and crassulacean acid metabolism (CAM)) show inherent drought tolerance and water use efficiency differences.
Stomatal closure helps to reduce the ratio of transpiration-to-water uptake and delay dehydration [28]. Species with C4 and CAM photosynthetic pathways benefit from fixing a high rate of CO2 with partially or fully closed stomata [38–40] and are generally considered more drought tolerant than most C3 species. Plants employing C4 photosynthesis also have higher water use efficiency (WUE), as well as increased biomass production in both ideal and drought conditions [41, 42]. The extensive root systems of perennial C4 grasses also maximize water uptake from the soil [43]. CAM plants take up CO2 at night, making them better suited for chronically dry environments than C3 and C4 plants [44]. It has been estimated that CAM crops require only 20 % of the irrigation of the most efficient C3 and C4 crops [44].
Mechanisms for flood tolerance, including hormonal, molecular, and physiological mechanisms, have been reviewed in detail by a number of authors [e.g., 45–47]. Major morphological adaptations to flooding include production of aerenchyma tissue, enlargement of stem lenticels, and development of new roots [31]. Movement of oxygen to roots through aerenchyma not only allows root cells to reestablish aerobic respiration but also decreases toxic compounds outside of the root cortex through diffusion into soil and oxidation of reduced soil ions [32]. Formation of adventitous roots can compensate for decreased absorptive capacity or death and decay of existing roots and can lead to reopening of closed stomata [32].
Drought- and Flood-Tolerant Biomass Crops
As discussed previously, we searched for stress tolerance literature relating to several promising biomass crops being cultivated or developed in the USA currently. It is important to note that, as a consequence, our list of tolerant biomass crops should not be considered exhaustive. In addition, many of the available studies were designed to test relative tolerance among varieties or species. Thus, this analysis is not meant to provide absolutes or guarantee stress tolerance under every circumstance. However, our analysis still represents a more comprehensive review of multiple biomass crops and multiple stressors than currently exists. Table 1 details evidence of drought stress tolerance, and Table 2 details evidence of flooding tolerance in 17 biomass crops.
Of the 17 crops evaluated, six species were highly drought tolerant, and others had drought-tolerant species or genotypes within the genus (Table 1). Several of the most tolerant taxa were C4 perennial grasses, including Andropogon gerardii, Pennisetum purpurem, and Sorghum bicolor. For example, Sorghum bicolor is highly productive in dry African climates [109], likely due to the high WUE and large root systems found in many cultivars [110]. Panicum virgatum shows low tolerance during establishment [64], possibly because of lower water use efficiency related to lower carbon assimilation during drought [111]. Although when drought was imposed after establishment, Panicum virgatum plants appeared to be drought hardy [64, 65]—particularly upland cytotypes [67, 68]. In addition, a long-term field evaluation of biomass crops (34 herbaceous taxa assessed over 10 years across a wide range of soil and sites) indicated that Panicum virgatum and certain Sorghum bicolor varieties outperformed other crops under drought conditions [112]. As expected, the one CAM crop we included in our database, Agave spp., showed high drought tolerance due to several morphological and physiological adaptations to the arid climates in which it evolved [44, 48]. A number of woody crops were also drought tolerant, depending on genotype. These included several Eucalyptus species, Jatropha curcas, several Pinus species, Populus hybrids, Robinia pseudoacacia, and several Salix species (Table 1). Several studies identified particular genotypes that were more drought tolerant than the wild type (e.g., sugarcane genotype Co 99004) or identified congeners with higher tolerance than the target crop (e.g., Helianthus argophyllus) (Table 1). This information could potentially be used in future breeding programs to develop more tolerant biomass crops for marginal lands.
Several species and genotypes have evolved in wetland conditions and are moderately to strongly tolerant of flooded conditions (Table 2). For example, because Spartina pectinata is native to North American moist prairies, marshes, and drainage ways [113], it can be grown in soils that are too wet to grow corn, big bluestem, or switchgrass [114, 115], although lowland types of switchgrass are tolerant of flooded conditions [64, 68]. Other flood-tolerant crops include Eucalyptus camaldulensis, Miscanthus × giganteus, several hybrid Populus spp., Pinus elliotti, and Sorghum bicolor (Table 2). Eucalyptus camaldulensis formed adventitous roots and maintained moderate growth rates in flooded conditions [32], while the most tolerant Populus hybrids allocated more carbon to belowground structures, formed adventitious roots, and maintained stomatal function, net photosynthetic rate, and relative growth rate [116]. Again, novel genotypes of traditional crops showed greater flood tolerance than their parents, highlighting the potential for improvement in these and other taxa (Table 2). One example is a Japanese sugarcane (Saccharum spp.) hybrid which showed an increase in dry biomass in response to flooding. Continuous flooding is often deleterious to sugarcane growth [117], but because it is typically cultivated in wet tropical regions, it is important to develop varieties that are productive under flooded conditions.
Several of the focal biomass crops have not been the subject of study related to flooding tolerance (i.e., “N/A” in Table 2), but this lack of evidence should not be interpreted as flood sensitivity for these taxa.
Salt Stress
Framing the Issue
Salinity is a major environmental stressor affecting arid, semi-arid, and irrigated land worldwide [118, 119] and contributing to the abandonment or marginalization of land [118]. Salinization can occur naturally, through aerosolization, deposition, or contact with sea salts in coastal locations [120], or through proximity to saline seeps, shallow water tables, and degradation of parent rock materials inland [121, 122]. Alternatively, so-called “secondary salinization” occurs anthropogenically, as a result of replacing deep-rooted native vegetation with shallow-rooted crops and pasture or from adding irrigation water to soils [120, 123]. Both actions can result in changes to water table depth, causing salts to accumulate in the root zone as excess water evaporates from the soil surface [120, 123]. While some dissolved salts can improve soil texture, an excess of salts, including sodium, can cause soil dispersion and reduced permeability [124]. Salt accumulation can render soil unsuitable for many traditional food crops by decreasing plant-available water and creating toxic cellular products [29].
More than 6 % of the global land area (>800 million hectares) [125] and at least 8.5 million hectare in the USA [124] are salt-affected. Secondary salinity, resulting from irrigation or land clearing, affects 20 [125] to 50 % [118, 126] of the irrigated land area globally. There is evidence that the land area affected by salinization is growing through anthropogenic causes [127] and due to changing hydrologic patterns related to climate change [128], resulting in an increasing proportion of marginal land. However, production of tolerant biomass crops on salt-affected soil could result in soil quality improvement and soil carbon sequestration [129].
Effects of Salt Stress
Effects of salinity on plant growth and physiology have been reviewed comprehensively elsewhere e. g [130–132], but common effects are discussed here. Under prolonged or severe salt stress, plants can experience negative developmental effects [126], from seed germination [133] and emergence [134] through maturation [135]. Dissolved salt ions in the soil solution can substantially reduce osmotic potential values (typical saline soil water potentials range between −1.6 and −10 MPa [136]), altering water potential gradients that drive water uptake and solute movement through plant tissues [133], resulting in decreased water uptake even when soils are wet. This functional reduction in water availability can lead to symptoms typical of drought-affected plants: reduced shoot and root growth rates, reduced leaf number, declines in stomatal conductance and photosynthesis rates, and damage or death of leaves [30, 130, 137–139]. In addition, salt ions can cause cellular toxicity, as well as disruption of normal membrane functioning, nutrient uptake, protein synthesis, and enzyme activation [29]. Secondary effects, including oxidative damage [140] and cell death, can also result from salt stress.
Salt Stress Tolerance Strategies
Halophytes (“salt-loving” plants) have specialized strategies for growth in saline conditions [130, 141–143]. These include succulence, which maintains water-to-salt ratios at acceptable levels as the overall cell volume increases, compartmentalization of salt ions into vacuoles or specialized salt glands on leaf surfaces, and efficient ion pumping mechanisms to exclude or remove ions from cytosol into plant apoplast [29]. However, halophytes are not the only plants that can tolerate salinity. Because saline soils are functionally similar to dry soils, plants with high water use efficiency (e.g., C4 and CAM plants) are predicted to perform well when exposed to salinity. In addition, many plants are capable of moderate levels of osmotic adjustment, in which salts accumulate in vacuoles to maintain cellular turgor and reestablish whole-plant water potential gradients. This adjustment takes place over a matter of hours to days [130], during which time growth is restricted and wilting may occur. More salt-tolerant plants go beyond compartmentalizing salts into vacuoles by excluding NaCl from xylem channels, actively exporting Na+ into the soil solution, and regulating K+ loss in cation channels [80]. Several comprehensive reviews offer additional information about salt tolerance mechanisms [e.g., [125, 144, 145].
Salt-Tolerant Biomass Crops
Some potential biomass crops, such as Pennisetum purpureum, show no more salinity tolerance than conventional agricultural crops [146, 147]. Thus, the current challenge is to find biomass crop species that can grow and maintain high yields on marginal salt-affected soils. Of the 17 crops evaluated, several species or genotypes were highly tolerant of salinity (Table 3). Deep-rooted perennial grasses are often recommended for drought- and salt-affected soils [180–183], and our literature search corroborated this recommendation. However, some of these grasses were more tolerant than others. For example, Andropogon gerardii, Arundo donax, and Spartina pectinata were highly salt tolerant, with the latter two classified as halophytes [152, 179]. In contrast, Pennisetum purpureum showed major reductions in shoot biomass in saline conditions [146], and M. × giganteus was only moderately salt tolerant [160]. Upland ecotypes of Panicum virgatum (e.g., “Blackwell,” “Trailblazer,” and “PV-1777”) were among the more salt-tolerant cultivars [151, 164, 166, 184], although the upland ecotype, “Cave-in-Rock,” was not tolerant at the seedling stage [167].
Several salt-tolerant woody crops are also available (Table 3). For example, Eucalyptus camaldulensis cultivars “Silverton” and “Local” efficiently excluded or compartmentalized salts in saline and saline + hypoxic conditions [154]. Pinus pinea showed no growth reduction under saline conditions [168], and Pinus banksiana growth may have been stimulated by certain levels of salinity [169]. Among tree crops, short-rotation woody crop (SRWC) species have particularly strong bioenergy potential because of fast growth and high yields [185–188]. Salt-tolerant SRWC species include several poplar (Populus spp.) and willow (Salix spp.) hybrids and tetraploid Robinia pseudoacacia (Table 3). These hybrids and others identified in Table 3 highlight the possibility of breeding salinity tolerance into many of the biomass crops destined for production on marginal lands.
Temperature Stress
Framing the Issue
Temperature is a major factor governing plant growth and biomass production [189], and temperature extremes can cause severe abiotic stress and inhibit plant growth. Climate comparisons between the most recent decade and historical climates indicate unmistakable and consistently warming surface temperatures on a global scale and throughout much of the USA; however, some small regions in the southern USA are now experiencing cooler than average trends [190]. Irrigation and soil amendments in traditional production systems may offset some of the negative effects of heat and cold temperatures [191]. In order to avoid heat-related crop damage, some growers may also opt to shift production to alternate regions where summer temperatures are milder. However, moving perennial crops to more northern locations will introduce more extreme winter weather to crops that may be adapted to mild winter climates. In addition, thermal climate changes may impact crops grown on marginal lands to a greater extent than prime agricultural land [192]. With greater temperature fluctuations and movement of crops outside of their traditional production regions, it will be important to develop biomass crops that can tolerate temperature extremes.
Effects of Temperature Stress
All plant species are adapted to a range of optimal temperatures, but when they are subjected to temperatures outside that range, physiological, metabolic, and molecular changes occur to maintain homeostasis under suboptimal conditions [193]. If the plant experiences suboptimal temperatures for an extended period, these processes become more impaired and abnormal until temperatures reach lethal levels [193]. Both low and high temperatures can cause physiological stress symptoms and physical damage in plants. Low-temperature stress can be caused by both freezing (temperatures less than −1 °C) and chilling (0–18 °C). The injuries caused by low temperatures for both freezing and chilling can be seen within 48 to 72 h and may include phenotypic changes (e.g., wilting, reduced leaf expansion, chlorosis, and necrosis) [193]. Reproductive processes and structures are also severely affected by cold, which can lead to pollen and flower sterility [193]. Likewise, exposure to cold in the germination and establishment phases can lead to low germination rate, stunting of seedling growth, chlorosis, and reduced tillering in grasses [193]. On a physiological level, this damage can be caused by disruption of membrane and organelle functioning as fluid phosolipids become crystalline and dysfunctional in colder temperatures [193]. In addition, ice crystals can form in apoplastic space, physically damaging cells and causing dehydration through the movement of water out of cells down water potential gradients to join the extracellular ice [193, 194]. Cold exposure can also affect photosynthetic functioning, enzymatic activity [195], protein mechanics, and other metabolic processes [193].
High temperatures can affect plants directly through growth inhibition and indirectly through evaporative water loss [196]. Sensitive species can be affected when air temperatures exceed 35 °C, but tolerant species can withstand air temperatures approaching 65 °C [29, 196]. Most plant species, however, cannot survive for extended periods above 45 °C [29]. As in chilling and freezing stress, membrane stability can be affected by heat. In the case of heat, however, membranes can become excessively fluid, causing ion leakage and inhibition of photosynthesis, respiration, and other processes that involve membrane-embedded proteins and electron carriers [29, 30]. High temperature damage to heat-sensitive photosynthetic components (e.g., chlorophyll, thylakoid membranes, and photosystem II) can significantly affect photosynthetic function [30]. Moderate heat stress can inhibit photosynthesis and thus decrease productivity and yields [197, 198]. Photosynthesis is affected before respiration for most plants, meaning that the production of sugars stops before the demand for them does. This can result in the breakdown of stored sugars (e.g., in fruits, leading to decreased sweetness) [29]. Further, heat stress can significantly reduce ethanol yield of some fuel crops [88]. Additional problems associated with, and responses to, thermal stress are reviewed in greater depth elsewhere [e.g., 196, 197, 199–203].
Temperature Stress Tolerance Strategies
Both cold and heat tolerance can be induced in most species through gradual exposure to non-lethal temperatures. Chilling-resistant species overcome membrane fluidity problems by increasing the proportion of unsaturated relative to saturated fatty acids in the membrane [29, 204, 205], lowering the temperature at which membranes solidify. In addition, sucrose and other soluble sugars accumulate in cells and cell walls to lower the temperature at which freezing can occur and to restrict the growth of ice [29]. Some species, particularly woody taxa, are able to avoid cellular freezing until temperatures dip to −40 °C through the mechanism known as “deep supercooling” [206, 207]. This occurs because of an absence of ice nucleation sites within cells, though ice may form in extracellular spaces. Freezing-resistant species produce antifreeze proteins that halt the growth and spread of ice crystals in extracellular spaces [207, 208].
When ample water is available, most plants are able to cool leaves through evaporative/transpirational cooling [197, 209]. However, when stomata close to prevent water loss in dry conditions, heat damage can occur. Plants adapted to hot climates have evolved morphological adaptations to minimize heat load, including pubescent, vertically oriented, or light-colored leaves [197, 209]. In many plants, increases in temperature initiate translation of heat shock proteins (HSPs), which serve to prevent and repair misfolding of other proteins and facilitate proper cellular functioning at high temperatures [200, 210]. At the whole-plant level, synthesis of HSPs increases tolerance of temperatures that could otherwise be lethal [29, 210]. Although HSPs protect cells against damage, the heat shock response increases the rate of maturation in crops and can decrease yields [211]. Further, the heat shock response can halt the synthesis of other proteins [210] and cause oxidative stress [212]. Many heat-tolerant plants are able to maintain higher photosynthetic rates and membrane stability by increasing the proportion of saturated and monounsaturated fatty acids and maintain overall tissue water balance through osmotic adjustment [197]. A number of additional physiological changes occur in response to heat in tolerant taxa, including hormonal changes, increases in protective pigments, and synthesis of secondary metabolites. These are detailed, along with molecular tolerance mechanisms, in several comprehensive reviews [e.g., 196, 197, 199–201].
Heat- and Cold-Tolerant Biomass Crops
Several woody biomass crops are naturally cold tolerant (Table 4), as many of them evolved in cold climates, including alpine or boreal ecosystems. For example, the phenomenon of cellular “supercooling” is common among conifer species, and some Pinus species can survive temperatures as low as −196 °C [202]! Other cold-hardy woody crops include Populus [75, 227] and Salix spp. [86, 234] (Table 4), with Robinia pseudoacacia introduced into several Canadian provinces (http://plants.usda.gov/core/profile?symbol=rops). Moreover, in unpublished University of Illinois research, several hundred black locust genotypes survived the abnormally cold 2013–2014 winter in Urbana, IL (40.0645 N, −88.2078 W), when average January and February temperatures were 5.5 and 5.7 °C lower than 30-year averages; furthermore, all trees grew productively the following season (T. Voigt, personal observation). Several herbaceous biomass crops tolerate cold conditions, as well. These include Spartina pectinata [239, 241], as well as Andropogon gerardii cv. “Bison” [214], Panicum virgatum cv. “Dakota” [214] and other upland cytotypes [222], Miscanthus sinensis [242] and, to a lesser extent, M. × giganteus [60] (Table 4). Commonly cultivated Panicum virgatum cultivars “Alamo,” “Cave-in-Rock,” and “Kanlow” were sensitive or moderately sensitive to low temperatures [243]. Although many Agave species are associated with warm desert ecosystems, a number of Agave spp. that evolved in high elevations (e.g., Agave utahensis and Agave parryi) are able to withstand temperatures down to −28 °C. In addition, cold-tolerant genotypes of subtropical and tropical biomass crops Eucalyptus spp. and Saccharum spp. have been developed (Table 4), indicating the possibility for cold tolerance to be improved in future breeding programs for these and other crops.
Because C4 and CAM species have inherent mechanisms to resist heat stress, it makes sense to consider biomass crops with these photosynthetic pathways (see Table 5). Agave species (CAM) can withstand temperatures between 57 and 65 °C because of thick cuticle, low absorbance of short-wave radiation, and deployment of heat shock proteins [244, 260]. A number of C4 and highly efficient C3 perennial grasses are heat tolerant, including Andropogon gerardii, Arundo donax, Miscanthus sinensis, and some Sorghastrum nutans and Saccharum varieties (Table 5). Panicum virgatum cultivars exhibit variable heat tolerance, with lowland cytotypes generally performing better in warm, southern climates [222]. For example, several Panicum virgatum genotypes show intermediate (cv. “Alamo” and others) to high tolerance (cv. “Summer”) to heat stress during germination [243] and thus may be good candidates for production on marginal lands in warm regions. Commonly grown cultivars “Cave-in-Rock” and “Kanlow” were heat sensitive [243]. Heat-tolerant woody species include Jatropha curcas, and Eucalyptus occidentalis and others, Pinus densiflora and others, Populus euphratica, Robinia pseudoacacia, and Salix nigra (Table 5). Many of these crops evolved in hot climates, but others have been improved through breeding for greater heat tolerance. For example, a heat tolerant Saccharum spp. (CP-4333) has been developed and shows rapid recovery following heat stress [256 Table 5].
Additional Considerations in Evaluating Stress-Tolerant Biomass Crops
Multiple Stressors
While research into genetically modifying biofuel crops to enhance abiotic stress tolerance may expand the area suitable for cultivation [64], breeders will need to anticipate the combined stressors that are likely to occur in many marginal production systems. Different combinations of stressors may cause conflicting responses [261], but there are species that are well adapted to multiple stressors. For example, xerohalophytes are specialized halophytes (salt-tolerant species) that are found in dry conditions (e.g., Salsola kali [262]). Conversely, most true halophytes are adapted to wetlands and therefore have adaptations to withstand inundated and saline soils (e.g., Spartina alterniflora [263]). Some of these may be suitable for improvement as energy crops on marginal land. In contrast, multiple stressors often cause damage to growing plants, even if the plant is tolerant of a particular type of environmental stress. For example, Jatropha curcas, a highly heat-tolerant species, suffers more from the combination of salinity and heat stress than from either stressor alone [159]. Therefore, it will be important to identify the prevailing stressor(s) in the marginal area under production and choose the most tolerant biomass crops. It will also be important for producers to be aware of the possibility of reduced yield even among the most tolerant crops in years when multiple stressors occur (e.g., low rainfall years in saline conditions). Further, this review focused on a narrow, but physiologically important, set of stressors. We acknowledge that additional stress factors will influence biomass crop productivity on marginal land. Some of these, like nutrient deficiencies, can be ameliorated with available agronomic management practices.
Several of the crops we have highlighted are suitable for a number of stressful conditions. These will be discussed further in the “Conclusions” section.
Invasiveness
The ability to produce high biomass yields under unfavorable growing conditions is correlated with invasiveness, and several authors have cautioned against the use of non-native and potentially invasive biomass crops [264–270]. Some of the crops mentioned in this review have been evaluated as high-risk species and have received attention from environmental groups and invasion ecologists (e.g., Arundo donax, seed-bearing Miscanthus spp., Jatropha curcas, Pennisetum purpureum) [265, 267, 268, 271–275]. Therefore, these and other high invasion-risk crops should only be chosen when they can be grown and transported with strict containment procedures in place [276] and when state and federal regulations allow their introduction and cultivation [277, 278]. Other crops in this review, however, are either US natives or have been evaluated as low-risk for invasion in the USA [279]. The authors encourage the choice of native biomass crops, but note that most “native” species are only native to a specific region of the USA and can, in fact, be “weedy” or invasive outside of the native range (e.g., Robinia pseudoacacia, which is native to small areas in the Piedmont and Missouri regions, but has invaded and naturalized throughout the continental USA) [273]. In addition, some native species can be pests within their native regions. For example, Helianthus annuus is native to the entire continental USA but is a regulated noxious weed in Iowa due to its negative impacts on agriculture [277]. As such, it will be important for producers to choose biomass crops that are native and/or low-risk in the production region [279]. Growers can consult online databases to determine invasion risk [280–282] or choose from a recently released list of low-risk biomass crops [279].
Conclusions
Predicted climate changes will increase the likelihood of abiotic stress throughout the country, including various combinations of multiple stressors. For example, heat waves are predicted to become more intense throughout the country while precipitation is expected to increase in the northern USA and to decrease in the southwest [11]. Our literature review has revealed several “all purpose” biomass crops that are moderately or highly tolerant of multiple environmental stressors (Table 6). For example, Andropogon gerardii, Eucalyptus spp., Miscanthus spp., Panicum virgatum, Pinus spp., Populus spp., Robinia pseudoacacia, and Spartina pectinata were shown to be moderately or highly tolerant of four or more stress types. For particular growing conditions such as some hot and dry areas, growers could choose among Agave americana, Andropogon gerardii, Jatropha curcas, Miscanthus sinensis, Pinus sylvestris, Pinus taeda, Populus euphratica, or Robinia pseudoacacia. Many wet and saline environments could likely support Arundo donax, Eucalyptus camaldulensis (particularly Eucalyptus camaldulensis “Silverton” and “Local”), Miscanthus × giganteus, Panicum virgatum “Trailblazer,” Sorghum bicolor varieties, and Spartina pectinata. Genera such as Pinus and Populus comprise a host of species that are adaptable to different stressors and combinations of stressors.
As previously mentioned, our list is not exhaustive and, in some cases, is based on studies that assessed relative—not absolute—stress tolerance, but it represents a much more comprehensive biomass crop selection guide for growers than currently exists. Based on this review, growers could choose from a variety of plant types representing a variety of industrial uses from ethanol (e.g., Miscanthus spp.) to combustion (e.g., Pinus spp.), depending on their preferences and the capabilities of local processing plants. In addition, we have indicated here that a number of biomass crops have already been improved for greater stress tolerance, and we assume that breeding programs will continue to develop additional stress-tolerant crops. Therefore, it appears that there will be a number of options available for marginal lands now and into the increasingly stressful future [105].
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The authors thank the Energy Biosciences Institute for funding this work.
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Quinn, L.D., Straker, K.C., Guo, J. et al. Stress-Tolerant Feedstocks for Sustainable Bioenergy Production on Marginal Land. Bioenerg. Res. 8, 1081–1100 (2015). https://doi.org/10.1007/s12155-014-9557-y
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DOI: https://doi.org/10.1007/s12155-014-9557-y