Sweetcane (Erianthus arundinaceus) as a native bioenergy crop with environmental remediation potential in southern China: A review

Sweetcane (Erianthus arundinaceus [Retzius] Jeswiet) is an ecologically dominant warm‐season perennial grass native to southern China. It traditionally plays an important role in sugarcane breeding due to its excellent biological traits and genetic relatedness to sugarcane. Recent studies have shown that sweetcane has a great potential in bioenergy and environmental remediation. The objective of this paper is to review the current research on sweetcane biology, phenology, biogeography, agronomy, and conversion technology, in order to explore its development as a bioenergy crop with environmental remediation potential. Sweetcane is resistant to a variety of stressors and can adapt to different growth environments. It can be used for ecological restoration, soil and water conservation, contaminated land repairing, nonpoint source pollutants barriers in buffer strips along surface waters, and as an ornamental and remediation plant on roadsides and in wetlands. Sweetcane exhibits higher biomass yield, calorific value and cellulose content than other bioenergy crops under the same growth conditions, thereby indicating its superior potential in second‐generation biofuel production. However, research on sweetcane as a bioenergy plant is still in its infancy. More works need be conducted on breeding, cultivation, genetic transformation, and energy conversion technologies.

Some famous second-generation bioenergy crops such as miscanthus are derived from China (Clifton-Brown et al., 2017;Wang et al., 2014;Xue, Kalinina, & Lewandowski, 2015;Xue, Lewandowski, Wang, & Yi, 2016). Also, some other excellent native bioenergy grass has been identified in recent years, including the sweetcane (Erianthus arundinaceus (Retzius) Jeswiet) (Dao et al., 2013;Zeng, Zhang, Liu, & Liu, 2013). Sweetcane is a warm-season, tall-growing perennial species native to much of southern China, and has traditionally been considered as a potentially important genetic resource for use in sugarcane breeding programs, thereby resulting in much research with respect to its biological characteristics and genetic resources. Recently, this species has been targeted for use as a bioenergy perennial because of its high fiber content and biomass yield. As a potential feedstock for bioethanol production, an increasing amount of research now focuses on its biomass characteristics and conversion technologies. Meanwhile, there are studies showing that the sweetcane has great potential for environmental restoration. The use of an environmentally stress-tolerant plant for energy production has been considered as a Win-Win paradigm (Robertson et al., 2017). Therefore, the purpose of this paper is to systematically summarize current knowledge on sweetcane: its biology, phenology, biogeography, agronomy and conversion, as well as analyze its potential in bioenergy production and environmental restoration.
As a perennial grass, every year, the aboveground system of this species usually shoots in mid-March, the first month of spring in southern China, and the tillering occurs in late April. In late June, the first month of summer, it begins to joint. In late September, sweetcane heads, and flowers approximately 1 month later, the caryopsis matures. In December, the first month of winter, the shoot system begins to wither ( Figure 1) (Hou et al., 2015;Liang, 2011).

| Taxonomy and genetic diversity
Sweetcane belongs to the family Gramineae; however, its assignment at the genus-level is disputed between Saccharum and Erianthus. In literature, the commonly used Latin names of sweetcane are Saccharum arundinaceum Retz. and Erianthus arundinaceus (Retzius) Jeswiet. Both Saccharum and Erianthus belong to the Saccharum complex, which includes the genera Saccharum, Erianthus, Sclerostachya, Narenga, and Miscanthus, as they are thought to be involved in the origin of Saccharum (Daniels, Smith, Paton, & Williams, 1975;Mukherjee, 1958). Some species in this complex have been identified as promising bioenergy crops, such as M. sinensis, M. sacchariflorus, and S. officinarum.
Molecular phylogenetic analysis based on ITS sequences of some species in the Saccharum complex from Genbank indicated that sweetcane had a close genetic relationship with Erianthus ( Figure 2). Moreover, other molecular classification methods, such as random amplified polymorphic DNA (RAPD) (Nair & Mary, 2006), amplified fragment length polymorphism (AFLP), microsatellites, and chloroplast genome analysis, all showed that sweetcane should be classified either as Erianthus or within a new genus (Feng, Wu, & Chen, 1997;Tsuruta, Ebina, Kobayashi, & Takahashi, 2017). Lignin gene-based TRAP markers also showed that sweetcane genotypes clustered as a distinct group that was highly divergent from the Saccharum (Suman et al., 2012). Thus, we use the Latin name Erianthus arundinaceus for sweetcane in this paper. F I G U R E 1 Annual growth cycle of sweetcane in southern China (Hou et al., 2015;Liang, 2011) As sweetcane is of interest in sugarcane breeding programs and has a great potential in bioenergy production, a large number of wild germplasm resources have been collected by several research institutes (Table 1). These collections have covered almost all of the sweetcane distribution areas in China. Knowledge of the wild germplasm is important for efficient breeding programs because it provides the basis for development of desirable plants.
Sweetcane has a high level of genetic differentiation with great differences in phenotypes, number of chromosomes and molecules. Some morphological differences of sweetcane have been observed. According to Liang (2011), stem diameter had the largest variation, from 8.86 to 37.36 mm, with a coefficient of variation as high as 49.66%. Flag leaf length and penultimate leaf width were also highly variable, with variation coefficients of 45.10% and 44.20%, respectively.

| Photosynthetic characteristics
Sweetcane is a C 4 plant with Kranz anatomy (Yang, Li, Yu, & Liu, 2011). Research showed that the daily variation in net photosynthetic rate (Pn) of sweetcane leaves had a bimodal curve and a 'midday depression' phenomenon (Zhang, Gan et al., 2017). The Pn of sweetcane was related to its altitude, with relatively high rates for populations distributed below 1,000 meters altitude (Yang, Pan, Yang, Li, & Xiao, 2006).
Preliminary field studies in southern China (Hubei Province) showed that the maximum Pn observed under field conditions of sweetcane was slightly lower than Pennisetum purpureum, but higher than other bioenergy grass, such as M. floridulus and A. donax (Zeng, 2013). However, the differences between sweetcane genotypes were not considered in those studies; more research regarding the features of different genotypes could be conducted by following examples of other bioenergy crops (Kalinina et al., 2017;.

| Resistance
Sweetcane can adapt to a variety of environments, resist to abiotic and biotic stressors including drought, saline soils, cold, and disease, thus playing an important role in sugarcane breeding. This is also beneficial for its cultivation in different types of marginal land.

| Drought
Sweetcane has the agronomic trait of drought tolerance, which can be used for sugarcane improvement by hybridization. It has been proved that the drought resistance in hybrid offspring of sweetcane and sugarcane was significantly enhanced (Chen, Deng, & Guo, 2007). Moreover, different cultivars of sweetcane have distinct drought resistance. Two cultivars with remarkable drought resistance were identified in Hainan Province of China by Wu, Pan, Chen, and Zhang (2008).

| Salt
Sweetcane can also be tolerant to salt stress (Mirshad, Chandran, & Puthur, 2014). Under NaCl stress, sweetcane could maintain a dynamic balance of active oxygen metabolism (Guo, Guo, Guo, & Zhang, 2005). The potential of high NaCl tolerance made sweetcane an appropriate choice for growing in marginal lands, which was affected by high NaCl levels. Some genes related to drought resistance were shown to play a role in salt resistance (Augustine, Ashwin et al., 2015).

| Cold
Sweetcane is a warm-season perennial distributed in both tropical and subtropical regions, so its cold resistance, especially its ratoon cold tolerance, is not very strong (Burner et al., 2017). However, some accessions and breeding lines have demonstrated overwintering abilities in Nasushiobara, Japan, where the mean minimum air temperature in winter was −4.4°C (Matsunami et al., 2018). Moreover, the ability of hybrid sweetcane-sugarcane offspring to resist low temperatures was much stronger than that of sugarcane (Ram, Sreenivasan, Sahi, & Singh, 2001).

| Habitat diversity
Sweetcane can grow in a variety of habitats in southern China, such as roadsides, hill slopes, riversides, abandoned agricultural lands, courtyards, and even the rocks (Figure 3). Generally, this species favors areas with abundant sunlight.
The roadside, including highways and common roads, is the most common habitat of sweetcane (Dao et al., 2013;Fan, Wu, & Du, 2017;Hu, Wang, Yu, & Yang, 2015;Zhang, Lei, Zhen, Tao, & Yu, 2006). As a species that can thrive in barren landscapes, sweetcane is usually the first to grow along new roadsides. Furthermore, planting sweetcane on the roadside is conducive to soil and water conservation.
Sweetcane has a wide range of adaptability to water; it can grow on dry hill slopes as well as on wet riversides (Hao et al., 2016;Ou, Jin, Peng, Fang, & Fang, 1997). It can even be used in constructed wetlands (Jiang et al., 2005). Moreover, biomass from wetland plants is a good raw material for biomass energy production .

| Distribution in China
The occurrence of sweetcane was mapped using records obtained from the Chinese Virtual Herbarium (http://www.cvh. org.cn/cms/en), the Specimen Resources Sharing Platform for Education (http://mnh.scu.edu.cn/new/), the Global Biodiversity Information Facility (www.gbif.org) and other references (Dao et al., 2013;Yan, Bai, Ling, & Chang, 2009;Zhang et al., 2013) (Figure 4). All sweetcanes were found in the tropical and subtropical areas of China, specifically in the regions east of the Tibetan Plateau, south of Huai River-Qinling Mountains line. Sweetcane was generally found below an altitude of 1,500 m; however, it could be distributed up to 2,350 m (Yan et al., 2016).

| Global distribution
As a warm-season species, sweetcane is mainly distributed in the subtropical to tropical areas of East Asia, South Asia, and Southeast Asia, including Bhutan, India, China, Myanmar, Thailand, Philippines, Laos, Sri Lanka, Vietnam, Indonesia, Malaysia, New Guinea, and Nepal (Chen, & Phillips, 2006;Peet, Watkinson, Bell, & Kattel, 1999). According to predictions using MAXENT species distribution modeling based on Global Climate Data WorldClim Version 2 (http:// worldclim.org/version2), southern Japan, southern South Korea, the east coast of Australia, the Caribbean coast, and the southeast coast of Brazil are also suitable for sweetcane cultivation ( Figure 5).

| Introduction and invasiveness
Sweetcane was introduced as an energy grass to Japan (Matsunami et al., 2018;Tagane et al., 2011;Uwatoko et al., 2011;Yamamura et al., 2013), as well as to Florida and North Carolina of USA (Fedenko et al., 2013;Palmer, Gehl, Ranney, Touchell, & George, 2014). The potential invasiveness of sweetcane in Florida was evaluated using the Australian Weed Risk Assessment system, and the results showed that sweetcane had a low probability of becoming invasive (Gordon, Tancig, Onderdonk, & Gantz, 2011).

| Biomass composition and calorific value
The composition of lignocellulosic biomass determines its utilization potential as energy crop. Higher levels of cellulose and hemicellulose are beneficial for biofuel production after enzymatic hydrolysis, whereas higher lignin content can negatively affect the conversion efficiency. The amount of cellulose, hemicellulose and lignin of different sweetcanes are shown in Table 2. The cellulose contents of different sweetcanes range from 30.36% to 55.4%, while the hemicellulose amount ranges from 22.79% to 41.48%. Lignin content is generally from 5% to 10%, but a few can reach up to 17% ( Table 2). The biomass composition of sweetcane was comparable to that of other bioenergy crops, such as P. virgatum, Miscanthus × giganteus, Pennisetum × purpureum, and M. floridulus ( Figure 6). When grown under the same conditions, sweetcane contained relatively higher cellulose content than other bioenergy crops (Hou et al., 2015). Furthermore, the cellulose content of tetraploid sweetcane was usually higher than hexaploid individuals, while the opposite was true for hemicellulose content (Yan et al., 2016).
The gross calorific value (GCV) of sweetcane ranged from 16.44 to 19.32 KJ/g (Liang, 2011). Under the same growth conditions, the GCV of sweetcane was equivalent to other energy plants, such as Pennisetum × purpureum and M. floridulus, whereas the ash free calorific value was slightly higher than other energy plants (Figure 7) (Ning, Chen, Wang, Zhang, & Qiu, 2010;Zeng, 2013).
As a perennial plant, the shoot system of sweetcane withers each winter. In a year's growth cycle, the cellulose content increases from June to December. However, the contents of hemicellulose and lignin decrease in October. Accumulation of calorific value per unit area reaches its highest level in November (Figure 8) (Yan et al., 2014). This indicates that November is the optimal time for harvesting sweetcane as a bioenergy feedstock.

| Biomass yield
Biomass yield is another important indicator of a grass' efficacy as a bioenergy crop. Sweetcane had a relatively high F I G U R E 5 The predicted potential global distribution of sweetcane

F I G U R E 4
The occurrence records of sweetcane in China biomass yield when comparing with other bioenergy plants grown in the same environment (Singh et al., 2015;Zeng, 2013). The high yield of sweetcane corresponded to growth conditions, planting time, and harvest time (Palmer et al., 2014;Singh et al., 2015;Yan et al., 2014). For instance, sweetcane biomass yield reached a maximum of 43.76 t/ha in China, while its yield for the first year of growth in North Carolina, USA, was only 5.7 t/ha (Table 3). In the subtropical region of China, the highest sweetcane biomass yield was obtained in November (Yan et al., 2014).
There are also variations in dry biomass yield between sweetcane individuals. Analysis of 20 sweetcane individuals from Sichuan Province showed that the variation coefficient of dry matter production per plant was 25% (Liang, 2011). Hence, careful selection of individuals for bioenergy feedstock is required.

| Conversion of sweetcane biomass into biofuels
Traditionally, sweetcane was collected in winter and directly burnt as fuel source in rural areas of southern China. The high calorific value of sweetcane allows for direct combustion to generate electricity or heat, as well as the production of solid  (Hou et al., 2015) F I G U R E 7 Comparison of gross calorific value (GSV) and ash free calorific value (AFCV) of sweetcane with other bioenergy grasses under the same growth condition (Zeng, 2013) molded fuel. More importantly, sweetcane has great potential as biomass feedstock for bioethanol and methane production (Hu et al., 2017).

| Bioethanol production
The high cellulose content of sweetcane makes it possible to be converted into bioethanol. The practical ethanol yield of sweetcane reported by Zhang, Gan et al. (2017) was 0.17 L/ kg (based on dry biomass), with broth ethanol concentration of 4.6% (v/v). Hu et al. (2017) gained a better ethanol yield of 0.19 L/kg by using other pretreatment method, but it was still lower than the ethanol yield of switchgrass (Schmer, Vogel, Mitchell, & Perrin, 2008). Therefore, the ethanol yield of sweetcane would be further increased with the improvement of pretreatment and fermentation technologies. Pretreatment is a key step in the lignocellulose biorefinery with respect to both technology and economic aspects. Alkali pretreatment is one of the most commonly used methods for herbaceous feedstocks. Pretreatment with 2% NaOH for 1 hr, lignin content of sweetcane was reduced from 11.01% to 3.34%, while cellulose content was increased from 43.77% to 72.54% (Zhang, Xie, & Lin, 2011). Other similar pretreatments indicated that sweetcane pretreated with 1% NaOH (1 hr) resulted in the highest sugar yield of 467.9 mg/g from enzymatic hydrolysis (Panneerselvam, Sharma, Kolar, Clare, & Ranney, 2013). Ammonia based pretreatment is a type of alkali pretreatment catalyzed by ammonia under different thermodynamic states of ammonia-water mixtures and ammonia concentrations. Liquid ammonia treatment (LAT) of sweetcane could result in 70% glucan conversion and 83% xylan conversion, respectively, under the optimal pretreatment condition. The glucose and xylose yields were 573% and 1,056% higher than those of the untreated biomass . Furthermore, pretreatment with ozone could effectively de-lignify sweetcane with negligible sugar loss while achieving a 50% delignification and total fermentable sugar concentrations greater than 400 mg/g (Panneerselvam, Sharma, Kolar, Clare et al., 2013;Panneerselvam, Sharma, Kolar, Ranney, & Peretti, 2013).

| Biogas production
Sweetcane can also be used as feedstock for biogas production. In rural areas of southern China, sweetcane was usually added into household biogas digesters as supplementary substrate. Potential biogas production of sweetcane was first investigated by Deren, Snyder, Tai, Turick, and Chynoweth (1991) and the results revealed that its methane yield was in the range of 0.28-0.31 L/g volatile solids (VS), which was comparable to other energy crops (Deren et al., 1991;Zhang et al., 2016). A recent study of methane production from sweetcane showed that the highest methane yield was about 83.5 L/kg (based on total solids) (Hu et al., 2017). Moreover, the yields could be further enhanced if suitable pretreatment F I G U R E 8 Monthly variations of biomass composition and calorific value accumulation per unit area (Yan et al., 2014)  on the feedstock and optimization of anaerobic digestion parameters were conducted. In India, the fibers produced by mechanical compression of sweetcane were used for paper production. The chemical oxygen demand (COD) of the resulting liquid was approximately 93,974 mg/L, indicating that 1 L of liquid can produce 40 m 3 biogas (Jayabose et al., 2017).

| Nutrient removal
Low nutrient input is an advantage for the second-generation bioenergy crops compared with the first-generation bioenergy crops (Holland et al., 2015). Some perennial bioenergy grasses such as switchgrass and miscanthus can gain high biomass yields under low-input conditions while having low nutrient removal (Casler et al., 2017;Yu, Ding, Huai, & Zhao, 2013). It has been found that sweetcanes grow well in barren lands in southern China (Dao et al., 2013). The other field study regarding four bioenergy grasses (Pennisetum purpureum × P. americanum, P. purpureum, sweetcane, and S. spontaneum) from Saccharum complex showed that sweetcane had the highest K utilization efficiency (106%) and the lowest K content (1.14%) . This indicates that it has a low-input characteristic.
On the other hand, a field experiment in USA showed that the nitrogen (N), phosphorus (P) and potassium (K) removal capacity of sweetcane could reach up to 240 kg/ha, 65 kg/ha, and 390 kg/ha, respectively (Singh et al., 2015). The N content of sweetcane biomass, which was harvested 2 years after planting, was 309 kg/ha in Japan (Matsunami et al., 2018). Moreover, sweetcane exhibited the ability to accumulate N and P in constructed wetland, which was used to treat light eutrophic water in southern China (Jiang et al.2005). This also proves the great nutrient removal ability of sweetcane. However, due to the ability to absorb N from deeper soil and store N in underground parts during winter for the next growing season, only 20% of N in sweetcane individual plant originated from fertilizer (Matsunami et al., 2018).
Genotype plays an important role in nutrient removal efficiency of perennials (Yu et al., 2013). Many low-input cultivars of switchgrass and miscanthus were selected (Casler et al., 2017;Xu, Gauder, Gruber, & Claupein, 2017), although some of those cultivars were also superior in high-input environments (Rose, Das, Fuentes, & Taliaferro, 2007). Unfortunately, so far few data are available for sweetcane in cultivars selection, even though many genetic resources have been collected in China (Table 1). A study on six sweetcane varieties showed that the N content and carbon (C) content of the harvested sweetcane were in the range of 0.37%-0.83% and 44.7%-45.8%, respectively (Hu et al., 2017). As a result, the C/N ratio of sweetcane was from 62.6 to 121.6, and the highest value was comparable with Miscanthus × giganteus (Michel et al., 2011;Wilk & Magdziarz, 2017). In addition, the harvest time also affects the nutrient removal efficiency of sweetcane. The removed N and K in biomass being harvested in late winter was 55% of that being harvested in autumn (Matsunami et al., 2018).
In summary, due to the high nutrient utilization efficiency, sweetcane can be planted on barren marginal lands as a sustainable biomass feedstock. In this case, low-input cultivars need to be selected in the future and the best harvest time should be winter. On the other hand, since sweetcane has the ability to accumulate nutrients from surroundings, it can be grown in buffer strips along surface waters and be used to block nonpoint source pollutants entering rivers or lakes. The aboveground parts of sweetcane could be harvested as the feedstock for bioethanol, biogas or power generation, while the fermentation residues and ash could subsequently be used as fertilizer. However, a suitable harvest time needs to be determined in further research.

| Remediation of heavy metal
Sweetcane exhibited high bio concentration factors for Mn and Ni in constructed wetlands, which were used to treat wastewater from the pulp and paper industry (Arivoli, Mohanraj, & Seenivasan, 2015). In heavy metal contaminated mining areas, sweetcane could efficiently accumulate Cu, Zn, Pb, and Cd, with enrichment factors and transport coefficients greater than 1 for Zn, Pb, and Cd . This indicates that sweetcane can be used as a remediation plant for abandoned farmlands, which have been contaminated by these metals.
Approximately 1/6 of the cultivated land in China suffered from heavy metal pollution (Wei, Chen, & Lin, 2013). Sweetcane has a strong ability to absorb Cd and Pb, which are common pollutants in southern China. Therefore, cultivation of sweetcane in heavy metal contaminated farmlands will be helpful for land remediation. Moreover, the biomass obtained from these lands can also be used for energy production. However, the residues derived from anaerobic fermentation or direct combustion of sweetcane growing in heavy metal contaminated farmland cannot be further used as fertilizer, because the biomass contains heavy metals. Some post processing technologies like pyrolysis or thermal treatment are needed (Keller, Ludwig, Davoli, & Wochele, 2005;Sas-Nowosielska et al., 2004).

| Germplasm resource exploitation and breeding
Although some sweetcane resources have been collected, relatively few works have been done on screening and breeding of fine traits associated with biomass utilization. Further research is required to obtain varieties with low lignin and high cellulose content for the purpose of cellulosic ethanol production; this entails initially screening the collected germplasm resources and then improving it through traditional breeding or transgenic methods. Therefore, an efficient genetic transformation system in sweetcane is needed.

| Cultivation management
Sweetcane is a potential bioenergy crop; however, there are few studies on cultivation management. Future research should focus on the management of pests, diseases, harvesting, and fertilization.

| Comprehensive development and implementation of the technology
The cost of raw materials is one of the limiting factors affecting large-scale commercialization of bioenergy. Development of a multi-channel, comprehensive utilization strategy for bioenergy crops is important for solving this problem. At present, research of bioenergy products, such as ethanol produced from sweetcane, is still laboratory-based. Future studies need to include pilot-scale and large-scale implementation. Additionally, consideration must be given to the disposal or utilization of residues, as well as the development of high value-added products from sweetcane ( Figure  9).

| CONCLUSION
Sweetcane not only plays an important role in sugarcane breeding, but also has great potential in environmental remediation and as a biofuel feedstock. It can be planted in wastelands, abandoned farmlands, and roadsides below an altitude of 1,000 m in southern China. Sweetcane can adapt to a variety of growth environments due to its wide resistance to abiotic and biotic stresses. Compared with other bioenergy grasses under the same growth conditions, sweetcane usually has a higher photosynthetic efficiency, biomass yield, cellulose content and calorific value. Moreover, sweetcane could be a highly effective phytoremediator for wetlands, buffer strips along surface waters, and contaminated lands due to its highly efficient uptake of nutrients and heavy metals. Additionally, the subsequent biomass can be harvested for bioenergy production. However, the study of sweetcane as a bioenergy is still in its infancy. More works on breeding, cultivation, genetic transformation, biorefinery, and energy conversion technologies need be done.