Ricinus communis: A robust plant for bio-energy and phytoremediation of toxic metals from contaminated soil

Ecological Engineering 84 (2015) 640–652

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Ecological Engineering journal homepage: www.elsevier.com/locate/ecoleng

Review

Ricinus communis: A robust plant for bio-energy and phytoremediation of toxic metals from contaminated soil Kuldeep Bauddh a , Kripal Singh b , Bhaskar Singh a , Rana P. Singh c,∗ a b c

Centre for Environmental Sciences, Central University of Jharkhand, Brambe, Ranchi 835205, India Division of Agronomy and Soil Science, CSIR-Central Institute of Medicinal and Aromatic Plants, Lucknow 226015, Uttar Pradesh, India Department of Environmental Science, Babasaheb Bhimrao Ambedkar University (A Central University), Lucknow 226025, Uttar Pradesh, India

a r t i c l e

i n f o

Article history: Received 9 March 2015 Received in revised form 18 July 2015 Accepted 7 September 2015 Keywords: Biodiesel Heavy metals Multipurpose crop Phytoremediation Ricinus communis

a b s t r a c t Phytoremediation is an age old technology. Recently, it has emerged as one of the most accepted, economical, eco-friendly and esthetically important strategy adopted for removal of toxic metals from the contaminated sites. However, it is observed that its application suffers from several imperfections. Edible crops with low biomass and plants having low metal extracting ability have been studied extensively for their use to extract heavy metals. It is found that most of the edible crops are low biomass producing plant with shorter lifespan and sensitive to most of the abiotic and biotic stresses. Several non-edible plants have also been studied for their metal extraction potential. Ricinus communis is a non-edible emerging phytoremediator which is a robust and industrially important oil yielding multipurpose shrub of wild as well as cultivable nature. The application of R. communis for phytoremediation purpose in place of edible as well as non-edible stress sensitive crops/herbs may become a good alternative for the remediation of contaminated land. Its other important uses are biodiesel production, medicinal products, societal development, employment generation to the local peoples, carbon sequestration, reduction in green house gases (GHG), etc. It also increases the fertility of the soil and reduces soil erosion. R. communis has been found to possess excellent ability to extract majority of toxic metals like Cd, Pb, Ni, As, Cu, etc. as well as some organic contaminants like pesticides. © 2015 Elsevier B.V. All rights reserved.

1. Introduction Ricinus communis (castor) is an oilseed crop belonging to family Euphorbiaceae, which includes some other important energy plants such as cassava (Manihot esculenta), rubber tree (Heveabra siliensis) and physic nut (Jatropha curcas). Among non-edible oils, the castor oil is the most popular for a variety of industrial, cosmetic and medical applications (Scarpa and Guerci, 1982; Martín et al., 2010; Lavanya et al., 2012; Perdomo et al., 2013; Wale and Assegie, 2015). The presence of a high proportion of ricinoleic acid in castor oil makes it suitable for the production of high quality lubricants (Sanzone and Sortino, 2010). The castor oil is used in Brazil to extract the ethyl esters using ethanol from sugarcane fermentation, in which all natural products are used for production of ethyl esters. One of the major attractions associated with castor is its easy cultivation even in dry waste lands. Two years field experiment conducted in south Italy using local ecotypes yielded 2.3 t h−1 of castor bean seeds possessing 38.0% oil

∗ Corresponding author. E-mail address: [email protected] (R.P. Singh). http://dx.doi.org/10.1016/j.ecoleng.2015.09.038 0925-8574/© 2015 Elsevier B.V. All rights reserved.

content which is considered a good yield for dry land farming in that region (Sanzone and Sortino, 2010). Recently dwarf hybrids of R. communis have been preferred for the mechanization of harvesting (Clixoo, 2010). Recently, castor is also becoming popular as a value added plant for the phytoremediation of contaminated sites along with economic and ecological services. Castor contains some distinguished features like unpalatable nature, high biomass productivity, tolerance to both biotic and abiotic stresses i.e. heavy metals, salinity, drought, pests, persistent organic pollutants (POPs), etc. (Heikal et al., 1980; Shi and Cai, 2009; Babita et al., 2010; Huang et al., 2011; Bauddh and Singh, 2012a,b, 2014; Zhang et al., 2015). The remediation of contaminated soils is a difficult task. However, are various methods such as mechanical removal and chemical engineering are available which are often expensive and incompatible to soil structure and fertility (Cunningham et al., 1997; Gaur and Adholeya, 2004). Phytoremediation, i.e. the use of plant systems to remove the contaminants from the soils and water has recently attracted a great deal of attention as an alternative means of soil decontamination, since it is a cost-effective, environment-friendly approach, applicable to large areas. In order to fully utilize the contaminated sites and to overcome the disadvantage of phytoremediation, a

new strategy of combining phytoremediation with oil crop cultivation, with a view to achieving low cost decontamination of soil through the production of biofuels. Implementation of this strategy requires the selection of energy crops that can tolerate the particular contaminants present in soil is being used. An understanding of the contaminants’ tolerance of the potential energy crops is necessary for studying the plant–metal interactions before application of these crops for phytoremediation and biodiesel production. Further soil is the key compartment of the environment which provides major share of food and nutrition with numerous ecosystem services (Rutgers et al., 2011; Dominati, 2013; Morel et al., 2014). Status of soil health determines its efficiency to work and to provide its services. Due to some natural and majority of anthropogenic activities cause the degradation of soil fertility, water retention capacity, microbial diversity, nutrient, etc. For the restoration of services provided by the soil, it is important to restore the degraded and contaminated land. The aim of this review is to synthesize the available information regarding phytoremediation potential of R. communis as well as other crops to propose a cost effective approach to remediate contaminated sites and simultaneously increase the soil fertility, biodiesel production, employment generation and promote environmental conservation which will help to develop sustainable livelihoods in nearby areas. 2. Ecology and geographical distribution of R. communis Castor is a species of flowering plant in the spurge family, Euphorbiaceae. The castor bean can vary greatly in its growth habit and appearance. The variability has been increased for a range of cultivars for oil production. It is a fast growing and perennial shrub which can reach the size of a small tree around 12 m, but the commercial height of cultivars ranges from 1 to 4 m. Its height depends on different environmental conditions. The leaves of these plants are 15–45 cm long, long-stalked, alternate with 5–12 deep lobes. The flowers are borne in terminal panicle like inflorescences. The fruit of castor is a spiny, greenish (to reddish-purple) capsule containing large, oval, highly poisonous seeds with variable brownish mottling. Castor is basically a warm season crop, cultivated in tropical and subtropical regions as a perennial shrub and in temperate climate as an annual plant throughout the world (Roger and Rix, 1999). Temperature ranging from 20 to 26 ◦ C and rainfall between 500 and 600 mm is considered suitable for obtaining higher yields. It has a capacity to tolerate long dry spells as well as heavy rains but is very susceptible to water logged conditions. Castor plant has been found worldwide but it is cultivated mostly in tropical and sub-tropical countries like India, China, Brazil, USSR, Argentina, Thailand, Philippines, etc. (Fig. 1) (Lavanya et al., 2012; Perdomo et al., 2013). In India, it is distributed throughout the warmer parts of the country, also found wild near habitation, roadside and on wastelands (FAOSTAT, 2011). There are some agronomic characteristics such as moderately fertile soil, slightly acidic conditions (pH 5.0–6.5), well drained, sandy loams which favor castor cultivation, however, heavy clays with poor drainage, and marshy soils are unsuitable. The propagation of castor oil crops is by seeds. Castor is the host plant of many insects like Ariadne merione (common castor butterfly), Samia cynthia ricini (Eri silk moth), and Achaea janata (castor semi-looper moth). It is also used by the larvae of few other species of Lepidoptera, including Hypercompe hambletoni and the Nutmeg (Discestra trifolii) as a food plant. 3. Biofuel production efficiency of R. communis It is reported that there are more than 350 species of oil crop in the world. Among the prominent ones are castor, rapeseed,

Production of seeds (MT)

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2,600,000 2,400,000 2,200,000 2,000,000 1,800,000 1,600,000 1,400,000 1,200,000 1,000,000 800,000 600,000 400,000 200,000 0

Porducing counties Fig. 1. Top ten castor (R. communis) producing countries (FAOSTAT, 2011; Bauddh, 2014).

sunflower, soybean, palm, etc. (Torres et al., 2013). India is the world’s largest exporter of castor oil followed by China and Brazil (Ogunniyi, 2006). Castor oil is known for its high concentration of ricinoleic acid (12-hydroxy-9-octadecenoic acid) that constitutes 89% in the oil. Other fatty acids are present in minor amount that includes linoleic acid (4.2%), oleic acid (3.0%), stearic acid (1%), palmitic acid (1%), dihydroxystearic acid (0.7%), linolenic acid (0.3%) and eicosanoic acid (0.3%). The molecule present in ricinoleic acid is known to show three points functionality. These include carboxyl group which provides sites for esterification; the single point unsaturation which provides feasibility of alteration by hydrogenation, epoxidation, vulcanization; and hydroxyl group that could be subjected to acetylation, alkoxylation that could be removed by dehydration to enhance the unsaturation of ricinoleic acid in the oil. The chemical characteristics of the oil are found to get changed by about 10% in 90 days storage. As the castor oil has only one double bond in the fatty acid chain, it is classified as non-drying oil (Ogunniyi, 2006; Conceicao et al., 2007). The double bond in ricinoleic acid which is close to a hydroxyl group imparts characteristics physical and chemical properties (Echeverri et al., 2013). Ricin is the toxic compound present in the castor oil that could be removed by treatment with ammonia, causing soda, lime and heat (Ogunniyi, 2006). Castor oil has good shelf life and does not turn rancid except when subjected to heating at high temperature (Encinar et al., 2012). India is the chief producer of castor oil contributing 60% of the total world’s production (Dias et al., 2013). Castor oil is known for its better solubility in methanol as well as methyl esters. Maleki et al. (2013) reported that blending of jatropha and palm oil with castor for biodiesel synthesis via single step enzymatic methanolysis reaction in a solvent free medium led to a better yield of biodiesel (that exceeded the maximum theoretical yield of lipozyme TL IM, i.e. 67%). The reason for it is attributed to the fact that methanol has a better solubility in castor oil as compared to other oils. The major advantage with castor oil as feedstock for biodiesel is its solubility in alcohol at 30 ◦ C. A high solubility of castor oil with methanol facilitates the reaction even with heating that could ultimately lower the production cost of biodiesel. There is a limit for the presence of double bonds in the feedstock oil for biodiesel. As per the specification for biodiesel, the feedstock oil should not contain linolenic acid and acid with four double bonds in excess of 12.0 and 1.0% respectively. The castor oil contains just 0.3% linolenic acid and does not contain any fatty acid with four double bonds which makes it an ideal feedstock for biodiesel (Lavanya et al., 2012). The presence of monounsaturated fatty acid as the major constituent makes the feedstock best suited as feedstock for biodiesel. There is an inverse relationship between cold flow property and the oxidation stability of the fuel. A high

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Fig. 2. Remediation techniques for metal polluted soils (Stegmann, 2001).

amount of unsaturated fatty acid is preferable for cold flow property of fuel, whereas, a high amount of saturated fatty acid is desirable. The castor oil possesses a high density. It has been attributed to the presence of ricinoleic acid that contains a hydroxyl group which causes strong intermolecular interactions through hydrogen bonds. This increases the bulk density of the castor oil (Ustra et al., 2013). Castor oil is hygroscopic and thus it becomes necessary to restrict its exposure to moisture as moisture content in feedstock may cause hindrance to transesterification. Among the non-edible oils, the acid value (2.1 mg KOH g−1 ) of castor oil is very less. Mejia et al. (2013) also reported the acid value of castor oil to be low i.e. 1.8 ± 0.1. This is an advantage as a low acid value will render an easy single step of transesterification. It is assumed that feed stocks with acid value lower than 4 mg KOH g−1 could undergo single step transesterification (Dias et al., 2013). The presence of water in the oil causes hydrolysis of the esters produced during the reaction. Sánchez-Cantú et al. (2013) reported the synthesis of biodiesel from castor oil using hydrocalumite-type compound as heterogeneous catalyst. A high conversion of the castor oil to biodiesel was reported in 14 h reaction time at room temperature. Encinar et al. (2012) reported a high yield of biodiesel (93.3%) from castor oil using ultrasound irradiation. The fuel properties of the biodiesel (acidity index, flash point) obtained from castor oil was found to meet the specification of biodiesel. However, the castor oil derived biodiesel was found to have a high value of cold filter plugging point (CFPP) (18 ◦ C) which will be a hindrance in its utilization in cold countries and in winter months in tropical countries. However, on contrary, Zuleta et al. (2012) studied the oxidation stability and CFPP of palm, jatropha and castor oils observed a much better fuel quality of biodiesel derived from castor oil. The induction time and cold filter plugging point of the castor oil biodiesel has been reported to be 31 h and −7 ◦ C. Zuleta et al. (2012) suggested blending of castor oil with jatropha oil to obtain biodiesel with better fuel characteristics. With a blend ratio of 75:25 of jatropha oil and castor oil, the induction time and CFPP were reported to be 7.56 h and −7 ◦ C respectively. A low vale of CFPP will enhance the usability of fuel at a low temperature. Thus, the biodiesel as fuel will have worldwide acceptance with a low temperature value of CFPP. However, a disadvantage with castor oil is its high viscosity

and high water content as compared to other plant oils (Kılıc¸ et al., 2013). Kılıc¸ et al. (2013) reported a high yield of biodiesel (99.81%) obtained from castor oil in a very short reaction time (10 min) at 65 ◦ C using catalyst, CH3 OK (1.5% wt of oil) and methanol to oil molar ratio of 7:1. Rodríguez-Guerrero et al. (2013) also studied about the synthesis of biodiesel from castor oil at supercritical temperature (200–350 ◦ C). The advantage with supercritical conditions and the pressure generated due to high temperature was a very less requirement of catalyst (0.1% wt) which was even lesser than that required for neutralization of the castor oil. A high biodiesel yield of 98% has been reported. Thomas et al. (2013) reported esterification of various oils (safflower, cottonseed, castor, used cotton seed) and found that the viscosity reduction among the oils was highest for castor oil even though it was most viscous. The highest conversion as fatty acid methyl ester has been reported to be observed with castor oil (93%) followed by safflower (89%), cottonseed (83%) and used cottonseed (80%) oil. Tsoutsos et al. (2013) utilized wastewater for the cultivation of sunflower and castor crop. It was observed that wastewater could be one of the medium for cultivation of the crops with a positive influence on the quality of oil for production of biodiesel. 4. Phytoremediation Environmental pollution with organic and inorganic contaminants like heavy metals, pesticides, petroleum compounds, PAHs, PCBs, etc. is a global problem and the development of sound technologies for the decontamination of impacted sites are therefore urgently required. These contaminants are frequently present in agricultural field near the industries like electroplating, leather, paint, coal based industries, etc. and make the soil unfit for the cultivation of the agricultural crops (Pandey and Singh, 2011; Sainger et al., 2011; Pandey et al., 2012). Heavy metals are not biodegradable, and are thus able to circulate in various ecosystems and bio-accumulate in different food chains. As described in Fig. 2 there are many physical, chemical and biological methods have been using for the remediation of contaminated sites from a very long time (Lee and Huffman, 1989; Felsot and Dzantor, 1995; Johnson et al., 1997; Hatakeda et al., 1999; Kummling et al., 2001; Stegmann,

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Table 1 Estimates of phytoremediation costs versus costs of established technologies. Contaminant

Phytoremediation costs

Estimated cost using other technologies

Reference

Heavy metals 1 hectare to a 15 cm depth (various contaminants) Site contaminated with petroleum hydrocarbons (site size not disclosed) 10 acres lead contaminated land Heavy metals

$80 per cubic yard $2500 to $15,000

$250 per cubic yard None listed

Black (1995) Cunningham et al. (1996)

$70,000

$850,000

Jipson (1996)

$500,000

$12 million

Plummer (1997)

$15–$40 per cubic meter

$100–$400

Schnoor et al. (1995)

2001; Yang et al., 2007). Phytoremediation has been recognized as a cost effective method for the remediation of contaminated soil and water resources (Table 1) (Black, 1995; Schnoor et al., 1995; Cunningham et al., 1996; Plummer, 1997). Phytoremediation is the process of removing of organic and/or inorganic pollutants (metals, pesticides, persistent organic pollutants, polycyclic aromatic hydrocarbon) from contaminated air, water and soil using plants which can accumulate, degrade or eliminate pollutants (Huang et al., 2011; Sainger et al., 2011; Pandey et al., 2012; Bauddh and Singh, 2012a,b, 2014; Pandey, 2013; Kumar et al., 2014) (Fig. 3). Although this is a cost effective method as plants can be managed easily, valuable metals can be recovered and reused. There are some limitations of this process especially when we are using edible crop plants of short life span with shallow rooting which produce comparatively less biomass and are more sensitive to toxicity. Further, incorporation of pollutants in human food chain is of the major concern. In this context, it becomes imperative to non-edible (even those are not being consumed by animals) industrial crops which can remediate polluted site with capital return. This technology can be used on large area for the remediation of water, soil, and even sediments contaminated with metals or other toxic chemicals (Ghosh and Singh, 2005; Huang et al., 2011; Sainger et al., 2014). In this review, therefore, we discuss the phytoremediation potential of one of the non-edible crop i.e. R. communis. Numerous plants have been identified to bear the high tolerance and efficiency of metal accumulation termed as hyperaccumulators (Brooks et al., 1977; Baker, 1981; Reeves and Brooks, 1983; Bani et al., 2015). Hyperaccumulators bear two basic features first tolerance to contaminants and second high biomass production (Antonovics et al., 1971; Baker, 1981; Reeves and Brooks, 1983; Brown et al., 1994; Kumar et al., 1995; Robinson et al., 1997; Rascio and Navari-Izzo, 2011). According to Van der Ent et al. (2013) the hyperaccumulator plants have the ability to accumulate 100 ␮g g−1 for Cd, Se and Tl; 300 ␮g g−1 for Co, Cu and Cr; 1000 ␮g g−1 for Ni, Pb and As; 3000 ␮g g−1 for Zn; and 10,000 ␮g g−1 for Mn, with plants cultivating in the natural environment. According to them, if above mentioned criteria are adopted, there are more than 500 plant taxa have been cited in the literature to date as hyperaccumulators for metals. Some examples of the plants which have been identified as hyperaccumulators are Alyssum murale, Sebertia acumulnata, Phyllanthus balgooyi, Noccaea caerulescens, Thlaspi caerulescens and Arabidopsis halleri, Pimelea leptospermoides, Rorippa globulosa, Solanum nigrum, Sedum alfredii, Viola baoshanensis, etc. (Reeves et al., 2001; Bert et al., 2002; Liu et al., 2004; Wei et al., 2006; Sun et al., 2007; Deng et al., 2008; Gao et al., 2010; Li et al., 2010a,b; Van der Ent et al., 2013). Albeit, hyperaccumulators has the ability to accumulate the metal in substantially higher amount but it is also important that the selected plant has the ability to acclimatize the contaminated environment. Numerous edible plants e.g. Oryza sativa (Jamil et al., 2013), Brassica sp. (Panwar et al., 2002; Robinson et al., 2003; P. Sharma

et al., 2008; Sankaran and Ebbs, 2008; Nouairi and Ammar, 2009; A. Sharma et al., 2010; Giansoldati et al., 2012; Sainger et al., 2014), Raphanus sativus (Shevyakova et al., 2011), etc. A few non-edible plants e.g. J. curcas, Ipomoea carnea, Calotropis procera, Lantana camara, Parthenium hysterophorus, Millettia pinnata (Sanghamitra et al., 2011; Varun et al., 2011; Pandey et al., 2012; Tulod et al., 2012) have also been tested and recommended for phytoremediation of contaminated sites. In previous studies it has been also found that biomass production of these crops grown in metal contaminated soil decreased drastically due to the high bioaccumulation in their roots and shoots (Bauddh and Singh, 2011, 2012a,b; Sainger et al., 2014). Therefore, to address this problem many scientists have been suggested to use chemical chelants for the enhancement of phytoextraction of soils contaminated with heavy metals (Huang et al., 1997; Liphadzi et al., 2003; Garba et al., 2012a). Many chelants including EDTA (ethylenediaminetetraacetic acid), CDTA (trans-1,2-diaminocyclohexane-N,N,N ,N -tetraacetic acid), EDDHA [etylenediamine-di (o-hydroxyphenylacetic acid)], etc. have been addressed by several researchers to enhance phytoextraction potential of the plants (Shen et al., 2002; Meers et al., 2005a; Lin et al., 2009; Garba et al., 2012a,b). The chemical chelating agents have been reported to change the physicochemical and biological properties of soil (Ultra et al., 2005). Several chelating agents have been reported to cause adverse effects of soil nematodes (Romkens et al., 2002), and inhibition of arbuscular mycorrhizal development (Grcman et al., 2001). It has been also reported in many studies that the application of these chemical chelants decrease biomass yields of the plants (Chen and Cutright, 2001; Madrid et al., 2003; Chen et al., 2004). The in situ application of chelants may pose the potential risk of causing groundwater pollution through uncontrolled metal solubilization and migration (Wu et al., 1999; Lombi et al., 2001; Nowack, 2002; Romkens et al., 2002; Shen et al., 2002; Jiang et al., 2003; Madrid et al., 2003; Thayalakumaran et al., 2003; Wenzel et al., 2003; Chen et al., 2004). 4.1. Phytoremediation of efficiency of edible crops Many studies conducted to evaluate the potential of edible crops (Table 2) for phytoremediation of toxic contaminants throughout the world in last few decades (Ebbs and Kochian, 1997; Marguí et al., 2009; Adesodun et al., 2010; Angelova et al., 2012). Herbaceous species have been also reported as a promising candidate (Chaney et al., 1997). Sunflower (Helianthus annuus), commonly grows as oil yielding crop, has been found to be very extensively studied crop to find its suitability toward phytoremediation of many toxic heavy metals like Pb, Zn, Cd, Ni, etc. (Marguí et al., 2009; Adesodun et al., 2010; Mukhtar et al., 2010; Angelova et al., 2012). Many crop species have been used for phytoremediation purposes like wheat (Triticum aestivum L) (Chitra et al., 2011), potato (Solanum tuberosum L.), tomato (Solanum lycopersicum) etc. (Antonious and Snyder, 2007; Uera et al., 2007; Khan et al., 2011; Salaskar et al., 2011), corn (Zea mays) (Chitra et al., 2011; Mojiri, 2011) sunflower (Zadeh et al., 2008). Many leafy vegetables like

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spinach (Spinacia oleracea L.), radish (Raphanus sativus), Amaranthus, etc. are also using for the phytoremediation of hazardous metals (Shevyakova et al., 2011; Brar and Malhi, 2007). A Scopus based survey was carried out by Vamerali et al. (2010) for the period 1995–2009 in order to take a census of crop species involved in phytoremediation research of heavy metals throughout the world (Fig. 4). According to this study, Brassica juncea (L.) an oil producing crop was found to be most cited (148 citations) among eight studied crops followed by H. annuus (57 citations), Brassica napus and Z. mays (both 39 citations). Maximum species (8) of Poaceae family are using for the phytoremediation followed by Brassicaceae (5), Fabaceae (4) and Asteraceae (1). Brassicaceae family attracted maximum number of researchers for phytoremediation purposes due to its high accumulating ability of contaminants such as Cd, Cr, Cu, Mn, Pb, Se and Zn (Vamerali et al., 2010). It has been appeared that the above discussed edible crops cannot be recommended for the phytoremediation of the contaminated sites due to (1) very short lifespan, (2) high palatability and (3) low biomass productivity (Pandey and Singh, 2011). In

addition, toxic impacts of contaminants may expand through food chain and can cause diseases in human as well as animals. In the phytoremediation context of contaminated sites, the plants should be perennial in nature, un-palatable, high biomass productive, tolerant to local biotic and abiotic stresses (Pandey and Singh, 2011). The non-edible crops (unpalatable) including R. communis, J. curcas, I. carnea, C. procera, L. camara, P. hysterophorus, M. pinnata, Sacharum munja, Sacharum raveni, Nerium oleander, etc. have been recognized for their application to mitigate the contaminated sites (Mubeen et al., 2010; Sanghamitra et al., 2011; Varun et al., 2011; Pandey et al., 2012; Tulod et al., 2012). In above crops, R. communis and J. curcas seem sustainable crops for phytoremediation purposes because they have commercial values worldwide and can be used globally to remediate the contaminated large areas of agricultural lands. R. communis is able to grow easily in the wasteland soils having the multiple stresses like salinity, drought as well as heavy metals (Babita et al., 2010; Bauddh and Singh, 2012a,b). J. curcas is also able to grow in a similar manner but the yield of this plant does not meet till the date in some countries of the world for commercialization purposes. Therefore,

Fig. 3. Schematic presentation of mechanism and types of phytoremediation of trace metals.

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Table 2 Edible crops used for the phytoremediation of contaminated of different sites. Plants

Nature of the plants

Used for removal of contaminants

Reference

Amaranthus sps Tomato (Lycopersicon esculentum) Sun flowers (Helianthus annuus) Sunflowers (Helianthus annuus) Sunflowers (Helianthus annuus) Sunflower (Helianthus annuus) Tobacco (Nicotiana tabacum L.) corn (Zea mays L.) and wheat (Triticum aestivum L.) Potato (Solanum tuberosum L.) Wheat (Triticum vulgare) Tomato (Solanum lycopersicum) Spinach (Spinacia oleracea L.) Corn (Zea mays) Sunflower (Helianthus annuus) Amaranthus (Amaranthus sp.) Spinach (Spinacia oleracea L.)

Leafy vegetal (herb) Vegetable herb

Ni and Fe Co

Shevyakova et al. (2011) Thomas et al. (2013)

Oil yielding crop (herb)

Zn and Pb

Adesodun et al. (2010)

Oil yielding crop (herb)

Pb and Zn

Marguí et al. (2009)

Oil yielding crop (herb)

Pb, Zn and Cd

Angelova et al. (2012)

Oil yielding crop (herb)

Ni and Pb

Mukhtar et al. (2010)

Herbs

Cd

Chitra et al. (2011)

Herb

Cd, Cr, Ni, Pb, Zn, Cu and Mo

Antonious and Snyder (2007)

Herb Vegetable (herb)

Methyl parathion and p-nitrophenol Ethidium bromide (EtBr)

Khan et al. (2011) Uera et al. (2007)

Leafy vegetable (herb)

Cd

Salaskar et al. (2011)

Herb Oil yielding crop (herb)

Cd and Pb Cd

Mojiri (2011) Zadeh et al. (2008)

Leafy vegetable (herb)

Cd

Zadeh et al. (2008)

Leafy vegetal (herb)

Cr

Brar and Malhi (2007)

148

140 120 100 57

Asteraceae

Brassicaceae

Fabaceae

9

9

4

2

Sorghum spp

Triticum spp.

Avena sativa L.

Oryza sativa L.

Hordeum vulgare

2

19 16 13 Festuca spp

7

Lolium spp

8

Zea mays

9

Pisum sativum

4

Medicago sativa

11

Phaseolus vulgaris

13

Glycine max

Brassica napus

Brassica juncea

Helianthus annuus

20 0

39

39

40

Sinapis alba

60

Brassica carinata

80

Raphanus sativus

Number of citations*

160

Poaceae

Fig. 4. Citation matrixof edible crops used as phytoremediation. *Citations of the papers are presented are of 9 years for Helianthus annuus, 14 years for Brassica juncea, 13 years for B. napus, 10 years for Raphanus sativus, 11 years for Brassica carinata, 4 years for Sinapis alba, 5 years for Glycine max, 7 years for Phaseolus vulgaris, 7 years for Medicago sativa, 4 years for Pisum sativum, 10 years for Zea mays, 7 years for Lolium spp., 11 years for Festuca spp., 7 years for Hordeum vulgare, 7 years for Sorghum spp., 5 years for Triticum spp., 10 years for Avena sativa and 1 years for Oryza sativa (Vamerali et al., 2010).

for sustainable phytoremediation point of view, R. communis can be established as a most commercial oil yielding crops for various industrial uses than the previous one globally. 4.2. Phytoremediation potential of tree species The suitability of various tree species e.g. willow (Salix spp.) Delonex regia, Leucaena leucocephala, Thespesia populneoides, Populus tremula, Pinus sylvestris, Betula pendula, etc. have been investigated for the phytoremediation of heavy metals (Rosselli

et al., 2003; Pulford and Watson, 2003; Meers et al., 2005b; Mleczek et al., 2009, 2010; Harada et al., 2011; Nevel et al., 2011; Vollenweider et al., 2011; Langer et al., 2012; Ismail et al., 2013; Dmuchowski et al., 2014). These trees have been found to bear excellent tolerance and potential to accumulate numerous heavy metals. Besides of good potential, the tree requires very long time to complete its life cycle. Several tree species have life cycle of more than 100 years. This time period is enough for the completion of 100 life cycles of annual herbs and shrubs which also possess excellent tolerance and metal accumulation efficiency.

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4.3. Phytoremediation potential of R. communis Many reports are available which indicate that castor has good tolerance and phytoremediation potential to remove the toxic metals from the contaminated sites (Table 3) (Raskin et al., 1994; Rockwood et al., 2004; Cecchi and Zanchi, 2005; Romeiro et al., 2006; Malarkodi et al., 2008; Rajkumar and Freitas, 2008; Niu et al., 2009; Shi and Cai, 2009; Mubeen et al., 2010; Ma et al., 2011; Huang et al., 2011; Adhikari and Kumar, 2012; Bauddh and Singh, 2012a,b, 2014). R. communis is a perennial and oil yielding crop and can continue the removal of toxic metals as well as other contaminants throughout the year for a longer time within the same sowing which will reduce the operating and maintenance cost. R. communis is a wild plant and having capacity to produce high biomass without using any fertilizer as well as there is no need of chelants for phytoremediation. R. communis is one of such plant species, which has attracted extensive attention because of its capability to grow in heavily polluted sites having multiple stresses i.e. salinity and drought (Babita et al., 2010; Bauddh and Singh, 2012b). In addition, R. communis is an industrial crop with manifold non-food uses and has been considered as a cash companion crop. Bauddh and Singh (2012b, 2014) conducted a study and compared castor plant with Indian mustard for phytoremediation potential of Cd in presence of salinity and drought. The results revealed that in presence of salinity and drought, castor showed stronger self-protection ability in the form of proline bioaccumulation than Indian mustard. Total Cd extraction was much higher in the roots of R. communis than that of B. juncea in the salinity and drought and it accumulated 17 and 1.5 fold higher Cd in the roots and shoots, respectively than that of B. juncea. A study conducted in 2014 by Bauddh and Singh was aimed to evaluate the effects of different fertilizers (vermicompost, biofertilizers, slow released fertilizers and inorganic fertilizers; urea and diammonium phosphate) on Cd phytoremediation potential of R. communis and B. juncea. The results revealed that the application of inorganic fertilizers and biofertilizers reduced the toxic effects of Cd with enhanced accumulation of the metal in both the species. Vermicompost and slow release fertilizers reduced the mobility of Cd as well as the metal toxicity with enhanced biomass production. R. communis produced substantially higher biomass which results the many fold higher Cd extraction by this plant in comparison with B. juncea. Niu et al. (2009) has been also reported that R. communis is able to accumulate a higher amount of Cd and Pb in its roots and shoots. Romeiro et al. (2006) recommended R. communis as hyperaccumulator species for Pb. R. communis accumulated 10.54–24.61 g Pb kg−1 dry weight of the plants and according to Raskin et al. (1994), Pb hyperaccumulator plants are those capable of extracting and accumulating over 1.0 g kg−1 dry weight in their tissues. In a study conducted by Malarkodi et al. (2008), it was found that R. communis accumulated higher amount of Ni (i.e. 747.3–874.6 mg kg−1 dry weight) during its cultivation in a field condition and which was further increased by the application of organic manure (farm yard manure and poultry manure). R. communis plant is found to have good efficiency to extract the heavy metals (Mn, Ni, Pb and V) from spent lubricating oil contaminated soil at concentrations of 1–6% (w/w oil/soil) with an increased plants growth which make the plant advance in this perspective (Vwioko et al., 2006). R. communis is also reported to absorb barium (Ba) grown in area polluted with scrap metal residue by Abreu et al. (2012). Coscione and Berton (2009) reported that R. communis has good potential to extract the Ba from the contaminated soil. Many authors reported that the plant has ability to grow smoothly and extract a number of heavy metals (Cd, Zn, Cr, CU, Pb, Mn and Fe) when cultivated in the fly ash contaminated lands (Pandey, 2013; Coscione and Berton, 2009). Different microbial inoculation e.g.

Pseudomonas sp. PsM6 or P. jessenii PjM15 (Rajkumar and Freitas, 2008), PGPB SRS8 (Ma et al., 2011), PGPRs (Romeiro et al., 2006) increased the shoot and root biomass, reduces the toxicity of the metal for plants and facilitate its mobilization from soil when incorporated as amendment in soil with cultivation of R. communis. Adhikari and Kumar (2012) have reported that roots of Ni treated R. communis show decreased number of cells in the cortex region. To assess the potential of native plant species for phytoremediation, Mahmud et al. (2008) collected plant and soil samples from 4 As contaminated (groundwater) districts in Bangladesh. They made the criteria used for selecting plants for phytoremediation of high bioconcentration factors (BCFs) and translocation factors (TFs) of As. From the results of a screening of 49 plant species belonging to 29 families, only one species of fern (Dryopteris filix-mas), three herbs (Blumea lacera, Mikania cordata, and Ageratum conyzoides), and two shrubs (Clerodendrum trichotomum and R. communis) were found to be suitable for phytoremediation. Mahmud et al. (2008) conducted a study to evaluate and compare As accumulation, resistance, tolerance and avoidance by two plant species: common buckwheat (Fagopyrum esculentum L.) and R. communis. They demonstrated that castor oil plant has higher tolerance and lower avoidance to arsenic, whereas common buckwheat has higher resistance, lower tolerance and higher avoidance to arsenic, respectively. The findings of their study suggest that castor plants may be an important crop for phytoremediation of arsenic contaminated soils. Olivares et al. (2013) performed a study in mine tailings containing high concentrations of Cu, Zn, Mn, Pb and Cd by using R. communis. The Ricinus seed-oil content was high between 41% and 64%, seeds from San Francisco site 6 had the highest oil content, while these from site 7 had the lowest. A negatively correlated value was observed with seed-oil content and root concentration of Cu, Zn, Pb and Cd, but no correlation was observed with the extractable-metals. According to its shoot metal concentrations and translocation factor, castor bean is not a metal accumulator plant. They suggested that primary colonizing plant is well suited to cope with the local toxic conditions and can be useful for the stabilization of these residues, and for then decreasing metal bioavailability, dispersion and human health risks on these barren tailings heaps and in the surrounding area. They also suggested that the application of this plant for the purpose of phytoremediation is with combined oil production and a phytostabilization role for Ricinus plants in metal mine tailings and this may be give a new value to suitable metal-polluted areas. Huang et al. (2011) compared 23 genotypes of R. communis to assess the ability to mobilizing and uptake of Cd and DDTs (p,p0DDT, o,p0-DDT, p,p0-DDD and p,p0-DDE) in the co-contaminated soil. For the experiment, they collected the soil which was contaminated naturally with DDT (0.35 mg kg−1 ) and Cd (0.42 mg kg−1 ). Again the soil samples were spiked with DDTs and Cd at the rate of 1.7 and 2.8 mg kg−1 soil, respectively. The plant genotypes varied largely in uptake and accumulation of DDTs and Cd, with concentrations of 0.37, 0.43 and 70.51 for DDTs, and 1.22, 2.27 and 37.63 mg kg−1 dw for Cd in leaf, stem and root, respectively. The total uptake of DDTs and Cd varied from 83.1 to 267.8 and 66.0 to 155.1 g per pot, respectively. The results of this study indicate that R. communis has great potential for removing DDTs and Cd from contaminated soils attributed to its fast growth, high biomass, strong absorption and accumulation for both DDTs and Cd. Andreazza et al. (2013) cultivated castor bean plants in soil with toxic levels of Cu for 57 d exhibited high biomass production. They reported a high tolerance index of roots’ fresh mass and shoots’ dry mass, a high level of Cu bioaccumulation in the roots and also, a robust capacity for Cu phytostabilization of this plant. According to them castor bean plants did not significantly deplete soil N, P, and Mg during its cultivation. Plants cultivated in three different

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Table 3 Heavy metal accumulation potential of Ricinus communis from contaminated soils. Metal contamination

Contamination level

Exposure time

Accumulation of metal (␮g g−1 dry wt) Root

Shoot

Cadmium (CdCl2 )

2.8 mg Cd kg−1 soil

60 days

37.63

1.22 (leaves) and 2.27 (stem)

Cadmium (CdCl2 )

25–150 mg Cd kg−1 soil

60 days

1328.47

189.92 (shoots)

90 days

1255.52

235.82 (shoots)

28 days

2779

915

40 days

24,000–25,000

550–600 (shoots)

–

217.8

174.5 (stem) and 97.80 (leaves)

35 days

185.00

35.0 (stem) and 53.0 (leaves)

5 weeks

45–50

30–35 (shoots)

5 weeks

300

150–200 (shoots)

300–320 455

30–40 (stem) and roots 0–30 (leaves) 300 (shoots)

Cadmium (CdCl2 ) Zinc (ZnSO4 ·7H2 O) Lead Nickel (NiCl2 )

−1

100 mg Cd kg soil with salinity (100 mM) 0.0–800 mg kg−1 soil 400 ␮mol L−1 nutrient solution 164.5 mg kg−1 soil −1

Nickel

275 mg Ni kg

Cadmium

20 mg L−1

Lead

400 mg L−1

soil

−1

Nickel (NiCl2 ) Nickel (NiCl2 )

450 mg kg soil 0–250 Ni kg−1 soil

45 days 45 days

Barium (BaSO4 )

0–300 mg Ba kg−1 soil

7, 14, 21 and 28 days

Arsenic (Na2 HASO4 ·7H2 O) Arsenic (NaZHAsO4 )

0–5000 ␮mol L−1

30 days

467.38

44.60

9.13 (␮g g

–

40

48.75

Arsenic (NaZHAsO4 )

0–100 ppm

6 weeks

Nickel (NiSO4 )

150, 300 and 600 ppm

12 months

Lead Pb(NO3 )2·H2 O

50, 100 and 200 mg Pb kg−1 soil 5, 10 and 20 mg Pb kg−1 soil

5 weeks

446.03 (plant)

5 weeks

42.56 (plant)

Cadmium (CdCl2 )

−1

)

types of soil contaminated with Cu viz. two Cu contaminated vineyard soils (Inceptisol and Mollisol) and a Cu mining waste (40% of native soil + 60% of Cu mining waste) exhibited a strong potential for Cu phytoaccumulation, with values of 5900, 3052 and 2805 g ha−1 . Wang et al. (2013) conducted a research to evaluate the effects of co-planting of S. alfredii with ryegrass (L. perenne) or castor (R. communis) on the heavy metals and polycyclic aromatic hydrocarbon (PAH) extraction from the contaminated soils. They found that co-planting of S. alfredii with ryegrass or castor significantly enhanced the pyrene and anthracene dissipation as compared to that in the bare soil or S. alfredii monoculture. This appears to be due to the increased soil microbial population and activities in both co-planting treatments. Co-planting of S. alfredii with rye grass or castor provides a promising strategy to mitigate both metal and PAH contaminants from the soils. Shi and Cai (2009) conducted a study to compare eight energy crops for the removal of Cd from the contaminated soil. All the studied crops were moderately tolerant to Cd toxicity, with 4 species i.e. hemp (Cannabis sativa), flax (Linum usitatissimum), castor (R. communis) and peanut (Arachis hypogaea) were found to be more tolerant than the others. These results demonstrate that it is possible to grow energy crops on Cd contaminated soil and they may become excellent candidates for phytoremediation. Giordani et al. (2005) studied seven herbaceous crops viz. barley (Hordeum vulgaris), cabbage (B. juncea), spinach (S. oleracea), sorghum (Sorgum vulgare), bean (Phaseolus vulgaris), tomato (S. lycopersicum), and one shrub i.e. castor (R. communis) to assess the phytoremediation potential of Ni from contaminated soil. They found that R. communis has good efficiency to accumulated the metal in their roots and shoots. Zhi-Xin et al. (2007) studied Cd and Pb accumulation ability of four plants i.e. sunflower (H. annuus L.), mustard

16.6

16.74 (plant) 67.2

48.7 (shoots)

Reference

Huang et al. (2011) Bauddh and Singh (2012a) Bauddh and Singh (2012b) Shi and Cai (2009) Romeiro et al. (2006) Malarkodi et al. (2008) Rajkumar and Freitas (2008) Niu et al. (2009) Niu et al. (2009) Ma et al. (2011) Adhikari and Kumar (2012) Abreu et al. (2012) Melo et al. (2009) Mahmud et al. (2008) Mahmud et al. (2006) Giordani et al. (2005) Zhi-Xin et al. (2007) Zhi-Xin et al. (2007)

(B. juncea L.), alfalfa (Medicago sativa L.), castor (R. communis L.) in hydroponic cultures. They estimated that R. communis accumulated a substantial amount of both the metals during five weeks of cultivation. 5. Restoration of degraded land Rehabilitation of vegetation is single and most important process among physical, chemical and biological mode for the restoration of degraded soils (Zhou et al., 2003). Castor bean (R. communis L.) is not only important oilseed crop but also has tolerance to many abiotic stresses like heavy metal, salinity and drought (Babita et al., 2010; Bauddh and Singh, 2012b). These properties of castor bean make them a capable candidate for amelioration of such soils with some value added benefits like biofuel productions (Barnes et al., 2009). Wu et al. (2012) conducted a study and found that after planting castor bean for two continuous growing seasons, soil salinity (salt content) was 0.92% lower than that under the control scenario (2.86%) and the value of electrical conductivity (EC) was also decreased significantly as well as it showed significant ameliorative effects on soil bulk density and soil nutrients availability (Fig. 5). Alguacil et al. (2012) have reported that the soil microbial activity and diversity increased in the castor planted plots than that of the control with other nutritional components. Bacterial population like halophilic, phosphate-solubilizing, potassium-solubilizing, cellulose decomposing, ammonifying and nitrogen-fixing bacteria increased in population significantly in the planted plots. Some other studies have also shown that castor bean (R. communis) has high salt tolerance and may grow up to 6–15 feet (2–5 m) in one season with full sunlight, heat and adequate moisture on saline land (Li et al., 2010a,b).

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35

a

Before R. communis cultivation After R. communis cultivation

b

30 25 20

a 15 10

a

b b

a

a

a

a

b

5

b

0

Organic matter Hydrolyzable N (g kg−1) (mg kg−1)

pH (1:2.5)

Available P (mg kg−1)

CEC (mol kg−1)

EC (1:5) (mS/cm)

Soil physicochemical characteristics

Soil erosion is one of the serious reasons for the degradation of agricultural lands throughout the world. There are various soil management practices applied, such as the use of diverse crops, strip cropping, increasing crop cover, multiple cropping, agroforestry, mulching, conservation tillage, ridging, and furrowing help to decrease the soil erosion. Growing of shrubs, which are deep rooted, may help to protect soil erosion which may also provide some value added products. Many crop plants including shrubs are not able to grow in the waste land soil. Castor can be easily cultivable in the waste land being its wild nature; simultaneously, it will give an opportunity to the farmers to earn money by using its seeds as a byproduct. 6. Industrial byproducts The production of oil from castor generates two main byproducts i.e. capsule husks and cake. Capsule husk produced when the seeds separated from the fruits and cake produced, when the oil is extracted from seeds. As discussed by Lima et al. (2011) castor seed weight corresponds of about 62% of the fruit weight and the efficiency of oil extraction is about 47% (w:w). The production of one ton of castor oil results in 1.31 tons of husks and 1.13 tons of cake. It has been investigated that the annual castor seed production in the world is around 1.2 × 103 tons (Miller et al., 2009). It is demonstrated that the toxic protein ricin is destroyed by heat in the oil extraction process (Zhou et al., 2003). While the feed alternative is not possible, most of the castor meal produced in the world is used as organic fertilizer (Gupta et al., 2004; Udeshi, 2004). Castor cake has about 43% protein content and is often used as an organic fertilizer because it is as an excellent source of nitrogen with insecticide and nematicide properties (Lima et al., 2011). Martín et al. (2010) have proposed that the high protein and carbohydrate content in castor press cake can be used as a potential feedstock following some fermentation processes. Lima et al. (2011) was found castor cake and husks fit for the agricultural purposes as fertilizer due to its composition (Fig. 6). Both the cake and husks of castor contain good amount of nitrogen, phosphorous, potassium, calcium and magnesium. 7. Other potential uses of R. communis R. communis has a numbers of potential uses like biofuel production, medicinal and industrial applications. The plants are cultivated at a major scale throughout the world due to

Nutrient content in castor meal and husk (%)

Fig. 5. Physico-chemical characteristics of the soil before and after planting R. communis for two growth seasons in a wasteland soil (Wu et al., 2012). Different alphabets express the significant differences between the data observed before and after R. communis cultivation.

80 70 60 50 40 30 20 10 0

Castor cake

Nitrogen

Phosphorus

Castor husks

Potassium Nutrients

Calcium

Magnesium

Fig. 6. Chemical composition of castor cake and castor husks (Zahir et al., 2010).

its multipurpose nature (Scarpa and Guerci, 1982). The oil of R. communis and its derivatives have many applications in the manufacturing of jet engine, aircraft and space rockets lubricants, soaps, hydraulic and brake fluids, paints varnish industry, dyes, cold resistant plastics, coatings, inks, waxes and polishes, pharmaceuticals and perfumes. It is also used in the manufacturing of a wide range of products like artificial leather, nylon fibers, fiber optics, bullet proof glass and bone prostheses and as an antifreeze for fuels (Ogunniyi, 2006; Torres et al., 2013). The extracts of castor have acaricidal and insecticidal properties which work against Haemaphysalis bispinosa and hematophagous fly Hippobosca maculata (Zahir et al., 2010). Oil of R. communis is of economic interest having multiple applications like cosmetic, medical and chemical applications. Wale and Assegie (2015) have been investigated the biocidal activity of castor bean oil against a maize weevil, Sitophilus zeamais. They found that the mortality of S. zeamais was increased with increasing dose of castor bean oil. It has been observed that 2 ml of castor bean oil was enough to destroy almost 50% of the weevils. Different parts of this plant such as roots, stem leaves and fruits collected as raw drugs by local communities and traded in the market as a raw material for herbal industries (Uniyal et al., 2006; Archana et al., 2011). The presence of significant concentration of total protein, total sugar, reducing sugar, some identified free amino acids and sugars provided good correlation among antimicrobial compounds which are present in the plants’ extracts and have capability to kill the pathogens or inhibit the growth of microbes (Singh et al., 2009; Solomon and Shittu, 2010). In the medical point of view, castor bean has been used with confidence for the treatment of several diseases like asthma, boils burns cold, cholera, cancer, carbuncle convulsions, etc. (Boeck-Neto et al.,

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employment generation, wastelands utilization, carbon sequestration, soil erosion controller as well as a potential phytoremediator.

Acknowledgments Authors are thankful to Dr. Rahul Chaturvedi, Assistant Professor, Centre for English Studies, CUJ, Ranchi for his help and support to improve the language of the paper. We are also thankful to anonymous reviewers for their constructive suggestions and comments which have substantially improved the quality of the manuscript.

References

Fig. 7. Multi-aspects of Ricinus communis.

2005; Lakshminarayana and Sujatha, 2005; Korwar et al., 2006; Naqvi et al., 2011). 8. Conclusion and future prospects From the aforesaid discussion, it is clear that R. communis may be developed as multipurpose crop with especial attention of its ability to accumulate the higher amount of heavy metals (Fig. 7). New biotechnological approaches should be applied for making enhanced desirable characteristics in genetically modified crop. The non-edible nature of this plant makes it more suitable for the purpose of phytoremediation with energy production. Generally farmers cultivate this crop in the fertile and agricultural land, however, this plant could be cultivate in industrially polluted soil. It is also found that R. communis tolerant to other two major abiotic stresses i.e. salinity and drought. This property makes R. communis able to cultivate in salt or drought affected land which are not fit for the agronomic practices. It has also reported that the cultivation of this plant in waste land may be helpful to improve the quality of soil. In contrast to jatropha which is a major biodiesel plant, the yield of R. communis is much better and there are no technical interventions required in this regards. The seed yield may be increased also by using some agronomic practices such as mass multiplication of elite germplasm by tissue culture or macropropagation, standardization of optimum plant density (spacing between plants), making good plant architecture by pruning, using flower and growth enhancing hormones, to appropriate male: female ratio in the flowers. Major oil crops are shrubs which may help in carbon sequestration and provide socio-economic returns. Furthermore, R. communis biodiesel offers to development a clean and sound environment with economic and ecological advantages that include lowering of pollutant emissions (greenhouse gases), increasing of rural employment, energy security and decreasing the dependency on fossil fuel (imported oil). Multiple benefits of R. communis can be achieved by future critical research efforts to provide new impetus for local and regional sustainable development. There are many benefits and potential of R. communis such as reliable biodiesel supply, reduction of green house gas emissions, cost effectiveness, community development, biogas production, medicinal value,

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