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Accelerating Phytoremediation of Degraded Agricultural Soils Utilizing Rhizobacteria and Endophytes: a review

Journal: Environmental Reviews

Manuscript ID er-2019-0020.R3

Manuscript Type: Review

Date Submitted by the Author: 07-Sep-2019

Complete List of Authors: Song, Chun; Sichuan Agricultural University - Chengdu Campus, Sarpong, Clement; Sichuan Agricultural University - Chengdu CampusHe, Jinsong; Sichuan Agricultural University - Chengdu CampusShen, Fei; Sichuan Agricultural University - Chengdu CampusZhang, Jing; Sichuan Agricultural University - Chengdu CampusYang, Gang; Sichuan Agricultural University - Chengdu CampusLong, Lulu; Sichuan Agricultural University - Chengdu CampusTian, Dong; Sichuan Agricultural University - Chengdu CampusZhu, Ying; Sichuan Agricultural University - Chengdu CampusDeng, Shihuai; Sichuan Agricultural University - Chengdu Campus

Is this manuscript invited for consideration in a Special

Issue? :Not applicable (regular submission)

Keyword: Rhizobacteria, Plasticulture, Heavy metals, Agrochemicals, Hyperaccumulation

https://mc06.manuscriptcentral.com/er-pubs

Environmental Reviews

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1 Accelerating Phytoremediation of Degraded Agricultural Soils

2 Utilizing Rhizobacteria and Endophytes: a review

3 Chun Song, Clement Kyei Sarpong, Jinsong He, Fei Shen, Jing Zhang, Gang Yang, Lulu Long,

4 Dong Tian, Ying Zhu, Shihuai Deng

5 Institute of Ecological and Environmental Sciences, College of Environmental Sciences, Sichuan

6 Agricultural University, Chengdu 611130, China

7 Corresponding author: Chun Song (email: [email protected]).

8 Chun Song and Clement Kyei Sarpong contributed equally to this manuscript, considered as co-first

9 authors.

10 Abstract: Agricultural activities and agro-inputs particularly chemical fertilizers, farmyard manure,

11 pesticide, sewage sludge, plastic mulch, irrigation, etc. are the primary source of pollutants in

12 farmlands. Agricultural land degradation has become a major concern as it poses a threat to crop

13 productivity. In recent years, microbial assisted phytoremediation has gained much attention as a

14 promising in situ remediation technology for cleaning polluted soils. Several beneficial rhizobacteria

15 and endophytes facilitate phytoremediation by stimulating innate plant growth-promoting traits such

16 as the production of siderophores, phytohormones, and chelators in addition to their ability to

17 biodegrade contaminants and enhance their removal. Current studies on microbial mediated

18 phytoremediation are demonstrating significant remediation potential. However, there are several

19 challenges in the field that restrict the remediation process. Here we highlight the specific traits,

20 mechanisms, roles, advantages, and problems associated with microbial assisted phytoremediation.

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21 Keywords: Rhizobacteria; Plasticulture; Heavy metals; Agrochemicals; Hyperaccumulation

22 1. Introduction

23 Agricultural activities have increased significantly and represent one of the largest and major

24 economically essential sectors in many countries. It serves as a primary source of livelihood and

25 economic backbone. In spite of its multiple benefits, pollution caused by agricultural activities lead to

26 several environmental and health hazards (Abbasi et al. 2014). Its activities contribute vast list of

27 pollutants including heavy metals, toxic substances, plastic, greenhouse gases, particulates, pathogens,

28 etc. through excessive use of synthetic chemical fertilizer and pesticides (Vejan et al. 2016). Polluted

29 agricultural ecosystems are impacting adversely on plants, microorganisms, aquatic organism, and

30 critical life functioning activities such as mineralization, immobilization, and nitrification that is

31 ultimately affecting soil productivity (Batayneh 2012). As a matter of fact, agriculture is potentially

32 falling prey to its success (Emilie et al. 2017).

33 As noted, humans engender a broad spectrum of pollutants from a myriad of the hard-to-pinpoint

34 source. For that reason and several others, numerous agricultural pollutants go unnoticed and

35 unmeasured (Emilie et al. 2017). Nevertheless, for every single effect of soil deterioration, there is an

36 underlying cause (Saturday 2018). Dubois (2011) reported that one-third to half of the agricultural

37 lands worldwide was in a deteriorating state whereas a quarter was extremely degraded. For a

38 sustainable agricultural production, not only should polluted soils be remediated, however, crops

39 produced need to be equipped with drought tolerance, disease resistance, heavy metal stress resistance,

40 salt tolerance and better nutritional value (Vejan et al. 2016). The available physicochemical

41 remediating techniques are already providing encouraging remediation results (Emilie et al. 2017),

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42 however, these remediating techniques mostly cause secondary pollution and further annihilate soil

43 productivity (Oh et al. 2013). Further, the costs involved in carrying out these remediation technologies

44 are extremely high impeding its extensive application (Oh et al. 2013). Generally, technical

45 applicability, cost-effectiveness and eco-friendliness are crucial parameters in selecting a suitable

46 remediation solution (Glick 2010; Acheampong et al. 2010). One possibility to remediate

47 contaminated soils and achieve the aforementioned crop qualities is the use of rhizobacteria and

48 endophytes. Plant-microorganism bioremediation could ameliorate contaminated soils, stimulate plant

49 health and enhance plant growth without environmental effects (Calvo et al. 2014). Bioremediation is

50 the application of biological processes to remediate polluted soils. Phytoremediation is a technique of

51 the bioremediation process that utilizes hyperaccumulator plant species to assimilate contaminants into

52 their tissues (Oh et al. 2013). The efficiency of plant-microbes to decontaminate soils is due to the

53 potential of rhizospheric microorganisms and plants to phytoextrate, phytodegrade, and rhizofiltrate

54 pollutants as well as their ability to alter pH, produce phytohormones, and to release chelators, etc.

55 (Chaudhry et al. 2005; Glick 2010).

56 This technique of plant-microbes bioremediation is still at an early stage, and large-scale application

57 is still limited. For global and commercial use of this technology, it is relevant that public awareness

58 and precise information is made available to facilitate its acceptability as a useful worldwide

59 sustainable technology. This article is aimed at reviewing the causes of agricultural pollutants and

60 provides a state-of-the-art description of how beneficial the integration between plant and rhizobacteria

61 can be exploited as a unique biotechnology that can accelerate the remediation of degraded soils and

62 yield economic value.

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63 2. Degradation of Farmland Soils

64 Since the early days of agriculture, human activities have altered vegetation cover and soil properties.

65 Soil degradation is a repercussion of anthropogenic activity and ecosystem disturbances that cause

66 alternation in various aspects of soil properties and reduce crop production (Mikha et al. 2014). Among

67 all soil degradation examples, chemically degraded farmlands deserve special attention. With rapid

68 worldwide industrialization, urbanization and intensive use of farmland, a wide variety of chemicals

69 including heavy metals, chlorinated solvents, pesticides, among others are constantly being discharged

70 into the soil milieu. (FAO 2015). Primarily, contaminations of farmlands are chiefly mediated by

71 excess use of agrochemicals (pesticides, insecticides, synthetic fertilizers, etc.), sewage sludge,

72 livestock manure and plastic materials. However, chemical intrusion in soils differs significantly

73 among regions due to the difference in location and activities (Tetteh 2015). Contaminants in most

74 Asian arable lands are related to parent material, mining, and smelting. In Southeast Asia (China, India,

75 Bangladesh, Vietnam, Thailand, and Nepal) arsenic (As) is naturally present in groundwater (Smedlley

76 2003; Brammer and Ravenscroft 2009). In Europe and Eurasia, contaminants are driven by intensive

77 industrial activities, inadequate waste disposal, mining and military activities (FAO 2015). The

78 utilization of untreated industrial and city effluents on farmlands as a source of plant nutrients contain

79 large quantities of organic and inorganic materials (Chhonkar et al. 2000). Among all the contaminants,

80 organic contaminants including organochlorine pesticides, polychlorinated biphenyls, phthalates esters,

81 and polycyclic aromatic hydrocarbons (PAHs) and heavy metals are of concern to human health due

82 to their toxicity, persistence, and bioaccumulation in the environment (Pies et al. 2007; Sun et al. 2016).

83 Heavy metals, in particular, are mutagenic, cytotoxic, and carcinogenic (Lim and Schoenung 2010).

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84 Further, excessive accumulation of heavy metals in soils affect microbial activity, soil fertility, soil

85 quality and impede crop yield.

86 2.1. Heavy Metals Pollution

87 Generally, metallic chemical elements with a relatively high density, and that are toxic at low

88 concentrations, and are classified under the generic term heavy metal. All metals, irrespective of

89 whether essential or non-essential can exhibit toxic effects at high concentrations (Mani and Kumar

90 2013). As trace elements, some heavy metals (selenium (Se), copper (Cu), zinc (Zn)) are required to

91 maintain the metabolism of organisms. However, at elevated concentrations, these can be lethal (Singh

92 et al. 2015). The severity of metal toxicity becomes predominant in an acidic, nutrient-deficient

93 ecosystem (Mukhopadhyay and Maiti 2010). The US Agency for Toxic Substances and Disease

94 Registry (ATSDR) ranked lead (Pb), mercury (Hg), arsenic (As), and cadmium (Cd) as first, second,

95 third and sixth, respectively, in terms of toxicity levels.

96 Heavy metals accumulation in farmlands is elevating. Natural and anthropogenic (industrial waste,

97 domestic effluent, agricultural inputs) activities discharge large quantities of metals into the

98 environment. Anthropogenic activities notably mining, smelting, and agriculture have polluted vast

99 agricultural lands in China, Japan, and Indonesia with metals such as Cd, Cu, and Zn. In northern

100 Greece, Albania and Australia, Cr, Cu, Pb, and Ni, predominate (Nagajyoti et al. 2010). Fertilizers

101 (organic and inorganic) are also potential sources of heavy metals. Phosphate fertilizers, in particular,

102 contain a variable level of Cd, Cr, Ni, Pb and Zn (Nagajyoti et al. 2010). Sewage sludge, liming,

103 untreated irrigation water, and pesticides are the principal sources of metals in agricultural soils.

104 Wastewater for irrigation has resulted in the accumulation of metals in soils and plants beyond the

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105 maximum permissible limits for livestock consumption in Gaza, Egypt (FAO 2015). Kapungwe (2013)

106 found that metal (Co, Cr, Cu, Pb, and Ni) pollution of soils, water, and crops at wastewater irrigation

107 sites in Zambia, indicated that heavy metal accumulation in soils and crops from the two sites exceeded

108 the acceptable limits.

109 2.2. Organic Pollution

110 Organic pollution of agricultural soil has been observed worldwide. Several organic contaminants

111 including organochlorine pesticides, polychlorinated biphenyls, phthalates esters, and PAHs are

112 characterized by toxicity, persistence, and bioaccumulation in the soil (Pies at el. 2007; Sun et al. 2016).

113 Large areas of agricultural lands are the major reservoir for organic pollutants (Zhang et al. 2013;

114 Zhong and Zhu 2013). The accumulation of compounds in agricultural soils may enter food chains and

115 present potential hazards to human health through trophic transfers (Liu et al. 2016; Fantke and Jolliet

116 2016).

117 Extensive use of agrochemicals (synthetic fertilizers, chemical pesticides, weedicides, fungicides,

118 etc.) in agricultural practices deposits vast volumes of organic pollutants in farmlands. Pesticides find

119 their way into the soil from spray drift, wash off from treated foliage, release from granulates or treated

120 seeds in the soil (Mittal 2014). Many organic contaminants in farmlands are difficult to degrade

121 biologically under normal environmental conditions (Sun et al. 2018). Residues of organochlorine

122 pesticides used for pest control over decades remain ubiquitous in the environment (Liu et al. 2016).

123 The cumulative pilling of organic pollutants in soils may pose threats to living functional activities of

124 microbes, plant growth and microbial populations (Sun et al. 2018). For instance, nitrobenzene has

125 been reported to inhibit the growth of soybean seedlings and genotoxicity in soybean root tip cells

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126 (Guo et al. 2010). PAHs are observed to alter the abundance of functional genes in soils (Sawulski et

127 al. 2014). Further, organochlorine pesticide residues in foodstuffs, water, soil, and sediments could

128 cause cancer throughout the food web (Taiwo 2019). Benomyl and dimenthoate are also reported to

129 induce mycorrhizal fungi symbiotic activity (Chiocchio et al. 2000).

130 2.3. Plastic Pollution

131 The application of plastic materials in industrial (packaging, car manufacturing, building, and

132 construction) and agricultural practices are increasing significantly (Gionfra 2018). A wide range of

133 plastic films including polyolefin, polyethylene, polypropylene, ethylene-vinyl acetate copolymer,

134 poly-vinyl chlorine, etc. is used in agricultural fields, and are collectively referred to as plasticulture.

135 These plastics provide mulching, greenhouses, micro-irrigation and pond liners (Shah et al. 2008).

136 Plastic mulching is an agronomic practice that uses plastic films on crops that act as insulation to

137 protect seedling and shoots (Gionfra 2018). The plastic mulch technique creates a microclimate

138 condition, prevents soil erosion and reduces pest pressure. A quadruple increase of plastic mulch use

139 in China was reported between 1991 and 2011 from 319 to 1,245 million tons (Steinmetz et al. 2016).

140 In semiarid regions of China, it was reported that there were approximately 680,000 greenhouses used

141 for crop production that were covered with 130 million m2 of plastic mulch (Wang et al. 2016; Chen

142 et al. 2017).

143 Although these plasticulture techniques reduce moisture loss, moderate soil temperature and

144 prevent weed growth, the residues of these plastic sheets reduce soil porosity and air circulation, alter

145 microbial communities, decrease soil fertility and impede seed emergence and seedling growth

146 (Moreno and Moreno 2008; Wang et al. 2016). Plastic residues exceeding 58.5 Kg ha-1 have been

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147 reported to decrease crop yield (Dong et al. 2015). Further, plastic residue releases dangerous toxins

148 including carcinogenic and mutagenic phthalate acid and can be absorbed by crops, especially

149 vegetables (Song et al. 2018). In addition, the application of sewage sludge contaminated with

150 microfibers and microplastic in agricultural lands is causing significant accumulation of plastics in

151 farmlands (Horton et al. 2017). The practice is prevalent in developed countries. Annually, agricultural

152 lands in Europe receive an estimated amount of 125-850 tons of microplastics/million inhabitants

153 (Nizzeto et al. 2016). Further, modern fertilizer application technology (controlled-release fertilizers)

154 discharges a vast volume of microplastic in soils. The controlled-release fertilizers technology regulate

155 both the quantity of fertilizer discharge per unit area and the time of application. Although the

156 technology is very effective and beneficial, the nutrient elements (N, P, K) are encapsulated within a

157 nutrient pill that is synthesized from a polymer that does not degrade after the nutrients have been

158 released (GESAMP 2016).

159 3. Bioremediation of Degraded Agricultural Soils

160 The amelioration of agricultural degraded soils is a task of utmost importance, considering the

161 intensity and adverse effects of the soil degradation. It is highly essential to employ suitable

162 remediation approaches to polluted soils (Mani and Kumar 2013). Remediation of polluted soils can

163 be attempted through conventional remedial techniques such as excavation and burial, landfilling,

164 leaching and soil washing (Wuana et al. 2010; Veselý et al. 2012). The excessive use of solid-waste

165 landfills to eliminate municipal and industrial waste, discharges a huge amount of leachate that results

166 in groundwater pollution (Nouri et al. 2008). Contaminated farmlands could be decontaminated using

167 physicochemical processes including precipitation, ion exchange, reverse osmosis, evaporation and

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168 chemical reduction (Tang et al. 2007). Nevertheless, higher energy requirement, high cost, membrane

169 fouling, and low removal efficiency of these approaches show minimal improvements (Mani and

170 Kumar 2013). The biological approach used to ameliorate polluted soils mediated by plants is known

171 as phytoremediation, or another popular clean-up method involves augmented bioremediation with the

172 addition of specific microbial strains to degrade the pollutants (Pilon-Smit et al. 2009; Conesa et al.

173 2012). The bioremediation technique involves processes that uses microorganisms, fungi, green plants

174 or their enzymes with the aim to decontaminate the ecosystem altered by pollutants to its natural

175 condition (Chakraborty et al. 2012). Bioremediation techniques offer the possibility to neutralize or

176 render harmless, various pollutants under natural biological activity (Gupta and Mahaptra 2003). The

177 application of genetically modified microorganisms and metal-tolerant marine bacteria can be utilized

178 as advanced bioremediation techniques (Paliwal et al. 2012). Generally, remediation technologies,

179 whether in situ or ex-situ, aim to either remove contaminants from the substratum (decontamination),

180 or reduce exposure (stabilization) (Varjani et al. 2016).

181 3.1. Plant-Microbes Interaction for Decontaminating Polluted Soils

182 Pilon-Smits (2005) defined phytoremediation as “the use of plants and their associated microbes for

183 environmental ‘cleanup’ which is a cost-effective, noninvasive alternative technology for engineering-

184 based remediation techniques”. Phytoremediation process categorization is based on the method and

185 nature of soil pollutants (Salt et al. 1998). Several aspects of the phytoremediation process in relation

186 to organic and inorganic pollutants are depicted in Fig. 1. Phytoremediation of polluted farmlands

187 involves one or more of these mechanisms: (a) Phytodegradiation: involves the enzymatic breakdown

188 of complex organic contaminants to simpler forms; (b) Phytoextraction: process by which plants

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189 absorb metals from a contaminated environment and store them in aboveground shoots and the

190 harvestable parts of roots; (c) Phytovolatilization/ Rhizovolatilization: process in which plants absorb

191 pollutants through the roots, transport to the leaves and are volatilized through the stomata where gas

192 exchange occurs; (d) Phytostabilization: immobilization of contaminants by plant roots and their

193 exudates which is achieved by accumulation and absorption onto roots or precipitation within the

194 rhizosphere; (e) Rhizofilitration: primarily used to remediate an aquatic system with low levels of

195 contaminants. It is usually used for heavy metals including Cd, Cr, Cu, Ni, Pb and Zn which are

196 retained within roots and do not translocate to the shoots. (f) Rhizodegradation/ Phytostimulation:

197 process by which plant roots stimulate soil microbial communities in plant root zones to breakdown

198 contaminants. Phytoremediation utilizes the inherent capacity of plants to take up and/or metabolize a

199 pollutant to less toxic substances. This remediation technology is applicable to a wide range of

200 contaminants including heavy metals, organic compounds such as chlorinated solvents, PAHs,

201 pesticides, insecticides, explosives as well as radionuclides (Wang et al. 2003; Oh et al. 2013). Plant

202 species used in phytoremediation are characterized by the ability to tolerate and accumulate

203 contaminants, the depth of their root zone, their potential to transpire groundwater, growth rate and

204 biomass production.

205 Although several plant species are capable of hyperaccumulating pollutants in their tissues,

206 phytoremediation in practice has numerous challenges as there are a variety of contaminants (Wu et

207 al. 2006). Moreover, the success of phytoremediation is a function of the plant’s ability to resist and

208 accumulate high concentrations of pollutants while producing a large amount of plant biomass

209 (Grčman et al. 2001). Efficient phytoremediation processes depend on the complex interactions among

210 soil, contaminants, microbes, and plants (Mandal et al. 2016). Due to the significant interaction

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211 between plant and microorganism for practical phytoremediation applications, the combined

212 phytoremediation with microorganisms has been encouraged widely due to the potential of

213 microorganisms to bioaccumulate contaminants from polluted soils or their effect on

214 mobilization/immobilization of pollutants that can effectively enhance decontamination and plant

215 growth (Ma et al. 2011).

216 The synergistic exploitation of microbes and plants has been successfully used to decontaminate

217 metalliferous soils (Jing et al. 2007; Glick 2010). The association between plant roots and a diverse

218 range of soil microbes, particularly rhizospheric microbes, is an essential determinant of

219 phytoremediation potential (Glick et al. 2007). Soil microbes influence plant growth in various ways:

220 some soil microbes infect plants with diseases and impede their growth; others actively or passively

221 enhance growth through several mechanisms (solubilization of phosphate, nitrogen fixation,

222 phytohormones, production of siderophores and AAC deaminase) (Ma et al. 2011). The two micro

223 partners (plant-associated microbes and the host plant) regulate the functioning of associative

224 symbioses in the polluted soil.

225 The adaptive capabilities of the plant and microorganism partnership in associative symbiosis and

226 the bioremediation potential of the microsymbiont, play a significant role in degrading contaminants

227 in soil (Mandal et al. 2016). The bioavailability of contaminants in the rhizosphere significantly

228 influences the volume of contaminants that accumulate in plants because a considerable proportion of

229 pollutants are bound to a variety of inorganic and organic constituents in contaminated soils and their

230 bioavailability is largely related to their chemical speciation (McBride 1994). Rhizospheric microbes

231 have different inherent traits that can alter the solubility and bioavailability of these contaminants in

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232 soil (Mitch 2002; McGrath et al. 2001). The rhizosphere harbors a diverse range of microorganisms.

233 Among these rhizospheric microbes that are involved in plant interaction with contaminated soils, the

234 plant growth-promoting bacteria (PGPB) or rhizobacteria are of great importants (Ma et al. 2011).

235 Rhizobacteria viz., Azotobacter, Bacillus, Pseudomonas, Arthrobacter, Achromobacter and

236 Enterobacter (Gray and Smith 2005) as well as Streptomyces spp. have been reported to have an

237 advantageous influence on various plants growing in contaminated soils (Tokala et al. 2002; Dimkpa

238 et al. 2009).

239 3.2. Rhizobacteria and Endophytes in Accelerating Phytoremediation

240 The intensity of industrial contamination on soils and the ecosystem is far higher than contamination

241 from agricultural sources, however, farmland degradation covers a larger landmass (Sun et al. 2016).

242 Unlike industrial fields, amelioration of agricultural soils demands protection and improvement in soil

243 productivity and ecological function. Several researchers have demonstrated the ecological

244 conservation potential and fertility enhancement of phytoremediation/bioremediation or

245 (biophytremediation) (Gerhardt et al. 2009; Ma et al. 2011). With metal pollutants, the remediation

246 goal is to extract and translocate the cation or oxyanion into harvestable tissues or immobilize the

247 elemental pollutants in the rhizosphere to prevent leaching whiles, organic pollutants and plastic

248 involve complete mineralization into non-toxic component basically nitrate, carbon dioxide, ammonia

249 and chlorine (Cunningham et al. 1996).

250 The bioavailability of pollutants in soil solution is a fundamental basis for the success of

251 phytoremediation. Several soil microbes, particularly bacteria and fungi, have the potential to stimulate

252 the bioavailability of precipitated contaminants in soil colloids for plant uptake (Gonzalez et al. 2005).

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253 Rhizobacteria and fungi also degrade and accumulate pollutants in their tissues (Chang et al. 2002;

254 Qin et al. 2017; Meckenstock et al. 2016). Endophytic bacteria are bacteria colonizing the internal

255 tissues of plants without causing adverse effects or symptomatic infections on the host (Schulz and

256 Boyle 2006). Endophytes exist aberrantly and transiently in plants apoplastic or symplasm (van

257 Overbeek and van Elsas 2008), yet they induce the physiological change that influences the growth

258 and development of plants (Conrath et al. 2006). Generally, the advantageous effects of endophytes

259 outweigh the effects of several rhizobacteria (Pillay and Nowak 1997) especially when plants are

260 growing under abiotic or biotic stress conditions (Barka et al. 2006; Hardoim et al. 2008). Several

261 endophytes from different plant species have been isolated (Lodewyckx et al. 2002; Idris et al. 2004;

262 Mastretta et al. 2009), and in some instances, they made the plants more resistant to heavy metals stress

263 and induced host plants growth via different mechanisms such as: induction of systemic resistance in

264 plants to pathogens, biological control, production of growth regulators, nitrogen fixation, solubilizing

265 of phosphate and improvement of mineral nutrients and water uptake (Ryan et al. 2008). Further,

266 endophytes similar to other bacteria are capable of degrading xenobiotics and enhance plant tolerance

267 to pollutants.

268 3.2.1. Heavy Metals Remediation

269 Rhizobacteria and endophytes enhance phytoremediation by stimulating metal bioavailability via

270 modification of pH, releasing of chelators, synthesis of phytohormones, immobilization and the

271 precipitation of metals in the rhizosphere (Ma et al. 2011). Several hyperaccumulating plants have

272 been utilized to accumulate diverse toxic heavy metals. A number of bacteria strains have been

273 reported to significantly promote phytoremediation (Table 1). Hassan et al. (2016) isolated metal

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274 resistant bacteria strains from sugarcane rhizosphere that have ACC- deaminase and N fixing

275 capabilities. The bacteria strain (SAN1) significantly enhances Triticum aestivun L. plants to hyper

276 accumulate Cd and also promote plant growth. When Eruca sativa plants were inoculated by

277 Pseudomonas putida (ATCC39213), Kamran et al. (2015) reported an increase in Cd uptake. Brassica

278 napus inoculated with the Paracoccus sp. strain significantly accumulated Cu in the roots and shoots,

279 improving plant growth and biomass production (Sun et al. 2010). Saravanan et al. (2007) reported an

280 increase in Zn uptake in plants by the action of 5-ketogluconic acid secreted by Gluconacetobacter

281 diazotrophicus which dissolves Zn containing compounds such as ZnO, ZnCO3, Zn(PO4)2. Further,

282 Pereira et al. (2015) inoculated Trifolium repens with Rhodococcus erythropolis (EC10) growing in

283 Zn-rich soils, and reported an increase in the availability of the metal in soil solution. Wheeler et al.

284 (2001) reported a decrease in Ni accumulation and increased nodulation when Frankia sp was

285 inoculated to Alnus glutinosa. Certain endophytic bacteria strains have been reported to increase heavy

286 metal mobilization through the production of low-molecular-weight organic acid (oxalate, gluconate,

287 acetate, 2-ketogluconate, malate, succinate, and citrate) (Ma et al. 2011). Further, Rhizobacteria and

288 endophytes assist phytostabilization of heavy metals by decreasing metal bioavailability through

289 immobilization. Generally, physical and cellular metal sequestration, and metal exclusion via

290 permeability barrier are the mechanisms put forward to explain the process that microbes use to induce

291 immobilization of metals (Brown et al.1995). Remediation of heavy metals contaminated soils through

292 mycobacteria strategy is better than phytoremediation alone.

293 3.2.2. Organic and Plastic Pollutants Remediation

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294 The mechanism by which microorganism degrade and mineralize organic contaminants has been

295 well demonstrated in agricultural soils under natural conditions (Odukkathil and Vasudevan 2016;

296 Labana et al. 2005; Ayotamnuo et al. 2006). Ayotamuno et al. (2006) investigated the efficiency of

297 heterotrophic bacteria in remediating crude-oil contaminated agricultural soil and reported 93 to 95%

298 degradation efficiency. Degradation/bioavailability of organic pollutants is an enzymatic process. For

299 instance, in monoaromatic hydrocarbons (benzene, xylene, toluene, etc.,) microorganisms secrete

300 mono- and dioxygenase enzymes that inject oxygen atoms into benzene rings and destructs the

301 resonance structure, inducing ring cleavage (Abbasian et al. 2015). For PAHs, four enzymatic reactions

302 (addition of fumarate, methylation of unsubstituted aromatics, hydroxylation of an alkyl substituent

303 and direct carboxylation) are involved (Varjani and Upasani 2016). These sequential enzymatic

304 reactions yield central metabolites for example benzoyl-CoA which is incorporated into biomass or

305 oxidized (Mecknenstock et al. 2016). Mineralization and accumulation of a diverse range of organic

306 pollutants in plant tissues have been reported (Vidali 2001; Gonzalez et al. 2005). Plant tissues can

307 accumulate organochlorine pesticide concentrations up to 4-45 times higher than in soils (Sun et al.

308 2016).

309 Polymers, especially plastics, are potential substrates for microorganisms. In compost and soil,

310 partial aerobic and anaerobic conditions mediate the biodegradation process of plastics (Shah et al.

311 2008). The initial breakdown of plastics resulting from several physical and biological forces, are

312 substantial enough to disintegrate polymer solids. Abiotic hydrolysis of synthetic polymers including

313 poly (ethylene terephthalate), polycarboxylates, polylactic, polydimethylsiloxanes, etc. facilitates the

314 biodegradation process (Heidary and Gordon 1994; Fan et al. 1996). Intracellular and extracellular

315 depolymerase are the two active enzymes utilized in plastic biodegradation (Gu et al. 1998). The

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316 extracellular enzyme disintegrates complex polymers into smaller chain molecules such as monomers,

317 dimers and oligomers, which are assimilated via the cellular membrane and degraded by intracellular

318 enzymes (Hamilton et al. 1995; Shah et al. 2008). Several extracellular enzymes including esterases,

319 lipases, and cutinases secreted by Pseudomonas sp. are hydrolase enzymes that actively stimulates the

320 degradation of plastics.

321 Remarkably, polyethylene, the most synthetic plastic product (Sangale et al. 2012) that is widely

322 used in agriculture, contributes millions of tons of plastic pollutants to the environment. Several

323 microorganisms have been reported to effectively degrade plastic (Table 2). Sivan et al. (2006),

324 reported that Rhodococcus ruber, a biofilm stimulating strain (C208), has a 0.86% per week

325 polyethylene degrading rate. Metabolism of vinyl chloride (VC) by P. putida was studied by Danko et

326 al. (2004) and reported to yield 0.15 to 0.2 mg of suspended solid per mg VC. Further, Tribedi and Sil

327 (2013) isolated Pseudomonas sp from soils and cultured them in a medium containing purpose

328 polyethylene succinate (PES) as a sole carbon source. These researchers reported a degradation rate of

329 1.15 mg/day of PES. Further, Pseudomonas sp., with its diverse metabolic ability and genetic

330 plasticity (Nikel et al. 2016) has been reported to be the most efficient microbial strain for degrading

331 polyethylene (Mohan et al. 2016; Sangale et al. 2012). Pseudomonas sp. degrade polyethylene through

332 the inclusion of a pro-oxidant additive which induces hydrophilicity of polyethylene and stimulates

333 chain scission of the polymer producing carbonyl functional units and low molecular weight

334 constituents (Chiellini et al. 2006).

335 3. 3 Rhizobacteria and Endophytes in Regulating Plant Growth

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336 In both natural and managed ecosystems, plant-bacteria associations are crucial for the adaptation

337 of the host to a modifying environment. Rhizobacteria and endophytes microbes can alter plant cell

338 metabolism to the extent that plants can endure high concentrations of pollutants and withstand

339 exposure to adverse pollutant stress (Welbaum et al. 2004). Several plant-associated bacteria have been

340 reported to speed up phytoremediation in contaminated soils by promoting plant growth and health

341 (Grandlic et al. 2008; Kidd et al. 2009; Dary et al. 2010). Rhizospheric microbes induce plant growth

342 by increasing nutrient availability and phytohormone production (Fig. 2). The availability of macro-

343 and micro-nutrients particularly N, P, Fe2+ are governed by N2 fixation, P solubilization/mineralization

344 and Iron (Fe2+) chelating by siderophore respectfully (Brigido and Glick 2015). They also suppress the

345 activities of phytopathogens through siderophores production, antibiotic metabolites, cell wall lytic

346 enzymes and stimulation of systemic resistance in plants (Kloepper et al. 2004; Backman and Sikora

347 2008). The siderophores defend plants against microbial pathogens that are reliant on iron by reducing

348 its availability through iron chelation in the rhizosphere (Brigido and Glick 2015). Beneficial

349 microorganisms also suppress abiotic stresses. For instance, under stressed conditions, the production

350 of the plant-stress suppressing hormone, ethylene, is significantly accelerated so as to alleviate the

351 stress condition and improve plant growth (Abeles et al. 1992).

352 3.3.1. Plant Growth Regulators

353 Plant growth regulators are synthetic plant exogenous hormones similar to natural plant hormones.

354 They regulate the growth of the plant and are relevant measures for boosting biomass production

355 (Vejan et al. 2016). Plant growth regulators or phytostimulators are rhizobacteria or endophytes that

356 secrete or alter the concentration of growth regulators such as ethylene, GA, IAA and cytokinins

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357 (Lugtenberg et al. 2002; Somers et al. 2004). Ethylene (C2H2) plays a significant role in modulating

358 the cellular metabolism and growth of plants (Ping and Boland 2004) and is associated with disease-

359 tolerant biotic/abiotic stress resistance, plant-microbe partnership and plant nutrient dynamics (Ma et

360 al. 2011). Ethylene regulates several physiological changes in plants at the molecular level, however,

361 at high concentrations, it induces defoliation and cellular processes, and inhibits root elongation, lateral

362 root growth and root hair formation (Mayak et al. 2004). Rhizobacteria and endophytes are capable

363 of mitigating the deteriorating impact of high concentrations ethylene on plants by hydrolyzing (ACC)

364 1-aminocyclo propane-1-carboxylic acid (Glick et al. 2007). The ACC deaminase enzyme is actively

365 involved in the mechanism that rhizobacteria utilize to degrade ethylene. The ACC is the processor for

366 ethylene as it mediates the conversion of methionine to ethylene through the biosynthetic sequence:

367 methionine- S- adenosylmethionine (SAM) - ACC- C2H4 (Adams and Yang 1979).

368 Plant hormones or phytohormones that are synthesized by plant-associated bacteria include

369 gibberellins, indole-3-acetic acid (IAA) and cytokinins (Ma et al. 2011). These phytohormones

370 frequently induce germination, differentiation, reproduction, and bergh plants against abiotic and

371 biotic stress (Taghavi et al. 2009). Gibberellin and cytokinins stimulate the growth of several plants

372 and modify the morphology of plants and under both non-stressed and stressed conditions (Arkhipova

373 et al. 2007). Further, rhizobacteria and endophytes contribute to reducing metal phytotoxicity through

374 bioaccumulation and biosorption mechanisms. Since the bacteria cells (1.0-1.5 mm3) have relatively

375 high surface area to volume ratios, they can absorb large quantities of heavy metals than inorganic soil

376 components (vermiculite, kaolinite) (Khan et al. 2007). Several publications have reported that bacteria

377 bioaccumulation/ biosorption mechanisms, in addition to other plant growth-promoting features such

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378 as the production of phytohormones and ACC deaminase, can influence and improve plant growth in

379 contaminated soil (Madhaiyan et al. 2007; Kumar et al. 2009).

380 3.3.2. Nutrients Activation

381 Rhizobacteria and endophytes have the capacity to enhance the availability of nutrients

382 concentration in the rhizosphere (Choudhary et al. 2011). Nutrient deficiency in soils, particularly

383 nitrogen (N) and phosphorus (P), is frequently one of the principal limitations for plant development.

384 In recent years, beneficial microbes are widely used as inoculants, biofertilizers or biostimulants to

385 promote plant growth through nutrient mobility, thereby alleviating abiotic stress (Abhiliash et al. 2016;

386 Adak et al. 2016). In the symbiotic nitrogen fixation (NF) process, a direct net transfer of biologically

387 fixed N from the bacteria to the host occurs concurrently with a significant transfer of

388 photosynthetically fixed plant carbon to the NF bacteria (Pankievicz et al. 2015). As a rule, two

389 primary formative procedures are required for the arrangement of harmonious N-fixing knobs:

390 bacterial infection and knob organogenesis (Gage 2004; Oldroyd and Downie 2008). The fixation of

391 atmospheric nitrogen by rhizobacteria and endophytes contributes a high amount of N to soils. For

392 instance, Peoples et al. (1995) reported 100-300 Kg N ha-1 fixed by rhizobacteria. In another study by

393 Herridge et al. (2008), it was estimated that the rhizobia-legume symbiosis association incorporates an

394 average of 227 Kg N ha-1. Similarly, 100-200 Kg N ha-1 in faba bean was reported by Jensen et al.

395 (2010). Although data on associative N fixation estimates are scarce, a recent study by Ladha et al.

396 (2016), reports 13, 22 and 13 Kg N ha-1 in maize, rice and wheat, respectively. Although the rhizobia

397 inoculation have significant impact on N nutrition, the process is sensitive to a diverse range of

398 environmental constraints (such as variation in pH, temperature, and nutrient availability, particularly

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399 P deficiency) leading to high variations in growth and nodulation and hence low N2 fixation rates in

400 legumes (Deng et al. 2005; Hauggaard–Nielsen et al. 2010). For instance, early stages in the beneficial

401 interaction procedure such as molecular signaling, root hair curling, rhizobia attachment, and infection

402 thread formation and nodule initiation are generally sensitive to extreme temperatures, acidity, heavy

403 metals, salinity, etc. (Zheng et al. 2005; Ibekwe et al. 1997). Further, during the infection procedure

404 rhizobia likewise need to manage unfavorable conditions inside the host cells and with the plant’s

405 intrinsic immunity may interfere with the beneficial interaction (Soto et al. 2009). Notwithstanding,

406 some leguminous-based rhizobia strains have developed diverse mechanisms to alleviate the adverse

407 effects associated with the abiotic stresses, thereby enhancing growth under stressed conditions

408 (Brígido and Glick 2015). Further, a plethora of non-symbiotic rhizobia strains with PGPR traits can

409 facilitate phytoremediation processes.

410 Phosphorus (P) is a major essential plant macronutrient for growth and development. It is well

411 known that soluble P (H2PO4−/HPO4

2−) in soil solution is a mostly deficient nutrient for biomass

412 production (Glass 1989), and the high concentration of pollutants in soil interferes with phosphorus

413 adsorption and retards plant growth (Hamid and Ahmad 2012). Most rhizobacteria have the ability to

414 convert insoluble phosphates into readily available forms through chelation, acidification, exchange

415 reactions and secretion of organic acid (Chung et al. 2005), or mineralization of organic phosphates

416 by secretion of extracellular phosphatase (van der Heijden et al. 2008). Solubilization of P involves

417 several mechanisms, yet organic acids are the major contributors (Khan et al. 2007; Wei et al. 2018;

418 Chen et al. 2015). P solubilizing by organic acids is attributed to lowering pH and to the chelation of

419 cations (Behera et al. 2017). The acidification in the perimeter of microbial cells causes the discharge

420 of P anions by substitution of H+ and Ca2+ (Behera et al. 2017). Aside from microbial solubilization of

421 mineral P, mineralization of organic P plays an essential role in P nutrition (Shen et al. 2011). The

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422 mineralization procedure is generally controlled by specialized P-hydrolyzing enzymes (phytases and

423 phosphates) synthesized mainly by bacteria and fungi (Sato et al. 2015). The mineralization process

424 involves dephosphorylation of phosphoester compounds and phosphoanydrid bonds by acid

425 phosphates (Alori et al. 2017).

426 Iron, a micronutrient essential for many enzymatic reactions in plants and microorganisms is mostly

427 unavailable for direct assimilation. In nature, iron occurs predominantly as Fe3+ and reacts to form

428 insoluble hydroxides and oxyhydroxides (Kong et al. 2017; Ma et al. 2011). This form is unavailable

429 to plants and microbes, and in order to acquire sufficient iron, some bacteria synthesize low-molecular-

430 weight iron-binding molecules (siderophores), which bind Fe3+ with a high affinity to solubilize iron

431 for efficient uptake (Ma et al. 2011).

432 Even though the establishment of successful vegetation on degraded soils is challenging, utilization

433 of rhizobacteria and endophytes to immobilize contaminants and enhance plant tolerance to a high

434 concentration of pollutants and/or promote plant growth and biomass production, could ensure a

435 practical technology for accelerating phytoremediation processes.

436 3.4. Challenges to the Application of Microbial Mediated Phytoremediation

437 Generally, microbial assisted phytoremediation is a promising technique for cleaning polluted soils,

438 however, there are some challenges that interfere with the practical application of remediation

439 processes in the field. The efficiency of the remediation process depends on numerous factors

440 including plant species, plant and microbial tolerance to the pollutants, pollutant type and

441 concentration, nutrient availability, soil pH, and competition among organisms (Kong and Glick 2017).

442 Further, microbial-mediated phytoremediation is particularly appropriate for sites containing

443 pollutants within moderate to a shallow root depth zones. Pollutants that occure beyond the root depth

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444 of accumulating plant (particularly herbaceous plants), may be remediated using trees. However, trees

445 take quite a long to achieve adequate biomass for successful phytoremediation (Mani and Kumar 2013;

446 Schoenmuth and Pestemer 2004). Again, hyperaccumulating plants including L. multiflorum and S.

447 caprea, are usually impeded by their low biomass and slow growth rate (Waigi et al. 2017). Generally,

448 the survival and competitive capacity of inoculated microorganisms barely outweigh indigenous

449 strains in the rhizosphere, which restricts the efficiency of the inoculants and further limits the

450 remediation effect (Ma et al. 2009). The successful use of microbial-mediated phytoremediation

451 depends on the survival and formation of a large number of inoculated microbial strains, as well as the

452 adaptation of nonnative plants and microbial species to the environmental conditions in the field (Kong

453 and Glick 2017).

454 Another consideration is that inoculant products are susceptible to thermo-, photo-, hydro-, and bio-

455 ability, leading to a poor shelf and field life (Abilash et al. 2016). There is also a growing concern

456 about biosafety issues with the use of inoculants because some rhizobia strains including Pseudomonas

457 aeruginosa and Burkholderia cepacia are opportunistic pathogens and may pose ecological and plant

458 health threats (Li et al. 2013; Kumar et al. 2013). Further, the efficacy and longevity of inoculants

459 under fluctuating climatic conditions also affects the remediation process. There is mounting evidence

460 that climate change is altering biogeochemical cycles, rhizosphere biodiversity, and resource

461 availability, all of which affect plant-microbe interactions (Abhilash et al. 2016). In order to fully

462 harness the potential of microbial-assisted phytoremediation, intensive research is required on

463 understanding the environmental stressors that impair the process in the field. Further, the ecological

464 and human hazards related to inoculants ought to be appropriately evaluated before undertaking large-

465 scale applications.

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466 4. Conclusions

467 Plant-microbes association plays a crucial role in ameliorating extensively polluted soils to a healthy

468 state. Although the mechanisms associated with the degradation of contaminants through

469 phytoremediation is complicated and involves different pathways occurring simultaneously, a

470 thorough understanding of the adaptation mechanisms, survival, and colonization processes, as well

471 as the resistance/tolerance features of inoculants in polluted soil, is necessary to improve the

472 remediation efficiency. Further, published results of the microbial assisted phytoremediation under

473 field conditions demonstrate limited effectiveness. In this regard, assessment of in situ environmental

474 conditions, characterization of the physicochemical and biological features of contaminants, and

475 evaluation of competitive interactions between native microbial communities and foreign strains is

476 crucial for screening plant and microbial species that can survive and remediate the polluted site. Also,

477 information and knowledge about the in situ environment is important for proper bioagumentation

478 processes before implementation of remedial methods. The aim of remediating agricultural lands is to

479 scale down land scarcity and improve crop productivity. It is therefore imperative that the biosafety

480 issues (ecological and human health risk) associated with inoculants are properly evaluated before

481 applying microbial phytoremediation practices.

482 Acknowledgements

483 The work was funded by National Natural Science Foundation of China (31771726). Any opinions,

484 finding, and conclusions or recommendations expressed in this material are those of authors and do

485 not necessarily reflect the views of National Natural Science Foundation of China.

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Table 1. Examples of microbial assisted phytoremediation of metal- contaminated soils.

Plant species

Bacteria strain Condition Elemental pollutant

Role of Microbial on plant growth and phytoremediation process

Concentration of metal in plant (mg/Kg)

Reference.

Shoot Root

Soil - 1605

Prosopis juliflora

Ecterobacter sp. (HU 38).

Contaminated site

Chromium Synthesize IAA, ACC-deaminase, induce P-solubilization and siderophore. Increase the plant growth, root development, availability and uptake of Cr IN 384 213

Khan et al. 2015

Shoot Root

CT - -

Sedum alfredii

Acinetobacter calcoceticu

Pot experiment Cadmium Induce root elongation, plant growth, and biomass and significantly stimulate Cd uptake (phytoextraction).

IN 192±08 168±08

Chen et al. 2015

Shoot Root

CT 4.45 ± 0.85

2.81 ± 0.19

Triticum aestivum l.

Rhizobacteria SAN2

Pot experiement

Cadmium Synthesize ACC deaminase, increase shoot biomass and decrease Cd uptake (phytostabilization)

IN 0.63 ± 0.09

0.53 ± 0.09

Hassan et el. 2016

Shoot Root

CT 5.67 3.72

Zea mays L.

Rhizobacteria ANI2

Pot experiment Lead Synthesize ACC deaminase, decrease the bioavailabilty of Pb by cheating, promote maize growth and reduce Pb uptake.

IN 0.82 0.41

Hassan et al. 2014

Plant

CT 2.13

Eruca sativa

Pseudomonas putida

Pot experiment Cadmium Increase plant growth, chlorophyll content and uptake of Cd (phytoextraction).

IN 3.78

Kamran et al. 2015

Shoot Root

CT 19.70 13.90

Brassica napus

Pseudomonas tolaasii (ACC23)

Pot experiment Cadmium Secrete IAA, siderophore, increase biomass production and Cd uptake

IN 20.43 14.07

Dell’Amico et al. 2008

Shoot Root

CN 8.50 9.32

Brassica napus

Paracocuus sp. (YM22)

Pot experiment Copper Synthesize siderophore, increase plant growth and Cu uptake.

IN 24.80 43.60

Sun et al. 2010

Shoot Root

CN 3.60 25.40

Brassica juncea

Achromobacter xylosoxidans (Ax10)

Pot experiment (Cu 100).

Copper Produce IAA, solubilize phosphate enhance root development and biomass production. Increase Cu uptake.

IN 6.20 64.50

Ma et al. 2009

Soil Av. Ex

CT 21.75 188.7

Trifolium repens L.

Rhodococcu erythropolis (EC10)

Pot experiment

(Zn 250).

Zinc Release IAA, HCN, siderophore, ACC and stimulate the bioavailability of Zn in soil

IN 23.12 208.72

Pereira et al. 2015

Shoot Root

CT 252 -

Alyssum murale

Microbacteria oxydans AY509223

Pot experiment

Nickel (moderate)

Nickel Increase the solubility and bioavailability of Ni

IN 468 -

Abou-Shanab et al. 2008

Abbreviations: ACC deaminase =1-aminocyclopropane-1-carboxylate; HCN=hydrogen cyanide; IAA=indole-3-acetic acid; CT = control; IN = inoculation; Av = available; Ex = exchangeable

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Table 2. List of reported microorganism that degraded plastics.

Plastic Microorganism Reference

Polyethylene Curvularia senegalensis

Brevibacillus borstelensis

Rhodococcus rubber

Howard 2002

Hadad et al. 2005

Sivan et al. 2006

Polyvinyl chloride Pseudomonas putida AJ Danko et al. 2004

Polyurethane (PUR) Pseudomonas chlororaphis Zheng et al. 2005

Polyvinyl alcohol (PVA) P. vesicularis PD Kawai and Hu 2009

Polyethylene succinate (PES) Pseudomonas sp. AKS2 Tribedi et al. 2013

Polystyrene (PS)

Vinyl chloride

High impact

Pseudomonas putida AJ

Pseudomonas sp.

Danko et al. 2004

Mohan et al. 2016

Poly(3-hydroxybutyrate) Schlegelella thermodepolymerans Romen et al. 2004

Poly(3-hydroxybutyrate-co-3

hydroxypropionate)

Acidovorax sp. TP4 Wang et al. 2002

Polycaprolactone Fusarium moniliforme Torres et al. 1996

Polyethylene glycol (PEG) Pseudomon stutzerias Obradors and Aguilar 1991

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Fig. 1 Plant-microbes processes in bioremediation organic and inorganic pollutants.

Rhizofilitration

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Mod

erat

ing

phot

ohor

mon

es

)

Fig.2 The mechanisms used by Endophytes and Rhizobacteria to enhance growth of plants.

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