Brown gold of marginal soil: Plant growth promoting bacteria to overcome plant abiotic stress for agriculture, biofuels and carbon sequestration

Journal Pre-proofs Review Brown Gold of Marginal Soil: Plant Growth Promoting Bacteria to Overcome Plant Abiotic Stress for Agriculture, Biofuels and Carbon Sequestration Wusirika Ramakrishna, Parikshita Rathore, Ritu Kumari, Radheshyam Yadav PII: DOI: Reference:

S0048-9697(19)35054-5 https://doi.org/10.1016/j.scitotenv.2019.135062 STOTEN 135062

To appear in:

Science of the Total Environment

Received Date: Revised Date: Accepted Date:

23 July 2019 30 September 2019 17 October 2019

Please cite this article as: W. Ramakrishna, P. Rathore, R. Kumari, R. Yadav, Brown Gold of Marginal Soil: Plant Growth Promoting Bacteria to Overcome Plant Abiotic Stress for Agriculture, Biofuels and Carbon Sequestration, Science of the Total Environment (2019), doi: https://doi.org/10.1016/j.scitotenv.2019.135062

This is a PDF file of an article that has undergone enhancements after acceptance, such as the addition of a cover page and metadata, and formatting for readability, but it is not yet the definitive version of record. This version will undergo additional copyediting, typesetting and review before it is published in its final form, but we are providing this version to give early visibility of the article. Please note that, during the production process, errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.

© 2019 Elsevier B.V. All rights reserved.

Brown Gold of Marginal Soil: Plant Growth Promoting Bacteria to Overcome Plant Abiotic Stress for Agriculture, Biofuels and Carbon Sequestration

Wusirika Ramakrishna*, Parikshita Rathore, Ritu Kumari, Radheshyam Yadav

Department of Biochemistry and Microbial Sciences Central University of Punjab, Bathinda, Punjab, India

*Corresponding author Email: [email protected]; [email protected]

1

ABSTRACT Marginal land is defined as land with poor soil characteristics and low crop productivity with no potential for profit. Poor soil quality due to the presence of xenobiotics or climate change is of great concern. Sustainable food production with increasing population is a challenge which becomes more difficult due to poor soil quality. Marginal soil can be made productive with the use of Plant Growth Promoting Bacteria (PGPB). This review outlines how PGPB can be used to improve marginal soil quality and its implications on agriculture, rhizoremediation, abiotic stress (drought, salinity and heavy metals) tolerance, carbon sequestration and production of biofuels. The feasibility of the idea is supported by several studies which showed maximal increase in the growth of plants inoculated with PGPB than to uninoculated plants grown in marginal soil when compared to the growth of plants inoculated with PGPB in healthy soil. The combination of PGPB and plants grown in marginal soil will serve as a green technology leading to the next green revolution, reduction in soil pollution and fossil fuel use, neutralizing abiotic stress and climate change effects.

Key Words: Marginal land, Rhizoremediation, Plant growth promoting bacteria, Salinity, Heavy metals, Sustainable food production.

2

1

INTRODUCTION

2

Marginal land is defined as land which is less fertile and can be used for cultivation

3

again if it is feasible from an economic perspective. Marginal land is a broad term which

4

includes areas with limited rainfall, extreme temperature, low quality, steep terrain, shallow

5

depth, reduced fertility, coarse-textured, stony, heavy cracking clays, salt-affected,

6

waterlogged, marshy lands, barren rocky soils, or other problems related to agriculture

7

(Shahid and Al-Shankiti, 2013). Marginal land has received considerable attention as it

8

possesses the potential to increase food security and support bioenergy production (Tilman et

9

al., 2006).

10

One of the reasons for turning fertile land into marginal land is contamination with

11

heavy metals due to excessive use of chemical fertilizers. Heavy metals exist in soil for a

12

long time as they are mostly non-biodegradable. They reduce soil health and are toxic to

13

living organisms when they enter the food chain. Remediation of heavy metals is an

14

important area of research which focuses on decreasing the negative impact of heavy metals

15

on the soil. Phytoremediation is one of the methods where hyperaccumulators or high

16

biomass plants are used to rehabilitate metal contaminated soil. Rhizoremediation is another

17

method where plant growth promoting bacteria (PGPB) are introduced in the soil, which not

18

only enhance plant growth and metal uptake but also improve the quality of the soil. Marginal

19

soil enriched with PGPB is a good alternative for growing plants for biofuel production

20

considering depleting fossil fuel stocks and limited fertile land. This review deals with the

21

multitasking of PGPB in improving soil quality, crop productivity, bioenergy production, and

22

carbon sequestration.

23 24

Historical Perspective and Dynamic Properties of Marginal Land

3

25

The notion of marginal land was developed with time and space. It refers to land which is

26

unproductive, wasteland, underutilized or degraded (Gibbs and Salmon, 2015). It was

27

Ricardo (1817) who came up with the idea of marginal land in his land rent theory. Hollander

28

(1895) described marginal lands as the poorest lands above the margin of rent-paying land.

29

Later, many theories were proposed. The three prefixes used for marginal lands are physical,

30

production, and economical. Marginal soils reflect the dynamic state of land resources and

31

are sensitive towards the natural processes. The concept of marginal land was developed with

32

reference to multiple needs and concerns. With current knowledge, the concept of marginal

33

land can be further defined as the land that is physically inaccessible; it has soil and climate

34

restrictions, or high environmental risk and fragile ecosystem with low production which is

35

unprofitable. Following this concept, marginal lands can be assessed quantitatively so that the

36

most suitable management practices are applied. Land degradation is caused by poor

37

management of productive land. Marginal land can be restored to fertile land by improving

38

land function. A large area of land became marginal in Europe and parts of Asia due to

39

economic development and food demands. Transitional properties of marginal lands are

40

crucial for explaining marginal soil dynamics. Restoration of unproductive lands can give rise

41

to marginal land, and by enhancing the quality of marginal land, we can get productive land.

42

Similarly, degradation of productive land gives marginal land and the degradation of

43

marginal land ultimately gives rise to unproductive land. Land degradation neutrality (LDN)

44

concept was developed and adopted by United Nations Convention to Combat Desertification

45

(UNCCD) in an attempt to avoid, reduce and reverse land degradation (Cowie et al., 2018).

46 47

Occurrence of Marginal Land Globally

48

Marginal land covers the area that has nutrient-deficient soil, contaminated soil, or

49

receives little or no rainfall, which makes the soil unfit for agriculture. It includes dryland,

4

50

marshy land, salinity affected land, metal-contaminated land, barren rocky areas, and high

51

mountains. Of these, drylands account for about 45% of the world’s land area. About 40% of

52

the Earth’s land covers dryland ecosystem, mostly Africa (13 x 106 km2) and Asia (11 x 106

53

km2) (Shahid and Al-Shankiti, 2013). Many issues such as scanty rainfall, extremely high

54

temperatures, poor fertility soils, salinity in soils, and, drought are associated with dryland

55

ecosystems. These features constrain the land for agriculture. Water-stressed lands are

56

sensitive to land degradation. About 10-20% of drylands are known to be degraded

57

(Millennium Ecosystem Assessment, 2005). According to the 4th National UNCCD Report,

58

about 228 mha (69%) of India’s total geographical area (about 328 mha) falls under dry land.

59

Soil contamination by heavy metals is another major problem that has affected about 235

60

million hectares of arable land globally (Bermudez et al., 2012). For instance, Europe has

61

more than 2.5 million potentially contaminated sites (Panagos et al., 2013). Overall, the total

62

marginal land globally is estimated to be around 13.1 global hectares (Gha) and its worldwide

63

distribution is shown in figure 1 (Mehmood et al., 2017). About 430 to 580 Mha of the total

64

degraded land is suitable for biomass production (Lewis and Kelly 2014). India has about

65

46.67 Mha of wasteland, out of which 39.2 Mha has the potential for the plantation of

66

bioenergy crops (Edrisi and Abhilash, 2016). The distribution of marginal land in India and

67

their utilization for the growth of bioenergy crops are given in Table 1.

68

Soils affected by salts are considered as marginal because of high salinity and

69

sodicity. Globally, salinity affected area is estimated to be nearly 1307 million hectares with

70

North and Central Asia, South America and Australia having most of the salt-affected soil

71

(Singh, 2018; FAO/IIASA/ISRIC/ISS-CAS/JRC, 2008). In India, about 6.7 million hectares

72

constitute salty lands. About 6.7 million ha (6.7 x 106) of soil is reported to be salt-affected in

73

India (Mandal, 2016). The upward movement of salt with the rising water table due to the

74

introduction of canal irrigation has been cited as one of the reasons for salt enriched soil in

5

75

parts of India (Singh et al., 2010a). Another reason attributed to the secondary salt

76

enrichment of soil is the use of salty groundwater for irrigation purpose (Gupta, 2010).

77

Salinity and drought are two major abiotic factors which drastically reduce crop

78

productivity. Soil salinity affects 45 million hectares of land which is irrigated, leading to a

79

loss of about US$ 27 billion per annum in global agriculture (Qadir et al., 2014). Salinity not

80

only reduces agricultural productivity and farmer income but also results in soil erosion. The

81

possible reasons for soil salinity include saltwater intrusion and wind-borne salt deposition.

82

The soluble salts near plant roots restrict the uptake of water and balanced absorption of

83

essential nutrients resulting in osmotic stress. Soil salinization involves the accumulation of

84

cations (Na+, Ca2+, K+) and anions (Cl- and, NO3-). Higher levels of these salts change soil

85

texture, hydraulic properties, pH, water infiltration and aeration, leading to soil compaction

86

and erosion (Umara et al., 2013). The elevated level of sodium (Na+) disturbs the uptake of

87

other nutrients and also causes ion toxicity (Ashraf and Wu 1994).

88 89

Exploiting Beneficial Traits of Plant Growth Promoting Bacteria for Next Green

90

Revolution in Agriculture

91

Biofertilizers contain living microorganisms which promote plant growth when

92

applied to seeds, plant surfaces, or soil by colonizing the rhizosphere or endosphere.

93

Biofertilizer products are usually based on plant growth-promoting bacteria (PGPB), which

94

enhance crop productivity and soil fertility without exerting any toxic effect on the

95

environment like chemical fertilizers. Instead, they help to get the soil free from toxic heavy

96

metals. Hence, the use of PGPB will lead to sustained agriculture and forestry. A healthy

97

rhizosphere is created by the rhizobacteria at sufficient densities so that they help in

98

promoting plant growth and converting nutritionally essential elements through various

99

biological processes. They increase the availability of key macro and micronutrients which

6

100

enhance not only soil fertility and health but also the survival of microbes in soil (Vejan et

101

al., 2016). PGPB inoculation of wheat plants led to increased Zn, Fe and Cu content, thus

102

showing their ability to promote translocation and mobilization of micronutrients (Rana et al.,

103

2012). PGPB treatment of rice helped in overcoming salt stress at the seedling stage. PGPB

104

treated plants showed a significant increase in shoot dry weight, root dry weight and total dry

105

matter accumulation (Sen and Chandrasekhar, 2014). PGPB treatment of chickpea, maize and

106

wheat have shown a significant increase in nutrient uptake and growth (Agbodjato et al.,

107

2016; Dogra et al., 2019; Yadav et al., 2019).

108

Phytohormones are growth regulators which affect seed growth, time of flowering,

109

sex of flowers, senescence of leaves, and ripening of fruits. These are mediated by

110

biochemical, molecular and physiological changes including gene expression and cell

111

division. The levels of phytohormones are regulated to enhance tolerance to abiotic and biotic

112

stress in order to minimize effect on plant growth. PGPB have been found to produce indole

113

acetic acid (IAA), an auxin, regulating cell division, cell elongation, differentiation, and

114

extension by increasing the osmotic content of the cell, increasing cell permeability,

115

decreasing wall pressure and inducing cell wall synthesis (Chandra et al., 2018). IAA is the

116

product of L-tryptophan metabolism by PGPB. IAA also delays or inhibits leaf abscission,

117

induces flowering and fruiting, and helps in increasing size, weight, branching number of the

118

root system, and its surface area. All these factors result in the increased ability of root to

119

explore soil for nutrient availability, thus having a positive effect on growth and nutrition

120

pool of plants (Goswami et al., 2016).

121

Phosphorus is an important macronutrient required for photosynthesis, signal

122

transduction, energy transfer, biosynthesis of macromolecules and respiration. The

123

availability of soluble P to the plant roots is influenced by the activity of soil microorganisms.

124

PGPB make the phosphorus available to plants by phosphate solubilization aided by the

7

125

release of mineral-absorbing compounds and liberating extracellular enzymes for phosphate

126

mineralization. Inorganic soil phosphates (example Ca3(PO4)2) are solubilized by the

127

production of siderophores and organic acids by PGPB (de Souza et al., 2015). In the case of

128

commercially important crops, phosphorus is provided by NPK fertilizers, but this

129

phosphorus reacts with many constituents in the soil and becomes inaccessible to the plants.

130

This phosphorus needs to be solubilized which is done by the microbes present in the

131

rhizosphere (Ahemad, 2015).

132

Siderophores are iron chelating agents produced by rhizobacteria which make the

133

inaccessible iron in the soil available to the plants. In the aerobic environment, iron exists as

134

hydroxides and iron oxides, which reduces their bioavailability for plants. Siderophores

135

released by the rhizobacteria scavenge iron from the mineral phases. Thus, the plants are

136

provided with soluble Fe3+ complexes which can be actively transported into the plant

137

system. Another advantage of the siderophore production is that it deprives the other

138

pathogenic bacteria of this metal, thus indirectly promoting plant growth.

139

Maize and sorghum grown in marginal soil with PGPB producing IAA

140

(phytohormone) and siderophore, and solubilizing phosphate promoted plant growth

141

compared to uninoculated control plants (Li et al., 2011; Li et al., 2014; Dhawi et al., 2015;

142

Dhawi et al., 2016). The growth promotion mediated by PGPB was significantly higher in

143

marginal soil compared to normal soil.

144

Plant growth promoting rhizobacteria (PGPR) colonize the root of the plant and

145

multiply to form microcolonies or produce biofilms. Biofilms are microbial populations that

146

have surface-adherent properties and are embedded within a self-produced matrix material

147

(de Souza et al., 2015). The biofilm also helps in increasing crop yield and quality by

148

protecting from biotic stresses (microbial competitors) and abiotic stresses by the secretion of

149

exopolysaccharides (Enebe and Babalola, 2018).

8

150

Biological nitrogen-fixation is brought about by nitrogen-fixing microorganisms,

151

using nitrogenase enzyme to reduce N2 to NH3. Nitrogenase is a complex enzyme encoded by

152

nitrogenase gene (nif). Of the total nitrogen fixed biologically, 80% is done with the help of

153

microbes associated symbiotically with the roots of the plants. Field studies in Brazil and

154

Mozambique showed higher production of soybean (Glycine max L.) through the

155

employment of biological nitrogen fixing PGPB belonging to Bradyrhizobium sp. (Chibeba et

156

al., 2018). Non-symbiotic nitrogen fixers are also important in nature as they help in the

157

accumulation of a significant amount of nitrogen. The nitrogen thus fixed by the microbes is

158

present in the bacterial cytoplasm in the form of ammonium ions which are finally secreted

159

into the host cytoplasm due to the concentration gradient (Li et al., 2017).

160

PGPB play an important role in biocontrol of pests and pathogens of plants by

161

triggering various plant defense mechanisms. One of them is the antagonism i.e., exclusion of

162

pathogens due to the ability of some bacteria to colonize a niche faster and more effectively,

163

reducing nutrient availability for harmful bacteria, producing antibiotics and organic

164

compounds that are lethal in low concentration for growth and metabolic activities of other

165

microorganisms. PGPB confer induced systemic resistance (IRS) to plants by the synthesis of

166

defense metabolites without causing a disease (Salomon et al., 2017). Fluorescent

167

pseudomonads are a major group of bacteria that play a key role in plant growth promotion,

168

induced systemic resistance and biological control of pathogens. Rhizobia are also known to

169

control the growth of many soilborne plant pathogenic fungi belonging to different genera

170

like Fusarium, Rhizoctonia, Sclerotium, and Macrophomina. P. polymyxa is well-known for

171

its ability to act as a biocontrol agent against a wide array of plant pathogens. It produces

172

antibiotic compounds like polymyxin and antifungal compounds like fusaricidin, which

173

suppress the growth of pathogens (Padda et al., 2017). The property of PGPB to act as

9

174

biocontrol agents enhances crop productivity indirectly preventing or reducing the crop loss

175

caused by pathogens.

176 177

PGPB Aided Phytoremediation (Rhizoremediation) as an Environment Friendly Green

178

Technology

179

There are several physicochemical and biological techniques in practice for the

180

remediation of soil. Out of these, remediation processes which are based on physicochemical

181

parameters are expensive and also affect the properties of soil, soil fertility, and biodiversity.

182

These remediation processes include vitrification, landfilling, chemical treatment, and

183

electrokinetics. In comparison, phytoremediation takes place at a marginal cost as it involves

184

harvesting plants. In addition, the biomass of plants used for phytoremediation can be utilized

185

for heat and energy production (Peuke and Rennenberg, 2005). Phytoremediation is an

186

emerging technology which includes the growth of plants on the impacted soil to degrade or

187

sequester the contaminants. Rhizoremediation is the exploitation of rhizospheric microbes to

188

enhance phytoremediation by increasing metal bioavailability in soil i.e., bio-augmentation.

189

Heavy metals are metallic elements having a density higher than 4 g/

190

cm3, are non-degradable and poisonous at low concentration (Kumar and Verma, 2018). In

191

China, approximately 19% of farmland is contaminated with heavy metals (Takahashi, 2016).

192

Another study estimated the total arable land in China contaminated with heavy metals to be

193

approximately ten million hectares (Teng et al., 2010; Shifaw, 2018). These heavy metals

194

persist for centuries once they are introduced into the soil as they cannot be degraded or

195

destroyed by microbial or chemical processes (Bolan et al., 2014). Land polluted with heavy

196

metals becomes unfit for agricultural use as high metal toxicity inhibits the activity of

197

cytoplasmic enzymes in plant cells and causes damage to cell structures as well as DNA due

198

to oxidative stress which ultimately affects plant growth and metabolism (Ojuederie and

10

199

Babalola, 2017). Certain PGPB show metal tolerance and can directly improve plant growth

200

by producing beneficial substances including solubilization/ transformation of mineral

201

nutrients, production of organic acids, phytohormones, siderophores and antioxidant enzymes

202

(Chirakkara et al., 2016; Ma et al., 2016). There are two possible ways microbes can help in

203

soil remediation. One of them is increasing bioavailability and mobility of metal(loid)s by

204

producing chelating and desorbing agents that enhance their removal. Another way is

205

decreasing their bioavailability and mobility by secreting precipitating agents that reduce

206

their transfer to the food chain. Bacteria including PGPB have devised several resistance

207

mechanisms (Gadd, 2010). These include reducing the bioavailability of toxic metals through

208

metal transformation, metal biosorption, metal accumulation and siderophore production

209

(Figure 2). Metal transformation is the process of conversion of the toxic form of metal to its

210

less toxic or non-toxic form by the action of microbes. Biosorption is a passive process which

211

involves the binding of metals to the cell surface. Outer polysaccharide coating, S-layer of

212

bacteria, and the extracellular matrix can provide many sites for adsorbing and trapping

213

metals due to the presence of many anionic functional groups (e.g., sulfhydryl, carboxyl,

214

hydroxyl, sulfonate, and amine and amide groups), thereby immobilizing the toxic elements

215

resulting in local detoxification (Rajkumar et al., 2010). Biofilms, generally composed of

216

extracellular polymeric substances (EPS), have also been reported to adsorb heavy metals

217

(Harrison et al., 2006). The ability to bind metals extracellularly has been reported in

218

Klebsiella aerogenes, Pseudomonas putida, Bacillus sphaericus, and Arthrobacter viscosus

219

(Bruins et al., 2000). The EPS produced by the bacterium Paenibacillus jamilae and the

220

cyanobacterium Nostoc spongiaeforme form complexes with Pb and Zn, respectively (Pérez

221

et al., 2008; Hietala and Roane, 2009). Siderophore (pyoverdine and pyochelin)-producing P.

222

aeruginosa also decreased the toxicity of Al, Co, Cu, Ni, Pb and Zn by the same mechanism

11

223

(Braud et al., 2010). It has been reported that Proteobacteria, Firmicutes, and Actinobacteria

224

reduced the high concentrations of Mn, Pb and As in metal polluted soil (Chen et al., 2015).

225

PGPB are known to produce biosurfactants which increase mobility and subsequent

226

phytoremediation of toxic metals. These biosurfactants develop complexes with insoluble

227

heavy metals at soil surface inducing desorption of metals from soil matrix and thereby

228

enhance metal bioavailability by increasing metal solubility (Gadd 2010; Rajkumar et al.,

229

2012). For example, biosurfactant di-rhamnolipid produced by Pseudomonas aeruginosa BS2

230

increased mobility and solubility of Cd and Pb (Ullah et al., 2015).

231

PGPB have been shown to reduce metal accumulation or their harmful effects in food

232

crops. For instance, two metal-resistant bacteria belonging to genus Bacillus and

233

Neorhizobium decreased cadmium bioavailability in soil and bioaccumulation in polished rice

234

(Li et al., 2017). In another study, two rhizobacterial strains were shown to promote growth

235

in maize by producing phytohormones and antioxidant enzymes that decreased the

236

deleterious effects of lead (Hassan et al., 2014). Acinetobacter Sp. nbri05 increased the

237

growth and yield of chickpea and at the same time reduced the arsenic uptake by shoots

238

(Srivastava and Singh, 2014). Some microbes have the ability to degrade heavy metals. For

239

example, Pseudomonas sp. MBR has been shown to perform biotransformation of single Fe

240

(III), Zn and Cd–citrate complexes followed by their elimination (Kumar and Verma, 2018).

241 242

Drought Stress Amelioration Mediated by PGPB

243

Climate change has affected crop production globally. High temperature accompanied

244

with lack of rainfall will result in drought and the effect will be more pronounced on marginal

245

soil. Drought alters not only plant responses to pathogens but also microbial communities

246

adapted. Drought stress affects various growth parameters, and stress-responsive genes as

247

limited water content reduces cell size, membrane integrity, generates reactive oxygen

12

248

species and promotes senescence (Tiwari et al., 2016). Further, it increases ethylene

249

production, reduces chlorophyll content, and inhibits photosynthesis. Drought also affects

250

enzymes such as nitrate reductase (NR) due to lower uptake of nitrate from the soil (Caravaca

251

et al., 2005). Abscisic acid (ABA) is an important growth regulator during drought stress.

252

ABA is responsible for inducing stomatal closure which reduces water consumption in plants,

253

thus, improving drought tolerance (Helander et al., 2016). The concentration of ABA

254

increases in plants inoculated with PGPB, which ameliorates drought stress by regulating

255

transcription of drought-related genes and root hydraulic conductivity (Cohen et al., 2015;

256

Kumar and Verma, 2018). Several bacterial isolates (eg. Bacillus sp., Pseudomonas sp.,

257

Paenibacillus sp., Acinetobacter sp., Sphingobacterium sp., Enterobacter sp., and Delftia sp.)

258

improved resistance to drought by increasing the overall fitness of the plant which is

259

dependent on production of plant hormones, abscisic acid (ABA), IAA and gibberellin as

260

well as genotype by environment effect (Salomon et al., 2014; Naylor and Coleman-Derr,

261

2018). Exopolysaccharide producing bacteria also produce proline which improved drought

262

tolerance through regulation of physiological and biochemical parameters such as relative

263

water content and production of protein and sugars (Kumar and Verma, 2018; Naseem et al.,

264

2018). Thus, bacterial strains isolated from prolonged water deficit environment can enhance

265

drought tolerance and water homeostasis by colonizing plant roots.

266 267

Salt Stress Signaling and Rhizoremediation of Saline Soils

268

Osmotic stress increases ABA production which reduces the photosynthetic capacity

269

in plants due to partial closure of stomata (Chaves et al., 2009; Zörb et al., 2013). ABA has

270

also been shown to up-regulate the expression of vacuolar Na+/H+ antiporter gene under

271

salinity stress (Figure 3; Shi and Zhu, 2002). The use of PGPB and other associated

272

symbiotic microorganisms has proved beneficial to develop potential strategies to facilitate

13

273

plant growth in saline soils (Kohler et al., 2010). The increased levels of 1-

274

aminocyclopropane-1-carboxylate during salt stress is majorly responsible for causing plant

275

damage (Botella et al., 2000). Rhizobacteria act as a sink for 1-aminocyclopropane-1-

276

carboxylate and can further hydrolyse it to ammonia and α-ketobutyrate, thereby reducing the

277

level of ethylene. Further, 1-aminocyclopropane-1-carboxylate deaminase producing bacteria

278

can degrade 1-aminocyclopropane-1-carboxylate present in plants and supply nitrogen and

279

energy, thus promoting plant growth under salinity stress conditions (Nadeem et al. 2010;

280

Siddikee et al. 2010).

281

The genetic basis of salt tolerance has been well defined in the model plant

282

Arabidopsis by identification of Salt-Overly Sensitive (SOS) pathway. The harmful effects of

283

excess sodium ions are minimized by moving them into vacuoles using Na+/H+ exchanger 1

284

(NHX1) located in the tonoplast and SALT OVERLY SENSITIVE 1 (SOS1) located in the

285

plasma membrane (Munns and Tester 2008). In addition, the SOS signaling pathway is

286

reported to export Na+ out of the cell (Deinlein et al., 2014). HKT1 (High-affinity

287

K+ transporter) is another transporter essential in the long-distance transport of Na+ (Platten

288

et al., 2006). Plants activate HKT to increase the uptake of K+ ions over Na+ ions and

289

K+ concentration, resulting in higher Na+ in the cytoplasm, which confers salinity tolerance

290

(Ilangumaran and Smith, 2017). Significant increase in the expression of SOS1 and SOS4 was

291

observed in wheat plants subjected to salinity stress and PGPR (Dietzia natronolimnaea)

292

treatment compared to plants subjected to salinity stress (Bharti et al., 2016).

293

Salinity stress enhances the production of phytohormones, ABA, SA and ethylene

294

(Xiong et al., 2002). These phytohormones initiate a signaling cascade. For instance, ABA

295

upregulates specific genes under the control of transcription factors such as the ABA-

296

responsive element binding protein (Shinozaki and Yamaguchi-Shinozaki, 2007). A

297

carotenoid-producing halotolerant PGPB modulates transcriptional machinery to confer

14

298

salinity tolerance in wheat (Bharti et al. 2016). In addition to modulation in the expression of

299

SOS pathway-related genes, the study revealed the involvement of ABA-signalling cascade

300

and enhanced expression of TaST (a salt stress-induced gene) in PGPB inoculated plants in

301

comparison to uninoculated control plants. Thus, it can be concluded that PGPB-mediated

302

salinity tolerance is a complex phenomenon involving modulation of ABA signalling, SOS

303

pathway, ion transporters and antioxidant machinery.

304

PGPB promote plant growth in saline soils by producing the enzyme ACC deaminase

305

which cleaves 1-aminocyclopropane-1-carboxylic acid (ACC), thereby lowering ethylene

306

(stress hormone) in plants (Etesami and Beattie, 2018). These bacteria can help in improving

307

the soil conditions as well as plant growth through direct and indirect mechanisms. The direct

308

mechanism involves solubilization of mineral phosphates, asymbiotic nitrogen fixation, and

309

the production of plant hormones. The indirect improvement of such soils can take place

310

through the production of antibiotics, cell wall degrading enzymes, hydrogen cyanide, and

311

siderophores leading to biological control of pathogenic microbes. Some rhizobacteria such

312

as Pseudomonas fluorescens MSP-393, confer salt tolerance through the synthesis of

313

osmolytes, alanine, glutamic acid, and threonine in their cytosol (Paul and Nair, 2008).

314

Certain PGPR strains protect plants from the harmful effects of high Na+ concentration in the

315

saline soil environment via producing exopolysaccharides (Banerjee et al., 2019). The

316

exopolysaccharides reduce Na+ uptake in the plant by binding it and also by biofilm

317

formation. The reduced availability of Na+ results in lowering its uptake, thereby maintaining

318

high K+/Na+ ratio which is essential for salinity tolerance and maintenance of osmotic

319

potential in a plant (Nadeem et al., 2014). Alteration of cell envelope is another mechanism

320

which is accomplished through the production of exopolysaccharides, which enhance water

321

retention and regulate the diffusion of carbon sources (Kaushal and Wani, 2016).

15

322

Saline-tolerant Azospirillum strain increased shoot dry weight, grain yield and N

323

concentration of wheat grown under saline soil (Nia et al., 2012). Another study conducted

324

using halotolerant bacteria, Hallobacillus sp. and Bacillus halodenitrificans showed a

325

significant increase in root elongation and dry weight of wheat compared to uninoculated

326

control in saline soil (Shrivastava and Kumar 2015). Plant phosphorus uptake is reduced in

327

saline soil as phosphate ions precipitate in the presence of calcium ions (Bano and Fatima,

328

2009). The characteristics of PGPB such as phosphate solubilization, production of IAA and

329

siderophores can aid in the tolerance to salinity of soils (Ilangumaran and Smith, 2017).

330

Lowering the precursor of ethylene concentrations through the activity of 1-

331

aminocyclopropane-1-carboxylate (ACC) deaminase is one of the strategies adopted by

332

PGPB (Bharti and Barnawal, 2019). The enzymatic activity of ACC deaminase improves

333

plant growth by lowering the available ACC in the ethylene biosynthetic pathway. This

334

pathway produces ACC which is secreted by the plant into the rhizosphere, where ACC

335

deaminase producing PGPR can consume ACC as a source of fixed nitrogen. This ultimately

336

leads to the development of more PGPB around the rhizosphere in saline soils. IAA

337

producing PGPB secrete the auxin into the rhizosphere, where the plant can take up the

338

hormone, resulting in improved cell growth. Such an increase in IAA concentration leads to

339

an upregulation of ACC synthase production and activity. The above strategies adopted by

340

PGPB and halotolerant bacteria are helpful for remediation of saline soils and improve plant

341

growth under saline stress.

342 343

Carbon Sequestration by PGPB: An Underexplored Field with Huge Implications

344

Atmospheric CO2 levels are more than 400 ppm, which have to be reduced to 300-350

345

ppm (Kittredge, 2015). To achieve this target, it is not enough to reduce greenhouse gas

346

emissions but also to return the carbon to soil for long term storage. Globally, soils are

16

347

estimated to contain twice as much carbon as the atmosphere affirming them as a

348

predominant sink for atmospheric carbon dioxide and organic carbon (Schlesinger and

349

Bernhardt, 2013). Soil and plant biomass together can hold nearly 2.5 times more carbon than

350

the atmosphere (Singh et al., 2010b). Microorganisms are involved in nutrient cycling as they

351

carry out biochemical transformations involved in the decomposition process of organic

352

matter which is either assimilated and incorporated into biomass or immobilized in the form

353

of soil biomass (Figure 4; Grover et al., 2015; Mellado-Vázquez et al., 2019). Removal of

354

plant biomass by annual clipping changed soil microbial community structure accompanied

355

with an increase in carbon degrading genes (Xue et al., 2018). Despite the significant role of

356

soil microbes, in general and specifically PGPB on carbon sequestration, it is an

357

underexplored research area.

358

Land management practices influenced the total carbon in soil with the use of

359

fertilizer, reducing the soil microbial activity and total carbon (Wu et al., 2009). Soil

360

microbial communities including PGPB, contribute to soil organic carbon which is dependent

361

on available nitrogen levels (Grover et al., 2015). Addition of PGPB (P. fluorescens) have

362

been shown to increase plant C:N under enhanced CO2 (Nie et al., 2015). PGPB also reduced

363

microbial respiration elevated due to enhanced CO2. Future climate change would involve

364

higher temperature which leads to higher microbial degradation resulting in elevated CO2

365

emitted in the atmosphere and soil (Sofi et al., 2016). Growing energy crops on marginal

366

lands can sequester soil carbon between 0.25 and 4 Mg C ha−1 yr−1, thereby restoring

367

contaminated soils (Blanco-Canqui, 2016). The soil organic carbon (SOC) pool indicates soil

368

health and quality which has an essential role in soil sustainability. Understanding the role of

369

plant-PGPB interactions in carbon sequestration will be the key to improving the process in

370

marginal soil where the returns will be much higher than healthy soils.

371

17

372

Biofuels from Plant Biomass Enhanced by PGPB Introduced in Marginal Soil

373

The demand for food and energy is increasing with the rise in world population. The

374

shortage of energy has become a key issue all over the world. Biomass is biological material

375

from living organisms (mostly plants), which is a renewable source. Biomass can be used

376

both directly and indirectly for the production of biofuel. Scientific and stakeholder

377

communities have been discussing and debating whether restricting the development of

378

biofuel crops to marginal agricultural land can ameliorate the conflicts among food

379

production, biofuel production, and the environment (Cai et al., 2010). Phytoremediation

380

involving hyperaccumulating plants to clean up the legacy of contamination, including metal

381

and salts, is promising as the contaminants are completely removed from the soil system (Wu

382

et al., 2006). In this context, PGPB play multiple roles as they help their host plant to cope

383

not only with contaminant induced stress but also in improving plant growth. Plants grown in

384

contaminated soil aided by PGPB cannot be used as food and fodder, but they are suitable for

385

use as stocks for biofuel and carbon sequestration through biomass production (Taghavi et

386

al., 2009). Phytoremediation utilizing bioenergy crops/plants is an efficient method for

387

remediation of saline and sodic soil as well as for metal-contaminated soil because the

388

harvested biomass can be used to produce biofuel (biodiesel or bioethanol) or other

389

commercial by-products such as fiber, wood, charcoal, alkaloid, and bioplastic while helping

390

in soil amelioration (Bharti et al., 2017). The best bioenergy crops for soil amelioration

391

should have high biomass production, be cost-effective, less nutrient, and water requirements,

392

and be carbon neutral for the whole life cycle.

393

Biofuels are categorized based on their feedstocks. The first-generation biofuels are

394

obtained from the food crops such as sugar cane, sugar beets, rapeseed, soybeans, oil palms,

395

and corn, but this raises the food versus fuel crisis and contributes to higher food prices.

396

Second-generation biofuels are produced from non-food crop feedstocks such as Jatropha,

18

397

Pongamia and Miscanthus), but the major problem is the requirement of vast areas of land for

398

their cultivation (Elrayies, 2018). Therefore, growing them on marginal lands is a good idea

399

to overcome some of the aforementioned limitations of the first-generation crops. Some of

400

the energy crops that are extensively used worldwide include Miscanthus, Ricinus, Jatropha,

401

and Populus. A recent study showed that application of PGPB such as Azotobacter and

402

Azospirilum alone as well as in combination with quarter dose of NP fertilizers markedly

403

improved the oil quality of safflower by improving the oxidation stability, cetane number,

404

viscosity and cold flow properties which are very important variables affecting biodiesel

405

quality (Nosheen et al., 2018).

406

Foxtail millet (Setaria italica) is an annual C4 grass grown in arid and semi-arid

407

regions of the world and it is considered to be a good candidate for biofuel production

408

(Pandey et al., 2017) due to high production of biomass which is suited for saccharification

409

(Dhawi et al., 2018). Sweet sorghum (Sorghum bicolor L) is considered one of the most

410

drought-resistant energy crop with high biomass yield and photosynthetic efficiency and

411

lower production costs than many other energy plants. Heavy metals such as Cd, Pb, and Cu

412

could be removed by using sweet sorghum and therefore, it is a good candidate for biofuel

413

production on marginal land.

414

Growth and productivity of plants are highly compromised due to abiotic stress, poor

415

nutrition and heavy metal contamination. There is a need for an in-situ selection of high

416

biomass and/ or metal accumulating clones. High metal-resistant bacteria which can

417

accumulate heavy metals like- lead and zinc, may take advantage of their cellular metabolism

418

and metal detoxification mechanism to take up the metals with an increase in biomass when

419

grown in marginal soil (Li and Ramakrishna, 2011). Pseudomonas sp. TLC 6-6.5-4 which is

420

a free-living metal resistant PGPB isolated from Torch lake sediment promoted maize growth

421

and nutrient uptake and increased biomass (Li et al., 2014). The interaction between PGPB

19

422

and maize is mutualistic, where PGPB helps in promoting plant growth by the production of

423

IAA and other compounds and in turn maize plant gives out phenolic compounds in root

424

rhizosphere, which serve as the carbon source for PGPB. With the help of PGPB, plants

425

grown in very poor soil can cope with heavy metal stress by regulating a number of proteins

426

and metabolic pathways (Li et al., 2014; Pidatala et al., 2018). Another related study

427

evaluated the effect of arbuscular mycorrhiza and PGPB on element uptake, biomass and

428

metabolic responses in maize roots grown in mining-affected soil. The element uptake and

429

biomass were significantly higher in the plants treated with arbuscular mycorrhiza and PGPB

430

as compared to normal plants. These were attributed most likely to changes in galactose

431

metabolism, fatty acid synthesis, and phenylpropanoid biosynthesis, among others. A similar

432

study with sorghum grown in marginal soil with mycorrhiza and PGPB resulted in increased

433

uptake of elements and enhanced the root and shoot biomass (Dhawi et al., 2016). The

434

metabolites upregulated by PGPB are part of galactose metabolism and fatty acid

435

biosynthesis.

436

Plants under abiotic or biotic stress are known to induce the production of reactive

437

oxygen species (ROS). ROS at low levels provide a balanced cellular redox for growth

438

regulation whereas, at high concentrations, ROS interfere with lipid peroxidation, DNA

439

synthesis, and enzymatic activities. Analysis of sorghum treated with microbial inoculations

440

showed the upregulation of proteins such as superoxide dismutase (SOD) which is involved

441

in scavenging of ROS (Dhawi et al., 2017). Foxtail millet is considered as a good biofuel

442

source due to high biomass production. Foxtail millet inoculated with mycorrhiza and PGPB

443

increased metabolites which led to an increase in sugar yield (Dhawi et al., 2018).

444

The third-generation biofuels are generated from cyanobacterial, microalgae and other

445

microbes, which hold the most promising approach to meet the global energy demand. They

446

provide several advantages over energy crops such as low-cost requirement, high oil

20

447

productivity, high yield per acre and most importantly it can be cultivated on non-productive

448

or deteriorated land or marginal land that is unsuitable for agriculture. The potential for

449

biodiesel production from microalgae is 15 to 300 times more than traditional crops on an

450

area basis (Dragone et al., 2010). These reasons make algae an alternative source for

451

biodiesel production. In this context, certain PGPB have been known to enhance algal

452

growth (Dao et al., 2018). Azospirillum sp. (N2-fixing bacterium), Bacillus sp. and

453

Rhizobium sp. have been implicated in growth promotion of unicellular microalgae Chlorella

454

vulgaris by regulating cell count and morphology, lipid and pigment production (Fuentos et

455

al., 2017; Ramos-Ibarra et al., 2019). Although microalgae cultured with PGPB would be a

456

new potential strategy for improving large-scale microalgal cultivation, there are issues with

457

the high cost of production which have to be optimized (Quinn and Davis, 2015).

458

Third world countries are mostly dependent on foreign countries for their oil

459

requirement which is a huge drain on their foreign currency reserves. For instance, the 1970

460

oil crisis led to the establishment of bioenergy promotion in India (Bharti et al., 2017).

461

Energy production from biomass in India is estimated at 12.8% of the total renewables.

462

Sustainable utilization of wasteland for biomass and bioenergy production and soil carbon

463

sequestration would be a better choice for regaining a healthy ecosystem and decreasing the

464

dependence on foreign countries. Overall, a better understanding of metabolic pathways will

465

help in enhancing PGPB interactions with plants to exploit them for promoting plant growth

466

in marginal soil.

467 468

Conclusion

469

Higher food production for the ever-growing population is a key issue facing the

470

world. The energy crisis is another important issue. The exploitation of marginal land with

471

poor soil health can lead to mitigation of one or both of the above issues. Employment of 21

472

high biomass and/ or metal hyperaccumulating plants in combination with PGPB can produce

473

biofuels and/ or enhance crop productivity depending on the type of marginal land.

474

Furthermore, the use of PGPB in increasing algal biomass is a new theme and requires

475

attention and can prove advantageous in terms of biofuel. In short, marginal soil can be

476

termed as brown gold whose full potential will be realized when mining is performed with

477

the help of plants and PGPB.

478 479

Funding: This study was funded by Science and Engineering Board (SERB), Department of

480

Science and Technology, Government of India (grant number EMR/2016/006311) to

481

Wusirika Ramakrishna, Council of Scientific and Industrial Research (CSIR) Junior Research

482

Fellowship University Grants Commission (UGC) Senior Research Fellowship to

483

Radheshyam Yadav.

484 485 486 487 488 489

22

490

Figure 1. Distribution of marginal land worldwide. The total marginal land globally is

491

estimated to be around 13.1 global hectares (Gha) of which Asia, Africa, Latin America &

492

Caribbean constitutes more than 50% of the total area. Adapted from Mehmood et al. (2017).

493 494

Figure 2.

Alleviation of heavy metal contamination by PGPB employing various

495

mechanisms. Biotransformation is the process of conversion of a toxic form of metal to

496

lesser toxic form by the action of micro-organisms. Bioaccumulation is a process where

497

heavy metals are transported across the bacterial membranes through dedicated ion pumps

498

and ion channels. Biosorption is the process of adsorption of metal/metal pollutants to the

499

cell surface of micro-organisms. Bioassimilation is the mechanism by which microbes

500

increase metal solubilization in soils by secreting organic acids and metal-specific ligands

501

(e.g., siderophore) which enhance chelation efficacy. Bioleaching is the metal precipitation

502

process carried out by some sulfate-reducing bacteria (SRB) that modify metal bioavailability

503

in soil. Biosurfactant production by certain PGPB can increase mobility and help in

504

subsequent phytoremediation of toxic metals. All these processes alter metal bioavailability

505

and help in phytoremediation. Rhizoremediation is the use of rhizospheric microbes for

506

enhancing phytoremediation.

507 508

Figure 3. Molecular signalling pathways involved during salt stress in plants. An unknown

509

sensor senses the high Na+ concentration and initiates Ca2+, ROS, and hormone signaling

510

cascades which trigger the SOS pathway through calcium-dependent protein kinase pathway.

511

Ca2+-signaling pathway involves CBLs, CIPKs, and CDPKs which change the overall

512

transcriptional profile of the plant by activating expression of several detoxification

513

mechanisms including HKT, NHX, SOS, ROS and other osmotic protection strategies. SOS3

514

senses the cytosolic calcium signal and on interaction activates SOS2 which in turn activates

23

515

SOS1 that maintains/balance Na+ concentration by extrusion of excess Na+ into the soil

516

solution and loading Na+ into the xylem for long-distance transport to leaves via

517

transpirational stream. Na+/H+ exchangers (NHX) located on the tonoplast regulate the

518

intracellular compartmentation of Na+ driven by a proton gradient. PGPB-mediated salinity

519

tolerance involves modulation of ABA signalling and SOS pathway. Adapted from Deinlein

520

et al. (2014) and Zhu (2016).

521

Figure 4. Soil carbon sequestration mediated by bacteria. The root exudates released by

522

plants in the rhizosphere serve as an ecological niche where microbes compete for organic

523

carbon compounds. The beneficial bacteria interact with plants by colonizing roots, while the

524

growth of pathogenic bacteria is inhibited. The microbial biomass multiplies, thereby

525

increasing plant biomass via plant growth promotion activity. Microbial communities help in

526

the conversion of dead plant tissue into CO₂. The result is an increase in soil organic carbon

527

content through the process of rhizodeposition of organic compounds such as sugars, amino

528

acids, and carboxylic acids exuded by roots, thereby sequestering atmospheric C into the soil.

529

Adapted from Grover et al. (2015).

530 531

References

532

Agbodjato NA, Noumavo PA, Adjanohoun A, Agbessi L, Baba-Moussa L., 2016. Synergistic

533

effects of plant growth promoting rhizobacteria and chitosan on in vitro seeds

534

germination, greenhouse growth, and nutrient uptake of maize (Zea mays L.).

535

Biotechnol. Res. Intl. 2016, 7830182.

536 537

Ahemad

M.,

2015.

Phosphate-solubilizing

bacteria-assisted

phytoremediation

of

metalliferous soils: a review. 3 Biotech 5, 111–121.

24

538 539

Ashraf M, Wu L., 1994. Breeding for salinity tolerance in plants. Crit. Rev. Plant Sci. 13, 1742.

540

Banerjee A., Sarkar S., Cuadros-Orellana S., Bandopadhyay R., 2019. Exopolysaccharides

541

and biofilms in mitigating salinity stress: The biotechnological potential of halophilic

542

and soil-inhabiting PGPR microorganisms. In: Giri B., Varma A. (eds)

543

Microorganisms in Saline Environments: Strategies and Functions. Soil Biology, 56,

544

133-153 Springer, Cham.

545 546

Bano A, Fatima M., 2009. Salt tolerance in Zea mays (L). following inoculation with Rhizobium and Pseudomonas. Biol. Fertil. Soils 45, 405-413.

547

Bermudez G.M., Jasan R., Plá R., Pignata M.L., 2012. Heavy metals and trace elements in

548

atmospheric fall-out: their relationship with topsoil and wheat element composition. J.

549

Hazard. Mater. 213, 447-56.

550

Bharti N, Pandey SS, Barnawal D, Patel VK, Kalra A., 2016. Plant growth promoting

551

rhizobacteria Dietzia natronolimnaea modulates the expression of stress responsive

552

genes providing protection of wheat from salinity stress. Scientific Rep. 6, 34768.

553

Bharti P, Singh B, Bauddh K, Dey R, Korstad J., 2017. Efficiency of bioenergy plant in

554

phytoremediation of saline and sodic soil. In: Phytoremediation Potential of

555

Bioenergy Plants pp. 353-69, Springer.

556

Bharti N, Barnawal D., 2019. Amelioration of salinity stress by PGPR: ACC deaminase and

557

ROS scavenging enzymes activity. In: PGPR Amelioration in Sustainable

558

Agriculture: Food Security and Environmental Management Ed: Singh AK, Kumar A,

559

Singh PK, pp. 85-106, Woodhead Publishing.Blanco-Canqui, H., 2016. Growing

560

dedicated energy crops on marginal lands and ecosystem services. Soil Sci. Soc.

561

Amer. J. 80, 845-858.

25

562

Bolan N, Kunhikrishnan A, Thangarajan R, Kumpiene J, Park J, Makino T, Kirkham MB,

563

Scheckel K., 2014. Remediation of heavy metal(loid)s contaminated soils–to mobilize

564

or to immobilize? J. Hazard. Mater. 266, 141-166.

565

Botella MÁ, Del Amor F, Amorós A, Serrano M, Martínez V, Cerdá A., 2000. Polyamine,

566

ethylene and other physico‐chemical parameters in tomato (Lycopersicon esculentum)

567

fruits as affected by salinity. Physiologia Plantarum 109, 428-434.

568

Braud A, Geoffroy V, Hoegy F, Mislin GL, Schalk IJ. 2010. Presence of the siderophores

569

pyoverdine and pyochelin in the extracellular medium reduces toxic metal

570

accumulation in Pseudomonas aeruginosa and increases bacterial metal tolerance.

571

Environ. Microbiol. Rep. 2, 419-425.

572 573 574 575

Bruins MR, Kapil S, Oehme FW., 2000. Microbial resistance to metals in the environment. Ecotoxicol. Environ. Safety 45, 198-207. Cai X, Zhang X, Wang D., 2010. Land availability for biofuel production. Environ. Sci. Technol. 45, 334-339.

576

Caravaca F, Alguacil M, Hernández J, Roldán A., 2005. Involvement of antioxidant enzyme

577

and nitrate reductase activities during water stress and recovery of mycorrhizal

578

Myrtus communis and Phillyrea angustifolia plants. Plant Sci. 169, 191-197.

579

Chandra S, Askari K, Kumari M., 2018. Optimization of indole acetic acid production by

580

isolated bacteria from Stevia rebaudiana rhizosphere and its effects on plant growth.

581

J. Genet. Eng. Biotechnol. 16, 581-586.

582 583

Chaves MM, Flexas J, Pinheiro C., 2009. Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell. Annals Bot. 103, 551-560.

584

Chen M, Xu P, Zeng G, Yang C, Huang D, Zhang J., 2015. Bioremediation of soils

585

contaminated with polycyclic aromatic hydrocarbons, petroleum, pesticides,

26

586

chlorophenols and heavy metals by composting: applications, microbes and future

587

research needs. Biotechnol. Adv. 33, 745-755.

588

Chibeba AM, Kyei-Boahen S, Guimarães MF, Nogueira MA, Hungria M., 2018. Feasibility

589

of transference of inoculation-related technologies: A case study of evaluation of

590

soybean rhizobial strains under the agro-climatic conditions of Brazil and

591

Mozambique. Agric. Ecosyst. Environ. 261, 230-240. Chirakkara RA, Cameselle C,

592

Reddy KR., 2016. Assessing the applicability of phytoremediation of soils with mixed

593

organic and heavy metal contaminants. Rev. Environ. Sci. Bio/Technol. 15, 299-326.

594

Cohen AC, Bottini R, Pontin M, Berli FJ, Moreno D, Boccanlandro H, Travaglia CN, Piccoli

595

PN., 2015. Azospirillum brasilense ameliorates the response of Arabidopsis thaliana

596

to drought mainly via enhancement of ABA levels. Physiologia Plantarum 153, 79-90.

597

Cowie AL, Orr B, Sanchez VMC, Chasek P, Crossmane ND, Erlewein A, et al., 2018. Land

598

in balance: The scientific conceptual framework for land degradation neutrality.

599

Environ. Sci. Policy 79, 25-35.

600

Dao G-H, Wu G-X, Wang X-X, Zhang T-Y, Zhan X-M, Hu H-Y., 2018. Enhanced

601

microalgae growth through stimulated secretion of indole acetic acid by symbiotic

602

bacteria. Algal Res. 33, 345-351.

603

de Souza R, Meyer J, Schoenfeld R, da Costa PB, Passaglia LM., 2015. Characterization of

604

plant growth-promoting bacteria associated with rice cropped in iron-stressed soils.

605

Annals Microbiol. 65, 951-964.

606 607

Deinlein U, Stephan AB, Horie T, Luo W, Xu G, Schroeder JI., 2014. Plant salt-tolerance mechanisms. Trends Plant Sci. 19, 371-379.

608

Dhawi F, Datta R, Ramakrishna W., 2016. Mycorrhiza and heavy metal resistant bacteria

609

enhance growth, nutrient uptake and alter metabolic profile of sorghum grown in

610

marginal soil. Chemosphere 157, 33-41.

27

611

Dhawi F, Datta R, Ramakrishna W., 2017. Proteomics provides insights into biological

612

pathways altered by plant growth promoting bacteria and arbuscular mycorrhiza in

613

sorghum grown in marginal soil. Biochim. Biophys. Acta (BBA)-Prot. Proteomics

614

1865, 243-251.

615

Dhawi F, Datta R, Ramakrishna W., 2018. Metabolomics, biomass and lignocellulosic total

616

sugars analysis in foxtail millet (Setaria italica) inoculated with different

617

combinations of plant growth promoting bacteria and mycorrhiza. Comm. Plant Sci.

618

8, 8-14.

619

Dragone G, Fernandes BD, Vicente AA, Teixeira JA., 2010. Third generation biofuels from

620

microalgae. Curr. Res. Technol. Education Topics in Appl. Microbiol. Microbial

621

Biotechnol. 2, 1355-1366.

622

Dogra N, Yadav R, Kaur M, Adhikary A, Kumar S, Ramakrishna W., 2019. Nutrient

623

enhancement of chickpea grown with plant growth promoting bacteria grown in local

624

soil

625

https://doi.org/10.1007/s12298-019-00661-9

of

Bathinda,

Northwestern

India.

Physiol.

Mol.

Biol.

Plants

626

Edrisi S.A., Abhilash P., 2016. Exploring marginal and degraded lands for biomass and

627

bioenergy production: an Indian scenario. Renewable Sustainable Energy Rev. 54,

628

1537-1551.

629 630

Elrayies GM., 2018. Microalgae: prospects for greener future buildings. Renewable Sustainable Energy Rev. 81, 1175-1191.

631

Enebe MC, Babalola OO., 2018. The influence of plant growth-promoting rhizobacteria in

632

plant tolerance to abiotic stress: a survival strategy. Appl. Microbiol. Biotechnol. 102,

633

7821-7835.

28

634

Etesami H, Beattie GA., 2018. Mining halophytes for plant growth-promoting halotolerant

635

bacteria to enhance the salinity tolerance of non-halophytic crops. Front. Microbiol. 9,

636

148.

637 638

FAO/IIASA/ISRIC/ISS-CAS/JRC., 2008. Harmonized world soil database (version 1.0). Rome: FAO.

639

Fuentes JL, Garbayo I, Cuaresma M, Montero Z, González-del-Valle M, Vílchez C., 2016.

640

Impact of microalgae-bacteria interactions on the production of algal biomass and

641

associated compounds. Mar. Drugs 14, 100.

642 643 644 645 646 647

Gadd GM., 2010. Metals, minerals and microbes: geomicrobiology and bioremediation. Microbiol. 156, 609-643. Gibbs HK, Salmon JM., 2015. Mapping the world's degraded lands. Appl. Geography 57, 1221. Goswami D, Thakker JN, Dhandhukia PC., 2016. Portraying mechanics of plant growth promoting rhizobacteria (PGPR): A review. Cogent Food Agric. 2, 1127500.

648

Grover M, Maheswari M, Desai S, Gopinath KA, Venkateswarlu B., 2015. Elevated CO2:

649

Plant associated microorganisms and carbon sequestration. Appl. Soil Ecol. 95, 73–

650

85.

651 652 653 654

Gupta, SK., 2010. Management of alkali water (Technical Bulletin CSSRI/Karnal/2010/01, p. 62). Karnal: Central Soil Salinity Research Institute. Harrison JJ, Rabiei M, Turner RJ, Badry EA, Sproule KM, Ceri H., 2006. Metal resistance in Candida biofilms. FEMS Microbiol. Ecol. 55, 479-491.

655

Hassan W, Bano R, Bashir F, David J., 2014. Comparative effectiveness of ACC-deaminase

656

and/or nitrogen-fixing rhizobacteria in promotion of maize (Zea mays L.) growth

657

under lead pollution. Environ. Sci. Pollut. Res. 21, 10983-10996.

29

658 659 660 661

Helander JD, Vaidya AS, Cutler SR., 2016. Chemical manipulation of plant water use. Bioorg. Med. Chem. 24, 493-500. Hietala K, Roane T., 2009. Microbial remediation of metals in soils. In: Advances in Applied Bioremediation Springer pp. 201-220.

662

Hollander JH., 1895. The concept of marginal rent. Quarterly J. Econ. 9, 175-187.

663

Gayathri I, Donald S., 2017. Plant growth promoting rhizobacteria in amelioration of salinity

664

stress: A systems biology perspective. Front. Plant Sci. 8, 1768.

665

Kaushal M, Wani SP., 2016. Rhizobacterial-plant interactions: strategies ensuring plant

666

growth promotion under drought and salinity stress. Agric. Ecosyst. Environ. 231, 68-

667

78.

668 669

Kittredge J., 2015. Soil carbon restoration: Can biology do the job? Northeast Organic Farming Association/Massachusetts Chapter, Inc. August 14, 2015.

670

Kohler J, Caravaca F, Roldán A., 2010. An AM fungus and a PGPR intensify the adverse

671

effects of salinity on the stability of rhizosphere soil aggregates of Lactuca sativa.

672

Soil Biol. Biochem. 42, 429-434.

673 674

Kumar A, Verma JP., 2018. Does plant-microbe interaction confer stress tolerance in plants: a review? Microbiol. Res. 207, 41-52.

675

Lewis S., Kelly M., 2014. Mapping the potential for biofuel production on marginal lands:

676

differences in definitions, data and models across scales. ISPRS Internat. J. Geo-

677

Information 3, 430-59.

678

Li HB, Singh RK, Singh P, et al., 2017. Genetic diversity of nitrogen-fixing and plant growth

679

promoting Pseudomonas species isolated from sugarcane rhizosphere. Front.

680

Microbiol. 8, 1268.

30

681

Li K, Pidatala VR, Shaik R, Datta R, Ramakrishna W., 2014. Integrated metabolomic and

682

proteomic approaches dissect the effect of metal-resistant bacteria on maize biomass

683

and copper uptake. Environ. Sci. Technol. 48, 1184-1193.

684

Li K, Ramakrishna W., 2011. Effect of multiple metal resistant bacteria from contaminated

685

lake sediments on metal accumulation and plant growth. J. Hazard. Mat. 189, 531-

686

539.

687

Li Y, Pang H-D, He L-Y, Wang Q, Sheng X.-F., 2017. Cd immobilization and reduced tissue

688

Cd accumulation of rice (Oryza sativa wuyun-23) in the presence of heavy metal-

689

resistant bacteria. Ecotoxicol. Environ. Safety 138, 56-63.

690 691

Ma Y, Rajkumar M, Zhang C, Freitas H., 2016. Beneficial role of bacterial endophytes in heavy metal phytoremediation. J. Environ. Management 174, 14-25.

692

Mandal A., 2016. Mapping and characterization of salt-affected and waterlogged soils in the

693

Gangetic plain of central Haryana (India) for reclamation and management. Cogent

694

Geosci. 2, 1213689.

695

Mehmood M.A., Ibrahim M., Rashid U., Nawaz M., Ali S., Hussain A., Gull M., 2017.

696

Biomass production for bioenergy using marginal lands. Sustainable Production

697

Consumption 9, 3-21.

698

Mellado-Vázquez PG, Lange M, Gleixner G., 2019. Soil microbial communities and their

699

carbon assimilation are affected by soil properties and season but not by plants

700

differing in their photosynthetic pathways (C3 vs. C4). Biogeochem. 142, 175-187.

701

Mishra J, Fatima T, Kumar N., 2018. Role of secondary metabolites from plant growth-

702

promoting rhizobacteria in combating salinity stress. In: Egamberdieva D, Ahmad P

703

(Eds.), Plant Microbiome: Stress Response. Microorganisms for Sustainability, 5,

704

127-163.

31

705 706

Munns R, Tester M., 2008. Mechanisms of salinity tolerance. Annu. Rev. Plant Biol. 59, 651681.

707

Nadeem SM, Ahmad M, Zahir ZA, Javaid A, Ashraf M., 2014. The role of mycorrhizae and

708

plant growth promoting rhizobacteria (PGPR) in improving crop productivity under

709

stressful environments. Biotechnol. Adv. 32, 429-448.

710

Nadeem S.M., Zahir Z.A., Naveed M., Asghar H.N., Arshad M., 2010. Rhizobacteria capable

711

of producing ACC-deaminase may mitigate salt stress in wheat. Soil Biol. Biochem.

712

74, 533-542.

713

Naseem H, Ahsan M, Shahid MA, Khan N., 2018. Exopolysaccharides producing

714

rhizobacteria and their role in plant growth and drought tolerance. J. Basic Microbiol.

715

58, 1009-1022.

716 717

Naylor D, Coleman-Derr D., 2018. Drought stress and root-associated bacterial communities. Front. Plant Sci. 8, 2223.

718

Nia SH, Zarea MJ, Rejali F, Varma A., 2012. Yield and yield components of wheat as

719

affected by salinity and inoculation with Azospirillum strains from saline or non-

720

saline soil. J. Saudi Soc. Agric. Sci. 11, 113-121.

721

Nie M, Bell C, Wallenstein MD, Pendall E., 2015. Increased plant productivity and decreased

722

microbial respiratory C loss by plant growth-promoting rhizobacteria under elevated

723

CO2. Sci. Rep. 5, 9212.

724

Nosheen A, Naz R, Tahir AT, Yasmin H, Keyani R, Mitrevski B, Bano A, Chin ST, Marriott

725

PJ, Hussain I., 2018. Improvement of safflower oil quality for biodiesel production by

726

integrated application of PGPR under reduced amount of NP fertilizers. PloS One 13,

727

e0201738.

728 729

Ojuederie OB, Babalola OO., 2017. Microbial and plant-assisted bioremediation of heavy metal polluted environments: A review. Intl. J. Environ. Res. Public Health 14, 1504.

32

730

Padda KP, Puri A, Chanway CP.. 2017. Paenibacillus polymyxa: A prominent biofertilizer

731

and biocontrol agent for sustainable agriculture. In: Agriculturally Important

732

Microbes for Sustainable Agriculture pp. 165-191. Springer.

733

Panagos P., Van Liedekerke M., Yigini Y., Montanarella L., 2013. Contaminated sites in

734

Europe: review of the current situation based on data collected through a European

735

network. J. Environ. Public Health 2013, 158764.

736

Pandey G, Yadav CB, Sahu PP, Muthamilarasan M, Prasad M., 2017. Salinity induced

737

differential methylation patterns in contrasting cultivars of foxtail millet (Setaria

738

italica L.). Plant Cell Rep. 36, 759-772.

739

Paul D, Nair D., 2008. Stress adaptations in a Plant Growth Promoting Rhizobacterium

740

(PGPR) with increasing salinity in the coastal agricultural soils. J. Basic Microbiol.

741

48, 378-384.

742

Pérez JAM, García-Ribera R, Quesada T, Aguilera M, Ramos-Cormenzana A, Monteoliva-

743

Sánchez M., 2008. Biosorption of heavy metals by the exopolysaccharide produced

744

by Paenibacillus jamilae. World J. Microbiol. Biotechnol. 24, 2699.

745

Peuke AD, Rennenberg H., 2005. Phytoremediation: molecular biology, requirements for

746

application, environmental protection, public attention and feasibility. EMBO Rep. 6,

747

497-501.

748

Pidatala VR, Li K, Sarkar D, Wusirika R, Datta R., 2018. Comparative metabolic profiling of

749

vetiver (Chrysopogon zizanioides) and maize (Zea mays) under lead stress.

750

Chemosphere 193, 903e911.

751

Platten JD, Cotsaftis O, Berthomieu P, Bohnert H, Davenport RJ, Fairbairn DJ, Horie T,

752

Leigh RA, Lin H-X, Luan S., 2006. Nomenclature for HKT transporters, key

753

determinants of plant salinity tolerance. Trends Plant Sci. 11, 372-374.

33

754

Ramos-Ibarra JR, Rubio-Ramírez TE, Mondragón-Cortez P, Torres-Velázquez JR, Choix FJ.,

755

2019.

756

accumulation of cell compounds in Chlorella vulgaris and Tetradesmus obliquus

757

cultured under nitrogen stress. J. Appl. Phycol. https://doi.org/10.1007/s10811-019-

758

01862-1.

759 760

Azospirillum

brasilense-microalga

interaction

increases

growth

and

Schlesinger, WH., Bernhardt ES., 2013. Biogeochemistry: an analysis of global change. Third Edition. Academic press.

761

Qadir M, Quillérou E, Nangia V, Murtaza G, Singh M, Thomas RJ, Drechsel P, Noble AD.,

762

2014. Economics of salt‐induced land degradation and restoration. In: Natural

763

Resources Forum, pp. 282-295. Wiley Online Library.

764

Quinn JC and Davis R., 2015. The potentials and challenges of algae based biofuels: A

765

review of the techno-economic, life cycle, and resource assessment modeling.

766

Bioresource Technol. 184, 444-452.

767 768 769 770

Rajkumar M, Ae N, Prasad MNV, Freitas H., 2010. Potential of siderophore-producing bacteria for improving heavy metal phytoextraction. Trends Biotechnol. 28, 142-149. Rajkumar M, Sandhya S, Prasad M, Freitas H., 2012. Perspectives of plant-associated microbes in heavy metal phytoremediation. Biotechnol. Adv. 30, 1562-1574.

771

Rana A, Joshi M, Prasanna R, Shivay YS, Nain L., 2012. Biofortification of wheat through

772

inoculation of plant growth promoting rhizobacteria and cyanobacteria. European J.

773

Soil Biol. 50, 118-126.

774

Ricardo D., 1817. On the principles of political economy and taxation. Piero Sraffa (Ed.)

775

Works and Correspondence of David Ricardo, Volume I, Cambridge University

776

Press, 1951.

777 778

Rodríguez-Navarro A, Rubio F., 2006. High-affinity potassium and sodium transport systems in plants. J. Exp. Bot. 57, 1149-1160.

34

779

Salomon MV, Bottini R, de Souza Filho GA, Cohen AC, Moreno D, Gil M, Piccoli P., 2014.

780

Bacteria isolated from roots and rhizosphere of Vitis vinifera retard water losses,

781

induce abscisic acid accumulation and synthesis of defense‐related terpenes in in vitro

782

cultured grapevine. Physiologia Plantarum 151, 359-374.

783

Salomon MV, Pinter IF, Piccoli P, Bottini R., 2017. Use of plant growth-promoting

784

rhizobacteria as biocontrol agents: Induced systemic resistance against biotic stress in

785

plants. In: Microbial Applications 2, pp. 133-152. Springer.

786 787 788 789 790 791 792 793 794 795

Sen S, Chandrasekhar C., 2014. Effect of PGPR on growth promotion of rice (Oryza sativa L.) under salt stress. Asian J. Plant Sci. Res. 4, 62-67. Shahid SA, Al-Shankiti A., 2013. Sustainable food production in marginal lands—Case of GDLA member countries. Intl. Soil Water Conservation Res. 1, 24-38. Shi H, Zhu J-K., 2002. Regulation of expression of the vacuolar Na+/H+ antiporter gene AtNHX1 by salt stress and abscisic acid. Plant Mol. Biol. 50, 543-550. Shifaw E., 2018. Review of heavy metals pollution in China in agricultural and urban soils. J. Health Pollut. 8, 180607. Shinozaki K, Yamaguchi-Shinozaki K., 2007. Gene networks involved in drought stress response and tolerance. J. Exp. Bot. 58, 221-227.

796

Shrivastava P, Kumar R., 2015. Soil salinity: a serious environmental issue and plant growth

797

promoting bacteria as one of the tools for its alleviation. Saudi J. Biol. Sci. 22, 123-

798

131.

799

Siddikee MA, Chauhan P, Anandham R, Han G-H, Sa T., 2010. Isolation, characterization,

800

and use for plant growth promotion under salt stress, of ACC deaminase-producing

801

halotolerant bacteria derived from coastal soil. J. Microbiol. Biotechnol. 20, 1577-

802

1584.

35

803

Singh G, Bundela D, Sethi M, Lal K, Kamra S., 2010a. Remote sensing and geographic

804

information system for appraisal of salt-affected soils in India. J. Environ Quality 39,

805

5-15.

806

Singh H., Anderson B., Brune W., Cai C., Cohen R., Crawford J., Cubison M., Czech E.,

807

Emmons L., Fuelberg H., 2010b. Pollution influences on atmospheric composition

808

and chemistry at high northern latitudes: Boreal and California forest fire emissions.

809

Atmospheric Environ. 44, 4553-4564.

810 811

Singh G., 2018. Climate change and sustainable management of salinity in agriculture. Res. Med. Eng. Sci. 6, 1-7.

812

Sofi, JA, Lone AH, Ganie MA, Dar NA, Bhat SA, et al., 2016. Soil microbiological activity

813

and carbon dynamics in the current climate change scenarios: A review. Pedosphere

814

26, 577–591.

815

Srivastava S, Singh N., 2014. Mitigation approach of arsenic toxicity in chickpea grown in

816

arsenic amended soil with arsenic tolerant plant growth promoting Acinetobacter sp.

817

Ecol. Eng. 70, 146-153.

818

Taghavi S, Garafola C, Monchy S, Newman L, Hoffman A, Weyens N, Barac T,

819

Vangronsveld J, van der Lelie D., 2009. Genome survey and characterization of

820

endophytic bacteria exhibiting a beneficial effect on growth and development of

821

poplar trees. Appl. Environ. Microbiol. 75, 748-757.

822 823

Takahashi G., 2016. Damage and heavy metal pollution in China's farmland: Reality and solutions. J. Contemporary East Asia Studies 5, 11-25.

824

Teng Y, Ni S, Wang J, Zuo R, Yang J., 2010. A geochemical survey of trace elements in

825

agricultural and non-agricultural topsoil in Dexing area, China. J. Geochem.

826

Exploration 104, 118-127.

36

827 828

Tilman D, Hill J, Lehman C., 2006. Carbon-negative biofuels from low-input high-diversity grassland biomass. Science 314, 1598-1600.

829

Tiwari S, Lata C, Chauhan PS, Nautiyal CS., 2016. Pseudomonas putida attunes

830

morphophysiological, biochemical and molecular responses in Cicer arietinum L.

831

during drought stress and recovery. Plant Physiol. Biochem. 99, 108-117.

832

Ullah A, Heng S, Munis MFH, Fahad S, Yang X., 2015. Phytoremediation of heavy metals

833

assisted by plant growth promoting (PGP) bacteria: a review. Environ. Exp. Bot. 117,

834

28-40.

835

Umara B, Abdullahi A, Dibal J, Ahmad D., 2013. Effects of salts concentration on emergence

836

and growth of tomato (Lycopersicon esculentum) in tropical areas. lntl. J. Eng. Innov.

837

Technol. (UEIT) 3, 288-291.

838 839

Vejan P, Abdullah R, Khadiran T, Ismail S, Nasrulhaq Boyce A., 2016. Role of plant growth promoting rhizobacteria in agricultural sustainability—a review. Molecules 21, 573.

840

Wu CH, Wood TK, Mulchandani A, Chen W., 2006. Engineering plant-microbe symbiosis

841

for rhizoremediation of heavy metals. Appl. Environ. Microbiol. 72, 1129-1134.

842

Wu CH, Bernard SM, Andersen GL, Chen W., 2009. Developing microbe–plant interactions

843

for applications in plant-growth promotion and disease control, production of useful

844

compounds, remediation and carbon sequestration. Microbial Biotechnol. 2, 428–440.

845 846 847

Xiong L, Schumaker KS, Zhu JK., 2002. Cell signaling during cold, drought, and salt stress. Plant Cell 14, S165-1283. Xue G, Xishu Z, Lauren H, Mengting Y, Jiajie F, Daliang N, et al., 2018. Taxonomic and

848

responses of soil microbial communities to annual removal of aboveground plant

849

biomass. Front. Microbiol. 9, 954.

37

850

Yadav R, Ramakrishna W., 2019. Nutrient enhancement and growth promotion of wheat

851

cultivars by native plant growth promoting bacteria from Punjab state, India. J.

852

Pharmacognosy Phytochem. 8, 2938-2943.

853

Zhu J-K., 2016. Abiotic stress signaling and responses in plants. Cell 167, 313-324.

854

Zörb C, Geilfus C-M, Mühling KH, Ludwig-Müller J., 2013. The influence of salt stress on

855

ABA and auxin concentrations in two maize cultivars differing in salt resistance. J.

856

Plant Physiol. 170, 220-224.

857 858

Conflict of Interest

859

The authors declare that there are no conflicts of interest.

860

861 862

Communicating author (on behalf of all authors)

863 864 865 866 867 868 869 870

Dr. Ramakrishna Wusirika Professor Department of Biochemistry and Microbial Sciences Dean, School of Global Relations Central University of Punjab, Bathinda, India Email – [email protected]; [email protected]

871 872 873

Table 1. Distribution of marginal land in India Marginal land States Area covered by used for marginal land biofuel crops Andhra Pradesh 3,680,000 73,985 Arunachal Pradesh 578,000 309 Assam 757,000 3916 Bihar 379,000 9660

% Marginal land used for biofuel crops 2.01 0.05 0.52 2.55 38

874 875 876

Chhattisgarh 1,139,000 Delhi 7000 Dadra Nagar Haveli 5223 Gujarat 1,975,000 Haryana 209,000 Himachal Pradesh 746,000 Jammu and Kashmir 5,216,000 Jharkhand 1,083,000 Karnataka 1,294,000 Kerala 244,000 Madhya Pradesh 3,866,000 Maharashtra 3,726,000 Manipur 565,000 Meghalaya 413,000 Mizoram 496,000 Nagaland 527,000 Orissa 1,559,000 Punjab 74,000 Rajasthan 8,329,000 Sikkim 44,000 Tamil Nadu 848,000 Tripura 96,000 Uttarakhand 378,000 Uttar Pradesh 782,000 West Bengal 189,000 Total 39,204,223 Adapted from Edrisi and Abhilash, 2016

3,28,497 3501 575 46,366 14,547 2,187 226 14,726 48,953 18,239 4,44,833 69,805 1,137 1,012 380 490 20,197 13,492 75,174 204 1,02,813 594 17,378 90,604 41,764 14,45,564

28.84 50.01 11.01 2.35 6.96 0.29 0 1.36 3.78 7.48 11.51 1.87 0.20 0.25 0.08 0.09 1.30 18.23 0.90 0.46 12.12 0.62 4.60 11.59 22.10 3.69

877

39

878 879

Highlights

880 881 882 883

   

Marginal soil is an untapped resource which can be exploited using plants and bacteria Some PGPB enhance abiotic stress (drought, salinity and heavy metals) tolerance Molecular approaches employed by plant-soil-PGPB interactions crucial for the success Efficient utilization of marginal soil will enhance crop productivity and soil remediation

884

40