Phytoremediation: A Novel Approach of Bast Fiber Plants 1

(Hemp, Kenaf, Jute and Flax) for Heavy Metals Decontamina- 2

tion in Soil – Review 3

Nur Zaida Zahari 1,2*, Pavitra A/P Murugayah1, Fera Nony Cleophas1,2, Sahibin Abd Rahim1 and Ahmad Norazhar 4
Mohd Yatim1 5

1 Environmental Science Programme, Faculty of Science & Natural Resources, Universiti Malay- 6
sia Sabah, UMS Road, 88400 Kota Kinabalu, Sabah Malaysia. 7
2 Small Islands Research Center, Universiti Malaysia Sabah, UMS Road, 88400, Kota Kinabalu, 8
Sabah, Malaysia 9
* Correspondence: zaidazahari@ums.edu.my ; Tel.: +60138988754; (N.Z.Z) 10
11
Abstract: Heavy metal pollution in the environment is a major concern for humans as it is non- 12
biodegradable and can bring a lot of effects on the environment, humans as well as plants. At 13
present, a solution to this problem is suggested in terms of a new innovative eco-friendly technology 14
known as phytoremediation. The use of bast fiber plants collected from the bast surrounding are 15
known as non-edible crops with a short life cycle. This plant composed of cellulose and hemicellu- 16
lose with a mixture of lignin or pectinis makes it a significant crop for many industrial sectors. Due 17
to its low maintenance requirements with minimum economic investment, bast fiber plants have 18
Citation: Zahari, N. Z..; Murugayah, been widely used in phytoremediation. Nevertheless, these plants have the ability to extract metals 19
P.; Cleophas, F.N.; Rahim, S.A.; from the soil through their deep roots, combined with their commercial prospects, making them an 20
Yatim, A.N.M. Phytoremediation: ideal candidate as a profit-yielding crop for phytoremediation purposes. Therefore, a 21
A Novel Approach of Bast Fiber
comprehensive review is needed for a better understanding of the morphology and 22
Plants (Hemp, Kenaf, Jute and Flax)
phytoremediation mechanism of four commonly bast fiber plants which are hemp (Cannabis sativa), 23
for Heavy Metals Decontamination
kenaf (Hibiscus cannabinus), jute (Corchorus olitorius) and flax (Linum usitatissimum). This review ar- 24
in Soil – Review. Toxics 2022, 10, x.
ticle summarizes existing research on the phytoremediation potential of these plants grown in dif- 25
https://doi.org/10.3390/xxxxx
ferent toxic pollutants such as Lead (Pb), Cadmium (Cd), and Zinc (Zn). This work also discusses 26
Academic Editor: Firstname Last- several aids including natural and chemical amendments to improve phytoremediation. The role of 27
name
these amendments in the bioavailability of contaminants, their uptake, translocation, and bioaccu- 28
Received: date mulation, as well as their effect on plant growth and development, has been highlighted in this 29
Accepted: date paper. This paper helps in identifying, comparing, and addressing the recent achievements of bast 30
Published: date fiber plants for the phytoremediation of heavy metals in contaminated soil. 31

Publisher’s Note: MDPI stays neu-

tral with regard to jurisdictional
Keywords: phytoremediation; bast fiber plants; heavy metals; hemp; kenaf; jute; flax; soil 32

claims in published maps and institu- 33

tional affiliations.

1. Introduction 34

Copyright: © 2022 by the authors.

Submitted for possible open access
publication under the terms and
conditions of the Creative Commons
Attribution (CC BY) license
(https://creativecommons.org/li-
censes/by/4.0/).
Industrialization is a rapid growth in manufacturing, production, and technological 35
changes. This growth is required for better productivity, an increase in the standard of 36
living, growth in population, urbanization, and more. This rising in urbanization is also 37
expected to go up to 60% by 2030. However, this transformation caused a drastic change 38
in Earth’s ecosystem, negatively impacting the environment with air pollution, topsoil 39
contamination, groundwater contamination, and water pollution. Industrial wastes are 40
more toxic compared to municipal wastes due to the presence of oil, grease, heavy metals, 41
phenols, ammonia, and more. Emissions from mining, power plants, and refineries are 42
one of the major sources of hazardous toxic chemicals that pollutes the environment. 43

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Toxics 2022, 10, x FOR PEER REVIEW 2 of 19

Soil pollution is characterized as the accumulation of persistent toxic compounds, 44

chemicals, salts, radioactive materials, or disease-causing agents, which adversely affect 45
plant growth and animal health, in soils. This pollution decreases the quality of the crop 46
as the effect of the usage of pesticides and chemical fertilizers. Exposure to toxic and dan- 47
gerous chemicals would increase the health risks to people living nearby and on polluted 48
land. For example, heavy metals can enter humans' bodies through food, water, air, and 49
bioaccumulation over a period of time [1]. This will lead to acute and chronic illness in the 50
central nervous system and peripheral nervous system [2]. Moreover, the toxic effects of 51
heavy metals can cause an imbalance in the ecosystem of the soil. Heavy metals in soils 52
exist in four different forms:, dissolved ions, organic complexes, exchangeable ions, and 53
precipitates [3]. This metal cannot be detected by color and smell, and it is not dangerous 54
on a low level in the environment. Metals such as zinc (Zn), nickel (Ni), manganese (Mn), 55
iron (Fe), and copper (Cu) do contribute their importance in plant growth and help phys- 56
iological processes such as the electron transfer system in photosynthesis. Other metals 57
such as cadmium (Cd), arsenic (As), chromium (Cr), mercury (Hg), and lead (Pb) do not 58
carry any known biological roles in plants. However, an excessive amount of heavy metal 59
will affect the biological and biochemical processes negatively by restraining the growth 60
and lowering the chlorophyll content of the plants. It destructs the cell membrane and 61
damages different types of biomolecules by producing reactive oxygen species (ROS) on 62
a certain level in the environment [4]. 63

Heavy metal contamination in soil has a negative impact on the environment espe- 64
cially on soil quality and plant growth. Once the plant is saturated with heavy metal, the 65
plant dies due to the interruption in photosynthesis and protein synthesis. Elimination of 66
heavy metals is difficult as it is irreversible, and remediation needs to be done. Remedia- 67
tion can be divided into in-situ and ex-situ remediation. In-situ remediation is a process 68
of remediation that doesn’t require transport of contaminated soil to off-site treatment 69
facilities. Ex-situ remediation, on the other hand, is the remediation technique that re- 70
quires excavation of contaminated soil to an off-site treatment facility [3]. This process 71
requires additional costs. However, the treatments are controlled and accelerated and pro- 72
vide better results in a shorter time. Examples of in-situ remediation are surface capping, 73
encapsulation, electro-kinetics, soil flushing, immobilization, phytoremediation, and bio- 74
remediation. Examples of ex-situ remediation techniques are landfilling, soil washing, so- 75
lidification, and vitrification [3]. 76

Phytoremediation is a cost-effective remediation technique with ecological benefits 77

and high public acceptance. This method is scientifically proven for the remediation of 78
contaminants with the only limitations are time-consuming process and possess the possi- 79
bility of adverse effects on living beings due to biomagnification. This limitation can be 80
overcome using non-edible commercial plants that have rapid growth rates and are easy 81
to be maintained. With these characteristics, a bast fiber plant with various plant parts is a 82
good option for phytoremediation. They are also used in the production of a variety of 83
products, such as paper, textiles, wrapping materials, rope, strings, baskets, and so on, 84
which will improve the socioeconomic status of people who live in contaminated areas or 85
who have contaminated lands for agricultural purposes. Bast fibre, also known as phloem 86
fibre, is a type of plant fibre derived from the phloem or bast that surrounds the stem of 87
certain dicotyledonous plants. Bast fibres plants can be obtained from either cultivated 88
herbs like flax, hemp, and ramie or from wild plants like linden, wisteria, and mulberry. 89
There are several characteristics that need to be considered before using bast fibres plants 90
for phytoremediation. Firstly, the ability of these plants to take up contaminants from soil 91
and accumulate them in their cells. Second, the resistance of these plants against the 92
Toxics 2022, 10, x FOR PEER REVIEW 3 of 19

toxicity of the contaminants. Third, the roots, the rate of growth, the plant biomass, the 93
adaptation to the climate, and the tolerance to salty soil [5]. Among all these aspects, the 94
main production of high biomass in parts of plants will affect more on the phytoremedia- 95
tion capacity [6]. 96

It is also crucial to understand that edible plants are not appropriate for phytoreme- 97
diation because they may affect the health of humans or animals once it is consumed[7]. 98
Therefore, fiber crops are said to be the best fit for phytoremediation. This is because fiber 99
plants involve a cycle of planting and harvesting, which will help to reduce the heavy 100
metal contamination in the soil over time, and the harvested fiber is used to manufacture 101
biomaterials such as paper and textiles. In this case, it does not enter the food chain and 102
affects the environment negatively, such as harming human or animal health. Apart from 103
that, different plants have different methods for the removal and accumulation of heavy 104
metals. For example, some plants can stabilize or decrease the mobility of the pollutants 105
in the soil through accumulation by roots through root hairs to stop contaminants' run- 106
off, bulk erosion, and air-borne transport [8]. Other plants may be involved in the process 107
of the plant uptake and release to the atmosphere through transpiration which is known 108
as phytovolatilization. Many phytoremediation processes are possible through better re- 109
lationships in between plants, microbes, soil, and contaminants. These different processes 110
of phytoremediation perform different management options for a better end product to 111
the environment [6]. 112

This paper discusses the potential of four commonly used bast fiber plants namely 113
Cannabis sativa (Hemp), Hibiscus cannabinus (Kenaf), Corchorus olitorius (Jute) and Linum 114
usitatissimum (Flax) for phytoremediation of selective heavy metals cadmium (Cd), lead 115
(Pb) and zinc (Zn) from contaminated soil. The main goal of this paper is to provide ref- 116
erences for suitable bast fiber plants for heavy metal treatment . In addition, this review 117
summarises these plants' ability to accumulate heavy metal elements and reveals their 118
potential for use as phyotoaccumulators or phytostabilizers via their uptake mechanisms.. 119
This emerging technology can be improved with natural and chemical amendments that 120
make heavy metals bioavailable and soluble. 121
122
123
Phytovolatilization – vo- 124
latilization of metals into 125
Phytoextraction – uptake of metals
the atmosphere 126
from plant root to the above part tis-
sues 127
128
129
130
131
132
133
134
Rhizodegradation – degradation of
organic pollutants in the root zone 135
Phytostabilization – reduction of bi-
oavailability of metals in root 136
137
138
139
140
141
Figure 1. Mechanisms involved in the phytoremediation process. 142
Toxics 2022, 10, x FOR PEER REVIEW 4 of 19

2. Bast Fiber Plants 143

2.1 Morphology and Characteristics of Bast Fiber Plants (Hemp, Kenaf, Jute and Flax) 144

Bast fibre is a natural fibre derived from the bast environment of certain dicotyle- 145
donous angiosperm plant stems. It is made up of cellulose and hemicellulose combined 146
with a lignin or pectin mixture. In this paper, the potential of four different fiber plants 147
from various places in the uptake of heavy metals from contaminated soil was high- 148
lighted. The four fiber plants are Hemp (Cannabis sativa), Kenaf (Hibiscus cannabinus), Jute 149
(Corchorus olitorius), and Flax (Linum usitatissimum). 150
151
Hemp is a member of the Cannabaceae plant family, and the fibre derived from this 152
plant is one of the strongest forms of natural fibre [9]. It has the potential to be an envi- 153
ronmentally friendly and highly sustainable crop if it is well managed. On the other hand, 154
Kenaf and Jute comes from the same family of Malvacea. Kenaf is one of the non-wood 155
fibers that can be used for reinforcement and it is the world’s third traditional crop after 156
wood and bamboo which originated from Asia and Africa [10]. Jute fibers are totally bio- 157
degradable as it is partially wood [11]. Flax is a member of the Linaceae family of plants, 158
and due to its exceptional qualities, flax fibres are significant raw material for textiles [11]. 159
The Flax and Hemp do not have much difference because they are both cellulose fibers 160
except that Hemp has ten chromosomes (2n = 20) while Flax has 15 pairs of chromosomes 161
(2n = 30) [12] wheareas, Kenaf and Jute are woody-stemmed herbaceous dicotyledons 162
grown in the tropics and subtropics. 163
164
165
166
167
168
169
170
 171
172
Table 2. Morphology and specifics characteristics of bast fiber plants (Hemp, Kenaf, Jute and Flax) 173
174
Fiber Plants Morphology 175
Roots Stems Leaves Flowers Seeds Reference 176
177
Hemp Root system is The stems are nor- The first true leaves are Male flowers and female Hemp seeds are [13] 178
(Cannabis sa- well developed mally hollow with di- single leaflets, later flowers available. Female achenes seeds. Seeds in 179
tiva) with depth of ameter ranging from leaves become palmately flowers are more com- ellipsoid shape, 2 to 7 180
about 1 to 1.5m 5 to 25 mm. The base compound. The second pact. mm long and 2 to 4 mm 181
and top stem has dif- leaf pair consist of three wide in diameter. Seeds 182
ferent diameters. Ma- leaflets per leaf, the third vary in colour from
183
ture plant reaches up leaf pair has five leaflets light brown to dark
184
to 5 m. per leaf, and so on, up to green
185
eleven leaflets per leaf.
186
187
188
189
Kenaf It has a prolific It mainly has un- Young leaves are simple It produces large showy, The seeds are normally [14] 190
(Hibiscus can- root system with a branched stems and and entire. Divided leaf light yellow, creamy col- brown with 6 mm long 191
nabinus) long taproot and grows up to 4.5 m tall can produce 3 to 10 entire oured flowers that are and 4 mm wide. The 192
extensive lateral young leaves prior to the bell-shaped and widely seeds of Kenaf are pro- 193
roots. first divided leaf open. The flowers duced by the fruits, 194
are solitary, short-stalked known as fruit capsules 195
and auxiliary which are 8 in 1.9 to 2.5 cm long and 196
to 13 cm in diameter with 1.3 and 1.9 cm in diame- 197
5 petals, 5 sepals, and ter with many seeded 198
numerous stamens. around 20 to 26 seeds.
199
200
201
202
203
204

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Toxics 2022, 10, x FOR PEER REVIEW 2 of 19

Table 2. Specifics characteristics of bast fiber plants (Hemp, Kenaf, Jute and Flax) 205
206
Fiber Plants Morphology 207
Roots Stems Leaves Flowers Seeds Reference 208
[15] 209
Jute It has extensive The height range of The leaves are edible It consists of small pale- Seeds are greyish black, 210
(Corchorus lateral branching the jute plant is be- with a bitter taste. Leaves yellow flower, bracts angled. 211
olitorius) and deep tap root tween 2 and 4 m. The are usually 6-10 cm long lanceolate; 2 to 3 cm 212
system. stems are about 1 to 2 and 3.5-5 cm broad. wide, sepals 3 mm long, 213
cm in diameter with and petals are 5 mm 214
few branches. The long.
215
colour of the stem,
216
petiole and leaf var-
217
ies.
218
219
220
221
Flax It has short and It has one main stem, The leaves are normally The flowers parts are The seeds are flat, oval [16] 222
(Linum usitatis- branched tap root but two or more small and in lance normally in the units of and pointed at one end. 223
simum) which can extend branches (tillers) may shaped. five and they can range Normally the seeds are 224
to a depth, 1m develop from the base from a dark to a very covered mucilage giv- 225
with side when plant density is light blue, white or pale ing it a high shine 226
branches spread- low or high of soil ni- pink 227
ing to 30cm trogen levels. 228
229
230
231
232
233
 2.2 Application of Bast Fiber Plants (Hemp, Kenaf, Jute and Flax) 234

Fiber plants are useful not only for phytoremediation but also in a variety of other 235
fields. Bast fibre of hemp plants is used in the automotive industry and textile industry 236
while the whole plant part is used for feedstock and biofuel. Hurds are used for paper 237
production and as a building material such as fiberglass. Hemp oil from the seeds is used 238
in shampoo, soaps, and bathing gels. Seeds are also applicable in the food industry as 239
hemp milk and are used as a salad dressing. Technical commercial products such as oil 240
paints, ink, and coatings are also produced by these plants [17]. However, the usage of the 241
plants is based on the quality of the hemp. On the other hand, jute is the second most 242
important fiber plant in the world, and it is also one of the cheapest-grown fiber plants in 243
the tropical region. It is traditionally used to manufacture packaging materials such as 244
sacking, ropes, twines, and carpet backing cloth. Moreover, diversified jute is also used in 245
the production of home textiles, composites, geotextiles, paper pulp, technical textiles, 246
chemical products, handicrafts, and fashion accessories. The woody central core is used 247
as a rural building material, for fences, fuel, and for charcoal-making. In the Philippines, 248
the leaves of jute are used to treat headaches [18]. 249
250
Kenaf also has its own uses and one of them is the paper production . Kenaf paper is 251
stronger and more resistant to yellowing compared the wood paper and it requires less 252
bleaching agent. Furthermore, Kenaf seeds produce edible oil, which is one of the best 253
cooking oils. Dried Kenaf leaves are consumed as a vegetable in some countries because 254
it contains 30% of crude protein. The fruit of Kenaf helps in lowering blood pressure and 255
the presence of vitamin C and antioxidants in Kenaf help in fighting some diseases. Kenaf 256
will be used in new applications such as medicines, textiles, natural fiber compounds and 257
environmental cleaning [19]. Flax is used for fruit, medications and textiles and has there- 258
fore been used for food processing. It has been of considerable significance for human 259
civilization and growth for more than 8000 years. At the time, flax was commonly used 260
for the manufacture of fabrics, and now, oil is the main production[20]. 261
262
263
Table 1. World countries ranking of producing fibre plants. 264
265
Types of fi- Hemp
ber plants Kenaf (Hibiscus Jute (Corchorus Flax (Linum
(Cannabis sa-
cannabinus) olitorius) usitatissimum)
Ranking tiva)
1 China India India Russia
2 Canada China Bangladesh Canada
United Syaye
3 Thailand China Kazakhstan
of America
4 France Brazil Uzbekistan China
5 Chile Vietnam Nepal United States
6 North Korea Cuba South Sudan India
7 Indonesia Zimbabwe
8 Pakistan Egypt
9 Pakistan Vietnam
10 Cambodia Bhutan
References [21] [22] [23] [24]
266

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Toxics 2022, 10, x FOR PEER REVIEW 2 of 19

2.3 Case study on Phytoremediation of Heavy Metals Pb, Zn, and Ni by Bast Fiber Plants 267
In this study, Hemp (Cannabis sativa), Kenaf (Hibiscus cannabinus), Jute (Corchorus 268
olitorius), and Flax (Linum usitatissimum) were chosen to compare their potential for phy- 269
toremediation of Pb, Cd, and Zn in the soil. Hemp plants were harvested from agricultural 270
activities with acidic soil value. The concentrations of these metals were higher in the root 271
than in the leaves and shoots. Hemp can tolerate high concentrations of Zn and most of 272
the Zn absorbed is retained in the roots [25]. The uptakes of these heavy metals are signif- 273
icantly influenced by the pH of the soil. This statement is supported by the study caried 274
out by Gray et al., [26], where the results showed that increasing in pH will caused a sig- 275
nificant reduce in the concentration of cadmium in clover, lettuce, carrot and ryegrass. 276
277
Research conducted by Nizam et al., [27], highlighted that the concentration and up- 278
take of Pb by the shoot were significantly higher than the root in the Kenaf plant. Most of 279
the varieties grown in Pb contaminated soil accumulated more Pb in shoots than roots, 280
indicating that Pb was easily transported from root to shoot in Pb contaminated soil. This, 281
could be related to the Pb content and its relationship with other essential ions during 282
nutrient uptake. Other studied by Shehata et al.,[7], mentioned that Kenaf plants were ir- 283
rigated with wastewater and sulfur soil addiction with humic acid were used as foliar 284
spraying and it showed the significant highest accumulation of cadmium which 0.87 285
mg/kg in the roots and 0.36 mg/kg in the shoots. They noticed that humic acids are the 286
most active components in soil and compost as it improves the uptake and accumulation 287
of heavy metals in the tissues' plant [28]. Cecília et al., [29], studied the phytoremediation 288
of zinc and the results showed that Kenaf is able to take 233 mg/kg of zinc in the roots and 289
264 mg/kg in the shoots. 290
291
Furthermore, the studies about phytoremediation in untreated industrial 292
wastewater form textile factories by Ahmed & Slima [30], shows that there was very high 293
concentration of Cd in the roots with 261.83 mg/kg and 41.35 mg/kg in the shoots of the 294
Jute. In contrast the concentration of Pb in the roots was 367.83 mg/kg while in the shoots 295
was 370.43 mg/kg. This findings showed that the nutrients in the roots and shoots were 296
decreased significantly due to contamination stress. Lead (Pb) is a toxic heavy metal that 297
can inhibit plant growth, seedling development and root elongation [31]. They also state 298
that flax is a fibre plant that is suitable for growing in industrially polluted areas because 299
its root system removes significant amounts of heavy metals from the soil and can be used 300
as a potential crop for cleaning soil of heavy metals [32]. Hosman et al., [33], studied the 301
bioremediation potential of flax under different concentration of Pb, Cd and Zn. The aver- 302
age ability of the flax plant to remove heavy metals from soil was 49% for Cd, 68.6% for 303
Pb, and 71.76% for Zn. Following that, the highest accumulation of Cd was found in the 304
root, while the highest accumulation of Pb and Zn was found in the capsule. He also re- 305
ported that by increasing in metal concentration in the soil, there was a gradual increase 306
in metal uptake in flax plant. Several phytotoxicity effects was observed when these metals 307
are exceeded the endogenous level [34]. 308
309
310
311
312
313
314
315
316
317
318
319
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Table 2. Heavy metal concentration in Bast Fiber Plants. Listed tissues represent those 320
with the highest concentration of metals in roots, leaves, and shoots. 321
322

Types of Concentration (mg/kg-1)

fiber Metals Reference
plants Roots Leaves Shoots
Pb 38.2 16.5 23.5 [32]
Pb 14.6 2.22 2.07 [35]
Hemp
Cd 2.82 0.23 0.37 [35]
(Cannabis
Cd 1.03 0.55 0.98 [32]
sativa)
Zn 688.6 323.1 156 [35]
Zn 66.8 40.0 54.5 [32]
Pb 2.43 - 8.9 [29]
Pb 329.66 - 867.55 [36]
Kenaf Cd 0.87 - 0.36 [7]
(Hibiscus
Cd 0.25 - 0.14 [37]
cannabi-
nus) Zn 233.0 - 264.0 [29]
Zn 114 65 - [38]
Zn 377.78 133.33 - [39]
Pb 21.74 - - [40]
Jute Pb 367.83 370.43 - [41]
(Corcho-
Cd 163 - 48 [42]
rus olito-
rius) Cd 261.83 41.35 - [41]
Zn 148.53 151.42 - [41]
Pb 104.4 14.5 30.2 [32]
Flax Pb 310.56 - - [43]
(Linum Cd 13.06 - - [43]
usitatissi- Cd 8.69 1.62 7.27 [32]
mum) Zn 255.71 - - [43]
Zn 211.8 32.6 62.9 [32]
323
324
2.4 Enhancing Phytoremediation of Heavy Metals of Bast Fiber Plants by Chemical and Microbio- 325
logical Amendments 326
The phytoremediation potential of bast fiber plants can be increased by using chem- 327
ical amendments in the soil and microbial enhancement through inoculation in the roots 328
of plants. This increase the ability of metals and chelators to form complexes, the level of 329
plant resistance to metals, and escalate the translocation and accumulation of metals in- 330
side the plants, thereby improving the phytoremediation efficiency. Previous studies have 331
reported that various chelators are employed to increase the solubility of metals in soil, 332
including 1,2-cyclohexane-diaminetetraacetic acid (CDTA), ethylene glycol tetraacetic 333
acid (EGTA), and diethylene-triaminepentaacetic acid (DTPA) [44],[45][46] One of the 334
most effective chelating agents is ethylenediaminetetraacetic acid (EDTA) which can in- 335
crease the solubility, absorption, and complexation of metals (including Pb ions in soil) 336
[47],[48],[49],[50]. Furthermore, metal-EDTA complexes may form and function to signif- 337
icantly boost Pb ion absorption by plant roots and translocate them to shoots [51]. Hasan 338
et al., [52] reported that metallothioneins produced by certain genes could withstand con- 339
ditions where metal stress is present in the environment. Furthermore, this metal-binding 340
Toxics 2022, 10, x FOR PEER REVIEW 4 of 19

protein with low molecular weight can facilitate the metal ion into the plant cells and 341
translocate them via the xylem. In phytoremediation technologies, the addition of nutri- 342
ents to plants may results in healthy plant growth with the development of flowers, 343
leaves, and branching of the root system thus can increase the level of uptake contaminant 344
in the study area. However, an excessive amount of nutrients given to the plants can result 345
in a significant reduction in plant growth. This symptom is known as nutrient toxicity. In 346
a nutrient-enriched environment, the bioavailable fraction of metals may be reduced be- 347
cause of the binding to the nutrient anions. The uptake of heavy metals in plants may also 348
be affected by competition since nutrient cations compete with the metal for uptake sites 349
[53]. Thus, the uptake of the metal under investigation decreases with increasing concen- 350
tration of nutrients. However, a generous availability of nutrients promotes plant growth, 351
which in turn creates an increasing number of uptake sites for metal in plants. This may 352
increase the uptake as well as the metal concentrations in plants. 353
354
Interactions between plants and microbes are crucial factors in determining the effi- 355
ciency of phytoremediation [54]. These interactions are implicated to play an essential role 356
in plant metal uptake. The beneficial microbes associated with plants directly improve the 357
efficiency of the phytoremediation process by altering metal accumulation in plant tissues 358
and indirectly by promoting shoot and root biomass production. Whiting et al., [55], re- 359
ported that the biomass and zinc concentration in shoots of Thlaspi caerulescens has been 360
increased with the presence of rhizospheric bacteria. These bacteria can promote plant 361
growth by inhabiting the plant roots [56] and are known as plant growth-promoting rhi- 362
zobacteria (PGPR)[57]. The generation of phytohormones, specialized enzymatic activity, 363
nitrogen fixation in the atmosphere, and pathogen-depressing chemicals such sidephores 364
and chelating compounds all contribute to the role of PGPR in promoting plant 365
growth[58]. Sidephores and chelating compounds have been shown to promote plant 366
growth even in the presence of heavy metals [59]. 1- aminocyclopropane- carboxylic acid 367
deaminase is another plant growth-promoting compound that has been studied in rela- 368
tion to heavy metals (ACC deaminase). ACC is an intermediate of ethylene produced by 369
stressed plants, and bacteria that produce ACC deaminase can reduce ethylene levels in 370
plants, promoting plant growth [60]. 371
372
In another study, Belimov et al., [61] discovered that bacteria containing ACC deam- 373
inase can improve plant growth in metals polluted conditions. Whereas, Braud et al., [62], 374
studied the phytoextraction of agricultural Cr and Pb with sidephore- producing bacteria, 375
and highlighted that the inoculated Maize plant with the bacteria enhanced the bioavail- 376
ability and uptake of Cr and Pb. Khan et al., [63], investigated the (Ni) accumulation of 377
mycorrhizal and non-mycorrhizal flax plants at various concentrations of Ni, i.e., 0, 250, 378
350, and 500 ppm. He reported that the accumulation of metals was higher in mycorrhizal 379
than the non-mycorrhizal plants. Additionally, mycorrhizal plants showed noticeably 380
greater growth and development than non-mycorrhizal plants. The production of 381
phytohormones by Arbuscular Mycorrhizal Fungi (AMF) can improve nutrient and water 382
uptake as well as improves metal bioavailability and aid in the phytoremediation process 383
[64]. Figure 3 showed the mechanism of plant-microbe association that support metal phy- 384
toremediation. 385
386
387
388
389

390

391

392
Toxics 2022, 10, x FOR PEER REVIEW 5 of 19

393

394
Improved plant 395
growth and yield
396

397
Production of glu-
398
tathione-phyto-
chelatin mediated 399
resistance
PGPR 400
Metal transformation
401
Phytoprotection into soluble forms
via bacteria metal 402
resistance Sidephores
403
production
404
Improved root Metals tolerance from EPS 405
length and root (extracellular polymeric sub-
area stances) formation 406

407

408

Figure 3: The mechanism of plant-microbe association that support metals phytoremedia- 409

tion[65]. 410

411
412
2.5 Molecular Mechanisms Involved in Microbial Resistance to Heavy Metals 413
Microorganisms have been involved in the mechanisms of adapting with heavy metals 414
either in water or soil [66]. Some metals, such as copper, nickel, and cobalt, are given to micro- 415
organisms as micronutrients for use in redox processes, to stabilise molecules through electro- 416
static interactions, to act as components of various enzymes, and to regulate osmatic pressure. 417
Otherwise, non-essential metals are recognized to have little nutritional value and may be toxic 418
to microorganisms. To overcome the toxicity value, there are six metal mechanism that exists 419
in the microorganism includes the exclusion of permeability barrier, intra, and extra-cellular 420
sequestration, active transport efflux pumps, enzymatic detoxification, and reduction in the 421
sensitivity of cellular targets to metal ions. 422
423
2.5.1 Metal Exclusion by Permeability Barrier 424
The metal exclusion by the permeability barrier involved the changes in the cell wall, 425
membrane, or envelope of microorganisms. This mechanism is an attempt by the organism to 426
protect metal-sensitive and essential cellular components. Previous research has shown that 427
bacteria form an extracellular polysaccharide coating that has the ability to bio-absorb heavy 428
metal ions and prevent them from interacting with vital cellular components [67]. These 429
bacteria's exopolysaccharide coating may provide sites for metal cation attachment [67]. For 430
example, there are several strains of bacteria that demonstrated the ability to bind metals 431
extracellularly such as Klebsiella aerogenes, Pseudomonas putida, and Arthrobacter viscosus. 432
According to Scott & Palmer, [67] a protective layer of exopolysaccharide improves the survival 433
of K. aerogenes strains in Cd (II) solutions. When compared to strains without their protective 434
layer, these strains show a 2-fold increase in Cd (II) accumulation. This protective layer appears 435
to help reduce toxicity by preventing metal ion uptake and keeping metal ions away from 436
sensitive cellular components. 437
438
2.5.2 Active Transport of the Metals Away from the Microorganisms 439
One of the largest categories of metal resistance systems is an active transport or efflux 440
system by microorganisms. These methods involved the cytoplasmic export of harmful metals. 441
Toxics 2022, 10, x FOR PEER REVIEW 6 of 19

These processes may be plasmid- or chromosomal-encoded. Normally, nutrient transport 442

systems allow non-essential metals to enter the cell, but they are quickly expelled. These efflux 443
mechanisms are extremely selective for the cation or anion they export and can be either non- 444
ATPase or ATPase-linked [68]. Bacillus subtilis, S. aureus, and E. coli [69] are only a few of the 445
microorganisms that have shown resistance to Cd (II). The plasmid-encoded cad system in S. 446
aureus, as reported by Smith &Novick, [70] is the best-characterized Cd (II) resistance efflux. 447
Early research showed that there was two distinct plasmid-mediated Cd (II) resistance mecha- 448
nisms. The first has single cad loci (cadA) responsible for conferring resistance and the second 449
has two loci cadA and cadB [70]. cadA shares strong amino acid sequence homology with P- 450
class ATPase, which functions as an ion pump [71]. CadA proteins have six major domains that 451
work together to form a pump that removes Cd (II) from the cell's interior. An outer cytoplas- 452
mic metal binding region, a transmembrane domain, and a transduction 'funnel' that may move 453
bound Cd (II) to the membrane surface comprise the domain. 454
455
2.5.3 Intracellular and Extracellular Sequestration of Metals by Protein Binding 456
The accumulation of metals within the cytoplasm to avoid exposure to essential cellular 457
components is known as intracellular sequestration. Metals that are commonly sequestered 458
include Cd (II), Cu (II), and Zn (II). Otherwise, extracellular sequestration is the mechanism 459
involved in the secretion of large amounts of glutathione. The production of metallothionein 460
by Synechococcus sp. is one of the intracellular sequestration [72]. Two genes, smtA, and smtB, 461
make up Synechococcus sp metal .'s resistance system. A metallothionein that binds Cd (II) and 462
Zn is encoded by smtA. (II). High levels of Cd (II), Zn (II), and Cu (II) stimulate these genes, 463
which are then suppressed by the smtB gene product. The smtB protein functions as a 464
transacting transcriptional repressor, inhibiting the expression of smtA and the synthesis of 465
metallothionein.[73]. For extracellular sequestration inyeast, Murata et al., [74], reported that 466
Saccharomyces cerevisiae may reduce the absorption of Ni (II) by excreting a gluthathione. 467
Gluthathione binds with great affinity to heavy metals and carrying the methyglyoxal 468
resistance gene demonstrates the ability to form extracellular metal- gluthathione complexes in 469
metal rich media [74]. 470
471
2.5.4 Enzymatic Detoxification of Metals to a Less Toxic Form 472
Mercury resistance is a prime example of an enzymatic detoxifying system in bacteria. 473
Mercury is classified as a toxic metal because it binds to and inactivates essential thiols found 474
in enzymes and proteins. Microorganisms such as Gram-positive (S. aureus, Bacillus sp.) and 475
Gram-negative bacteria (E. coli, P. aeuruginosa and Thiobacillusf errooxidans) had shown to 476
demonstrate resistance to Hg (II) (mer) resistance operon. This operon not only transports and 477
self-regulates resistance, but it also detoxifies Hg (II)[75]. The same side of genes also encodes 478
the creation of a periplasmic binding protein and membrane-associated transport proteins. Hg 479
(II) in the immediate surroundings is gathered by the periplasmic binding protein and 480
transported to the cytoplasm by transport proteins for detoxification. 481
482
2.5.5 Reduction in Metals Sensitivity of Cellular Targets 483
Rouch et al., [76], demonstrated that some microorganisms can adapt to the presence of 484
hazardous metals by changing how sensitive some vital cellular components are, offering some 485
degree of natural defense. Protection is achieved either by boosting the production of a specific 486
cellular component to prevent a metal inactivation or by mutations that reduce sensitivity 487
without changing basic function. The microorganism may potentially defend itself by creating 488
metal-resistant parts or an alternative pathway to get around vulnerable parts. This adaptation 489
was discovered in E. Coli after exposure to Cd (II)[76]. Rouch et al., [76], highlighted that the 490
longer an organism is exposed to Cd, the shorter its growth at the lag phase is (II). The extended 491
lag phase is thought to be caused by a period of induction of DNA repair mechanisms. Natural 492
resistance can develop as a result of normal cellular functions that provide the organism with 493
a basic level of tolerance to heavy metals[76]. 494
495
Toxics 2022, 10, x FOR PEER REVIEW 7 of 19

3. Advantages and Limitations of Phytoremediation 496

As mentioned earlier, phytoremediation is a promising method for cleaning up heavy metal- 497
contaminated soils. Despite the numerous challenges, phytoremediation is regarded as a green 498
remediation technology with enormous potential. The main advantages of this method will be 499
cost effectiveness, eco-friendly and practicable compared to the other mediation technologies. 500
However, there is some limitation need to be addressed in this process. This includes huge funds 501
expenditure and human resources as well as favorable weather and climatic conditions for 502
plants. The advantages and limitations of phytoremediation are described detailed in Table 3. 503
504
Table 3. The advantages and limitations of the phytoremediation process. 505
506
Advantages Limitations Reference
It is cost-efficient It takes longer time to achieve the re- [77], [78]
sults as it is a slow process
Soil properties will not be The toxins, pH, and concentration of
affected during the process of contaminants must be below the
phytoremediation, as it is plant's tolerance level.
environmentally friendly
Applicable for large, contami- Cannot be carried out in a medium [79]
nated areas with excessive concentration of
contaminants suitable for shallow
contamination (within the rooting
zone) at non-excessive concentra-
tions
Helps to reduce the possibility Possibility of high toxic entering
of soil erosion and prevent the food chain in case of poor manage-
metals in the affected area from ment
leaching
Can be used for both in situ Only suitable for shallow contamina- [80]
and ex situ application tion which is until the depth of the
root
Have the potential to be a The remediated plant biomass could
permanent treatment in treat- be dangerous as it contains hazard-
ing a wide range of contami- ous wastes.
nants.
507
508
4. Summary 509
Global trends toward sustainable development have brought phytoremediation as one of the 510
emerging technologies for the decontamination of heavy metals in soil. Bast fiber plants are very 511
promising candidates since they show tolerance to toxic trace elements in soils, have fast-grow- 512
ing and yield high biomass, have low maintenance, and are well known in the industrial sector. 513
Based on the heavy metal content results in the fiber crops studied, the following conclusions 514
can be drawn: 515
516
1. Heavy metal accumulation in bast fiber plants is clearly showed in vegetative and repro- 517
ductive organs. Hemp (Cannabis sativa) is the crop that most strongly accumulates Zn fol- 518
lowed by Kenaf (Hibiscus cannabinus), Jute (Corchorus olitorius), and Flax (Linum usitatissi- 519
mum). It is notable that Jute is more tolerant and best uptake potential for Cd as compared 520
to others crops. 521
2. It is reported that the distribution of heavy metals Pb, Zn, and Cd is selective to roots as 522
compared to shoot for all bast fiber plants studied. 523
Toxics 2022, 10, x FOR PEER REVIEW 8 of 19

3. It is suggested that Hemp, Kenaf, and Jute are suitable species for soil remediating of heavy 524
metals Pb and Zn. Therefore, these species can be successfully cultivated for phytoremedia- 525
tion purposes since their root system can remove significant amounts of heavy metals from 526
the soil. 527
528
529
Author Contributions: Conceptualization, N.Z.Z and P.M.; data curation, N.Z.Z and P.M.; 530
methodology, N.Z.Z, and F.N.C.; validation, S.A.R and N.Z.Z.; writing—original draft prepara- 531
tion, N.Z.Z and P.M.; writing—review and editing, N.Z.Z and A.N.M.Y.; supervision, N.Z.Z and 532
S.A.R; funding acquisition, N.Z.Z and F.N.C. All authors have read and agreed to the published 533
version of the manuscript. 534
535
Funding: This work was supported by the Project No. (SDN0063) the Centre for Research and 536
Innovation, Universiti Malaysia Sabah, Malaysia. 537
538
Institutional Review Board Statement: Not applicable. 539
540
Informed Consent Statement: Not applicable. 541
542
Data Availability Statement: Not applicable. 543
544
Acknowledgments: The authors express their sincere appreciation to the Researchers Support- 545
ing for this project. 546
547
Conflicts of Interest: The authors declare no conflicts of interest. 548
549

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