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Phytoremediation of
Environmental Pollutants
http://taylorandfrancis.com
Phytoremediation of
Environmental Pollutants
Edited by
Ram Chandra
N. K. Dubey
Vineet Kumar
CRC Press
Taylor & Francis Group
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Boca Raton, FL 33487-2742
© 2018 by Taylor & Francis Group, LLC

CRC Press is an imprint of Taylor & Francis Group, an Informa business
No claim to original U.S. Government works
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Library of Congress Cataloging-in-Publication Data
Names: Chandra, Ram (Biotechnology professor), editor. | Dubey, N. K., editor. | Kumar, Vineet
(Vineet Kumar Rudra), editor.
Title: Phytoremediation of environmental pollutants / editors, Ram Chandra, N.K. Dubey and
Vineet Kumar.
Description: Boca Raton : Taylor & Francis, CRC Press, 2018. | Includes bibliographical references
and index.
Identifiers: LCCN 2017029046| ISBN 9781138062603 (hardback : alk. paper) | ISBN 9781315161549 (ebook)
Subjects: LCSH: Phytoremediation.
Classification: LCC TD192.75 .P47835 2018 | DDC 628.4--dc23
LC record available at https://lccn.loc.gov/2017029046
Visit the Taylor & Francis Web site at

http://www.taylorandfrancis.com
and the CRC Press Web site at

http://www.crcpress.com
Contents
Preface............................................................................................................................................. vii
Editors...............................................................................................................................................ix
Contributors.....................................................................................................................................xi
1. Phytoremediation: A Green Sustainable Technology for Industrial Waste

Management.............................................................................................................................1
Ram Chandra and Vineet Kumar
2. Hyperaccumulator versus Nonhyperaccumulator Plants for Environmental

Waste Management...............................................................................................................43
Ram Chandra, Vineet Kumar, and Kshitij Singh
3. Adaptation Strategies of Plants against Heavy Metal Stress....................................... 81

Supriya Tiwari and N. K. Dubey
4. Molecular Mechanisms of Heavy Metal Hyperaccumulation in Plants.................... 99

Anupa Fonia, Preeti Singh, Vijetna Singh, Dhananjay Kumar, and Bhumi Nath Tripathi
5. Effects of Heavy-Metal Accumulation on Plant Internal Structure

and Physiological Adaptation........................................................................................... 117
B. B. Maruthi Sridhar, Fengxiang X. Han, and Yi Su
6. Role of Rhizospheric Mycobiota in Remediation of Arsenic Metalloids................ 137

Manvi Singh, Pankaj Kumar Srivastava, and Ravindra Nath Kharwar
7. Bacteria-Assisted Phytoremediation of Industrial Waste Pollutants

and Ecorestoration............................................................................................................... 159
Vineet Kumar and Ram Chandra
8. Nutrient Availability and Plant–Microbe Interactions in Phytoremediation

of Metalliferous Soils......................................................................................................... 201
Dipanwita Saha, Shibu Das, Prosenjit Chakraborty, and Aniruddha Saha
9. Phosphate-Solubilizing Bacteria as Plant Growth Promoters and Accelerators

of Phytoremediation........................................................................................................... 227
Munees Ahemad and Jawed Iqbal
10. Quorum Sensing and Siderophore Formation Mechanism of Rhizospheric

Bacteria during Phytoremediation of Environmental Pollutants............................. 245
Sangeeta Yadav and Ram Chandra
11. Common Weeds as Potential Tools for In Situ Phytoremediation

and Eco-Restoration of Industrially Polluted Sites...................................................... 271
Dhananjay Kumar, Sanjeev Kumar, and Narendra Kumar
v
vi Contents
12. Endophytic Bacterial Diversity in Roots of Wetland Plants and Their

Potential for Enhancing Phytoremediation of Environmental Pollutants.............. 285
Ram Chandra and Kshitij Singh
13. Phytoremediation as a Green and Clean Tool for Textile Dye Pollution
Abatement............................................................................................................................. 327
Niraj R. Rane, Rahul V. Khandare, Anuprita D. Watharkar, and Sanjay P. Govindwar
14. Phytotoxicity: An Essential Tool in Ecological Risk Assessment............................. 361

Rajesh Kumar Sharma, Bhanu Pandey, and Shivani Uniyal
15. Vermicomposting of Lignocellulosic Waste: A Biotechnological Tool

for Waste Management....................................................................................................... 387
Kavita Sharma and V. K. Garg
16. Phytocapping Technology for Sustainable Management of Landfill Sites............. 413

Sunil Kumar and Abhishek Khapre
17. Plant–Endophytic Bacterial Diversity for Production of Useful Metabolites

and Their Effect on Environmental Parameters........................................................... 421
Ajit Kumar Passari, Vineet Kumar Mishra, Zothanpuia, and Bhim Pratap Singh
18. Phytoremediation of Industrial Pollutants and Life Cycle Assessment.................. 441

Ram Chandra, Vineet Kumar, Sonam Tripathi, and Pooja Sharma
19. Biochemical and Molecular Aspects of Arsenic Tolerance in Plants....................... 471

Preeti Tripathi, Surabhi Awasthi, Reshu Chauhan, Pradyumna Kumar Singh,
Sudhakar Srivastava, and Rudra Deo Tripathi
Index.............................................................................................................................................. 487
Preface
The discharge of complex environmental pollutants from various industrial sectors has
created a challenge for scientists and environmentalists concerning the sustainable devel-
opment of mankind. Currently, the management of pollutants present in soil, water,
air, and food is a serious problem worldwide due to its direct effect on human health.
Consequently, the problems of global warming, climate change, change in biodiversity,
and extinction of numerous important flora and fauna have been observed by scientific
communities the world over.
Therefore, international researchers have reoriented their minds for environmental
waste management and bioremediation of toxic compounds present in the environment.
However, microbial technologies’ current cleanup techniques are not offering real solu-
tions for removal of complex toxic pollutants and safe recycling of natural resources. There
is a growing need among remediation professionals for effective, affordable, nonpollut-
ing alternatives to energy-intensive engineering processes for sustainable development.
Therefore, phytoremediation has recently arisen as an important technique to augment
the bioremediation process because it is an emerging green technology that uses a broad
range of plants to remediate soil, sediment, surface water, and groundwater environmen-
tal contaminants with toxic metals, organics, pesticides, and radionuclides.
Consequently, convergences of phytoremediation and microbial bioremediation strate-
gies have been suggested as a more successful approach for remediation of contaminants,
particularly organic compounds. Microbe-assisted phytoremediation with naturally
occurring microbes deliberately stimulated via seed inoculation has been investigated
in in situ and ex situ conditions globally for the real solution of problems for sustain-
able development. Further, to investigate the mechanism of plant–microbe interaction
for detoxification of complex pollutants, a variety of contaminant-degrading enzymes
(i.e., peroxidases, dioxygenases, laccases, P450 monooxygenases, phosphotases, dehaloge-
nases, and nitroreductases) has been reported in plants, fungi, and endophytic and rhi-
zospheric bacteria. But, this knowledge is fragmentary, specific, and limited to only a few
researchers. Therefore, the application of suitable technology for sustainable development
is still urgently warranted.
Hence, the aim of this book is to provide and disseminate detailed, up-to-date knowl-
edge regarding the various aspects of phytoremediation and plant–microbe interaction
to researchers, students, and industry professionals to inspire collective responsibility
to develop innovative technology for ecological restoration and environmental health.
Therefore, this book has compiled timely knowledge of various process and molecular
mechanisms for industrial waste detoxification during phytoremediation in wetland plants.
In addition, the book has highlighted phytoextraction speciation potential and adaptation
of hyperaccumulator wetland plants for the detoxification of heavy metals from organic
waste for ecorestoration. Further, the book has illustrated details regarding siderophore
formation and nutrient availability during plant–microbe interaction in rhizospheric
zones of plants growing in polluted environments.
The book has also provided the rare knowledge for in situ and ex situ phytoextraction
potential of common weeds growing on heavy metal–polluted sites for ecorestoration and
recycling of natural resources. The book has placed special emphasis on the role of endo-
phytic bacteria for phytoremediation of environmental pollutants during plant–microbe
vii
viii Preface
interaction in the presence of heavy metals. Lastly, the book has imbibed the special
knowledge on constructed wetland treatment systems as a promising technology for treat-
ment and recycling of hazardous wastewater, which is a plant–microbe-based technol-
ogy required in the current scenario for treatment of complex wastewater generated from
textile and agrobased industries. The book has also covered adequate knowledge on phy-
tocapping, vermicomposting, and life cycle assessment of environmental pollutants as a
new technique and tools for monitoring of environmental pollutants. Thus, this book will
be a unique compendium of up-to-date knowledge on phytoremediation of environmental
pollutants contributed by various experts in this area from universities, government labo-
ratories, and other academic global institutions.
Editors
Ram Chandra is currently professor and dean, Department of

Environmental Microbiology, School for Environmental Sciences,
Babasaheb Bhimrao Ambedkar (A Central) University, Lucknow,
Uttar Pradesh, India. He obtained his MSc from Banaras Hindu
University, India, in 1987. Subsequently, his PhD was awarded in 1994.
He has led work for bacterial degradation of lignin from pulp paper
mill waste and molasses melanoidins from distillery waste. He has
published more than 100 original research articles in peer-reviewed
journals of high impact. He has also published six books and 22 book
chapters on biodegradation and bioremediation of industrial pollut-
ants. He has been named a fellow of the Academy of Environmental Biology (FAEB), fellow
of the Association of Microbiologists of India (FAMI), and fellow of the Biotech Research
Society, India (FBRSI).
N. K. Dubey is currently working as a professor in the Center of

Advanced Studies in Botany, Department of Botany, Banaras Hindu
University, Varanasi, Uttar Pradesh, India. He obtained his MSc
and PhD degrees from Gorakhpur University, Uttar Pradesh, India.
He has produced more than 227 publications, four patents, and six
books. He has 33 years of teaching experience and is the recipient
of several awards, such as the National Academy of Science, India,
SR memorial gold medal for best teacher of the faculty of science,
BHU, and the young scientist award of the Indian Science Congress
Association. He has also worked in several administrative positions
at the university. He has visited Japan, France, South Korea, Belgium, Malaysia, the United
Kingdom, and Italy. Currently, he is on the editorial boards of several national and interna-
tional publications. He has guided several MSc and PhD students in their studies.
Vineet Kumar is currently a PhD scholar in the Department of

Environmental Microbiology, School for Environmental Sciences,
Babasaheb Bhimrao Ambedkar (A Central) University, Lucknow,
Uttar Pradesh, India. He received his MSc and MPhil from Chaudhary
Charan Singh University, Meerut, Uttar Pradesh, India, in 2010 and
2011. His research is focused on understanding the mechanism of
rhizospheric bacterial communities in the degradation and detoxi-
fication of organic and inorganic pollutants of complex industrial
wastewater. Key components of his research include the use of rhi-
zospheric bacteria to address metal uptake by wetland plants and
assessment of bioaugmentation/integration technologies for the phytoremediation of
wastewater pollutants from the environment. He is a life member of several scientific soci-
eties, including the Association of Microbiologists of India, the Biotech Research Society,
India, and the Indian Science Congress Association. He has authored or coauthored of five
research papers, twelve book chapters, and five scientific articles.
ix
http://taylorandfrancis.com
Contributors
Munees Ahemad Anupa Fonia

Department of Agricultural Microbiology Laboratory of Algal Biotechnology
Faculty of Agricultural Sciences Department of Botany
Aligarh Muslim University School of Life Sciences
Aligarh, Uttar Pradesh, India Hemwati Nandan Bahuguna Garhwal
University
Surabhi Awasthi Srinagar, Uttarakhand, India
Plant Ecology and Environmental Science
Division V. K. Garg
CSIR-National Botanical Research Institute Department of Environmental Science and
Lucknow, Uttar Pradesh, India Engineering
Guru Jambheshwar University of Science
Prosenjit Chakraborty and Technology
Molecular Plant Pathology Laboratory Hisar, India
Department of Botany and
University of North Bengal Center for Environmental Science and
West Bengal, India Technology
Central University of Punjab
Ram Chandra Bathinda, Punjab, India
Department of Environmental
Microbiology Sanjay P. Govindwar
School for Environmental Sciences Department of Biochemistry
Babasaheb Bhimrao Ambedkar (A Central) Shivaji University
University Vidyanagar, Kolhapur, Maharashtra, India
Lucknow, Uttar Pradesh, India
Fengxiang X. Han
Department of Chemistry and
Reshu Chauhan
Biochemistry
Jackson State University
Division
Jackson, Mississippi
CSIR-National Botanical Research Institute
Lucknow, Uttar Pradesh, India Jawed Iqbal
Department of Microbiology and
Shibu Das Immunology
Molecular Plant Pathology Laboratory H. M. Bligh Cancer Research Laboratories
Department of Botany Rosalind Franklin University of Medicine
University of North Bengal and Science
West Bengal, India Chicago Medical School
Chicago, Illinois
N. K. Dubey
Department of Botany Rahul V. Khandare
Institute of Science Department of Biotechnology
Banaras Hindu University Shivaji University
Varanasi, Uttar Pradesh, India Vidyanagar, Maharashtra, India
xi
xii Contributors
Abhishek Khapre Vineet Kumar

Solid and Hazardous Waste Management Department of Environmental
Division Microbiology
CSIR-National Environmental Engineering School for Environmental Sciences
Research Institute Babasaheb Bhimrao Ambedkar (A Central)
Nagpur, Maharashtra, India University
Ravindra Nath Kharwar
Department of Botany Vineet Kumar Mishra
Banaras Hindu University Molecular Microbiology and Systematics
Varanasi, Uttar Pradesh, India Laboratory
Department of Biotechnology
Dhananjay Kumar Mizoram University
Department of Environmental Sciences Aizawl, Mizoram, India
Babasaheb Bhimrao Ambedkar (A Central)
University Bhanu Pandey
Lucknow, Uttar Pradesh, India Department of Botany
Banaras Hindu University
Dhananjay Kumar Varanasi, Uttar Pradesh, India
Laboratory of Algal Biotechnology
Department of Botany Ajit Kumar Passari
School of Life Sciences Molecular Microbiology and Systematics
Hemwati Nandan Bahuguna Garhwal Laboratory
University Department of Biotechnology
Srinagar, Uttarakhand, India Mizoram University
Aizawl, Mizoram, India
Narendra Kumar
Department of Environmental Sciences Niraj R. Rane
Babasaheb Bhimrao Ambedkar (A Central) Department of Biotechnology
University Shivaji University
Lucknow, Uttar Pradesh, India Vidyanagar, Maharashtra, India
Sanjeev Kumar Aniruddha Saha

Department of Environmental Sciences Molecular Plant Pathology Laboratory
Babasaheb Bhimrao Ambedkar (A Central) Department of Botany
University University of North Bengal
Lucknow, Uttar Pradesh, India West Bengal, India
Sunil Kumar Dipanwita Saha

Solid and Hazardous Waste Management Department of Biotechnology
Division University of North Bengal
CSIR-National Environmental Engineering Siliguri, West Bengal, India
Research Institute
Nagpur, Maharashtra, India
Contributors xiii
Kavita Sharma Preeti Singh

Department of Environmental Science and Laboratory of Algal Biotechnology
Engineering Department of Botany
Guru Jambheshwar University of Science School of Life Sciences
and Technology Hemwati Nandan Bahuguna Garhwal
Hisar, Haryana, India University
Srinagar, Garhwal, Uttarakhand, India
Pooja Sharma
Department of Environmental Vijetna Singh
Microbiology Department of Biotechnology
School for Environmental Sciences Indira Gandhi National Tribal University
Babasaheb Bhimrao Ambedkar (A Central) Amarkantak, Madhya Pradesh, India
University
Lucknow, Uttar Pradesh, India B. B. Maruthi Sridhar
Department of Environmental and
Rajesh Kumar Sharma Interdisciplinary Sciences
Department of Botany Texas Southern University
Banaras Hindu University Houston, Texas
Varanasi, Uttar Pradesh, India
Pankaj Kumar Srivastava
Bhim Pratap Singh Department of Environmental Sciences
Molecular Microbiology and Systematics CSIR-National Botanical Research Institute
Laboratory Lucknow, Uttar Pradesh, India
Department of Biotechnology
Mizoram University Sudhakar Srivastava
Aizawl, Mizoram, India Institute of Environment and Sustainable
Development
Kshitij Singh Banaras Hindu University
Department of Environmental Varanasi, Uttar Pradesh, India
Microbiology
School for Environmental Sciences Yi Su
Babasaheb Bhimrao Ambedkar (A Central) School of Science and Computer
University Engineering
Lucknow, Uttar Pradesh, India University of Houston-Clear Lake
Houston, Texas
Manvi Singh
Department of Environmental Sciences Supriya Tiwari
CSIR-National Botanical Research Institute Department of Botany
Lucknow, Uttar Pradesh, India Institute of Science
Pradyumna Kumar Singh Varanasi, Uttar Pradesh, India
Division Bhumi Nath Tripathi
CSIR-National Botanical Research Institute Department of Biotechnology
Lucknow, Uttar Pradesh, India Indira Gandhi National Tribal University
Amarkantak, Madhya Pradesh, India
xiv Contributors
Preeti Tripathi Anuprita D. Watharkar

Plant Ecology and Environmental Science Department of Biochemistry
Division Shivaji University
CSIR-National Botanical Research Institute Vidyanagar, Kolhapur, Maharashtra, India
Sangeeta Yadav
Rudra Deo Tripathi Department of Environmental
Plant Ecology and Environmental Science Microbiology
Division School for Environmental Sciences
CSIR-National Botanical Research Institute Babasaheb Bhimrao Ambedkar (A Central)
Lucknow, Uttar Pradesh, India University
Sonam Tripathi
Department of Environmental Zothanpuia
Microbiology Molecular Microbiology and Systematics
School for Environmental Sciences Laboratory
Babasaheb Bhimrao Ambedkar (A Central) Department of Biotechnology
University Mizoram University
Lucknow, Uttar Pradesh, India Aizawl, Mizoram, India
Shivani Uniyal
Department of Botany
Varanasi, Uttar Pradesh, India
1
Phytoremediation: A Green Sustainable
Technology for Industrial Waste Management
Ram Chandra and Vineet Kumar
CONTENTS
1.1 Introduction.............................................................................................................................2
1.2 Categories of Phytoremediation, Their Principles, and Their Applications.................. 3
1.2.1 Phytoextraction....................................................................................................... 4
1.2.1.1 Bioconcentration and Translocation Factors............................................ 5
1.2.1.2 Bioaccumulation Factor and Phytoextraction Rate.................................6
1.2.1.3 Metal Extraction Amount and Phytoremediation Time........................7
1.2.1.4 Types of Phytoextraction.......................................................................... 7
1.2.2 Phytofiltration.............................................................................................................. 8
1.2.2.1 Rhizofiltration..............................................................................................8
1.2.2.2 Caulofiltration............................................................................................. 11
1.2.2.3 Blastofiltration............................................................................................ 11
1.2.3 Phytostabilization..................................................................................................... 12
1.2.4 Phytovolatilization.................................................................................................... 14
1.2.4.1 Direct Phytovolatilization......................................................................... 15
1.2.4.2 Indirect Phytovolatilization...................................................................... 16
1.2.5 Phytodegradation................................................................................................. 16
1.2.6 Rhizodegradation............................................................................................ 17
1.2.7 Phytodesalination..................................................................................................... 18
1.3 Categories of Plants That Grow on Metal-Contaminated Sites.................................... 18
1.3.1 Metal Excluders......................................................................................................... 18
1.3.2 Metal Indicators........................................................................................................ 19
1.3.3 Accumulators.....................................................................................................19
1.4 Mechanisms for Heavy Metal Tolerance, Accumulation, and Detoxification
in Plants.................................................................................................................................. 19
1.4.1 Tolerance in Plants.................................................................................................... 20
1.4.2 Accumulation and Detoxification in Plants.......................................................... 21
1.5 Mechanisms of Organic Pollutant Detoxification in Plants........................................... 21
1.5.1 Sorption, Uptake, and Translocation of Organic Compounds to Roots........... 21
1.5.2 Enzymatic Transformation of Organic Compounds...........................................22
1.6 Phytoremediation of Complex Industrial Wastes............................................................ 24
1.6.1 Distillery Wastes....................................................................................................... 24
1.6.2 Pulp and Paper Mill Wastes.................................................................................... 27
1.6.3 Tannery Wastes......................................................................................................... 30
1.6.4 Textile Wastes............................................................................................................ 32
1
2 Phytoremediation of Environmental Pollutants
1.6.5 Agrochemicals........................................................................................................... 32
1.6.6 Petroleum Waste.............................................................................................. 33
1.7 Advantages, Limitations, and Disadvantages of Phytoremediation.............................34
1.8 Challenges and Future Perspectives of Phytoremediation in Environmental
Waste Management.............................................................................................................. 35
1.9 Conclusions............................................................................................................................ 36
Acknowledgments......................................................................................................................... 36
References........................................................................................................................................ 36
1.1 Introduction
Global industrialization, urbanization, and population in the last two decades have
resulted in the generation of huge quantities of toxic waste. This hazardous waste includes
a variety of organic and inorganic compounds which pose serious threats to ecosystems.
Organic contaminants include different compounds such as petroleum hydrocarbons (e.g.,
benzopyrene), chlorinated solvents (i.e., polychlorinated benzenes, also known as PCBs),
linear halogenated hydrocarbons (e.g., trichloroethylene), volatile organic carbons, and
explosives such as trinitrotoluene. Inorganic compounds include nitrates, phosphates, met-
als and metalloids, such as mercury (Hg), arsenic (As), lead (Pb), cadmium (Cd), chromium
(Cr), copper (Cu), nickel (Ni), selenium (Se), silver (Ag), and zinc (Zn), and nonradioactive
or radioactive nuclides, like uranium (U), strontium (Sr), and cesium (Cs). Despite require-
ments for pollution control measures, these wastes are generally dumped on land or dis-
charged into water bodies (rivers, canals, lakes, etc.) without adequate treatment, and thus
they become a large source of environmental pollution and health hazards. It is, therefore,
urgent to adequately remove these pollutants from contaminated sites. Contamination of
soil and water poses major environmental concerns in the present scenario. A wide range
of methods based on not only physical and chemical but also biological means have been
available for the remediation of soil and water for decades, but environmental preservation
requires development of more sustainable approaches that promise thorough, economical,
and environmentally friendly ways, compared to conventional methods (Salt et al. 1995).
In recent decades, phytoremediation has provided a cost-effective, long-lasting, and aes-
thetic solution for remediation of hazardous pollutants from contaminated sites (Kramer
2005, Suresh and Ravishankar 2004). The idea that plants can be used for environmental
remediation is very old and cannot be traced to any particular source (Raskin et al. 1997).
About 300 years ago, plants were proposed for use in the treatment of wastewater. The term
phytoremediation (“phyto” meaning plants and the Latin suffix “remedium” meaning to
clear or restore) refers to a diverse collection of plant-based green technologies that use
either naturally occurring or genetically engineered plants to remove, transfer, stabilize,
and/or degrade contaminants located in soil, sediment, and water (Cunningham et al. 1997,
Newman and Reynolds 2004). Phytoremediation has also been called green remediation,
botano-remediation, agroremediation, and vegetative remediation (Chaney et al. 1997).
It is socially accepted by surrounding communities and regulatory agencies as a poten-
tially effective and beautiful technology (Newman and Reynolds 2005). A number of green
plants, including herbs, shrubs, and trees (both terrestrial and aquatic) have been reported
to be endowed with magnificent abilities for restoration and reclamation of contaminated
environments (Yoon et al. 2006, Gupta and Sinha 2007a, Qixing et al. 2011). Plants naturally
provide roots, stems, and leaves as habitats for a wide array of microorganisms which can
Phytoremediation 3
break down contaminants, enhancing the treatment process. Plants, through several nat-
ural biophysical and biochemical processes, such as adsorption, transport and transloca-
tion, hyperaccumulation or transformation, and mineralization, can remediate pollutants.
Recently, Environment Canada released a database, PHYTOREM (PHYTOREmediation of
Metals), which contains a worldwide inventory of 775 terrestrial and aquatic plants with
capabilities for accumulating or hyperaccumulating one or several of the 19 key metal-
lic elements (Padmavathiamma and Li 2007). The U.S. Environmental Protection Agency
(EPA) also maintains a website for researchers and the general public with information on
the growing field of phytoremediation (http://www.clu-in.org).
The purpose of this chapter is to provide a concise discussion of the processes associated
with the use of phytoremediation as a cleanup and decontamination technique for remedia-
tion of hazardous industrial waste-contaminated sites. In this chapter, we describe various
processes of phytoremediation, including phytoextraction, phytofiltration, phytostabili-
zation, phytovolatilization, phytodegradation, rhizodegradation, and phytodesalination,
with special emphasis on remediation of organic and inorganic pollutants. We also discuss
the potential and challenges of phytoremediation strategies for the removal of organic and
inorganic pollutants from contaminated sites, and we provide some information on costs.
Furthermore, the use of transgenic plants in phytoremediation progress is highlighted.
1.2 Categories of Phytoremediation, Their

Principles, and Their Applications
Phytoremediation is a broad expression comprising different strategies used by plants to
decontaminate soil, sludge, sediment, and wastewater. Depending on the contaminants,
the site conditions, the level of cleanup required, and the type of plants, phytoremediation
technology can be divided into different categories, namely, phytoextraction, phytofiltra-
tion, phytostabilization, phytovolatilization, and phytodegradation, with each category
having a different mechanism of action for remediating organic and inorganic pollutants
from contaminated soil, sludge, sediment, groundwater, surface water, and wastewater
(Raskin et al. 1997, Alkorta et al. 2004). The different mechanisms of phytoremediation are
illustrated in Figure 1.1
1. Phytoextraction: The use of plants that absorb pollutants and accumulate them
in organs removed from fields, together with crops, in order to purify soil from
heavy metal and organic substance contamination
2. Phytofiltration: Use of plant roots, seedlings, and excised shoots, which also take
up stored contaminants from an aqueous growth matrix
3. Phytostabilization: Plant-mediated immobilization or binding of contaminants
into the soil matrix, thereby reducing their bioavailability
4. Phytovolatilization: Contaminant uptake by plants and volatilization into the
atmosphere
5. Phytodegradation: The use of plants and associated microorganisms to degrade
organic pollutants
6. Rhizodegradation: Enhancement of degradation of organic pollutants in the plant
root zone by microorganisms
Phytovolatilization
excretion of volatile pollutants
Phytoextraction
metal accumulation in plant biomass
Harvest of shoot
Biomass can be
-reduced (compaction, composting, thermal Phytodegradation
treatment) for disposal in-plant detoxification of organic pollutants
-used to metal recovery (phytomining)
Phase-III Phase-I
Aboveground/above water Translocation

Phase-II
Underground/in water Biconcentration
Phytodegradation Phytostabilization
ex-planta detoxification of organic pollutants pollutants are stabilized in root zone
Rhizofiltration
adsorption or precipitation of metal on root
Phytoextraction
metal accumulation in plant root
Metals
Stabilized metals
Organic pollutants
Stabilized organic pollutants Phytouptake of pollutants
Uptake of metals and organic pollutants
FIGURE 1.1
Schematic representation of various phytoremediation strategies.
1.2.1 Phytoextraction
Phytoextraction, also called phytoaccumulation, phytoabsorption, or phytosequestration,
refers to the use of plants to absorb, translocate, and store toxic contaminants from soil, sedi-
ments, and/or sludge in the root and shoot tissues (Salt et al. 1998, Garbisu and Alkorta 2001).
Phytoextraction is the most recognized and applied phytoremediation technique for the
removal of toxic metals from contaminated environments (Figure 1.2). The idea of using plants
to extract metals from contaminated soil was introduced and developed by Utsunamyia (1980)
and Chaney (1983). Phytoextraction requires long-term maintenance and routine harvesting
of the plants, as well as safe disposal of polluted plant materials. The cost involved in phy-
toextraction, when compared with the those of conventional soil remediation techniques, is
10-fold lower. This means that phytoextraction is a cost-effective technique (Salt et al. 1995).
Phytoextraction does not work for some metals, including Pb, but it can be effective for As, Cd,
and Ni removal. Phytoextraction occurs in the root zone of the plant. The root zone may typi-
cally be relatively shallow, with the bulk of the root at a shallower rather than a deeper depth.
This can be a limitation of phytoextraction. Numerous factors, including pH of wastewater and
sediment, mobilization and uptake from soil, compartmentalization and sequestration within
Phytoremediation 5
Factor affecting phytoextraction

• Plant physiology
• Plant species
• Environment factors
Translocation
(temperature, weather, etc.)

of metals
• Transpiration rate
• Growth and biomass of
plant services
Contaminated soil
Accumulation
Factor affecting phytoextraction
of metals
• Soil pH, type, texture,
moisture, organic matter
Redox potential
• Rhizosphere microorganisms
• Plant root depth and density
Rhizosphere bacteria • Rhizosphere exudates and
secreation
Metal
Organic pollutants
Rhizosphere
FIGURE 1.2
Illustration of phytoextraction and factors that affect its efficacy.
the root, efficiency of xylem loading and transport (transfer factors), distribution between
metal sinks in the aerial parts, sequestration and storage in leaf cells, and plant growth and
transpiration rates can also affect the remediation process of a contaminated site. Generally,
the ideal plants to be used in phytoextraction should have the following characteristics
1. Tolerates high levels of metal concentration

2. Fast growth rate and high biomass production
3. Accumulates high level of metals in harvestable parts
4. Widely distributed and with a deep root system
5. Resistance to disease and pests and is unattractive to animals
6. Easy cultivation, harvesting, and processing
7. Low cultivation requirements
8. Repulsive to herbivores, to avoid food chain contamination
1.2.1.1 Bioconcentration and Translocation Factors

Two important factors that make a plant an efficient phyoextractor are its biomass produc-
tion and its bioconcentration efficiency (McGrath and Zhao 2003). The bioconcentration
efficiency of a plant is its ability to accumulate metals from contaminated soils and can
be estimated using the bioconcentration factor (BCF), which is defined as the ratio of the
metal concentration in the root of the plant to that in the soil/sludge (Yoon et al. 2006,
Gupta and Sinha 2007b). A plant’s ability to translocate metals from the root to the shoot is
measured using the translocation factor (TF), which is defined as the metal concentration
in the shoots versus that in the roots (Deng et al. 2004, Yoon et al. 2006). The BCF and TF
are calculated by the following equations.
BCF = (metal concentration in plant root)/(metal concentration in soil or sludge)
TF = (metal concentration in plant shoot)/(metal concentration in plant root)
The evaluation and selection of plants for phytoremediation purposes entirely depend on
the BCF and TF (MacFarlane et al. 2007). The BCF is a more important measure than the
shoot metal concentration when considering the potential of a given candidate species
for phytoextraction. A plant with both BCF and TF values of >1 has potential for use in
phytoextraction (Yoon et al. 2006). In addition, a plant with a BCF of >1 and TF of <1 has
potential for phytostabilization (Fitz and Wenzel 2002). However, the heavy metal uptake
by the roots and the successive translocation to the aboveground plant parts and organs
are primarily driven by the plant’s transpirational pool. Together with translocation to
aboveground organs, the distribution and accumulation of heavy metals in the different
organs of the plant also represent key factors for successful phytoremediation.
1.2.1.2 Bioaccumulation Factor and Phytoextraction Rate

The processes of phytoextraction generally require translocation of heavy metals to the
easily harvestable green plant parts. Enrichment occurs when a contaminant taken up by
a plant is not degraded rapidly, i.e., it accumulates in the plant. The enrichment factor, also
known as the bioaccumulation factor (BAF) or biological accumulation coefficient (BAC), is
calculated based on the ratio of the plant shoot concentration versus the soil concentration
(Li et al. 2007, Cui et al. 2007):
BAF = (metal concentration in plant shoot)/(metal concentration in soil)
Accumulation and translocation of metals depend on various biological or physico-

chemical factors and change according to environmental conditions, such as temperature,
pH, water ion content, salinity conditions, availability of heavy metals, and so on. To make
a crude evaluation of the general phytoextraction efficiency of plants, the depth of the root-
ing zone, the density of soil, the biomass production, and mortality of the aboveground
biomass component that is harvested are taken to into account to calculate the metal phyto-
extraction rate (PR) of the growing plant. Zhao et al. (2003) suggested that phytoextraction
efficiency can be estimated by calculating the percentage of metals or nutrients in the
harvestable biomass versus the concentration of metals in the soil mass where the species
were planted, as shown in the following equation:
PR (%) = (Cplant × Mplant )/(Csoil/sludge × Mrooted zone )  × 100
where Mplant is the mass of the harvestable aboveground plant biomass produced in one
harvest, Cplant is the metal concentration in the harvested component of the plant biomass,
Phytoremediation 7
Mrooted zone is the mass of the soil volume rooted by the species under study, and Csoil is the
metal concentration in the soil volume.
1.2.1.3 Metal Extraction Amount and Phytoremediation Time

The metal extraction amount and phytoremediation time also can be used to evaluate
plant phytoextraction efficiency; these measures of efficiency are calculated as follows
(Zhang et al. 2010):
Metal extracted (µg/plant) = (metal concentration in plant tissue) × (plant biomass)
Phytoremediation time (years) = (metal concentration × soil mass)/

(metal concentration in plant shoot × plant shoot biomass × 4)
The total metal distribution rate for a plant part is determined to identify roots or aerial
parts that are accumulators; the rate is calculated using the following equation:
(
Rate = [M]ij × DWi × 100 ) (∑ I [M] × DW )
i i
where [M]ij represents the j heavy metal content in plant part i (i.e., roots, stems, leaves, and
shoots) and DWi represents the weight of part i (Santos-Jallath et al. 2012).
1.2.1.4 Types of Phytoextraction
According to Salt et al. (1998), there are two basic strategies of phytoextraction:
1. Chelate-assisted phytoextraction
2. Continuous phytoextraction
1.2.1.4.1 Chelate-Assisted Phytoextraction
Chelate-assisted phytoextraction is also called induced phytoextraction. The phytoex-
traction mechanism has its own limitations, e.g., low mobility and low bioavailability of
some heavy metals (especially Pb) in polluted environments. An increase of heavy metal
mobility can be achieved by adding synthetic chelating agents which are capable of solu-
bilizing and complexing with heavy metals in a soil solution as well as promoting heavy
metal translocation from roots to the harvestable parts of the plant (Evangelou et al. 2007).
Chelating agents have been used as soil extractants and to maintain the solubility of
trace elements in hydroponic solutions. This strategy of phytoextraction is based on
the fact that the application of metal chelates to a soil significantly enhances metal
accumulation in plants. Enhancing metal accumulation in existing high-yielding crop
plants without diminishing their yield is the most feasible strategy in the develop-
ment of phytoremediation. To improve the metal accumulation capacities and uptake
speed of nonhyperaccumulating plants, the addition of chelating agents has been pro-
posed. Several studies have reported that the application of chelating agents, such as
ethylene diamine triacetic acid (EDTA), N-(2-hydroxyethyl)-ethylene diaminetriacetic
acid (HEDTA), diethylene–tetramine-pentaacetate acid (DTPA), ethylenediamine di-o-

hydroxy phenylacetic acid (EDDS), ethylene glycol-O,O′-bis-(2-amino-ethyl) N,N,N′,N′-
tetraacetic acid (EGTA), and citric acid, can enhance the effectiveness of phytoextraction
by mobilizing metals and increasing metal accumulation in plants (Chen and Cutright
2001, Turgut et al. 2004, Nowack et al. 2006).
1.2.1.4.2 Continuous Phytoextraction
The process of phytoextraction via use of hyperaccumulator plants is called continuous
phytoextraction. Continuous phytoextraction generally depends on the natural ability of
plants to accumulate, translocate, and resist high amounts of metals over the complete
growth cycle (Garbiscu and Alkorta 2001). Continuous phytoextraction is also environ-
mentally friendly, as it leaves the site suitable for cultivation of other plants. In urbanized
areas, continuous phytoextraction may be used in two types of sites. One type comprises
degraded soils in postindustrial areas, while the other, which is a highly promising future
application of phytoextraction, is connected with soils in the vicinity of transportation
routes and in urban green areas. The phytoextraction potentials of ornamental plant spe-
cies that are most frequently planted in urban locations are under investigation in many
research centers worldwide. Such species include Tagetes erecta L.
1.2.2 Phytofiltration
Phytofiltration is a cost-competitive technology that is primarily used to remediate or
adsorb pollutants, mainly metals, from water and aqueous waste streams (Dushenkov et al.
1995). Phytofiltration may be achieved via rhizofiltration, blastofiltration, or caulofiltration.
1.2.2.1 Rhizofiltration
Rhizofiltration is a root zone technology in which terrestrial and aquatic plants interact
with pollutants present in wastewater (Figure 1.3). It reduces the mobility of contaminants
and prevents their migration to the groundwater, thus reducing bioavailability for entry
into the food chain. Rhizofiltration can be used for metals that are retained only within
the roots (U.S. EPA 2000a). It is particularly effective and economically compelling when
low concentrations of contaminants and a large volume of water are involved. An ideal
plant for rhizofiltration should comprise rapidly growing roots with the ability to remove
toxic metals from solution over an extended period of time. The advantages of rhizofiltra-
tion include it ability to be used as in in situ or ex situ applications, and species other than
hyperaccumulators can also be used. The production of hydroponically grown transplants
and the maintenance of successful hydroponic systems in the field requires the expertise
of qualified personnel, and the facilities and specialized equipment required can increase
overhead costs.
Rhizofiltration works via several physical and biochemical processes, such as adsorption,
precipitation, rhizodegradation, and bioaccumulation. Rhizofiltration of metals involves
the absorption into or adsorption or precipitation onto plant roots of metals present in
a complex industrial wastewater. In addition to surface absorption, other slower mecha-
nisms underlying rhizofiltration may also occur: these include biological processes (intra-
cellular uptake, deposition in vacuoles, and translocation to the shoot) or precipitation of
the metal from the wastewater by the action of plant exudates. Based upon the nature of
pollutants present in wastewater, rhizofiltration processes may occur with phytoextrac-
tion, phytostabilization, or phytovolatilization processes. The efficiency of the mechanism
Wetland plants
Phytoremediation
Wetland plant values

• Wood for construction
• Phytomining
• Basket preparation
• Packaging material preparation
• Composting
First step treated Sand layer

wastewater integrated
into constructed
wetland treatment Gravels layer
system
Fibrous plant root Pebbles layer
working as biofilter
Wastewater released
after wetland plant
Air space treatment
Bacteria attached Cemented layer or impervious layer Biofilm formation occurs on

to plant root the surface of supporting matrix
along with root
FIGURE 1.3
Simplified schematic of a subsurface horizontal flow CW used for wastewater treatment.
9
of rhizofiltration lies in the efficiency of roots to synthesize certain chemicals which cause
heavy metals to accumulate in the plant body and then precipitate on the plant root sur-
face. Several aquatic species have been identified and tested for their phytoremediation
capacities in removing heavy metals from polluted waters. These species include sharp
dock (Polygonum amphibium L.), duck weed (Lemna minor L.), water hyacinth (Eichhornia
crassipes), water lettuce (P. stratiotes), water dropwort [Oenathe javanica (BL) DC], calamus
(Lepironia articulate), pennywort (Hydrocotyle umbellate L.) (Zaranyika and Ndapwadza 1995,
Zayed et al. 1998). However, these plants have limited potential for rhizofiltration, because
they are not efficient in removing metals due to their small, slow-growing roots. Sunflower
(Helianthus annus L.) and Indian mustard (Brassica juncea Czern.) are the most promising
terrestrial candidates for removing metals from contaminated water. The roots of Indian
mustard have been found to be effective in removal of Cd, Cr, Cu, Ni, Pb, and Zn, and sun-
flower can remove Pb, U, 137Cs, and 90Sr from hydroponic solutions (Dushenkov et al. 1995,
Prasad and Freitas 2003).
1.2.2.1.1 Rhizofiltration and Constructed Wetlands for Phytoremediation of Pollutants

A constructed wetland (CW) is an engineered wetland, in a more controlled environ-
ment, that has been applied for treatment of wastewaters for more than five decades.
Phytoremediation with wetland plants is an eco-friendly, aesthetically pleasing, cost-
effective, solar-driven, reliable, and robust wastewater treatment technology that is useful
for cleaning up nutrient overloads, toxic metals, and organic pollutants present in waste-
waters, municipal solid waste leachates, industrial wastewaters, agricultural, aquacultural,
and dairy farm effluent, storm runoff, sludges, pharmaceutical waste, and mine drainage,
as well as polluted river and lake waters with low to moderate levels of contamination
(Vymazal 2014). In addition, these treatment systems are good at removing pathogenic
microorganisms from wastewater. Macrophytes are the main biological component of
wetland ecosystems; they contribute directly to pollution reduction through uptake and
assimilation and indirectly by facilitating the growth of important pollutant-reducing
microorganisms through complex interactions in the rhizosphere (Guan et al. 2015). They
not only assimilate pollutants directly into their tissues but also act as catalysts for purifi-
cation reactions by increasing the microbial diversity in the root zone through the release
of oxygen and exudates and promotion of a variety of chemical and biochemical reactions
that enhance purification (Stottmeister et al. 2003). Wetland plants have fibrous root sys-
tems with large contact areas and the ability to accumulate large metal concentrations in
their organs compared to plants in the surrounding water. However, the principal pollut-
ant removal mechanisms in CW include biological processes, such as microbial metabolic
activity and plant uptake, as well as physico-chemical processes, including sedimen
tation, adsorption, filtration, volatilization, and precipitation of the waste–sediment,
root–sediment, and plant–water interfaces (Kadlec 2003). Although filtration is considered
an important process in these removal mechanisms, additional interactions occur among
media, plants, and water. The complex microbial community associated with filter material
roots, created by interactions with wastewater, is mainly responsible for the degradation
efficiency of pollutants and ecosystem stability (Stottmeister et al. 2003, Desta et al. 2014).
In addition, wetland plants have high remediation potentials for macronutrients due to
their generally fast growth and high biomass production. The common plants in wetlands
are the common reed (Phragmites spp.), cattails (Typha spp.), rush (Juncus spp.), and bulrush
(Scirpus spp.). These plants can withstand extreme environmental conditions, including
the presence of toxic contaminants such as heavy metals. The capacity of constructed wet-
lands for accumulation of heavy metals in shoots and roots of plants and the CW bed have
Phytoremediation 11
been demonstrated in many studies. These systems provide habitats for wildlife and as a
consequence, increased biodiversity; thus, they can be implemented to restore degraded
areas. The advantages of wetland plants include their ability to be used as in situ or ex situ
applications and can include plant species other than hyperaccumulators. However, one of
the limitations for CW is the requirement of a large land area to achieve proper pollutant
removal, due to the low hydraulic loading rate. It is necessary then to find the optimal CW
design characteristics in order to maximize pollutant removal efficiencies and to keep the
treatment area to a minimum. The main parameters that affect the removal efficiency of
CW are the hydraulic residence time and temperature. A well-designed CW should be able
to maintain the wetland’s hydraulic properties, namely, the hydraulic loading rate (HLR)
and the hydraulic retentention time (HRT), as these factors affect the treatment perfor-
mance of a CW. The HRT is determined by the mean surface area of the wetland system
(A), the flow depth (y), and the porosity of the substrate (p), i.e., the space available for water
to flow through the media, roots, and other solids in a CW system (Ghosh and Gopal 2010).
A CW requires a large land area to achieve proper pollutant removal, due to low HLRs:
HRT = V/Q = ( A × y × p)/Q
where Q (in liters per day) is the design flow rate, an assumed constant A (in square meters)
is the mean surface area of the system, V (in cubic meters) is the system volume, and y (in
meters) is the flow depth.
In these systems, the wastewater is fed into the system at an inlet and it flows slowly
through the porous media under the surface of the bed in a more or less horizontal path
until it reaches the outlet zone, where it is collected before leaving a level control arrange-
ment at the outlet (Figure 1.3). During its passage through the system, the wastewater
comes into contact with a network of aerobic, anoxic, and anaerobic zones. There are dif-
ferent CW types, depending on the flow type, and these can be divided into the subsur-
face flow (which includes vertical and horizontal subsurface flow CWs, depending on the
direction of the flow) and the surface flow (which includes the free water table on top of
the soil).
1.2.2.2 Caulofiltration
The term caulofiltration (with the Latin root caulis, for shoot) was first proposed by
Mesjasz-Przybyłowicz et al. in 2004, when excised plant shoots were used for removal of
heavy metals from contaminated wastewater (Figure 1.4a). In the study, the metals were
absorbed or adsorbed, and thus their movement in underground water was minimized.
Mesjasz-Przybyłowicz et al. (2004) used a nickel-hyperaccumulating plant, Berkheya cod-
dii, for phytoextraction and phytofiltration of the heavy metals from the wastewater; they
immersed the cut ends of shoots (excised shoots) in concentrated solutions of Cd, Ni, Pb, or
Zn and observed that large amounts of these metals accumulated in the leaves.
1.2.2.3 Blastofiltration
Blastofiltration is based on a concept similar to that of rhizofiltartion, but with blasto-
filtration plant seedlings are used for the removal of heavy metals from aqueous solu-
tions. Blastofiltration may turn out to be an alternative plant-based wastewater treatment
technology that takes advantage of the fast increase in the surface area-to-volume ratio
Excised plant
shoot
Plant seeding
Wastewater
(a) (b)
FIGURE 1.4
Removal of heavy metals in contaminated wastewater through caulofiltration (a), and blastofiltration (b).
after germination and the ability of the seedlings employed to absorb large quantities of
heavy metals, thus making this method suitable for wastewater treatment (Figure 1.4b).
The mechanisms involved in biosorption processes include chemisorption, complexation,
ion exchange, microprecipitation, hydroxide condensation onto a biosurface, and surface
adsorption. Lin et al. (2002) researched six kinds of crop seedlings for the capacity to
remove Pb from water via the blastofiltration method. Under the selected experimental
conditions, they found that a concentration of 100 mg/L Pb was reduced to below 5 mg/L
Pb in 72 h. In the dry roots of sunflower, pea, or castor oil plants, Pb accumulated to 91.6,
40.7, and 52.8 mg/g, respectively, while corn and Chinese sorghum also exhibited an abil-
ity for accumulation of Pb in the roots. Several traditional crop seedlings with a “super-
accumulation tendency” have been suggested for better blastofiltration prospects in the
phytoremediation of Pb pollution in water. It was recently reported that young seedlings
of Indian mustard may be as effective as roots in removing heavy metals from water when
grown in aquaculture in aerated water.
1.2.3 Phytostabilization
Phytostabilization, also called in situ or in place inactivation or phytimmobilization,
is another strategy by which plant species can reduce the mobility and biovailability
of pollutants in the environment, via either immobilization or prevention of migration
(U.S. EPA 2000a,b). In this process, certain plant species immobilize contaminants in
the soil through adsorption and accumulation by the roots, adsorption on roots, or
precipitation within the root zone and physical stabilization of soil, reducing the risk
to human health and environment (Barcelo and Poschenrieder 2003). The phytostabi-
lization technique is useful for immobilizing many heavy metals, for example, Pb, As,
Cd, Cr, Cu, and Zn. In addition, phytostabilization can be used to restore vegetation
cover in areas with limited vegetation that has resulted due to high levels of pollu-
tion. The microorganisms (bacteria and mycorrhiza) living in the rhizosphere of these
plants also have an important role in these processes: not only can they actively con-
tribute to change the trace element speciation, but also they can assist the plants in
Phytoremediation 13
overcoming phytotoxicity, thus assisting in the revegetation process (Mastretta et al.

2006). The process is applied in situations where there are potential human health
impacts and exposure to substances of concern can be reduced to acceptable levels by
contaminants. Phytostabilization requires the growth of a healthy and strong layer of
plants before human activity can resume on the treated land. However, there may be
potential for phytostabilization of organic pollutants, since some organic pollutants
and metabolic by-products of these pollutants can be attached to or incorporated into
plant components, such as lignins. This form of phytostabilization has been called
phytolignification (Cunningham et al. 1995). One difference between the two methods,
however, is that phytostabilization of metals is generally intended to occur in the soil,
whereas phytostabilization of organic pollutants through phytolignification occurs
aboveground. Unlike phytoextraction or hyperaccumulation of metals into shoots or
root tissues, phytostabilization primarily focuses on sequestration of the metals within
the rhizosphere but not in plant tissues (Figure 1.1). Characteristics of plants appropri-
ate for phytostabilization at a particular site include the following: tolerance to high
levels of the contaminant(s) of concern; high production of root biomass that will
be able to immobilize the contaminants through uptake, precipitation, or reduction;
retention of applicable contaminants in roots, as opposed to transfer to shoots, to avoid
a need for special handling and disposal of shoots. However, the amendments used
for stabilizing trace elements in contaminated soils commonly include liming agents,
phosphates (H3PO4, triple calcium phosphate, hydroxyapatite, phosphate rock), trace
element (Fe/Mn) oxyhydroxides, organic materials (e.g., biosolids, sludge, composts),
natural and synthetic zeolites, cyclonic and fly ash, and steel shots (Vangronsveld et al.
2009). Yadav et al. (2009) reported that the use of organic amendments, such as dairy
sludge increased plant growth and reduced bioavailability of As, Cr, and Zn in soil,
whereas biofertilizers reduced the uptake of As, Cr, and Zn by plants. Jatropha cur-
cas grows in Cr-contaminated soils and accumulates Cr in roots followed by shoots.
Accumulation of Cr induces oxidative stress in J. curcas, and the plant is able to tolerate
this stress through hyperactivity of an antioxidant defense system (Yadav et al. 2010).
The examples of some commonly reported heavy metal hyperacccumulator plants are
provided in Table 1.1.
TABLE 1.1
Some Plants Capable of Phytostabilization of Heavy Metals
Plant Species Metal(s) Reference
Isocoma veneta (Kunth) Greene Cd, Cu, Mn, Pb, Zn Gonzalez & Gonzalez-Chavez 2006
Teloxys graveolens Cd, Cu, Mn, Pb, Zn Gonzalez & Gonzalez-Chavez 2006
Euphorbia sp. Cd, Cu, Mn, Pb, Zn Gonzalez & Gonzalez-Chavez 2006
Dalea bicolor Humb. & Bonpl. ex Willd. Cd, Cu, Mn, Pb, Zn Gonzalez & Gonzalez-Chavez 2006
Lygeum spartum L. Cu, Pb, Zn Conesa et al. 2006
Piptatherum miliaceum L. Coss. Cu, Pb, Zn Conesa et al. 2006
Atriplex lentiformis (Torr.) S. Wats. As, Cu, Mn, Pb, Zn Mendez et al. 2007
Atriplex canescens (Pursh) Nutt. As, Hg, Mn, Pb Rosario et al. 2007
Bidens humilis Ag, As, Cd, Cu, Pb, Zn Bech et al. 2002
Baccharis neglecta Britt. As Flores-Tavizon et al. 2003
Schinus molle L. Cd, Cu, Mn, Pb, Zn Gonzalez & Gonzalez-Chavez 2006
1.2.4 Phytovolatilization
The release of volatile contaminants to the atmosphere via plant transpiration is known
as phytovolatilization (Figure 1.5). Phytovolatilization is a specialized form of phytotrans-
formation that can be used only for those contaminants that are highly volatile in nature
(Terry et al. 2000). It is a complex process driven by biophysical mechanisms of mass trans-
port through vegetation. Contaminants like Hg, As, and Se, once they are taken up by
plant roots, can be converted into nontoxic forms and volatilized into the atmosphere from
the roots, shoots, or leaves (U.S. EPA 2000b). During the process of Se phytovolatiliza-
tion, plants metabolize various inorganic or organic species of Se (e.g., selenate, selenite,
and Se-Met [Met]) into a gaseous form (Berken et al. 2002). Se volatilization in the form
of methyl selenate was proposed as major mechanism of Se removal from soil. Indian
mustard (Brassica juncea) has a high rate of Se accumulation and volatilization, and also
a fast growth rate, making it a promising species for Se remediation (Pilon-Smits et al.
1999). Recently, S-adenosyl-l-Met:l-Met S-methyltransferase, an enzyme involved in the
Direct
Phytoevaporation phytovolatilization
Air
Soil
Gas exchange
Indirect
phytovolatilization
Pollutants
Uptake of pollutants
FIGURE 1.5
Various processes in the phytovolatilization method.
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Title: Chinese mettle
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*** START OF THE PROJECT GUTENBERG EBOOK CHINESE

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Chinese Mettle
A Temple of Healing.
CHINESE METTLE
Written and Illustrated by E. G. KEMP, F.R.S.G.S.
Author of “The Face of China,” “The Face of Manchuria, Korea
and Russian Turkestan,” “Wanderings in Chinese Turkestan,”
“Reminiscences of a Sister” illustrated....
“Travaile, in the younger Sort is a Part of Education; in

the Elder, a Part of Experience.... When a Travailer
returneth home, let him not leave the countries, where he
hath travailed, altogether behind him.... Let it appeare that
he doth not change his country manners for those of
Forraigne Parts; But onely pricke in some Flowers of that
he hath Learned abroad, into the Customs of his own
Country.”—Bacon’s Essays.
Hodder and Stoughton Ltd.

Toronto London New York
St Paul’s House Warwick Square E.C.4
Printed in 1921
DEDICATED
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Prologue
Books of a descriptive nature, especially on a foreign country, are

most difficult to write. Under ordinary circumstances, writers of such
books, due to the differences of historical setting and social
background, may find it hard to free themselves from prejudice.
When the visit is confined to a section of the country, their views are
liable to be provincial. On the other hand, hasty travelling, however
large an area they may cover, makes their impressions superficial.
It is well said that modern travellers see nothing but the interior of
trains and hotels. This is gradually becoming true along the eastern
coast of China. To-day one who confines his visit to Shanghai or
Tientsin can not be said to have seen China, for it is not there that
one sees the real Chinese life. Civilization means more than
mechanical improvements. Herein lies the value of Miss Kemp’s
book. She has wisely neglected the “show window” by putting
seaports at the end. By acquainting the public with the wealth and
beauty of the interior—places seldom traversed by sojourners,—she
reveals to the readers the vitality and potential energy, both natural
and cultural, of a great nation. Throughout the book the authoress
combines the sincerity of description with the picturesqueness of
details.
Equally instructive is the authoress’ description of Chinese society
and some of the prominent Chinese men and women. Great
changes are going on in China. Nothing could afford more interest
and knowledge to the friends of China than to witness the shifting
scenes of the young Republic. The general tendency is undoubtedly
towards stability and progress, evolving order out of derangement
resulting from so immense a change as absolute monarchy to a
modern democracy. The authoress has well illustrated by facts the
advance which China has made in education, industry, commerce,
etc.
It is a common conviction nowadays that “the future of the world
depends largely on what happens in China during the next few
decades.” To know China, and to know her intimately, is the first step
towards a better international understanding and the assurance of
future peace in the Far East. The present volume serves as an
admirable guide.
Since the days of Marco Polo scores of books describing China,
both good and poor, have been written. As an intimate friend and
careful observer of China, Miss Kemp’s new production together with
her previous works are certainly to be classified among the best
ones. From cover to cover, this volume contains facts and
experiences that are entertaining, informative, and valuable.
SAO-KE ALFRED SZE.
Chinese Legation, Washington, D.C.
October 24, 1921.
Contents
Prologue by His Excellency Sao Ke Alfred Sze (Chinese

Minister at Washington)
CHAP. PAGE
Introduction 11
I The Long Road 17

Provinces visited: 1 Shansi, the Progressive—Railway Journey
from Shanghai to Taiyuanfu. 2 Chihli—A few words about Peking.
3 Shantung—The Japanese domination—Tsinan, a great
Educational Centre. 4 Kiangsi—Shanghai, the centre of Great
National Movements. 5 Chekiang—Railway Trip to Hangchowfu
—Down the Coast by Steamer to Hong Kong and Tongking.
Through Indo-China by Rail to 6 Yünnan. From Yünnanfu by
Chair into 7 Kweichow, a most backward Province. From Chen
Yüen by House-boat through 8 Hunan. By Steamer from
Changsha into 9 Hupeh. Down the Yangtze from Hankow through
10 Nganhwei, 11 Kiangsi to Shanghai.
II The Model Governor—Yen Hsi-Shan 49

Description of Taiyuanfu, the Capital—The Hall of Public Worship
—Girls’ Schools—Sports—New Institutions for Cattle Breeding,
Agriculture, Sericulture—Beggars removed into Workhouses—
Introduction of the New Script—Unification of the Language—The
Governor as Author—Famine Relief Works—Four Hundred Miles
of Road-making—The Model Gaol—Quick Methods of
Communication—Transport Lorries from England.
III The Province of Yünnan 67

French Influence—Activity of Brigands—A Modern Robin Hood—
Chinese Home Missions—Women’s Initiative—A Visit to the Lake
and its Places of Pilgrimage—Mineral Resources of Yünnan—
Preparations for Road Journey—Wonderful Scenery and Flora—
Stormy Weather—Opium Culture—The Chinese View of Opium
Smoking—Sale of Children—Difficulties with Coolies—Weather
Symbols.
IV The Province of Kweichow 87

A Land of Mountains and Valleys—Extraordinary Rock Formations
—Surface Coal—The Rose Garden of the World—Post Office
Facilities—Varieties of Inns—Buffaloes as Neighbours—Wild
Animals—Industries at Lang-tai-Fung—Roman Catholic Missions
—Anshunfu—Hospitals Needed—Visits to the Haunts of
Aborigines—First Miao Church—Tenten—Baptismal Service—A
Chinese Farm—Village Shrines—Ta-ting, the Mission Centre for
many Tribes—Bridges of Various Kinds—Kwei Yang, the Capital—
Buddhist Monks—Valuable Trees—Military Escort Needed—Strict
Rules not Strictly Observed—Chen Yüen—Start on River Journey
in small House-boat.
V Some Aboriginal Tribes in Kweichow 117

The Miao Family—Their Character, Habits, Dress, Embroideries,
Hairdressing, Food, Morals—Tribes Numerous: Not yet Classified
—Language: no Written Language—Great Flowery and Small
Flowery Miao—The “Wooden Combs” and Black Miao—Ancestor
Worship—The I-chia—A Different Set of Tribes—Written as well
as Spoken Language—Notes from Dr. Henry’s Observations—On
Death Rites, on various Superstitions, on Types, on Language—
Animistic Religion—Theory of Nestorian Influence—Sacrifice—
MS. Story of Creation and Deluge—Black Miao Version—
Festivals—“Courting-talk”—Music and Dancing—Witchcraft—
Chinese Attitude towards the Tribes.
VI The Province of Hunan 141

Boat Travel—Fear of Robbers and Evil Spirits—Yuanchowfu—
White Wax Industry—Hong Kiang—Medical Work—Shenchowfu
—American Ideals—Standard Oil Company—Changteh—Journey
by Launch across Tong Ting Lake to Changsha, Capital of Hunan
—Fear of Southerners—Red Cross Preparations—Various
Missions—Yale College—Dr. Keller’s Bible School—An English
Consulate.
VII Present-Day Ironsides—General Feng Yu Hsiang 159

Changsha Headquarters—Work of 16th Mixed Brigade in Sze-
Chuan—Arrival at Changsha—Changes in City Life—Suppression
of Opium Dens, Gambling Hells, Theatres, etc.—Open-air
Evening Schools—Industrial Schools—Women’s Education—
General Feng’s Career—Murder of Dr. Logan—The General’s
Patriotism—Industrial Training of Army—Strict Discipline—Sunday
in the Army—Service for the Ladies—Officers’ Service—Recent
Events—Withdrawal of Northern Army from Changsha—Entry of
Southern Troops—No Pay for the 16th Mixed Brigade.
VIII The New Chinese Woman—Miss Tseng, B.Sc.

(Lond.) 175
Chinese ideas of Woman’s Sphere—Confucius on Woman
—“Rules for Women”—Modern Women—Their Patriotic Spirit—
Miss Tseng’s Early Life and Training—Adoption of Christianity—
English University Career—Return to China—School started for
Chinese Girls of Middle Classes—Sports—Decision of Students
not to Strike—Miss Tseng’s Influence—Women Journalists and
Doctors.
IX The Youth of China 189

Veneration of Old Age Modified—Young Chinese in responsible
posts—Youth criticizes Antiquity: Seizes Responsibility—Attitude
to Japan—Organized Union defeats Government—Co-operation
with Shopkeepers—Effect of Spirit on Literature—Change of
Education by Dowager Empress—Further Development under
Republic—Contrast between Renaissance of China and Japan—
Attitude towards Religion—Noxious Effects of Propaganda by
Missions—Importance of Improved Educational Work—Students
and Social Service—Famine Relief—National University of Peking
—Foreign Lectureships—Hong Kong University—Projected
University at Amoy—St. John’s College, Shanghai, and Others—
Child Labour—The Boy Scout Movement—Student Demands—
Youth Accepting Christian Ideals.
X Some Chinese Seaports and Commerce 205

Wênchowfu and Its Waterways—Foochow—Trinity College and
Union—Many Institutions and Industries—Floods—Amoy—
Curious Scenery—Y.M.C.A.—Chambers of Commerce—Guilds—
Trade Relations—Swatow—Great Commercial Centre and Outlet
for Hinterland—Journey by Railway to Home of Tan Family—Fine
Ancestral Tablets—American Baptist Community—City of Chao
Chowfu—Results of Earthquake—New Hospital—Missionary
Memorial Tablet in Buddhist Temple—Swatow’s Industries—Light
Railway—Presbyterian Missions—Hong Kong contrasted with
Macao—Trip to Canton—Wonderful Maze of Narrow Streets—
Many Industries—City of the Dead—Railways—Commercial
Outlook—Britain’s Opportunity for Service.
Index 223
Illustrations
PAGE
A Temple of Healing Frontispiece
A Chinese Ritz 40
Yen Hsi Shan, Statesman 48
Temple of Heaven and Hell, Workhouse 56
The Pilgrim Way, Yünnanfu Lake 72
In Cloudland 72
The Gate of the Elements 80
“Lonely I Stand on the Loneliest Hill-top” 96
Robbers’ Haunts 104
Light for the Spirits 112
Little Flowery Miao Coat 120
Ancient I-chia Script 128
Great Flowery Miao 136
A Roadside Restaurant 136
A Man of Mark 160
A Chinese Leader of Thought 176
“Nor soul helps body more
Than body soul.” 184
“Girls,
Knowledge is now no more a fountain seal’d:
Drink deep.” 184
Storm-driven Boats 208
Chinese Mettle
Introduction
“Why do you go on journeys to such impossible places?” is a

question which I am continually asked. “Can it possibly be for
pleasure? How can any one like,” and here the eyebrows are raised
and a shade of disgust, politely veiled, is visible, “to stop in awful
inns and visit cities full of dirt and smells? What is your real reason
for travelling in the interior of China?”
Strange as it may seem to the comfort-loving Britisher, Pleasure
is the main lure to China, and a sort of basilisk fascination which is
quite irresistible. Naturally, there are other reasons also—this time it
was to take a young doctor niece to see what the Chinese Empire
was like (we passed through thirteen out of the eighteen provinces)
before she settled down to work in her own hospital. Besides this, in
the interests of geography and a better understanding of the Chinese
people by our own people it seems worth while for an artist to try and
show what China is like at the present time. That is the reason for
writing this book. I frankly own that I hate writing, but am consumed
with a desire that people should know what is now going on in China.
My rooted conviction is that the future of the world depends largely
on what happens in China during the next decade. This is the
decisive hour. An American deplored to a Chinaman the troublous
condition of the country, and received a reply to the following effect:
“You must have patience with us, we are only a nine-year-old
Government, and, if my memory does not deceive me, the United
States did not get their constitution for thirteen years.”
The amazing fact is that an empire that has outlived every other
world-empire of antiquity is now completely changing its whole
government and institutions in a time of world-wide disintegration,
and is steadily moving forward, despite internecine warfare.
What is more remarkable still is the changing mettle of the race. Its
temperamental characteristics seem to be undergoing as great a
change as the social fabric. China has an inward force that is
stronger than appears: her faults are so glaring that they have
obscured this fact completely. She has been wise enough—unlike all
other countries—to entrust certain branches of her administration to
foreigners until she is capable of taking over control; these branches
are the Customs, the Salt Gabelle and the Post and Telegraph
Service; and she has been admirably served by them, despite some
flaws in the administration. The vital need of to-day is for honest,
incorruptible, educated Chinese who will save their country from their
worst enemies—the self-seeking, ambitious, unscrupulous Chinese,
who play off one party against another and, through fear of foreign
foe as well as home treachery, are dragging China to the verge of
the precipice.
To the Chinese themselves, therefore, this book is very specially
addressed, and I search for winged words to summon them to their
great task to act as true patriots and to devote every energy and
talent they possess to building up a new and more glorious empire
than the Celestial Empire of the past.
The conditions of China are changing not merely from day to day,
but from hour to hour, so that my book must seem strangely
paradoxical. The mutable jostles the immutable, and—as in life itself
—all sorts of things get mixed up together. There are no watertight
compartments in nature, and I have taken the liberty of making my
book as miscellaneous as the page of a dictionary. It tells of great
personalities, of great movements, of wild tribes, of nature and of
human nature, of politics, commerce, religion and education, and
scores of other things.
The account of the Miao and I-chia tribes opens up a question of
considerable importance in the new China, for there are
unaccounted tribes throughout the whole of Western China, not to
mention those in other parts, such as the Hakka tribe, whose
picturesque boats ply on the Han Kiang (= river) on which Chao
Chowfu is situated.
The task has been a heavy one, because the worthy treatment of
such a vast and complex subject is far beyond my powers, but in
past days readers have always treated my books so far more
generously than they deserved, that I take courage and send forth
this fledgling of my pen and brush.
London, 1921.
Chapter I
The Long Road
“Travel abroad for one year is more profitable than study at

home for five years.... Mencius remarks that a man can learn
foreign things best abroad; but much more benefit can be
derived from travel by older and experienced men than by the
young.”—Chang Chih Tung.
Chapter I
The Long Road
The journey through thirteen provinces of China brought us into

contact with such an amazing variety of people that it is no easy task
to describe clearly what we saw. I propose to give first of all a brief
account of the journey as a whole, and then deal with the more
important and less-known provinces somewhat in detail. The one
salient fact which emerges from the welter of experiences is that the
mettle of the Chinese people is changing, even to the remotest
bound of the empire. What it will eventually become, the wisest man
cannot foretell, but it is amazingly interesting to watch the changes
taking place, and I hope that the sympathetic interest of my readers
will be quickened by the record.
The journey in China itself lasted six months. We reached
Shanghai February 1, via the United States, and at once went by rail
to Taiyuanfu, the capital of Shansi. Visitors to China nowadays can
get on fairly comfortably without any knowledge of the language, if
they keep to the beaten track. The railway runs from Shanghai up to
Peking, and only two changes have to be made during the journey of
two days and a night; the first is at the Pukow ferry, a very easy
OUR FELLOW TRAVELLERS.
matter and well arranged. The train goes down to the Yangtze at
Chen Kiang, and the steam tug takes you across in about ten
minutes. At the other side we got into a more comfortable train
where we had secured sleeping places; in all the long-distance trains
there are restaurant cars, where you can get fairly good meals at
reasonable prices.
The next afternoon we reached Tientsin at 4.40, and had to
change into a crowded train to Peking; there is always, I believe, a
sort of free fight to get in at all, and the weakest go to the wall,
except in the case of children, for the Chinese are very fond of
children, and never fail to make room for them. Peking is reached by
8 p.m. After leaving the train we passed through two great old
gateways, linking Past and Present, to another railway station close
at hand, and had only sufficient time to get our luggage through the
customs, and to start at 9.30 on the Peking-Hankow line for the
junction at Shihchiah Chwang. It is not pleasant to do cross-country
travelling in any country at night, and to reach a place at 4.20 a.m.
on a cold February morning where you have to change stations
would be far too difficult a matter for foreigners were it not for
mission friends. They never seem to think anything of such trifles as
spending nights looking after helpless travellers. We soon got all our
goods and chattels out, and handed them over to a Chinese, whom
our friend had engaged to look after them till the train left at 7 a.m.
for Taiyuanfu. Meanwhile he escorted us to a clean inn, and
comforted us with tea and cake and bedding till it was time to start.
The bright cold dawn saw us off once more at 6 o’clock, rather
enjoying a walk to the station; there we got into quite a comfortable
train, and our friend travelled with us back to his own station, the first
up the line. All day we passed through fascinating scenery, often
following the course of a river, where turbine water-wheels in groups
were busy grinding corn.
The line was only begun in 1903 by a French company, but the
Chinese have bought it up, and it ought to be increasingly valuable,
chiefly for the transport of coal, in which product Shansi is specially
rich. How well I remember in the old days seeing the long files of
donkeys, each laden with basketfuls of coal, slowly wending their
way across the plains and over the hills; whereas now the railway
taps some of the chief coal-mines in the Pingtau district. The seams
are from eleven to thirty feet in thickness and quite near the surface,
and the coal is of excellent quality. The length of the line is only one
hundred and fifty-five miles, and we did it in nine hours, whereas on
my first journey we were more than nine days travelling up by mule
litter and on horseback!
The railway station at Taiyuanfu is outside the great city wall, and
we saw as we approached it fine new barracks—Governor Yen has
had a macadamized road built to reach one of his barracks, leading
through a gate which has been closed over three hundred years.

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Phytoremediation of Environmental

Pollutants 1st Edition Chandra

Microbe-Assisted Phytoremediation of Environmental

Phytoremediation Potential of Perennial Grasses 1st

Phytoremediation Management of Environmental

Phytoremediation Management of Environmental

Measurement Analysis and Remediation of Environmental

Environmental Pollutants and Their Bioremediation

Enhancing Cleanup of Environmental Pollutants Volume 1

Enhancing Cleanup of Environmental Pollutants Volume 2

© 2018 by Taylor & Francis Group, LLC

No claim to original U.S. Government works

Printed on acid-free paper

International Standard Book Number-13: 978-1-138-06260-3 (Hardback)

Library of Congress Cataloging-in-Publication Data

Visit the Taylor & Francis Web site at

and the CRC Press Web site at

1. Phytoremediation: A Green Sustainable Technology for Industrial Waste

2. Hyperaccumulator versus Nonhyperaccumulator Plants for Environmental

3. Adaptation Strategies of Plants against Heavy Metal Stress....................................... 81

4. Molecular Mechanisms of Heavy Metal Hyperaccumulation in Plants.................... 99

5. Effects of Heavy-Metal Accumulation on Plant Internal Structure

6. Role of Rhizospheric Mycobiota in Remediation of Arsenic Metalloids................ 137

7. Bacteria-Assisted Phytoremediation of Industrial Waste Pollutants

8. Nutrient Availability and Plant–Microbe Interactions in Phytoremediation

9. Phosphate-Solubilizing Bacteria as Plant Growth Promoters and Accelerators

10. Quorum Sensing and Siderophore Formation Mechanism of Rhizospheric

11. Common Weeds as Potential Tools for In Situ Phytoremediation

12. Endophytic Bacterial Diversity in Roots of Wetland Plants and Their

14. Phytotoxicity: An Essential Tool in Ecological Risk Assessment............................. 361

15. Vermicomposting of Lignocellulosic Waste: A Biotechnological Tool

16. Phytocapping Technology for Sustainable Management of Landfill Sites............. 413

17. Plant–Endophytic Bacterial Diversity for Production of Useful Metabolites

18. Phytoremediation of Industrial Pollutants and Life Cycle Assessment.................. 441

19. Biochemical and Molecular Aspects of Arsenic Tolerance in Plants....................... 471

Ram Chandra is currently professor and dean, Department of

N. K. Dubey is currently working as a professor in the Center of

Vineet Kumar is currently a PhD scholar in the Department of

Munees Ahemad Anupa Fonia

Abhishek Khapre Vineet Kumar

Sanjeev Kumar Aniruddha Saha

Sunil Kumar Dipanwita Saha

Kavita Sharma Preeti Singh

Preeti Tripathi Anuprita D. Watharkar

Ram Chandra and Vineet Kumar

1.2 Categories of Phytoremediation, Their

Aboveground/above water Translocation

Factor affecting phytoextraction

(temperature, weather, etc.)

1. Tolerates high levels of metal concentration

1.2.1.1 Bioconcentration and Translocation Factors

BCF = (metal concentration in plant root)/(metal concentration in soil or sludge)

TF = (metal concentration in plant shoot)/(metal concentration in plant root)

1.2.1.2 Bioaccumulation Factor and Phytoextraction Rate

BAF = (metal concentration in plant shoot)/(metal concentration in soil)

Accumulation and translocation of metals depend on various biological or physico-

PR (%) = (Cplant × Mplant )/(Csoil/sludge × Mrooted zone )  × 100

1.2.1.3 Metal Extraction Amount and Phytoremediation Time

Metal extracted (µg/plant) = (metal concentration in plant tissue) × (plant biomass)

Phytoremediation time (years) = (metal concentration × soil mass)/

acid (HEDTA), diethylene–tetramine-pentaacetate acid (DTPA), ethylenediamine di-o-

Wetland plant values

First step treated Sand layer

1.2 Categories of Phytoremediation, Their

1.2.1.1 Bioconcentration and Translocation Factors

1.2.1.2 Bioaccumulation Factor and Phytoextraction Rate

1.2.1.3 Metal Extraction Amount and Phytoremediation Time

1.2.2.1.1 Rhizofiltration and Constructed Wetlands for Phytoremediation of Pollutants