The Plant Family Brassicaceae ENVIRONMENTAL POLLUTION

VOLUME 21

Editors Brain J. Alloway, Department of Soil Science, The University of Reading, U.K. Jack T. Trevors, School of Environmental Sciences, University of Guelph, Ontario, Canada

Editorial Board I. Colbeck, Interdisciplinary Centre for Environment and Society, Department of Biological Sciences, University of Essex, Colchester, U.K. R.L. Crawford, Food Research Center (FRC) 204, University of Idaho, Moscow, Idaho, U.S.A. W. Salomons, GKSS Research Center, Geesthacht, Germany

For further volumes: http://www.springer.com/series/5929 Naser A. Anjum l Iqbal Ahmad M. Eduarda Pereira l Armando C. Duarte Shahid Umar l Nafees A. Khan Editors

The Plant Family Brassicaceae

Contribution Towards Phytoremediation Editors Naser A. Anjum Iqbal Ahmad Centre for Environmental and Centre for Environmental and Marine Marine Studies (CESAM) & Studies (CESAM) & Department Department of Chemistry of Chemistry and Biology University of Aveiro University of Aveiro 3810-193 Aveiro 3810-193 Aveiro Portugal Portugal

M. Eduarda Pereira Armando C. Duarte Centre for Environmental and Centre for Environmental and Marine Studies (CESAM) & Marine Studies (CESAM) & Department of Chemistry Department of Chemistry University of Aveiro University of Aveiro 3810-193 Aveiro 3810-193 Aveiro Portugal Portugal

Shahid Umar Nafees A. Khan Department of Botany Department of Botany Faculty of Science Faculty of Life Sciences Hamdard University Aligarh Muslim University New Delhi, 110062 Aligarh 202002 India Uttar Pradesh, India

ISSN 1566-0745 ISBN 978-94-007-3912-3 ISBN 978-94-007-3913-0 (eBook) DOI 10.1007/978-94-007-3913-0 Springer Dordrecht Heidelberg New York London

Library of Congress Control Number: 2012936075

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Springer is part of Springer Science+Business Media (www.springer.com) Foreword

Plant Biology is reaching an extraordinary degree of conceptual complexity, especially since the crucial technological advances during the last two decades, halfway between the twentieth and twenty-first centuries. Integration from the molecular to the whole plant level of the mechanisms governing growth and developmental processes provides now a better and an increasingly diverse vision of the functioning of plants in different habitats and under changing environmental conditions. This is featuring a solid body of scientific knowledge which covers the various levels of plant research: cellular, biochemical, genetic, molecular, physiological, ecological and evolutionary. This plethora of knowledge and meth- odological consolidation now allows to more precisely understand the physiological and molecular mechanisms, to see the richness of phenotypic responses of plants to the diverse environmental situations, to deepen consistently in the evolutionary lines, to discern the molecular basis of variation for including all within the system’s biology, and to consider the diversity and specificities of plant functionalism. Spectacular progress is being made in the fundamental knowledge of reception of external signals and internal signaling pathways, the vital mechanisms of regulation of homeostasis, the integration of metabolic functions, and the differen- tiation and development of plants exposed to biotic or abiotic stress factors. As expected, this advanced insight into basic processes governing plants under adverse environmental conditions has substantially improved our expertise in practical applications, not only in the field of agronomy, but also in that of environmental restoration. Phytoremediation as a clean, sustainable technology is becoming an attractive way to recover degraded land. No wonder that research and publications on this topic have increased exponentially during the last years and that we face a rapidly expanding area where basic knowledge is being turned into effective environmental technology. It is not accidental that this new book entitled ‘The Plant Family Brassicaceae: Contribution Towards Phytoremediation’ focuses the issue of phytoremediation on the Brassicaceae. This large botanical family with 360 genus and 3,700 species not

v vi Foreword only includes important food and industrial plants, but also Arabidopsis thaliana the plant model species par excellence. Small genome size, self-compatibility, short life cycle, small biomass, and large production of seeds make this Arabidopsis thaliana an ideal research object for studies into functional genomics. Identification of genes involved in metal uptake, transport and compartmentation and knowledge of key enzymes in metabolic pathways able to transform and detoxify organic pollutants provide the fundamental tools for the development of phytoremediation technologies. This extensive basic research in Arabidopsis thaliana allowed fast advances in the knowledge of the functioning of Brassicaceae species of high interest in phytoremediation processes, such as the close relative Arabidopsis halleri and Thlaspi caerulescens (Noccaea caerulescens), both species with ability to hyperaccumulate cadmium and zinc. Also the nickel hyperaccumulators of the genus Alyssum are within the Brassicaceae. Furthermore, the non-hyperaccumulating species of the genus Brassica, especially Brassica juncea and Brassica napus,the seed-oil canola which combines both industrial applications and phytoremediation potential, are being explored for phytoremediation technologies. These Brassica species have considerably lower shoot metal concentrations than metal hyperaccumulators. This is compensated, however, by the much higher biomass in Brassica sp. Thus, the focus on Brassicaceae in this new book is fully awarded by this predominant presence of representatives of this family in current research in phytoremediation. This leads to the question about the characteristics that makes Brassicaceae species so outstandingly attractive for recovering contaminated land. To our opinion, two features common to Brassicaceae may contribute to this: special pathways of secondary sulphur metabolism for glucosinolate synthesis and, probably in part related to this, the fact that most Brassicaceae, are non mycorrhizal. A high tissue level of antioxidants is a further characteristic of importance for performance under stressful conditions. Brassicaceae have a high sulphur requirement. Sulphur availability in mine spoils uses to range from normal to extremely high and most contaminated soils can fully satisfy the higher sulphur demand of the Brassicaceae. Moreover, in Brassicaceae the levels of sulphur containing metabolites that are important for basic metal tolerance, such as glutathion and phytochelatins seem to be affected only under extreme sulphur deficiency. Many Brassicaceae species are pioneers on waste areas and seem well- adapted to recently formed, badly structured substrates. No need for mycorrhization under these conditions implies high nutrient efficiency, especially for phosphorous. In Brassica crops differences in phosphorus acquisition are closely related to both root architecture traits and internal phosphorus use efficiency. Metal hyperaccumulators like Thlaspi caerulescens seem well adapted to the low phosphorus availability of mine waste areas and surplus phosphorus supply may not enhance their biomass production and/or metal extraction potential. Many species that perform well on mine spoils are mycorrhizal. Considerable amounts of heavy metals can be retained in the cell walls, especially of ecto- and ericoid mycorrhizal fungi, thus limiting metal uptake by the plants. Metallophytes that are non- mycorrhizal, such as most Brassicaceae and Caryophyllaceae species Foreword vii

(e.g. Silene vulgaris), have their own mechanisms to exclude metals from either or both roots and shoots. Nonetheless, on polluted soils they tend to take up higher amounts of heavy metals than mycorrhizal plants. Thus tolerance to higher tissue concentrations of metals is a prerequisite for good performance of these species on metal contaminated sites. The evolution of metal hyperaccumulation behavior with an especially high number of representatives in the Brassicaceae is a further argument for meriting special attention. These plants do not efficiently exclude metals neither from the roots nor the shoots, but even forage and accumulate metals from soils with low concentrations. Binding of the metals in non-toxic form and efficient compartmentation into cell walls and vacuoles are fundamental mechanisms in the hyperaccumulation life style. So the great achievement and novelty of this book edited by eminent scientists Naser A. Anjum, Iqbal Ahmad, M. Eduarda Pereira, Armando C. Duarte, Shahid Umar and Nafees A. Khan resides in the focus on phytoremediation referred to the Brassicaceae family containing species that are well adapted to harsh conditions on waste land and with efficient metal uptake and tolerance mechanisms. The different chapters written by experienced specialists provide a unique compilation of the dispersed literature on this topic. By sure, the readers of the book will benefit from this joint vision of the actual and the potential contribution of this botanical family to the emerging discipline of phytoremediation. Therefore, we believe that this book targets a potentially broad spectrum of audience ranging from the researchers in this field of increasing importance to undergraduate and graduate students who want an overview of current knowledge referred to the Brassicaceae and its utility in phytoremediation. No less important is this text for all those interested in the agricultural use of the Brassicaceae and their contribution to the sustainable production of healthy food.

Charlotte Poschenrieder and Juan Barcelo´ Lab. Fisiologı´a Vegetal, Facultad de Biociencias Universidad Auto´noma de Barcelona, E-08193 Bellaterra Spain. e-mail: [email protected] (C.P.), [email protected] (J.B.)

Preface

The sustainability of agriculture (the only source of food) and the civilization of mankind rely on two precious natural resources namely land and water. Unfor- tunately, both land and water have been subjected to maximum exploitation and severely degraded or polluted by kinds of contaminants originating mainly from anthropogenic activities. Majority of contaminants get accumulated in plants and either directly or indirectly, find their way into food web thus cause severe secondary consequences. Above facts together can produce severe deterioration of natural resources, disturbance of ecosystems thus, creating enormous human health and welfare challenges globally. The remediation of varied environmental contaminants using plants (phytoremediation; “phyto” meaning plant, and the Latin suffix “remedium” meaning to clean or restore) have been accepted advantageous over commonly used physical remediation methods in costs, practice and the scale at which the processes operate. This approach is emerging as an innovative tool with greater potential for achieving sustainable development and also to decontaminate air, soils/sediments and water, and for other environmental restoration applications. The angiosperm family Brassicaceae – commonly termed as the mustard family (or Cruciferae, because of their characteristic flowers consisting of four petals in the form of a Greek cross), is a large dicot plant family comprising nearly 338 genera (assigned to 10–19 tribes) and 3,700 species with worldwide distribu- tion, of major agro-economic and scientific importance. The family Brassicaceae represents hundreds of plant families reported so far for their potential use in the remediation of varied environmental contaminants including toxic metals- metalloids. The most of the members of the Brassicaceae plant family well repre- sent the metal hyperaccumulation among 0.2% of all angiosperms and thus, have key role in phytoremediation technology. Many of the plant species within Brassicaceae family such as Alyssum, Arabidopsis, Berkheya, Bornmuellera, Cardamine, Cochlearia, Crambe, Peltaria, Pseudosempervivum, Stanleya, Strep- tanthus,Thlaspi including oilseed Brassicas grow fast, yield high biomass and are well adapted to a range of environmental conditions. Some species are tolerant

ix x Preface to high levels of trace metals, and there is the potential to select superior genotypes for phytoremediation. Of 87 different metals/metalloids-hyperaccumulator plant species in the family Brassicaceae, in particular model metals/metalloids hyperaccumulators Alyssum sp., Thlaspi sp. and Arabidopsis sp. have been studied extensively for their ability to hyperaccumulate varied environmental contaminants including metals and metalloids. In addition, they are well suited to genetic manipulation and in vitro culture techniques and are attractive candidates for the introduction of genes aimed at phytoremediation. Although, the number of publications focused on plant-based remediation of varied environmental contaminants has been growing exponentially in the last decade but the significant role/contribution of the members of the plant family Brassicaceae for decontaminating varied environmental compartments either remained untouched or little debated. Written by an international team of authors and as a significant addition to the Springers’ Environmental Pollution book series the current volume ‘The Plant Family Brassicaceae: Contribution Towards Phytoremediation’ aims mainly to update our understanding on the recent breakthroughs in the area of differential adaptation of the plant species within Brassicaceae family to contaminants through mechanisms involving physiological, biochemical and molecular processes and their cumulative role in contaminants accumulation, tolerance and remediation. Besides highlighting the taxonomy of the family Brassicaceae, the current status of contaminants (metals/metalloids)-addition to varied environment and its consequences, the information included in this book will bring very stimulating insights into the mechanism involved in the physiological, biochemical and molecular processes responsible for environmental contaminants accumulation, tolerance and remediation in Brassicaceaeans. Additionally, the book also intends to explore the various potential strategies (such as the physiological, biochemical, plant breeding and genetic engineering approaches) for the enhancement of contaminants-tolerance, -accumulation and -remediation potentials of the members of the plant family Brassicaceae. This volume promises to be a useful asset for researchers, students, other academicians and policy makers involved in sustainable remediation of varied environmental compartments. We are thankful to contributors for their interests, significant contributions and cooperation that eventually made the present volume possible. Thanks are also due to all the well-wishers, teachers, seniors, research students and family. Without their unending support, motivation and encouragement the present grueling task would have never been accomplished. We would like to offer our sincere thanks to Professors Brian J Alloway and Jack T Trevors, Environmental Pollution book series editors for their kind consent to include the current volume to the series. Exceptional kind support provided by Tamara Welschot, Judith Terpos and their team at Springer deserves praises which made our efforts successful. Last, but not least, the financial supports to our research from Foundation for Science & Technology (FCT), Portugal, the Aveiro University Research Preface xi

Institute/Centre for Environmental and Marine Studies (CESAM), University Grants Commission (UGC) and Department of Science and Technology (DST), New Delhi, India, Indian Potash Research Institute (IPRI), Gurgaon, India and International Potash Institute (IPI), Switzerland are gratefully acknowledged.

Editors Naser A. Anjum Iqbal Ahmad M. Eduarda Pereira Armando C. Duarte Shahid Umar Nafees A. Khan

Contents

1 The Plant Family Brassicaceae: An Introduction...... 1 Naser A. Anjum, Sarvajeet S. Gill, Iqbal Ahmad, M. Pacheco, Armando C. Duarte, Shahid Umar, Nafees A. Khan, and M. Eduarda Pereira 2 Current Status of Toxic Metals Addition to Environment and Its Consequences...... 35 Qaisar Mahmood, Audil Rashid, Sheikh S. Ahmad, Muhammad R. Azim, and Muhammad Bilal 3 Cadmium Accumulation by Plants of Brassicaceae Family and Its Connection with Their Primary and Secondary Metabolism...... 71 Petr Babula, Vojtech Adam, Ladislav Havel, and Rene Kizek 4 Metal Hyperaccumulation and Tolerance in Alyssum, Arabidopsis and Thlaspi:AnOverview...... 99 Sarvajeet S. Gill, Naser A. Anjum, Iqbal Ahmad, P. Thangavel, G. Sridevi, M. Pacheco, Armando C. Duarte, Shahid Umar, Nafees A. Khan, and M. Eduarda Pereira 5 Brassica Rhizosphere-Microbe Interactions and Their Role in Phytoremediation...... 139 Mushtaq Ahmed, V.K. Singh, and R.S. Upadhyay 6 Phytoremediation of Heavy Metals by Brassica juncea in Aquatic and Terrestrial Environment ...... 153 Anamika Singh and M.H. Fulekar 7 Toxic Metals Accumulation, Tolerance and Homeostasis in Brassicaoilseed Species: Overview of Physiological, Biochemical and Molecular Mechanisms...... 171 Vinay Kumar, Monika Mahajan, and Sudesh K. Yadav

xiii xiv Contents

8 The Role of Plant Growth-Promoting Rhizosphere Bacteria in Toxic Metal Extraction by Brassica spp...... 213 Oguz C. Turgay and Serdar Bilen 9 Biochemical and Functional Responses of Arabidopsis thaliana Exposed to Cadmium, Copper and Zinc...... 239 Adriano Sofo, Antonio Scopa, Tony Remans, Jaco Vangronsveld, and Ann Cuypers 10 Brassicas in Turkey and Their Potential Role for Degraded Habitats’ Remediation...... 265 Munir Ozturk, Abdul R. Memon, Salih Gucel, and M. Serdal Sakcali 11 Chelate Assisted Phytoextraction Using Oilseed Brassicas...... 289 Firdaus-e-Bareen 12 Roles of Rhizospheric Processes and Plant Physiology in Applied Phytoremediation of Contaminated Soils Using Brassica Oilseeds...... 313 Sarah Neilson and Nishanta Rajakaruna Index ...... 331 Contributors

Vojtech Adam Department of Chemistry and Biochemistry, Faculty of Agronomy/ Central European Institute of Technology, Mendel University in Brno/Brno Univer- sity of Technology, Zemedelska 1, CZ-613 00 Brno, Czech Republic/Technicka 3058/10, CZ-616 00 Brno, Czech Republic Iqbal Ahmad Centre for Environmental and Marine Studies (CESAM) & Depart- ment of Chemistry and Biology, University of Aveiro, 3810-193 Aveiro, Portugal Sheikh S. Ahmad Department of Environmental Science, Fatima Jinnah Women University, Rawalpindi, Pakistan Mushtaq Ahmed Department of Botany, Laboratory of Mycopathology and Microbial Technology, Centre of Advanced Study in Botany, Banaras Hindu University, Varanasi 221005, India Naser A. Anjum Centre for Environmental and Marine Studies (CESAM) & Department of Chemistry, University of Aveiro, 3810-193 Aveiro, Portugal Muhammad R. Azim Department of Botany, Federal Government Post Graduate College, H-8, Islamabad, Pakistan Petr Babula Department of Natural Drugs, Faculty of Pharmacy, University of Veterinary and Pharmaceutical Sciences, Palackeho 1-3, CZ-612 42 Brno, Czech Republic Firdaus-e-Bareen Department of Botany, University of the Punjab, Lahore 54590, Pakistan Muhammad Bilal Department of Environmental Sciences, COMSATS Institute of Information Technology, Abbottabad 22060, Pakistan Serdar Bilen Department of Soil Science, Faculty of Agriculture, Ataturk University, Erzurum, Turkey

xv xvi Contributors

Ann Cuypers Centre for Environmental Sciences, Hasselt University, Agoralaan Building D, 3590 Diepenbeek, Belgium Armando C. Duarte Centre for Environmental and Marine Studies (CESAM) & Department of Chemistry, University of Aveiro, 3810-193 Aveiro, Portugal M.H. Fulekar Department of Life Sciences, University of Mumbai, Santacruz (E), Mumbai 400 098, India Sarvajeet S. Gill Plant Molecular Biology Group, International Centre for Genetic Engineering and Biotechnology, Aruna Asaf Ali Marg, New Delhi, India Stress Physiology and Molecular Biology Lab, Centre for Biotechnology, MD University, Rohtak, Haryana, India Salih Gucel Environmental Sciences Institute, Near East University, Nicosia, The Northern Cyprus Ladislav Havel Department of Plant Biology, Faculty of Agronomy, Mendel University in Brno, Zemedelska 1, CZ-613 00 Brno, Czech Republic Nafees A. Khan Department of Botany, Faculty of Life Sciences, Aligarh Muslim University, Aligarh 202002, Uttar Pradesh, India Rene Kizek Department of Chemistry and Biochemistry, Faculty of Agronomy/ Central European Institute of Technology, Mendel University in Brno/Brno Univer- sity of Technology, Zemedelska 1, CZ-613 00 Brno, Czech Republic/Technicka 3058/10, CZ-616 00 Brno, Czech Republic Vinay Kumar Plant Metabolic Engineering and Nanobiology Laboratory, Biotechnology Division, CSIR-Institute of Himalayan Bioresource Technology (CSIR-IHBT), Council of Scientiﬁc and Industrial Research, Palampur 176061, HP, India Monika Mahajan Plant Metabolic Engineering and Nanobiology Laboratory, Biotechnology Division, CSIR-Institute of Himalayan Bioresource Technology (CSIR-IHBT), Council of Scientiﬁc and Industrial Research, Palampur 176061, HP, India Qaisar Mahmood Department of Environmental Sciences, COMSATS Institute of Information Technology, Abbottabad 22060, Pakistan Abdul R. Memon Department of Genetics and Bioengineering, Faculty of Engineering and Information Technologies, International Burch University, 71000 Sarajevo, Bosnia and Herzegovina Sarah Neilson College of the Atlantic, 105 Eden Street, Bar Harbor, ME 04609, USA Munir Ozturk Botany Department, Science Faculty, Ege University, Bornova- Izmir, Turkey M. Pacheco Centre for Environmental and Marine Studies (CESAM) & Department of Biology, University of Aveiro, 3810-193 Aveiro, Portugal Contributors xvii

M. Eduarda Pereira Centre for Environmental and Marine Studies (CESAM) & Department of Chemistry, University of Aveiro, 3810-193 Aveiro, Portugal Nishanta Rajakaruna College of the Atlantic, 105 Eden Street, Bar Harbor, ME 04609, USA Audil Rashid Department of Environmental Sciences, PMAS Arid Agriculture University, Rawalpindi, Pakistan Tony Remans Centre for Environmental Sciences, Hasselt University, Agoralaan Building D, 3590 Diepenbeek, Belgium M. Serdal Sakcali Faculty of Science and Arts, Fatih University, Buyukcekmece, Istanbul, Turkey Antonio Scopa Dipartimento di Scienze dei Sistemi Colturali, Forestali e dell’Ambiente, Universita` degli Studi della Basilicata, Via dell’Ateneo Lucano 10, 85100 Potenza, Italy Anamika Singh Department of Life Sciences, University of Mumbai, Santacruz (E), Mumbai 400 098, India V.K. Singh Department of Botany, Laboratory of Mycopathology and Microbial Technology, Centre of Advanced Study in Botany, Banaras Hindu University, Varanasi 221005, India Adriano Sofo Dipartimento di Scienze dei Sistemi Colturali, Forestali e dell’Ambiente, Universita` degli Studi della Basilicata, Via dell’Ateneo Lucano 10, 85100 Potenza, Italy G. Sridevi Department of Plant Biotechnology, School of Biotechnology, Madurai Kamaraj University, Madurai 625021, Tamil Nadu, India P. Thangavel Department of Environmental Science, Periyar University, Salem 636011, Tamil Nadu, India Oguz C. Turgay Department of Soil Science, Faculty of Agriculture, Ankara University, Diskapi, 06110 Ankara, Turkey Shahid Umar Department of Botany, Faculty of Science, Hamdard University, New Delhi 110062, India R.S. Upadhyay Department of Botany, Laboratory of Mycopathology and Microbial Technology, Centre of Advanced Study in Botany, Banaras Hindu University, Varanasi 221005, India Jaco Vangronsveld Centre for Environmental Sciences, Hasselt University, Agoralaan Building D, 3590 Diepenbeek, Belgium Sudesh K. Yadav Plant Metabolic Engineering and Nanobiology Laboratory, Biotechnology Division, CSIR-Institute of Himalayan Bioresource Technology (CSIR-IHBT), Council of Scientiﬁc and Industrial Research, Palampur 176061, HP, India