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Selenium in plants: Molecular, Physiological, Ecological and Evolutionary Aspects PDF

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Plant Ecophysiology Elizabeth A.H. Pilon-Smits Lenny H.E. Winkel Zhi-Qing Lin Editors Selenium in plants Molecular, Physiological, Ecological and Evolutionary Aspects Plant Ecophysiology Volume 11 Series Editors Luit J. De Kok, University of Groningen, The Netherlands Malcolm J. Hawkesford, Rothamsted Research, United Kingdom Aims & Scope: The Springer Series in Plant Ecophysiology comprises a series of volumes that deals with the impact of biotic and abiotic factors on plant functioning and physiological adaptation to the environment. The aim of the Plant Ecophysiology series is to review and integrate the present knowledge on the impact of the environment on plant functioning and adaptation at various levels: from the molecular, biochemical and physiological to a whole plant level. This series is of interest to scientists who like to be informed of new developments and insights in plant ecophysiology, and can be used as advanced textbooks for biology students. More information about this series at http://www.springer.com/series/6193 Elizabeth A.H. Pilon-Smits • Lenny H.E. Winkel Zhi-Qing Lin Editors Selenium in plants Molecular, Physiological, Ecological and Evolutionary Aspects Editors Elizabeth A.H. Pilon-Smits Lenny H.E. Winkel Department of Biology Eawag, Swiss Federal Institute of Aquatic Colorado State University Science and Technology Fort Collins, CO, USA Duebendorf, Switzerland Institute of Biogeochemistry Zhi-Qing Lin and Pollutant Dynamics Environmental Sciences Program and ETH Zurich Department of Biological Sciences Zurich, Switzerland Southern Illinois University Edwardsville Edwardsville, IL, USA ISSN 1572-5561 ISSN 2405-4321 (electronic) Plant Ecophysiology ISBN 978-3-319-56248-3 ISBN 978-3-319-56249-0 (eBook) DOI 10.1007/978-3-319-56249-0 Library of Congress Control Number: 2017939733 © Springer International Publishing AG 2017 This work is subject to copyright. All rights are reserved by the Publisher, whether the whole or part of the material is concerned, specifically the rights of translation, reprinting, reuse of illustrations, recitation, broadcasting, reproduction on microfilms or in any other physical way, and transmission or information storage and retrieval, electronic adaptation, computer software, or by similar or dissimilar methodology now known or hereafter developed. The use of general descriptive names, registered names, trademarks, service marks, etc. in this publication does not imply, even in the absence of a specific statement, that such names are exempt from the relevant protective laws and regulations and therefore free for general use. The publisher, the authors and the editors are safe to assume that the advice and information in this book are believed to be true and accurate at the date of publication. Neither the publisher nor the authors or the editors give a warranty, express or implied, with respect to the material contained herein or for any errors or omissions that may have been made. The publisher remains neutral with regard to jurisdictional claims in published maps and institutional affiliations. Printed on acid-free paper This Springer imprint is published by Springer Nature The registered company is Springer International Publishing AG The registered company address is: Gewerbestrasse 11, 6330 Cham, Switzerland Preface The element selenium (Se) is fascinating and important for several reasons. It is an essential micronutrient for many life forms including bacteria, archaea, some algae, and most animals. Essential Se metabolism appears to have been lost, however, in plants and fungi. Organisms that require Se for their survival utilize Se in the form of selenocysteine (SeCys) in the active site of the so-called selenoproteins (humans have 25), which have redox functions and are involved in immune function, thyroid metabolism, and spermatogenesis. Interestingly, SeCys in proteins is encoded by the opal stop codon, if it is flanked by a specific SeCys insertion sequence, which is different in prokaryotes and eukaryotes. At high tissue levels, Se becomes toxic to organisms, due to oxidative stress and to the replacement of S amino acids in pro- teins by their Se analogs. Relative to other micronutrients, Se has a very narrow window between adequacy and toxicity, which is around one order of magnitude. As a consequence, both Se deficiency and toxicity are prevalent worldwide and coincide with soils that are naturally low and high in Se, respectively. More than a billion people have been estimated to be affected, particularly by Se deficiency, which compromises their immune system (higher chance of infections including HIV and cancer), thyroid activity and male fertility, as well as mental function. While not essential for plants, Se is a beneficial nutrient that enhances plant growth and antioxidant activity. Plants readily take up Se due to its similarity to sulfur (S) and assimilate it into a variety of organic Se compounds, analogous to S. Different plant species vary in the degree to which they take up and metabolize Se and in their capacity to tolerate Se. Some plants native to seleniferous soils even have evolved the capacity to hyperaccumulate Se to levels between 0.1 and 1.5% of their dry weight. This variation in plant Se accumulation, metabolism, and tolerance is not only of intrinsic interest but important because of its relevance for human, animal, and environmental health. Different forms of Se have different nutritional values. Crop Se content and Se speciation (chemical forms) are highly relevant for consumers, since the majority of the world’s population directly depends on plants v vi Preface for its dietary Se, and all people obtain their Se ultimately from plants, even if indirectly via animals that feed on plants. Crops with optimal Se concentration and speciation may be selected or bred via classical or genetically enhanced breeding strategies. The levels and forms of Se in plants are not only a function of the genetic properties of the plants but also of their growth substrate. Soils vary in the concen- tration and forms of Se and Se bioavailability, which is influenced by abiotic and biotic factors. Selenium may be added in chemical or green fertilizer to crops grow- ing on low-Se soils, a practice called biofortification. On the other end of the spec- trum, if soils are particularly high in Se, this may cause toxicity, especially if Se-rich soil is used for irrigated agriculture or if Se-rich fossil fuels are used for energy. Plants may be used to extract excess Se from soil or water, a technology termed phytoremediation. In the absence of other contaminants, the resulting Se-rich plant material may be used to supply dietary Se in low-Se areas. Apart from these applications, there are also many intrinsically interesting aspects of plant Se accumulation. Why and how do different plant species differ so much in the degree to which they accumulate and metabolize Se? Which processes underlie Se hyperaccumulation? Which benefits and disadvantages may Se accumu- lation confer to the plant? In other words, which selection pressures may favor or constrain Se accumulation? How does plant Se affect ecological interactions with herbivores, pollinators, microbes, and other plants, and how does this drive the evo- lution of both plant and ecological partners? How may plant Se accumulation and metabolism affect Se movement through the food chain, ecosystem, and ultimately global Se cycling? In this book about Se, the plant has center stage, but the plant is placed in the context of its environment and its evolutionary history. The book starts with an overview of global Se distribution and the geological and biological processes that affect global Se movement in water, air, or soil particles. In subsequent chapters, the reader can follow Se from the point when it becomes bioavailable; is taken up by algae and plants and then metabolized, translocated, and sequestered; and is ulti- mately volatilized, consumed, and moved up in the food chain or redeposited in litter to the soil and recycled after decomposition. Relevant for Se bioavailability and for Se movement in the food chain, Se metabolism is also reviewed in prokary- otes and in mammalian consumers, and the nutritional effects of the consumed plant Se for consumers are discussed. The reader will learn about the profound ecological effects of plant Se on interactions with herbivores, pollinators, microbes, and other plants and the likely selection pressures that drive the evolution of Se hyperaccumu- lation. Furthermore, the latest knowledge is presented about the molecular pro- cesses involved in Se uptake, metabolism, tolerance, and (hyper)accumulation, as well as successful approaches to optimize Se accumulation and speciation via clas- sical crop breeding and genetic engineering. The book concludes by highlighting global Se deficiency and toxicity issues in the world and successful applications of plant Se accumulation for biofortification and phytoremediation. Preface vii We are happy to be able to present this book in this special year, 200 years after the discovery of Se by Jons Jacob Berzelius in Sweden. We thank everyone who has contributed to this book and helped highlight the many fascinating facets of Se in plants from their respective vantage point and area of expertise. We hope the book will be of use for the Se research community and anyone who is interested in learn- ing about this interesting and important element. Fort Collins, CO, USA Elizabeth A.H. Pilon-Smits Zurich, Switzerland Lenny H.E. Winkel Edwardsville, IL, USA Zhi-Qing Lin January 24, 2017 Contents Part I Selenium Distribution, Bioavailability and Metabolism in Plants 1 Multi-scale Factors and Processes Controlling Selenium Distributions in Soils . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3 Gerrad D. Jones and Lenny H.E. Winkel 2 Biochemistry of Plant Selenium Uptake and Metabolism . . . . . . . . . . . 21 Zackary Guignardi and Michela Schiavon 3 Molecular Mechanisms of Selenium Responses and Resistance in Plants . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 35 Masanori Tamaoki and Akiko Maruyama-Nakashita 4 Mechanisms of Plant Selenium Hyperaccumulation . . . . . . . . . . . . . . . 53 Elizabeth A.H. Pilon-Smits Part II Selenium Metabolism in Non-plant Organisms – Influence on Se Fluxes in Ecosystems and Relevance for Human Health 5 Selenium and Algae: Accumulation, Tolerance Mechanisms and Dietary Perspectives . . . . . . . . . . . . . . . . . . . . . . . . . . 69 Michela Schiavon and Francesca Dalla Vecchia 6 Bacteria Versus Selenium: A View from the Inside Out . . . . . . . . . . . . 79 Lucian C. Staicu, Ronald S. Oremland, Ryuta Tobe, and Hisaaki Mihara 7 S elenium and the Plant Microbiome . . . . . . . . . . . . . . . . . . . . . . . . . . . 109 Alyssa T. Cochran ix x Contents 8 Selenium Metabolism in Herbivores and Higher Trophic Levels Including Mammals . . . . . . . . . . . . . . . . . . . . . . . . . . . 123 Lutz Schomburg and Elias S.J. Arnér Part III Genetic, Evolutionary and Ecological Aspects of Plant Se Accumulation 9 The Genetics of Selenium Accumulation by Plants . . . . . . . . . . . . . . . 143 Philip J. White 10 Manipulating Selenium Metabolism in Plants: A Simple Twist of Metabolic Fate Can Alter Selenium Tolerance and Accumulation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 165 Doug Van Hoewyk and Ozgur Çakir 11 Ecology of Selenium in Plants . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 177 Colin F. Quinn, Ali F. El Mehdawi, and Elizabeth A.H. Pilon-Smits 12 Evolutionary Aspects of Plant Selenium Accumulation . . . . . . . . . . . 189 R. Jason B. Reynolds, Jennifer J. Cappa, and Elizabeth A.H. Pilon-Smits Part IV The Societal Relevance of Se for Human and Environmental Health: Biofortification and Phytoremediation 13 O verview of Selenium Deficiency and Toxicity Worldwide: Affected Areas, Selenium-Related Health Issues, and Case Studies . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 209 André Rodrigues dos Reis, Hassan El-Ramady, Elcio Ferreira Santos, Priscila Lupino Gratão, and Lutz Schomburg 14 S elenium Biofortification . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 231 Gary S. Bañuelos, Zhi-Qing Lin, and Martin Broadley 15 E ffects of Selenium on Plant Metabolism and Implications for Crops and Consumers . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 257 Michela Schiavon, Leonardo Warzea Lima, Ying Jiang, and Malcolm J. Hawkesford 16 O verview and Prospects of Selenium Phytoremediation Approaches . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 277 Karaj S. Dhillon and Gary S. Bañuelos Index . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 323

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This book covers many facets of plant selenium (Se) accumulation: molecular genetics, biochemistry, physiology, and ecological and evolutionary aspects. Broader impacts and applications of plant Se accumulation also receive attention. Plant Se accumulation is very relevant for environmental and huma
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