Environmental Plant Physiology Taylor & Francis Taylor & Francis Group http://taylorandfrancis.com Environmental Plant Physiology Neil Willey GS Garland Science Taylor & Francis Group NEW YORK LONDON Vice President: Denise Schanck Assistant Editor: David Borrowdale Production Editor: Georgina Lucas Illustrators: Neil Willey and Nigel Orme Layout: Georgina Lucas Cover Designer: Andrew Magee Copy Editor: Josephine Hargreaves Proofreader: Sally Livitt Indexer: Bill Johncocks © 2016 by Garland Science, Taylor & Francis Group, LLC Neil Willey is Reader in Environmental Plant Physiology at the University of the West of England (UWE), Bristol, UK. He holds a BSc (Hons) in Biology & Geography and a PhD in Botany, both from the University of Bristol, UK. He’s an active teacher of plant biology to undergraduate and postgraduate students from a variety of disciplines. His research focuses on the behavior and effects of pollutants, especially radioisotopes, in the soil-plant system. He’s the Director of the UWE Graduate School and the Chair of the UK Coordinating Group for Environmental Radioactivity. Front Cover. Close-up of Rhododendron flower. This book contains information obtained from authentic and highly regarded sources. Every effort has been made to trace copyright holders and to obtain their permission for the use of copyright material. Reprinted material is quoted with permission, and sources are indicated. A wide variety of references are listed. Reasonable efforts have been made to publish reliable data and information, but the author and the publisher cannot assume responsibility for the validity of all materials or for the consequences of their use. All rights reserved. No part of this publication may be reproduced, stored in a retrieval system or transmitted in any form or by any means—graphic, electronic, or mechanical, including photocopying, recording, taping, or information storage and retrieval systems—without permission of the copyright holder. ISBN 978-0-8153-4469-8 Library of Congress Cataloging-in-Publication Data Names: Willey, Neil, author.. Title: Environmental plant physiology / Neil Willey. Description: New York, NY : Garland Science, 2016. Identifiers: LCCN 2015039662 | ISBN 9780815344698 (alk. paper) Subjects: LCSH: Plant ecophysiology. Classification: LCC QK717 .W55 2016 | DDC 571.2--dc23 LC record available at http://lccn.loc.gov/2015039662 Published by Garland Science, Taylor & Francis Group, LLC, an informa business, 711 Third Avenue, New York, NY, 10017, USA, and 3 Park Square, Milton Park, Abingdon, OX14 4RN, UK. Printed in the United KIngdom 15 14 13 12 11 10 9 8 7 6 5 4 3 2 1 Garland Science GS Taylor & Francis Group Visit our website at http://www.garlandscience.com Preface Environmental plant physiology focuses on the foundations of life on land, with direct implications for the possibility of humans inhabiting Earth sustainably. I hope that readers of this book will gain an understanding of the importance of plant–environment interactions and be inspired to help humanity face some of its major challenges—in particular, global food security and the conservation of the natural world. This book is intended for upper-level undergraduate and graduate students, but will also be use- ful to some researchers. Several excellent textbooks inspired my interest in plant–environment interactions, but so significant are recent scientific advances that I felt a new textbook was needed. Its approach is intended to be useful across the biological, environmental, and agricultural sciences. In an era in which science is progressively focusing on the major challenges facing humanity, the ability to engage with a topic using both disciplinary and trans-disciplinary perspectives is increasingly important. In this book my aim is to provide a synthesis that is useful to individual biological, envi- ronmental, and agricultural disciplines, whilst also providing a framework for understanding across them all. As is evident from the structure of the book, I think that a useful contem- porary understanding of environmental plant physiology can be built by focusing on environmental variables, each of which is important to the bio- logical, environmental, and agricultural sciences. These environmental vari- ables are grouped into ‘resources’, ‘stressors’, and ‘xenobiotics’ according to whether they help synthesize biomass, limit biomass production, or poison plants. Each chapter is structured to focus on plant responses to progres- sively more profound variation in the environmental variable. This is used to suggest a hierarchy of responses from molecular to ecological scales in each chapter, and then as an overall framework in the final chapter. Throughout, examples are drawn from both unmanaged and managed ecosystems, and the importance of evolutionary history is acknowledged whenever possible to help to explain the occurrence of adaptations. In each chapter the text is enhanced by large boxes that include additional stories of interest, small boxes in the margins that elucidate some key points, and by tables and figures. In particular, I have made an effort to provide a new set of figures for understanding environmental plant physiology. Further read ing and references for each section are listed at the end of each chapter, and all bold terms are defined in the glossary. The book is complemented by resources available to students online: the glossary and flashcards; image gallery of the key species discussed in the text as indicated in bold green font; audio files that provide a commentary for each topic; and a set of multiple- choice questions. For instructors, all of the figures from the book are available to download in both PowerPoint® and JPEG format. Overall, this textbook provides a heuristic framework that enables students, in the midst of the torrent of information published in scientific journals, not only to think about guiding principles and concepts in environmental plant physiology, but also to form their own perspectives. I would be interested in any feedback from anyone (contact me at [email protected]). vi PREFACE Acknowledgments I am very grateful to the students who have taken my courses; the discus- sion that their interest stimulates has been vital to developing this book. I would also like to express my appreciation for the very helpful comments of colleagues and reviewers. Many thanks to staff from Garland Science: Dave Borrowdale for steering the project from beginning to end, Gina Almond for her role in getting it off the ground, and Georgina Lucas for all her efforts during the publication process. And finally, particular thanks must go to Lorna and the rest of my family without whose support this book, and much else, would never have happened. Neil Willey Reviewers Habib-ur-Rehman Athar (Bahauddin Zakariya University); Juergen Burkhardt (University of Bonn); Ivan Couée (University of Rennes); Peter S. Curtis (The Ohio State University); Stephen Ebbs (Southern Illinois University); David E. Evans (Oxford Brookes University); Ros Gleadow (Monash University); Kevin Griffin (Columbia University); Stuart Lane (Plymouth University); Richard Leegood (University of Sheffield); Denis Murphy (University of South Wales); Bob Nowak (University of Nevada, Reno); Léon-Etienne Parent (Université Laval); David Tissue (University of Western Sydney); Alyson Tobin (University of St Andrews); Marcos Yanniccari (CONICET, Universidad Nacional de La Plata); Jianhua Zhu (University of Maryland). vii Contents Chapter 1 Contexts, Perspectives, Leaf optical properties are adapted to long-term and Principles 1 variation in light regimes 41 Adjustments in leaf position and plant architecture Plant interactions with the atmosphere, hydrosphere, adapt plants to different light regimes 44 and geosphere underpin terrestrial ecosystems 1 Photoinhibition is most severe in alpine Minimizing human impact on ecosystems and environments 46 achieving global food security are significant challenges 3 Summary 48 Proximate and ultimate questions elucidate how and Further reading 49 why plants interact with the environment 5 Resources, stressors, and toxins affect plant biomass Chapter 3 Carbon Dioxide 51 production and quality 6 Environmental factors that affect plant growth are CO2 fixation underpins the primary production of  interacting but independent variables 10 biomass 51 Many reference soil groups are a product of Variation in the supply of CO2 to plants is significant interacting environmental variables 10 and affected by human activity 53 Spatial and temporal analyses provide insights into The regulation of rubisco activity controls CO2 entry into the Calvin–Benson cycle 56 plant responses to environmental variation 11 Oxygenation of RuBP decreases growth but provides Plants process information about environmental rapid metabolic flexibility 58 variation using signaling networks 14 When there is a sustained low CO supply, C Differences in gene expression and in the genes 2 4 plants maintain a high CO :O ratio in the vicinity expressed underpin a hierarchy of plant adaptations 14 2 2 of rubisco 60 Environmental plant physiology is ecologically useful C –C intermediates and C plants show distinct in defining plant traits and niches 19 3 4 4 responses to chronic differences in the Studying plant–environment interactions can help to environment 63 increase agricultural efficiency and sustainability 20 Crassulacean acid metabolism adapts plants to Modeling is improving our understanding of plant– chronically difficult CO -fixation conditions 66 environment interactions 21 2 Long-term increased CO levels can increase Summary 21 2 plant growth, but limiting factors can moderate Further reading 22 this effect 69 Plant responses to increasing CO levels will affect 2 the hydrological cycle and Earth’s climate 72 Chapter 2 Light 23 An understanding of CO fixation by plants is 2 In plants, ancient photosynthetic systems provide important for sustainable food production and the chemical energy for terrestrial ecosystems 23 ecosystem conservation 73 Photosystems, cytochromes, and ATP synthases Summary 75 transduce light energy into chemical energy 25 Further reading 75 Terrestrial plants have to adapt to a generally high and very variable light regime 28 Plants can adjust quickly to variation in PAR using Chapter 4 Water 77 non-photochemical quenching 31 Plant–water relations affect physiological processes Plants can adjust electron flows to help them to from a cellular to a global scale 77 withstand variable light intensities 34 Water management is vital for ensuring global food PSII repair is important in plants that tolerate high security and minimizing the impact of human light intensities 36 activity on the environment 80 Chloroplast movements can be used to adjust fairly Water potential gradients drive water movement, rapidly the amount of light absorbed 37 including transpiration in trees over 100 m tall 83 Photosystems, grana, and thylakoids adapt to Short-term adjustments of resistance to water flux differences in light regime 39 allow water homeostasis 85 viii CONTENTS Many plants adapt physiologically to short-term Mycorrhizas are major adaptations for phosphorus water deficit 88 acquisition in low-phosphorus environments 142 Extended water deficit induces changes in Some species use cluster root systems to root growth 90 intensively mine phosphorus from the soil 146 Leaf adaptations aid drought survival and provide Carnivorous plants digest organic phosphorus alternative ways of capturing water 92 using phosphatases 150 Succulent xerophytes are physiologically Summary 150 decoupled from their chronically arid environments 94 Further reading 151 Resurrection plants cope with complete desiccation 95 Interactions between water and other stressors Chapter 7 Essential and provide important environmental insights 99 Beneficial Elements 153 Summary 100 Further reading 101 Terrestrial plants evolved to mine the soil for an ancient suite of available elements 153 The availability of essential nutrients limits Chapter 5 Nitrogen 103 biomass production and quality in many ecosystems 156 Nitrogen assimilated in plants is vital for the production of biomolecules in terrestrial organisms 103 Elemental homeostasis is achieved using both ion-binding compounds and transport proteins 157 Artificially fixed nitrogen significantly affects the biosphere and atmosphere 104 Plants adjust to a variable supply of micronutrients by overexpressing homeostatic The concentration of different forms of soil components 159 nitrogen varies significantly 107 Beneficial elements help many plant species to Plant nitrogen-transporter uptake capacity is cope with a wide range of abiotic stresses 160 tuned to variation in soil nitrogen supply 111 Sub-optimal sulfur availability can inhibit the Plants integrate nitrogen from different sources by synthesis of ecophysiologically important converting it to NH for assimilation 113 3 compounds 162 Whole-plant physiological adjustments help to use Potassium can limit ecosystem production, but  different patterns of nitrogen supply 115 its use in fertilizer has a moderate environmental Plants adjust their root morphology in response to impact 164 shortages of nitrogen 116 Calcium deficiency can occur in a variety of Symbioses contribute significantly to plant plants, and magnesium deficiency in a variety nitrogen uptake in nitrogen-deficient environments 117 of crops 166 Carnivorous plants are mixotrophs that can Adaptations of root anatomy and morphology obtain nitrogen opportunistically from an erratic help plants to respond to chronic nutrient supply 123 deficiency 168 Summary 126 Many plants use symbioses with fungi and Further reading 127 changes in rhizosphere microflora to aid nutrient uptake 170 Ionomics 171 Chapter 6 Phosphorus 129 Summary 173 Phosphorus availability often controls terrestrial Further reading 174 biomass production and ecosystem processes 129 Current phosphorus fertilizer regimes are unsustainable, inefficient, and often polluting 131 Chapter 8 Temperature 175 Phosphorus homeostasis is a key challenge for Plants are static poikilotherms, so significant plants in terrestrial ecosystems 133 variation in temperature is a considerable Plants have numerous transporters that regulate challenge 175 uptake and translocation 135 Changing global temperature regimes are affecting Plants can increase the availability of inorganic plant growth, development, and distribution 177 phosphorus and the breakdown of organic Plants detect temperature changes via physical phosphorus 136 changes in numerous biomolecules 180 Plants can adjust their root system morphology Chilling, freezing, and heat initiate changes in key to optimize phosphorus uptake 140 components of different signaling pathways 183 CONTENTS ix In some plants, chilling temperatures can induce Plant cells have multiple mechanisms for buffering an acclimation response based on the CBF regulon 184 cytosolic pH 233 Adaptation to non-optimal temperature Acid soils contain high solution concentrations necessitates maintaining membranes in the of ions that are toxic to plant cells 234 liquid–crystal state 186 Some plants resist the effects of moderate soil Freezing-tolerant plants produce cryoprotectants acidity by excluding aluminum from the and osmoprotectants 188 cytoplasm 237 Heat-tolerant plants have protein curation For many plants on acid soils, mycorrhizal mechanisms adapted to increase the rate of associations increase aluminum resistance 240 protein repair 191 On very acidic soils, some plants take up and Anatomical and morphological adaptations of compartmentalize aluminum 241 leaves aid plant tolerance of prolonged cold Basic soils are low in important nutrients and and heat 194 induce characteristic symptoms in plants 243 Temperature-induced physiological changes trigger Some plants have adapted to scavenge iron, zinc, developmental and phenological responses 198 and manganese from basic soils 246 Summary 199 Nicotianamine aids iron homeostasis, and in Further reading 199 grasses evolved into root exudates that chelate iron 247 Ecologically important iron and zinc deficiency responses are finding important agricultural uses 249 Chapter 9 Salinity 201 Summary 250 Terrestrial plants are descended from freshwater Further reading 251 algae, so saline water is generally toxic to them 201 Plant responses to salinity are important in irrigated agriculture and in salt marshes and Chapter 11 Flooding 253 mangrove swamps 204 Flooding is a significant variable in both Exposure to salt induces osmotic and ionic unmanaged and managed terrestrial ecosystems 253 stresses in plants 208 Human activity is adversely affecting wetlands Sodium can enter plants via symplastic and and increasing the incidence of flooding 255 apoplastic pathways, but can be removed from Waterlogged soils are low in oxygen and some the cytoplasm 211 nutrients, but high in toxins 255 Salt-tolerant plants compartmentalize sodium, Soil waterlogging rapidly induces hypoxia, and halophytes also control potassium:sodium cellular acidosis, and decreased water uptake 258 ratios 213 Physiological adjustments enable some plants to At high salinity, halophytes synthesize withstand soil waterlogging for short periods 259 specialized metabolites in order to adapt to osmotic challenges 215 Ethylene signaling is central to plant responses to excess water 261 Salt tolerance in crops has been increased by manipulating biochemical and physiological In many plants, waterlogging-induced hypoxia traits 217 induces changes in root anatomy 262 Halophytes that face severe osmotic stresses have Wetland plants form extensive constitutive morphological and physiological adaptations 219 aerenchyma and adapt morphologically to flooding 266 Some halophytes use specialized organs to excrete sodium chloride from their leaves 221 In some flooded soils, pneumatophores help woody plants to aerate their roots 268 Mangrove and salt-marsh plants tolerate waterlogging and salinity 223 The adaptations of wetland plants often produce oxidized rhizospheres 269 Summary 224 Some plants can adapt to submergence of their  Further reading 225 shoots 271 Emergent aquatic macrophytes can force oxygen Chapter 10 Soil pH 227 down through organs buried deep in anoxic mud 273 Some aquatic macrophytes are adapted to living Soil pH affects the growth of both wild and permanently submerged 275 domesticated plants 227 Summary 275 Soil pH is operationally defined and human activities are affecting it on a global scale 229 Further reading 276