Plant Roots Growth, Activity and Interaction with Soils Peter J Gregory Director, Scottish Crop Research Institute, Invergowrie, Dundee Visiting Professor of Soil Science, University of Reading 1405119063_1_pretoc.indd i 18/01/2006 12:49:38 © 2006 Peter Gregory Editorial Offices: Blackwell Publishing Ltd, 9600 Garsington Road, Oxford OX4 2DQ, UK Tel: +44 (0)1865 776868 Blackwell Publishing Professional, 2121 State Avenue, Ames, Iowa 50014-8300, USA Tel: +1 515 292 0140 Blackwell Publishing Asia, 550 Swanston Street, Carlton, Victoria 3053, Australia Tel: +61 (0)3 8359 1011 The right of the Author to be identified as the Author of this Work has been asserted in accordance with the Copyright, Designs and Patents Act 1988 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, electronic, mechanical, photocopying, recording or otherwise, except as permitted by the UK Copyright, Designs and Patents Act 1988, without the prior permission of the publisher First published 2006 by Blackwell Publishing Ltd ISBN-10: 1-4051-1906-3 ISBN-13: 978-1-4051-1906-1 Library of Congress Cataloging-in-Publication Data Gregory, P J Plant roots : their growth, activity, and interaction with soils / Peter J Gregory p cm Includes bibliographical references and index ISBN-13: 978-1-4051-1906-1 (hardback : alk paper) ISBN-10: 1-4051-1906-3 (hardback : alk paper) Roots (Botany) I Title QK644.G74 2006 575.5’4 dc22 2005025239 A catalogue record for this title is available from the British Library Set in Times 10/12.5 pt by Sparks Computer Solutions Ltd, Oxford – www.sparks.co.uk Printed and bound in India by Replika Press Pvt Ltd, Kundli The publisher’s policy is to use permanent paper from mills that operate a sustainable forestry policy, and which has been manufactured from pulp processed using acid-free and elementary chlorine-free practices Furthermore, the publisher ensures that the text paper and cover board used have met acceptable environmental accreditation standards For further information on Blackwell Publishing, visit our website: www.blackwellpublishing.com 1405119063_1_pretoc.indd ii 24/01/2006 13:07:28 To Jane, Tom and George ‘What greater stupidity can be imagined than that of calling jewels, silver and gold “precious”, and earth and soil “base”? People who this ought to remember that if there were as great a scarcity of soil as of jewels or precious metals, there would not be a prince who would not spend a bushel of diamonds and rubies and a cartload of gold just to have enough earth to plant a jasmine in a little pot, or to sow an orange seed and watch it sprout, grow, and produce its handsome leaves, its fragrant flowers and fine fruit.’ Dialogue on the Two Chief World Systems: Ptolemaic and Copernican, Galileo 1405119063_1_pretoc.indd iii 18/01/2006 12:51:29 Contents Preface ix Plants, Roots and the Soil 1.1 The evolution of roots 1.2 Functional interdependence of roots and shoots 1.2.1 Balanced growth of roots and shoots 1.2.2 Communication between roots and shoots 1.3 Roots and the soil 1.3.1 The root–soil interface 1.3.2 Root-induced soil processes Roots and the Architecture of Root Systems 2.1 Nomenclature and types of root 2.2 Root structure 2.2.1 Primary structure 2.2.2 Secondary structure 2.3 Extension and branching 2.3.1 Extension 2.3.2 Branching 2.3.3 Root hairs 2.4 The root tip 2.4.1 The root cap and border cells 2.4.2 Mucilage 2.5 Architecture of root systems Development and Growth of Root Systems 3.1 Measurement of root systems 3.1.1 Washed soil cores 3.1.2 Rhizotrons and minirhizotrons 3.1.3 Other techniques 5 10 10 13 18 18 21 22 25 26 26 28 29 32 32 34 37 45 45 45 49 52 v 1405119063_2_toc.indd v 17/01/2006 18:24:43 vi CO NTENTS 3.2 Root system development 3.3 Size and distribution of root systems 3.3.1 Mass and length 3.3.2 Depth of rooting 3.3.3 Distribution of roots 3.4 Root:shoot allocation of dry matter 3.5 Root longevity and turnover 3.6 Modelling of root systems The Functioning Root System 4.1 Root anchorage 4.1.1 Uprooting 4.1.2 Overturning 4.2 Water uptake 4.2.1 The concept of water potential 4.2.2 The soil–plant–atmosphere continuum 4.2.3 Water uptake by plant root systems 4.3 Nutrient uptake 4.3.1 Nutrient requirements of plants and the availability of nutrients 4.3.2 Nutrient movement in soil solution 4.3.3 Nutrient uptake and movement across the root 4.3.4 Nutrient uptake by root systems 52 54 54 59 61 64 65 68 80 80 81 84 89 90 91 103 108 108 109 113 118 Roots and the Physico-Chemical Environment 131 5.1 Temperature 5.1.1 Root development and growth 5.1.2 Root orientation 5.1.3 Other root functions 5.2 Gravity and other tropistic responses 5.2.1 Gravisensing and the response of roots 5.2.2 Phototropism, hydrotropism and thigmotropism 5.3 Soil mechanical properties 5.3.1 Root elongation and mechanical impedance 5.3.2 Root responses to mechanical impedance 5.3.3 Roots and soil structure 5.4 Soil pores and their contents 5.4.1 Soil water 5.4.2 Soil aeration 5.4.3 Waterlogging and aerenchyma 5.5 The soil chemical environment 5.5.1 Plant nutrients 5.5.2 Low pH and aluminium 5.5.3 Salinity 5.6 Atmospheric CO2 concentration 131 132 136 137 137 138 139 142 143 145 149 149 150 152 153 156 156 161 163 164 1405119063_2_toc.indd vi 17/01/2006 18:26:36 CONTENTS Roots and the Biological Environment 6.1 Interactions of roots with soil organisms 6.1.1 Root–rhizosphere communication 6.1.2 Interactions with bacteria 6.1.3 Interactions with fungi 6.1.4 Interactions with protozoa 6.1.5 Interactions with nematodes and mesofauna 6.2 Symbiotic associations 6.2.1 Rhizobia and N fixation 6.2.2 Mycorrhizas 6.3 Root pathogens and parasitic associations 6.3.1 Fungal diseases 6.3.2 Nematodes 6.3.3 Parasitic weeds 6.4 Root herbivory by insects The Rhizosphere vii 174 174 174 177 182 182 183 185 185 189 201 201 202 205 209 216 7.1 Rhizodeposition 7.1.1 Quantities of rhizodeposits 7.1.2 Composition of rhizodeposits 7.1.3 Nitrogen rhizodeposits 7.2 Chemical changes affecting nutrient acquisition 7.2.1 Rhizosolution composition and replenishment 7.2.2 Changes in pH 7.2.3 Changes in redox conditions 7.2.4 Root exudates and phytosiderophores 7.2.5 Enzyme activity 7.3 Physical changes in the rhizosphere 7.3.1 Bulk density and porosity 7.3.2 Water 216 217 220 221 222 223 227 238 241 243 244 244 246 Genetic Control of Root System Properties 253 8.1 Genotypic differences in root systems 8.1.1 Size and architecture 8.1.2 Functional properties 8.2 Genetics of root systems 8.2.1 Genetic control of root development and growth 8.2.2 Genetic control of root properties 8.3 Breeding better root systems 8.3.1 Use of markers and QTL 1405119063_2_toc.indd vii 253 254 260 267 267 271 275 277 17/01/2006 18:26:36 viii CO NTENTS Root Systems as Management Tools 9.1 Optimal root systems and competition for resources 9.2 Intercropping and agroforestry 9.3 Crop rotations 9.3.1 Biological drilling 9.3.2 Utilization of subsoil water 9.3.3 Allelopathy 9.3.4 Biofumigation by brassicas 9.4 Phytoremediation Index 1405119063_2_toc.indd viii 286 286 288 296 297 298 300 302 304 309 17/01/2006 18:26:36 Preface Since about the age of ten, I have been fascinated by plants and their use for decoration as flowers, and for food Much of my pocket money as a child came from the sale of plants and flowers and I quickly learned the practical benefits to be gained from controlling soil fertility in the garden and from good quality potting media in the glasshouse It was this interest in plants, together with the misery of the famine in India during my teenage years, which led me to study soil science at the University of Reading, although my interest in plants was temporarily put on hold as much of my degree was essentially chemistry For my PhD at Nottingham University, I was able to choose a topic that interested me, and after a false start on the kinetics of phosphate adsorption by soil minerals, I came across two papers in the library, one by Glyn Bowen and Albert Rovira, and the other by Howard Taylor and Betty Klepper, which enthused me with the possibility of combining my interests in plants and soils by studying roots and their interactions with soil I quickly found that roots in soil were difficult to study, not least because they cannot be seen, but the satisfaction of patient discovery was considerable The early encouragement in this endeavour by my supervisors David Crawford and Mike McGowan was essential, as was that of those who eventually became co-workers and colleagues, John Monteith, Paul Biscoe and Nick Gallagher Much of my professional career has been spent at the University of Reading where I was allowed the freedom by Alan Wild to continue and build my studies on root:soil interactions Projects in the UK and overseas followed, and with a succession of PhD students and postdoctoral research workers I have been able to work on a wide range of crops and practical problems, all with a basis in the growth and activity of root systems When I started my work, the emphasis was on how various soil properties affect the plant and its ability to take up water and nutrients, but recently the emphasis has changed, as it has come to be appreciated that plant roots also change the properties of soils and are not merely passive respondents The idea for this book first came in a conversation with my friend Rod Summerfield but for various reasons, including a career change in Australia, it is only now that I have had the determination to bring the project to a conclusion In fact, I think it is a better book as a result because I believe that the recent development of techniques and the improved understanding of root:soil interactions make this a particularly exciting time to try and write such a book I have tried to draw together information from diverse elements of the plant and soil literatures to illustrate how roots interact with soil, both to modify it and to obtain ix 1405119063_3_posttoc.indd ix 19/01/2006 17:37:53 x PREFACE from it the resources required for the whole plant to grow My emphasis has been on whole plants and root systems, although I have drawn on the growing body of literature at plant molecular and cellular levels as appropriate A particular difficulty in the writing has been that roots of relatively few plant species have been studied and of these most are cereal crops such as maize and wheat This means that the desire to generalize findings as one might in an introductory undergraduate textbook has had to be tempered with an appreciation of the paucity of information I hope that I have been able to convey useful principles while at the same time indicating that plant species other than those studied might respond differently A second area of caution is that many studies in the plant literature have been conducted on young, seedling roots in solutions or in non-soil media Extrapolation of such findings to older plants, with roots of different anatomy, with fungal and bacterial associations, and with gradients of solutes and gases resulting from past activity, must be undertaken cautiously Finally, there has been until recently a tendency to regard all roots on a plant as anatomically similar and functionally equivalent; this notion is beginning to be challenged as results indicating particular arrangements of cell types and functional specialisms appear Measurements are few at present, but we may yet find that roots within a root system make particular contributions to the activities of the whole So, this is a personal view of the subject aimed at those who already have a background knowledge of soils and plants Besides those I have already mentioned, I should like to thank Christopher Mott, Bernard Tinker, Dennis Greenland, Peter Cooper, Lester Simmonds, Ann Hamblin, Neil Turner and Derek Read for sustaining my enthusiasm in root studies at various points in my career, and to thank Michelle Watt, Glyn Bengough, Margaret McCully, John Passioura, Rana Munns, Sarah Ellis, Steve Refshauge, Mark Peoples, Ulrike Mathesius, Sally Smith, Ken Killham, Philippe Hinsinger, Richard Richards, Greg Rebetzke, Tim George, Manny Delhaize, Wolfgang Spielmeyer and John Kirkegaard for reading and suggesting improvements to various parts of the manuscript I am very grateful to the University of Reading for giving me study leave to undertake this project, and to the Leverhulme Trust for a Study Abroad Fellowship that enabled me to spend a very productive period in Canberra, Australia As ever, CSIRO Division of Plant Industry, Australia provided a challenging academic environment in which to work (my thanks to the Chiefs Jim Peacock and Jeremy Burdon) and I am indebted to Carol Murray and her staff, especially Michelle Hearn, at the Black Mountain Library for helping me locate reference materials Finally, my thanks to my personal assistant, Tricia Allen, the staff of the ITS unit at the University of Reading and Ian Pitkethly at SCRI for help with the figures, and to Nigel Balmforth and the staff at Blackwell Publishing for seeing the manuscript through to publication Peter J Gregory 1405119063_3_posttoc.indd x 19/01/2006 17:39:30 31 I NDEX modelling 71–2 radial expansion 147 resistance 100 seminal 261, 262 temperature effects 133, 134 root cap 32–4 aluminium toxicity 162 gravity perception 138, 139 mucilage 33, 34–7 root hairs 29–30, 31, 32 allelochemicals 301, Plate 9.2 anchorage 83 curling 186, Plate 6.4 evolution nutrient uptake 121, 123 phosphorus uptake 265, 267 root systems breeding trials 275–7 competition 288–9 development 52–4 dry mass accumulation 55, 57 genetics 267–9, 270, 271–4, 275 genotypic differences 253–67 genotypic variation in size 254–60 measurement 45–52 modelling 68–73 nutrient uptake 118–24 optimal 286–8 separation of live/dead 48 size 286 spatial heterogeneity modelling 72–3 root tip 32–7 modelling of movement 72 soil deformation 142 soil structure 149 Root Typ model 72–3 root washing devices 46–7 ROOTEDGE software 48–9 rootlets, hairy 21 ROOTMAP model 72 root–rhizosphere communication 174–7 root:shoot ratio 5–7 root–soil cone 88, 89 root–soil interface 10–12 root–soil plate 85–6, 87 root:total plant mass ratio 64, 65 rotational torque 84 runoff 299 rye chromosome 1RS (1RS) 268–9 salinization 163–4, 299 1405119063_6_index.indd 316 salt tolerance 164 semi-permeable membranes 91 senescence 8–9 shared control hypothesis shear strength of soil 81, 85 shear stress 81 shoots balanced growth with roots 5–7 development 53–4 dry matter allocation 64 evolution 2, evolutionary sequence 4–5 growth modulation signalling long-distance 9–10 molecules 176 pathways in root–rhizosphere communication 174–5 signal-mimic compounds 177 sink term for water uptake 107–8 sinker roots 85, 86 Sitona lepidus 209–10, Plate 6.6 smectite 224, 225 sodium 109, 163–4 soil 10–15 aeration 152–3 aggregation 14–15 anaerobic 240 biodiversity 10 carbon dioxide levels 152, 165 chemical environment 156–64 chemical release 300–2 compaction 147, 148 depth for sinker roots 86 drought resistance 259 dry 150–1 duplex 297, 298, 299 formation 1, 13 heterogeneity 40, 72–3 hydraulic characteristics 246, 247 mechanical impedance 145, 146, 147–9 elongation 143, 144, 145 mechanical properties 142–3, 144, 145, 146, 147–9 nutrients accumulation 40 chemical environment 156–61 composition 109 concentration 110 distribution 157–8 movement 109–13 18/01/2006 17:02:31 INDEX oxygen level 152–3 pH 161–2 proliferation of roots in layers 69–70 properties in overturning 85 resistance to flow 95 root returns 1–2 root-induced processes 13–15 salinity 163–4 shear strength 81, 85 strength 145, 146, 147, 148, 149 structure 149 surface drying 150 temperature gradients 93–4 type and rooting depth 62–3 water content 106–7, 147, 150–2 crop reliance 298 seasonal variation 299, 300 tree–crop systems 292 water movement 93–4 waterlogging 153–6 weathering 297 wet 239–40 wetness zones 102 wetting/drying cycles 14–15 zinc 305 soil cores, washed 45–9, 51 soil organisms, root interactions 174–85 soil pores 142, 149–56 soil profile, amount of root length 63–4 soil samples 46 soil–plant–atmosphere continuum 91–103 solutes channels 114 co-transport/countertransport 114–15 efflux 118 transport and temperature effects 137 sorghum, allelopathy 300–1, Plate 9.2 sorgoleone 301, Plate 9.2 source–sink relationships, growth of roots 136 split root techniques 102 spread, lateral, radioisotope methods 52 statocytes 138 stem flexing 87–8 sterols 113 stomata 95–6, 100–2 storage roots 20 strengthening of roots 83–4 stress factors 70–1 Striga (witchweed) 206–8 structure of roots 21–5 suberin 22, 23, 24, 98 1405119063_6_index.indd 317 317 subsoil 297, 298–300, Plate 9.1 sustainability of production 288 symbiotic associations 185–93, 194, 195–7, 198, 199–201 symplast, nutrient transport pathway to xylem 113 synchrony hypothesis 294 take-all fungi 202, 302–3, Plate 6.5 tap root 18–19 anchorage 84–5 carbon dioxide atmospheric concentration 165 emergence 53 investment 84 temperature 131–7 carbon disoxide elevation combination 165 development of roots 132–6 gradients in soils 93–4 growth of roots 132–6 plagiotropism effects 136–7, Plate 5.1 response to 131–2 root turnover 67 solute transport 137 water transport 137 thickening, root 147, 148 drought resistance 256–8 thigmotropism 140–1, 142 tillers 53 tonoplast transport 304 topology of roots 39–40, 53 touch effects 140–1, 142 trait heritability 276–7 transpiration 95, 102–3, 110, 299 transport proteins 113–14, 115, 116 tree roots crop root systems 289–92, 293 length 291–2, 293, 296–7 lifespan 67 longevity 66 nitrogen capture 294 plate system 85–6 stability 85–8 trees agroforestry systems 289–92, 293 biomass 296–7 crop interactions 292 nutrient interception 295–6 root length 291–2, 293 trench-profile technique 52 trichoblasts 29, 30, 31 18/01/2006 17:02:31 31 I NDEX turgor pressure 26, 143, 144 turnover of roots 65–8 uprooting 81, 82, 83–4 ureide exporters 188 vascular plant characteristics vascular tissue 24–5 vermiculite 224, 225 vitamins 176 wall pressure 143, 145 walnut, black 301 water atmospheric evaporative demand 106 content in soil 106–7, 147, 150–2 crop reliance 298 seasonal variation 299, 300 tree–crop systems 292 demand for 289 diffusivity 93 extraction patterns 106, 255 flow 92–103 hydrotropism 140 rhizosphere 246–7 soil pores 149–52 soil resistance to flow 95 subsoil 298–300 supply determination 255 temperature gradients in soils 93–4 transfer from soil to plant to atmosphere 91–103 transport 137 use and depth of rooting 103 volumetric soil content 106–7 water balance changes 299 water movement in root 95 from root to leaf 99–100 1405119063_6_index.indd 318 from root xylem to stomata 100–2 in soil 93–4 from soil layer to soil layer via roots 102–3 from soil to root 94–5 water potential 90–1 gradients 92, 93 water stress 278 water supply, mucilage role 36 water uptake 89–108 modelling 105–8 plant root systems 103–8 single root model 105–6 sink term 107–8 water vapour 94, 95–6 waterlogging 153–6, 262–3 water-table change 299 weathering 13 weeds allelochemicals 302 parasitic 205–9 wind force 84 witchweed 206–8 X-ray micro-tomography 52 xylanase 203 xylem 24–5 cavitation 100 conductance 100 embolism 100 hydraulic resistance 99–100 nutrients 113–14, 118 sap pH 101 vessel diameter 262 water movement to stomata 100–2 zinc phytosiderophore complex 243 soil level 305 zone of influence of plants 287 18/01/2006 17:02:31 Plant Roots: Growth, Activity and Interaction with Soils Peter J Gregory Copyright © 2006 Peter Gregory (a) (b) (c) (d) Plate 2.1 Different types of root: (a) aerial roots of the banyan tree (Ficus macrophylla ssp columnaris); (b) aerial roots of the orchid Ascocenda cv Heda; (c) air roots and stilt roots of the grey mangrove tree (Avicennia marina); and (d) cluster roots of white lupin (Lupinus albus) grown in nutrient solution in the absence of P; the bar is mm (I am grateful to Dr M Watt for this photograph.) Plate 2.2 Transverse section of a lateral root of maize taken at about mm from a tip that is becoming determi- nate The endodermis is mature and the developing hypodermis is already strongly suberized on the anticlinal and outer tangential walls The epidermis with root hairs is intact (Reproduced with permission from McCully, Plant Physiology; American Society of Plant Biologists, 1995.) 1405119063_8_plates.indd 17/01/2006 17:43:42 Plate 2.3 Root development in a herbaceous, woody plant showing (a) the primary meristems; (b) the completion of primary root development; (c) the commencement of secondary development with the appearance of vascular cambium; (d) after formation of some secondary phloem and additional secondary xylem; (e) the formation of additional secondary xylem, the appearance of the periderm and the sloughing off of the cortex and epidermis; and (f) the conclusion of secondary development In (d) to (f), the radiating lines represent rays (Based on, and reproduced with permission from Esau, Anatomy of Seed Plants; John Wiley & Sons Inc., 1977.) 1405119063_8_plates.indd 17/01/2006 17:45:52 Plate 2.4 Transverse section of a young root of northern catalpa (Catalpa speciosa) The considerable secondary growth has displaced the endodermis which has remained intact by new anticlinal divisions A periderm is forming from cortical cells (I am grateful to Dr M McCully for this previously unpublished figure.) (a) (b) Plate 2.5 Early stages of lateral root growth (a) An Arabidopsis lateral root emerging through the cortical and epidermal cell layers of the main root axis Note the buckling of the epidermal cells and gaps in the root surface The cell walls have been stained red with the fluorochrome propidium iodide, and the green lateral shows phloem unloading of green fluorescent protein (GFP) expressed in response to a sucrose transporter (I am grateful to Kath Wright, SCRI, Dundee, for this previously unpublished image.) (b) Junction of a young lateral root of field-grown maize with the root axis In this example, the cortex, hypodermis and epidermis of the root axis press against the lateral to make a tight seal The large, immature late metaxylem in the lateral adjoins phloem in the root axis and a bed of connecting xylem is developing in the stele of the root axis (Reproduced with permission from McCully, Plant Physiology; American Society of Plant Biologists, 1995.) 1405119063_8_plates.indd 17/01/2006 17:45:55 (a) (b) Plate 2.6 (a) Longitudinal section of a P-deficient nodal root of barley showing red biorefringence of GUS crystals indicating activity of the Pht1 phosphate transporter gene in the root hairs (b) Transverse section of a P-deficient nodal root of barley showing GFP expression in green indicating activity of the Pht1 phosphate transporter gene in the root hairs (Reproduced with permission from Schünmann et al., Journal of Experimental Botany; Oxford University Press, 2004.) Plate 2.7 Living root cap cells and mucilage on the flanks of a field-grown maize root The root was sectioned longitudinally and stained with neutral red Living root cap cells have accumulated this vital stain and mucilage has expanded in the aqueous solution The dark material is soil (I am grateful to Dr M McCully for this previously unpublished figure.) Plate 3.1 A global map of the percentage of root biomass found in the upper 0.3 m of soil (Reproduced with permission from Jackson et al., Oecologia; Springer Science and Business Media, 1996.) 1405119063_8_plates.indd 17/01/2006 17:45:59 Plate 4.1 Factors influencing the formation and intensity of the ABA long-distance signal On the left side, plant water shortage is illustrated, while on the right, the plant is well supplied with water The numbering indicates the number of factors involved (Reproduced with permission from Sauter et al., Journal of Experimental Botany; Oxford University Press, 2001.) (a) (b) Plate 5.1 Zones of the Arabidopsis thaliana root tip involved in early phases of gravitropism (a) Confocal image of a propidium iodide-stained root tip showing the root cap (RC), the promeristem (PM), and the distal elongation zone (DEZ) The root cap comprises three layers of columellar cells at the centre (L1, L2 and L3), lateral cells (LC), and tip cells (TC) (b) Confocal image of a propidium iodide-stained gravistimulated root tip showing the site of gravity sensing (columella of the root cap – outlined in blue and marked by a blue star), and the site of graviresponse (the DEZ marked with a lightning sign) The green arrow illustrates the need for signal transmission between the root cap and the elongation zone The gravity vector (g) is represented by a white arrow (Reproduced with permission from Boonsirichai et al., Annual Review of Plant Biology; Annual Reviews, 2002.) 1405119063_8_plates.indd 17/01/2006 17:46:04 (a) (b) Plate 5.2 The ‘fountain’ model of auxin transport in roots Auxin mainly synthesized in young shoot tissues is transported via the vasculature to the young root tip where it is redistributed to more peripheral tissues It is then transported basipetally to the elongation zone where it regulates cell expansion (a) When a root grows vertically downward, auxin redistribution to the outer tissues is symmetrical (b) On gravistimulation, auxin is preferentially transported toward the bottom side of the tip resulting in the formation of a lateral auxin gradient; this gradient is then transmitted to the elongation zone where it is partly responsible for the differential growth that underlies gravitropic curvature Green arrows represent the direction of auxin transport (width is a relative representation of auxin fluxes), and white arrows represent the gravity vector (g) (Reproduced with permission from Boonsirichai et al., Annual Review of Plant Biology; Annual Reviews, 2002.) Plate 5.3 Transverse section of 4-day-old maize nodal roots: (a) well-oxygenated root lacking aerenchyma; (b) hypoxic root with lysigenous aerenchyma in the mid cortex; (c) well-oxygenated root treated for days with okadaic acid, an inhibitor of protein phosphatases, with aerenchyma beginning to form; and (d) hypoxic root treated for days with EGTA to complex Ca2+, thereby eliminating aerenchyma formation Scale bars: 0.25mm (Reproduced with permission from Drew et al., Trends in Plant Science; Elsevier, 2000.) 1405119063_8_plates.indd 17/01/2006 17:46:08 Plate 6.1 Spatial and temporal overlaps and differences in the accumulation of plant compounds induced in response to nodule-inducing rhizobia, plant signals which induce lateral roots, and gall-inducing nematodes This model suggests that by varying the cell specificity of responses, a plant can form different organs even though the same genes and physiological changes are involved in all cases (A) The plant perceives a signal from rhizobia (symbolized by curled root hair), from the pericycle (cells from which lateral roots are derived) or from an invading nematode (black worm inside root) (B) Target cells in the cortex which later divide accumulate flavonoid in their vacuoles (C) Cortex cells targeted for division accumulate auxin probably because flavonoid inhibits auxin breakdown (D) After division of cells in the forming primordium, a different flavonoid (formononetin) accumulates which stimulates auxin breakdown The auxin promoter is no longer active (Reproduced with permission from Mathesius, Plant and Soil, Springer Science and Business Media, 2003.) 1405119063_8_plates.indd 17/01/2006 17:46:10 Plate 6.2 Fast-growing (A and C) and slow-growing (B and D) nodal roots of field-grown wheat (cv Janz) A and B are whole mounts of root apices (bar = 250 µm) The elongation zone is white on the fast-growing root (A), and short and distorted on the slow-growing root (B) C and D are tangential hand sections from approximately mm from the root tip of both root types, stained with PAS reaction and DAPI, and excited with UV epifluorescence to observe bacteria in situ Few bacteria are visible on the fast-growing root (C, bar = 20 µm), while many bacteria (bright spots, some indicated by an arrow) are visible on the slow-growing root (D, bar = 40 µm) E = epidermis, n = nucleus, and rh = root hair (Reproduced with permission from Watt et al., Functional Plant Biology; CSIRO Publishing, 2003.) Plate 6.3 The rhizobium infection process (A) Symbiotic rhizobial bacteria release Nod factors that are per- ceived by two transmembrane receptors initiating rapid calcium influx and swelling of root hair tips Simultaneous activation of the NORK/DMI complex results in plant responses to both bacterial and fungal symbionts (B) Rhizobial bacteria entrapped in a curling root hair For rhizobia to enter the root hair and to initiate formation of infection threads and nodulation, the Nod factors must be recognized by highly specific plant receptors (e.g LYK and LYK 4) (C) The chemical domains of some receptors (Reproduced with permission from Cullimore and Dénarié, Science; illustration by Katharine Sutliff, Copyright AAAS, 2003.) 1405119063_8_plates.indd 17/01/2006 17:46:15 Plate 6.4 Colonization of host cells by rhizobia causes root hair curling (left figure) and the formation of an infection thread (indicated by arrow) which originates as an intrusion of the host cell wall and propagates from cell to cell as a transcellular tunnel in the root cortex (right figure) (Reproduced with permission from Brewin, Biologist; Institute of Biology, 2002.) (A) (B) (C) (D) Plate 6.5 Take-all of wheat caused by Gaeumannomyces graminis var tritici (A) Stem base covered by black mycelium and showing blackened roots and internal mottled black and grey tissue (B) Pigmented runner hyphae on the surface of a fine root (C) Take-all suppression in one field by transfer of soil from another field that had undergone take-all decline (right) compared with the unamended soil (left) or soil transferred from a non-cropped site near the cropped site (centre) (D) Take-all in cv Madsen winter wheat (far left) and Penawawa spring wheat (far right) compared to two collections of Dasapyrum villosum (centre).(Reproduced with permission from Cook, Physiological and Molecular Plant Pathology; Elsevier, 2003.) 1405119063_8_plates.indd 17/01/2006 17:46:24 a b c d Plate 6.6 X-ray tomographic images of the sequential movement of a neonatal Sitona lepidus larva through soil towards the lower clover root nodule Location at (a) h, (b) h, (c) h, and (d) h The larva was subsequently recovered from the nodule when the column was dismantled; white bar = 10 mm (Reproduced with permission from Johnson et al., Ecological Entomology; Blackwell Publishing, 2004.) Plate 7.1 Effects of N source and plant species on rhizosphere pH The soil was infiltrated with agar containing bromocresol purple (A) pH calibration standards; (B) split root experiment with maize which received 67 mg N kg–1 soil as either calcium nitrate (left) or ammonium sulphate (right); and (C) mixed culture of sorghum and chickpea supplied with 83 mg N kg–1 soil as calcium nitrate Bar represents 10 mm (Reproduced with permission from Marschner et al., Z Pflanzenernaehr Bodenk; Wiley-VCH Verlag GmbH, 1986.) 1405119063_8_plates.indd 10 17/01/2006 17:46:27 (a) (b) Plate 7.2 pH changes around roots (a) Changes in rhizosphere pH of a root axis and associated lateral roots of a 40-day-old maize plant growing in soil of pH 6.0 and supplied with 66 mg N kg–1 soil as calcium nitrate Colours/pH as for Plate 7.1 Bar represents 10 mm (Reproduced with permission from Marschner et al., Z Pflanzenernaehr Bodenk; Wiley-VCH Verlag GmbH, 1986.) (b) Map of pH values around the root of a 7-day-old maize seedling after embedding it in an agarose sheet containing bromocresol green at a pH of 4.6 for 120 minutes The apical region released hydroxyl equivalents while basal regions released protons (Original research by Jaillard et al (1996); reproduced with permission from Hinsinger, Advances in Agronomy; Elsevier, 1998.) (a) (b) Plate 7.3 Oxidation of iron around roots of rice (a) Roots embedded in 0.2% agar containing ferrous sulphate and sodium sulphide giving a black precipitate of ferrous sulphide which has been rendered clear by oxidation close to the root (b) Roots grown in sand with a ferrous sulphide nutrient medium (Reproduced with permission from Trolldenier, Z Pflanzenernaehr Bodenk; Wiley-VCH Verlag GmbH, 1988.) 1405119063_8_plates.indd 11 17/01/2006 17:46:31 Plate 9.1 A wheat root growing through the pore created by a lucerne root which is now decaying Plate 9.2 Sorghum root hairs exuding yellow drops of sorgleone (I am grateful to Leslie Weston for this previ- ously unpublished photograph.) 1405119063_8_plates.indd 12 17/01/2006 17:46:35 ... 17:39:30 Plant Roots: Growth, Activity and Interaction with Soils Peter J Gregory Copyright © 2006 Peter Gregory Chapter Plants, Roots and the Soil This book focuses on vascular plants and their interactions... CONTENTS Roots and the Biological Environment 6.1 Interactions of roots with soil organisms 6.1.1 Root–rhizosphere communication 6.1.2 Interactions with bacteria 6.1.3 Interactions with fungi 6.1.4 Interactions... Bowen and Albert Rovira, and the other by Howard Taylor and Betty Klepper, which enthused me with the possibility of combining my interests in plants and soils by studying roots and their interactions