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Functional Diversity of Mycorrhizaand Sustainable Agriculture

Goss-1611461 978-0-12-804244-1 00009


Goss-1611461 978-0-12-804244-1 00009


Functional Diversityof Mycorrhizaand SustainableAgricultureManagement to Overcome Biotic andAbiotic Stresses

Michael J. GossSchool of Environmental Sciences, University of AU:1Guelph,

Guelph, Ontario, Canada

Mario CarvalhoInstitute of Mediterranean Agriculture and Environmental Sciences,

University of Evora, Evora, Portugal

Isabel BritoInstitute of Mediterranean Agriculture and Environmental Sciences,

University of Evora, Evora, Portugal

Goss-1611461 978-0-12-804244-1 00009


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Contents

List of Figures ixList of Tables xixList of Plates xxiPreface xxiiiTaxonomy of Arbuscular Mycorrhizal Fungi Referred to in this Book xxvii

1. Challenges to Agriculture Systems

1.1 Current and Future Challenges to Agriculture Systems 11.2 The Approach to Meeting the Challenges to World Agriculture 51.3 Conclusions 14

2. Agronomic Opportunities to Modify Cropping Systemsand Soil Conditions Considered Supportive of anAbundant, Diverse AMF Population

2.1 Components of Cropping Systems 162.1.1 Land Preparation 162.1.2 Cropping 252.1.3 Application and Use of Mineral Fertilizers, Organic,

and Inorganic Amendments in Crop Production 282.1.4 The Application of Pesticides 34

2.2 Key Aspects of Agricultural Systems on Diversity of Mycorrhiza 352.3 Conclusions 38

3. The Roles of Arbuscular Mycorrhiza and CurrentConstraints to Their Intentional Use in Agriculture

3.1 Benefits of Arbuscular Mycorrhiza 393.1.1 Acquisition of Mineral Nutrients 413.1.2 Defense Against Abiotic Stresses 493.1.3 Defense Against Biotic Stresses 503.1.4 Water Relations in Arbuscular Mycorrhizal Plants 52

3.2 Constraints to Intentional Use of AMF in Agriculture 543.3 Conclusions 58

v

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4. Diversity in Arbuscular Mycorrhizal Fungi�

With Clarisse Brıgido

4.1 Ecological Roles of Arbuscular Mycorrhizal Fungi 614.2 Basis of Functional Diversity in Arbuscular Mycorrhizal Fungi 62

4.2.1 Taxonomy of Arbuscular Mycorrhizal Fungi 624.2.2 Diversity of Arbuscular Mycorrhizal Fungi Related to

Growth Habit 644.2.3 Interaction Between the Genotypes of Fungi and Host

Plants and the Diversity of Arbuscular Mycorrhiza 654.3 Functional Diversity Associated With Host-Plant Benefits 66

4.3.1 Acquisition of Mineral Nutrients 674.3.2 Protection Against Abiotic Stresses 694.3.3 Protection Against Biotic Stresses 734.3.4 Improvement in Soil Structure 74

4.4 AMF Diversity Associated With the Management of DifferentEcosystems 75

4.5 Conclusions 78

5. Impacts on Host Plants of Interactions Between AMFand Other Soil Organisms in the Rhizosphere�

With Luıs Alho and Sabaruddin Kadir

5.1 Interactions Between AMF and Other Soil Microbes 825.1.1 The Tripartite Interaction Between AMF, Rhizobia, and

Legumes 855.1.2 Other Interactions With Bacteria 103

5.2 Interactions Between AMF and Other Fungi 1075.3 Interactions Between AMF and Soil Fauna 107

5.3.1 Interactions With Arthropods 1075.3.2 Interactions With Earthworms 108

5.4 Conclusions 109

6. The Significance of an Intact Extraradical Myceliumand Early Root Colonization in Managing ArbuscularMycorrhizal Fungi

6.1 Importance of Early Arbuscular Mycorrhizal FungiColonization 112

6.2 Arbuscular Mycorrhizal Fungi Inoculum Sources 1146.2.1 Spores 1146.2.2 Colonized Root Fragments 1166.2.3 Extraradical Mycelium 116

6.3 ERM as an Effective Arbuscular Mycorrhiza InoculumSource for Field Crops 1196.3.1 Persistence of Infective Extraradical Mycelium in Soil 1196.3.2 AMF Taxonomic Cluster Colonizing Strategies 120

vi Contents

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6.3.3 The Presence of Adequate Host Plants and the ERMIntegrity: Crop Rotations and Tillage Regime 123

6.4 Multiple Roles of ERM and Common Mycorrhizal Networks 1266.4.1 Transfer of Nutrients Between Plants 1266.4.2 Communication Between Plants 1286.4.3 Development of Soil Structure 128

6.5 Conclusions 129

7. New Tools to Investigate Biological Diversity andFunctional Consequences�

With Diederik van Tuinen

7.1 Genetic Markers 1327.1.1 Small Ribosomal Subunit 1327.1.2 Large Ribosomal Subunit 1337.1.3 Delineation of Operational Taxonomic Units 1347.1.4 Mitochondrial Large Ribosomal Subunit 1357.1.5 RNA Polymerase II 136

7.2 Functional Diversity 1367.3 Conclusions 140

8. Management of Biological and Functional Diversityin Arbuscular Mycorrhizal Fungi Within CroppingSystems

8.1 Managing Indigenous AMF in Agroecosystems 1468.1.1 Managing Indigenous AMF to Overcome Abiotic Stresses 1468.1.2 Managing Indigenous AMF to Overcome Biotic Stresses 1618.1.3 Discussion of the Results from the Case Studies 166

8.2 Opportunities to Develop ERM From Indigenous AMFWithin the Cropping System 1688.2.1 Criteria to Select Developer Plants 171

8.3 Some Final Comments 173

References 175Index 223

Contents vii

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HTU1 List of Figures

Figure 1.1 The rapid increase in world population since1960 and the associated reduction in the averagearea of arable land per person. Note that theaverage area of arable land area per person is lessthan half that in 1960 and is now smaller than0.2 ha.

2

Figure 1.2 The urbanization of the world population since1961.

3

Figure B1.2.1 Increment in the use of fertilizers (million tonnesof nutrients; adapted from Bumb, B.L., Baanante,C.A., 1996. World trends in fertilizer use andprojections to 2020. International Food PolicyResearch Institute, 2020 Brief 38, 4 pp),pesticides (million US$, adapted from Zhang, W.J., Jiang, F.B., Ou, J.F., 2011. Global pesticideconsumption and pollution: with China as afocus. Proc. Int. Acad. Ecol. Environ. Sci. 1,125�144) and production (million tonnes of 20most valuable commodities, source: http://faostat3.fao.org/) in the world between 1960 and1990.

7

Figure B1.2.2 Effect of soil organic matter (SOM) on the useefficiency of inputs to wheat production in theSouth of Portugal. Conv., conventional agriculturesystem based on inversion tillage and bailing ofthe cereal straw; CA, conservation agriculturebased on no-till and maintenance of crop residueson soil surface. The same crop rotation was usedfor the two systems.

8

Figure B2.1.1 Effect of soil organic matter on wheat response tonitrogen fertilizer application according to the fitmodel: Y=631+35.4 N-0.07 N2+2718 ln(SOM)-8.6 N SOM (y, wheat grain yield; N, nitrogenapplied; SOM, soil organic matter (% 0�30 cm)).Black line, SOM 1%; dark gray line, SOM 2%;

22

ix

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http://faostat3.fao.org/

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light gray line, SOM 3%. Numbers in italicsrepresents the economic optimum for appliednitrogen (x axis) and the expected grain yield (yaxis) according to the model.

Figure 2.1 Rhizosphere and mycorrhizosphere interactionsunder cover crops and crop rotations thatencourage the presence and diversity of AMF andthe benefits of these and other beneficialmicrobes in plant productivity.

27

Figure 4.1 The proportion of root colonized by arbuscularmycorrhizal fungi (AMF) relative to that of thesame plant dependant mainly on spores forcolonization. Results for maize based on Kabirand Koide (2000). Results for wheat based onBrito et al. (2013).

77

Figure 5.1 Effects of adding phosphorus in the form ofhydroxyapatite on the formation of nodules onbean roots by R. phaseoli in the absence (Control)and presence of arbuscular mycorrhiza. Theeffects of P on the growth of the inter- andextraradical mycelium is also shown. Withoutaddition of P to the soil, the mycorrhizasupported a significant development of nodules,whereas there was almost no development in theControl treatment. With applications of 100 mghydroxyapatite or more, there was no significantincrease in nodule formation in either treatmentbut the mycorrhizal plants formed a little morethan half of those present in Controls. Theintraradical mycelium increased threefold withthe addition of P, whereas the increase inextraradical mycelium (ERM) was almost fivefold.Root dry weight in the mycorrhizal plantsincreased by 26%, whereas in the Controltreatment the increase was 45% (data not shown).

93

Figure 5.2 The effects of applying phosphate fertilizer on thedevelopment and effectiveness of the tripartitesymbiosis between soybean, indigenous AMF,and Bradyrhizobium japonicum. (A) Variation inshoot dry weight (red markers) and total leaf area(blue markers) at podfill in plants colonized usinginoculum with extraradical mycelium (ERM) keptintact (solid markers) or made up mainly of root

99

x List of Figures

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fragments, spores, and disrupted ERM (openmarkers). The application of phosphorus in excessof 20 mg kg21 to disturbed soil without an intactERM was not beneficial to growth but plantscolonized from intact ERM showed a significantresponse up to 40 mg kg21. (B) At podfill therewas no effect of inoculum type on colonization,except for the concentration of vesicles within theroots, where the effect of the presence of anintact ERM was significant at P, 0.001. Redmarkers, ERM intact; blue markers, ERMdisrupted. Negative effects on colonization ofapplying phosphorus were small. (C) The negativeimpact of phosphorus on colonization was greaterin soybeans that were genetically incapable ofestablishing a viable symbiosis with Rhizobia andcould not form nodules (blue markers) than in thenodulating isoline (red markers). The benefit tocolonization from an inoculum containing intactERM (closed markers) was also less consistent inthe nonnodulating isoline. (D) Both colonizationby Rhizobia, as indicated by nodule weight(dashed lines), and biological nitrogen fixation(solid lines) were enhanced by the presence ofintact ERM (closed markers) when soybeans wereplanted compared with those colonized fromspores, root fragments and disrupted ERM (openmarkers).

Figure 5.3 Effect of keeping the extraradical mycelium intactrather than disrupted prior to

sowing soybeans on the effectiveness of nodulescolonized by free-living wild type rhizobium andthe added benefit from inoculation withthe more effective strain 532C.

100

Figure 5.4 Pots of Trifolium subterraneum L. 6 weeks afterplanting in soil containing 22.6 mg Mn kg-1. Left,soil was sieved after the growth of the previousplants (Ornithopus compressus L.) and the rootswere cut into sections and mixed back into the soilbefore subterraneum clover was sown. Roots werecolonized by indigenous AMF from spores,colonized root fragments, and short pieces ofdisrupted extraradical mycelium (ERM). Note the

101

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sparse formation of nodules. Right, prolific growthof T. subterraneum in undisturbed soil, colonized byindigenous AMF from intact ERM and spores. Morelarge nodules were formed on the main axis (arrowpoints to nodule on enlargement of main axis).

Figure 5.5 Effects of developer ERM, presence and integrity,on colonization rate by indigenous AMF (basedon arbuscule formation) and dry weight of shootsand root nodules of Trifolium subterraneum L. 21days after sowing. Mycorrhizae were initiallyformed in association with roots of two commonMediterranean weed species (Ornithopuscompressus L. or Lolium rigidum), both beingmycotrophic (Mic1). A third plant, Rumexbucephalophorus is considered not to formmycorrhiza (Mic-) and hence provided a controlfor soil disturbance and the contribution ofdisrupted ERM. ERM intact2 ERM1 , ERMdisrupted2 ERM2 .

102

Figure 5.6 Relationship between colonization rate, based onarbuscule formation 21 days after sowing, andshoot dry weight , and Mn concentration inthe roots of Trifolium subterraneum L.42 days after sowing.

102

Figure 5.7 Relationship between Mn concentration in theroots, shoot N content and Nodule dryweight in Trifolium subterraneum L. 42days after sowing.

103

Figure 5.8 Main bacterial groups considered to participate inactivities in the mycorrhizosphere (based onBonfante and Anca, 2009). Althoughalphaproteobacteria include the rhizobia thatform the tripartite symbiosis with legumes, somemembers of the betaproteobacteria can also fixnitrogen from the atmosphere and have beenidentified as endobiotrophs (Cage, 2004;Leveau and Preston, 2008).

104

Figure 6.1 Arbuscular colonization (%) of the second plantin a succession, grown in undisturbed soil withERM as the main source of AMF propagule. S,Silene galica (nonmycotrophic plant); R, Rumexbucephalophorus (scarcely mycotrophic pant); O,Ornithopus compressus (mycotrophic plant); and

118

xii List of Figures

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W, Triticum aestivum (mycotrophic plant). In xaxis labels first letter corresponds to the first plantand second letter to the second plant in thesuccession (e.g., OR, is Rumex bucephalophoruspreceded by Ornithopus compressus).

Figure 6.2 Shoot dry weight (µg plant21) of the second plantin a succession, grown in undisturbed soil withERM as the main source of AMF propagule. S,Silene galica (nonmycotrophic plant); R, Rumexbucephalophorus (scarcely mycotrophic pant); O,Ornithopus compressus (mycothrophic plant); andW, Triticum aestivum (mycotrophic plant). In xaxis first letter corresponds to the first plant andsecond letter to the second plant in thesuccession (e.g., OR, is Rumex bucephalophoruspreceded by Ornithopus compressus).

118

Figure 8.1 Arbuscular colonization (AC) of wheat byindigenous AMF 10 days (W 10 DAP), 21 days(W 21 DAP), and subterranean clover 21 daysafter planting, (C 21 DAP). Colonization wasinitiated by different propagules. A, Spores only;B, Spores, fragmented mycelium and colonizedroot fragments of Lolium rigidum or Ornithopuscompressus; C, Spores and intact extraradicalmycelium (ERM) associated with the roots of L.rigidum; and D, Spores and intact ERM associatedwith the roots of O. compressus. The soilcontained 22.6 mg Mn kg-1.

148

Figure 8.2 Shoot dry weight of wheat (diamond) andsubterranean clover (square) shoots 21 days afterplanting. Colonization by indigenous AMF wasinitiated by different propagules. A, Spores only;B, Spores, fragmented mycelium, and colonizedroot fragments of Lolium rigidum or Ornithopuscompressus; C, Spores and intact extraradicalmycelium (ERM) associated with the roots of L.rigidum; and D, Spores and intact ERM associatedwith the roots of O. compressus. The soilcontained 22.6 mg Mn kg-1.

149

Figure 8.3 Effect of the native AMF propagule type in thesoil at the time of planting on wheat shoots (WsMn) and subterranean clover shoots (Cs Mn) androots (Cr Mn) manganese concentration at 21

150

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days after planting. Colonization by indigenousAMF was initiated by different propagules: A,Spores only; B, Spores, fragmented mycelium,and colonized root fragments of Lolium rigidumor Ornithopus compressus; C, Spores and intactextraradical mycelium (ERM) associated with theroots of L. rigidum; and D, spores and intact ERMassociated with the roots of O. compressus. Thesoil contained 22.6 mg Mn kg-1.

Figure 8.4 Relationship between shoot dry weight, 21 daysafter planting and Mn concentration in the shootsof wheat (solid line and markers) or roots ofsubterranean clover (hatched line, open markers).The soil contained 22.6 mg Mn kg-1.

151

Figure 8.5 Effect of the indigenous arbuscular mycorrhiza(AM) on (1) nodule dry weight, (2) Shoot Ncontent, and (3) shoot dry weight of subterraneanclover 6 weeks after planting. Colonization byindigenous AMF was initiated by differentpropagules: A, Spores only; B, Spores, fragmentedmycelium and colonized root fragments of Loliumrigidum or Ornithopus compressus; C, Spores andintact extraradical mycelium (ERM) associatedwith the roots of L. rigidum; D, Spores and intactERM associated with the roots of O. compressus.The soil contained 22.6 mg Mn kg-1.

152

Figure 8.6 Relationship between mycorrhizal colonizationand P and S concentration in the shoots of thewheat at 21 days after planting. The soilcontained 22.6 mg Mn kg-1.

153

Figure 8.7 Representation of the similarities between thecommunity structures of AMF present in wheatroots in succession toOrnithopus compressus orLolium rigidum plants with or without soildisturbance, evaluated by 454-pyrosequencingtechnique. OW,O. compressus, only spores asAMF propagules; LW, L. rigidum, only spores asAMF propagules; WLD, wheat after L. rigidum,Disturbed soil; WLU, wheat after L. rigidum,Undisturbed soil; WNU, wheat, only spores as AMFpropagules; WOD, wheat afterO. compressus,Disturbed soil; WOU, wheat afterO. compressus,Undisturbed soil (after Brıgido et al., 2017).

153

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Figure 8.8 Representation of the similarities between thecommunity structures of AMF present in roots ofsubterranean clover in succession to Ornithopuscompressus or Lolium rigidum plants with orwithout soil disturbance, evaluated by 454-pyrosequencing technique. CLD, subterraneanclover after L. rigidum, Disturbed soil; CLU,subterranean clover after L. rigidum, Undisturbedsoil; CNU, subterranean clover, only spores asAMF propagules; COD, subterranean clover afterO. compressus, Disturbed soil; COU,subterranean clover after O. compressus,Undisturbed soil; OW, O. compressus, onlyspores as AMF propagules; LW, L. rigidum, onlyspores as AMF propagules (after Brıgido et al.,2017).

154

Figure 8.9 Comparison of an intact extraradical mycelium(ERM) with ERM disrupted on, shoot dry weight(black bars), P content (dark gray barks), andarbuscular colonization rate (light gray bars), inwheat. Results show the average for 21 days afterplanting (After Brito et al., 2013b).

157

Figure 8.10 Comparison of the presence of an intact with adisrupted ERM at planting on the content ofalkaline elements and S in wheat. Results showthe average for 21 and 31 days after planting. Thecondition of the ERM was created by previouslygrowing mycotrophic Developer plants(Ornithopus compressus L. or Lolium rigidum G.)and applying differential soil disturbancetreatments (Undisturbed soil, ERM kept intact;Disturbed soil, ERM disrupted) (After Brito et al.,2014). The soil contained 22.6 mg Mn kg-1.

158

Figure 8.11 Effect of the presence of an intact or disruptedERM at the time maize planting on AMFarbuscular colonization (AC %) and colonizedroot density (CRD cm of colonized root cm-3 ofsoil), under four P levels applied to the soil (P1,P2, P3, and P4 stands for 0, 6, 12, and 18 mg Pkg-1 of dry soil, respectively). ERM was previouslydeveloped in the soil by O. compressus andindigenous AMF. For each parameter the sameletter indicates values are not significantlydifferent at P=.05.

158

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Figure 8.12 Effect of the presence of intact or disruptedextraradical mycelium (ERM) of arbuscularmycorrhizal fungi (AMF) at the time of maizeplanting on the shoot dry weight and P content,under four P levels applied to the soil (P1, P2, P3,and P4 stands for 0, 6, 12, and 18 mg P kg-1 ofdry soil, respectively). U (Undisturbed soil) and D(Disturbed soil) corresponds to ERM being intactor disrupted, respectively. ERM was previouslydeveloped in the soil by Ornithopus compressusand indigenous AMF. For each parameter thesame letter indicates values are not significantlydifferent at P=.05.

159

Figure 8.13 Effect of the presence of an intact or disruptedextraradical mycelium (ERM) at the time of maizeplanting on the shoot N and K content, under fourP levels applied to the soil (P1, P2, P3, and P4stands for 0, 6, 12, and 18 mg P kg-1 of dry soil,respectively). ERM was previously developed inthe soil by Ornithopus compressus andindigenous arbuscular mycorrhizal fungi (AMF).For each parameter the same letter indicatesvalues are not significantly different at P=.05.

160

Figure 8.14 Effect of the presence of intact or disruptedextraradical mycelium (ERM) at the time of maizeplanting on the shoot Ca and S content, underfour P levels applied to the soil (P1, P2, P3, andP4 stands for 0, 6, 12, and 18 mg P kg-1 of drysoil, respectively). ERM was previously developedin the soil by Ornithopus compressus andindigenous arbuscular mycorrhizal fungi (AMF).For each parameter the same letter indicatesvalues are not significantly different at P=.05.

160

Figure 8.15 Effect of the presence of an intact or disruptedextraradical mycelium (ERM) of arbuscularmycorrhizal fungi (AMF) at the time of tomatoplanting on the shoot dry weight (bars), DI(square marker) and arbuscular colonization (AC)(triangles) under inoculation of tomato plants withFusarium oxysporum f.sp. radicis-lycopersici (C1,C2, C3, and C4 stands for inoculation with 0,103, 106, and 109 conidia plant-1 at planting).ERM was previously developed in the soil by

163

xvi List of Figures

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Lolium rigidum and indigenous AMF. For eachparameter, the same letter indicates values arenot significantly difference at P=.05.

Figure 8.16 Diagram of the field experiment with tomato. Thedark gray color corresponded to the area (6 ha)where significant yield loss (20 tonne-1) occurredin the 2013 season due to infection by Fusariumoxysporum. The light gray shows the area whereno visible symptoms of the disease wereidentified and yield of the crop was considerednormal for the region (100 tonnes ha-1).

164

Figure 8.17 Field experiment to evaluate the benefits of acover crop (barley) in the yield of tomato in afield with the presence of Fusarium oxysporum.The Cover crop treatment with minimum soildisturbance before the planting of tomato aimedto keep intact the ERM developed in associationwith barley roots; Traditional treatment relates tothe traditional production system with no covercrop, deep, and intensive tillage, includingsecondary disk arrowing before planting thetomato. For each parameter the letter indicatesvalues significantly difference at P=.05.

166

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List of Tables

Table 1.1 Estimation of Relative Contributions to ImprovedCrop Production of Increases in Harvested LandArea, Crop Yielda and Cropping Intensity ofAgriculture Over the Period from 1961 to 2005(Bruinsma, 2011)

2

Table 2.1 The Characteristics, Aims, and Some EssentialEffects of Common Tillage Systems and PotentialImpacts on Arbuscular Mycorrhiza (AM)

17

Table 2.2 Effects of Tillage, Application of N Fertilizer, Use ofCover Crops and Effects of Crop Rotation on theChanges in Soil Organic Carbon in the top 0.3 mSoil During a 15-year Experiment in Central Italy.In the First 5 years (A), Maize Was Grown in EachYear; in the Following 10 years Crops Were Grownin Rotation (B) (Based on Mazzoncini et al. (2011))

23

Table B2.2.1 Effect of P Applied to the Soil (mg P kg21 of Soil):on the Arbuscular Colonization (AC, % of rootcolonized by arbuscules), on the Root Density (RD,cm of root cm23 of soil), and on Colonized RootDensity (CRD, cm of root colonized witharbuscules cm23 of soil) of maize (Values followedby the same letter are not significantly different atP5 50.05. Adapted from Brito et al. (2013a))

31

Table 5.1 The Concentration of Main Groups of Microfloraand Fauna in Soil

83

Table 6.1 Arbuscular Colonization (AC) of Host Plants Usedto Develop Extraradical Mycelium (ERM) and ACof Wheat and Clover Grown for 21 days after thefirst plants in undisturbed soil (ERM intact) anddisturbed soil (ERM disrupted)

124

Table 7.1 Characteristics of the Mycelium of the Members ofThree Families of Arbuscular Mycorrhizal Fungi(AMF), including speed of colonization(Source: Data from Hart and Reader, 2002a)

137

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Table 8.1 Design of Cropping Systems to EnhanceArbuscular Mycorrhizal Fungi (AMF) Diversity andDeliver Functional Benefits to Crops andEcosystem Services

145

Table 8.2 Summary of the Proposed Strategy; Mechanismsand Benefits for the Constructive Management ofArbuscular Mycorrhizal Fungi (AMF) WithinAgricultural Systems

169

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HTU3 List of Plates

Plate B1.3.1 Arbuscule (4003 ). 11Plate B1.3.2 Hyphal Coils (2003 ). 11Plate B1.3.3 Vesicle (2003 ). 12Plate 3.1 AMF colonized root (200X). Root hair (RH) and

extraradical mycelium (ERM). ERM is longer andthinner than a RH and is branched.

40

Plate 6.1 (A) Hyphopodium (200X); (B) Hyphal intercellulargrowth and arbuscules (200X); (C) arbuscule (400X).

115

Plate 6.2 Vesicle (400X). 116Plate 6.3 Wheat roots colonized with “fine endophytes”

(200X).121

Plate 8.1 Growth of wheat in soil containing excessive levelsof Mn following colonization initiated by differentpropagules. A, B, and D are the propaguletreatments indicated in Fig. 8.1 (A, Only spores; B,Spores, fragmented mycelium, and colonized rootfragments of Ornithopus compressus; and D,Spores and intact ERM of the native AMFassociated with O. compressus). The protection ofwheat plants by arbuscular mycorrhizal fungi(AMF) was only conferred when an intactextraradical mycelium (ERM) was present in thesoil at the time of planting.

149

Plate 8.2 Growth of wheat in soil containing excessive levelsof Mn following colonization initiated by differentpropagule sources of indigenous arbuscularmycorrhizal fungi (AMF). C and D are thepropagule treatments shown in Figs. 8.1, 8.4 (C,Spores and intact extraradical mycelium (ERM) ofthe native AMF associated with Lolium rigidum;D, Spores and intact ERM of the native AMFassociated with Ornithopus compressus). Thefunctional consequences of the different AMFassociated with the two Developer plants areevident.

150

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Plate 8.3 Effect of the presence of an intact extraradicalmycelium (ERM) of native arbuscular mycorrhizalfungi (AMF) developed in association withOrnithopus compressus on the growth of the rootsof maize (related to data presented in Fig. 8.11). (UP1, Undisturbed soil treatment ERM intact and noP applied to the soil; D P1, Disturbed soiltreatment ERM disrupted and no P applied to thesoil).

161

Plate 8.4 Grade for evaluation of disease incidence (DI) atthe stem base of tomato.

162

Plate 8.5 Tomato plants inoculated with a suspension of 10-9

conidia of Fusarium oxysporum f.sp. radicis-lycopersici (inoculum level C4). Und and Dist areUndisturbed and Disturbed soil treatmentsdescribed in Fig. 8.15. For Dist the soil wasdisturbed after the growth of Lolium rigidum G.(ERM disrupted) and in Und the soil remainedundisturbed at the planting of tomato (ERM intact).

164

Plate 8.6 Field experiment with tomato. (A) Winter seedingof the barley cover crop after land preparation;(B) Barley cover crop in February; (C) Barley killedby systemic herbicide; (D) Traditional landpreparation in spring before the planting of tomato.

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Preface

The current world population of 7.5 billion is expected to be 20% greater by

2050 and so we have little over 33 years to ensure the means of producing

sufficient food to meet the expected demand. One of the options that previ-

ously were available to us for expanding world production of cereals, vegeta-

bles, fruits, and meat, namely bringing more land into production, is no

longer possible and consequently we must everywhere increase the produc-

tivity of the land. But this time we must not attempt it without making every

effort to safeguard the environment. Put in a slightly different way, we have

to grow more but conserve the soil and its biodiversity, be more efficient in

terms of water use, improve nutrient-use efficiency so that fewer applied

nutrients end up contaminating our freshwater and eutrophying our lakes and

shallow seas or adversely affecting the quality of our air and contributing to

the atmospheric loading of greenhouse gases. If we add in a desire to reduce

the application of pesticides, especially those targeting root pathogens, it

would seem to represent an extremely challenging task. Perhaps it will be a

surprise to some that the answer to many of these challenges might well be

one result of the development of techniques that allow us to determine the

make-up of microorganisms, which has had huge impacts on soil science and

its application in agronomy.

Beginning with the ability to differentiate the fatty acid and phospholipid

profiles of microbial communities in soil and reaching the current status,

where the whole genetic code of an organism can be determined, the previ-

ously rather opaque world of soil microbiology is being clarified at an

unprecedented rate. From around the time that the word mycorrhiza was

coined by Frank in 1885, mycorrhizal fungi have been of interest because of

their special relationship with the vast majority of land plants. For agrono-

mists the most important are the endomycorrhizal fungi that produce tree-

shaped branched structures called arbuscules inside the cortex of most crop

plants. Evidence steadily accrued that established their importance in supply-

ing the essential element phosphorus to plants but the availability of mineral

fertilizers, such as superphosphate, caused many to assume that the contribu-

tion from mycorrhiza was unnecessary and even in fertile soils the organisms

were more like parasites than partners of their hosts. But eventually there

came the realization that arbuscular mycorrhiza provided far more services

than supplying phosphorus. The recent appreciation of the biological

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diversity of mycorrhizal fungi and the functional consequences for mycor-

rhiza with different abilities to protect their host from the impacts of toxic

metals, to counter the invasion of root diseases and to enhance the formation

and stabilization of soil aggregates, renewed interest in the ecological signifi-

cance of mycorrhiza.

The challenge for agronomists and those interested in availing their crops

of the potential benefits from arbuscular mycorrhiza is how to manage them.

One obvious approach is to develop a source of inoculum that can be applied

to a field prior to or as part of seeding a crop that could benefit from the for-

mation of a mycorrhizal symbiosis. However, not only is that a relatively

expensive activity it is also fraught with uncertainty over its efficacy.

Another approach is to encourage the adoption of farming practices that sup-

port a wide variety of indigenous arbuscular mycorrhizal fungi (AMF) that

will provide specific benefits sought for the crop. But in many respects this

is not enough. It is a long way from providing the supportive environment

for a specific fungus or consortium of fungi to dominate the mycorrhiza that

form on most crop plants in a field. That goal requires the development of

new farming strategies.

The approach we take in this book is to expand on the current challenges

to meeting the requirements for feeding a much larger world population and

suggest how arbuscular mycorrhiza can contribute to the solution under

many agricultural climatic zones. We consider the farming practices that can

be deleterious to maintaining a diverse population of mycorrhizal fungi and

the systems and practices that can encourage their survival and effectiveness.

We discuss the interactions between the fungi and other soil organisms,

some of which are now known to improve the functioning of arbuscular

mycorrhiza, and how the symbiosis influences many of the basic plant pro-

cesses. The possibilities for obtaining specific information on individual

fungi offered by the new generation of molecular methods are also presented.

Finally we present a view as to how indigenous AMF might be managed in a

practical setting.

The opportunity to put our combined thoughts and ideas into a book

owes a lot to the discussions we had with Marisa LaFleur, commissioning

editor with Elsevier, and subsequently with commissioning editor Nancy

Maragioglio. Both have been wonderfully supportive and we can’t thank

them enough. We are equally indebted to Billie Jean Fernandez, who has

been of enormous help in pulling us over the finish line. Lisa Jones, the

Production Editor, has been superb in converting our ideas on presentation

into reality; she has worked tirelessly to ensure we would be proud of the

finished product. We sought the help of two experts to ensure that the chap-

ters on new generation molecular methods and diversity among the AMF

would be as up-to-date as possible. It is difficult to express just how grateful

we are to Diederik van Tuinen, a very good friend and colleague, for his

contribution on modern molecular methods in relation to the elaboration of

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functional diversity. The contribution of Clarisse Brıgido in developing the

chapter discussing the complexity of functional diversity in AMF was also

critical and she too has been of incalculable help and support. We are

extremely grateful to Sabaruddin Kadir and Luis Alho, who generously pro-

vided material used in Chapter 5, Impacts on Host Plants of Interactions

Between AMF and Other Soil Organisms in the Rhizosphere, as well as pro-

vided important feedback on the contents.

Michael Goss, Mario Carvalho, and Isabel Brito

March 2017

Preface xxv

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AU:1, Page 27 Please confirm the title “Taxonomy of Arbuscular

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Taxonomy of ArbuscularMycorrhizal Fungi Referred to inthis Book

There have been some major changes in the taxonomy associated with arbus-

cular mycorrhizal fungi (AMF). In consequence, some have undergone more

than one name change in the last 30 years. To avoid as much confusion as

AU:1

possible, the names used in the text are those reported by the authors of the

papers referenced. We have used Schußler and Walker (2010) and Redecker

et al. (2013) to provide a list of the current names of these species.

Former Name Genera Specific

Epithet

Acalulospora leavis Acalulospora leavisAcaulospora morrowiae Acaulospora morrowiaeEntrophospora schenckii Archaeospora schenckiiGigaspora albida Gigaspora albidaGigaspora gigantea Gigaspora giganteaGigaspora margarita Gigaspora margaritaGigaspora rosea Gigaspora roseaGlomus caledonium (Nicol. & Gerd.) Trappe andGerdemann

Funneliformis caledonium

Glomus claroideum Claroideoglomus claroideumGlomus clarum Rhizophagus clarusGlomus constrictum5 Funneliformis constrictum Septoglomus constrictumGlomus coronatum Funneliformis coronatusGlomus diaphanum Rhizophagus diaphanusGlomus etunicatum Claroideoglomus etunicatumGlomus fasciculatum Rhizophagus fasciculatusGlomus fasciculatum Gerd. And Trap Rhizophagus fasciculatusGlomus fasciculatum (Thaxter sensu Gerd) Rhizophagus fasciculatusGlomus geosporum Funneliformis geosporum

(Continued )

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(Continued)

Former Name Genera Specific

Epithet

Glomus intraradicesa Rhizophagus sp.Glomus intraradices Rhizophagus irregularisGlomus intraradices Rhizophagus intraradicesGlomus macrocarpum Glomus macrocarpumGlomus mosseae Funneliformis mosseaeGlomus tenue Glomus tenueRhizophagus intraradices Rhizophagus intraradicesScutellospora calospora Scutellospora calosporaScutellospora fulgida Racocetra fulgida

aIdentifying the current name for Glomus intraradices is problematic. The isolate DAOM197198 wasrenamed from Glomus intraradices to Glomus irregularis and then to Rhizophagus irregularis. As not allisolates have been reanalyzed, we now have some which are Rhizophagus sp., some R. irregularis, andsome still R. intraradices.

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xxviii Taxonomy of Arbuscular Mycorrhizal Fungi Referred to in this Book

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