Mycorrhizal Mediation of Soil: Fertility, Structure, and Carbon Storage

Mycorrhizal Mediation of Soil

Fertility, Structure, and Carbon Storage

Editors

Nancy Collins Johnson

Catherine Gehring

Jan Jansa

Table of Contents

Cover image

Title page

Copyright

List of Contributors

Preface

Chapter 1. Mycorrhizas: At the Interface of Biological, Soil, and Earth Sciences

1.1. Successful Coexistence of Plants and Fungi

1.2. Mycorrhizal Research: Past, Present, and Future

1.3. Goals and Objectives

Section I. Mycorrhizal Mediation of Soil Development

Chapter 2. Mycorrhizal Symbioses and Pedogenesis Throughout Earth’s History

2.1. The Importance of Reciprocal Effects of Plant–Mycorrhiza–Soil Interactions in the Evolution and Assembly of Terrestrial Ecosystems

2.2. Plants and Mycorrhizas as Agents of Pedogenesis: Coupling Plant Photosynthate Energy to the Actions of Fungal Mycelial Networks

2.3. Evolutionary Origins of Plants and Mycorrhizas

2.4. Coevolution of Plants, Mycorrhizas, and Photosynthate-Driven Weathering and Pedogenesis

2.5. Feedback Between Plant-Driven Pedogenesis, Global Biogeochemical Cycles, and the Evolution of Plants and Mycorrhizal Functioning

2.6. Conclusions

Chapter 3. Role of Mycorrhizal Symbiosis in Mineral Weathering and Nutrient Mining from Soil Parent Material

3.1. Introduction

3.2. Mechanisms of Mineral Weathering

3.3. Fungal Weathering in the Laboratory

3.4. From Laboratory to Field

3.5. Conclusions and Future Research Directions

Chapter 4. Mycorrhizal Interactions With Climate, Soil Parent Material, and Topography

4.1. Introduction

4.2. Mycorrhizal Interactions With Climate

4.3. Mycorrhizal Interactions With Parent Material

4.4. Mycorrhizal Interactions With Topography

4.5. Conclusions

Chapter 5. Mycorrhizas Across Successional Gradients

5.1. Succession

5.2. Succession in Mycorrhizal Fungal Communities

5.3. Habitat Drivers

5.4. Plant Drivers

5.5. Fungal Drivers

5.6. Interacting Drivers

Section II. Mycorrhizal Mediation of Soil Fertility

Chapter 6. Introduction: Perspectives on Mycorrhizas and Soil Fertility

6.1. Introduction

6.2. Contributions of Mycorrhizal Fungi to Soil Fertility

6.3. Soil Fertility Influences Mycorrhizal Fungi

6.4. Principles for Management of Mycorrhizal Fungi for Soil Fertility

6.5. Looking Forward

Chapter 7. Fungal and Plant Tools for the Uptake of Nutrients in Arbuscular Mycorrhizas: A Molecular View

7.1. Introduction

7.2. Nitrogen Nutrition Within Arbuscular Mycorrhizas

7.3. Phosphate Transport in Arbuscular Mycorrhizal Symbiosis

7.4. Sulfur Metabolism and Arbuscular Mycorrhizal Symbiosis

7.5. From Root to Shoot and Back: Evidence for a Systemic Signaling and Gene Regulation in Mycorrhizal Plants

7.6. Perspectives and Conclusions

Chapter 8. Accessibility of Inorganic and Organic Nutrients for Mycorrhizas

8.1. Introduction

8.2. Movement of Phosphate and Nitrate Ions to Roots

8.3. Inorganic Phosphorus and Nitrogen Acquisition by Arbuscular Mycorrhizal Fungi

8.4. Inorganic Phosphorus and Nitrogen Acquisition by Ectomycorrhizal Fungi

8.5. Arbuscular Mycorrhizal Fungi and Organic Nutrient Forms

8.6. Ectomycorrhizal Fungi and Organic Nutrient Forms

8.7. Conclusions

Chapter 9. Mycorrhizas as Nutrient and Energy Pumps of Soil Food Webs: Multitrophic Interactions and Feedbacks

9.1. Introduction

9.2. Mycorrhizas and Saprotrophs

9.3. Mycorrhizas and Herbivores

9.4. Mycorrhizas and Fungivores

9.5. Mycorrhizas and Bacterivores

9.6. Mycorrhizas and Higher Trophic Levels

9.7. The Way Forward

Chapter 10. Implications of Past, Current, and Future Agricultural Practices for Mycorrhiza-Mediated Nutrient Flux

10.1. Introduction

10.2. Agriculture in the Past

10.3. Modern Agriculture

10.4. Agriculture in the Future

10.5. Conclusion

Chapter 11. Integrating Ectomycorrhizas Into Sustainable Management of Temperate Forests

11.1. Introduction

11.2. Harvesting Systems

11.3. Stand Reestablishment

11.4. Seedling Production

11.5. Stand Management

11.6. Conclusions

Chapter 12. Mycorrhizal Mediation of Soil Fertility Amidst Nitrogen Eutrophication and Climate Change

12.1. Introduction

12.2. Mechanisms of Mycorrhizal Nutrition and Stoichiometry

12.3. Nutrient Uptake and Mycorrhizal Fungi: the Basics

12.4. Mycorrhizas and Global Change

12.5. Mycorrhizas and Nitrogen Deposition

12.6. What is Needed? A Stoichiometric Challenge

Section III. Mycorrhizal Mediation of Soil Structure And Soil-Plant Water Relations

Chapter 13. Introduction: Mycorrhizas and Soil Structure, Moisture, and Salinity

13.1. Introduction

13.2. Soil Structure

13.3. Soil Salinity

13.4. Soil Moisture

Chapter 14. Mycorrhizas and Soil Aggregation

14.1. Introduction: Soil Aggregation, Its Component Processes, and Significance of Soil Structure

14.2. Evidence for Involvement of Different Types of Mycorrhizas in Soil Aggregation

14.3. Mechanisms of Soil Aggregation

14.4. Relative Importance of MycorrhizaS

14.5. Avenues and Needs for Future Research

Chapter 15. Arbuscular Mycorrhizal Fungi and Soil Salinity

15.1. Introduction

15.2. Arbuscular Mycorrhizal Fungi and Salt Stress

15.3. Salinity in Combination with Drought and Warming

15.4. Studies of Salinity Responses of Indigenous Arbuscular Mycorrhizal Fungi

15.5. Plant Root Properties, Mycorrhizal Fungi and Salinity Stress

15.6. Signaling, Mycorrhizal Fungi, and Salinity Stress

15.7. Tripartite Interactions and Salinity Stress

15.8. Agronomical Consequences of Using Mycorrhizal Fungi in Saline Fields

15.9. Conclusions and Future Perspectives

Chapter 16. Mycorrhizas, Drought, and Host-Plant Mortality

16.1. Introduction

16.2. Mycorrhizas, Plants, and Drought

16.3. Drought-Related Host Mortality and Consequences for Mycorrhizas

Chapter 17. Soil Water Retention and Availability as Influenced by Mycorrhizal Symbiosis: Consequences for Individual Plants, Communities, and Ecosystems

17.1. Introduction

17.2. Influence of Vegetation on Soil Hydraulic Properties

17.3. Mycorrhizal Fungal Influence on Soil Hydraulic Properties: Review of Published Evidence

17.4. Mycorrhizal Fungal Role in Hydraulic Redistribution and Hydraulic Connectivity in the Vadose Zone

17.5. Mycorrhizal Fungal Role in Reducing Soil Erosion

17.6. Consequences for Individual Plants, Communities, and Ecosystems, and Implications for Terrestrial Ecosystems Response to Global Change

17.7. Knowledge Gaps, Research Needs, and Future Research Directions

Chapter 18. Mycorrhizal Networks and Forest Resilience to Drought

18.1. Introduction

18.2. Forest Resilience

18.3. The Role of Mycorrhizas in Water Uptake

18.4. Mycorrhizal Networks and Their Role in Hydraulic Redistribution and Drought Responses

18.5. Rooting Depth

18.6. The Role of Drought in Global Forest Decline

18.7. Climate Change Projections for Drought Effects on Forests and the Domino Effect

18.8. Incorporating Mycorrhizal Networks in Forest Management

18.9. Knowledge Gaps and Future Research Directions

18.10. Conclusions

Section IV. Mycorrhizal Mediation of Ecosystem Carbon Fluxes and Soil Carbon Storage

Chapter 19. Introduction: Mycorrhizas and the Carbon Cycle

19.1. The Carbon Cycle

19.2. The Key Role of the SOM in Soil Processes

19.3. Position of Mycorrhizal Fungi Within the Soil Food Webs

19.4. Mycorrhizal Symbiosis and the Soil C Cycling

19.5. Functional Diversity in Mycorrhizal Symbioses with Respect to C Cycling

19.6. Open Questions, Experimental Challenges

Chapter 20. Carbon and Energy Sources of Mycorrhizal Fungi: Obligate Symbionts or Latent Saprotrophs?

20.1. Introduction

20.2. Two Concepts of Saprotrophy

20.3. Phylogenetic Evidence

20.4. Enzymatic Evidence

20.5. Carbon Signatures

20.6. Ectomycorrhizal Fungi Involved

20.7. Nonenzymatic Nutrient Mining by Ectomycorrhizal Fungi

20.8. Stoichiometric Considerations

20.9. Modeling Studies

20.10. Arbuscular Mycorrhizal Fungi

20.11. Saprotrophic Capabilities of Ectomycorrhizal Fungi: The Way Forward

Chapter 21. Magnitude, Dynamics, and Control of the Carbon Flow to Mycorrhizas

21.1. Introduction

21.2. How Does the Physiology and Magnitude of Plant-to-Fungus C Flow Depend on Mycorrhizal Functional Group?

21.3. How Does C Availability (CO2 and Shading) Influence the CARBON Flux Between Plant and Mycorrhizal Fungal Communities?

21.4. To What Extent Is the CARBON Flow between Plant and Symbiotic Fungal Partners Regulated by Reciprocal Nutrient Exchange?

21.5. Conclusions

Chapter 22. Trading Carbon Between Arbuscular Mycorrhizal Fungi and Their Hyphae-Associated Microbes

22.1. Mycorrhizas and Hyphae-Associated Microbes

22.2. Carbon Allocation From Mycorrhizal Fungi to the Hyphae-Associated Microbes in the Hyphosphere

22.3. Involvement of the Hyphae-Associated Microbes in Nutrient Cycling and Carbon Transformation in the Hyphosphere

22.4. Dynamics of the Mycorrhizosphere Associations Under Fluctuating Environmental Conditions

22.5. Unresolved Questions on Trading Carbon and Nutrient Between Mycorrhizas and Hyphae-Associated Microbes

Chapter 23. Immobilization of Carbon in Mycorrhizal Mycelial Biomass and Secretions

23.1. Introduction

23.2. Mycelial Biomass Production and Turnover

23.3. Secretions of Mycorrhizal Mycelia

23.4. Necromass Properties and Decomposition

23.5. Incorporation Into Stable Carbon

23.6. Conclusions

Chapter 24. Mycorrhizal Interactions With Saprotrophs and Impact on Soil Carbon Storage

24.1. Introduction

24.2. Mycorrhizal Fungi As a Source of C in Soil

24.3. Competition for Nutrients and Habitat

24.4. Interactions Among Mycorrhizal Fungi, Soil Fauna, and Soil Organic Carbon

24.5. Conclusion

Chapter 25. Biochar—Arbuscular Mycorrhiza Interaction in Temperate Soils

25.1. Introduction

25.2. Biochar and Mycorrhizas

25.3. Biochar Influences Mycorrhizal Colonization via Its Effects on Soil Properties

25.4. Biochar Influences Plant Response to Mycorrhizal Colonization via Its Impact on the Level of Plant Stress

25.5. Conclusions

Chapter 26. Integrating Mycorrhizas Into Global Scale Models: A Journey Toward Relevance in the Earth’s Climate System

26.1. Introduction

26.2. Existing Model Frameworks

26.3. Critical Mycorrhizal Functions for Terrestrial Biosphere Models

26.4. Mycorrhizal Fungi as Trait Integrators

26.5. Challenges Moving Forward

26.6. Conclusion

Index

Copyright

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List of Contributors

L.K. Abbott,     University of Western Australia, Perth, WA, Australia

S.A. Alghamdi

University of Sheffield, Sheffield, United Kingdom

King Abudul Aziz University, Jeddah, Kingdom of Saudi Arabia

E.B. Allen,     University of California, Riverside, CA, United States

M.F. Allen,     University of California, Riverside, CA, United States

P.M. Antunes,     Algoma University, Sault Ste. Marie, ON, Canada

P. Bonfante,     Università degli Studi di Torino, Torino, Italy

E.R. Brzostek,     West Virginia University, Morgantown, WV, United States

D.D. Cameron,     University of Sheffield, Sheffield, United Kingdom

K.E. Clemmensen,     Swedish University of Agricultural Sciences, Uppsala, Sweden

S.J. Davidson,     University of Sheffield, Sheffield, United Kingdom

R.J. Deckert,     Northern Arizona University, Flagstaff, AZ, United States

I.A. Dickie,     Lincoln University, Lincoln, New Zealand

S. Donn,     Western Sydney University, Penrith, NSW, Australia

B. Drigo

Western Sydney University, Penrith, NSW, Australia

University of South Australia, Mawson Lakes, SA, Australia

C.W. Fernandez,     University of Minnesota, St. Paul, MN, United States

K.J. Field,     University of Leeds, Leeds, United Kingdom

R.D. Finlay,     Swedish University of Agricultural Sciences, Uppsala, Sweden

C.A. Gehring,     Northern Arizona University, Flagstaff, AZ, United States

M. Giovannetti

Università degli Studi di Torino, Torino, Italy

Gregor Mendel Institute (GMI), Austrian Academy of Sciences, Vienna Biocenter (VBC), Vienna, Austria

C. Hamel,     Agriculture and Agri-Food Canada, Quebec, QC, Canada

A. Hodge,     University of York, York, United Kingdom

J. Jansa,     Academy of Sciences of the Czech Republic, Prague, Czech Republic

N.C. Johnson,     Northern Arizona University, Flagstaff, AZ, United States

M.D. Jones,     University of British Columbia Okanagan Campus, Kelowna, BC, Canada

R.T. Koide,     Brigham Young University, Provo, UT, United States

A. Koyama,     Algoma University, Sault Ste. Marie, ON, Canada

T.W. Kuyper,     Wageningen University, Wageningen, The Netherlands

J.R. Leake,     The University of Sheffield, Sheffield, United Kingdom

A. Lehmann,     Freie Universität Berlin, Berlin, Germany

E.F. Leifheit,     Freie Universität Berlin, Berlin, Germany

R.M. Miller,     Argonne National Laboratory, Lemont, IL, United States

M. Miransari,     AbtinBerkeh Scientific Ltd. Company, Isfahan, Iran

R. Pena,     University of Goettingen, Goettingen, Germany

R.P. Phillips,     Indiana University, Bloomington, IN, United States

B.J. Pickles,     University of Reading, Reading, England, United Kingdom

C. Plenchette,     Consultant in Agronomy and Soil Biology and Microbiology, Quetigny, France

J.I. Querejeta,     Spanish Research Council (CEBAS-CSIC), Murcia, Spain

D.J. Read,     The University of Sheffield, Sheffield, United Kingdom

K.T. Rebel,     University of Utrecht, Utrecht, Netherlands

M.C. Rillig,     Freie Universität Berlin, Berlin, Germany

A. Salvioli,     Università degli Studi di Torino, Torino, Italy

S.W. Simard,     University of British Columbia, Vancouver, BC, Canada

K.R. Smith,     West Virginia University, Morgantown, WV, United States

M.M. Smits,     Hasselt University, Diepenbeek, Belgium

J.L. Soong,     University of Antwerp, Wilrijk, Belgium

R.L. Swaty,     The Nature Conservancy’s LANDFIRE Team, Evanston, IL, United States

F.P. Teste

Grupo de Estudios Ambientales, IMASL-CONICET, Universidad Nacional de San Luis, San Luis, Argentina

The University of Western Australia, Crawley (Perth), WA, Australia

K.K. Treseder,     University of California, Irvine, CA, United States

E. Verbruggen,     University of Antwerp, Wilrijk, Belgium

V. Volpe,     Università degli Studi di Torino, Torino, Italy

H. Wallander,     Lund University, Lund, Sweden

G.W.T. Wilson,     Oklahoma State University, Stillwater, OK, United States

Preface

Mycorrhizas have long been recognized for their key roles in plant health and production of food and fiber, but increasingly they are recognized for moving matter and energy through ecosystems. These widespread plant–fungus partnerships function at the interface between living roots and soil. In this regard, they integrate the biotic and abiotic components of ecosystems. The purpose of this book is to review and synthesize information about mycorrhizas and provide new insights about their roles in soil fertility, structure, and carbon storage. Current global carbon models vary widely in their predictions of the dynamics of the terrestrial carbon pool, ranging from a large sink to a large source. A better understanding of mycorrhizal mediation of soil could inform earth system models and may improve the accuracy of their predictions.

The idea for this book arose while planning the Eighth International Conference on Mycorrhizas that was hosted in Flagstaff Arizona in August 2015. The goal of the conference was to unite mycorrhizal science across disciplines and scales. A well-timed query from Marisa LaFleur at Elsevier sparked the idea to integrate the knowledge and perspectives of a broad range of mycorrhizal researchers into a single edited volume designed to explore mycorrhizal mediation of soil processes. After the conference, chapter authors were selected based on their expertise in particular areas so that a broad spectrum of knowledge and ideas is represented in the book.

This has truly been a team effort, with the contributions of more than 50 scientists included in the 26 chapters of the book. We express sincere gratitude to the chapter authors for contributing their expertise, time, and hard work toward synthesizing and communicating complex information and ideas. Without these contributions, this book would not be possible. We also wish to thank our publisher Candice Janco and project manager Emily Thompson who worked patiently and tirelessly throughout the process of creating this book. Finally, we thank the many peer reviewers who contributed their expertise by evaluating each of the chapters. The scientific merit of the final product is much improved through this critical and constructive evaluation.

Nancy Collins Johnson, Catherine Gehring, and Jan Jansa

August 2016

Cover Photos

San Francisco Peaks from Flagstaff Arizona, USA, courtesy of Rick Johnson Photography. Micrographs of Gigaspora gigantea spore, ectomycorrhizal roots, and Rhizophagus sp. hyphal network courtesy of Jan Jansa and Jan Borovička.

List of Scientific Reviewers

Chapter 1

Mycorrhizas

At the Interface of Biological, Soil, and Earth Sciences

N.C. Johnson¹, and J. Jansa²     ¹Northern Arizona University, Flagstaff, AZ, United States     ²Academy of Sciences of the Czech Republic, Prague, Czech Republic

Abstract

Mycorrhizas are among the most widespread and ancient symbioses on Earth. These plant–fungus associations improve nutrition and water relations of most plants. This chapter introduces key features of four main types of mycorrhizas: arbuscular, ericoid, and orchid mycorrhizas, and ectomycorrhizas. The published literature on mycorrhizas has evolved over time. During the past 130  years, the study of mycorrhizas has progressed from descriptions of their nutritional benefits to recognition of their: (1) importance as components of soil fertility, (2) role in structuring and stabilizing soils, and (3) importance for below-ground carbon storage. This book provides a unique perspective of mycorrhizal research advances at the interface of biological, soil, and earth sciences. Its 26 chapters review and synthesize the burgeoning literature about mycorrhizas by bringing together the perspectives and expertise of more than 50 mycorrhizal experts, including some of the pioneers in the field.

Keywords

History of mycorrhizal research; Interdisciplinary sciences; Types of mycorrhizal symbioses; Web of Science

1.1. Successful Coexistence of Plants and Fungi

Mycorrhizas are symbioses between plants and fungi. These nutritional partnerships have evolved independently hundreds of times in multiple lineages in the plant and fungal kingdoms (Bidartondo et al., 2011; Tedersoo and Smith, 2013). Estimates suggest that approximately 50,000 species of fungi form mycorrhizal associations with approximately 250,000 species of plants (van der Heijden et al., 2015). Photosynthetic plants require minerals and water to synthesize organic compounds, but these essential resources are often in limited supply. Mycorrhizas greatly expand the capacity of plants to acquire nutrients and water because fungi have several traits that make them particularly well suited for mining minerals from organic and inorganic substrates and improving the hydraulic properties of soil. Fungal mycelium is composed of fine, threadlike hyphae that can access pores too small for roots to enter; consequently by associating with mycorrhizal fungi, plants substantially increase their contact with mineral particles and organic residues in the soil. Also, fungi have the capacity to synthesize organic acids and other compounds that may depolymerize organic compounds and solubilize mineral nutrients (Smith and Read, 2008). From the perspective of biological markets, plants can often increase their fitness by investing photosynthate in fungal partnerships (Werner et al., 2014). The prevalence of mycorrhizas in all types of vegetation throughout the Earth’s history suggests that this symbiosis is a mechanism for innovation in a constantly changing environment.

Although mycorrhizas have evolved independently many times, four general types are often recognized based upon the identities of the plant and fungal partners (Table 1.1). Arbuscular mycorrhizas, the most ancient and widespread type of mycorrhiza, form between fungi in the phylum Glomeromycota and the majority of plant species, ranging from nonvascular plants to angiosperms (Parniske, 2008; Brundrett, 2009). Ectomycorrhizas form between thousands of Basidiomycota or Ascomycota and many important trees and woody species that are often stand dominants in temperate and boreal forests (Tedersoo et al., 2010; Tedersoo and Smith, 2013). Ericoid mycorrhizas are associations between highly specialized Ascomycota (and a few Basidomycota) and several large families within the order Ericales and also bryophytes that occur in vast areas of tundra, boreal forests, and heathlands (Straker, 1996; van der Heijden et al., 2015). Orchid mycorrhizas are associations between Basidiomycota and all members of the Orchidaceae, a remarkably diverse family encompassing 9% of all angiosperm species (Brundrett, 2009). Orchid mycorrhizas are particularly interesting because orchids have a prolonged seedling stage, during which they are unable to photosynthesize and are entirely dependent upon mycorrhizal symbioses to provide an exogenous supply of carbohydrate (Smith and Read, 2008). In this regard, orchid mycorrhizas represent an unconventional carbon dynamic in which a heterotrophic fungus provides carbohydrate to its plant host. Although orchid mycorrhizas are fascinating, only Chapter 21 will consider orchid mycorrhizas. The other chapters will mainly focus on the arbuscular mycorrhizal (AM), ectomycorrhizal (EcM), and ericoid mycorrhizal (ErM) symbioses because of their key roles as mediators of soil fertility, structure, and carbon storage.

Table 1.1

Four Major Types of Mycorrhizas Distinguished by the Taxa of Host Plants, Fungal Symbionts, and the Biomes Where the Mycorrhizas Are Most Common

Information derived from Smith, S.E., Read, D.J., 2008. Mycorrhizal Symbiosis. Academic Press, New York and van der Heijden, M.G.A., Martin, F.M., Selosse, M.-A., Sanders, I.R., 2015. Mycorrhizal ecology and evolution: the past, the present, and the future. New Phytologist 205, 1406–1423.

1.2. Mycorrhizal Research: Past, Present, and Future

It has long been recognized that fungi inhabit plant roots. Frank coined the term mycorrhiza in 1885; but, many published descriptions of fungal associations with plant roots predate this classic paper (Frank, 1885; Trappe and Berch, 1985). In a subsequent paper, Frank suggested that EcM fungi aided nitrogen uptake from humus and thus increased the growth of host plants (Frank, 1894). This insight initiated a period of experimentation on the nutritional role of EcM symbioses (Harley, 1985). Although AM fungi were described inside plant roots several decades before Frank’s publication, the identity of the fungal partner remained elusive because Glomeromycota are obligate biotrophs that cannot be cultured using traditional mycological methods (Koide and Mosse, 2004). Consequently most of the early studies of mycorrhizas focused on orchid, EcM, and ErM symbioses. The first serious work on the importance of AM symbioses for plant nutrition was published much later by Mosse (1957).

Figure 1.1  Web of Science analysis of the number of publications per year with: mycorrhiza∗ OR ectomycorrhiza∗ as the sole topic search terms. This analysis was performed on July 26, 2016.

Frank recognized the nutritional benefits of mycorrhizas for plants more than 130  years ago, but recognition of their link to soil fertility, structure, and carbon is more recent. A Web of Science analysis of published works since 1900 shows that the number of publications on mycorrhizas remained relatively low until the late 1960s and then steadily increased, with more than 1500 publications on mycorrhizas in 2015 alone (Fig. 1.1). Stunning as this might seem, the growth of total publications about mycorrhizas has closely tracked the exponential growth of all scientific publications, which have been increasing at a rate of approximately 3% annually (Bornmann and Mutz, 2015). More advanced analyses show that the first publications related to both mycorrhizas and fertility occurred in 1976 (Fig. 1.2A), and the first publications related to mycorrhizas and soil structure or soil carbon occurred in the mid-1980s (Fig. 1.2B and C). It is notable that the growth of these three groups of publications is considerably higher (9%, 15%, and 17% for fertility, structure, and carbon, respectively) than the background growth of scientific publications as a whole. This coarse analysis of literature suggests that there is a growing interest in mycorrhizal mediation of soil properties and processes, and mycorrhizas are becoming integrated into the interdisciplinary fields of soil science and earth science.

During the past century, mycorrhizal literature has progressed from descriptions of botanical curiosities to reports that mycorrhizas may be primary controllers of ecosystem responses and feedbacks to climate change (Terrer et al., 2016). The burgeoning literature about mycorrhizas challenges even the most conscientious students and researchers. This book addresses the need for a review and synthesis of recent scientific discoveries and ideas about mycorrhizas.

Figure 1.2  Web of Science analysis of the number of publications per year with the search terms: (A) mycorrhiza∗ OR ectomycorrhiza∗ AND fertile OR fertility OR nutri∗; (B) mycorrhiza∗ OR ectomycorrhiza∗ AND soil OR soils AND structur∗ or stabili∗, (C) mycorrhiza∗ OR ectomycorrhiza∗ AND soil OR soils AND carbon. This analysis was performed on July 26, 2016. Thanks to Joseph Sweet and Mary DeJong for their assistance.

1.3. Goals and Objectives

The purpose of this book is to explore the ways that mycorrhizas facilitate the formation and functioning of soils. Mycorrhizas integrate the biosphere with the atmosphere, lithosphere, and even the hydrosphere (Chapter 2). This book examines mycorrhizas at the interface of biological, soil, and earth sciences. The perspectives of more than 50 experts, including some of the early pioneers in mycorrhizal research, are complied in this volume. Each chapter summarizes the state of the art, and often articulates more questions than answers, largely because relatively few studies have examined mycorrhizas from a soil science or earth science perspective. This perspective is unique and complementary to excellent books that are available on mycorrhizal biology (Smith and Read, 2008), ecology (Allen, 1991; van der Heijden and Sanders, 2002; Horton, 2015), and management for sustainable agriculture(Solaiman et al., 2014).

The book is organized in four sections that explore mycorrhizal mediation of: (I) soil development, (II) fertility, (III) soil structure and plant–water relations, and (IV) carbon flux and soil carbon storage. Section I examines the role of mycorrhizas in soil-forming processes across a range of temporal and spatial scales. In Chapter 2, Leake and Read describe the tandem evolution of plants, mycorrhizal fungi, and soil, and provide evidence that through increased weathering the early mycorrhizal symbioses influenced climate as well as soil development. In Chapter 3, Smits and Wallander delve deeper into the mechanism of mycorrhizal weathering of parent material in modern-day ecosystems. Then in Chapter 4, Johnson, Miller, and Wilson examine how climate, parent material, and topography influence the formation of mycorrhizas and in turn how mycorrhizas influence these three physicochemical soil-forming factors. Finally, Teste and Dickie consider temporal changes in mycorrhizas during the course of ecosystem development in Chapter 5. The goals of Sections II, III, and IV are reviewed in Chapters 6, 13, and 19, respectively.

References

Allen M.F. The Ecology of Mycorrhizae. New York: Cambridge University Press; 1991.

Bidartondo M.I, Read D.J, Trappe J.M, Merckx V, Ligrone R, Duckett G. The dawn of symbiosis between plants and fungi. Biology Letters. 2011;7:574–577.

Bornmann L, Mutz R. Growth rates of modern science: a bibliometric analysis based on the number of publications and cited references. Journal of the Association for Information Science and Technology. 2015;66:2215–2222.

Brundrett M.C. Mycorrhizal associations and other means of nutrition of vascular plants: understanding the global diversity of host plants by resolving conflicting information and developing reliable means of diagnosis. Plant and Soil. 2009;320:37–77.

Frank A.B. Uber die auf wurzelsymbiose beruhende ernahrung gewisser Baume durch unterirdische pilze (on the nutritional dependence of certain trees on root symbiosis with belowground fungi). Berichte der Deutschen Botanischen Gesellschaft. 1885;3:128–145.

Frank A.B. Die bedeutung der mykorrhiza-pilze fur die gemeine Kiefer. Forstwissenschaftliches Centralblatt. 1894;16:183–190.

Harley J.L. Mycorhiza: the first 65 years, from the time of Frank till 1950. In: Molina R, ed. 6th North American Conference on Mycorrhizae. Bend, Oregon: Forest Research Laboratory; 1985:26–33.

Horton T.R, ed. Mycorrhizal Networks. Ecological Studies. vol. 244. Springer; 2015.

Koide R.T, Mosse B. A history of research on arbuscular mycorrhiza. Mycorrhiza. 2004;14:145–163.

Mosse B. Growth and chemical composition of mycorrhizal and non-mycorrhizal apples. Nature. 1957;179:923–924. .

Parniske M. Arbuscular mycorrhiza: the mother of plant root endosymbioses. Nature Reviews Microbiology. 2008;6:763–775.

Smith S.E, Read D.J. Mycorrhizal Symbiosis. New York: Academic Press; 2008.

Solaiman Z, Abbott L.K, Ajit V, eds. Mycorrhizal Fungi: Use in Sustainable Agriculture and Land Restoration. Springer; 2014.

Straker C.J. Ericoid mycorrhiza: ecological and host specificity. Mycorrhiza. 1996;6:215–225.

Tedersoo L, May T.W, Smilth M.E. Ectomycorrhizal lifestyle in fungi: global diversity, distribution, and evolution of phylogenetic lineages. Mycorrhia. 2010;20:217–263.

Tedersoo L, Smith M.E. Lineages of ectomycorrhizal fungi revisited: foraging strategies and novel lineages revealed by sequences from belowground. Fungal Biology Reviews. 2013;27:83–99.

Terrer C, Vicca S, Hungate B.A, Phillips R.P, Prentice I.C. Mycorrhizal association as a primary control of the CO2 fertilization effect. Science. 2016;353:72–74.

Trappe J.M, Berch S.M. The prehistory of mycorrhizae: A.B. Frank’s predecessors. In: Molina R, ed. 6th North American Conference on Mycorrhizae. Bend, Oregon: Forest Research Laboratory; 1985:2–11.

van der Heijden M.G.A, Martin F.M, Selosse M.-A, Sanders I.R. Mycorrhizal ecology and evolution: the past, the present, and the future. New Phytologist. 2015;205:1406–1423.

van der Heijden M.G.A, Sanders I.R, eds. Mycorhizal Ecology. Berlin, Heidelberg, New York: Springer; 2002.

Werner G.D.A, Strassmann J.E, Ivens A.B.F, Engelmoer D.J.P, Verbruggen E, Queller D.C, Noe R, Johnson N.C, Hammerstein P, Kiers E.T. The evolution of microbial markets. Proceedings National Academy of Science United States of America. 2014;16:1237–1244.

Section I

Mycorrhizal Mediation of Soil Development

Outline

Chapter 2. Mycorrhizal Symbioses and Pedogenesis Throughout Earth’s History

Chapter 3. Role of Mycorrhizal Symbiosis in Mineral Weathering and Nutrient Mining from Soil Parent Material

Chapter 4. Mycorrhizal Interactions With Climate, Soil Parent Material, and Topography

Chapter 5. Mycorrhizas Across Successional Gradients

Chapter 2

Mycorrhizal Symbioses and Pedogenesis Throughout Earth’s History

J.R. Leake, and D.J. Read     The University of Sheffield, Sheffield, United Kingdom

Abstract

The evolution of land plants and of their symbiosis with soil fungi to form mycorrhiza-like associations were pivotal steps in Earth's history. They enabled the establishment of terrestrial ecosystems in which plants of increasing biomass, rooting depth, nutrient demand, and ability to capture and convert solar energy into chemical energy helped to drive mineral weathering and soil formation. Here we review evidence of the coevolutionary history of land plants and mycorrhizal symbioses, placing particular emphasis on their likely impacts upon silicate weathering, pedogenesis, and the resulting interlinked changes in the biogeochemical cycles of carbon, silicon, calcium and phosphorus. These, in turn, affect atmospheric carbon dioxide concentrations, ocean productivity, and climate over geological time. We conclude that, over time, coevolutionary advances in plants and fungi have increased photosynthate fluxes through mycorrhizas into soils, intensifying pedogenic processes, and mineral weathering, thereby strengthening the biosphere–geosphere–ocean–atmosphere interactions that regulate the Earth’s climate.

Keywords

Biosphere–geospherse–ocean–atmosphere feedbacks; Evolution of biogeochemical cycles; Mineral weathering; Pedogenesis; Plant and fungal evolution; Symbioses

2.1. The Importance of Reciprocal Effects of Plant–Mycorrhiza–Soil Interactions in the Evolution and Assembly of Terrestrial Ecosystems

Soil provides the foundation of terrestrial biomes, being both the product of biosphere–geosphere–atmosphere interactions, and a pivotal factor in controlling the assembly of terrestrial ecosystems and their roles in carbon (C) and nutrient cycles (Jenny, 1980; Bardgett, 2005). The biological, chemical, and physical properties of soils and the functions they provide underpin or directly deliver most of the ecosystem services upon which humans depend, including food, fiber, biofuels, fresh water, and regulating services such as hydrological functioning affecting flooding incidence, greenhouse gas emissions, and climate (MEA, 2005). The importance of the biotic component in soil development was made explicit in Jenny’s model (1941, 1980), which defined the five factors that drive pedogenesis. This model sees soil (S) as a function (f) of climate (c), organisms (or), relief (topography) (r), parent material (p) and time (t), together with stochastic factors (…) such as fires and floods, so that S  =  f(cl, or, r, p, t,…). In this model, organisms are recognized both as drivers of soil development, and responsive to the environmental context in which they occur and the soils they have helped to create, so that Or  =  f(s, cl, r, p, t,…). Jenny (1941) emphasized that soil is an open system in which substances may be added or removed, and that soil and environment form coupled systems that can be changed when the functions that have created them change. Together these insights provide a conceptual model of pedogenesis with far-reaching consequences both for considering the effects of terrestrial organisms and their evolution on processes of soil development, and their long-term effects and reciprocal interactions with the wider environment. Soil plays an especially important role in global C cycling, storing about 75% of the organic C stock in contemporary terrestrial ecosystems (Hiederer and Köchy, 2011; Scharlemann et al., 2014). This is approximately three times the preindustrial atmospheric carbon dioxide (CO2) C stock of the late Holocene epoch. This reflects the accumulation of plant photosynthate–C stabilized in soil organic matter pools through plant–microbial interactions.

Whereas the importance of plants as agents of soil formation were well established after Jenny (1941), the potential role of coevolutionary advances in the almost universal symbiosis between plants and mycorrhizal fungi in impacting soil forming processes and global biogeochemical cycles over the past 400-500  Ma, has not been considered in depth previously. Nonetheless, reciprocal effects of plants on soil development and of soil properties on plants in different climate zones underpins our understanding of the present day global distribution of soil types, biomes, dominant types of mycorrhizal plant communities (Read, 1991; Read et al., 2004; Soudzilovskaia et al., 2015), and their specific effects on soil C and nitrogen (N) cycling processes (Clemmensen et al., 2013; Augusto et al., 2015). Contemporary global patterns of plant-root colonization intensity by arbuscular mycorrhizal (AM) fungi, and the independently and more recently evolved ectomycorrhizal (EcM) fungi, are similarly explained by their climate and soil chemistry type preferences (Soudzilovskaia et al., 2015). However, only recently have the potential long-term reciprocal effects of evolutionary advances in land plants and mycorrhizal symbionts on biogeochemical cycles, the atmosphere, and climate been recognized (Taylor et al., 2009), and the role of evolution in processes of pedogenesis started to be investigated (Morris et al., 2015). In turn, changes caused by advances in plants and their symbionts will have fed back to influence both the evolution of terrestrial ecosystems and their roles in pedogenesis and biogeochemical cycles.

Two important questions arise from reciprocal plant–soil interactions involving mycorrhizas. First, how has the coevolution of plants and mycorrhizal fungi changed the rates and processes of soil formation and altered global biogeochemical cycles through the period of Earth’s history during which land plants and their symbionts have evolved and diversified? Second, how have changes in the Earth’s system and climates over the history of land–plant evolution, in part caused by effects of pedogenesis on global biogeochemistry, influenced the trajectory of evolutionary advances in plant and mycorrhiza functional traits?

To address these questions, we integrate advances in palynology, paleontology, paleopedology, and phylogenetics, with experimental studies of plant and mycorrhizal fungal below-ground C allocation and mineral weathering under past and present atmospheric CO2 concentrations, in taxa selected across key nodes of evolutionary advancement. This synthesis seeks to better understand the evolutionary history of mycorrhizas and how their role in pedogenesis has changed with evolutionary advancement in both plant and fungal partners. We consider how these organisms and their interactions with soils have bioengineered the planet through feedbacks on biogeochemical cycles of calcium (Ca), phosphorus (P), C, and silicon (Si). These regulate Earth’s atmospheric CO2 concentration and climate over geological timescales via the geochemical C cycle, in turn affecting rates of terrestrial and marine productivity (Berner, 2006; Algeo and Scheckler, 1998; Lenton, 2001; Taylor et al., 2009).

2.2. Plants and Mycorrhizas as Agents of Pedogenesis: Coupling Plant Photosynthate Energy to the Actions of Fungal Mycelial Networks

Central to the role of plants and associated mycorrhizal fungi in pedogenesis is their transformative effects on soil chemistry and physical properties through their inputs of organic matter, selective uptake of elements and water, and capacities to directly and indirectly accelerate chemical and physical weathering processes that liberate essential nutrient elements from rocks and minerals (Haselwandter, 2008; Leake et al., 2008; Taylor et al., 2009; Brantley et al., 2011; Chapters 3 and 4). Mycorrhizas can affect these actions directly and indirectly through their effects in improving plant nutrition, biomass production, and plant health. Their effects are intrinsically scale-dependent in that the evolution of larger plants with deeper roots (Algeo and Scheckler, 1998; Morris et al., 2015) and more extensive mycorrhizal hyphal networks (Quirk et al., 2012) tend to have larger effects on mineral weathering, in assisting the formation of pedogenic minerals such as clays, in accumulating soil organic matter, and in developing soil structure such as soil aggregates and pores. In turn, these factors control the core soil functions including C, water, and nutrient storage capacity and some of the major pathways by which particles, fluids, and gases pass into and out of soil. These soil functions will have fed back to influence the assembly of terrestrial ecosystems as plants and mycorrhizal fungi have evolved, and selected for traits that increase their fitness through the mutualistic interactions between the plant and fungal partners.

The driving force behind the effects of the rise of terrestrial ecosystems on soil and biogeochemistry is conversion of atmospheric CO2 into organic C by photosynthesis, empowering biomass accumulation, proton-pumping, and secretion of organic acids and enzymes such as reductases that change the solubility of elements and together enable the selective uptake of essential nutrients from soils via mycorrhizal fungi and roots (Taylor et al., 2009). About 85% of extant vascular plant species form mycorrhizal associations (Brundrett, 2009), typically investing between 5% and 15% of their photosynthate in supporting mycorrhizal fungal partners to facilitate nutrient and water uptake from soil. The C energy hypothesis links below-ground allocation of photosynthate to mineral weathering and element mass-transfers by mycorrhizas (Leake et al., 2008; Quirk et al., 2014). This underpins C-for-nutrient exchanges between autotrophic plants and mutualistic soil fungi, and defines the bioenergetics of mycorrhizal mycelial networks of power and influence that are typically two to three orders of magnitude longer than roots (Leake et al., 2004). Globally, we estimate mycorrhizal hyphae in the top 10  cm of soils extend over distances of approximately 4.5  ×  10¹⁷  km, which is half the width of our galaxy (9.5  ×  10¹⁷  km), and the surface area of these hyphae, assuming a mean diameter of only 4  μm, is nearly 2.5 times the area of the continental land masses¹. Most of this mycelium is relatively short-lived and replaced several times per year.

This vast mycorrhizal hyphosphere interacts with soil minerals, organic matter, and other soil microorganisms in ways that inevitably affect the chemical, physical, and biological properties of soils. C flow through mycorrhizal hyphae into the mycorrhizosphere supports other microorganisms, some of which operate synergistically in enhancing nutrient uptake (Chapters 9 and 22). AM fungal mycelium supplies C that supports phosphate-solubilizing and plant-growth promoting rhizobacteria such as Pseudomonas and Burkholderia that ultimately impact soil processes and soil functions, such as mineralization of organic P (Zhang et al., 2014, 2016), and weathering of mineral P, such as the Ca phosphate apatite via local acidification (Taktek et al., 2015). The effects of mycorrhizal plants on pedogenesis were therefore conceptualized by Brantley et al. (2011) as solar to-chemical conversion of energy by plants regulates flows of carbon, water, and nutrients through plant-microbe soil networks, thereby controlling the location and extent of biological weathering. This is consistent with the suggestion that photosynthate allocation affects landscape evolution, the potential energy of present day net primary production being three to seven orders of magnitude greater than the kinetic energy generated by tectonic uplift and the exogenic forces of denudation that have traditionally been considered to control changes in topography over time (Phillips, 2009). If only a small percentage of plant photosynthate allocated to roots and mycorrhizas is directly involved in processes of geomorphological significance, such as physical or chemical weathering of rocks and minerals, the effects of mycorrhizas on soils and landscapes would be extremely important over geological time.

Key to these long-term pedogenic and global biogeochemical effects of the coevolution of plants and mycorrhizal fungi is their enhancement of weathering of continental silicate rocks. Release of Ca and magnesium (Mg) into the oceans from weathering of terrestrial silicate rocks such as basalt ultimately removes CO2 from the atmosphere for millions of years in the geochemical C cycle (Fig. 2.1), which precipitates marine carbonates such as limestone and chalk until these rocks are either uplifted onto land or subducted and CO2 is released by volcanic degassing (Berner, 2006). In addition, the dissolution of continental silicates and the fluvial export of dissolved and particulate Si into the oceans supports the productivity and C sequestration by marine organisms that build Si skeletons, such as sponges that date back to at least 600  Ma (Yin et al., 2015), Radiolaria that first appeared over 540  Ma (Braun et al., 2007) ago, and diatoms that first evolved no earlier than 250  Ma ago (Medlin, 2011).

According to Conley and Carey (2015), the rise and expansion of grassy biomes that now dominate the terrestrial Si cycle led to increased rates of dissolved Si transport to the oceans, which in turn supported the coincident rise, over the past 65  Ma, of the diatoms that contribute about 50% of marine net C fixation. Intriguingly, AM fungi may themselves be involved in the global Si cycle because strong linear relationships have been found between P and Si contents of AM fungal vesicles (Olssen et al., 2011). Although it remains to be proven whether these fungi are directly involved in Si uptake by plants, evidence is emerging of their involvement in processes of silicate weathering. Dissolution and trenching of primary silicate minerals by AM fungi growing in association with liverworts and trees has been demonstrated by Quirk et al. (2014, 2015). These observations suggest roles for plant–mycorrhiza associations in the global biogeochemical cycling of Si, as well as of P and Ca. These activities would be expected to have influenced terrestrial and marine productivity, as well as atmospheric CO2 concentrations, with effects that are likely to have become increasingly important from as early as the Ordovician period when liverwort-like plants first evolved and likely developed symbiotic associations with soil fungi (Section 2.3).

Figure 2.1  The effects of evolutionary advancement in plants and mycorrhizas in the geochemical carbon cycle, increasing the weathering of calcium (Ca)-, phosphorus (P)-, and silicon (Si)-bearing minerals and generating clays. Plants and their mycorrhizal fungi have increased the rates of dissolution of continental silicates especially calcium silicate (CaSiO 3 ), and apatite (Ca phosphate-CaPO 4 ), but a portion of the Ca, P, and Si released from rocks is washed into the oceans where these elements increase productivity. Some of the Ca and P end up in limestone and chalk deposits produced by marine organisms such as corals and foraminifera, thereby sequestering carbon dioxide (CO 2 ) that was dissolved in the oceans into calcium carbonate (CaCO 3 ) rock for millions of years. Dissolved Si is used in sponges, radiolarians, and diatoms that can accumulate on the sea floor. The ocean sediments are recycled by subduction or uplift by tectonic forces, with volcanic degassing and eruptions of base-rich igneous rocks such as basalt returning Ca, P, Si, and other elements back to the continents, thereby reinvigorating ecosystems with new nutrient supplies through weathering. Note for simplicity that magnesium is not shown in the figure, but follows parallel pathways to Ca and is co-involved in sequestering CO 2 into dolomitic limestones. aq , Liquid state; g , gaseous state.

In considering the broader effects of plant evolution on biogeochemical cycling of silica and ocean productivity, Trembath-Reichert et al. (2015) indicate that many extant members of early diverging land plant lineages, some of which were dominant treelike components of Devonian and Carboniferous terrestrial floras, are involved in amorphous silica (SiO2) biomineralization and cycling. These include lycophytes and monilophytes in the Marratiales, Equisetales, and Osmundales, some, but not all, of which may have formed mycorrhizal partnerships with AM fungi.

Plants in partnership with mycorrhizal fungi contribute to a number of other processes affecting weathering and pedogenesis (Taylor et al., 2009). Roots and mycorrhizal hyphae directly interact with soil minerals through exudation of protons associated with cation uptake and low–molecular-weight organic chelators, both of which facilitate mineral dissolution, ion exchange, and element leaching through soil profiles. Roots and mycorrhizal fungal exudates provide C sources that support specialist mycorrhizosphere bacteria such as species of Pseudomonas involved in mineral dissolution (Zhang et al., 2014, 2016) and plant growth promotion (Chapter 22). The anchoring and binding of particles by roots and mycorrhizal hyphae stabilizes soil, thereby intensifying chemical alteration by preventing erosion and reburial in less chemically and biologically reactive environments. Mycorrhizal fungi in the Glomeromycota are also strongly implicated in contributing directly to soil organic matter (Verbruggen et al., 2016) through hyphal enmeshment, generating water-stable macroaggregates that store organic C (Wilson et al., 2009), improve soil drainage, and reduce surface run-off and erosion. Studies that have attributed C stabilization to an AM fungal hydrophobic protein glomalin, which is a holologue of heat shock protein 60 and mainly bound to the hyphae (Bendini et al., 2009; Hammer and Rillig, 2011), remain contentious because resolving the relative importance of hyphae versus their products on soil properties is difficult. In parallel, EcM fungi, through selective uptake of the most labile forms of organic N and P enhance the recalcitrance of soil organic matter (Clemmensen et al., 2013) and secrete siderophores and organic acids that facilitate mineral dissolution (Haselwandter, 2008). Inputs of EcM fungal necromass that is often rich in polyphenolic acids such as tannins and melanin may also be important in C sequestration. In addition, the extent to which mycorrhizas increase plant growth, productivity, biomass, and resultant nutrient and hydrological fluxes through evapotranspiration will contribute incrementally to the overall effect of plants on pedogenesis (Taylor et al., 2009).

2.3. Evolutionary Origins of Plants and Mycorrhizas

Important developments in our understanding of the evolution of early land plants and fungal symbionts in soil have come from the fossil record, phylogenetics, and molecular genetics, giving increasingly strong evidence of coevolution of plant–fungal symbioses in the Middle Ordovician era, 470  Ma. The first land plants (embryophytes) evolved from a charophycean algal ancestor that was preadapted with signaling pathways involved in initiating symbiosis with fungi, including strigolactones (Delaux et al., 2015). Phylogenetic and molecular genetic information supports the view that bryophytes were the earliest land plants, liverworts being the basal group, with hornworts probably being the sister group to vascular plants (Qiu et al., 2006). Extant basal liverworts ubiquitously host symbiotic fungi (Bidartondo et al., 2011) in mutualistic mycorrhiza-like partnerships in which plant photosynthate is exchanged for fungal-acquired soil nutrients including P and N (Field et al., 2014, 2015). The earliest fossil evidence of land plants comes from spores, and the nature of early terrestrial plant community components, including cyanobacteria (Strother and Wellman, 2016), putative lichens, cryptophytes, and basal tracheophytes, have been reviewed (Steemans et al., 2010; Edwards et al., 2014, 2015; Gerrienne et al., 2016). The earliest putative fossil of the obligately biotrophic and asexual Glomeromycota fungi is provided by spores that date to the same epoch 460-455  Ma (Redecker et al., 2000). In slightly more recent rocks at 450-440  Ma, trilete spores that are associated with vascular land plants have been found (Steemans et al., 2009). However, the earliest fossil of a liverwort thallus dates only to the Early Devonian age (411-407  Ma) (Guo et al., 2012) with a second, better preserved and different species found in the Middle Devonian era, which shows both a few rhizoids and some fungi, but mutualistic associations with fungi have not been reported (Hernick et al., 2008).

The first vascular plants (tracheophytes) date to about 430  Ma in the Silurian period with the appearance of the diminutive sporophytes of Cooksonia, which were only a few centimeters tall. The basal portions of these plants, which may be thalloidlike gametophytes (Gerrienne et al., 2006), have been found in a more recent deposit dated to approximately 415  Ma, and indicate very shallow depth of interaction with soil, but the preservation has been too poor to resolve whether they formed symbioses with fungi. By the late Silurian age, more advanced early trachaeophytes, Rhynia and Zosterophyllum, which had better developed vascular tissues, lacked roots but had prostrate rhizomes with rhizoids, and lacked leaves but had stomata and much more robust shoots than Cooksonia, appeared (Edwards et al., 2015). In the same community, one of the earliest lycophytes, Drepanophycus, was found. Like its sister genus Baragwanathia, which first appeared about 425  Ma (Rickards, 2000), Drepanophycus has both microphylls and adventitious rootlike appendages arising directly from the substantial aerial shoots that attained lengths of up to over 1  m (Edwards et al., 2015). Despite these anatomical advances, the pre-Devonian mycorrhizal status of all these plants remains unknown.

The earliest unequivocal fossil evidence for mycorrhiza-like symbiotic fungal associations with land plants (Remy et al., 1994) comes from the early Devonian Rhynie Chert (411.5  Ma), at a time when, with the exception of the rootlike appendages of the sporophytes of lycophytes, plants had not evolved roots (Strullu-Derrien et al., 2015). The exceptionally well-preserved early land-plant flora at this site has enabled detailed studies of plant–fungal interactions at the cellular scale, including studies of fungal vesicles and highly branched fungal structures in cells that appear to be arbuscules, which in modern plants provide the major interfaces for nutrient-for-C exchange in the symbiosis, together with spores that are definitively members of the Glomeromycota (Remy et al., 1994; Dotzler et al., 2006, 2009; Strullu-Derrien et al., 2014). Spores of the derived Glomeromycota genera Acaulospora and Scutellospora in the Rhynie Chert reveal remarkably little change to these fungal structures over more than 400  million years (Dotzler et al., 2006, 2009) and establish that major diversification of AM fungi had occurred by the early Devonian age. This corroborates that these plant–fungal symbioses coevolved with earlier land plants through the epochs from which we have no fossil record of plant–fungal interactions.

The mycorrhizal fungal partnerships in the Lycopodiophyta are especially critical in understanding the evolutionary significance of these symbioses in land-plant evolution and Earth’s history. This is the earliest group of vascular plants for which we have records of rootlike structures, dating back to the Silurian age (Kenrick and Strullu-Derrien, 2014), together with substantial shoots with the earliest microphyll leaves. The earliest fossil record of fungal symbiosis with lycopods comes from rhizomes supporting roots of Asteroxylon mackiei in the Rhynie Chert, but the aseptate fungal partner found in the prostrate rhizomes is enigmatic, chytrid-like, possibly zoosporic, and appears to be neither of Mucoromycotina nor Glomeromycota affinities (Strullu-Derrien et al., 2015). The functional role of the fungal partner is unclear but on the basis of the available evidence cannot be assumed to be a mutualistic symbiont. The absence of evidence of AM symbionts in Asteroxylon is notable, and surprising, in view of the host plant typically being of substantial biomass and nutrient demand, having shoots up to 12  mm wide and up to at least 45  cm long in an environment in which co-occurring early vascular plants like Horneophyton were forming mutualistic associations with both groups of endosymbiotic fungi: Aglaophyton major associated with AM fungi and contained arbuscules, and Nothia aphylla hosted fungal partners (Krings et al., 2007) that have been interpreted as likely Mucoromycotina (Selosse and Strullu-Derrien, 2015). From the late Silurian age, lycopsids advanced in biomass, rooting depth, and structural complexity, and in the early Devonian period, 411  Ma, Drepanophycus had developed rooting axes with vascular tissues that extended decimeters down into soil, and from which finer bifurcating rootlets of 0.4–0.7  mm wide and 5–6  mm long emerged laterally (Matsunaga and Tomescu, 2016). The rootlets either lacked root hairs or these have not been preserved. By the Middle Devonian era (398-385  Ma), lycophytes had already achieved trunks more than 4  m long and 11  cm in diameter (Stein et al., 2012). They were minor components of the earliest forest ecosystems that were dominated by more than 8-m tall cladoxylopsid tree-fern–like plants and aneurophytalean progymnosperms (Stein et al., 2012). By the Carboniferous era, over 300  Ma, arborescent lycopsids had become dominant components of extensive swamp forest ecosystems, rising to over 30  m tall with stems of 1  m in diameter (Krings et al., 2011). They were then major players in soil C sequestration, including the formation of coal, and clearly were important in pedogenesis. Well-preserved fossils of the rootlike appendages of an arborescent lycopsid in the Carboniferous period (313-304  Ma), has shown evidence of AM symbiosis with arbuscules, vesicles, and spores apparently of the Glomeromycota type (Krings et al., 2011). In contemporary wetland forests in the southern United States, the dominant trees in the permanently waterlogged sites form AM associations, confirming that waterlogging is not incompatible with this symbiosis (Jurgensen et al., 1997).

The arborescent lycophytes have since become extinct. Cytological studies of fungal symbionts in extant lycophytes have noted unusual features that are distinct from Glomeromycota type AM associations and have been followed with the molecular studies by Rimington et al. (2015). They investigated sporophytes of 20 lycopod species, and AM fungi were found in seven of these, four of which hosted Mucoromycotina and three that hosted Glomeromycota. The incidence of fungal colonization of these plants was surprisingly low, with only 17 out of 101 plant samples apparently supporting symbiotic fungi. Because the ability to form mycorrhiza-like associations with soil fungi first occurred with the gametophytes of nonvascular plants, the role of mycorrhiza in the gametophytes of early lycopsids is of particular interest but not apparently preserved in the fossil record. Most extant lycophytes have subterranean achlorophyllous mycoheterotrophic gametophytes that are obligately dependent on their mycorrhizal fungal partners for growth, sexual reproduction, and establishment of their autotrophic sporophyte generations (Winther and Friedman, 2007), but this likely evolved in response to the increasing competition from closed canopies developed under faster-growing modern plants.

In contrast to the lycopods, the later diverging Monilophytes (ferns and fern allies) show a much higher occurrence of AM symbiosis in extant taxa, with the exception of the basal Equisetopsida, which diverged in the Devonian age, and in which the single extant lineage Equisetum shows inconsistent and generally low colonization by AM fungi (Hodson et al., 2009). The Equisetopsida rose to global importance in the Carboniferous period both as forest understory and in the form of giant horsetails like Calamites, and are likely to have played a significant role in the silica cycle (Trembath-Reichert et al., 2015); however, on the basis of current evidence, mycorrhizas are unlikely to have played a role in this. Within extant fern species, 33 out of 58 samples formed arbuscular mycorrhizas, with a very clear specificity to Glomeromycota and only the derived genus Anagramma out of 18 fern species containing Mucoromycotina, and in this case as a dual partnership with Glomeromycota (Rimington et al., 2015). The extent of compatibility of more advanced vascular plant lineages with Mucoromycotina remains to be thoroughly investigated, but there is emerging evidence that this symbiosis may be widespread (M. Bidartondo pers. comm).

The earliest forest ecosystems in the Middle Devonian age (398-385  Ma) were dominated by more than 8-m tall cladoxylopsid tree-fern–like plants and aneurophytalean progymnosperms (Stein et al., 2012) that share intermediate features between ferns and gymnosperms (Stein et al., 2007). The rise of the first forests with plants that produced woody tissues (lignophytes) and substantial roots that penetrated over 1  m into the soil heralded a period of intensified silicate mineral weathering with organic and inorganic C sequestration, drawing down over 90% of atmospheric CO2, mainly into marine carbonate sediments (Figs. 2.1 and 2.2), and nearly doubling atmospheric oxygen concentrations from 400-350  Ma (Royer et al., 2004; Berner, 2006; Algeo and Scheckler, 1998; Lenton, 2001; Morris et al., 2015). Whereas there is no fossil evidence for mycorrhizas in the first forests, the presence of AM fungi in both phylogenetically ancestral and later diverging groups to cladoxylopsids and aneurophytes, and the constancy of mycorrhization in present day trees, strongly implicates the symbionts in facilitating fulfillment of the nutrient demands of these increasingly large plants as they evolved. The rise of the Middle Devonian forests has been linked to the development of new major soil orders and soil processes, including organic rich histosols and clay-rich alfisols (Morris et al., 2015). These innovations reflect both the increasing quantities of organic matter sequestered in soils as a result of the large biomass, litter inputs, and likely the C allocation to mycorrhizal partners from trees causing intensification of weathering processes and stabilization of soil, leading to neoformed expandable mixed-layer clays of the smectite group (Morris et al., 2015) (Figs. 2.1 and 2.2). Although smectite clays have also been formed on the planet Mars, apparently in the absence of life (Mahaffy et al., 2015), this probably took billions of years of chemical weathering, whereas on Earth these clays are most strongly developed and formed quickly under forests that act as clay mineral factories (Kennedy et al., 2006). This is consistent with the mineralogical shift in paleosols from mica, illite and chlorite toward increasing dominance by smectite and kaolinite from the Middle Devonian age onwards, when forest ecosystems started to become locally dominant (Morris et al., 2015).

The phylogeny and divergence times of the next major land plant group, the gymnosperms, has been evaluated using nuclear genes (Lu et al., 2014) indicating the crown age of the group is about 350  Ma, with all five extant lineages (cycads, ginkgos, cupressophytes, Pinaceae, and gnetophytes) originating before 300  Ma. However, the crown ages of all families except Ginkgoaceae and Sciadopityaceae are younger than 200  Ma, suggestive of major extinction events possibly caused by extreme cooling in the Carboniferous age (Lu et al., 2014) after the draw-down of atmospheric CO2 into carbonate rocks. The cycads (Cycadaceae and Zamiaceae) that exclusively form AM symbioses (Fisher and Vovides, 2004) are confirmed as basal groups, but most extant species diversified mainly over the past 150  Ma and were followed by the AM Ginkoaceae. The next diverging group was the Pinaceace, which have developed mycorrhizas with the independently evolved EcM fungi from a wide diversity of basidiomycete and ascomycete fungi and have risen to dominance in the Boreal forest region in the Northern Hemisphere (Fig. 2.2). However, in its sister group, the Gnetales, the basal Ephedra together with Welwitschia form arbuscular mycorrhizas, whereas Gnetum is EcM, sometimes specialized on a clade of hypogeous basidiomycetes in the Boletales that have been shown to facilitate P release from apatite (Bechem and Alexander, 2012). All of the later diverging groups retain associations with AM fungi (Araucariaceae and its sister Podocarpaceae, the Sciadopidaceae, and the Cephalotaxaceae-Taxaceae that are sister to the Cupressaceae) (Lu et al., 2014).

Figure 2.2  Key stages in the evolution of plants and mycorrhizas and changes in atmospheric carbon dioxide (CO 2 ) (based on modeled estimate ranges from Berner, 2006 ; in Field et al., 2012 ) linked to changes in rates of mineral weathering and episodic volcanic degassing of CO 2 over the past 450   million years. Only the most important types of plants are shown with respect to key evolutionary advances in structure and mycorrhizal associations. The greening of the continents with the evolutionary advance in plants from microbial mats of algae to liverworts with rhizoids and mycorrhiza-like partnerships with Mucoromycetes and Glomeromycota, to vascular plants with roots and mycorrhizas and the development of arborescence in the first forests led to progressive intensification of mineral weathering (see also Fig. 2.1 ). The rise of forest ecosystems initially dominated by aneurophytalean progymnosperms in which roots (and mycorrhizas) could interact with soil to depths of 1   m or more coincides with a rapid fall in atmospheric CO 2 , in the Devonian ( dotted line ), and the sequestering of carbon (C) in limestone and coal in the Carboniferous era. The rise of angiosperms and ectomycorrhizal associations with both angiosperms and gymnosperms has further intensified weathering since the Cretaceous ( dotted line ). Cam , Cambrian; Carb , Carboniferous; Dev , Devonian; Jur , Jurassic; Neo , Neogene; Ord , Ordovician; Pal , Paleogene; Per , Permian; Pre-Cam , Precambrian; Sil , Silurian. The key stages in greening of the earth by different dominant landscapes are adapted from Gerrienne et al. (2016).

The most recent, successful, and diverse group of land plants, the Angiosperms that have risen from about 167 to 199  Ma and rapidly diversified from the Cretaceous period (Bell et al., 2010) to dominate most of the world’s biomes today (Fig. 2.2), are strongly mycorrhizal, with over 85% of a sample of over 10,000 species forming the symbiosis (Brundrett, 2009). AM fungi associate with 72% of plant species, including many temperate and tropical trees as well as forbs and grasses. EcM symbiosis involving both basidiomycete and ascomycete fungi is found in only 2% of plant species, although most of these are comprised of trees and woody shrubs, so this is the second most important type of mycorrhiza in terms of global plant biomass and extent of pedogenic processes at biome scales (Read, 1991). Because EcM fine roots are enveloped by a fungal sheath, the establishment of this kind of mycorrhiza was the most profound alteration in root functioning to occur in plant evolutionary history with the plant interface with soil being entirely mediated by the fungal partners and has far-reaching implications for soil biogeochemistry and weathering processes. Of the other kinds of angiosperm symbioses, ericoid mycorrhizas, which are found in 1.4% of angiosperm species, are the most important for facilitating organic C sequestration in soils and pedogenic processes such as podsolization and metal solubilization via siderophores (Haselwandter, 2008). However, they have low rates of photosynthesis and low productivity as a consequence of growing in nutrient-poor and climatologically harsh environments such as montane and tundra environments that constrain their rates of pedogenesis. Orchids, most of which are rare, and a high proportion of which are epiphytes, comprise