Molecular Mycorrhizal Symbiosis

Francis Martin, Francis Martin

• Publisher: Wiley-Blackwell
• Year: 2016
• ISBN:
  9781118951422
• Edition: 1
• Topic: Biowissenschaften
• Subtopic: Mikrobiologie

Recent years have seen extensive research in the molecular underpinnings of symbiotic plant-fungal interactions. Molecular Mycorrhizal Symbiosis is a timely collection of work that will bridge the gap between molecular biology, fungal genomics, and ecology. A more profound understanding of mycorrhizal symbiosis will have broad-ranging impacts on the fields of plant biology, mycology, crop science, and ecology.

Molecular Mycorrhizal Symbiosis will open with introductory chapters on the biology, structure and phylogeny of the major types of mycorrhizal symbioses. Chapters then review different molecular mechanisms driving the development and functioning of mycorrhizal systems and molecular analysis of mycorrhizal populations and communities. The book closes with chapters that provide an overall synthesis of field and provide perspectives for future research.

Authoritative and timely, Molecular Mycorrhizal Symbiosis, will be an essential reference from those working in plant and fungal biology.

SECTION 1
Structure and phylogeny of mycorrhizal symbioses

CHAPTER 1
Origins of the mycorrhizal symbioses

Christine Strullu‐Derrien^1,2, Paul Kenrick², and Marc‐André Selosse^3,4

¹ INRA, UMR 1136, INRA‐Université de Lorraine Interactions Arbres‐Microorganismes, Laboratoire d’excellence ARBRE, INRA‐Nancy, Champenoux, France

² Department of Earth Sciences, The Natural History Museum, London, UK

³ Institut de Systématique, Évolution, Biodiversité (ISYEB), Muséum national d’Histoire naturelle, Paris, France

⁴ Department of Plant Taxonomy and Nature Conservation, University of Gdansk, Poland

1.1 Introduction

Symbiosis means an intimate and often long‐term association between two or more different species. Ahmadjian and Paracer (1986) commented: “It is such a universal and important phenomenon that it should be an integral component of the education of biologists”. However, despite or because of its importance, this term has experienced much confusion, variation in usage, and controversy (Martin and Schwab, 2013 and references therein). De Bary coined the term in his monograph Die Erscheinung der Symbiose (1879) to mean “the living together of unlike organisms,” using it to describe a broad range of relationships (mutualism, commensalism, parasitism).

Our usage follows the original definition, rather than the more restrictive sense (i.e. symbiosis = mutualism) proposed by some biologists about 30–50 years ago (Martin and Schwab, 2013 and references therein). Symbioses encompass a wide variety of organismal associations in diverse environments, including: bacteria and fungi that form close alliances with the roots of plants; dinoflagellates that live within the endoderm of tropical corals; bacteria that sustain giant tube worms in the deep ocean; and so on. In addition, animals harbor many different microorganisms in their gastrointestinal tracts (Paracer and Ahmadjian, 2000; Benson et al., 2010). At the time De Bary developed his concept of symbiosis, Albert Bernhard Frank was working on plant‐fungal relationships. He already published the word Symbiostismus (1877), and he was the one who introduced the term mycorrhizas to designate the type of dual organ he observed: “the entire structure is neither tree root nor fungus alone but resembles the lichen thallus, a union of two different organisms into a single, morphological organ. It can be appropriately designated as a ‘fungus‐root’ or ‘mycorrhiza’” (Frank, 1885; English translation, Trappe, 2005).

The ability of fungi to form mycorrhizas with plants is one of the most remarkable and enduring adaptations to life on land. The relationship is a mutualistic one, and its occurrence is now well established in many plant species (Wang and Qiu 2006; Akhmetzhanova et al., 2012). By contrast, the number of fungal partners involved is less clear, and varies depending on mycorrhizal type (van der Heijden et al., 2015).

Molecular phylogenetics is providing insights into the evolution of different types of mycorrhizal association through time, and genomic studies of both plants and fungi are shedding light on how the complex set of interactions evolved (e.g., Floudas et al., 2012; Kohler et al., 2015). Evidence from fossils is also providing additional perspectives (e.g., Remy et al., 1994; Taylor et al., 1995; Krings et al., 2007a, 2007b, 2011; LePage et al., 1997), and recent work shows how a carefully targeted program of research can yield highly informative results (Strullu‐Derrien et al., 2009, 2014a). Moreover, extinction can generate a false signal regarding the origin of evolutionary novelties in a group when only living species are taken into account (Jablonski and Shubin, 2015). As a result, the fossil record has an important role to play in establishing a chronology of when fungi and key fungal associations evolved, and in understanding their importance in ecosystems through time (Figure 1.1).

Figure 1.1 Earliest occurrences of fungi, plants and fungal‐plant interactions in Palaeozoic times. Ages in millions of years are taken from the International Chronographic Chart of the International Commission on Stratigraphy, 2014.

Here we present a brief review of our current knowledge of the fossil record of mycorrhizas in the context of plant evolution. In addition to providing an overview of what is known, our aim is to identify areas in which the fossil record (palaeomycology) can be of relevance to genomics, and to recommend an approach that would bridge the two disciplines.

1.2 Extant mycorrhizal diversity

Mycorrhizas are widespread, occurring in over 80% of living plant species (Strullu, 1985; Smith and Read, 2008). The fungus uses the host as a source of carbon, while the host is supplied with mineral elements by the fungus. The two partners also protect each other against soil biotic (e.g., parasites) and abiotic (e.g., drought, toxic compounds) adversities. Some plants, such as the mosses and the angiosperm families Brassicaceae, Caryophyllaceae, Proteaceae, Cyperaceae, are generally believed to be predominantly non‐mycorrhizal (Smith and Read, 2008), although mycorrhizas are rare in some other families (e.g., Nymphaeaceae – Wang and Qiu, 2006).

Today, the most common associations are the arbuscular mycorrhiza (AM) symbioses, in which fungi are all members of the phylum Glomeromycota, which form a single and ancient clade (e.g., Redecker and Raab, 2006; Blair, 2009; Berbee and Taylor, 2010). These fungi can be found in the roots of 80% of all vascular plant species, and they are obligate symbionts. With our present state of knowledge, it is impossible to grow them independently from a host plant (Fortin et al., 2005).

AM associations are characterized by branched, tree‐like, intracellular fungal structures (i.e. arbuscules, hyphal coils) and, sometimes, storage organs termed vesicles (Strullu...