Plant Defense E-Book

Dale Walters

• Herausgeber: John Wiley & Sons
• Kategorie: Fachliteratur
• Sprache: Englisch

Seitenzahl: 478

Veröffentlichungsjahr: 2011

Beschreibung

Plants are sources of nourishment for thousands of fungi, bacteria, invertebrates, vertebrates, and other plants. Plants possess a truly remarkable diversity of mechanisms to fend off attackers and recent research has shown just how complex and sophisticated these defense mechanisms can be. Plant Defense provides comprehensive coverage of the range of different organisms that plants need to fend off, describes how plants coordinate their defenses against multiple attacks, explains the evolution of defense in plants, and how plant defences are exploited in crop protection strategies. Plant Defense: * Covers plants' defenses against pathogens, pests, and parasitic plants: together in one book * Brings together succinct, cutting edge information in a user-friendly format * Gives an understanding of how plants ward off attacks from multiple enemies * Is written by Dale Walters, an internationally known and respected researcher and teacher in crop protection, who distils his wealth of knowledge in a novel and exciting way * Is an essential purchase for all those involved in plant protection around the globe Plant Defense is primarily designed for use by upper undergraduates and post graduates studying crop protection, agricultural sciences, applied entomology, plant pathology, and plant sciences. Biological and agricultural research scientists in the agrochemical and crop protection industries, and in academia, will find much of great use in this excellent new book. Libraries in all universities and research establishments where agricultural and biological sciences are studied and taught should have multiple copies of this very valuable book on their shelves.

Leseprobe

Contents

Preface

Chapter 1 Why Do Plants Need Defenses?

1.1 Plants as sources of food

1.2 Organisms that use plants as food

1.3 Impact of infection and herbivory in natural andagricultural ecosystems

1.4 Conclusions

Recommended reading

References

Chapter 2 What Defenses Do Plants Use?

2.1 Introduction

2.2 Defenses used against pathogens

2.3 Defenses used against parasitic plants

2.4 Defenses used against nematodes

2.5 Defenses used against herbivorous insects

2.6 Defenses used against vertebrate herbivores

2.7 Defenses used against neighboring plants—allelopathy

2.8 Conclusions

Chapter 3 Sounding the Alarm: Signaling and Communication in Plant Defense

3.1 Introduction

3.2 Signaling in plant-pathogen interactions

3.3 Signaling in plant-nematode interactions

3.4 Signaling in plant-insect herbivore interactions

3.5 Signaling in interactions between plants and vertebrate herbivores

3.6 Signaling in interactions between plants and parasitic plants

3.7 Conclusions

Recommended reading

Chapter 4 Plant Defense in the Real World: Multiple Attackers and Beneficial Interactions

4.1 Introduction

4.2 Dealing with multiple attackers: cross-talk between signaling pathways

4.3 Can beneficial plant-microbe interactions induce resistance in plants?

4.4 Conclusions

Recommended reading

References

Chapter 5 The Evolution of Plant Defense

5.1 Introduction

5.2 Hypotheses of plant defense

5.3 Evolution of plant defense strategies

5.4 Patterns of plant defense evolution

5.5 Why do plants have induced defenses?

5.6 The coevolutionary arms race

5.7 Conclusions

Recommended reading

References

Chapter 6 Exploiting Plant Defense

6.1 Introduction

6.2 Using plant resistance to protect crops—breeding

6.3 Using plant resistance to protect crops—induced resistance

6.4 Using plant resistance to protect crops—biotechnological approaches

Index

This edition first published 2011

© 2011 by Blackwell Publishing Ltd.

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Library of Congress Cataloging-in-Publication Data

Walters, Dale.

Plant defense: warding off attack by pathogens, herbivores, and parasitic plants/Dale R. Walters. - 1st ed.

p. cm.

Includes bibliographical references and index.

ISBN 978-1-4051-7589-0 (pbk.: alk. paper) 1. Plants-Disease and pest resistance. I. Title.

SB750.W35 2011

632-dc22

2010011214

This book is dedicated to Beverley, for 30 years of love

Preface

Plants are virtually stationary packages of food. They are sources of nourishment for thousands of fungi, bacteria, invertebrates, vertebrates, and even other plants. With so much of the biotic environment of our planet dependent on plants, it is surprising that plants exist at all. The fact that plants not only survive but thrive in nearly all environments on earth is testimony to their remarkable ability to deal with, what can at times be, a hostile environment. Indeed, plants possess a truly remarkable diversity of mechanisms to fend off attackers, and recent research shows just how complex and sophisticated these defence mechanisms can be. And to top it all, there are the internal signaling networks coordinating defence responses within the plant and the ability to warn neighboring plants.

This ability of plants to defend themselves is important not just for plants in their natural environment but also for plants under cultivation. Indeed, humans have made use of an increasing knowledge of plant defenses over the years to breed crop plants able to resist pest or pathogen attack. Induced resistance, where the plant can be primed for an intense defense response on pest or pathogen attack, offers the prospect of a more durable approach to disease control in crop plants. However, transferring this to practice will require an understanding of the effects of crop ecology in determining the expression of induced resistance. Of course, plants do not just need to fend off pests and pathogens, they also need to deal with attacks by parasitic plants and a range of vertebrate herbivores. Indeed, most plants will need to cope with attack by multiple enemies at the same time, and our understanding of how plants coordinate their responses to such attacks is increasing rapidly.

Although plants have to coordinate and mobilize their defenses to deal with simultaneous attacks by different organisms, these topics tend to be dealt with in separate, disciplinebased textbooks, for example, plant pathology or entomology texts. This book is an attempt to remedy this deficiency. It deals with the range of different organisms plants need to fend off, how plants coordinate their defenses to deal with multiple attacks, the evolution of defense in plants, and the exploitation plant defenses in crop protection. I have written this book with senior undergraduates and postgraduates in mind and have included boxed readings dealing with particular topics in more detail, as well as a list of recommended reading, mostly books and review articles, at the end of each chapter.

I am very grateful to a number of colleagues for their encouragement during the preparation of this book, in particular Bill Spoor, Ian Bingham, and Adrian Newton. I am particularly grateful to Martin Heil, Adrian Newton, and Tony Reglinski, who kindly read, and provided comments on, some of the chapters. I am also grateful to Sergio Rasmann for providing some of the figures for Chapter 5. Thanks are also due to my wife Beverley, for love, encouragement, and incredible understanding—without this, I would never have completed the book.

I have been privileged to study plants for 31 years, and during that time, they have been a continual source of fascination and wonder. If I have managed to convey just a fraction of this in the following pages, I will be a happy man.

Dale Walters

Scottish Agricultural College

Edinburgh, UK

Chapter 1

Why Do Plants Need Defenses?

1.1 Plants as sources of food

All organisms need food to survive. To be more precise, they require a variety of chemical elements—the most important of which are carbon, nitrogen, and oxygen—to provide the building blocks for growth and development. This in turn requires a supply of energy, the only external supply of which comes from the sun. Plants are able to capture the energy from sunlight and convert it into chemical energy, thereby providing the means of financing the formation of carbohydrate from atmospheric CO2 and water. This autotrophic ability of plants comes at a price. Because most organisms are not autotrophic, they must obtain their energy and building blocks for growth and development from consuming other organisms, including plants. In fact, plants are a direct source of food for an array of organisms that include invertebrates, vertebrates, fungi, bacteria, and even other plants.

The popularity of plants as food sources for so many organisms begs the question “what do plants offer other organisms by way of nutrition?” Clearly, plant tissues will provide a source of carbon and nitrogen, much of which will be in the form of carbohydrates, lipids, andproteins.Theywillalsocontainmacroelementssuchasphosphorus,sulfur,calcium,and potassium, as well as various microelements such as iron, manganese, and zinc. However, the relative proportions of these components will vary depending on species. Moreover, different plant parts can have very different compositions (Figure 1.1). For example, fruits and phloem sap can be rich sources of carbohydrates, while seeds are usually good sources of fat. Some parts of the plant, such as bark, offer little in the way of nutrients, since they are composed largely of dead cells, with lignified walls. Nitrogen and protein content also varies between different parts of the plant, but in general, plants contain less nitrogen and protein than most of the organisms that use them as a food source. Typically, the total nitrogen content of plants is between 2 and 4% of their dry weight, while the nitrogen content of animals amounts to 8-14% of their dry bodyweight (Figure 1.2). The amount of nitrogen in insects is even greater than this and can be in the order of 30-40% of their dry weight (Southwood, 1973).

As indicated above, plants are used as food sources by a variety of organisms. Before we proceed further, it is worth considering the mechanisms used by these organisms to obtain the nutrients locked up in plant tissues.

Figure 1.1 Composition of different plant parts that can serve as food for herbivores. (Adapted from Townsend et al. (2003), with permission of Blackwell Publishing Ltd.)

1.2 Organisms that use plants as food

1.2.1 Microorganisms

Plants are infected by a wide range of microorganisms. Some of these establish symbiotic associations with plant roots, such as bacteria found in nodules on roots of legumes and mycorrhizal fungi, which form intimate associations with the roots of most plant species. Other microorganisms are parasitic on plants and use plants as food sources, causing damage and sometimes plant death, in the process. Some of these microbes, including viruses, protozoa, and some fungi, are biotrophs. These grow and reproduce in nature only on living hosts. Powdery mildew and rust fungi (Figure 1.3a), for example, produce feeding structures called haustoria that invaginate the host plasma membrane, forming an intimate association with the plant cell. Other microbes, mostly fungi and bacteria, are necrotrophic. They secrete enzymes to cause disintegration of plant cells and, either alone or in combination with toxins, often lead to cell and tissue death (Figure 1.3b). The nutrients released in the process are then available for uptake by the pathogen.

Figure 1.2 Variations in nitrogen concentration (dry weight percentage) of different plant parts compared with that in animals. Xylem and phloem sap concentrations are expressed as nitrogen weight/volume. (Adapted from Mattson (1980), with permission.)

1.2.2 Parasitic angiosperms

Plants are also parasitized by other plants. Indeed, parasitism among plants seems to have evolved many times during angiosperm evolution. It has been estimated that about 1% of angiosperms, some 3000 species in total, are parasitic on other plants (Parker & Riches, 1993). Parasitic angiosperms are distributed among 17 families, including the Viscaceae and the Cuscutaceae (Table 1.1), and include parasitic plants such as species of and (Figure 1.3c and 1.3d). There is considerable diversity in the extent to which parasitic angiosperms rely on the host for growth. Some, such as species of, have functional roots and can therefore take up inorganic nutrients from the soil, while others, such as the mistletoes, have nothing that resembles a root nor functions as one (Hibberd & Jeschke, 2001). There is also considerable variation in the extent to which parasitic plants rely on the host for photoassimilates. Thus, parasitic plants such as Rhinanthus minor are able to photosynthesize and can grow with a carbon supply from the host, while others, such as, possess a very low photosynthetic capacity and are unable to grow without a carbohydrate supply from the host (Hibberd & Jeschke, 2001).

Figure 1.3 (a) Yellow rust (Puccinia striiformis) on wheat, (b) Alternaria brassicae on pods and stems of oilseed rape (Brassica napus), (c) the parasitic angiosperm Rhinanthus minor, (d) the parasitic angiosperm Orobanche crenata, (e) the plant parasitic nematode Helicotylenchus, (f) caterpillar of the large cabbage white butterfly, Pieris brassicae, (g) an aphid on a leaf, (h) moose, (i) cows grazing. (Image (c) is the copyright of Glyn Baker and is licensed for reuse under the Creative Commons Licence. Images (d), (e), (f) and (h) are reproduced courtesy of Lytton Musselman, the American Phytopathological Society, Rosemary Collier of the University of Warwick HRI, and the United States Geological Survey, respectively.)

Table 1.1 Main families of parasitic plants

1.2.3 Nematodes

Nematodes are wormlike in appearance (Figure 1.3e) but are quite distinct from the true worms. Several hundred species are known to feed on living plants, obtaining their food with spears or stylets. Nematode feeding causes only slight mechanical damage to plants. The majority of the damage caused by nematodes appears to be caused by saliva injected into plants during feeding. Nematodes will puncture a cell wall, inject saliva into the cell, and withdraw part of the cell contents. Some nematodes feed rapidly and move on within a few seconds, while others feed more slowly and remain at the puncture for hours or even days. As long as the nematodes are feeding, they will inject saliva intermittently into the cell.

1.2.4 Insects

There are more species of insects than any other class of organisms on earth and nearly half of these, some 400,000 species, feed on plants (Schoonhoven et al., 2005). These herbivorous insects harvest their food inavariety of different ways. Chewing insects possess “toothed” mandibles that cut, crush, and macerate plant tissues. Many feed externally on the plant, while others, such as leaf miners, harvest tissue layers between the upper and lower epidermis of the leaf. Chewing insects include species belonging to the orders Lepidoptera (moths and butterflies) (Figure 1.3f) and Orthoptera (e.g., grasshoppers). Some insects do not remove chunks of plant tissue, but rather suck fluids from the plant using specialized tubular mouthparts. Thus, insects in the order Hemiptera include aphids (Figure 1.3g), which feed on phloem sap. Other members of the Hemiptera, for example, whiteflies, feed on the contents of leaf mesophyll cells. Yet other insects make galls on their plant host. These insects manipulate the host tissues, providing themselves with both shelter and nutrients. A striking feature of relationships between insects and plants is the extent of food specialization among insect herbivores. Some insects, including many lepidopterous larvae, hemipterans, and coleopterans, occur on only one or a few closely related plant species and are termed monophagous. Others, such as the Colorado potato beetle,, are oligophagous; these feed on a number of plant species, all belonging to the same family. Yet other insect herbivores, for example, the aphid, accept many plants belonging to different families. Such insects are polyphagous.

Table 1.2 Major categories of dietary specialization in herbivorous mammals, according to Eisenberg (1981)

Category Diet Nectarivores Nectar and pollen Gumivores Exudates from trees Frugivore/omnivore Pericarp or fleshy outer covering of plant reproductive parts, invertebrates and small vertebrates Frugivore/granivore Reproductive parts of plants, including seeds Frugivore/herbivore Fleshy fruiting bodies and seeds of plants, storage roots, and some green leafy material Herbivore/browser Stems, twigs, buds, and leaves Herbivore/grazer Grasses

1.2.5 Vertebrates

Herbivory is not confined to insects. In fact, it is a common trait among mammals (Figure 1.3h and 1.3i), with roughly half of the 1000 or so genera of mammals including plants in their diet (Danell & Bergström, 2002). While the majority of herbivorous insects are mono- or oligophagous, feeding on a few plant species, vertebrate herbivores tend to be polyphagous and feed on a wider range of plant species. Vertebrate herbivores are larger than their invertebrate counterparts and are thus able to remove a greater amount of plant tissue with each mouthful (Danell & Bergström, 2002). The classification of animals into functional groups is usually achieved using diet composition. Sixteen major categories of dietary specialization in mammals have been proposed (Eisenberg, 1981), and of these, seven refer to herbivores (Table 1.2). Categories range from nectarivores that feed on nectar and pollen to gumivores that feed on exudates from trees. The most dominant group is numerically the frugivores/omnivores, which represent approximately 33% of vertebrate herbivore genera (Table 1.2).

1.3 Impact of infection and herbivory in natural andagricultural ecosystems

1.3.1 Microorganisms

Pathogenic microorganisms can exert a profound effect on the structure and dynamics of individual plant species and plant communities. The extent and type of damage to individual plants is related to the lifestyle of the pathogen, that is, whether it is a biotroph or a necrotroph. Necrotrophs destroy plant tissue and it seems obvious therefore, that loss of leaf tissue, for example, will decrease rates of photosynthesis, thereby reducing plant growth. In contrast, biotrophs do not kill plant tissue, although effects on photosynthesis can be just as profound. Thus, effects on chloroplast structure and function can lead to dramatic reductions in rates of photosynthesis in plants infected with rust or powdery mildew fungi (Walters & McRoberts, 2006). Photosynthesis can also be affected by other means. In plants infected with vascular wilt pathogens, such as Verticillium albo-atrum, blockage of xylem vessels can lead to water stress and partial closure of stomata, thus reducing rates of photosynthesis. Of course, the effects of pathogens on the host plant are not restricted to photosynthesis, and some pathogens, for example, can alter water and nutrient uptake, while others produce toxins, which affect host metabolism. Whatever the mechanism, pathogen infection can lead to greatly reduced plant growth and reproductive output. Thus, Albugo candida and Peronospora parasitica, both biotrophs, reduce reproductive output in Capsella bursa-pastoris (Alexander & Burdon, 1984), while the tobacco leaf curl virus reduces growth and seed production in its host, Eupatorium chinense, and is an important cause of plant mortality (Yahara & Oyama, 1993).

Pathogen infection can also lead to plant death. Thus, fungal damping off and root diseases can cause mass mortality of seedlings, especially under humid conditions. Damping off was responsible for 64-95% of seedling deaths of the tropical tree Platypodium elegans in the first 3 months after emergence (Augspurger, 1983). Pathogens can also cause death of older plants. In Australia, an epidemic of the root rot pathogen, Phytophthora cinnamomi, devasted a dry sclerophyll forest (Weste & Ashton, 1994), while the pathogen Phacidiuminfestans was a significant cause of mortality in 5- to 10-year-old Pinus sylvestris (Burdon et al., 1994).

In crop production systems, losses due to pathogens can be substantial. In the period 1996-1998, global crop losses due to pathogens (fungi, bacteria, and viruses) were 12.6%, in spite of crop protection measures (Oerke & Dehne, 2004). Some crops seem to suffer more than others, and between 1996 and 1998, pathogens accounted for losses of 22% in global potato production. Even more devastating can be the spread of a pathogen into a new geographical area. For example, the soybean rust, Phakopsora pachyrhizi, was first reported in South America in 2001 (in Paraguay) and by 2003 was detected in most soybean-growing regions of Brazil, with losses estimated at 5% of total soybean production (Yorinori et al., 2005).

1.3.2 Parasitic angiosperms

The diversion of host resources to parasitic plants can have large effects on host growth and reproductive output. Infection of Poa alpina with the annual hemiparasite, R. minor, reduced host biomass by more than 50% (Seel & Press, 1996), while the phloem-tapping mistletoe, Tristerix aphyllus, greatly reduced the production of buds, flowers, and fruits by its cactus host, Echinopsis chilensis (Silva & Martínez del Rio, 1996). Death of the host plant can occur, particularly in extreme cases, such as heavy infestation with mistletoe (Aukema, 2003).

Parasitic plants can exert a considerable impact on plant communities (Press & Phoenix, 2005). Thus, Rhinanthus species have been shown to reduce total productivity in European grasslands by between 8 and 73% (Davies et al., 1997), while dwarf mistletoes can reduce volume growth of Douglas fir by up to 65% (Mathiasen et al., 1990).

Striga is a genus of root hemiparasite with some 35 species, most of which are of no agricultural importance. However, those species that parasitize crop plants can be devastating. Yield losses in cereals infected by Striga can reach 100%, and fields can be so heavily infested that they are abandoned by farmers (Berner et al., 1995). Some 40 million hectares of cereals are thought to be severely infested with Striga spp. in West Africa, and the Food and Agriculture Organization (FAO) estimates that annual yield losses in the savannah regions alone account for US$7 billion (Berner et al., 1995).

1.3.3 Nematodes

Nematode infestation can lead to substantial reductions in plant growth. In clover, the stem nematode, Ditylenchus dipsaci, reduced establishment from seeds and led to a 30% reduction in shoot growth (Cook et al., 1992), while the potato cyst nematodes, Globodera pallida and Globodera rostochiensis, reduced growth of potato roots within 1 day following inoculation onto root tips (Arnitzen et al., 1994). Nematodes have also been linked to plant deaths. Thus, pathogenic nematodes have been identified as the probable cause of die-out of the dunegrass, Ammophila breviligulata, on the mid-Atlantic coast of the USA(Seliskar,1995), while the pine wood nematode, Bursaphelenchus xylophilus, was responsible for the deaths of some quarter of a million mature pine trees in a single location in Japan (Numata, 1989).

1.3.4 Insects

Given the existence of more than 300,000 species of herbivorous insects (Schoonhoven et al., 2005), it is surprising that there is not more evidence of plant devastation. In fact, complete defoliation of vegetation occurs only sporadically. Some plants can compensate or overcompensate for sizeable amounts of damage, but even so, insect herbivory will reduce plant fitness (reproductive capacity) (Bigger & Marvier, 1998). We deal with the reasons for plant survival against such odds in later chapters. In the meantime, it is worth noting that some 10% of all annually produced biomass is consumed by insect herbivores (Barbosa & Schultz, 1987; Coupe & Cahill, 2003).

The extent of plant loss, however, is dependent on a number of factors, including vegetation type, timing of herbivory, and locality. Thus, herbivore pressure is likely to be greater in tropical dry forests than in temperate forests (Coley & Barone, 1996), with the result that rates of herbivory are significantly greater in forests in tropical regions than those in temperate zones (Coley & Aide, 1991; Figure 1.4). Variation in the damage caused by herbivory also exists between different species of plants. Thus, up to 50% of foliage production by Australian Eucalyptus trees can be lost as a result of insect herbivory, while other plant species, for example, Juniperus and Rhododendron, exhibit little damage from insects (Schoonhoven et al., 2005). Considerable variation in damage resulting from insect herbivory also exists within the same genus. In a study of herbivory among different Piper species, some suffered little damage from insects, while other species lost up to 25% of their leaf area (Marquis, 1991; Figure 1.5).

Insect herbivory affects many plant parts, including leaves, roots, and seeds. Perhaps the most obvious signs of insect herbivory are seen on leaves. It is estimated that rates of defoliation caused by insects lie within the range 5-15% of leaf area per year (Landsburg & Ohmart, 1989), although this is thought to be an underestimate (Crawley, 1997). Less obvious to the observer is perhaps root herbivory, although this is more likely to have an impact on plant dynamics than leaf herbivory (Crawley, 1997). Whatever plant part is used by insects as food, herbivory can have a sizeable impact on plant growth. For example, to study the effect of insect herbivory on tree growth in a eucalyptus forest, trees were sprayed with insecticide for several years (Morrow & LaMarche, 1978). Tree growth was substantially greater in sprayed trees, which had reduced insect loads, compared to unsprayed trees, which harbored greater insect numbers. Interestingly, while defoliating insects exerted little impact on acorn production by oaks (Quercus robur), the exclusion of sucking insects by spraying with insecticide increased acorn production consistently (Crawley, 1985).

Figure 1.4 Rates of herbivory in temperate and tropical forests. Plots indicate mean ±SD and range. (From Schoonhoven et al. (2005), with permission of Oxford University Press.)

Feeding by different types of insect herbivore can affect plant fitness more or less independently. For example, in Lupinus arboreus, the bush lupin, there was no statistical inter- action between above ground and below ground herbivory, and both types had significant cumulative effects on plant fitness. When bush lupin plants were protected from chronic above ground herbivory, seed output over a 3-year period increased by 78%, while suppression of below ground herbivory increased mean seed production by 31%. Interestingly, root herbivory was associated with a greater risk of plant mortality (Maron, 1998).

Figure 1.5 Rates of herbivory for different species of Piper. The data represent the mean percentage area missing for individual Piper species for a minimum of 50 freshly abscissed leaves per species. (From Schoonhoven et al. (2005), with permission of Oxford University Press.)

Plants in agricultural ecosystems often suffer more damage as a result of insect herbivory than their natural counterparts. As a result, considerable quantities of insecticide are used to control insect pests. Nevertheless, it is estimated that some 15% of global crop production is lost annually to insect damage, despite the use of insecticides. It is estimated that some 9000 species of insects attack agricultural crops worldwide, although only about 450 of these are considered as serious pests (Pimentel, 1991). Most insect pests are specialist feeders, with 75-80% of lepidopterous pests being monophagous or oligophagous (Barbosa, 1993).

1.3.5 Vertebrates

As mentioned above, because of their size, vertebrate herbivores are likely to remove more plant tissue per mouthful than their invertebrate counterparts. However, invertebrate herbivores are probably ten times more abundant than vertebrate herbivores (Peters, 1983). Herbivores are estimated to remove about 10% of net primary production in terrestrial environments (Crawley, 1983), and indeed, if we look at the Nylsvley savanna in southern Africa, for example, vertebrate grazers and browsers are estimated to remove 6% and invertebrate herbivores (grasshoppers and caterpillars) are estimated to remove 5% of the above ground primary production (Figure 1.6). The amount of vegetation removed by vertebrate herbivores depends greatly on habitat and the herbivore. For example, although in arctic areas, vertebrate herbivores remove between 5 and 10% of net primary production (Mulder, 1999), lemmings and geese can remove as much as 90% (Cargill & Jefferies, 1984), while muskoxen remove only 1-2% of vegetation (Bliss, 1986). Their greater body size—polyphagy, individual bite size, mobility, and tolerance of starvation—suggests that vertebrate herbivores should exert a more immediate, and in the long term a more profound impact on plant populations than invertebrate herbivores (Danell & Bergström, 2002).

Figure 1.6 Pathways of disappearance of leaf material in the broad-leaved savanna at Nylsvley, South Africa, and their approximate magnitude. (Reproduced from Danell & Bergström (2002), with permission of Blackwell Publishing Ltd.)

Some plants can tolerate vertebrate herbivory, and there is still debate about whether this tolerance is an evolutionary response to herbivory, and if so, whether grazing or browsing can benefit the plant in terms of increased fitness. The increase in net primary productivity of savanna grasses (McNaughton, 1979) and increased flower production in Ipomopsis aggregata (Paige, 1992) following herbivory are examples of the possible increase in plant fitness by vertebrate herbivory. However, vertebrate herbivory can deleteriously affect plant reproductive tissue and fecundity. Thus, simulating rodent damage to bilberry by branch cutting led to negative effects on flower production and berry development (Tolvanen et al., 1993), while sheep grazing on a shrub in the Karoo rangeland in South Africa reduced both flower production and seed size (Milton, 1995). Equally, there are examples where vertebrate herbivory exerts minimal impact on plant fitness, as in the case of ungulate grazing of Balsamorhiza sagittata (Asteraceae), a dominant native perennial forb in western Montana, USA. Here, in comparison to insect herbivory, vertebrate grazing had little impact on plant fecundity (Amsberry & Maron, 2006).

Plant size and shape can be altered by herbivory (e.g., removal of the leading shoot or apical bud in woody species), with consequences for interplant competition and effects on other organisms. Even removal of a small amount of plant biomass can have a profound effect on plant shape. Thus, removal of the leading shoot of a tree by vertebrate grazing can alter the architecture of the whole tree for many years.

Although vertebrate herbivory does not often result in plant death, mortality can occur, especially when vertebrates feed on small plants or seedlings (Hulme, 1994), or when older trees are debarked, by, for example, elephants, deer, squirrels, voles, and hares (Danell & Bergström, 2002).

1.4 Conclusions

Plants are attacked by a wide range of organisms, from viruses and bacteria to large vertebrates. These interactions can have a considerable impact on natural plant populations and indeed are thought to represent a major selective force on the evolution of plant structure and function. In crop situations, attack by pathogens and herbivores can result in serious losses in yield and quality. However, as we shall see in the following chapters, plants are not defenseless against such attacks, no matter how large the attacker.

Recommended reading

Crawley MJ, 1997. Plant-herbivore dynamics. In: Crawley MJ, ed. Plant Ecology. Oxford: Blackwell Publishing Ltd., pp. 401-474.

Danell K, Bergström R, 2002. Mammalian herbivory in terrestrial environments. In: Herrera CM, Pellmyr O, eds. Plant-Animal Interactions: An Evolutionary Approach. Oxford: Blackwell Pub lishing Ltd., pp. 107-131.

Parker C, Riches CR, 1993. Parasitic Weeds of the World: Biology and Control. Wallingford: CAB International.

Schoonhoven LM, van Loon JJA, Dicke M, 2005. Insect-Plant Biology. Oxford: Oxford University Press.

References

Alexander HM, Burdon JJ, 1984. The effect of disease induced by Albugo candida (white rust) and Peronospora parasitica (downy mildew) on the survival and reproduction of Capsella bursa pastoris (Shepherd’s Purse). Oecologia 64, 314-318.

Amsberry LK, Maron JL, 2006. Effects of herbivore identity on plant fecundity. Plant Ecology 187, 39-48.

Arnitzen FK, Visser JHM, Hoogendoorn J, 1994. The effect of the potato cyst nematode Globoderapallida on in vitro root growth of potato genotypes differing in tolerance. Annals of Applied Biology 124,59-64.

Augspurger CK, 1983. Seed dispersal of the tropical tree Platypodium elegans, and the escape of its seedlings from fungal pathogens. Journal of Ecology 71, 759-772.

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Chapter 2

What Defenses Do Plants Use?

2.1 Introduction

Although plants are attacked by a multitude of microorganisms, other plants, invertebrate, and vertebrate herbivores, most survive. The ability of plants to survive such assaults is due to the arsenal of defenses at their disposal, together with their ability to compensate for loss of tissue. This chapter deals with the defenses plants use to ward off attack. These defenses include structural mechanisms and biochemical responses that can slow down pathogen progress, ward off herbivores, and in some cases kill the invader. The variety of defenses used is staggering and ranges from the relatively simple to the very complex. The focus in this chapter is on defenses used against microbial pathogens, parasitic plants, nematodes, herbivorous insects, and vertebrate herbivores. There is also a brief foray into the realms of allelopathy—the defenses used by plants against neighboring plants.

Before we embark on our journey through plant defense, it is important to highlight definitions of two terms used throughout this book: defense and resistance. The latter term is used to describe the capacity of the plant to avoid or reduce damage caused by attackers. It is commonly used in the applied literature. Defense is used by some workers to mean that a particular trait has evolved or is maintained in the plant population as a result of selection exerted by attackers (Karban & Baldwin, 1997; Schoonhoven et al., 2005). Although use of the term “resistance” is preferred in those cases where a defensive function for a particular trait is still unproved, as pointed out by Karban & Baldwin (1997), it is extremely difficult, if not impossible, to determine the specific selective factors that shape a trait.

2.2 Defenses used against pathogens

2.2.1 Background

In nature, most plants are resistant to most pathogenic agents to which they come into contact. In this case, plants are able to completely prevent penetration by the pathogen, and suchplantsareconsideredtobeimmunetothatpathogen.Thus, wheat plants are not affected by pathogens of tomato plants, and vice versa. This is known as nonhost resistance. Of course, wheat can be infected by its own pathogens (pathogens with which it has coevolved) and so, for example, it can be infected by the black stem rust fungus, Puccinia graminis f.sp. tritici, while tomato plants can be infected by their pathogens, such as the leaf mold fungus, Cladosporium fulvum. Every plant will be host to a range of different pathogens, but the extent to which it can defend itself effectively against each of these pathogens will also be different. The plant might be highly resistant to one pathogen, allowing very little, if any pathogen growth in the tissue, but might be poorly resistant to another pathogen, allowing considerable growth of the pathogen in the tissue. This can also be looked at in terms of susceptibility, where high resistance would be equivalent to low susceptibility and vice versa (Figure 2.1). Resistance and susceptibility refer to the plant host, but, of course, the pathogen can also vary in its ability to infect the plant and cause disease. Any microbe incapable of causing disease in a plant is nonpathogenic on that plant. If the microbe can penetrate the plant, but its subsequent effects are insignificant, it is termed “avirulent.” If, however, its effects on the host are significant, it is said to be “virulent” (Figure 2.1). An interaction between a plant and a pathogen (e.g., a susceptible host and a virulent pathogen) where symptoms are expressed clearly is known as a compatible interaction, while an interaction where no symptoms develop (e.g., a resistant host and an avirulent pathogen) is described as incompatible (Figure 2.1). As one might expect however, not everything is quite so clear-cut.

Figure 2.1 Relationship between host plants, pathogens, and disease reaction. (Reproduced from Lucas (1998), with permission of Blackwell Publishing Ltd.)

When attacked by a pathogen, the plant can use a variety of preexisting or induced mechanisms to defend itself. These defenses can be structural or chemical, and depending on the attacking pathogen, the defense might be partial or nearly complete. All plants possess this type of resistance, and its level will vary depending on the attacking pathogen. This resistance is controlled by many genes and is known as polygenic resistance. It is also known as quantitative, partial, horizontal, multigenic, field, durable, and minor gene resistance (Agrios, 2005; see also Chapter 6). Plants also possess a resistance that, rather than being controlled by many genes, is controlled by one or just a few genes. Here, eachhost plant carries one gene or genes (known as resistance (R) genes) for every pathogen capable of attacking it. In turn, the pathogen carries a matching gene or genes (known as avirulence (A) genes). If a plant possessing a specific R gene is attacked by a pathogen carrying a matching A gene, defenses are triggered in the plant, which can kill the pathogen and halt the infection process. Often, the host cell being attacked dies, together with a few surrounding cells, in a process known as a hypersensitive response. This resistance, controlled by just one or a few genes, is called race-specific, R gene, major gene, or vertical resistance (Agrios, 2005; Chapter 6). Regarding the pathogen, some have a wide host range and are unspecialized, while others are highly specialized. The latter may be divided into a number of formae speciales (singular, forma specialis, f.sp.), which are morphologically identical, or nearly so, but which are capable of attacking different host genera, for example, cereal powdery mildews, Blumeria graminis, formae speciales of which attack barley (f.sp. hordei) and wheat (f.sp. tritici). Within each forma specialis, there are frequently large numbers of physiologic races, each capable of attacking a different spectrum of host species, or cultivars, according to the genes for virulence they possess.

We will look at how these types of resistance are triggered later, but in the meantime, let us turn our attention to the mechanisms plants use to defend themselves.

2.2.2 Passive or preexisting defenses

2.2.2.1 Preexisting structural defenses

The cuticle

In order to enter a plant and get at the nutrients within, a pathogen must attach itself to the surface, for example, of the leaf or root, prior to penetration. It stands to reason therefore that these plant surfaces represent the first line of defense against microbial invaders. The aerial surfaces of plants such as leaves and stems are covered with a structure known as the cuticle (Figure 2.2). The cuticle is formed from cut in, a hydrophobic material comprising fatty acids and fatty esters (Brett & Waldron, 1990), and it acts as an important barrier to pathogens. Cuticles vary in thickness and composition depending on the plant species, and a thick cuticle might increase resistance to pathogens that penetrate leaves or stems directly. However, cuticle thickness and pathogen resistance are not always correlated, since many plants with thick cuticles are readily invaded by pathogens capable of direct penetration. Below the cuticle lie the epidermal cells, the walls of which can vary in thickness and toughness depending on the plant. A thick, tough epidermal cell wall provides an almost impenetrable barrier to many fungal pathogens. Plant cells have a primary cell wall, which provides structural support, and many cells also form a secondary cell wall that develops inside the primary cell wall once the cell stops growing. The primary cell wall is composed mainly of cellulose, bundled into fibers known as microfibrils, which give strength and flexibility to the wall. The cell wall is also likely to contain two groups of branched polysaccharides, cross-linking glycans and pectins. The former include hemicellulose fibers that provide strength via cross-linkages with cellulose, while pectins form hydrated gels that help to cement neighboring cells together. Lignin, a heterogeneous polymer composed of phenolic compounds, is a component of many cell walls and provides rigidity to the cell. Lignified cell walls are highly impermeable to pathogens.

Figure 2.2 Cross-section of a leaf showing the barriers on the leaf surface: the cuticular layer, cuticle, and leaf surface waxes

In contrast to leaves and stems, roots contain suberin, which is deposited along with associated waxes in the cell walls of epidermal, exodermal, and endodermal cells. The root epidermis is in direct contact with the soil environment and is often the site of penetration by soilborne pathogens. As such, it offers the first line of defense against root pathogens.

Stomata

A leaf surface can have up to 300 stomata/mm2 occupying up to 2% of the total surface area of the leaf (Melotto et al., 2008). However, although abundant, in reality, stomata account for a very small proportion of the leaf surface. Nevertheless, stomata offer potential entry points for pathogens. Indeed, many fungal and bacterial pathogens only enter the host plant via stomata. Many pathogens force their way through closed stomata, although some, for example, P. graminis f.sp. tritici, the cause of wheat stem rust, can only enter wheat plants via open stomata. Indeed, stomata have been considered as passive entry points, with bacteria, for example, freely able to invade the plant via open stomata. However, work on Arabidopsis has shown that stomata close in response to live bacteria. When leaves were inoculated with a suspension of Pseudomonas syringae pv. tomato (Pst) DC3000, 70% of stomata closed within 1 hour, although this closure was transient, with most stomata reverting to the open state after 3 hours (Melotto et al., 2006). This work shows that stomatal guard cells can perceive live bacteria leading to significant stomatal closure and suggests that plants have evolved mechanisms to reduce entry of bacteria via stomata as an integral part of their defenses. Interestingly, Pst DC3000 produces a diffusible toxin (coronatine), which can reopen closed stomata (Melotto et al., 2006).

2.2.2.2 Preexisting chemical defenses

Although passive structural defenses keep many pathogens out of plants, they are not always effective and many pathogens can breach such barriers. Plants therefore possess a second line of preexisting defenses, based on chemicals, which can stop a pathogen in its tracks. Plants are capable of producing a diverse array of antimicrobial compounds (Wink, 1999). These compounds are the products of secondary plant metabolism, in contrast to metabolites arising from primary metabolism such as respiration (Figure 2.3). Those chemicals produced constitutively are called phytoanticipins, while those produced in response to pathogen attack are called phytoalexins (see Section 2.2.3.2) (Morrissey & Osbourn, 1999; Wittstock & Gerschenzon, 2002). Phytoanticipins are synthesized by unchallenged plants during normal growth and development, and accumulate in specific tissues, organs, or specialized structures, where they are usually sequestered in the vacuole or other subcellular compartments (Morrissey & Osbourn, 1999).

Figure 2.3 Plant secondary metabolism. This figure summarizes the major pathways involved in plant secondary metabolism and the main families of compounds formed. (Redrawn from Scott (2008), with permission of Blackwell Publishing Ltd.)

An aside—a quick excursion into plant chemistry

Three groups of compounds are produced by plants to act in defense: phenolics, terpenoids, and nitrogen-containing organic compounds (Figure 2.3). Defensive compounds can be virtually ubiquitous (e.g., terpenoids) or uniquetoone or two plant families (e.g., coumarins) (Table 2.1).

Terpenes are synthesized via the mevalonate pathway or the methylerythritol phosphate pathway (Figures 2.3 and 2.4).The former is located in the cytosol and leads to the formation of sesquiterpenes, triterpenes, sterols, and polyterpenes, while the latter pathway is located in the plastids and results in the formation of isoprene, monoterpenes, diterpenes, and carotenoids (Figure 2.5) (Lichtenthaler, 1999). Most terpenes are made from the basic unit isoprene, which is converted into isopentyl pyrophosphate.

Phenolic compounds are the second biggest group of plant secondary metabolites involved in plant defense. They are synthesized from the shikimic acid or malonic acid pathways (Figure 2.3) and possess an aromatic ring with one or more hydroxyl groups, and a number of other constituents. They range from simple phenolics with 6 or 7 carbon).atoms, such as catechol and salicylic acid, through coumarins with 9 carbon atoms, and on to more complex compounds with 15 carbon atoms, for example, flavonoids (Table 2.2 and Figure 2.6). The flavonoid nucleus is usually attached to a sugar molecule to yield a glycoside, which tends to be stored in the vacuole.

Table 2.1 Examples of secondary compounds used in chemical defense in plants

Source: Modified from Harborne (1993) and Strauss & Zangerl (2002), with permission of Blackwell Publishing Ltd.

Figure 2.4 Biosynthesis of terpenes. MEP, methyl erythritol phosphate; IPP, isopentenyl diphosphate; FPP, farnesyl diphosphate; GPP, geranyl diphosphate; DMAPP, dimethylallyl pyrophosphate; DMNT, (E)-4,8-dimethyl-1,3,7-nonatriene; TMNT, (E,E)-4,8,12-trimethyl-1,3, 7,11-tridecatetraene. (Reproduced by courtesy of Dr. Stefan Garms.)

Figure 2.5 Examples of terpenoids: limonene (a monoterpenoid), polygodial (a sesquiterpenoid), azadirachtin (a triterpenoid), and aescin (a saponin).

Nitrogen-containing organic compounds are synthesized from common amino acids and include cyanogenic glycosides, glucosinolates, and alkaloids. Cyanogenic glycosides are made through conversion of amino acids to oximes, which are then glycosylated. After synthesis, they are kept in separate cellular compartments from the enzymes that break them down and only come into contact when cells are ruptured following attack. The result is the liberation of hydrogen cyanide. Glucosinolates occur mainly in the Brassicaceae and contain sulfur as well as nitrogen. They are broken down by the enzyme myrosinase, leading to the formation of isothiocyanates (mustardoils), nitriles, and other compounds. Because of this, glucosinolates and myrosinase are kept in different cellular compartments to prevent autotoxicity. Alkaloids are cyclic compounds (Figure 2.7), produced from either amino acids (e.g., lysine, tyrosine, and ornithine) or purines and pyrimidines. Plants of the genus Nicotiana produce the alkaloid nicotine, which is made from ornithine. Other alkaloids include the tropane alkaloids (e.g., atropine) found in members of the Solanaceae, and quinolizidine alkaloids, which are derived from lysine and are commonly found in lupins. Concentrations of secondary compounds produced can vary enormously between plants and even within the same plant. For example, it would seem prudent for the plant to allocate most of its defensive chemicals to vulnerable tissues or plant parts that are important for successful reproduction and hence plant fitness. There is also increasing evidence from a number of plant species that chemicals are located where they are most readily perceived by attackers such as insect herbivores—the plant surface, including leaf waxes, trichomes, and so on (Harborne, 1993). Even within a tissue, for example, a leaf, concentrations of defensive chemicals can vary, with important consequences for the attacker. Concentrations of defensive chemicals can also be affected greatly by age of the tissue, and environmental factors such as light, water, and other soil factors, for example, mineral nutrition. Examples of variations in concentrations of chemicals and differences in location within the plant are given in the various sections below.

Table 2.2 Major classes of phenolic compounds in plants

Source: Modified from Schoonhoven et al. (2005), with permission of Oxford University Press.

Figure 2.6 Some plant phenolics: salicylic acid (a phenolic acid), ferulic acid (a hydroxycinnamic acid), umbelliferone (a coumarin), and genistein (an isoflavonoid).

Figure 2.7 Examples of alkaloids: scopolamine (a tropane alkaloid), nicotine (formed from ornithine and nicotinic acid), and caffeine (a purine alkaloid).

From this quick excursion into plant chemistry, it will be obvious that plants possess a formidable array of chemicals that can be deployed in defense against different attackers. Specific examples of the involvement of chemicals in plant defense against a range of attackers are given in the various sections below.

Chemicals on plant surfaces

Although it might be expected that preexisting chemical defenses would only be encountered once the pathogen has entered the plant, there are examples where the pathogen encounters such defenses while still on the plant surface. The classic example involves onion smudge, caused by the fungal pathogen Colletotrichum circinans. Onion cultivars with yellow/brown or red scales contain the phenolic compounds protocatechuic acid and catechol. C. circinans, like most fungal pathogens, requires liquid water for spore germination. However, these two fungitoxic compounds diffuse into water droplets on the surface of the onions, killing the pathogen, thereby protecting the plant from infection. Onion cultivars with colored scales tend therefore to be resistant to this pathogen. Interestingly, onion cultivars with white scales do not contain protocatechuic acid and catechol and are susceptible.

Chemicals within plant cells

Once inside the plant, the pathogen can be faced with a formidable chemical arsenal. Many plants accumulate phenolic compounds, tannins, or fatty acid-like compounds such as dienes in cells of young fruits, leaves, or seeds. These accumulated chemicals are thought to provide resistance in young tissues to various pathogens. Many dicotyledonous plant species produce glycosylated triterpenes and steroids known as saponins. Interestingly, among the monocots, although oats (Avena spp.) can produce saponins, it seems that most cereals and grasses cannot (Hostettmann & Marston, 1995). Oats produce two different families of saponins, steroidal avenacosides found in leaves and triterpenoid avenacins found in roots (Figure 2.8; Osbourn et al., 2003). Avenacin A-1 accumulates in epidermal cells of the root tip and is compartmentalized in the vacuoles. It is a powerful antifungal chemical, conferring resistance to a range of soil-inhabiting fungi (Field et al., 2006).

Figure 2.8 Representatives of the two different families of saponins synthesized by oat: the triterpenoid saponin avenacin A-1, which is the major saponin present in the roots (top); the steroidal saponin avenacoside B, which is found in the leaves (bottom). (Reproduced from Osbourn et al. (2003), with permission of Blackwell Publishing Ltd.)

Some constitutively produced chemicals are stored as inactive precursors and are converted into the biologically active form following pathogen attack. A good example involves glucosinolates produced by members of the Brassicaceae. In Arabidopsis, glucosinolates can be stored in vacuoles of specialized cells called S-cells, while the enzymes responsible for converting them to the active form (myrosinases) are located in myrosin cells. Following pathogen attack, damage to the tissues leads to breakdown of this compartmentalization and the myrosinases hydrolyze the glucosinolates to unstable aglucones. These, in turn, are converted to toxic chemicals such as isothiocyanates and nitriles (Wittstock & Halkier, 2002; Field et al., 2006).

In addition to the chemicals discussed above, several preformed plant proteins have been reported to play a role in plant defense against pathogens. One example is the lectins, proteins that bind with free sugar or with sugar residues such as polysaccharides, that are either free or attached to cell membranes. Indeed, many plant lectins have a high affinity for oligosaccharides, which are uncommon in plants, for example, those which bind chitin, a component of the cell walls of fungi and the exoskeleton of insects, but which is not found in plants (Debenham, 2005). This suggests that lectins play a role in plant defense, possibly via recognition of the attacking fungal pathogen or insect pest (the latter aspect is dealt with later in this chapter). In addition, various plants contain enzymes called ribosome- inactivating proteins (RIPs), which inhibit protein synthesis and can therefore block virus replication. RIPs have been shown to have broad-spectrum antiviral activity, affecting RNA, DNA, plants, and animal viruses (Wang & Turner, 2000). It is important to appreciate that the distinction between passive and active defense is not always clear-cut, and some of these plant proteins, for example, certain lectins, can also be produced following pathogen attack.

2.2.3 Active or inducible defenses

If a plant is to successfully ward off a pathogen, rapid mobilization of its defenses is necessary. This requires early recognition of the pathogen by the host plant. Amazingly, the plant starts to receive signals from the pathogen as soon as contact is established. Once it has breached the outer layers of the plant (e.g., cuticle and cell wall), it is subject to molecular recognition by individual plant cells. Plants have evolved two types of immune receptors to detect nonself molecules. First, there are pattern-recognition receptors (PRRs) that are located on the cell surface. PRRs sense microbes by perception of pathogen- associated molecular patterns (PAMPs; also referred to as MAMPs for microbe-associated molecular patterns, since they are not restricted to pathogenic microbes). MAMPs are conserved microbial molecules that include components of fungal cell walls such as chitin, lipopolysaccharides from Gram-negative bacteria, and short peptides derived from bacterial flagellin (Zipfel, 2008). This first level of immunity represents a basal resistance and is known as PAMP-triggered immunity (PTI) or innate immunity (Chisholm et al.