THIRD EDITION

CROP STRESS
Edited by

HANDBOOK OF PLANT AND

Mohammad Pessarakli

Boca Raton London New York

CRC Press is an imprint of the Taylor & Francis Group, an informa business

CRC Press Taylor & Francis Group 6000 Broken Sound Parkway NW, Suite 300 Boca Raton, FL 33487-2742 2011 by Taylor and Francis Group, LLC CRC Press is an imprint of Taylor & Francis Group, an Informa business No claim to original U.S. Government works Printed in the United States of America on acid-free paper 10 9 8 7 6 5 4 3 2 1 International Standard Book Number: 978-1-4398-1396-6 (Hardback) This book contains information obtained from authentic and highly regarded sources. Reasonable efforts have been made to publish reliable data and information, but the author and publisher cannot assume responsibility for the validity of all materials or the consequences of their use. The authors and publishers have attempted to trace the copyright holders of all material reproduced in this publication and apologize to copyright holders if permission to publish in this form has not been obtained. If any copyright material has not been acknowledged please write and let us know so we may rectify in any future reprint. Except as permitted under U.S. Copyright Law, no part of this book may be reprinted, reproduced, transmitted, or utilized in any form by any electronic, mechanical, or other means, now known or hereafter invented, including photocopying, microfilming, and recording, or in any information storage or retrieval system, without written permission from the publishers. For permission to photocopy or use material electronically from this work, please access www.copyright.com (http:// www.copyright.com/) or contact the Copyright Clearance Center, Inc. (CCC), 222 Rosewood Drive, Danvers, MA 01923, 978-750-8400. CCC is a not-for-profit organization that provides licenses and registration for a variety of users. For organizations that have been granted a photocopy license by the CCC, a separate system of payment has been arranged. Trademark Notice: Product or corporate names may be trademarks or registered trademarks, and are used only for identification and explanation without intent to infringe. Visit the Taylor & Francis Web site at http://www.taylorandfrancis.com and the CRC Press Web site at http://www.crcpress.com

in Plants and Crops 31 Stress Induced by Fungal Pathogens

Asghar Heydari and Giorgio M. Balestra
Contents
Introduction........................................................................................................................... 787 Attachment of Fungal Pathogens to Host Plants................................................................... 788 Host Plant Penetration by Fungal Pathogens Using Mechanical Forces............................... 789 Host Plant Penetration by Fungal Pathogens by the Aid of Enzymes................................... 790 Pathogenesis of Fungal Pathogens on Host Plants by Toxin Production............................... 791 31.5.1 Non-Host-Specific Toxins.......................................................................................... 791 31.5.2 Host-Specific (Selective) Toxins................................................................................ 791 31.6 Pathogenesis of Fungal Pathogens on Host Plants by Growth Regulators............................ 792 31.7 Stressful Effects of Fungal Pathogens on Host Plants........................................................... 793 31.7.1 Effects on Photosynthesis.......................................................................................... 793 31.7.2 Effects on Respiration............................................................................................... 794 31.7.3 Effects on Water and Nutrient Translocation............................................................ 794 31.7.4 Effects on Cell Membrane Permeability................................................................... 795 31.7.5 Effects on Transcription and Translation.................................................................. 795 31.8 Summary............................................................................................................................... 796 References....................................................................................................................................... 797 31.1 31.2 31.3 31.4 31.5

31.1  Introduction
Pathogenic fungi can attack a very wide range of plants, and by doing so can cause very serious losses to agricultural and horticultural crops (Agrios, 1988; Alexopolous and Mimms, 1996; Chen and Dickman, 2005; Doehlmann et al., 2006; Heydari, 2007; Heydari et al., 2005; Heydari and Misaghi, 2003; Mayer et al., 2001; Ortoneda et al., 2004; Park et al., 2005; Scully and Bidochka, 2006; St. Leger et al., 2000; Zaki et al., 1998). A great deal of research has been carried out to study the pathogens, but very little consideration has been given to the mechanisms involved in the pathogenic process of these types of organisms. As a result of fungal pathogen attack, different stressful conditions are induced and created in plants and crops. In this review, an attempt will be made to describe and discuss these stresses. In the case of fungal pathogen attack, severe damage is caused to the host, but this damage does not necessarily lead to death of the host plant (Alexopolous and Mimms, 1996; Chen and Dickman, 2005; Doehlmann et al., 2006; Heydari, 2007; Heydari et al., 2005; Heydari and Misaghi, 2003). The attack by necrotrophic fungi, in which host cells are killed, presents a slightly different situation (Alexopolous and Mimms, 1996; Chen and Dickman, 2005; Doehlmann et al., 2006; Heydari, 2007). Following location of the host, fungi in some way attach to the plant (Alexopolous and Mimms, 1996). The pathogen, after attachment, must penetrate the outer layers of the host, by mechanical breaching of the defense barriers or by using chemical mechanisms to disrupt physical barriers, for example, by the use of lytic enzymes or through existing openings such as stomata (Alexopolous and Mimms, 1996; Doehlmann et al., 2006; Heydari, 2007; Heydari et al., 2005).
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Following penetration of the hosts outer layers, the pathogen either enters into or fuses with the host tissue, permitting the withdrawal of nutrients from the host plant (Alexopolous and Mimms, 1996; Chen and Dickman, 2005; Doehlmann et al., 2006). In optimal parasitism, the attacking organism neutralizes the host defense responses so that a continued coexistence is possible, without death of the host cells. This process of neutralization involves a series of complex reactions, in which levels of host hormones (growth substances) are modified or hormones are secreted by the attacking organisms (Chen and Dickman, 2005; Doehlmann et al., 2006; Heydari, 2007). The pathogen creates a local environment, in which the parasite becomes a sink for the nutrients present in the host, without, however, completely depleting host resources (Alexopolous and Mimms, 1996). Fungal pathogens frequently produce toxins that have an adverse effect on the host, without necessarily killing it (Brodhagen and Keller, 2006; Daly and Knoche, 1982; Dubrin, 1981; Mitchel, 1984). In extreme cases, parasite toxins kill host cells or tissues. An important part of the pathogenhost interaction is the genetic mechanisms of compatibility or incompatibility (Belkhadir et al., 2004; Doehlemann et al., 2006; Dunkle, 1984; Feldbrugge et al., 2004). This involves the ability of the pathogen to recognize the host and the host to sense the presence of the pathogen. Incompatibility, in which the host recognizes and rejects the pathogen, is part of the resistance mechanism. The ability of the pathogen to recognize its host is also a very significant part of the attack process (Belkhadir et al., 2004; Doehlemann et al., 2006; Dunkle, 1984; Feldbrugge et al., 2004). The number of fungi is extremely large and the number of pathogens among them comprises probably thousands of species (Alexopolous and Mimms, 1996; Chen and Dickman, 2005; Doehlmann et al., 2006; Heydari, 2007; Heydari et al., 2005; Heydari and Misaghi, 2003; Mayer et al., 2001; Ortoneda et al., 2004; Park et al., 2005). It is characteristic of most pathogenic fungi to show a great deal of species specificity. Most of the biotrophic fungi are able to infect only a very limited number of plant species, whereas the necrotrophic fungi are far more versatile and are often able to infect hundreds of plant species (Alexopolous and Mimms, 1996; Chen and Dickman, 2005; Doehlmann et al., 2006; Heydari and Misaghi, 2003; Mayer et al., 2001; Ortoneda et al., 2004; Park et al., 2005). Fungal plant pathogens and the infection and diseases they cause in host plants can result in various stressful conditions. They may affect the physiological functions of plants and cause serious damage and disruptions to these functions. Almost all essential physiological functions of plants, including photosynthesis, translocation of water and nutrients, transpiration, respiration, permeability of cell membrane, and transcription and translation, can be affected by fungal pathogens (Allakhverdieva et al., 2001; Antunes and Sfakiotakis, 2000; Camejo et al., 2005; Crafts-Brander and Salvucci, 2002; Hancock and Huisman, 1981; Manners and Scott, 1983). As a result, serious stressful conditions may be induced and created in plants. In this chapter, the pathogenesis and the ways that fungal pathogens attack and cause diseases in their hosts will be first discussed and then their stressful impacts on the structures and functions of plants will be reviewed.

31.2 Attachment of Fungal Pathogens to Host Plants

The manner in which fungal pathogens reach their host plants depends on the part of the host that is attacked (Alexopolous and Mimms, 1996). If above-ground parts of the plants are attacked by pathogens, frequently the fungal pathogen reaches them in a fortuitous manner, due to the accidental spread of the fungal structural elements such as mycelium or spores, by wind, rain, or other environmental factors (Agrios, 1988; Podila et al., 1993). In some cases, the infecting fungal pathogen may be carried by insects or other organisms, but again, contact occurs in an accidental fashion. When plant roots are attacked, there is often an actual active mechanism by which the fungus reaches the host (Agrios, 1988; Alexopolous and Mimms, 1996). In some cases, fungal mobile structures such as zoospores are attracted to the roots by chemotactic mechanisms. In other instances, the infecting pathogen may reach the root accidentally or it may be carried there by organisms present in the soil (Agrios, 1988).

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Usually, fungal infection of a host plant is preceded by germination of a fungal spore (Alexopolous and Mimms, 1996). The spore lands on the surface of its host, germinates, and then one of a number of alternative pathways is followed. In the case of zoospores, after encystment and germination, growth is towards the host, probably by a chemotactic mechanism, although much remains to be elucidated in this respect (Alexopolous and Mimms, 1996). Hyphae may enter the host through natural openings, such as stomata, lenticels, or hydathodes, or through existing lesions or wounds in the surface. Sometimes the hyphae form an appressorium, a rigid structure, often containing melanin, which sticks to the surface of the host (Agrios, 1988; Alexopolous and Mimms, 1996; Dunkle, 1984; Francis et al., 1996; Hoch and Staples, 1987; Podila et al., 1993; Thines et al., 2000; Veneault-Fourrey et al., 2006). The appressorium sticks to the surface of the host with the aid of adhesive compounds, which include glycoproteins, polysaccharides, polymers of hexosamines and xylans, and perhaps also lipids (Agrios, 1988). The nature of the adhesive can be quite variable, depending on the host and the infecting fungus (Thines et al., 2000; Veneault-Fourrey et al., 2006). Eventually, the appressorium develops sufficient turgor pressure so that a mechanical breach of the cuticle is possible (Hoch and Staples, 1987; Thines et al., 2000; Veneault-Fourrey et al., 2006). The cuticle on the surface of the host may be softened by the action of enzymes, such as cutinase, enabling penetration.

31.3 Host Plant Penetration by FungalPathogens Using Mechanical Forces

Fungal Plant pathogens are very small and microscopic organisms that cannot generally apply a voluntary force to plant surface (Alexopolous and Mimms, 1996). In order to enter plant tissues and cells, they need to be equipped with some mechanical structures by which they reach and enter their host plants (Goodman et al., 1986; Isaac, 1992; Misaghi, 1982; Strange, 2003). The penetration of fungal pathogens to the tissue of their host has been well studied (Alexopolous and Mimms, 1996; Goodman et al., 1986; Isaac, 1992; Strange, 2003). Pathogenic fungi are facilitated with some mechanical structures such as haustorium and appressorium, which can be used when these pathogens penetrate host plants (Agrios, 1988; Alexopolous and Mimms, 1996; Thines et al., 2000; Veneault-Fourrey et al., 2006). The fungal haustorium is a well-recognized structure, which is basically an extension of part of a fungal hypha that penetrates into the cell or cells of the host, without lesion or lysis of the host cell wall (Alexopolous and Mimms, 1996). It can be likened to the finger of a glove, which deforms the cell wall of the host cell, but does not damage it. The fungal haustorium is well described and it is sufficient here to cite the general literature (Agrios, 1988; Alexopolous and Mimms, 1996; Thines et al., 2000; Veneault-Fourrey et al., 2006). The fungal haustorium is able to obtain nutrients from the host cells (Alexopolous and Mimms, 1996). Mechanical forces and stress induced by them in plants attacked by fungal pathogens are also mediated by appressorium, which is a swollen tip of a hyphae or germ tube that facilitates attachment and penetration of the host by the fungus (Agrios, 1988; Alexopolous and Mimms, 1996). Appressoria are either melanized, such as those of Colletotrichum and Magnaporthe, or non-melanized such as that belongs to Erysiphe, which is an obligate parasite and the causal agent of powdery mildew disease on many plants (Agrios, 1988; Alexopolous and Mimms, 1996). After penetration of the host plants, a considerable amount of mechanical force is exerted on host tissues by fungal pathogens. Through increased pressure created by this force, plant tissues, cell walls, and cuticle are expanded and pushed out, and finally break down (Alexopolous and Mimms, 1996; Goodman et al., 1986; Isaac, 1992; Strange, 2003). Once a pathogenic fungus has entered a plant cell, it usually secretes increased amounts of enzymes that complete the process of penetration and assist the pathogen to establish and settle down in the host plant (Alexopolous and Mimms, 1996; Goodman et al., 1986; Isaac, 1992; Misaghi, 1982; Strange, 2003).

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31.4 Host Plant Penetration by FungalPathogens by the Aid of Enzymes

In addition to mechanical penetration, fungal pathogens also use biochemical weapons including different enzymes to enter plant tissues (Francis et al., 1996; Idnurm and Howlett, 2002; Jennings et al., 1998; Kolattukudy, 1981, 1985; Koller et al., 1982, 1995; Kosuge and Nester, 1984; Mohavedi and Heale, 1990; Thines et al., 2000; Tian et al., 2004; Van Kan, 2006; Ten Have et al., 2004). Initial penetration may be through natural openings, such as stomata, lenticels, or cracks in the surface of the host. However, even when this occurs, enzymes are subsequently used to continue penetration. Such penetration is achieved by the formation of several groups of enzymes (Francis et al., 1996; Jennings et al., 1998; Kolattukudy, 1981, 1985; Koller et al., 1995). The first group comprises those that degrade the surface layers of the host, such as layers of waxes, cutins, and suberins (Francis et al., 1996; Koller et al., 1982, 1995). Degradation of cell wall substrates is the most important mode of action and mechanism of enzymes that enable fungal pathogens to penetrate plant tissues (Agrios, 1988; Idnurm and Howlett, 2002). The most thoroughly researched of these enzymes are the cutinases. Although the evidence of the function of cutinases in fungal penetration is not unambiguous, there is a great deal of evidence to show that they do play a role in penetration into the host (Francis et al., 1996; Koller et al., 1995). The next group of enzymes secreted by fungi that are well researched and extensively described are those involved in the degradation of pectins (Agrios, 1988; Kolattukudy, 1981, 1985). A wide range of enzymes varying in activity, specificity, distribution, and function are known. One way of discriminating among them is by a definition of their activity. On the one hand, there are the polygalacturonases, which cleave the galacturonide bonds in the pectin skeleton (Alexopolous and Mimms, 1996). These enzymes may be endo- or exo-polygalacturonases or in some cases endoor exo-methyl polygalacturonases (Alexopolous and Mimms, 1996; Mohavedi and Heale, 1990). Although having an entirely different mode of action, the pectin lyases or pectin trans-eliminases also break down the galacturonide bond of the pectin (Agrios, 1988). The number of these enzymes is very large, and they usually exist as a number of isozymes that are coded by a series of genes, the expression of which depends on the pathogen, its stage of development, and the host (Agrios, 1988). However, their importance in pathogen penetration into the host is not in doubt, although often, the specific isozyme that is important has not been determined. Frequently, the action of the polygalacturonases is preceded by the action of the pectin methyl esterases, which cleave the methyl group attached to the carboxylic acid present in pectins (Mohavedi and Heale, 1990). Again, endo- and exo-pectin methylesterases are known that are coded by a large number of genes. Many isozymes are known and in general it can be stated that the pectin methylesterases are an essential part of penetration of the fungal pathogen into its host. Also in this case, the literature is extensive and will not be reviewed here. Other enzymes present in many pathogens are the cellulases and xylanases, which act directly on the glycosidic bonds of cellulose or on those of arabinoxylans present in the plant cell wall (Agrios, 1988; Alexopolous and Mimms, 1996). These enzymes have been less well described and their role in fungal penetration is less clear. Although the cell wall of many plant cells is lignified, the degradation of lignin is probably not a crucial step in fungal penetration (Agrios, 1988). Lastly, proteases produced by fungal pathogens must be mentioned. These are apparently involved in pathogenicity and may be responsible for the initial damage to host cells (Alexopolous and Mimms, 1996; Doehlemann et al., 2006). Overall, the concept emerging from the studies of these enzymes reveal that fungi use an array of enzymes to break down host cell walls to separate host tissue and to permit penetration into host tissue, and, in addition, are often able to inactivate or kill the host cells, thereby liberating nutrients that are then available for growth and development of the fungal pathogen. In addition to fungal enzymes, hormones formed by the pathogen also often play a role in redirecting the flow of nutrients toward the site of infection, thereby improving the sink from which the pathogen obtains its nutrients (Agrios, 1988).

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31.5 Pathogenesis of Fungal PathogensonHostPlants by Toxin Production

In phytopathology, the term toxin is reserved for toxic chemicals (chemopathogens) that are able to cause effects similar to those of disease symptoms induced by microorganisms (Gardiner et al., 2005; Scheffer, 1983). This may be confused with two other names: phytotoxins (for any product of a living organism toxic to plants) and mycotoxins (produced by several fungi in infected seeds, feeds, or foods and capable of causing illnesses of varying severity and death to animals and humans that consume such substances). Most microbe toxins are low molecular weight compounds with diverse structures that act as positive agents of virulence or pathogenicity (Brodhagen and Keller, 2006; Daly and Deverall, 1983; Gardiner et al., 2005; Nishimura and Komoto, 1983; Palmer et al., 2004; Scheffer, 1983). Pathogenic fungi can produce toxins in infected plants as well as in culture medium. The toxin is produced only in the plant or under specific inductive conditions are much less likely to have been discovered. Toxins are usually effective in very low concentrations, target the cellular membranes by affecting the permeability, inactivate or inhibit enzymes, and inhibit or disturb the signal transduction (Brodhagen and Keller, 2006; Dally and Deverall, 1983; Mitchel, 1984; Nishimura and Komoto, 1983; Scheffer, 1983).

31.5.1 Non-Host-Specific Toxins

Toxins produced by phytopathogenic microbes have been shown to produce all or part of the disease syndrome, not only in the host plant but also in other species of plants that are not normally attacked by the pathogen in nature (Scheffer, 1983). These toxins increase the extent of disease caused by a pathogen but are not essential for the pathogen to cause disease (Scheffer, 1983). By definition, non-host-specific toxins are not primary determinants of host range. One of the typical fungal non-host-specific toxins is fusicoccin, which is a diterpenoid glycoside synthesized via the mevalonic acid pathway and is produced by Fusicoccum amygdali, causing the wilting syndrome in peach and almond trees (Agrios, 1988; Brodhagen and Keller, 2006; Scheffer, 1983). The fusicoccin toxin causes the opening of the stomata and increased transpiration and subsequent wilting in plants. The site and mode of action of this toxin is the direct activation of plant H+-ATPase and reversible interaction between its C-terminal region and regulatory 14-3-3. The 14-3-3 proteins are present in all eukaryotes and act as regulators in various signal transduction pathways (Brodhagen and Keller, 2006). Different Fusarium species produce a complex of several toxins including fusaric acid (5-butylpicolinic acid), fumonisin B1 (produced by F. moniliform and by Alternaria alternata f. sp. lycopersici as AAL-toxin), trichothecene vomitoxin-deoxynivalenol (DON), zearalenone (ZEN), T-2 toxin, etc. (produced by F. graminearum and other Fusarium species). These toxins are phytotoxic to a broader range of plants (Agrios, 1988). A number of other NHS-toxins such as oxalic acid have been isolated from phytopathogenic fungi (sclerotium and sclerotinia) and many others.

31.5.2 Host-Specific (Selective) Toxins

A host-specific toxin is a substance produced by a pathogenic microbe that, at physiological concentrations, is toxic to the hosts of that pathogen and shows little or no toxicity against non-susceptible plants (Brodhagen and Keller, 2006; Mitchel, 1984; Nishimura and Komoto, 1983; Scheffer, 1983). In general, host-specific (selective) toxins (HSTs) are determinants of host range or specificity in that plant species, varieties, or genotypes. HSTs have been critical factors in two major epidemics of crops in the United States in the twentieth century, including the southern corn leaf blight epidemics of 1970 that destroyed about 15% of that years crop (Mitchel, 1984). They are also important factors in several other economically significant diseases. In general, all known HSTs are

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produced by certain fungi. Even among the fungi, most known HSTs are produced by species or pathotypes in just two genera: Cochliobolus (also known by the old and new names for its imperfect stage, Helminthosporium or Bipolaris, respectively) and Alternaria (Brodhagen and Keller, 2006; Mitchel, 1984; Nishimura and Komoto, 1983; Scheffer, 1983). Victorin is one of the first host-specific toxins discovered, and its remarkable toxic effects have been recorded (Agrios, 1988). Its structure is a polypeptide linked to a nitrogen-containing sesquiterpene and is produced by Cochliobolus victoriae, which causes foot and root rot and leaf blight in certain oat varieties (Agrios, 1988; Brodhagen and Keller, 2006). Plant phenotypical reactions and stresses caused by this toxin include some general changes in the physiology of host that are common to infectious plant diseases. The site and mode of action of this toxin is the major 100-kD victorin-binding protein that has been purified, and its gene encodes the pyridoxal-phosphate-containing P subunit of glycine decarboxylase (GD) (Brodhagen and Keller, 2006). Another important toxin in this group is T-toxin (HMT-toxin). It is produced by race T isolate of C. heterostrophus, the causal agent of the southern corn leaf blight that is believed to be one of the most serious diseases in the recent history of plant pathology (Agrios, 1988; Brodhagen and Keller, 2006). Race O of C. heterostrophus, however, which does not produce T-toxin, is a minor pathogen of corn regardless of cytoplasm. Site and mode of action of T-toxin is active at about 10nM against Tcms maize and at about 10M against maize with normal cytoplasm. Mitochondria in vitro and in situ are quickly, specifically, morphologically, and biochemically affected by T-toxin (Agrios, 1988; Brodhagen and Keller, 2006). HC-toxin is another host-specific toxin, which is a cyclic tetrapeptide produced by C. carbonum race 1, a causative agent of the Northern corn leaf spot (Agrios, 1988; Brodhagen and Keller, 2006). This toxin inhibits root growth of compatible maize, but is not toxic to cells. Current evidence indicates that the site of action of HC-toxin is histone deacetylase (HD), an enzyme that reversibly deacetylates the core histone (H3 and H4) while they are assembled in chromatin (Brodhagen and Keller, 2006). Acetylation and deacetylation of the core histones alter the inducibility and suppressibility of certain classes of genes. Current research is aimed at understanding how the inhibition of HD activity promotes the infection of maize by C. carbonum race 1. Finally, AAL-toxin is the last host-specific toxin discussed in this section. The structure of this toxin is related to sphinganine and is produced by Alternaria alternata f. sp. lycopersici as AAL-toxin and by Fusarium moniliform as fumonisin B1 toxin (Agrios, 1988; Brodhagen and Keller, 2006). The AAL-toxin is essential for the pathogenesis of AAL in tomato, because the toxin-deficient mutants cannot infest healthy compatible tomato leaves. However, all strains of F. moniforme are not pathogenic on the AAL compatible tomato isoline, indicating that the toxin produced by F. moniforme is not sufficient for virulence on tomato (Brodhagen and Keller, 2006). Plant phenotypical reactions, toxicity, and resistance of this toxin indicates that it acts as a phytotoxin against plants. The AAL-toxin is toxic to all tissues of sensitive tomato cultivars at low concentrations and induces apoptosis in sensitive tomato lines (Brodhagen and Keller, 2006).

31.6 Pathogenesis of Fungal PathogensonHostPlants by Growth Regulators

Growth regulators are naturally occurring compounds in plants and act in very low concentrations (Agrios, 1988; Ashraf and Foolad, 2007; Cessna et al., 2000; Hamer and Holden, 1997; Mur et al., 2006; Tsitsigiannis and Keller, 2006; Viaud et al., 2002; Walters et al., 2006; Wang et al., 2003). The production and occurrence of growth regulators are usually changed and altered after fungal pathogens attack and infect plants. The most important growth regulators are discussed below. Auxin, which is also called IAA, is one of the most important growth regulators involved in fungal pathogenicity (Agrios, 1988; Ashraf and Foolad, 2007; Cessna et al., 2000; Hamer and Holden, 1997). Studies have shown that IAA levels are changed in many diseased plant tissues. Several fungal plant diseases such as corn smut (Ustilago maydis) and clubroot of cabbage (Plasmodiophora

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brassicae) show a typical gall symptom due to the increased levels of IAA (Agrios, 1988; Mur et al., 2006; Tsitsigiannis and Keller, 2006; Viaud et al., 2002). Many other fungal pathogens are also capable of production of IAA. Gibberellin is another growth regulator that is directly related to fungal pathogen infection (Agrios, 1988; Cessna et al., 2000; Hamer and Holden, 1997; Mur et al., 2006). A century ago, rice farmers in Asia noticed some exceptionally tall seedlings growing in their paddies (Agrios, 1988). Before these rice seedlings could mature and flower, they grew so tall and spindly that they toppled over. In Japan, this aberration in growth pattern became known as bakanae (foolish seedling disease) of rice. In 1926, Kurosawa, a Japanese scientist discovered that the disease was caused by a fungal pathogen, Gibberella fujikuroi (Agrios, 1988). By the 1930s, Japanese scientists had determined that this fungus produced hyper-elongation of rice stems by secreting a chemical, which was given the name gibberellin. Gibberellins are normal constituents of green plants and also produced by several other microorganisms. The best known gibberellin is gibberellic acid. In the past years, scientists have identified more than 80 different gibberellins, many of them occurring naturally in plants. Spraying of diseased plants with gibberellin overcomes some of the symptoms (Agrios, 1988). Ethylene is another important growth regulator that is induced and produced in fungal-pathogeninfected plants (Cessna et al., 2000; Hamer and Holden, 1997; Mur et al., 2006). Ethylene production in infected tissues can be dramatically induced. This induction is largely dependent on activation of the ethylene biosynthetic pathway in plant tissues. Genes encoding several key enzymes involved in the ethylene biosynthesis are highly activated at the transcriptional level (Cessna et al., 2000; Hamer and Holden, 1997; Mur et al., 2006). Ethylene has been considered as a signal in plants for wounding and senescent responses. Recent studies show that ethylene, together with another signal component jasmonic acid, may play an essential role in plant defense responses of several pathosystems (Mur et al., 2006). In addition to the chemicals described above, fungal pathogens use other chemical weapons in their pathogenesis including polysaccharides, plant defense suppressors, transporters, etc.

31.7 Stressful Effects of Fungal Pathogens on Host Plants 31.7.1 Effects on Photosynthesis
Photosynthesis is defined as a function that enables green plants to convert light energy to chemical energy. Plants then use this chemical energy in their processes. In photosynthesis, carbon dioxide taken from the atmosphere and water taken from the soil come together in the chloroplast of the plant cells and with the aid of light energy react and form glucose and release oxygen (Ellis et al., 1981; Wise et al., 2004). As a very important and basic function of green plants, any disruption or interference in photosynthesis can create and induce stressful conditions in plants. Fungal pathogens are among the most important biotic agents that can infect plants, disrupt the photosynthesis process, and induce serious stresses in plants (Agrios, 1988). A very obvious example of the interference of fungal pathogens with the photosynthesis is the chlorosis and necrosis that they cause on the green parts of plants, which then result in reduced growth of many infected plants (Agrios, 1988). In some diseases caused by fungal pathogens, such as blights or leaf spots, plant photosynthesis is significantly reduced due to the lessening of leaf surface area that is the main photosynthetic part of plants (Rollins, 2003). Photosynthesis in other fungal diseases is also reduced because of the impact of the disease on infected plant tissues and cells. It has been shown that in some fungal diseases, toxins that are produced by these fungal pathogens cause serious inhibition in the production of plant enzymes that are directly or indirectly involved in the photosynthesis (Agrios, 1988). In wilt diseases that are caused by vascular plant fungal pathogens, the stomata are partially closed, chlorophyll is reduced, and photosynthesis is stopped even before wilting symptoms are observed (Agrios, 1988; Van Kan, 2006). All the above-mentioned conditions and negative impacts of fungal plant pathogens on the photosynthesis result in serious pathological conditions in the infected and diseased plants.

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31.7.2 Effects on Respiration

The most evident effect of fungal diseases on infected plant respiration is the general increase of respiration as a result of the faster use of reserved carbohydrates by plant tissues (Agrios, 1988). An increase in the respiration usually begins shortly after pathogen attack and continues during multiplication and infection stages. When resistant plants are attacked by fungal pathogens, their respiration increases rapidly compared to susceptible ones, because in resistant plants, higher levels of energy are needed to activate the mechanism of resistance to the pathogen (Agrios, 1988). It has been shown that in infected plants, the activity and concentration of some enzymes involved in the respiration are significantly increased. In infected plants, the accumulation of phenolic compounds that are involved in respiration seems to be higher than healthy plants (Agrios, 1988). The increase of respiration in plants infected by fungal pathogens can also be explained by an increase in plant metabolism. Studies have indicated that when a plant is infected by a fungal pathogen, its growth is stimulated at first, protoplasmic streaming is increased, and materials are synthesized, translocated, and accumulated in infected tissues (Van Kan, 2006). The energy required for these activities derives from ATP produced during respiration. Since part of this energy is wasted during pathogen infection, an increased respiration is therefore induced to enable the plant to carry out its normal metabolism and activity. Infection of plants by fungal pathogens also results in the activation of the pentose pathway, compared to those of healthy ones (Palmer et al., 2004). Since the pentose pathway is not directly linked to ATP production, the increased respiration through this pathway fails to produce utilizable energy and is therefore a less efficient source of energy in fungal pathogen-infected plants. As discussed above, an alteration in the normal respiration of plants is also another stressful condition created in plants by fungal pathogens.

31.7.3 Effects on Water and Nutrient Translocation

Most of the plant pathogenic fungi negatively affect the translocation and the movement of water and nutrients in their host plants (Mace et al., 1981). Some fungal pathogens infect plant root and cause a reduced water uptake by the root cells, while many others may grow in the xylem vessels, which results in the blockage of water pathway (Mace et al., 1981). Increased and excessive respiration caused by some fungal pathogens may also create a stressful condition in plants and cause reduced water uptake and movement through the plant system (Mace et al., 1981). It is thought that many plant pathogenic fungi such as damping-off causal agents and the root-rotting fungi cause serious destructions in root tissues before appearance of above-ground symptoms (Mace et al., 1981). Root injuries directly affect the functioning of root cells in the absorption and uptake of water. Some vascular pathogens may affect and reduce water absorption by decreasing root hair production. The causal agents of fungal damping-off, stem rot, and canker diseases may reach the xylem vessels in the infected area and cause xylem tissue destruction in young plants (Mace et al., 1981). Affected vessels may also be filled with the pathogen structures and with substances produced by the pathogen or by the materials produced by the plant host in response to pathogen infection. The most typical and destructive damage to the xylem system in translocating water has been observed with some wilt-causing pathogens including Fusarium (Mace et al., 1981). These pathogenic fungi invade the root xylems and cause diseases primarily by interfering with upward movement of water through the xylem vessels. In addition to interference with water uptake, fungal pathogens may also affect and damage the plant nutrient translocation system seriously (Mace et al., 1981). Movement and translocation of nutrients produced in leaf cells through photosynthesis occurs through plasmodesmata into adjoining phloem elements and then they move to non-photosynthetic plant cells. Plant pathogens including fungi can potentially interfere with these processes and create stressful conditions in plants.

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Itisbelieved that obligate fungal pathogens such as rust and powdery mildew causal agents, can cause accumulation of photosynthetic products and inorganic nutrients in the infected tissues of the host (Mace et al., 1981). Plant pathogens may infect phloem tissues and interfere with the movement of organic nutrients from the leaf cells to phloem or with translocation through phloem elements and possibly with their movement from the phloem into the cells that need to utilize them. However, the synthesis of starch and dry weight are temporarily increased due to the movement and translocation of organic nutrients from uninfected areas of the leaves or from healthy leaves to the diseased tissues and parts of the host plants.

31.7.4 Effects on Cell Membrane Permeability

Plant cell membrane, consists of a double layer of lipid molecules and functions as a permeability barrier that allows passage into a cell only of substances needed by the cell and inhibits passage out of them (Agrios, 1988). Small water-soluble molecules such as ions, sugars, and amino acids flow through or are pumped through special membrane channels made of proteins. In plant cells, only small molecules reach the membrane because of their cell wall. Disruption or disturbance of cell membrane by chemicals or biological factors such as fungal pathogens usually increases permeability of cell membrane (Agrios, 1988; Van Kan, 2006). This results in the loss of useful substances by flowing out and excessive inflow of any substance. When a fungal pathogen attacks and infects its host plant, alteration in the permeability of plant cell membrane is the first detectable response of the plant to the pathogen invasion. The loss of electrolytes, which are small water-soluble molecules, is the most common result of alteration in cell membrane permeability (Agrios, 1988). Enzymes and toxins produced by fungal pathogens are the most important weapons of pathogens, which are used in this phenomenon. As a result of cell membrane permeability, essential and useful nutrients required for plant growth and reproduction are lost and this creates a stressful condition in plants, which most of the time causes serious damages to plant health and productivity.

31.7.5 Effects on Transcription and Translation

Transcription and translation are two important processes in plants and play very important roles in plant biology and metabolism (Agrios, 1988, Manners and Scott, 1983; Rollins, 2003). Proteins are made and produced by translation of messenger RNA that is made by transcription of plant cellular DNA. Any disturbance or interference with these processes results in serious damages to normal plant life and induces stressful conditions in plant environment. Fungal plant pathogens, particularly those that are obligate parasites such as powdery mildew and rust causal agents, can potentially affect and interfere with the transcription process in their host plants (Agrios, 1988). In some fungal infections, the composition, structure, and function of the chromatin associated with the cell DNA are changed by pathogen-induced irritations and this can affect the transcription process significantly. It has been shown that in some plants infected by fungal pathogens, especially in resistant ones, higher levels of RNA are observed compared to the healthy plants (Agrios, 1988). This is particularly true in the early stages of infection. The higher levels of RNA present in infected plants, therefore, cause an increase in transcription rate and the substances synthesized by plant cells. In addition to transcription, fungal plant pathogens may also affect the translation of messenger RNA to proteins (Manners and Scott, 1983; Van Kan, 2006). Fungal infection usually results in an increase in the level and production of plant enzymes, particularly those involved in the respiration or oxidation and production of phenolic compounds (Agrios, 1988). In addition to this, and as was described before, the level of RNA produced by plant cells are also increased after a plant is infected by fungal pathogens. The increased levels of RNA causes an additional synthesis of proteins through the translation process. An increased production of proteins by plant cells is reflected

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by additional levels of enzymes and creates an unusual situation in plant structure and function, which may induce serious stresses in the fungal pathogen-infected plants (Agrios, 1988).

31.8 Summary
Fungal plant pathogens attack plants and cause very serious losses to agricultural and horticultural crops. Plant pathogenic fungi and the infection and diseases they cause in the host plants can result in the induction of serious stresses in their hosts. They may affect physiological functions of plants and cause serious damages and disruptions in these functions. Penetration of fungi into the tissue of their host has been well researched. Pathogenic fungi are facilitated with some mechanical structures such as haustorium and appressorium that can be used in the penetration of fungus into the host plant. In addition to mechanical penetration of host plants, enzymes are also used as biochemical weapons in fungal penetration. Enzymes are subsequently used to continue penetration. Such penetration is achieved by the formation of several groups of enzymes that degrade plant cell walls and enable fungal pathogens to enter their host plant tissues. After penetration of the fungal pathogens into the host, disease-symptom induction takes place by means of toxins and growth regulators. Fungal toxins may be either non-host specific or host specific. Non-host-specific toxins are produced by phytopathogenic fungi not only in the host plant but also in other species of plants that are not normally attacked by the pathogen in nature. Pathogenic fungi produce host-specific-toxins only when they infect certain hosts. Growth regulators, which are chemical compounds that occur naturally in plants and act in very low concentrations are also very important in fungal pathogenesis. After fungal pathogens attack and infect plants, the production and occurrence of growth regulators are usually changed and altered and create stressful conditions in plants and crops. Auxin is one of the most important growth regulators. Studies have shown that auxin levels are changed in many diseased plant tissues. Several fungal plant diseases such as corn smut (Ustilago maydis) and clubroot of cabbage (Plasmodiophora brassicae) show a typical gall symptom due to the increased levels of auxin. Gibberellin is another plant growth regulator produced in some plants. In addition to auxin and gibberellin, ethylene is also produced as a growth regulator in plants. Ethylene has been considered as a signal in plants for wounding and senescent responses. Plant pathogenic fungi and their penetration, infection, and pathogenesis in plants affect basic plant functions and physiology and induce and create serious stressful conditions. Photosynthesis is the first plant function affected by pathogenic fungi. Fungal pathogens are among the most important agents that can disrupt photosynthesis and induce serious stresses in the plants. A very obvious example of the interference of fungal pathogens in the photosynthesis is the chlorosis and necrosis that they cause on the green parts of plants, which results in reduced growth of many infected plants. In addition to photosynthesis, the respiration of plants is also affected by fungal pathogens. The most evident effect of fungal diseases on infected plant respiration is the general increase of respiration as a result of faster use of reserved carbohydrates by plant tissues. Plant pathogenic fungi also negatively affect the translocation and the movement of water and nutrients in their host plants. Some fungal pathogens infect the plant root and cause a reduced water uptake by the root cells, while many others may grow in the xylem vessels, which results in the blockage of the water pathway. It is thought that many plant pathogenic fungi such as damping-off causal agents and the root-rotting fungi cause serious destructions in root tissues before appearance of above-ground symptoms. In addition to interference with water uptake, fungal pathogens may also affect and damage the plant nutrient translocation system seriously. It is believed that obligate fungal pathogens such as rust and powdery mildew causal agents, can cause accumulation of photosynthetic products and inorganic nutrients in the infected tissues of the host plant. Plant pathogens may infect phloem tissues and interfere with the movement of organic nutrients from the leaf cells to phloem or with translocation through phloem elements and possibly with their movement from the phloem into the cells that need to utilize them.

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Plant cell membrane consists of a double layer of lipid molecules and functions as a permeability barrier that allows passage into a cell only of substances that are needed by cell and inhibit passage out of them. Disruption or disturbance of cell membrane by chemicals or biological factors such as fungal pathogens usually increases permeability of cell membrane. This results in the loss of useful substances by flowing out and excessive inflow of any substances. Transcription and translation are two major processes in plants and play very important roles in plant biology and metabolism. Proteins are made and produced by translation of messenger RNA that is made by transcription of plant cellular DNA. Any disturbance or interference with these processes results in serious damages to plant normal life and induces stressful conditions in plant environment. In addition to transcription, fungal plant pathogens may also affect the translation of messenger RNA to proteins. Fungal infection usually results in an increase in the level and production of plant enzymes, particularly those involved in the respiration or oxidation and production of phenolic compounds. Additional levels of enzymes create an unusual situation in plant structure and function that may induce serious stresses in the fungal pathogen-infected plants. As was discussed in this review, plant pathogenic fungi are among the most important biotic agents that can seriously affect plant and crop health and cause serious damages and injuries to different parts of plants during various stages of their life cycle. These injuries and damages can result in the induction of stressful conditions in plants that make plants to suffer and even die due to the diseases and disorders caused by fungal pathogens. In order to have healthy and productive plants and crops, it is extremely important to protect them against fungal pathogens as was reported by several workers cited in this chapter. This can be done by using a combination of different strategies including chemical, cultural, biological, and genetic control methods to combat and overcome fungal plant diseases as was reported by several workers cited in this chapter. The successful application and implementation of control strategies will hopefully reduce damages and stresses caused and induced by fungal plant pathogens and will be a promising approach to a sustainable agriculture.

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