5 The Uredinales

K. MENDGEN

CONTENTS on most plant families and observed I. Introduction ,...... 79 that the extent of rust infection very often corre­ 11. Recent ,Studies on the Life Cycle of the lated with humid and foggy climatic conditions. Rust Fungi...... 80 He studied cross sections through infected leaves, Ill. Long-Distance Transport of Rust Spores and the Economic Importance of noted the degeneration of the chlorophyll in the Rust Diseases , , .. , , ' .... 81 cells of the diseased area, and described a matrix IV, The Infection Process of Basidiospores, between the leaf cells from which the different Aeciospores, and Urediospores 83 forms arise. Along with the scientific com­ V. Molecular Studies on Rust Fungi...... 84 VI. Cytology and Physiology of munity at his time, he believed in spontaneous the Host-Parasite System...... 85 generation of life. The matrix was assumed to be A. Cytology of the Monokaryotie Infection. ... 85 formed by diseased plant sap which, under the B. Cytology of the Dikaryotic Infection ...... 86 influence of the plant, produces the spores. The C. A New Physiological Unit. the Fungus in the Host Plant ... ,...... 87 failure of his infection experiments with spores D. Physiology and Molecular Biology of from Puccinia asarina and a rust from Salix the Aegricorpus ...... 87 supported his belief. VII. Methods of Rust Control...... 88 De Bary (1853) was the first to notice the VIII. Biological Control of Weeds with Rusts .,.. 88 IX. Conclusions...... 89 importance of the germ pore on spores for the References ,...... 89 production of germ tubes of rusts and smuts. He discussed the importance of tip growth for the ability of a fungus to grow through the stomatal I. Introduction opening. Excellent pictures of develop­ ment reflect his skills for correct observation and '. the improvement of the microscope at that time. Rust-infected wheat leaf fragments have been A few years later, De Bary (1865) elucidated the found in a storage jar from the Late Bronze Age life cycle of P. graminis, the of wheat, filled with wheat grains (Kislev 1982). This report, coined the term teleutospore as the final spore together with numerous others of plant diseases in form in the life cycle, and defined autoecious and the ancient literature, obviously indicating rust heteroecious rust fungi. fungus infections, emphasizes the importance of In the book Die Getreideroste, Eriksson and these pathogens for human food production (Leh­ Henning (1896) described the specialization of the mann et al. 1937; Chester 1946; Schafer et al. rust fungi on cereals. Stakman and Piemeisal 1984). In his book on agriculture, Duhamel du (1917) found races of wheat stem rust. This result Monceau (1779) mentions stem rust "as an ex­ was the basis for an effective breeding program for treme nuisance: the most beautiful grains are re­ resistance in cereals and other plants. In 1927, duced to nothing as soon as the stem is completely Craigie discovered heterothallism of wheat stem covered by rust". rust and elucidated the function of the pycnia The first comprehensive description of rust (spermogonia) as sexual organs. This was the final fungi, containing some 120 species, was published step in the explanation of the rust life cycle. by Unger (1833). He found different rust fungi or The gene-for-gene concept by Flor (1956), re­ sulted from experiments with flax rust, Melampso­ ra lini, and explained the interaction of genes for Fakultat fur Biologie, Lehrstuhl Phytopathologie, Univer­ sitat Konstanz. Universitats str. 10, D-78464 Konstanz, avirulence in the rust fungus and genes for resis­ Germany tance in plants. Today, rust fungi represent an important subject for basic research, since these fungi are unique in the way they recognize the stomatal opening of their host leaves (Hoch and Staples 1987, 1991. Chaps. 2, 3, Vo\. V, Parl A) or produce highly differentiated haustoria within host cells. This chapter on Uredinales cannot cover the Cl complete literature published even for a single C 'C year on rust fungi. It mainly presents key referenc­ 0. es from the past few years and cites review articles Cl) and books for access to the more specialized liter­ ature on most aspects of rust fungi. A general introduction into the life of rust fungi can be found in the books by Littlefield (1981) and Alexopoulos .... et al. (1996). A treatise on most questions consid­ Q) c ering cereal rusts has been edited by Bushnell -~ (Bushnell and Roelfs 1984) and Roelfs (RoeUs .... , and Bushnell 1985). More general morphological, Q) taxonomic and phylogenetic information on rusts E E has been published by Gaumann (1959), Cummins ::J Cl) and Hiratsuka (1983), Preece and Hick (1990) and Swann and Taylor (1995).

11. Recent Studies on the Life Cycle of the Rusts

Rust fungi exhibiting all spore forms are called Fig. 1. Life cycle of Uromyces viciae-Ialme. Aflc:r ovc:rwin­ macrocyclic. The following numbers are assigned tering on residual plant material. germinate, to the various fruiting structures (sori) and spores meiosis (M) occurs, and the metabasidium produces hap­ loid (n) basidiospores of two mating types (+.-): basid­ in the life cycle: 0 - pycnia and pycniospores (= iospores are ejected and land on the hostlear. differentiate spermogonia and spermatia), I- aecia and a~­ infection structures, and pycnia are produced on the upper ciospores (= aecidia and aecidiospores), 11 - ure­ side of the leaf: after spermatization (pycniospores may be dia and urediospores (= uredinia and uredospores transported by insects) dikaryotization occurs in aecial pri­ mordia (n --1 n + n), and the aecium differentiates on the or urediniospores), III - telia and teliospores lower side of the leaf: aeciospores (n + n) infect and ure­ (= teleutosori and teleutospores), IV diospores arc produced: Summer: urediospores infect and basidiospores. The existence of different spore produce urediospores repetitively: in autumn, uredia dif­ ferentiate into tclia: the nuclei fuse (n + n --1 2n) during names is due to historical reasons, when the origin sporogenesis and teliospores develop. (F. Meinhard, and the tasks of the different spore forms was not A. Klink, U. Labitzke, and M. Hahn contributed to the yet known. The introduction of new names is diagram) sometimes difficult to understand (Savile 1968). Rusts restricted to a single host are autoe­ gus deletes both aecia and uredia (uredinia), leav­ cious, such as Uromyces viciae-fabae (Fig. 1) on ing the telial and pycnial stage. The latter may be Vicia faba, rusts infecting an alternate host during missing also. In the abbreviated life cycle, all mi­ the life cycle are heteroecious, such as Puccinia crocyclic forms are autoecious. Thus, the gener­ graminis (Pers.) on barberry and cereals (Arthur al scheme as shown in Fig. 1 has many variations. 1962). This rust changes nuclear condition with A more extensive description can be found in the the host plant. The macrocyclic rusts produce re­ reviews by Petersen (1974) and Cummins and petitive infections in an asexual cycle by means of Hiratsuka (1983). urediospores. Fertilization generally occurs in the spermog­ A life cycle which deletes the uredial stage is onial stage. However, exchange or complementa­ termed demicyclic. Sometimes, pycnia with pyc­ tion of nuclei can also be carried out by dikaryotic niospores are also missing. A microcyclic rust fun- urediospores (Groth 1988). 81

Teliospores or teleutospores represent the evolved only once. Reductions could have easily final spore form of the rusts and, as a rule, provide occurred at any stage of evolution (Laundon the basis for rust nomenclature (Mendgen 1984). 1973). Wahl et al. (1984) discussed host-parasite For a recent example see the comparison of an­ coevolution processes for the cereal rust fungi. amorphs and. teleomorphs for the delimitation Since genetic recombination occurs in teliospores. of Phakopsora. Cerotelium. and Physopella (Ono its influence on diversity and distribution of viru­ et al. 1992). Sometimes this nomenclatural rule lences can be studied in the derived aecial popula­ is difficult to apply. For example, P. pampeana tions and is typical for various regions (Groth and (Speg), the rust of cultivated Capsicum spp., pro­ Roelfs 1982; Kolmer 1992; McCain et al. 1992). In duces Aecidillm-like and Pllccinia-Iike sori. Both centers for coevolution, genes responsible for spore types from these sori produce basidia con­ plant defenses and genes for fungal virulence have taining four basidiospores. Basidiospores of both accumulated. Redistribution of the maifb host or types of spores produce pycnia, followed, after the alternate host by human influence has given spermatization, by aecidoid and, a few weeks lat­ rise to subsequent independent evoluti'on of er, by telioid sori. Thus, this rust is both an Endo­ the gametophytic or the sporophytic generation phyllllm and a Puccinia species. The unicellular (Anikster and Wahl 1979: Anikster 1984). Endophyllllm spores are responsible for the rapid This diversification has complicated the spe­ dissemination and dispersion in the field. cies concept in rusts. Obviously, morphological The Gicellular Puccinia-like spores exhibit and physiological aspects need to be evaluated if a dormancy and thus can survive hot and rainy peri­ species or a forma specialis is to be defined (An­ ods in summer. This is an interesting alternative ikster 1984; Savile 1984). A modern concept is the for a tropical rust to survive unfavorable condi­ virulence formula to indicate race specificity and tions (Hennen et al. 1984; Figueiredo et al. 1987). the interaction with the host plant according to the The survival strategy is different from the well­ avirulencelvirulence pattern of a rust (Roelfs et al. known example of P. graminis (Pers.), which is 1992). long-cycled and heteroecious. P. graminis is native in the north temperature zone, where heteroecism is common. This fungus shows an adaptation to Ill. Long-Distance Transport of Rust seasonal climatic fluctuations, especially weather Spores and the Economic Importance of conditions during spring and winter (Anikster and Rust Disease Wahl 1979). As mentioned above, Endophyllum ae­ ciospores are generally produced in typical aecia. Long-distance spread of rust spores is an impor­ The nuclei fuse in these aeciospores and, upon tant factor for the damage that rust diseases in­ germination, a metabasidium is produced where duce (Nagarajan and Singh 1990). In the USA. meiosis takes place and basidiospores develop. spore movements occur with prevailing winds However, some races of Endophyllllm ellphorbiae from the southwest to the northwest. Such winds sylvaticae remain haploid during their whole life may transport many urediosporcs of P. graminis cycle (Gaumann 1959). Pers. f. sp. tritici. since a single wheat leaf infected From the examples given above, it can be with this fungus can produce more than a million assumed that the genes responsible for spore urediospores (Zadoks and Schein 1979: Burdon morphology and the genes that govern nuclear 1987). This long-distance transport occurs annual­ behavior can act independently. Other factors also ly (800km) across the North American Great act independently. Urediospores and aeciospores Plains (Roelfs et al. 1992) and nearly annually of U. vignae differ in genesis and morphology, but (2000km) from Australia to New Zealand (Luig their behavior, physiology, and development after 1985). Losses can be significant (McGrath and germination are very similar (Stark-Urnau and Pennypackers 1991). Mendgen 1993). Peanut rust (P. arachidis Speg) was confined Plants and their rusts are excellent examples to tropical America and China until 1969 and sud­ of coevolution. The rusts on ferns and conifers are denly appeared in southern Asia and Oceania dur­ believed to be descendants of ancient rusts. Nearly ing the early 1970s. on the Ivory Coast in 1976, all rusts on ferns are both heteroecious and macro­ and in Senegal in 1980 (Savary et a1. 1988). About cyclic. It can be speculated that the extraordinarily 80% of the world production of peanuts r'Jmes complex heteroecious macrocyclic life cycle from developing countries. most of it from the semiarid tropics. Here, yields are low, around speed of 10 m Si, horizontal transport of 2000 km 800-900kg ha-I, compared with approximately would occur during 2.3 days. In the Caribbean 2500 kg ha-I in the developed world. This is be­ region, the spores met the highly susceptible cane cause the farmers cannot afford the cost of crop cultivar B 4362, which had been grown in the re­ protection chemicals. Rust accounts for about gion for more than 20 years. Therefore, the rust 50% of the losses, sometimes for much more met no resistance and caused losses of some 40% (Subrahmanyam et a\. 1985). (Comstock et a\. 1992). Puccinia mefanicephala, the sugar cane rust, The coffee leaf rust () af­ has been present in scattered locations in Africa fecting wild coffee was discovered in 1861 in the and Asia and was of minor significance for many Lake Victoria region of Kenya. After appearing in years. During July 1978, this rust first appeared in Ceylon 1867, the rust literally had extinguished the Dominican Republic and 1 year later it had the coffee trees from the island by 1882. In Carfea spread to almost all sugarcane-growing areas in arabica, a single rust pustule may cause premature the Americas. In retrospective analysis of meso­ abscission of the leaf (Javed 1982). Rapid defolia­ cale meteorology during the I-month period be­ tion may follow and repeated infection by rust will fore July 1978, it was found that a Saharan dust cause death of a tree. The rust spread through cloud traveled through the Atlantic trade winds Southeast Asia in the following years and finally from the coast of West Africa to the Caribbean reached Bahia, Brazil, early in 1970. Two yeats area within 5 days in June 1978 (Purdy 1985). later, the rust fungus invaded Paraguay and Ar-, Assuming a terminal deposition velocity of gentinia. It reached Nicaragua in 1976, Peru in 12.2 mms-I, a urediospore at an altitude of 3000 m 1979, and was detected in Ecuador and Mexico could travel for 2.3 days. With a uniform wind during 1981. Wind alone was not always responsi-

Fig. 2. Spore, germ tube, and appressorium (over the stomatal opening) of Uromyces viciae-fabae on the host leaf (Vicia faba) as seen with a low-temperature scanning electron microscope at -150°C. Magnification 900 x 83

b a UREOOSPORE UREDOSPORE:

PENETRATION HYPHA J I \.

HAUSTORIAL MOTHER CELL c d BASIDIOSPORE BASIDIOSPORE PENETRATlON HYPHA _ APPRESSORIUM

INTflAEPlDERMAL VESICLE :-----:;:----.:::::

Fig.3a-d. Diagrammatic representation of direct and sto­ dikaryon. b Phakopsora pachyrhizi. dikaryon. c Crollar­ matal penetration by rusts in the haploid and in the dikary­ (hUll ribicola. monokaryon. d Urol11."ces appendicula(II.1'. otic stage (not drawn to scale), a Uromyces viciae-fahae. monokaryon ble for distribution of this disease. It could not dikaryotic stages of the same fungus on one host have spread this way from Brasilia to Nicaragua plant or, in the case of heteroecious rusts. on two because of prevailing natural geographical barri­ host plants from different plant families. In addi­ ers. The introduction into Nicaragua constitutes a tion. rust fungi may penetrate the plant cuticle good example of spread by migrant workers, who directly or through stomatal openings (Fig. 2: carried seedlings and thus seem to have imported Chap. 2. VoL V, Part A). Below. infection strate­ the disease (Schrieber and Zentmyr 1(84). Alto­ gies of urediospores, and basidiospores are com­ gether, it took coffee rust about 120 years to travel pared (Fig. 3). around the world. The spores differ considerably in their mor­ phology. Recent descriptions have been published in books by Littlefield and Healh (1979). Little­ field (1981), and Preece and Hick (1990). The IV. The Infection Process of physiology and the effect of germination stim­ Basidiospores, Aeciospores, ulators or inhibitors are reviewed by French (1992: and Urediospores see also Chap. 2, VoL V, Part A). Basidiospores are smooth, thin-walled, and do not withstand dry periods. Aeciospores have a thick wall and a typ­ Rust fungi offer the unique possibility to the study ical surface ornamentation with small knob-like of infection structures of monokaryotic and structures. Urediospores have a thick. darkly pig- 84 mented wall with germ pores and typical spine­ from the differentiation of the penetration hypha like ornamentations. (Deising and Siegrist 1995; Deising et a1. 1996). The development of infection structures from Surface carbohydrate patterns on hyphae of in­ these spores has been reviewed recently (Gold fection structures are typical either for the and Mendgen 1991; Mendgen and Deising 1993; monokaryon or for the dikaryon, and this is inde­ Mendgen et at. 1996). Upon landing on a wet leaf, pendent of whether or not a change of the host or under humid conditions, a gelatinous matrix plant is involved (Freytag and Mendgen 1991). forms an adhesion pad below the spores. Cutinase, The physiology of enzyme secretion by rust esterases, and other unspecific factors contribute infection structures is unique. The dikaryon of U. to the adhesion process of bean rust urediospores. viciae-fabae produces wall-degrading enzymes After germination, germ tubes adhere firmly to during differentiation. Starting with the growth of the plant surface, a prerequisite for the ability of the appressorium, acidic cellulases are secreted in bean rust germ tubes to recognize the stomatal the absence of the substrate. During infection hy­ opening (Epstein et al. 1985; Clement et al. 1993). pha development, pectin methyl esterase is syn­ The germling. including the appressorium, is thesized, also in the absence of the substrate. shown in Fig. 2. The recognition process of the During haustorium mother cell development, po­ dikaryon may be quite precise. Differences in Iygalacturonate lyase formation is controlled by height of the outer ledge of the stoma within a few both the differentiation stage and the availability microns are recognized (Hoch et al. 1987). For of substrate (Deising ct a1. 1995). Corresponding penetration, the guard cells can be pushed apart studies of enzyme production by basidiospore­ (Fig. 3a). However, the dikaryon of the soybean derived infection structures are not yet available. rust (Phakopsora spp.) produces appressoria on any hard surface and penetrates epidermal cells directly (Fig. 3b; Koch and Hoppe 1988). All ap­ v. Molecular Studies on Rust Fungi· pressoria derived from dikaryotic spores (ure­ diospores and aecidiospores) appear similar in morphology (Kwon and Hoch 1991; Swann and Molecular methods have dramatically increased Mims 1991). Also the development of infection our knowledge of the genome of rust fungi during structures derived from urediospores and aecid­ the past few years. Reassociation kinetics suggest iospores of the cowpea rust does not differ appre­ a haploid genome size of4.7 X 107bp for P. sorghi. ciably (Stark~Urnau and Mendgen 1993). In Half of it represented a moderately repetitive contrast, most haploid basidiospores barely d(ffer­ fraction (Anderson et a1. 1992). P. graminis f. sp. entiate typical appressoria and penetrate epider­ tritici has a haploid genome size of about 6.7 X mal cells directly (Fig. 3d; Morin et al. 1992); 107bp with about 64% unique, 4% foldback, and however Cronartium spp. basidiospores produce a 30% repetitive DNA sequences. The repetitive long germ tube and penetrate through the stomata sequences have a total complexity of 390 kb and (Fig. 3c). Studies on the process of stomatal recog­ are repeated on an average of 52 times. The aver­ nition by this monokaryon, such as have been age amount of DNA per ungerminated ure­ done with the dikaryon of Uromyces appendicula­ diospore was 435 fg. The spores were in G 2 tllS, would be interesting. (Backlund and Szabo 1993). The mitochondrial The penetration hypha of the dikaryon is genome of P. graminis f. sp. avenae has a size of highly differentiated to perform its tasks. It reach­ 80.2kb, with an average of 21 copies per ure­ es through the stoma in the case of most rusts, or diospore germling (Sock et al. 1994). Based on through the epidermal cell in the case of Phacop­ light microscopy, the haploid chromosome num­ sora spp., and is delimited by a septum (Koch and ber of P. graminis f. sp. tritici was assumed to be Hoppe 1988; Terhune et a1. 1993). In the haploid n = 6. However, recent ultrastructurally derived stage, the penetration hypha appears less differen­ reconstructions of sectioned fungal pachytene nu­ tiated. A septum is missing in most cases and a clei provided a definitive karyotype of n = 18 plug is produced which separates the more or less (Boehm et al. 1992). A similar number was found differentiated appressorium from the vesicle and for (Boehm and Bushnell 1992). the infection hypha in the host leaf. In all cases, This technology, applied for the analysis of however, the chitin of the fungal wall appears pachytene centromeres, allowed the discrimina­ masked by glycoproteins and glucans starting tion of the phylogenetically related moss parasite, R5

Eocronartium muscicola, from the Uredinales tion with rust (Melampsora lini) and in stem rust (Boehm and McLaughlin 1989, 1991). (P. graminis tritici) (Liu et al. 1993; Roberts and Biochemical and molecular methods also help Pryor 1995). These results demonstrate that mole­ to differentiate rust fungi from one another. The cular methods open a new door for the character­ rusts that attack cowpea (Vigna sinensis) or beans ization of rust gene products possibly influencing (Phaseolus vulgaris) have been considered to be the virulence of the fungus. A transformation sys­ either identical (Boerema and Verhoeven 1979), tem may help to elucidate the role of such genes or different varieties of the same species (Arthur (Bhairi and Staples 1992). The detection of dou­ 1962), or separate species (Fromme 1924). After ble-stranded RNA viruses has added a new di­ separation of proteins from urediospores by two­ mension to the possible biocontrol of rust fungi dimensional isoelectric focusing polyacrylamide (Zhang et al. 1994). gel electrophoresis, Uromyces appendiculatus (the bean rust) and Uromyces vignae (the cowpea rust) shared only 183 polypeptides out of 335 polypep­ VI. Cytology and Physiology of the tides (Kim et al. 1985). This result was confirmed by DNA hybridization techniques (Braithwaite et Host-Parasite System al. 1991). In addition, nuclear ONA content was used as a tool in fungal taxonomy. It had already A. Cytology of the Monokaryotic Infection been shown that variants observed after artificial culture of stem rust exhibited differences in ge­ In the monokaryotic stage, hyphae grow inter- and nome sizes (Williams and Mendgen 1975). Fluo­ intracellularly. The fungal cytoplasm is dense. rescence of nuclei in binucleate basidiospores and ·Endoplasmic reticulum-derived, tubular vesicular mononucleate pycniospores as a measure for rela­ complexes suggest high protein synthesis rates. tive amounts of DNA content among the rusts Golgi equivalents, mitochondria, filasomes, and ranged from 0.8 to 6.8 times that of P. graminis. microtubules are numerous (Mims et al. 1988; Isolates of P. recondita and P. hordei from differ­ Mims and Richardson 1989; Gold and Mendgen ent telial hosts differed considerably in DNA con­ 1991). Hyphae are covered with an amorphous, tent (Eilam et al. 1992). Also, DNA restriction electron-opaque extracellular matrix which close­ fragment length polymorphisms and the internal ly contacts host cells. Hyphae enter mesophyll transcribed spacer region in the nuclear ribosomal cells to form intracellular hyphae (also called repeat unit were useful to discriminate rust species monokaryotic haustoria) without evident modifi­ and races of P. graminis f. sp. tritici (Martinez et al. cation of the fungal protoplast (Littlefield and 1991; Anderson and Pryor 1992; Zambino and Heath 1979; Harder 1984; Hopkin and Reid 1988). Szabo 1992, 1993; Gardes and Bruns 1993). Poly­ Even the host vascular system is invaded, which morphic DNA analysis revealed relationships does not occur in the dikaryotic stage of rusts among diverse genotypes in Australian and Amer- (Larous and LoseI1993b). The different strategies l ican collections of V. appendiculatus (Maclean in the monokaryon and dikaryon for the acquisi­ et al. 1995). tion of host assimilates are discussed by Larous During differentiation of infection structures, and Losel (1993a). Host cell responses as a result the development of each morphological unit is of fungal penetration are quite variable (Heath correlated with the appearance or disappearance, 1989; Stark-Urnau and Mendgen 1995; Heath and increase or decrease in concentration of certain Skalamera 1997). polypeptides (Staples and Macko 1984; Deising The mononucleate hyphae finally aggregate and Mendgen 1992). By cascade hybridization and form the pycnium, a structure in which the several differential-specific genes have been iso­ gametes of the rust fungi are produced (Harder lated (Bhairi et al. 1989). The infection structure 1984). The sporophores are uninucleate and elon­ gene (INF 24) from Uromyces appendiculatus had gated. Spores are produced in chains (Mims et al. no homologues in nonrust fungi (Xuei et al. 1992). 1976; Harder and Chong 1978; Metzler 1981). Fer­ INF 56 represented a member of a multigene fam­ tilization occurs by means of pycniospores and ily preferentially expressed during development flexuous hyphae which reach out of the pycnium. of appressoria (Xuei et al. 1993). Genes expressed Following dikaryotization, the aecium is produced only during growth of the fungus within the host as the fruiting structure that produces aeciospores plant have been characterized in flax after infec- and reinitiates the dikaryotic phase. The dikaryo- 86 tization process is poorly understood (Harder 1984). It is known, however, that the dikaryotic primary aeciosporophores arise from multinucle­ ate fusion cells (Rijkenberg and Truter 1974).

B. Cytology of the Dikaryotic Infection

After the development of the infection hypha and during the differentiation of the primary haustori­ um, intercellular hyphal growth starts with a branching of the infection hypha. Growth and branching of hyphae continue together with pro­ duction of haustorial mother cells and haustoria until a certain leaf area - the amount of hyphae depends very much on the different rusts - is col­ onized. Composition and structure of the cyto­ plasm are comparable to the monokaryon (Littlefield and Heath 1979; Harder 1984; Welter et al. 1988: Gold and Mendgen 1991). The hyphal tip has, similar to the situation in other fungi, a Spitzenkorper (Hoch and Staples 1983). Nuclei and nuclear division have been studied in detail (Harder 1984; Swann and Mims 1991; Boehm and Bushnell 1992; Boehm et al. 1992). Haustorial differentiation starts with the de­ velopment of a haustorial mother cell at the hy­ Fig. 4. Haustorium of Uromyces vicilfe-fil!JGe (dikaryon) phal tip. Basically, the cytoplasmic contents do not after high-pressure freezing and freeze substitution. The haustorium is smoothly embedded within the cytoplasm of differ from those of intercellular hyphae. Howev­ the host plant. Magnilicalion 12250X. (U. Ba-chem and K. er, mitochondria undergo a change in conforma­ Mendgen,' unpubl.) tion and distribution. They round up and migrate to the periphery of the protoplast. Nuclei are more compact and the ER increasingly forms tub~lar vesicular complexes (Harder 1984; Knauf et al. plant cell symplastically into the haustorium 1989: Harder and Chong 1991). Walls become (Heath 1976). The haustorial body develops at the thicker and include additional layers. The septum end of the neck, increases in size during aging, and is composed of more layers than normal hyphal becomes a multilobed, rigid structure (Hahn and septa. A transfer apparatus is associated with this Mendgen 1992). The haustorium has a layered septurn and the whole structure seems to support wall, is surrounded by the extrahaustorial matrix the subsequent penetration of the host cells. and is embedded within the cytoplasm of the host Roughly in the middle of the contact area with plant (Fig. 4). This matrix contains various sub­ the plant cell wall, a penetration hypha develops. stances, including (X- and f3-linked sugars and The penetration hypha elongates to form the polysaccharides (Harder and Chong 1991). Al­ haustorial neck. The neck wall differs from that in though the detection off3-linked sugars in this area the area of host cell wall penetration and from the indicates a contribution from the fungus, the bulk wall of the subsequently formed haustorial body. of material seems to come from the host cell: the The neck wall is characterized by a neck ring, a extrahaustorial membrane smoothly surrounds structure with high mineral content (iron, phos­ the haustorium of both monokaryotic and dikary­ phorus, and silicon) and a zone with peroxidase otic infections. Many coated extensions of this activity. Evidence suggests that the neck ring has a membrane reach into the host cytoplasm and function similar to that of the Casparian strip in suggest endo- and exocytotic events. Although root endodermal cells in controlling apoplastic continuous with the host plasmalemma, the extra­ flow. It would force substances from the infected haustorial membrane is highly modified in several 87

respects. Freeze-etch studies have revealed a loss tions is hypersensitive cell death frequently ob­ of intramembrane particles, increased thickness, served. This event seems to interfere with the loss of ATPase activity (Woods and Gay 1987), growth of haustorial pathogens requiring living and a reduced reactivity with stains for poly­ plant cells. Programmed cell death is reminiscent saccharides. The meaning of these modifications of apoptosis in animals (Ryerson and Heath 1996). remains to be explained (Harder and Chong The recent characterization of the flax rust resis­ 1991 ). tance gene L 6 is a first step in the elucidation of a Some days after infection, fungal hyphae ag­ signal receptor in the plant membrane that seems gregate in an intercelJular space underneath the to be involved in the recognition process between epidermis. These celJs form the base of the fruiting plant and pathogen (Ellis et al. 1995: Lawrence et structure. Elongated, sporogenous cells give rise al. 1995). This result will help to explain the stcps to stalk cells and urediospores. Accessory cells from recognition of the fungus to activation of with no obvious function mingle with the ure­ defense and the final outcome, the hypersensitive diospores. The succession of urediospores from a reaction. sporogenous celJ and its development is described It is generally assumed that the new physio­ in detail by Harder (1984). Later in the season, logic status of the host benefits the fungus. Most such sporogenous cells also produce teliospores obvious are green islands, which develop in the (Mendgen 1984). colonized tissue when the surrounding tissue be­ comes chlorotic (Dekhuijzen 1976; Bushnell 1984: Durbin 1984). Even if the central area of the pus­ c. A New Physiological Unit, the Fungus in tule becomes necrotic. a green ring often will re­ the Host Plant main. In the infected cells. organelles (e.g.. the nucleus) change size and movements dramatically The pathogen and the host, both together, (BushneIl1984; Xu and Mendgen 1991). and very produce a symbiotic structure, the aegricorpus often migrate towards the site of fungal penetra­ (Loegering 1984). It is a result of coevolutionary tion. Changes in gene expression of the host plant processes (Heath 1991). A study of the pathogen during the early stage of infection and the increase or the host alone cannot explain the physiology of of the intermediary metabolism of the plant reflect the diseased plant. With biochemical and physio­ these changes (Chakravorty and Scott 1982). Cy­ logical methods, it is difficult to discriminate the tokinins (Durbin 1984). auxins (Pegg 1976) and contributions of each partner. Molecular methods ethylene (Daly 1976; Paradies et al. 1979) are pro­ have improved the situation by analyzing the ac­ duced in high concentrations. General defense tivity of single genes during infection (Liu et al. mechanisms (e.g., lignification) of the plant are 1993). They will help us find and analyze plant induced (Moerschbacher et al. 1988: Fink et al. ,disease resistance genes (Bennetzen and Hulbert 1991). Autofluorescence of cell walls and papillae 1992). Genetic studies of the interaction by FIar are observed (Ryerson and Heath 1992). Phytoal­ (i971) resulted in the gene-for-gene concept. Re­ exins may contribute to the defensc of the rust cent advances of this theory are summarized by fungus (Mayama et al. 1991). On the other hand. Knott (1989). It tells us about the outcome of the photosynthesis and chlorophyll content dccrease interaction of two clones, the host and the para­ and a considerable drop in activity of xanthine site, in which classical diploid inheritance occurs. oxidase is observed (Berghaus and Reisener 1985: Some problems with this model still exist (Loeger­ Montalbini 1992). This is followed by a loss of ing 1984), although it is generally accepted epidermal cell turgor and a reduction in the effi­ (Chaps. 1, 15, 16, this Vol.). ciency of the roots to replace water losses (Paul and Ayres 1985; Berryman et al. 1991). The inter­ action between host and parasite might be regu­ D. Physiology and Molecular Biology of lated by race specific or unspccific elicitors and the Aegricorpus suppressors of plant defense reactions induced by the fungus (Beissmann and Koge11991; KogeI and Rust fungi are biotrophic parasites. The infected Beissmann 1991; Beissmann et al. 1992: Heath host cells undergo many changes, but continue to 1995: Yamamoto 1995). live during fungal development (Heath and With the successful culture of rust fungi on Skalamera 1996). Only in incompatible combina- relatively simple media containing mainly sugars. 88 minerals, and amino acids (Maclean 1982; Will­ (1992). An overview on genes for resistance iams 1984), obligate parasitism has lost many of its against whe3t rusts is available (Mclntosh et al. mysteries. It seems that the increased metabolic 1995). As an alternative to the pure line cultivars, activity of the host mainly provides a generous intraspecific mixtures of different genotypes or supply of simple substrates such as sugars and interfield diversity together with a regional amino acids (Durbin 1984). A well-balanced sup­ deployment of resistance genes was discussed ply of such substrates induced the production of (Mundt and Browning 1985). The evolution of a infective urediospores and teliospores, but no superrace capable of overcoming many Sr genes haustoria on artificial media (Kuck and Reisener for resistance against rust may destroy such hopes 1985). In addition, rust fungi can be grown on (Gates and Loegering 1991). Also, cultural meth­ epidermal monolayers (Mendgen and DressIer ods such as early sowing to avoid stem rust or the 1983) and in liquid culture (Fasters et al. 1993). induction of resistance to rust by avirulent races (Van Asch et al. 1992) should not be forgotten. The detection of chemically induced resistance in VII. Methods of Rust Control wheat opens new dimensions to rust control (Gorlach et al. 1996). Biological control of rusts with hyperparasitic 1 The first known effective means to control rusts fungi has been tried often (Kranz 1981), but is still was mandated by a law in Rouen, France, from in its infancy. Of 24 species of fungi in 12 genera' 1660, requiring the destruction of barberries screened for their hyperparasitic activity towards near grain fields. The Connecticut barberry law of on oat seedlings, 7 Verticillium 1726, and subsequent barberry laws in other states spp. and Acremonium implicatllm were able to and countries, are proofs of farmers' powers of colonize uredial sori (Leinhos and Buchenauer observation. This method of control is still valu­ 1992). In addition, Erwinia spp., Bacillus spp., and able today (Roelfs 1982), but only for Pllccinia Trichoderma spp. have been recommended for graminis. rust control (Govindasamy and Balasubramanian Currently, chemical control and breeding for 1989; Kempf and Wolf 1989; Rytter et al. 1989). resistance go together. Buchenauer (1982) evalu­ However, because of the high humidity require­ ated the use of the more established fungicides ments of hyperparasitic fungi, such methods are such as dithiocarbamates, and compared them not effective in temperate or arid conditions with carboxylic acid anilides, morpholine deri­ (Grabski and Mendgen 1986). In the tropics, bet­ vates, Indar, and inhibitors of ergosterol bi..o­ ter results may be obtained (Saksiriat and Hoppe synthesis. Azole fungicides in general and the 1990). recently introduced triazole fungicides exhibit high biological activity at low application rates (Kuck and Scheinpflug 1986; Saur et al. 1991). VIII. Biological Control of Weeds with Rowell (1985) described the different in vitro tests Rusts for fungicides, such as spore germination and mycelial growth tests, or in vivo tests, such as seed­ ling assays and field evaluation. In Western Eu­ Biological control of weeds has a long and some­ rope, intensive cropping systems, high yield and times very successful history. Examples with rusts high grain prices permit economic use of chemical are the control of skeleton weed (Chondrilla jlln­ control of rusts. However, genetic resistance is cea) by P. chondrillina in Australia and California important under any circumstance. Most rust­ (Burdon 1987; Supkoff et a1. 1988) and blackberry resistant cereal cultivars have remained so for 5 (Rubus spp.) by Phragmidium violacellm (Tem­ years or more, which is about the life span of an pIeton et al. 1979). Other examples are cited by active breeding program (Roelfs et al. 1992). Oth­ Watson (1991) and Evans and Elliston (1990). ers have remained resistant for many years. A According to Charudattan (1991) some 107 fungal discussion of this problem can be found in several taxa, including many rust fungi, are presently reviews (Robbelen and Sharp 1978; Dyck and under investigation for the biological control of Kerber 1985; Parlevliet 1985; Knott 1989). Recent weeds. Currently, the control of diffuse and spot­ progress in the establishment of durable resistance ted knapweeds (Centaurea ditfusa and C. maC/l­ was explained by Steffensen (1992) and Mclntosh losa) with Puccinia jaceae appears promising, 89 since it forms heavy stem infections early in the Acknowledgments. Or. Matthias Hahn, Konstanz, season. This rust has a restricted and stable host Or. Stefan Wirsel, Konstanz, and Pro£. Or. Roland range and the danger of damaging safflower Rohringer, Gottingen, read the manuscript. (Carthamus tinctorius) is restricted to a short peri­ od during the seedling stage of the plant and thus appears to be of minor importance (Mortensen References et at. 1991). Cyperus esculentus was only recently intro­ duced into The Netherlands. Its growth capacity Alexopoulos Cl. Mims CW. Blackwell M (1996) Introduc­ tory mycology, 4th edn. Wiley. New York. ~68 pp and its insensitivity to many herbicides caused Anderson PA. Prym AJ (1992) DNA restriction fragment considerable losses. Integration of biological con­ length polymorphisms in the wheat stem rust fungus. trol with P. canaliculala and subsequent treatment Puccinia graminis tritici. Them Appl Gen 83:715­ with herbicides resulted in a rapid decline of the 719 Anderson PA. TyIer BM, Pryor A (1992) Genome com­ weed in the USA (Callaway et al. 1987). However, plexity of the maize rust fungus. Pllccinia sorghi. Exp since this rust also infects Cy. fuscus, it was not Mycol 16:302-307 introduced for use in Europe (Scheepens and Anikster Y (1984) The formae speciales. In: Bushnell WR, Hoogerbrugge 1991). Roelfs AP (eds) The cereal rusts, voll. Academic Press. Orlando. pp 115-130 Anikster Y. WahlI (1979) Coevolution of the rust fungi on Gramineae and Liliaceae and their hosts. Annu Rev Phytopathol 17:367- 403 IX. Conclusions Arthur JC (1962) Manual of the rusts in United States amI Canada. Hafner. New Yark Baeklnnd JE. Szabo LJ (1993) Physical characteristics of Rust fungi are a group of parasites highly adopted the genome of the phytopathogenic fungus Pllccillia to their host plants. They may be useful as .myco­ graminis. Curr Gen 24:89-93 Beissmann B. Kogcl KH (1991) Identification and charac­ herbicides but, in most cases, are deleterious to terization of suppressors. In: Linsken HF. Jackson JF many crops. The control of rusts by either geneti­ (eds) Plant toxin analysis. vol 13. Springer. Berlin cal resistance or the use of chemicals and, to a Heidelberg New York. pp 259-275 smaller extent, also by cultural methods is still a Beissmann B. Engels W. Kogel K. Marticke KH. Reisener Hl (1992) Elicitor-active glycoproteins in apoplastie major problem. Cultural methods, such as the in­ fluids of stem-rust-infected wheat leaves. Physiol Mol terruption of the life cycle or cultivation to remove Plant Pathol 40:79-89 volunteer plants from an earlier crop are effective, Bennetzen lL. Hulbert SH (1992) Organil.ation. instability but by far not sufficient means of control. Several and evolution of plant disease resistance genes. Plant Mol Bioi 20:575-578 fungicides are effective, safe, and easy to use. Berghaus R. Reisener HJ (1985) Changes in photosynthe­ However, they may represent a problem for our sis of wheat plants infected with wheat stem rust (Puc­ environment. Some pathogens have become resis­ cinia gral11inis 1'. sp. trith·i). Phytopathol Z 112:165-172 ta~t to fungicides and other methods are prefera­ Berryman CA. Eamus D. Farrar IF (1991) Variations in epidermal cell turgor of rust-infected barley seedlings. ble.l Therefore, the use of resistant cultivars is of New Phytol 119:535-540 major importance and adds no extra cost to farm­ Bhairi SM, Staples RC (1992) Transient expression of the ers. However, resistant cultivars are developed j3-glucaronidase gene introduced into Uromvccs appcll­ and released and, as soon as production increases diclllatlls uredospores by particle bombardmcnt. Phyto­ pathology 82:986-989 rapidly, new, virulent races appear. The breeding Bhairi SM, Staples RC, Freve p. Yodcr OC (1989) Charac­ cycle then starts over again. Therefore, research terization of an infection structure-specific gene from on the interaction of rusts with their host plants the rust fungus Uromyces appendicllla/lls. Gene 81 :237­ 243 should be increased. Physiological and cytological Boehm EWA. Bushnell WR (1992) An ultrastructural studies have helped us to understand this interac­ pachytene karyotypc for Mell1Jl1jJsora /ini. Phytopathol­ tion much better. Recent progress in the molecu­ ogy 82:1212-1218 lar biology of the host-parasite interaction will Boehm EWA. McLaughlin DJ (1989) Phylogeny and ultra­ structure in Eocronortiof/1 nlllscicola: meiosis and ba­ give us a new handle to modify host genes in a sidial development. Mycologia 81:98-114 more efficient way. The goal should be to explain Boehm EWA. McLaughlin DJ (1991) An ultrastructural the action of avirulence genes of the rusts and, karyotype for the fungus Eocronortiltnl /ll11scicolo using consequently, the action of resistance genes in the epifluarescence preselection of pachytene nuclei. Can J Bot 69:1309-1320 host. Thus, breeding for resistance may become Boehm EWA, Wenstroll1 lC, McLaughlin DJ. Szabo LJ. more efficient. Roelfs AP. Bushnell WR (1992) An ultrastructural 90

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