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1. Life cycle of Uromyces fabae . Overwintering diploid (2 n ) teliospores ( T ) germinate in the spring with a metabasidium ( M ) from which four haploid ( n ) basidiospores ( B ) of two mating types (+, −) are formed. Haploid pycniospores ( P ) are exchanged between pycnia of different mating types on the upper surface of a leaf. After spermatization dikaryo-
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Fungi belonging to the order Uredinales are commonly referred to as rust fungi. All members of the Uredinales are parasitic on plants, often causing dramatic losses in various important crop plants (Alexopoulos et al. 1996). Together with the powdery mildew fungi and the downy mildew-causing oomycetes, rust fungi form an extremely successful group...
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... A third distinctive characteristic for members of the Urediniomycetes is the formation of transversely septated metabasidia from which basidiospores are formed laterally (Gäumann 1959). Today the Uredinales are thought to comprise more than 100 genera and around 7000 species (Maier et al. 2003). These numbers correspond to about 75% of the genera and even 95% of the species of the class Urediniomycetes . Based on recent data the order Uredinales can be considered to be monophyletic (Swann et al. 1981). The order is divided into 13 families, each consisting of between three and 30 genera (Cummins and Hiratsuka 2003). Classic taxonomic classification is mainly based on spore and fruiting structure morphology, with a strong emphasis on teliospores morphology (usually two-celled for Puccinia , one- celled for Uromyces species; Cummins and Hiratsuka 2003). Some of these classifications, however, are controversial because the morphology of different spore types may leave some ambiguity with respect to final classification. Rust fungi and their host plants are excellent examples of coevolution. Rusts infecting members of such old plant divisions as ferns or conifers are almost exclusively heteroecious and macrocyclic (see Sect. IV). Since the order Uredinales seems to be monophyletic (Swann et al. 1981), it can be inferred that the extraordinarily complex heteroecious macrocyclic life cycle evolved only once. Reductions seem to have occurred at many different stages of evolution (Laundon 1973). Wahl et al. (1984) discussed host–parasite coevolution for cereal rusts. In centers of coevolution, genes responsible for plant defense and genes for fungal virulence have accumulated. Redistribution of a host subsequently gave rise to independent evolution (Anikster 1984). This diversification may at least in part be responsible for some of the com- plications associated with rust taxonomy. It would therefore be highly desirable to scrutinize the classic taxonomical system based on morphological and physiological characters and amend/correct it using more DNA sequence data as they become available, in order to better define the phylogeny and taxonomy of rust fungi (Aime 2006). Most rusts can attack more than one host. P. graminis for example can infect at least 365 species of cereals and grasses (Anikster 1984). Such rust species are sometimes subdivided into more specialized categories, each designated a forma specialis (f. sp.; variety, specialized form). There are virtually no distinctive morphological characteristics for the formae speciales , and they are identified by determination of the host species. This type of specialization was first described in the 1890s by Eriksson and Henning, working on cereal rusts (Eriksson 1894; Eriksson and Henning 1896). P. graminis f. sp. tritici for example exhibits a host preference for wheat and barley, while P. graminis f. sp. avenae shows a preference for oat. Within rust species or formae speciales , a further specialization is commonly observed. It is known that certain genotypes of a pathogen are able to attack only certain host cultivars. Such races of the pathogen are typically assigned a number in the order of their identification. The race concept is tightly linked to the virulence/avirulence pattern of rust fungi and the susceptibility/resistance pattern of their respective host plants according to the gene for gene hypothesis introduced by Flor (1955). It was shown that broadly virulent pathogens occur more frequently in highly resistant host populations, whereas avirulent pathogens dominate susceptible populations (Thrall and Burdon 2003). The non-random spatial distribution maintained despite high pathogen mobility implies that selection favors virulent races in resistant hosts and avirulent races in susceptible hosts. Physiological races were first described by Stakman and Piemeisal (1917), who established a first set of wheat cultivar differentials which allowed the identification of different P. graminis f. sp. tritici races. Now extended and refined, this system still provides the basis for modern plant breeding (Kolmer 1996). Rusts have one of the most complex life cycles of all fungi (Littlefield 1981). In its complete form the cycle includes five different spore forms. The already complex cycle also exhibits a high degree of plasticity, generating many different variations (see below). To make things even more complicated, there is also some ambiguity in the literature about the designation of the different spore types and fruiting structures (sori). Table 4.1 provides an overview of the terminology used for the different spore types and fruiting structures, with the most commonly used terms printed in bold. In addition to the morphological classification system, Table 4.1 also lists the Roman numerals assigned to the different developmental stages used in the ontogenic classification system (Littlefield 1981; Alexopoulos et al. 1996; Webster and Weber 2007). Figure 4.1 depicts the life cycle of U. fabae and also indicates the nuclear condition during the different stages. After overwintering on residual plant material, diploid teliospores germinate in the spring with a metabasidium. After meiosis, the latter produces four haploid basidiospores with two different mating types. These are ejected from the metabasidium by the aid of a drop of liquid (Buller’s drop; Webster et al. 1995), and after landing on the leaf surface of a host plant, they germinate and produce monokaryotic infection structures. Pycnia are produced on the upper surface of the leaf, which contain pycniospores and receptive hyphae. Pycniospores are exchanged between pycnia of different mating types (heterothallism), and after spermatization, dikaryotization occurs in aecial primordia. An aecium differentiates at the lower side of the leaf and dikaryotic aeciospores are produced. After landing on a leaf surface, these aeciospores germinate and form infection structures from which uredia which produce urediospores are formed. Urediospores are the major asexual spore form of rust fungi produced in massive amounts through repeated infection of host plants during the summer. In the fall, uredia differentiate into telia, the nuclei fuse during sporogenesis and single-celled, diploid teliospores develop for the winter, which closes the rust infection cycle. Rusts capable of completing their entire life cycle on a single host species are called autoecious (de Bary 1865). Examples for such species are U. fabae on broad bean and M. lini on flax. Rust fungi requiring two host species in order to complete their life cycle are termed heteroecious (de Bary 1865). The two host species are typically well separated taxonomically. The classic example for an heteroecious rust is P. graminis which switches between cereals as main host and barberry as alternate host (Arthur 1962). Host alteration takes place after the aecial and telial stages. P. graminis occurs as pycnia and aecia on barberry and as uredia and telia on cereals. However, the term alternate host is used to denote either the pycnial/aecial host or the uredia/telia host and is usually applied to the host of lesser economic importance. Not all rust fungi go through all five known spore forms. Rusts exhibiting all five spore forms are called macrocyclic. In so-called demicyclic rusts, the uredia stage (and sometimes the pycnial stage) is missing, and in microcyclic rust fungi usually only the pycnial and the telial stage are present (sometimes even only the telial stage). Since the aecial stage is missing in the latter case, all microcyclic rusts are necessarily autoecious. Macrocyclic and demicyclic rusts may be either autoecious or heteroecious. A more extensive description of the many variations of this topic can be found in the review by Petersen (1974) and the book by Cummins and Hiratsuka (2003). The different spore forms of rust fungi have different modes of dispersal. Pycniospores are released from their supporting cells into a viscous liquid and locally allocated by insects, splashing water, and contact among host plant organs (Littlefield 1981). Aeciospores are produced in tightly packed chains, released by the dissolution of intercalary cells, and aerially disseminated (Littlefield and Heath 1979). Teliospores may remain attached to the host organ they were produced on (Littlefield 1981). Alternatively, the pedicels on which teliospores are produced may break, and teliospores and attached pedicels are dispersed by the wind (Littlefield 1981). In any case, teliospores germinate to produce basidiospores, which are forcefully ejected from the metabasidium (involving Buller’s drop; Webster et al. 1995) and then aerially dispersed (Littlefield 1981). Basidiospores are only suited for local dispersal since they desiccate rapidly. Urediospores are the most important asexual spore form of most rust fungi. They are produced in enormous numbers through repeated infection of host plants for short- and long-range distribution during the vegetation period. Rust fungi are therefore typical “ r -strategists” (Deising et al. 2002). For P. graminis f. sp. tritici for example, it was determined that a single uredium can produce about 600 urediospores day −1 (Eversmeyer and Kramer 2000). Even moderate infection can thus easily result in the production of 10 12 –10 13 urediospores day −1 ha −1 (Deising et al. 2002). While it is generally accepted that the spores are dry-dispersed by wind (Littlefield 1981) or carried by vectors (Wandeler and Bacher 2006), rain also seems to have a dramatic effect at least for local dissemination (Geagea et al. 1999). Spores can also be carried over distances of several hundreds or even thousands of kilometers by winds causing dissemination across or even between continents (Nagarajan and Singh 1990; Eversmeyer and Kramer 2000; Brown and Hovmøller 2002; Kolmer 2005). Annual long-distance transport of P. graminis occurs across ...
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Puccinia substriata EII. & Barth. var. insolita (P. Syd. & H. Syd.) Ramachar & Cumm., Puccinia coronata Corda var. gibberosa (Lagerh.) Joerst., Puccinia coronata Corda var. avenae Fraser & Ledingham and Uromyces vossiae Barclay are described and illustrated. These taxa are new records from Pakistan.
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... A decrease in biomass was also reported in greenhouse studies using the Indian strain of Pkg by Currie et al. (2020) and occurs as infection by Pkg progresses. Sporulation of the rust, as recorded for many foliar pathogens, results in modifications to chlorophyll and photosynthetic activity, acting as a carbon sink by drawing key nutrients and water away from the plant and/or altering plant-gene expression (Voegele et al., 2009); as a consequent reproductive output is also compromised (Gilbert, 2002). Here, we also found Hb infected by Pkg to produce fewer flowers and seeds. ...
Himalayan balsam (Impatiens glandulifera) is one of the most prolific non-native species in Europe. Since 2014, the highly-specific rust fungus, Puccinia komarovii var. glanduliferae, has been released into Great Britain as a classical biological control agent for this invasive weed. Prior to its release, research focused on ensuring the safety of the pathogen; elucidating its life cycle and verifying its host-specificity. However, limited studies were conducted to determine the likely impact of the rust on its host. Due to difficulties in assessing field populations, unforeseen complexities in the plant-pathogen relationship and the requirement for long-term monitoring, inoculation experiments were conducted to evaluate the effect of the rust on both seedlings and mature plants of Himalayan balsam under semi-natural conditions. The impact of the rust was determined through measuring plant-growth parameters in addition to assessing reproductive output. The rust significantly increased seedling mortality, with up to 80% of seedlings dying as a result of rust infection, or indirectly through the colonisation of secondary pathogens. Mature plants infected with the rust produced fewer leaves with a decrease in total plant biomass. Reproductive output was negatively affected through a reduction in both flower and seed production, but with no observed effects on seed viability. This study demonstrates the high potential of the rust for controlling fully susceptible field populations of Himalayan balsam.
... Rust fungi are obligate biotrophic pathogens dependent on living host tissue for propagation (Voegele et al., 2009). The haustorium is a hallmark structure of rusts and other biotrophic fungi through which they interact with host cells (Voegele and Mendgen, 2003). ...
Haustoria of biotrophic rust fungi are responsible for the uptake of nutrients from their hosts and for the production of secreted proteins, known as effectors, which modulate the host immune system. The identification of the transcriptome of haustoria and an understanding of the functions of expressed genes therefore hold essential keys for the elucidation of fungus-plant interactions and the development of novel fungal control strategies. Here, we purified haustoria from infected leaves and used 454 sequencing to examine the haustorial transcriptomes of Phakopsora pachyrhizi and Uromyces appendiculatus, the causal agents of soybean rust and common bean rust, respectively. These pathogens cause extensive yield losses in their respective legume crop hosts. A series of analyses were used to annotate expressed sequences, including transposable elements and viruses, to predict secreted proteins from the assembled sequences and to identify families of candidate effectors. This work provides a foundation for the comparative analysis of haustorial gene expression with further insights into physiology and effector evolution.
... Like most rust fungi, M. larici-populina urediniospore germination results in a germ tube that differentiates into a series of infection structures in the intercellular space (Rinaldi et al. 2007). The haustorium invaginates host cells and makes near-direct contact with the host plasma membrane where it plays a crucial role in nutrient acquisition (Voegele et al. 2009). This structure is also the core of cellular communication involved in the redirection of host metabolism and the suppression of host defenses (Voegele et al. 2009), which allows the pathogen to deliver a suite of effector proteins to modulate plant innate immunity and enable parasitic colonization (Dodds et al. 2009). ...
... The haustorium invaginates host cells and makes near-direct contact with the host plasma membrane where it plays a crucial role in nutrient acquisition (Voegele et al. 2009). This structure is also the core of cellular communication involved in the redirection of host metabolism and the suppression of host defenses (Voegele et al. 2009), which allows the pathogen to deliver a suite of effector proteins to modulate plant innate immunity and enable parasitic colonization (Dodds et al. 2009). With the advent of genomics and bioinformatics, the identification of putative effectors was facilitated by tracking secreted proteins exported through the eukaryotic general secretory pathway via N-terminal amino acid sequences known as signal peptides (Torto et al. 2003). ...
... SSP expression during urediniospore germination or at early stages of infection (i.e., 24–48 hpi) supports an early manipulation of the plant defense system by the fungus in order to promote virulence (Figure 3). In contrast, transcripts encoding proteases and transporters were preferentially induced at 96 hpi when the fungus has already formed many haustoria in host cells, supporting the uptake of host resources and nutrients by the fungal structures as previously reported for the bean rust fungus U. fabae (see [53] for a complete review). At later stages of infection, the induction of transcripts encoding various lipases and carbohydrate active enzymes (CAZymes) was observed concomitantly with uredinia formation (96–168 hpi) reflecting a potential switch in lipid metabolism during the sporulation process [52] (Figure 3). ...
... However, specific in planta gene expression in other cell types (i.e., infection hyphae, sporogenous hyphae) was not assessed so far in rust fungi. Isolation of biotrophic infection hyphae from Colletotrichum higginsianum was successfully applied to Arabidopsis infected leaves for transcriptome analysis [58], and rust infection hyphae and derived infection structures were obtained artificially for the bean rust fungus U. fabae (see [53] for details). The use of laser capture microdissection (LCM) was a major breakthrough to dissect the genetic programs related to biotrophy and sporulation at a late stage of rust infection (168 hpi), whereas various fungal structures are formed in planta [9]. ...
... The purification of haustoria from rust-infected bean leaves has paved the way for the molecular analysis of these fungal cell types that play a key role in the establishment of obligate biotrophy. Such an approach has allowed the sequencing of haustoria-specific cDNA and the identification of genes expressed in these infection structures [53–56]. This approach was successfully used to identify several candidate effectors in haustorially expressed secreted proteins (HESPs) of the model rust fungus M. lini [57], including several avirulence genes. ...
Poplars are extensively cultivated worldwide, and their susceptibility to the leaf rust fungus Melampsora larici-populina leads to considerable damages in plantations. Despite a good knowledge of the poplar rust life cycle, and particularly the epidemics on poplar, the perennial status of the plant host and the obligate biotrophic lifestyle of the rust fungus are bottlenecks for molecular investigations. Following the completion of both M. larici-populina and Populus trichocarpa genome sequences, gene families involved in poplar resistance or in rust fungus virulence were investigated, allowing the identification of key genetic determinants likely controlling the outcome of the interaction. Specific expansions of resistance and defense-related genes in poplar indicate probable innovations in perennial species in relation with host-pathogen interactions. The genome of M. Larici-populina contains a strikingly high number of genes encoding small secreted proteins (SSPs) representing hundreds of candidate effectors. Transcriptome analyses of interacting partners in compatible and incompatible interactions revealed conserved set of genes involved in poplar defense reactions as well as timely regulated expression of SSP transcripts during host tissues colonisation. Ongoing functional studies of selected candidate effectors will be achieved mainly on the basis of recombinant protein purification and subsequent characterisation.
... Like most rust fungi, M. larici-populina urediniospore germination results in a germ tube that differentiates into a series of infection structures in the intercellular space (Rinaldi et al. 2007). The haustorium invaginates host cells and makes near-direct contact with the host plasma membrane where it plays a crucial role in nutrient acquisition (Voegele et al. 2009). This structure is also the core of cellular communication involved in the redirection of host metabolism and the suppression of host defenses (Voegele et al. 2009), which allows the pathogen to deliver a suite of effector proteins to modulate plant innate immunity and enable parasitic colonization (Dodds et al. 2009). ...
... The haustorium invaginates host cells and makes near-direct contact with the host plasma membrane where it plays a crucial role in nutrient acquisition (Voegele et al. 2009). This structure is also the core of cellular communication involved in the redirection of host metabolism and the suppression of host defenses (Voegele et al. 2009), which allows the pathogen to deliver a suite of effector proteins to modulate plant innate immunity and enable parasitic colonization (Dodds et al. 2009). With the advent of genomics and bioinformatics, the identification of putative effectors was facilitated by tracking secreted proteins exported through the eukaryotic general secretory pathway via N-terminal amino acid sequences known as signal peptides (Torto et al. 2003). ...
Cereal production plays a major role in both animal and human diets throughout the world. However, cereal crops are vulnerable to attacks by fungal pathogens on the foliage, disrupting their biological cycle and photosynthesis, which can reduce yields by 15-20% or even 60%. Consumers are concerned about the excessive use of synthetic pesticides given their harmful effects on human health and the environment. As a result, the search for alternative solutions to protect crops has attracted the interest of scientists around the world. Among these solutions, biological control using beneficial microorganisms has taken on considerable importance, and several biological control agents (BCAs) have been studied, including species belonging to the genera Bacillus, Pseudomonas, Streptomyces, Trichoderma, Cladosporium, and Epicoccum, most of which include plants of growth-promoting rhizobac-teria (PGPRs). Bacillus has proved to be a broad-spectrum agent against these leaf cereal diseases. Interaction between plant and beneficial agents occurs as direct mycoparasitism or hyperparasitism by a mixed pathway via the secretion of lytic enzymes, growth enzymes, and antibiotics, or by an indirect interaction involving competition for nutrients or space and the induction of host resistance (systemic acquired resistance (SAR) or induced systemic resistance (ISR) pathway). We mainly demonstrate the role of BCAs in the defense against fungal diseases of cereal leaves. To enhance a solution-based crop protection approach, it is also important to understand the mechanism of action of BCAs/molecules/plants. Research in the field of preventing cereal diseases is still ongoing.
Hemileia vastatrix is the most important fungal pathogen of coffee and the causal agent of recurrent disease epidemics that have invaded nearly every coffee-growing region in the world. The development of coffee varieties resistant to H. vastatrix requires fundamental understanding of the biology of the fungus. However, the complete life cycle of H. vastatrix remains unknown and conflicting studies and interpretations exist as to whether the fungus is undergoing sexual reproduction. Here we used population genetics of H. vastatrix to infer the reproductive mode of the fungus across most of its geographic range including Central Africa, SE Asia, the Caribbean, and South and Central America. The population structure of H. vastatrix was determined using eight simple sequence repeat markers (SSRs) developed for this study. The analyses of the standardized index of association, Hardy Weinberg equilibrium, and clonal richness all strongly support asexual reproduction of H. vastatrix in all sampled areas. Similarly, a minimum spanning network tree reinforces the interpretation of clonal reproduction in the sampled H. vastatrix populations. These findings may have profound implications for resistance breeding and management programs against H. vastatrix.
Rust fungi (Pucciniales, Basidiomycota) are obligate biotrophic pathogens that cause rust diseases in plants, inflicting severe damage to agricultural crops. Pucciniales possess the most complex life cycles known in fungi. These include an alternation of generations, the development of up to five different sporulating stages, and, for many species, the requirement of infecting two unrelated host plants during different parts of their life cycle, termed heteroecism. These fungi have been extensively studied in the past century through microscopy and inoculation studies, providing precise descriptions of their infection processes, although the molecular mechanisms underlying their unique biology are poorly understood. In this review, we cover recent genomic and life cycle transcriptomic studies in several heteroecious rust species, which provide insights into the genetic tool kits associated with host adaptation and virulence, opening new avenues for unraveling their unique evolution.
Expected final online publication date for the Annual Review of Phytopathology, Volume 59 is August 2021. Please see http://www.annualreviews.org/page/journal/pubdates for revised estimates.
Flutianil, a fungicide effective only on powdery mildew, was previously reported to affect the host cell's haustorial formation and nutrient absorption. Studies were conducted to investigate flutianil's primary site of action on Blumeria graminis morphology using transmission electron microscope (TEM) observation and RNA sequencing (RAN-seq) techniques. TEM observation revealed that flutianil caused the extra-haustorial matrix and fungal cell wall to be obscured, without remarkable changes of other fungal organelles. RNA-seq analysis indicated that, unlike other powdery-mildew fungicides, flutianil did not significantly affect the constantly expressed genes for the survival of B. graminis. Genes whose expression is up- or downregulated by flutianil were found; these are the three sugar transporter genes and various effector genes, mainly expressed in haustoria. These findings indicate that the primary site of action of flutianil might be in the haustoria.
Among the thousands of rust species described, many are known for their devastating effects on their hosts which include major agriculture crops and trees. Hence, for over a century, these basidiomycete pathogenic fungi have been researched and experimented with. However, due to their biotrophic nature, they are challenging organisms to work with and, needing their hosts for propagation, represent pathosystems that are not easily experimentally accessible. Indeed, efforts to perform genetics have been few and far apart for the rust fungi, though one study performed in the 1940s was famously instrumental in formulating the gene-for-gene hypothesis describing pathogen-host interactions. By taking full advantage of the molecular genetic tools developed in the 1980s, research on many plant pathogenic microbes thrived, yet similar work on the rusts remained very challenging though not without some successes. However, the genomics era brought real breakthrough research for the biotrophic fungi and with innovative experimentation and the use of heterologous systems, molecular genetic analyses over the last two decades have significantly advanced our insight into the function of many rust fungus genes and their role in the interaction with their hosts. This has allowed optimizing efforts for resistance breeding and the design and testing of various novel strategies to reduce the devastating diseases they cause.
