Heteroecious Rust Fungus Research Articles

New species, names, and type designation of rust fungi from New Zealand

ABSTRACT Rust fungi are obligate plant pathogens, usually restricted to a single host species or genus, although some species such as myrtle rust (Austropuccinia psidii) and some cereal and grass rusts (Puccinia spp.) can infect many members of the families Myrtaceae and Poaceae, respectively. The rust life cycle can involve up to five spore stages, both sexual and asexual. The cycle may be completed on a single host (autoecious rust) or require two, unrelated host plants (heteroecious rust) for completion. About 300 rust species are known in New Zealand, with approximately half comprising native rusts (usually pathogenic on native plants) and half being introduced rusts (usually pathogenic on exotic plants). In this paper, 26 new species of rust fungi discovered in New Zealand are described, comprising one species each of Aecidium and Milesina, two of Pucciniastrum, four of Uromyces and 18 of Puccinia. Puccinia ferocis-forsteri is a new heteroecious species producing uredinia and telia on the endemic Carex forsteri and aecia on endemic Urtica ferox. This is only the third native heteroecious rust fungus reported in New Zealand. In addition, two species are transferred to the genus Milesina, three to Uromyces and seven to Puccinia (including a nom. nov.), either following discovery of the sexual (telial) stage of these rusts or considering the most appropriate sexual genus. A new combination is proposed for Coleosporium based on morphology of its urediniospores and molecular data. Epitypes are designated for eight species, lectotypes are selected for five species and a neotype is designated. Apart from one new species on the introduced Fuchsia magellanica all the rusts are considered native to New Zealand. Where appropriate, DNA was extracted and the 28S region (nuclear large subunit ribosomal DNA [nuLSU]) was amplified with the resulting LSU sequences aligned with sequences from GenBank representing most of the major clades.

Light and scanning electron microscopy of aecia and aeciospores of Cronartium ribicola on Pinus koraiensis branch tissues

Morphological characteristics of aecia and aeciospores of Cronartium ribicola on Pinus koraiensis branch tissues were investigated using light and field emission scanning electron microscopy (FESEM). Mature P. koraiensis trees in Jeongseon, Korea, showed yellowish aecia on stems and branches. Aecia and surrounding tissues were excised from the lesions and vapor-fixed for FESEM imaging, which revealed morphology including intact blister-shaped, flattened, and burst forms. Light microscopy revealed yellowish aeciospores having surface projections. Aeciospores were mostly ovoid and measured approximately 20 µm long. The FESEM showed irregularly shaped cracks on the aecia that had erupted through the bark of P. koraiensis. Some aeciospores had germinated, producing two germ tubes from a spore in a burst aecium. Aeciospores had both smooth and verrucose regions on the surface, and some had concave or convex regions. Aeciospore layers and underlying fungal matrices including aecial columns were obvious in the cross-sections of aecia. Approximately 1 µm-high wart-like surface projections could be resolved and comprised less than 10 angular platelets stacked in vertical rows. Remains of the primary spore wall were present between surface projections. These results provide insights into the morphology of the heteroecious rust fungus with the help of vapor fixation and high-resolution surface imaging.

Gymnosporangium sabinae development cycle—Peculiarities and influencing factors

AbstractGymnosporangium sabinae (Dicks.) G. Winter, the causal agent of European pear rust, is a heteroecious rust fungus with a demicyclic life cycle—it produces teliospores and basidiospores on junipers, spermatia and aeciospores on pears. Environmental factors and agrotechnical methods influence the progress and duration of each stage, which is why the specifics and mechanisms of each stage of development are to be studied to predict the spread of the disease and its potential severity. A wide‐range study of European pear rust in Latvia started in 2008—the impact of agroecological factors on the biology of G. sabinae was studied. It was concluded that pears' infection depends on basidiospores' development and release, which is mainly influenced by favourable meteorological conditions—precipitation of at least 10 mm and an average air temperature not below 10°C. The pathogen develops on shoots in the same way as on leaves. However, the development on shoots is slower overall, and the pathogen cannot overwinter there.

Grasses are able to harbor the oversummering of urediospores and the overwintering of teliospores of Puccinia striiformis f. sp. tritici in China

Puccinia striiformis f. sp. tritici (Pst), the cause of wheat stripe rust, is a biotrophic and heteroecious rust fungus with five spore types. Cool and humid climatic conditions are conducive for the development of wheat stripe rust, and in turn, temperatures above 22 °C limit or even cease the disease. The survival of Pst during summer after wheat harvest is responsible for the infection on autumn-sown wheat to maintain disease cycle all the year round. Teliospores formed at late stage of wheat growth are essential for initiating sexual reproduction in spring. Although Chinese native grasses have been experimentally testified as susceptible hosts for Pst and teliospores produced on wheat have been shown to be potential inoculum sources causing infection on alternate hosts (mainly Berberis) in spring, the roles of grass hosts in harboring the survival of urediospores and teliospores of Pst and promoting the emergence of diverse races under field conditions in China have not been known. Herein, Gansu, as a hotspot and an important oversummering region for Pst, was exemplified to demonstrate these roles of grass hosts. As a result, 63 Pst isolates, derived from 2184 uredial samples collected from grass hosts during harvesting period (from mid-June to mid-to-late July) and seeding period (mid to late September) in 2012 and 2013, were identified as 52 diverse phenotypes (82.5%) on the Chinese differential hosts. Subsequently, after inoculation of barberry, 52 Pst isolates with high infection type, 20 known races and 32 new races, were recovered from 1,712 single aecium, which are derived from 35 telial samples of grass hosts. Our experiments showed that Pst urediospores can oversummer on grass species in Gansu or other oversummering regions with similar ecological and climatic conditions. Pst teliospores, which are produced on these grass hosts, are important inoculum source for barberry infection in spring. Therefore, treatment of grasses hosts should be taken into consideration in management of wheat stripe rust.

Host Adaptation and Virulence in Heteroecious Rust Fungi.

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.

Distinct Transcriptomic Reprogramming in the Wheat Stripe Rust Fungus During the Initial Infection of Wheat and Barberry.

Puccinia striiformis f. sp. tritici is the causal agent of wheat stripe rust that causes severe yield losses all over the world. As a macrocyclic heteroecious rust fungus, it is able to infect two unrelated host plants, wheat and barberry. Its urediniospores infect wheat and cause disease epidemic, while its basidiospores parasitize barberry to fulfill the sexual reproduction. This complex life cycle poses interesting questions on the different mechanisms of pathogenesis underlying the infection of the two different hosts. In the present study, transcriptomes of P. striiformis f. sp. tritici during the initial infection of wheat and barberry leaves were qualitatively and quantitatively compared. As a result, 142 wheat-specifically expressed genes (WEGs) were identified, which was far less than the 2,677 barberry-specifically expressed genes (BEGs). A larger proportion of evolutionarily conserved genes were observed in BEGs than that in WEGs, implying a longer history of the interaction between P. striiformis f. sp. tritici and barberry. Additionally, P. striiformis f. sp. tritici differentially expressed genes (DEGs) between wheat at 1 and 2 days postinoculation (dpi) and barberry at 3 and 4 dpi were identified by quantitative analysis. Gene Ontology analysis of these DEGs and expression patterns of P. striiformis f. sp. tritici pathogenic genes, including those encoding candidate secreted effectors, cell wall-degrading enzymes, and nutrient transporters, demonstrated that urediniospores and basidiospores exploited distinct strategies to overcome host defense systems. These results represent the first analysis of the P. striiformis f. sp. tritici transcriptome in barberry and contribute to a better understanding of the evolutionary processes and strategies of different types of rust spores during the infection process on different hosts.[Formula: see text] Copyright © 2021 The Author(s). This is an open access article distributed under the CC BY-NC-ND 4.0 International license.

Three formae speciales of Puccinia striiformis were identified as heteroecious rusts based on completion of sexual cycle on Berberis spp. under artificial inoculation

Puccinia striiformis Westend. is an obligate biotrophic parasite that could infect wheat and grasses to cause stripe rusts. P. striiformis, a species of rust fungi, is divided into several formae speciales based on host specialization, including P. striiformis f. sp. tritici, P. striiformis f. sp. hordei, P. striiformis f. sp. elymi, P. striiformis f. sp. agropyri, and P. striiformis f. sp. secalis. Among the five forms of P. striiformis, sexual stage was confirmed only for the wheat form of the rust, P. striiformis f. sp. tritici, but not known for the rest four forms. In the present study, we investigated the host specialization of three forms of P. striiformis including P. striiformis f. sp. agropyri, P. striiformis f. sp. elymi, and P. striiformis f. sp. hordei, compared the morphology of their urediniospores and teliospores, and analyzed the molecular phylogenic tree of the three forms of P. striiformis and other related species in the genus Puccinia. Each of the three forms was able to infect barberry to complete pycnial and aecial stages under artificial inoculation. Further inoculations of grass, barley cv. Guoluo and wheat cv. Mingxian 169, highly susceptible to P. striiformis f. sp. tritici, using the resultant aeciospores showed that the aeciospores could successfully infect their respective hosts and produce uredinia with high infection types, with the exception on wheat cv. Mingxian 169 where only necrosis was observed. The results suggested that Berberis spp. were alternate hosts for the three formae speciales of P. striiformis, and confirmed that the three rusts were macrocyclic and heteroecious rust fungi completing the whole life cycle on primary hosts and alternate hosts. Our study provides a basis for studying pathogenic variation of the rust fungi through sexual hybridization between formae speciales of P. striiformis.

異種寄生性さび病菌Puccinia moliniae のヌマガヤからリンドウへの伝搬

異種寄生性さび病菌Puccinia moliniae のヌマガヤからリンドウへの伝搬

The Rust Fungus Melampsora larici-populina Expresses a Conserved Genetic Program and Distinct Sets of Secreted Protein Genes During Infection of Its Two Host Plants, Larch and Poplar.

Mechanisms required for broad-spectrum or specific host colonization of plant parasites are poorly understood. As a perfect illustration, heteroecious rust fungi require two alternate host plants to complete their life cycles. Melampsora larici-populina infects two taxonomically unrelated plants, larch, on which sexual reproduction is achieved, and poplar, on which clonal multiplication occurs, leading to severe epidemics in plantations. We applied deep RNA sequencing to three key developmental stages of M. larici-populina infection on larch: basidia, pycnia, and aecia, and we performed comparative transcriptomics of infection on poplar and larch hosts, using available expression data. Secreted protein was the only significantly overrepresented category among differentially expressed M. larici-populina genes between the basidial, the pycnial, and the aecial stages, highlighting their probable involvement in the infection process. Comparison of fungal transcriptomes in larch and poplar revealed a majority of rust genes were commonly expressed on the two hosts and a fraction exhibited host-specific expression. More particularly, gene families encoding small secreted proteins presented striking expression profiles that highlight probable candidate effectors specialized on each host. Our results bring valuable new information about the biological cycle of rust fungi and identify genes that may contribute to host specificity.

The intriguing and convoluted life of a heteroecious rust fungus in New Zealand

Molecular phylogenetic analyses of New Zealand rust fungi suggested that four taxa, Aecidium otagense on Clematis spp., Puccinia tiritea on Muehlenbeckia spp., Puccinia rhei‐undulati sensu auct. NZ, non (Dietel) Hirats. f. on Rheum ×rhabarbarum, and an unidentified Puccinia species on Rumex sagittatus, are a single species. Morphological studies and multilocus molecular data, together with inoculation studies, confirmed this finding. This species is only the third heteroecious rust fungus known to be native to New Zealand.

Melampsora allii‐fragilis f. sp. galanthi‐fragilis reported for first time to cause rust on Galanthus plicatus in Latvia

In Europe, Melampsora allii-fragilis f. sp. galanthi-fragilis (syn. Melampsora galanthi-fragilis) has been reported on leaves of snowdrop (Galanthus nivalis) in Romania (Savulescu, 1953; Bagyanarayana, 2005) and on Galanthus plicatus in Ukraine (Gutsevich, 1952). The GBIF Database has additional records of this fungus on G. nivalis from Austria, Czech Republic and France but the USDA SMML Specimens Database has also records from Hungary and Poland. According to this database, the established distribution area of M. allii-fragilis f. sp. galanthi-fragilis is ‘Central Europe’. Melampsora allii-fragilis f. sp. galanthi-fragilis belongs to the heteroecious rust fungi that require two hosts to complete their life cycles, and includes five spore stages. The telial hosts are willows Salix fragilis, S. fragilis · pentandra and S. pentandra but the aecial host is Galanthus (Saccardo et al., 1925; Bagyanarayana, 2005). Melampsora allii-fragilis f. sp. galanthi-fragilis is a newly recognized forma specialis that resembles M. allii-fragilis morphologically but differs in having Galanthus as its aecial host (Bagyanarayana, 2005). In May 2009, snowdrops (G. plicatus) showing symptoms of rust were found in the Botanical Garden of University of Latvia in Riga, Latvia. A specimen of infected snowdrop leaves (F.1. 8616) was deposited in the herbarium of the Faculty of Biology University of Latvia (RIG). Symptoms were small orange pustules (aecia) of about 0AE7–1AE7 mm in diameter on the undersides of leaves. Tiny yellow aecia of about 1AE0–1AE5 mm in diameter appeared concurrently on the upper sides of leaves. The aecial state of this rust under light microscopy had the morphology of M. allii-fragilis f. sp. galanthi-fragilis (Saccardo et al., 1925; Bagyanarayana, 2005): aecia hypophyllous, yellow or orange, aeciospores globose or ellipsoid, 17AE4–24AE6 · 14AE5–21AE7 lm in size. This is the first report of Melampsora allii-fragilis f. sp. galanthi-fragilis causing rust on Galanthus plicatus in Latvia.

William Pollock Fraser (1867-1943) : Canadian pioneer plant pathologist-mycologist

William P. Fraser, the first Canadian-born plant pathologist-mycologist to be internationally recognized as such, began as an amateur collector of fungi, with emphasis on the plant rusts, while teaching school in his home province, Nova Scotia. He then became a widely acclaimed authority on the rusts and a professional plant pathologist-mycologist. He taught plant pathology and mycology, first at McGill University and then, after an interval as head of the first plant pathology laboratory in Western Canada, at the University of Saskatchewan. Fraser was a Canadian pioneer in research on physiological races of wheat rust; in the culture of heteroecious rust fungi, in forest pathology, and in the study of root and smut diseases of grasses in Western Canada.

Stem rust of small grains and grasses caused by Puccinia graminis

SUMMARY Stem rust has been a serious disease of wheat, barley, oat and rye, as well as various important grasses including timothy, tall fescue and perennial ryegrass. The stem rust fungus, Puccinia graminis, is functionally an obligate biotroph. Although the fungus can be cultured with difficulty on artificial media, cultures grow slowly and upon subculturing they develop abnormal ploidy levels and lose their ability to infect host plants [Bushnell and Bosacker (1982) Can. J. Bot. 60, 1827-1836]. P. graminis is a typical heteroecious rust fungus with the full complement of five distinct spore stages that occur during asexual reproduction on its gramineous hosts and sexual reproduction that begins in the resting spore stage and culminates on the alternate host, barberry (Berberis spp.). There appears to be little polymorphism for resistance/susceptibility in Berberis species, but complex polymorphisms of resistance/susceptibility and matching virulence/avirulence exist in gene-for-gene relationships between small grain species and the forms of P. graminis that infect them. Puccinia graminis is a rust fungus in the phylum Basidiomycota, class Urediniomycetes, order Uredinales, and family Pucciniaceae, which contains 17 genera and approximately 4121 species, of which the majority are in the genus Puccinia[Kirk et al. (2001) Ainsworth and Bisby's Dictionary of the Fungi. Wallingford, UK: CAB International]. Various subdivisions of P. graminis into subspecies, varieties and formae speciales have been proposed based on spore size and host range. Crossing studies and DNA sequence comparisons support the separation of at least two subspecies, but not the proposed separation based on spore size. The host range of P. graminis is very broad compared with that of most Puccinia spp.; it includes at least 365 species of cereals and grasses in 54 genera [Anikster (1984) The Cereal Rusts. Orlando, FL: Academic Press, pp. 115-130]. Wheat stem rust, P. graminis f. sp. tritici, was shown to infect 74 species in 34 genera in artificial inoculations of seedlings, but only 28 of those species belonging to eight genera were known to be natural hosts of the fungus. Other formae speciales of P. graminis have narrower host ranges than P. graminis f. sp. tritici. Disease symptoms: Infections in cereals or grasses occur mainly on stems and leaf sheaths, but occasionally they may be found on leaf blades and glumes as well. The first macroscopic symptom is usually a small chlorotic fleck, which appears a few days after infection. About 8-10 days after infection, a pustule several millimetres long and a few millimetres wide is formed by rupture of the host epidermis from pressure of a mass of brick-red urediniospores produced in the infection. These uredinial pustules are generally linear or diamond shaped and may enlarge up to 10 mm long. The powdery masses of urediniospores appear similar to rust spots on a weathered iron surface. With age, the infection ceases production of brick-red urediniospores and produces a layer of black teliospores in their place, causing the stems of heavily infected plants to appear blackened late in the season.

Fine structure of quiescent and germinating aeciospores of Cronartium fusiforme.

Aeciospores of the long-cycle heteroecious rust fungus, Cronartium fusiforme, were found to have an extremely thick cell wall with striking spicules protruding from it. The wall was readily degraded by commercial chitinase, but spicules were unaffected. Quiescent spores contained two nuclei with distinct nuclear membranes possessing many pores. Numerous membrane-bounded lipid bodies were found both in wild-type orange and in white mutant aeciospores. An abundance of irregularly ovoid mitochondria was present in quiescent spores. After glutaraldehydeosmium fixation, the surface of the mitochondria appeared to be covered with ribosomes or microtubules in a paracrystalline array, whereas after permanganate fixation only smooth outer mitochondrial membranes were noted. The latter fixative revealed abundant vesicular endoplasmic reticulum in the spore. Spores incubated at 20 C on agar produced one to five distinct germ tubes within 65 to 180 min. These thin-walled tubes exhibited varying degrees of branching, and reached a total hyphal length of 300 to 500 mu prior to rupturing. Emergence of germ tubes took place through a pore in the spore wall and appeared to be mainly a physical flowing of cytoplasm from the spore into the germ tube without division of nuclei or other cell organelles. On completion of germination, the protoplasm of the germ tube contained both nuclei and nearly all of the other spore contents. Mitochondria had smooth outer membranes, were greatly elongated, and possessed distinct longitudinal cristae. A limited amount of rough endoplasmic reticulum was arranged parallel to the germ tube wall. Other organelles seen in germ tubes were lipid bodies, concentric membrane figures, and numerous ribosomes. Lipid bodies appeared smaller and fewer in number than in quiescent spores.