Rust (fungus)

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Rusts
Bruine roest op tarwe (Puccinia recondita f.sp. tritici on Triticum aestivum).jpg
Example of wheat leaf from a disease differential of Puccinia recondita f.sp. tritici
Scientific classification OOjs UI icon edit-ltr.svg
Domain: Eukaryota
Kingdom: Fungi
Division: Basidiomycota
Class: Pucciniomycetes
Order: Pucciniales
Families

Rusts are fungal plant pathogens of the order Pucciniales (previously known as Uredinales) causing plant fungal diseases.

Contents

An estimated 168 rust genera and approximately 7,000 species, more than half of which belong to the genus Puccinia , are currently accepted. [3] Rust fungi are highly specialized plant pathogens with several unique features. Taken as a group, rust fungi are diverse and affect many kinds of plants. However, each species has a range of hosts and cannot be transmitted to non-host plants. In addition, most rust fungi cannot be grown easily in pure culture.

Most species of rust fungi are able to infect two different plant hosts in different stages of its life cycle, and may produce up to five morphologically and cytologically distinct spore-producing structures viz., spermogonia, aecia, uredinia, telia, and basidia in successive stages of reproduction. [4] Each spore type is very host specific, and can typically infect only one kind of plant.

Rust fungi are obligate plant pathogens that only infect living plants. Infections begin when a spore lands on the plant surface, germinates, and invades its host. Infection is limited to plant parts such as leaves, petioles, tender shoots, stem, fruits, etc. [3] Plants with severe rust infection may appear stunted, chlorotic (yellowed), or may display signs of infection such as rust fruiting bodies. Rust fungi grow intracellularly, and make spore-producing fruiting bodies within or, more often, on the surfaces of affected plant parts. [3] Some rust species form perennial systemic infections that may cause plant deformities such as growth retardation, witch's broom, stem canker, galls, or hypertrophy of affected plant parts.

Rusts get their name because they are most commonly observed as deposits of powdery rust-coloured or brown spores on plant surfaces. The Roman agricultural festival Robigalia (April 25) has ancient origins in combating wheat rust. [5]

Impacts

Rusts are among the most harmful pathogens to agriculture, horticulture and forestry. Rust fungi are major concerns and limiting factors for successful cultivation of agricultural and forest crops.[ citation needed ] White pine blister rust, wheat stem rust, soybean rust, and coffee rust are examples of notoriously damaging threats to economically important crops. [3] Climate change may increase the prevalence of some rust species while causing others to decline through increased CO2 and O3, changes to temperature and humidity, and enhanced spore dispersal due to more frequent extreme weather events. [6]

Life cycle

All rusts are obligate parasites, meaning that they require a living host to complete their life cycle. They generally do not kill the host plant but can severely reduce growth and yield. [7] Cereal crops can be devastated in one season; oak trees infected in the main stem within their first five years by the rust Cronartium quercuum often die. [8]

Germinating urediniospore of Puccinia graminis, model from the late 19th century, Botanical Museum Greifswald Modell von Puccinia graminis (Getreiderost) -Osterloh- -Brendel 10 h, 2-.jpg
Germinating urediniospore of Puccinia graminis , model from the late 19th century, Botanical Museum Greifswald

Rust fungi can produce up to five spore types from corresponding fruiting body types during their life cycle, depending on the species. Roman numerals have traditionally been used to refer to these morphological types.

Rust fungi are often categorized by their life cycle. Three basic types of life cycles are recognized based on the number of spore types as macrocyclic , demicyclic, and microcyclic. [3] The macrocyclic life cycle has all spore states, the demicyclic lacks the uredinial state, and the microcyclic cycle lacks the basidial, pycnial, and the aecial states, thus possess only uredinia and telia. Spermagonia may be absent from each type but especially the microcyclic life cycle. In macrocyclic and demicyclic life cycles, the rust may be either host alternating (heteroecious) (i.e., the aecial stage is on one kind of plant but the telial stage on a different and unrelated plant), or single-host (autoecious) (i.e., the aecial and telial states on the same plant host). [3] Heteroecious rust fungi require two unrelated hosts to complete their life cycle, with the primary host being infected by aeciospores and the alternate host being infected by basidiospores. This can be contrasted with an autoecious fungus, such as Puccinia porri , which can complete all parts of its life cycle on a single host species. [9] Understanding the life cycles of rust fungi allows for proper disease management. [11]

Host plant–rust fungus relationship

There are definite patterns of relationship with host plant groups and the rust fungi that parasitize them. Some genera of rust fungi, especially Puccinia and Uromyces , comprise species that are capable of parasitizing plants of many families.[ citation needed ] Other rust genera appear to be restricted to certain plant groups.[ citation needed ] Host restriction may, in heteroecious species, apply to both phases of life cycle or to only one phase. [3] As with many pathogen/host pairs, rusts are often in gene-for-gene relationships with their plants. This rust-plant gene-for-gene interaction differs somewhat from other gene-for-gene situations and has its own quirks and agronomic significance. Rust fungi decrease photosynthesis and elicit the emissions of different stress volatiles with increasing severity of infection. [12]

Infection process

The spores of rust fungi may be dispersed by wind, water or insect vectors. [13] When a spore encounters a susceptible plant, it can germinate and infect plant tissues. A rust spores typically germinates on a plant surface, growing a short hypha called a germ tube. This germ tube may locate a stoma by a touch responsive process known as thigmotropism. This involves orienting to ridges created by epidermal cells on the leaf surface, and growing directionally until it encounters a stoma. [14]

Rust hypha attacking stoma (1600x magnification) Rust attacking stoma.jpg
Rust hypha attacking stoma (1600x magnification)

Over the stoma, a hyphal tip produces an infection structure called an appressorium. From the underside of an appressorium, a slender hypha grows downward to infect plant cells. [15] It is thought that the whole process is mediated by stretch-sensitive calcium ion channels located in the tip of the hypha, which produce electric currents and alter gene expression, inducing appressorium formation. [16]

Once the fungus has invaded the plant, it grows into plant mesophyll cells, producing specialized hyphae known as haustoria. The haustoria penetrate cell walls but not cell membranes: plant cell membranes invaginate around the main haustorial body forming a space known as the extra-haustorial matrix. An iron and phosphorus rich neck band bridges the plant and fungal membranes in the space between the cells for water flow, known as the apoplast, thus preventing the nutrients reaching the plant's cells. The haustorium contains amino acid- and hexose sugar- transporters and H+-ATPases which are used for active transport of nutrients from the plant, nourishing the fungus. [17] The fungus continues growing, penetrating more and more plant cells, until spore growth occurs. The process repeats every 10–14 days, producing numerous spores that can be spread to other parts of the same plant, or to new hosts.

Common rust fungi in agriculture

[9] [11] [18]

Management

Research

Efforts to control rusts began to be scientifically based in the 20th century. [21] Elvin C. Stakman initiated the scientific study of host resistance, which had heretofore been poorly understood and handled by individual growers as part of the breeding process. [21] Stakman was followed by H. H. Flor's extensive discoveries of rust genetics. [21] In order to study rust metabolics, Tervet et al., 1951 developed the Cyclone Separator. [21] The cyclone separator uses the cyclonic separation mechanism to allow the mechanised collection of spores for study – Cherry & Peet 1966's improved version gathers even more efficiently. [21] This device was first put to work testing the composition of the spores themselves, especially substances coating the outside of the spores which signal population density. [21] When detected they help prevent crowding. [21]

Gene cloning and other methods of genetic engineering can provide a much wider range of R genes and other sources of rust resistance – with reduced delay before deployment – if regulation of genetic engineering permits. [22]

Control

The control methods of rust fungus diseases depend largely on the life cycle of the particular pathogen. The following are examples of disease management plans used to control macrocyclic and demicyclic diseases:

Macrocyclic disease: Developing a management plan for this type of disease depends largely on whether the urediniospores (rarely termed the "repeating stage") occur on the economically important host plant or the alternate host.[ citation needed ] For example, the repeating stage in white pine blister rust disease does not occur on white pines but on the alternate host, Ribes spp. During August and September Ribes spp. give rise to teliospores which infect white pines. Removal of the alternate host disrupts the life cycle of the rust fungi Cronartium ribicola , preventing the formation of basidiospores which infect the primary host. Although spores from white pines cannot infect other white pines, survival spores may overwinter on infected pines and reinfect Ribes spp. the following season. Infected tissue is removed from white pines and strict quarantines of Ribes spp. are maintained in high risk areas.[ citation needed ]

Puccinia graminis is a macrocyclic heteroecious fungus that causes wheat stem rust disease.[ citation needed ] The sexual stage in this fungus occurs on the alternate host – barberry – and not wheat. The durable spore type produced on the alternate host allows the disease to persist in wheat even in more inhospitable environments. Planting resistant crops will prevent disease, however, virulence mutations will give rise to new strains of fungi that overcome plant resistance.[ citation needed ] Although the disease cannot be stopped by removal of the alternate host, the life cycle is disrupted and the rate of evolution is decreased because of reduced genetic recombination. This allows resistance bred crops to remain effective for a longer period of time. [9] [23]

Demicyclic disease: Because there is no repeating stage in the life cycle of demicyclic fungi, removal of the primary or the alternate host will disrupt the disease cycle.[ citation needed ] This method, however, is not highly effective in managing all demicyclic diseases. Cedar-apple rust disease, for example, can persist despite removal of one of the hosts since spores can be disseminated from long distances. The severity of cedar-apple rust disease can be managed by removal of basidiospore producing galls from junipers or the application of protective fungicides to junipers. [24]

Home control

Rust diseases are very hard to treat. Fungicides, such as Mancozeb, may help but may never eradicate the disease.[ citation needed ] Some organic preventative solutions are available and sulphur powder is known to stop spore germination. High standards of hygiene, good soil drainage, and careful watering may minimize problems. Any appearance of rust must be immediately dealt with by removing and burning all affected leaves.[ citation needed ] Composting, or leaving infected vegetation on the ground will spread the disease.[ citation needed ]

Commercial control

In some large acreage crops, fungicides are applied by air. The process is expensive and fungicide application is best reserved for seasons when foliar diseases are severe. Research indicates, the higher the foliar disease severity, the greater the return from the use of fungicides. [25] Southern corn rust disease, can be confused with common rust. Southern rust's distinguishing characteristic is that pustules form mostly on the upper leaf surface and spores are more orange in color. Southern rust spreads more quickly and has a higher economic impact when hot, humid weather conditions persist. Timely fungicide applications to control southern rust are more crucial than with common rust. [26]

A variety of preventative methods can be employed for rust diseases:

  • High moisture levels may exacerbate rust disease symptoms. The avoidance of overhead watering at night, using drip irrigation, reducing crop density, and using fans to circulate air flow may decrease disease severity.
  • The use of rust resistant plant varieties
  • Crop rotation can break the disease cycle because many rusts are host specific and do not persist long without their host.
  • Inspection of imported plants and cuttings for symptoms. It is important to continuously observe the plants because rust diseases have a latent period (plant has the disease but shows no symptoms).
  • Use of disease-free seed can reduce incidence for some rusts [23]

Host plants affected

It is probable that most plant species are affected by some species of rust.[ citation needed ] Rusts are often named after a host species that they infect. For example; Puccinia xanthii infects the flowering plant cocklebur ( Xanthium ). Recently, a total of 95 rust fungi belonging to 25 genera associated with 117 forest plant species belonging to 80 host genera under 43 host families were reported from the Western Ghats, Kerala, India. [3] Rust fungi include:

Rust infected host genera include: [3]

Some of the better known hosts include:

Hyperparasites of rusts

In the family Sphaeropsidaceae of Sphaeropsidales fungi, species of the genus Darluca are hyperparasites on rusts. [27]

See also

Related Research Articles

<span class="mw-page-title-main">Heteroecious</span> Several-host parasite

A heteroecious parasite is one that requires at least two hosts. The primary host is the host in which the parasite spends its adult life; the other is the secondary host. Both hosts are required for the parasite to complete its life cycle. This can be contrasted with an autoecious parasite which can complete its life cycle on a single host species. Many rust fungi have heteroecious life cycles:

<i>Cronartium ribicola</i> Species of rust fungus

Cronartium ribicola is a species of rust fungus in the family Cronartiaceae that causes the disease white pine blister rust. Other names include: Rouille vésiculeuse du pin blanc (French), white pine Blasenrost (German), moho ampolla del pino blanco (Spanish).

<span class="mw-page-title-main">Stem rust</span> Fungus disease of cereal crops

Stem rust, also known as cereal rust, black rust, red rust or red dust, is caused by the fungus Puccinia graminis, which causes significant disease in cereal crops. Crop species that are affected by the disease include bread wheat, durum wheat, barley and triticale. These diseases have affected cereal farming throughout history. The annual recurrence of stem rust of wheat in North Indian plains was discovered by K.C. Mehta. Since the 1950s, wheat strains bred to be resistant to stem rust have become available. Fungicides effective against stem rust are available as well.

<span class="mw-page-title-main">Wheat leaf rust</span> Fungal disease of wheat, most prevalent

Wheat leaf rust is a fungal disease that affects wheat, barley, rye stems, leaves and grains. In temperate zones it is destructive on winter wheat because the pathogen overwinters. Infections can lead up to 20% yield loss. The pathogen is a Puccinia rust fungus. It is the most prevalent of all the wheat rust diseases, occurring in most wheat-growing regions. It causes serious epidemics in North America, Mexico and South America and is a devastating seasonal disease in India. P. triticina is heteroecious, requiring two distinct hosts.

This is a glossary of some of the terms used in phytopathology.

<i>Gymnosporangium juniperi-virginianae</i> Species of fungus

Gymnosporangium juniperi-virginianae is a plant pathogen that causes cedar-apple rust. In virtually any location where apples or crabapples (Malus) and eastern red cedar coexist, cedar apple rust can be a destructive or disfiguring disease on both the apples and cedars. Apples, crabapples, and eastern red cedar are the most common hosts for this disease. Similar diseases can be found on quince and hawthorn and many species of juniper can substitute for the eastern red cedars.

Puccinia schedonnardii is a basidiomycete fungus that affects cotton. More commonly known as a “rust,” this pathogen typically affects cotton leaves, which can decrease the quality of the boll at time of harvest. As large percentages of cotton in the United States are resistant to various rust varieties, there is little economic importance to this disease. In places where rust is prevalent, however, growers could see up to a 50% reduction in yield due to rust infection.

<i>Puccinia coronata</i> Species of fungus

Puccinia coronata is a plant pathogen and causal agent of oat and barley crown rust. The pathogen occurs worldwide, infecting both wild and cultivated oats. Crown rust poses a threat to barley production, because the first infections in barley occur early in the season from local inoculum. Crown rusts have evolved many different physiological races within different species in response to host resistance. Each pathogenic race can attack a specific line of plants within the species typical host. For example, there are over 290 races of P. coronata. Crops with resistant phenotypes are often released, but within a few years virulent races have arisen and P. coronata can infect them.

<i>Puccinia helianthi</i> Species of fungus

Puccinia helianthi is a macrocyclic and autoecious fungal plant pathogen that causes rust on sunflower. It is also known as "common rust" and "red rust" of sunflower.

<i>Uromyces viciae-fabae <span style="font-style:normal;">var.</span> viciae-fabae</i> Species of fungus

Uromyces viciae-fabae var. viciae-fabae is a plant pathogen commonly known as faba-bean rust. The rust is distinguished by the typical rust-like marks on the stem and leaves, causing defoliation and loss of photosynthetic surface along with reduction in yield. The disease is fungal and is autoecious meaning it has one plant host. The rust of faba beans is macrocyclic, or contains 5 spores during its life cycle.

<i>Gymnosporangium sabinae</i> Species of fungus

Gymnosporangium sabinae is a species of rust fungus in the subdivision Pucciniomycotina. Known as pear rust, European pear rust, or pear trellis rust, it is a heteroecious plant pathogen with Juniperus sabina as the main primary (telial) host and Pyrus communis as the main secondary (aecial) host.

<i>Puccinia monoica</i> Species of fungus

Puccinia monoica is a parasitic rust fungus of the genus Puccinia that inhibits flowering in its host plant and radically transforms host morphology in order to facilitate its own sexual reproduction.

<i>Puccinia horiana</i> Species of fungus

Puccinia horiana is a species of fungus that causes chrysanthemum white rust, is a disease of plant species of the genus Chrysanthemum.

<span class="mw-page-title-main">Wheat yellow rust</span> Fungal disease of wheat

Wheat yellow rust, also known as wheat stripe rust, is one of the three major wheat rust diseases, along with stem rust of wheat and leaf rust.

<span class="mw-page-title-main">Telium</span> Structure produced by rust fungi as part of the reproductive cycle

Telium, plural telia, are structures produced by rust fungi as part of the reproductive cycle. They are typically yellow or orange drying to brown or black and are exclusively a mechanism for the release of teliospores which are released by wind or water to infect the alternate host in the rust life-cycle. The telial stage provides an overwintering strategy in the life cycle of a parasitic heteroecious fungus by producing teliospores; this occurs on cedar trees. A primary aecial stage is spent parasitizing a separate host plant which is a precursor in the life cycle of heteroecious fungi. Teliospores are released from the telia in the spring. The spores can spread many kilometers through the air, however most are spread near the host plant.

Ruth Florence Allen (1879–1963) was an American botanist and plant pathologist and the first woman to earn her Ph.D. in botany from the University of Wisconsin. Her doctorate research focused on the reproduction and cell biology of ferns, particularly the phenomenon of apogamy. Later in her career, Allen shifted her focus to plant pathology. Her major contribution to the field of mycology was furthering the understanding of rust fungi, a group of economically important plant pathogens. Allen completed many studies on Puccinia graminis, once considered a catastrophically damaging disease-causing agent in cereal crops before the discovery of current management measures.

<span class="mw-page-title-main">Spruce broom rust</span> Species of fungus

Spruce broom rust or yellow witches' broom rust is a fungal plant disease caused by the basidiomycete fungus known as Chrysomyxa arctostaphyli. It occurs exclusively in North America, with the most concentrated outbreaks occurring in northern Arizona and southern Colorado on blue and Engelmann spruce, as well as in Alaska on black and white spruce. This disease alternates its life cycle between two hosts, with the spruce serving as the primary host and bearberry serving as the secondary or alternate host. The name for the disease comes from the distinctive “witches broom”, commonly yellow in color, which forms on the spruce after young needles have been infected. Management must be carried out through physical or mechanical methods, such as the pruning of brooms or the removal of the secondary host from the area, because no chemical control measures have yet been determined to be economically effective. Generally, spruce broom rust is seen as a mostly cosmetic issue, and it is very rarely the direct cause of tree death; however, research has shown a reduction in overall productivity and health of infected trees, making it an important issue for logging and timber companies.

Phakopsora euvitis is a rust fungus that causes disease of grape leaves. This rust fungus has been seen in regions including: Eastern Asia, Southern Asia, Southwestern Brazil, the Americas, and northern Australia. It is widely distributed in eastern and southern Asia but was first discovered on grapevines in Darwin, Australia in 2001 and was identified as Asian grapevine leaf rust by July 2007.

Melampsora amygdalinae is a fungal pathogen and part of the division Basidiomycota. It is known as a rust fungus that is host specific. M. amygdalinae commonly infects willows of the genus Salix. This fungus was first discovered in 1909 by Heinrich Klebahn who was a professor of soil biology in Hamburg. Neimi at el. explain how the pathogen occurs throughout the whole distribution of the host, and the small natural populations are an area of interest. This rust fungus is annual and autoecious, which references the fungus spending its entire life in a single host.

<i>Puccinia sorghi</i> Common rust of maize/corn fungal disease

Puccinia sorghi, or common rust of maize, is a species of rust fungus that infects corn and species from the plant genus Oxalis.

References

  1. 1 2 3 4 5 6 7 Aime, M. C.; McTaggart, A. R. (2021). "A higher-rank classification for rust fungi, with notes on genera". Fungal Systematics and Evolution. 7: 21–47. doi:10.3114/fuse.2021.07.02. PMC   8165960 . PMID   34124616.
  2. ↑ "Species Fungorum - Search Page". www.speciesfungorum.org. Archived from the original on 9 October 2023. Retrieved 27 October 2022.
  3. 1 2 3 4 5 6 7 8 9 Mohanan, C. (2010). Rust Fungi of Kerala. Kerala, India: Kerala Forest Research Institute. p. 148. ISBN   978-81-85041-72-8.
  4. ↑ Kolmer, James A; Ordonez, Maria E; Groth, James V (2001). eLS. John Wiley & Sons, Ltd. doi:10.1002/9780470015902.a0021264. ISBN   9780470015902. S2CID   1434349.
  5. ↑ Evans, R. (2007). Utopia Antiqua: Readings of the Golden Age and Decline at Rome. Taylor & Francis. ISBN   978-1-134-48787-5. Archived from the original on 2023-10-09. Retrieved 2018-01-12.
  6. ↑ Helfer, Stephan (2013-10-30). "Rust fungi and global change". New Phytologist. 201 (3): 770–780. doi: 10.1111/nph.12570 . ISSN   0028-646X. PMID   24558651.
  7. ↑ Central Science Laboratory. (2006). Plant Healthcare: Rusts [Fact Sheet]. Retrieved from www.csldiagnostics.co.uk
  8. ↑ "Rust Fungi". www.backyardnature.net. Archived from the original on 2010-09-17. Retrieved 2010-08-06.
  9. 1 2 3 4 Schumann, G. & D'Arcy, C. (2010). Essential plant pathology. APS Press
  10. ↑ Scott, K.J, & Chakravorty, A.K., (1982), The Rust fungi. Academic Press.
  11. 1 2 Peterson, R., (1974). The Rust Fungus Life Cycle. The Botanical Review. 40(4), 453-513.
  12. ↑ Sulaiman Eve, Hassan Y; Runno-Paurson; Kaurilind, Eve; Niinemets, Ülo (2023). "Differential impact of crown rust (Puccinia coronata) infection on photosynthesis and volatile emissions in the primary host Avena sativa and the alternate host Rhamnus frangula". Journal of Experimental Botany. 74 (6): 2029–2046. doi:10.1093/jxb/erad001. PMID   36610799.
  13. ↑ Craigie, J.H. (1931). Phytopathology, 21,1001
  14. ↑ Dickinson, M. Molecular Plant Pathology. 2003.
  15. ↑ Deising, H. B., S. Werner, and M. Wernitz, The role of fungal appressoria in plant infection. Microbes Infect, 2000. 2(13): pp. 1631–41.
  16. ↑ Zhou, X. L., et al., A mechanosensitive channel in whole cells and in membrane patches of the fungus Uromyces. Science, 1991. 253(5026): p. 1415.
  17. ↑ Voegele, R. T., and K. Mendgen, Rust haustoria: nutrient uptake and beyond. New Phytologist, 2003. 159(1): pp. 93–100.
  18. ↑ Cornell University. (2010). Daylily rust: Puccinia hemerocallidis [Fact sheet]. Retrieved from http://plantclinic.cornell.edu Archived 2010-08-18 at the Wayback Machine
  19. ↑ Hooker, Arthur L (1967). "The Genetics and Expression of Resistance in Plants to Rusts of the Genus Puccinia". Annu. Rev. Phytopathol. 5 (1): 163–178. doi:10.1146/annurev.py.05.090167.001115.
  20. ↑ Hurtado-Gonzales, O. P.; Valentini, G.; Gilio, T. A.; Martins, A. M.; Song, Q.; Pastor-Corrales, M. A. (2016). "Fine Mapping of Ur-3, a Historically Important Rust Resistance Locus in Common Bean". G3: Genes, Genomes, Genetics. 7 (2): 557–569. doi:10.1534/g3.116.036061. PMC   5295601 . PMID   28031244.
  21. 1 2 3 4 5 6 7 Staples, Richard (2000). "Research on the Rust Fungi During the Twentieth Century". Annual Review of Phytopathology . 38 (1). Annual Reviews: 49–69. doi:10.1146/annurev.phyto.38.1.49. ISSN   0066-4286. PMID   11701836. S2CID   4861612.
  22. ↑ Dracatos, Peter M.; Lu, Jing; Sánchez-Martín, Javier; Wulff, Brande B.H. (2023). "Resistance that stacks up: engineering rust and mildew disease control in the cereal crops wheat and barley". Plant Biotechnology Journal. 21 (10): 1938–1951. doi:10.1111/pbi.14106. PMC   10502761 . PMID   37494504. S2CID   260201756.
  23. 1 2 Marsalis, M. & Goldberg, N. (2006). Leaf, Stem, And Stripe Rust Diseases of Wheat. [Fact sheet]. New Mexico State University. http://pubs.nmsu.edu/_a/A415/ Archived 2022-11-27 at the Wayback Machine
  24. ↑ Wallis, C. & Lewandowski, D. (2008). Cedar Rust Diseases of Ornamental Plants. [Fact Sheet]. Ohio State University. https://woodlandstewards.osu.edu/sites/woodlands/files/d6/files/pubfiles/3055%20cedar%20rust.pdf Archived 2021-01-07 at the Wayback Machine
  25. ↑ "Stopsoybeanrust.com". www.stopsoybeanrust.com. Archived from the original on 2018-06-12. Retrieved 2010-08-06.
  26. ↑ "Common Corn Rust". www.channel.com. Archived from the original on 2019-12-16. Retrieved 2019-12-16.
  27. ↑ faculty.ucr.edu Archived 2016-03-03 at the Wayback Machine (retrieved December 2015)
  28. ↑ Thompson, Clive (14 February 2023). "How Rust went from a side project to the world's most-loved programming language". MIT Technology Review . Archived from the original on 15 February 2023. Retrieved 15 February 2023.
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