Puccinia xanthii

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Puccinia xanthii
Scientific classification OOjs UI icon edit-ltr.svg
Domain: Eukaryota
Kingdom: Fungi
Division: Basidiomycota
Class: Pucciniomycetes
Order: Pucciniales
Family: Pucciniaceae
Genus: Puccinia
Species:
P. xanthii
Binomial name
Puccinia xanthii
Schwein. (1822)
Distribution of Puccinia xanthii as of 2024. Distrubution of Puccinia xanthii.jpg
Distribution of Puccinia xanthii as of 2024.

Puccinia xanthii is a fungal pathogen of plants in the Asteraceae, and can infect hosts from at least 42 genera within that family [1] , most notably species in the Xanthium and Ambrosia genera. This pathogen was discovered growing on Xanthium strumarium in North Carolina, United States in 1822 [2] . Common names of P. xanthii include Summer Rust [3] and Cocklebur Rust [4] .

Contents

Distribution

Puccinia xanthii is native to the continental United States, Canada, Mexico, Hawaii, Cuba, Haiti, the Dominican Republic, Puerto Rico, and the Bahamas [5] [3] . This fungus has been reported in several countries throughout Europe, Asia, Africa and Australia; often following the introduction of invasive host plants from North America or intentional release as a biocontrol agent.

Europe

Researchers have detected P. xanthii in Bulgaria, southern France, Hungary, northern Italy, Romania, Spain, and the former Yugoslavia (Bosnia, Serbia, Slovenia, Montenegro, Macedonia, Herzegovina, and Croatia) [5] [6] [7] [8] . Puccinia xanthii was found growing on Xanthium orientale subsp. italicum in eastern Hungary in December 2002 [9] [7] .

Asia

Puccinia xanthii has been detected in India, Indonesia, Japan, Pakistan, and Korea [5] [6] [10] . Puccinia xanthii was found growing in lesions on leaves of Xanthium orientale in Okcheon-gun, Korea in October 2021 [5] and from Xanthium orientale subsp. italicum in the Liaoning Province of China in August 2013 [9] . Xanthium orientale subsp. italicum was first found in Beijing, China in 1991 and has been shown to decrease the biodiversity of native flora and cause human health hazards from allergenic pollen [9] . As a result of this, the P. xanthii is considered beneficial in this area as it may decrease the vigor of this weed. Puccinia xanthii was also found on Xanthium strumarium in Parachinar, Pakistan in 2018 [10] .

Australia

Puccinia xanthii was observed on Xanthium occidentale in Australia in 1975 [11] .

Africa

Puccinia xanthii was found growing on Helianthus annous in the Northwest Province of South Africa in February 2000 [12] .

Taxonomy

Puccinia xanthii is a rust in the phylum Basidiomycota, subphylum Pucciniomycotina, class Pucciniomycetes, order Pucciniales, and family Pucciniaceae [2] . Its full scientific name is Puccinia xanthii Schwein., Schriften der Naturforschenden Gesellschaft zu Leipzig 1:73 [13] . Using data from ITS (internal transcribed spacer) and TEF (translation elongation factor) phylogenetic analyses, the closest relative of P. xanthii is P. melampodii, and these species are a sister group to the fungus Dietelia portoricensis [14] . In 2005, Hennen et. al proposed that P. xanthii, P. melampodii, and 51 other microcyclic rusts from the Americas and Eurasia that infect members of the Asteraceae should be grouped under the single morphospecies name Puccinia cnici-oleracei [14] . This complex is based on morphology and needs further proof to be considered valid, however, P. xanthii and P. melampodii could not be easily separated at the species level using phylogenetic data from the  ITS and TEF regions [14] .

This fungus has a high level of intraspecies variation, resulting in many different strains that specialize on one or a few hosts in the Asteraceae [11] . Studies on the pathogenicity of Puccinia xanthii vary considerably based on where the isolate (which cannot be grown in culture) was taken. This high level of genetic variation is created through sexual recombination during karyogamy, somatic hybridization, mutations, and genes introduced from closely related species or other strains of P. xanthii [11] . For example, an Australian strain of P. xanthii was able to infect Calendula offinalis and some cultivars of Helianthus annus while an American strain was able to infect only Ambrosia trifida in cross inoculation tests [15] . Index Fungorum recognizes three classifications of P. xanthii below the species level: Puccinia xanthii var. ambrosiae-trifidae, Puccinia xanthii var. parthenii-hysterophorae, and Puccinia xanthii var. xanthii [2] . This pathogen requires more study as the number of reported host species of Puccinia xanthii comprises more species than those infected by these subclassifications.

Puccinia xanthii var. ambrosiae-trifidae

This is an obligate pathogen of Ambrosia trifida, commonly known as the giant ragweed [1] . Studies in the Liaoning Province of China show that P. xanthii var. ambrosiae-trifidae is a suitable biocontrol for this plant, which is highly allergenic and invasive throughout Asia, Europe, and Australia [1] . There is controversy over whether P. xanthii var. ambrosiae-trifidae is considered a forma specialis, as it was originally named in 1981, or a variety. Genetic evidence considering the degree or similarity between P. xanthii morphospecies suggests that the term variety is more accurate to distinguish between populations of P. xanthii, but literature varies in the use of f. sp. or var. [14] .  

Puccinia xanthii var. parthenii-hysterophorae

This variation is native to Mexico and specializes in infecting the plant Partheniumhysterophorus [3] . Outside of its native range, this North American weed has caused issues in agriculture via allopathic chemicals, decreased biodiversity, and its pollen is a human health hazard. P. xanthii var. parthenii-hysterophorae has been intentionally introduced to north and central Queensland, Australia in 2000 as a biocontrol for this invasive plant [3] . It was also introduced in South Africa as a biocontrol in 2010 as part of an effort to contain this weed from spreading through sub-Saharan Africa [16] .

Puccinia xanthii var. xanthii

This variation specializes on plants in the Xanthium genus.

Synonyms

Leptopuccinia xanthii [17]

Micropuccinia xanthii [17]

Dasyspora xanthii [17]

Disease Cycle

Puccinia xanthii is a microcyclic, autoecious obligate biotroph [1] [6] . This means that it only produces basidiospores and teliospores (and lacks spermatia, aeciospores, and urediniospores) and completes its life cycle on a single living host plant. Due to the cyclic nature of rusts, this lifecycle doesn’t have a ‘start’ point. In this case, a basidiospore landing on a leaf is arbitrarily chosen to begin the life cycle.

Basidiospores of P. xanthii are carried to new plants via wind or through physical contact with nearby plants [3] . These basidiospores germinate a polar, or occasionally lateral, germ tube that can be thin or thick [1] . Thicker germ tubes often lead to the formation of a non-sequential basidiospore, or a smaller, secondary basidiospore that forms from the germ tube of the original [6] . Thicker germ tubes can also lead to chains of basidiospores, which is most common in P. xanthii f. sp. ambrosiae-trifidae and functions as a form of asexual reproduction [1] . Germ tubes are highly variable in length, and have a roughly equal chance of being 0.5-1.5 µm or 5-10 µm long. In 3% of cases, germ tubes are several times the length of the basidiospore [6] .

At the end of the germ tube, an appressorium (specialized structure used to attach to and penetrate the leaf surface) is formed. Puccinia xanthii has been shown to produce its appressoria preferentially along the cellular gaps of the leaf epidermis [6] . The appressoria is attached to the leaf with a mucilaginous exudate that helps protect it from desiccation and may also provide a reservoir of enzymes to help penetrate the host epidermis [1] . This structure ranges in form from a swollen bump to a well defined lobing at the end of the germ tube [6] . Underneath the appressorium, numerous wedge-shaped papillae and a penetration peg are formed [1] . The penetration peg goes directly through the epidermis. While splitting the cuticle wall, the penetration peg is quite thin then expands when it reaches the cell membrane [1] . The penetration peg continues growing and forms intraepidermal vesicles to contain the remaining contents of the basidiospore before putting down a septum and differentiating into primary hyphae.

The hyphae colonizes the plant tissue as it grows and branches into neighboring epidermal cells, intercellular space, and finally into the spongy parenchyma cells [1] [6] . During this colonization, the hyphae forms haustoria 24 to 48 hours after inoculation [1] . The haustoria of P. xanthii look like swellings of the hyphae (lacking morphological specialization seen in haustoria with projections) that grow inside plant cells and absorb nutrients and water [1] .

Puccinia xanthii will form dark brown telia in a thallus that erupts through the leaf surface seven to eight days after inoculation [5] [6] [9] . Telia are 0.28-0.61 mm in diameter, round, and mostly form in circular groups 10 mm in diameter on the lower leaf surface (though telia can be found on either side of the leaf) [5] [18] . These telia will bore teliospores that can either germinate immediately if conditions are favorable or act as a survival structure for the fungus. The teliospores are darker or lighter yellowish-brown, smooth, 42-58 µm x 12-21 µm and thicker near the conical apex [5] [9] . They are two-celled and have a constricted septum [5] [9] . Teliospores also have a persistent yellowish-brown pedicel that is 22-70 µm long [9] [18] . The teliospores will germinate to form a tube-shaped basidium with three septations [1] . This basidium then forms four white, thin-walled, binucleate, single-celled basidiospores [3] [6] . The basidiospores are binucleate due to a mitotic division of the initial nucleus while the infective mycelium is monokaryotic [6] . These basidiospores break off of the basidium (usually attached to the teliospore and telia) and continue the infection cycle.

Signs and Symptoms

Puccinia xanthii forms dark brown pustules (raised spots) with a chlorotic halo on the adaxial, and sometimes abaxial leaf surface [5] [4] . In the early stage of infection, P. xanthii causes yellow lesions that gradually turn brown in the center as telia are produced [9] . Multiple infections cause necrotic lesions that can cover leaves, petioles, and stems. Depending on the susceptibility of the host and severity of the infection, P. xanthii can cause plant decline and death [3] [12] [19] .

Application as a Biocontrol

For information on where this species is being used as a biocontrol, please refer to the section on distribution. There are mixed results on the use of P. xanthii as a biocontrol, while it can cause significant damage on some host plants,it requires suitable environmental conditions to hinder plant growth. For example, while P. xanthii was able to infect and kill invasive cocklebur species in Hungary if infection starts when the plant is a cotyledon, natural infections that begin during the second part of the growing season and are seldom lethal [18] .

The Australian Department of Agriculture, Water and the Environment has put out an extension document on using P. xanthii var. parthenii-hysterophorae as a biocontrol agent. They advocate for people to intentionally spread summer rust onto invasive Parthenium spp. by collecting symptomatic leaves and pinning them to uninfected plants [3] . This strategy has been used in Australia to contain the spread of Parthenium. Kassai-Jager et al. has also recommended the use of this pathogen as a classical biocontrol agent in Australia against another invasive member of the Asteraceae from North America, Ambrosia artemisifolia. Puccinia xanthii from Ambrosia artemisifolia growing in the wild in Texas was “highly virulent on A. artemisifolia plants from Australia” [8] .  

Natural infections of Puccinia xanthii var. ambrosia-trifidae on Ambrosia trifida in Maryland caused severe decline on A. trifida and reduced its propagative potential [19] . Batra [19] performed pathogenicity tests on this variation and recommended using P. xanthii var. ambrosia-trifidae as a biocontrol in Eurasia where this plant is an invasive species.

Pathogenicity on Sunflowers

Puccinia xanthii may also pose a potential threat to the ornamental plant trade. Puccinia xanthii could infect and cause foliar damage to Helianthus annus and Calendula offiinalis in pathogenicity tests using strains from C. officinalis in Queensland [20] [21] . This is likely an undescribed variety of P. xanthii. More taxonomic research is needed to distinguish between the varieties of P. xanthii by host-pathogen interaction [14] .

See also

Related Research Articles

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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.

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>Urocystis agropyri</i> Species of fungus

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

Puccinia asparagi is the causative agent of asparagus rust. It is an autoecious fungus, meaning that all stages of its life cycle – pycniospores, aeciospores, and teliospores – all develop upon the same host plant . Rust diseases are among the most destructive plant diseases, known to cause famine following destruction of grains, vegetables, and legumes. Asparagus rust occurs wherever the plant is grown and attacks asparagus plants during and after the cutting season. Asparagus spears are usually harvested before extensive rust symptoms appear. Symptoms are first noticeable on the growing shoots in early summer as light green, oval lesions, followed by tan blister spots and black, protruding blisters later in the season. The lesions are symptoms of Puccinia asparagi during early spring, mid-summer and later summer to fall, respectively. Severe rust infections stunt or kill young asparagus shoots, causing foliage to fall prematurely, and reduce the ability of the plant to store food reserves. The Puccinia asparagi fungus accomplishes this by rust lowering the amounts of root storage metabolites. The infected plant has reduced plant vigor and yield, often leading to death in severe cases. Most rust diseases have several stages, some of which may occur on different hosts; however, in asparagus rust all the life stages occur on asparagus. Because of this, many observers mistake the different stages of the Puccinia asparagi life cycle as the presence of different diseases. The effects of Puccinia asparagi are present worldwide wherever asparagus is being grown. Asparagus rust is a serious threat to the asparagus industry.

<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>Puccinia menthae</i> Species of fungus

Puccinia menthae is a fungal plant pathogen that causes rust on mint plants. It was originally found on the leaves of Mentha aquatica.

<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 thaliae</i> Species of fungus

Puccinia thaliae is the causal agent of canna rust, a fungal disease of Canna. Symptoms include yellow to tan spots on the plant's leaves and stems. Initial disease symptoms will result in scattered sori, eventually covering the entirety of the leaf with coalescing postulates. Both leaf surfaces, although more predominant on the underside (abaxial) of the leaf, will show yellow to brownish spore-producing these pustulate structures, and these are the signs of the disease. Spots on the upper leaf-surface coalesce and turn to brown-to-black as the disease progresses. Infection spots will become necrotic with time, with small holes developing in older leaves. These infected leaves eventually become dry and prematurely fall.

<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.

<i>Puccinia jaceae <span style="font-style:normal;">var.</span> solstitialis</i> Species of fungus

Puccinia jaceae var. solstitialis is a species of fungus in the Pucciniaceae family. It is a plant pathogen that causes rust. Native to Eurasia, it is the first fungal pathogen approved in the United States as a biological control agent to curb the growth of the invasive weed yellow starthistle.

<i>Austropuccinia</i> Genus of fungi

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<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.

<i>Phragmidium</i> Genus of fungi

Phragmidium is a genus of rust fungus that typically infects plant species in the family Rosaceae. It is characterised by having stalked teliospores borne on telia each having a row of four or more cells. All species have a caeoma which is a diffuse aecidium lacking a peridium.

<i>Puccinia mariae-wilsoniae</i> Species of fungus

Puccinia mariae-wilsoniae, commonly known as the spring beauty rust, is a species of rust fungus found in North America. A plant pathogen, it grows on the leaves of the spring beauty flowering plants Claytonia caroliniana and C. virginica.

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.

<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.

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

Puccinia myrsiphylli is a rust fungus in the genus Puccinia, family Pucciniaceae, and is native to South Africa. It has been tested, introduced, and targeted in Australia and New Zealand as an effective biocontrol agent for Asparagus asparagoides, also known as bridal creeper.

References

  1. 1 2 3 4 5 6 7 8 9 10 11 12 13 Zhang, P., Lu, G., Sun, X., Zhang, W., Qu, B., & Tian, X. (2011). The infection process of puccinia xanthii f. sp.. ambrosiae-trifidae on ambrosia trifida. Botany, 89(11), 771–777. https://doi.org/10.1139/b11-067
  2. 1 2 3 Puccinia xanthii Schwein. Index fungorum . (2024). https://www.indexfungorum.org/names/NamesRecord.asp?RecordID=199752
  3. 1 2 3 4 5 6 7 8 Puccinia xanthii var. parthenii-hysterophorae. (2022). CABI Compendium. https://doi.org/10.1079/cabicompendium.48337333
  4. 1 2 Gulya, T. J., & Charlet, L. D. (2007). First report of Puccinia xanthii on sunflower in North America. Plant Disease, 86(5), 564–564. https://doi.org/10.1094/pdis.2002.86.5.564a
  5. 1 2 3 4 5 6 7 8 9 Ryu, M., Ryu, H., Jeon, E. J., Park, Y. J., Kang, B., Ono, Y., Kim, O.-K., & Lee, S.-J. (2024). First report of Puccinia xanthii causing rust disease on Xanthium orientale in Korea. Plant Disease, 108(6), 1895. https://doi.org/10.1094/pdis-01-24-0143-pdn
  6. 1 2 3 4 5 6 7 8 9 10 11 Morin, L., Brown, J. F., & Auld, B. A. (1992). Teliospore germination, basidiospore formation and the infection process of Puccinia xanthii on Xanthium Occidentale. Mycological Research, 96(8), 661–669. https://doi.org/10.1016/s0953-7562(09)80494-2
  7. 1 2 Dávid, I., Harcz, P., & Kövics, G. J. (2003). First report of Puccinia xanthii on Xanthium italicum in eastern Hungary. Plant Disease, 87(12), 1536–1536. https://doi.org/10.1094/pdis.2003.87.12.1536c
  8. 1 2 Kassai-Jáger, E., Seier, M. K., Evans, H. C., & Kiss, L. (2015). Molecular identification and pathogenicity assessment of a rust fungus infecting common ragweed (ambrosia artemisiifolia) in its native North American range. European Journal of Plant Pathology, 145(1), 81–87. https://doi.org/10.1007/s10658-015-0815-4
  9. 1 2 3 4 5 6 7 8 Zhao, Y.-Z., Feng, Y.-L., Liu, M.-C., & Liu, Z.-H. (2014). First report of rust caused by Puccinia xanthii on Xanthium orientale subsp. italicum in China. Plant Disease, 98(11), 1582–1582. https://doi.org/10.1094/pdis-03-14-0277-pdn
  10. 1 2 Afshan, N. S., Riaz, M., Ahmad, M. A., & Khalid, A. N. (2023). Puccinia malvacearum and P. xanthii newly recorded from Pakistan. Mycotaxon, 137(4), 893–897. https://doi.org/10.5248/137.893
  11. 1 2 3 Morin, L., Auld, B. A., & Brown, J. F. (1993). Host range of Puccinia xanthiiand postpenetration development on Xanthium occidentale. Canadian Journal of Botany, 71(7), 959–965. https://doi.org/10.1139/b93-108
  12. 1 2 Pretorius, Z. A., van Wyk, P. S., & Kriel, W. M. (2000). Occurrence of Puccinia xanthii on sunflower in South Africa. Plant Disease, 84(8), 924–924. https://doi.org/10.1094/pdis.2000.84.8.924a
  13. ↑ Puccinia xanthii. MycoBank Database. (2024). https://www.mycobank.org/page/Name%20details%20page/field/Mycobank%20%23/199752
  14. 1 2 3 4 5 Seier, M. K., Morin, L., van der merwe, M., Evans, H. C., & Romero, Á. (2009). Are the microcyclic rust species Puccinia melampodii and Puccinia xanthii conspecific? Mycological Research, 113(11), 1271–1282. https://doi.org/10.1016/j.mycres.2009.08.009
  15. ↑ Kiss, L. (2007). Is Puccinia xanthii a suitable biological control agent of Ambrosia artemisiifolia? Biocontrol Science and Technology, 17(5), 535–539. https://doi.org/10.1080/09583150701311705
  16. ↑ Studies from Agricultural Research Council Add New Findings in the Area of African Entomology. (2011). Veterinary Week, 92. https://doi.org/link.gale.com/apps/doc/A275098083/PPAG?u=gain40375&sid=bookmark-PPAG&xid=c1a031bf.
  17. 1 2 3 Puccinia xanthii. MycoBank Database. (2024). https://www.mycobank.org/page/Name%20details%20page/field/Mycobank%20%23/199752
  18. 1 2 3 David, I. (2006). Occurrence of Puccinia xanthii Schw. on cockleburs in Hungary. Folia Oecologica, 33(1).
  19. 1 2 3 Batra, S. W. (1981). Puccinia xanthii forma specialis ambrosia-trifidae. Mycopathologia, 73(2), 61–64. https://doi.org/10.1007/bf00562590
  20. ↑ Alcorn, J. L. (1976). Host range of Puccinia xanthii. Transactions of the British Mycological Society, 66(2), 365–367. https://doi.org/10.1016/s0007-1536(76)80078-2
  21. ↑ Alcorn, J., & Kochman, J. (1976). A field record of Puccinia xanthii on sunflower. Australasian Plant Pathology, 5(3), 33. https://doi.org/10.1071/app9760033


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