| Stem rust | |
|---|---|
 | |
Scientific classification | |
| Domain: | Eukaryota |
| Kingdom: | Fungi |
| Division: | Basidiomycota |
| Class: | Pucciniomycetes |
| Order: | Pucciniales |
| Family: | Pucciniaceae |
| Genus: | Puccinia |
| Species: | P. graminis |
| Binomial name | |
| Puccinia graminis Pers., (1794) | |
| Synonyms | |
See§ Synonyms | |
Stem rust, also known ascereal rust,black rust,[1][2]red rust orred dust,[3] is caused by thefungusPuccinia graminis, which causes significant disease incereal crops. Crop species that are affected by the disease includebread wheat,durum wheat,barley andtriticale.[1] 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.[4] Since the 1950s, wheat strains bred to be resistant to stem rust have become available.[5]Fungicides effective against stem rust are available as well.[6]
In 1999 a new virulent race of stem rust was identified against which most current wheat strains show no resistance. The race was named TTKSK (e.g. isolateUg99). Anepidemic of stem rust on wheat caused by race TTKSK spread acrossAfrica,Asia and theMiddle East, causing major concern due to the large numbers of people dependent on wheat for sustenance, thus threatening globalfood security.[7]
An outbreak of another virulent race of stem rust, TTTTF, took place inSicily in 2016, suggesting that the disease is returning to Europe.[5] Comprehensivegenomic analysis ofPuccinia graminis, combined with plant pathology and climate data, has pointed out the potential of the re-emergence of stem wheat rust in UK.[8][9]
The fungal ancestors of stem rust have infected grasses for millions of years and wheat crops for as long as they have been grown.[7] According to Jim Peterson, professor of wheat breeding and genetics atOregon State University, "Stem rust destroyed more than 20% of U.S. wheat crops several times between 1917 and 1935, and losses reached 9% twice in the 1950s," with the last U.S. outbreak in 1962 destroying 5.2% of the crop.[7]
Stem rust has been an ongoing problem dating back toAristotle's time (384–322 BC). An early ancient practice by the Romans was one where they would sacrifice red animals such as foxes, dogs, and cows toRobigus (fem.Robigo), the rust god. They would perform this ritual in the spring during a festival known as the Robigalia in hopes of the wheat crop being spared from the destruction caused by the rust. Weather records from that time have been reexamined and it has been speculated that the fall of the Roman Empire was due to a string of rainy seasons in which the rust would have been more harsh, resulting in reduced wheat harvests. Laws banning barberry were established in 1660 inRouen, France. This was due to the fact that European farmers noticed a correlation between barberry and stem rust epidemics in wheat. The law banned the planting of barberry near wheat fields and was the first of its kind.[2]
The parasitic nature of stem rust was discovered in the 1700s. Two Italian scientists,Fontana andTozzetti, first explained the stem rust fungus in wheat in 1767.[2] Italian scientistGiuseppe Maria Giovene (1753–1837), in his workLettera al dottor Cosimo Moschettini sulla ruggine, also thoroughly studied the stem rust.[10] Thirty years later it received its name,Puccinia graminis, byPersoon, and in 1854 brothersLouis René andCharles Tulasne discovered the characteristic five-spore stage that is known in some stem rust species. The brothers were also able to make a connection between the red (urediniospore) and black (teliospore) spores as different stages within the life cycle of the same organism, but the rest of the stages remained unknown.[2]
Anton de Bary later conducted experiments to observe the beliefs of European farmers regarding the relationship between the rust and barberry plants, and after connecting the basidiospores of the basidia stage to barberry, he also identified that the aeciospores in the aecia stage reinfect the wheat host. Upon de Bary's discovery of all five spore stages and their need for barberry as a host,John Craigie, a Canadian pathologist, identified the function of thespermogonium in 1927.[2]
Due to the useful nature of both barberry and wheat plants, they were eventually brought toNorth America by European colonists. Barberry was used for many things like making wine and jams from the berries to tool handles from the wood. Ultimately, as they did in Europe, the colonists began to notice a relationship between barberry and stem rust epidemics in wheat. Laws were enacted in manyNew England colonies, but as the farmers moved west, the problem with stem rust moved with them and began to spread to many areas, creating a devastating epidemic in 1916. It was not until two years later in 1918 that theUnited States created a program to remove barberry. The program was one that was supported by state and federal entities and was partly prompted by the threat it posed to food supplies duringWorld War I. The "war against barberries" was waged and called upon the help of citizens through radio and newspaper advertisements, pamphlets, and fair booths asking for help from all in the attempt to rid the barberry bushes of their existence. Later, in 1975–1980, the program was reestablished under state jurisdiction. Once this happened, a federal quarantine was established against the sale of stem rust susceptible barberry in those states that were part of the program. A barberry testing program was created to ensure that only those species and varieties of barberry that are immune to stem rust will be grown in the quarantine area.[2]
In 1969 two races not detected before inAustralia were found[11] and for decades one hypothesis was anAfrican origin,[11][12] and in 2018 DNA analysis confirmed that,[12] specificallySouth African.[11]
South Africa itself has an ongoing problem with various stem rust outbreaks which requires better response, including an indigenousbreeding for resistance program.[12]
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There is considerablegenetic diversity within the speciesP. graminis, and several special forms,forma specialis, which vary in host range have been identified.
P. graminis is a member of the phylumBasidiomycota within the kingdomFungi. The characteristicrust color on stems and leaves is typical of a general stem rust as well as any variation of this type of fungus. Different from most fungi, the rust variations have fivespore stages and alternate between two hosts. Wheat is the primary host, andbarberry is the alternate host.[citation needed]
The rust is sometimes termed "red rust" or "red dust"[3][16] owing to the spores on the leaf surfaces that range from orange to dark-red in color. Later, the spores change and become dark in color, which gives rise to another common name, "black rust".[17][2]
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The North American race nomenclature system[18][19][20] was introduced in 1988 by Roelfs and Martens.[21] This nomenclature is a series of letters each of which indicate virulence/avirulence against oneresistance gene, as diagnosed by performance against a group of cultivars known to bear that gene.
Pgt contains many races of wheat diseases, including some of the most significant in the world.Ug99 began as a race (TTKSK) ofPgt and now has proliferated into a large number ofraces of its own.[citation needed]
The virulent new race, against which most current wheat strains show no resistance, was identified in 1999. The race was named TTKSK (e.g. isolate Ug99), named after the country where it was identified (Uganda) and the year of its discovery (1999). It spread toKenya, thenEthiopia,Sudan andYemen, and becomes more virulent as it spreads. Anepidemic of stem rust on wheat caused by race TTKSK spread acrossAfrica,Asia and theMiddle East, causing major concern due to the large numbers of people dependent on wheat for sustenance,[7] thus threatening globalfood security. In 2011, after it had spread intosouthern Africa, theBill Gates Foundation donated $40 million towards research into Ug99, to be spent on critical infrastructure in Africa.[3] Scientists are working on breeding strains of wheat that are resistant to UG99. However, wheat is grown in a broad range of environments. This means that breeding programs would have extensive work remaining to get resistance into regionally adapted germplasms even after resistance is identified.[7] Similarly, in 2014, a Ug99 race called "Digalu" emerged and devastated the Digalu variety in Ethiopia.[22]: 25
JRCQC is a race affectingDurum inEthiopia.[23]
Affects barley.[14]
Successfully overwintered inKansas in 1989/90, and inTexas and Kansas in 1990/91, and so was expected to thereafter be a permanent part of the North AmericanPg population. Further pathogen adaptation, resulting in widening of the host range, is expected.[24]
Synonymous with QCCJB[15] or known as QCC-2 by some classifications.
Most commonPg race in 1991 in theUnited States, 68% of allPg samples, and 67% in 1990. Afflicted spring-sown barley in the northern Great Plains in 1990. Was the first barley stem rust to show up in the United States in 1991, insouthern Texas inUvalde. Thought to be responsible for rusting of wildHordea in theMidwestern United States and Great Plains, and overall was 94% ofPgs onHordea in 1991. 67% of QCCJ was from barley and 95% ofPg on barley was QCCJ. On wheat, QCCJ was still the most common race but only at 38% ofPg. Continues to threaten barley in theRed River Valley inNorth Dakota andMinnesota. Higher than normalinoculum production inSouth Central Oklahoma and the adjacent part ofNorth Texas before the 1991 season resulted in an epidemic inNorth Central and northwestern Kansas.[24]Virulent against barley bearingRpg1. Down to 26% ofPgs afflicting wheat in the US in 1995, 1% in 1996, and not at all in 1997 or 1998. Not found on barley in 1997 but found again in 1998.[25]
The first QCC race (since renamed QCCJ or QCCJB) was detected in the northwestGreat Plains in 1988, and by 1990 was over 90% ofPgs on barley in the United States.[15] Also afflicted wheat until a mass switch away from vulnerable cultivars resulted in complete absence in 1997 or 1998.[25][15] Barley virulence is temperature-sensitive: from 18–20 °C (64–68 °F)rpg4 andRpg5 are highly effective, but above 27 °C (81 °F) they are ineffective. Not necessarily distinguishable from QCCJ, used synonymously by some practitioners.[15]
Found in the US on wheat in 1997 and 1998 – but only in the West across both years. On barley in 1997 but not 1998.[25]
25% ofPgs on wheat in 1991. Traces found growing in northwestIllinois fields, also in 1991.[24] 8% of allPgs on wheat, barley, and oat in the US in 1997, and 31% in 1998. Displaced the previously dominantTPMK suddenly in 1998.[25]
36% ofPg samples from wheat in 1991 in the United States. Unusually severe insouthern Illinois in the first week of June, and in westcentral Indiana, in 1991.[24] TPMK was the worst at 69% ofPgs on wheat in 1997 in the United States – being absent only from the southern Great Plains and the west, but then was down to 10% in 1998. In the upper Great Plains it was already declining – to 26% of samples in 1997, and 12% in 1998. In the most fertile areas of the eastern US it was 96% ofPgs in 1997 but then suddenly fell to 29% in 1998. In a few other locations in the US, and overall across the US, this race declined 97–98 in favor of other races, and not because of overallPg decline.[25]
As listed bySpecies Fungorum;[26]
The stem rust fungus attacks the parts of the plant that are above ground. Spores that land on green wheat plants form a pustule that invades the outer layers of the stalk.[7] Infected plants produce fewertillers and set fewer seed, and in cases of severe infection the plant may die. Infection can reduce what is an apparently healthy crop about three weeks before harvest into a black tangle of broken stems and shriveled grains by harvest.[1]
Stem rust of cereals causes yield losses in several ways:[2]
Stem rust on wheat is characterized by the presence of uredinia on the plant, which are brick-red, elongated, blister-like pustules that are easily shaken off. They most frequently occur on the leaf sheaths, but are also found onstems,leaves,glumes andawns. On leaves they develop mostly on the underside but may penetrate to the upperside. On leaf sheaths and glumes pustules rupture the epidermis, giving a ragged appearance.[1]
Towards the end of the growing season blacktelia are produced. For this reason stem rust is also known as "black rust". The telia are firmly attached to the plant tissue.[1]
The site of infection is a visible symptom of the disease.
Pycnia appear onbarberry plants in the spring, usually in the upper leaf surfaces. They are often in small clusters and exudepycniospores in a sticky honeydew. Five to ten days later, cup-shaped structures filled with orange-yellow, powderyaeciospores break through the lower leaf surface. The aecial cups are yellow and sometimes elongate to extend up to 5 millimetres (13⁄64 in) from the leaf surface.[2] So important is its role in maintenance of prevalence that since the near extermination of thealternate host from the northernGreat Plains in the United States, epidemics in crops have become rare.[24]
Like otherPuccinia species,P. graminis is anobligate biotroph (it colonizes living plant cells) and has a complex life cycle[27] featuringalternation of generations. The fungus isheteroecious, requiring two hosts to complete its life cycle – the cereal host and thealternate host.[2] There are many species inBerberis andMahonia (and their hybrid genusx Mahoberberis) that are susceptible to stem rust, but thecommon barberry (B. vulgaris) is considered to be the most important alternate host.[1]P. graminis is macrocyclic[2] (exhibits all five of thespore types that are known for rust fungi[28]).
P. graminis can complete its life cycle either with or without barberry (the alternate host).[2]
P. g. tritici'sobligately biotrophic lifestyle involves the dramatic up-regulation of particular gene transcriptions, constituting its biotrophy genomic features. These genomic regions have parallels in other eukaryotic plant pathogens. These parallels – between these independently evolved and unrelated sets of genes – show a strong and broad pattern ofconvergent evolution around theplant pathogeniclifestyle.[29]
Due to its cyclical nature, there is no true 'start point' for this process. Here, the production ofurediniospores is arbitrarily chosen as a start point.
Urediniospores are formed in structures called uredinia, which are produced by fungalmycelia on the cereal host 1–2 weeks after infection. The urediniospores aredikaryotic (contain two un-fused, haploid nuclei in one cell) and are formed on individual stalks within theuredinium. They are spiny and brick-red. Urediniospores are the only type of spores in the rust fungus life cycle that are capable of infecting the host on which they are produced, and this is therefore referred to as the 'repeating stage' of the life cycle. It is the spread of urediniospores that allows infection to spread from one cereal plant to another.[2] This phase can rapidly spread the infection over a wide area.
Towards the end of the cereal host's growing season, the mycelia produce structures called telia. Telia produce a type of spore calledteliospores. These black, thick-walled spores aredikaryotic. They are the only form in whichPuccinia graminis is able to overwinter independently of a host.[2]
Each teliospore undergoeskaryogamy (fusion of nuclei) andmeiosis to form four haploid spores calledbasidiospores. This is an important source of genetic recombination in the life cycle. Basidiospores are thin-walled and colourless. They cannot infect the cereal host, but can infect the alternative host (barberry).[2] They are usually carried to the alternative host by wind.
Once basidiospores arrive on a leaf of the alternative host, they germinate to produce amycelium (which ishaploid) that directly penetrates the epidermis and colonises the leaf. Once inside the leaf the mycelium produces specialised infection structures called pycnia. The pycnia produce two types of haploid gametes, thepycniospores and the receptive hyphae. The pycniospores are produced in a sticky honeydew that attracts insects. The insects carry pycniospores from one leaf to another. Splashing raindrops can also spread pycniospores. A pycniospore can fertilise a receptive hypha of the oppositemating type, leading to the production of amycelium that isdikaryotic. This is the sexual stage of the life cycle and cross-fertilisation provides an important source of genetic recombination.[2]
This dikaryotic mycelium then forms structures calledaecia, which produce a type of dikaryotic spores calledaeciospores. These have a worty appearance and are formed in chains – unlike the urediniospores that are spiny and are produced on individual stalks. The chains of aeciospores are surrounded by a bell-like enclosure of fungal cells. The aeciospores are able to germinate on the cereal host but not on the alternative host (they are produced on the alternative host, which is usually barberry). They are carried by wind to the cereal host where they germinate and the germ tubes penetrate into the plant. The fungus grows inside the plant as a dikaryotic mycelium. Within 1–2 weeks the mycelium produces uredinia and the cycle is complete.[2]
Since the urediniospores are produced on the cereal host and can infect the cereal host, it is possible for the infection to pass from one year's crop to the next without infecting the alternate host (barberry). For example, infected volunteer wheat plants can serve as a bridge from one growing season to another. In other cases the fungus passes between winter wheat and spring wheat, meaning that it has a cereal host all year round. Since the urediniospores are wind dispersed, this can occur over large distances.[2] Note that this cycle consists simply of vegetative propagation – urediniospores infect one wheat plant, leading to the production of more urediniospores that then infect other wheat plants.
Puccinia graminis produces all five of thespore types that are known for rust fungi.[2]
Spores are typically deposited close to the source, but long-distance dispersal is also well documented[1] commonly out to hundreds of kilometres/miles.[30] The following three categories of long-distance dispersal are known to occur:[1]
This can occur unassisted (the robust nature of the spores allows them to be carried long distances in the air and then deposited by rain-scrubbing) or assisted (typically on human clothing or infected plant material that is transported between regions).[1] This type of dispersal is rare and is very difficult to predict.[1] This is especially known to rarely occur across thousands of km/mi from South Africa to Western Australia.[31][32]
This is probably the most common mode of long-distance dispersal and usually occurs within a country or region.[1]
This occurs in areas that have unsuitable conditions for year-round survival ofPuccinia graminis – typically temperate regions where hosts are absent during either the winter or summer.[1] Spores overwinter or oversummer in another region and then recolonise when conditions are favorable.[1]
A number of stem rustresistance genes (Sr genes) have been identified in wheat.[33] Some of them arose inbread wheat (e.g.Sr5 andSr6), while others have been bred in from otherwheat species (e.g.Sr21 fromT. monococcum) or from other members of the tribeTriticeae (e.g.Sr31 fromrye[22]: 15 andSr44 fromThinopyrum intermedium).
None of the Sr genes provide resistance to all races of stem rust. For instance many of them are ineffective against theUg99 lineage.[34] Notably Ug99 hasvirulence againstSr31, which was effective against all previous stem rust races. Recently, a new stem rust resistance geneSr59 fromSecale cereale was introgressed into wheat, which provides an additional asset for wheat improvement to mitigate yield losses caused by stem rust. Singh et al. (2011) provide a list of known Sr genes and their effectiveness against Ug99.[34]
There has been significant uptake of resistant wheat varieties amongEthiopian farmers since 2014[35][36] – a great deal of which is thanks toCGIAR andCIMMYT (the International Maize and Wheat Improvement Center).[37][36]
AlthoughSr5,Sr21,Sr9e,Sr7b,Sr11,Sr6,Sr8a,Sr9g,Sr9b,Sr30,Sr17,Sr9a,Sr9d,Sr10,SrTmp,Sr38, andSrMcN are no longer effective inLebanon,Sr11,Sr24, andSr31 still are which is diagnostic for the presence of various races of stem rust – but the complete absence of Ug99 specifically – from Lebanon.[38]
Discovered and found to provideUg99 resistance by Rouseet al., 2014.[22]: 24 However Ug99isolates fromSouth Africa andZimbabwe, both in 2010, already had virulence when retested against this new gene.[22]: 24 Both Rouse and Wesselset al., 2019 find the Ug99 resistance of cv. 'Matlabas' is probably due to this gene. Wessels finds it is present in less than 5% ofbreeding lines.[39]
Sr14 does not protect seedlings againstTTKSK[40] but does provide moderate resistance at later stages.[40] It is effective againstTTKST.[40]
There is considerable variation amongSr22 alleles, with some conferring resistance and some susceptibility.[41]
Sr27[42] is originally fromrye[33] (Imperial Rye),[43] now (as of 2021[update]) widely found intriticale and rarely in hexaploid wheat.[44] Located on the 3A chromosome arm,[42] originally from 3R.[45] Virulence has been observed in fieldPgs and in an artificialPgt × Pgs.[43] When successful,Sr27 is among the fewSrs that does not allow the underdevelopeduredinia and slight degree of sporulation commonly allowed by mostSrs.[33] Instead there arenecrotic orchlorotic flecks.[46]Pgt virulent on wheat with this gene was found inKenya in 1972.[45] Deployment in triticale inNew South Wales andQueensland, Australia, rapidly produced virulence between 1982 and 1984 – the first virulence on this gene in the world.[47][33][45] (This was especially associated with the cultivar Coorong.)[47][48] Therefore, CIMMYT's triticale offerings were tested and many were found to depend solely onSr27.[48][45] Four years later, in 1988, virulence was found inSouth Africa.Sr27 has become less common in CIMMYT triticales since the mid-'80s.[45]
Ug99 is virulent againstSr31, which was effective against all previous stem rust races.[34]
Anintrogression from a wild wheatAegilops tauschiiorthologous toMla inbarley. Confers broad resistance to multiple races includingUg99.[49][30]
Sr35 is anintrogression fromTriticum monococcum conferring some resistance.[30]AvrSr35 – aPgt gene so named because it was discovered causingavirulence onSr35 – is the ancestral allele to allPgt alleles that are virulent onSr35.AvrSr35 came first, followed by the selective pressure of widespread adoption ofSr35 wheat races, followed by the evolution of virulence onSr35 by way of nonfunctionalization mutations ofAvrSr35.[50]
Recently, a new stem rust resistance geneSr59 fromSecale cereale was introgressed into wheat, which provides an additional asset for wheat improvement to mitigate yield losses caused by stem rust.[34]
An NLR (or NB-LRR, orR gene) fromAegilops sharonensis, one of only threeresistance genes from that species.[51] Was discovered by Yuet al., 2017 and thenintrogressed intohexaploid by Milletet al., 2017.[51]Sr62encodes for a uniquetandem protein kinase which is composed ofdomains which are common among plants.[51] Yuet al., 2022[51]
Originally from the widespread Ethiopian 'Digalu'.[52] Resistant toUg99, susceptible to§ TKTTF.[52]
In the 1950s, theUnited States Air Force developed Operation Steelyard, a plan to drop wheat stem rust mixed with feathers over wheat farms in theSoviet Union. If the plan were enacted,Boeing B-29 Superfortress bombers would drop 500-poundM115 bombs over Soviet farms, with the intention of destroying up to 50% of the Soviet winter wheat harvest.[53]
Alone amongst cereals,rice is naturally immune to rusts. If a genetic source of this resistance could be identified,transgenic wheats with rice as thegene donor could be the future.[54][55]
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