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Oliver R.P., Tan K.-C. and Moffat C.S. (2016) Necrotrophic Pathogens of Wheat. In: Wrigley, C., Corke, H., and Seetharaman, K., Faubion, J., (eds.) Encyclopedia of Food Grains, 2nd Edition, pp. 273-278. Oxford: Academic Press.

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Necrotrophic Pathogens of Wheat

RPOliver, K-C Tan, and CS Moffat, Curtin University, Bentley, WA, Australia

ã 2016 Elsevier Ltd. All rights reserved.

Topic Highlights give information of trends over decades (Brennan and Murray,

1988, 1998). Table 2 lists estimates of current wheat disease • Diseases of wheat. losses in Australia. It can be seen that across all regions, TS is • Genetic analysis of resistance to tan spot and Septoria the major disease, currently costing more than all rusts com- nodorum blotch (SNB) necrotrophic effectors. bined. SNB is restricted to Western Australia where it ranks as Tan spot effectors. the second most costly wheat disease. STB has declined signif- • • SNB effectors. icantly, from an annual cost of $152 million in 1998 (Brennan • Lateral gene transfer, effector interactions, and new fungal and Murray, 1998) to the current figure of $1 million per pathogens. annum. Table 2 also lists estimates of potential losses if no disease control measures were carried out. The difference between the actual and potential is then ascribed differentially

Learning Objectives to breeding, fungicide, and cultural control methods.

The distribution and trends in the diseases are quite dis- • Appreciation of the relative importance of necrotrophic and tinct. SNB is almost exclusively located in Western Australia, other wheat diseases. with only sporadic reports from other regions. STB has sharply • An understanding of the term effector. declined in both the southern and western regions and has

Consideration of the nature of quantitative disease always been absent from the northern regions. TS is steadily • interactions. increasing in all regions although absolute levels are lower in • An understanding of the impact on plant breeding of the the southern region (Figure 1). effector model. The high levels of disease reported from TS and SNB was greeted with much skepticism in many quarters. The methodol- ogy of the report was based on questionnaires sent to regional

Diseases of Wheat plant pathologists. These data were combined with estimates of area and crop value to arrive at consolidated estimates. Valida- The diseases of wheat have received particular attention tion of the estimates has been provided by two recent reports throughout the ages because of their often devastating effect that used fungicide control to estimate disease losses (Oliver on this all-important crop. The full range of nematode, viral, et al., 2014; Salam et al., 2013). Salam et al. analyzed yield bacterial, oomycete, and fungal pathogens cause significant responses to fungicide under situations in which either or both diseases. Much international attention has been given to the TS and SNB were the only significant diseases. Not surprisingly, biotrophic rust diseases, but in some parts of the world, necro- three fungicide treatments gave higher yield gains than one trophic pathogens cause far higher losses and have proved (515 kg ha 1 versus 297 kg ha 1 averaged over the whole much harder to control by either genetic or chemical means. region). However, it is not clear if the three fungicide treatment

This article is primarily concerned with two major patho- schedule even gave complete control. Averaged over the entire gens of wheat from the order Pleosporales: Parastagonospora western region and using a figure of $263/tonne, this implies nodorum and Pyrenophora tritici-repentis. Some aspects of that the combined disease cost to WA growers is $300–600 m P. nodorum and P. tritici-repentis research have recently been per annum. Oliver et al. (2014) used a smaller number of reviewed, and these reviews contain detailed background that fungicide trials and estimated losses of 350 kg ha 1 to TS only. underpins our current knowledge (Faris et al., 2013; Lamari It therefore appears that the estimates in Brennan and Murray of and Strelkov, 2010; Oliver et al., 2012). $212 m per annum in Western Australia are of the right order Taxonomic instability of these and other related leaf blotch and may well be an underestimate. pathogens from the class Dothideomycetes has been an issue. The distribution of the pathogens in the rest of world is The current and past names of the pathogens and their diseases understudied. Lamari and Strelkov reviewed the literature in are summarized in Table 1 (Quaedvlieg et al., 2013). The three 2010 for TS (Lamari and Strelkov, 2010). There are widespread diseases, Septoria nodorum blotch (SNB), tan spot (TS), and reports that the range of TS is increasing in northern and Septoria tritici blotch (STB), coexist in many places and have western Europe. In Germany, TS is consistently comparable likely been confused and misidentified at times. with STB and in some years is the most damaging disease (M. Disease loss assessments are rarely carried out and subject Weigand, personal communication). In Denmark, TS is fre- to many caveats and exceptions, despite their obvious impor- quently observed (Jørgensen and Olsen, 2007). In the United tance for farmers, breeders, agrochemical companies, Kingdom, TS is now frequent and is ranked third behind STB researchers, and funding agencies. More frequently, pathogens and powdery mildew (J. Thomas, personal communication). are ranked in terms of importance. One of the more reliable The consistent pattern is that TS is strongly associated with and recent assessments of wheat disease losses has been carried limited tillage methods and wheat-on-wheat rotations. SNB is out in Australia (Murray and Brennan, 2009). Previous studies only reported as an occasional disease in Germany, but it is

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274 AGRONOMY OF GRAIN GROWING | Necrotrophic Pathogens of Wheat

Table 1 Nomenclature of wheat leaf blotch pathogens and their diseases

Preferred pathogen name Pathogen synonyms Order Preferred disease name Disease synonyms

Parastagonospora Stagonospora nodorum Pleosporales Septoria nodorum blotch Stagonospora nodorum nodorum Phaeosphaeria nodorum (SNB) blotch Leptosphaeria nodorum Glume blotch Septoria nodorum Pyrenophora tritici- Drechslera tritici-repentis Pleosporales Tan spot (TS) Yellow spot repentis Helminthosporium tritici-repentis Yellow leaf spot Zymoseptoria tritici Septoria tritici Capnodiales Septoria tritici blotch (STB) Septoria leaf blotch Mycosphaerella graminicola Septoria tritici blotch

Table 2 Potential and actual losses to selected wheat diseases in Australia

Contribution to control (potential minus actual) from breeding, fungicides, Disease Rank Actual/AUD million Potential/AUD million and cultural methods (AUD million)

Breeding Fungicide Cultural TS 1 212 676 200 108 155 SNB 3 108 230 36 35 51 STB 27 1 21 15 4 1 Stripe rust 2 127 994 431 359 78 Stem rust 8 8 478 438 8 24 Leaf rust 11 12 197 152 17 16

Data from Murray, G.M., Brennan, J.P., 2009. Estimating disease losses to the Australian wheat industry. Australasian Plant Pathology 38, 558–70.

9 8

7 6

5 TS 4 SNB 3 STB 2 1

0 1988 1998 2008 1988 1998 2008 1988 1998 2008

Northern Southern Western

Figure 1 Average annual disease losses to SNB, TS, and STB in the northern (Queensland and northern NSW), southern (southern NSW, Victoria, Tasmania, and South Australia), and western (Western Australia) cropping regions. Figures are % losses to each disease. Data from Murray, G.M. and Brennan, J.P., 2009. The current and potential costs from diseases of wheat in Australia.

common in parts of France (M. LeBrun, personal communica- (Oliver et al., 2014). This is not due to baseline levels of fungi- tion), western counties of England (S. Gurr, personal cide sensitivity, but rather to poor field performance (Beard communication), and Norway (M. Lillemo, personal commu- et al., 2009; Bhathal et al., 2003; Tormen et al., 2013). There nication). It seems that SNB is most apparent in regions with have been reports of evolved resistance to QoI fungicides (Blixt intense rain showers. Rain splash of spores is required for et al., 2009; Reimann and Deising, 2005). Overall, there is every progression of SNB throughout the canopy. It is clear that the reason to pursue the breeding of disease-resistant cultivars. incidence of these diseases and their economic impact need further study. Fortunately, molecular diagnostic tools are read- ily available (Oliver et al., 2008). Genetic Analysis of Resistance to TS and SNB

A range of fungicides are available for SNB and TS. The Necrotrophic Effectors primary modes of action in use are demethylation inhibitors, quinone outside inhibitors (QoIs), and succinate dehydrogenase Our understanding of the interaction between wheat and the inhibitors. In general, control levels in the field are modest TS and SNB pathogens has been revolutionized by the

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AGRONOMY OF GRAIN GROWING | Necrotrophic Pathogens of Wheat 275 recognition of the importance of necrotrophic effectors (NEs). selective’ toxins (HSTs). The reciprocal relations were revealed The dominant theory in the genetics of host–pathogen inter- when isolates of the pathogens that failed to produce these actions is, of course, the gene-for-gene (GFG) hypothesis HSTs were compared with the HSTþstrains. (Keen, 1990; van der Biezen and Jones, 1998). In recent years, When the HSTs were biochemically characterized, they this model has been refined to take into account non-host were shown to include polyketides and non-ribosomally resistance and the presence of PAMPs (pathogen-associated synthesized peptides and proteins. All are now called NEs molecular patterns) (Thomma et al., 2011). The GFG theory (Oliver and Solomon, 2010). The reciprocal relationships explained adequately the interaction of biotrophic pathogens have allowed the definition of wheat differential lines that (especially rusts and powdery mildews) and their hosts and exhibit specific sensitivity to particular NE and thus suscepti- provided a practical framework for breeding disease-resistant bility to particular isolates of the pathogens. cultivars, albeit that those cultivars tended to break down after a few years. However, the great majority of pathogens do not conform neatly to the GFG hypothesis, and this is especially true for pathogens that do not elaborate a haustorium and that Tan Spot are variously described as necrotrophs or hemibiotrophs

(Oliver and Ipcho, 2004).ThisisthecaseforSNBandTS. The TS pathogen P. tritici-repentis is included in this group of One of the predictions of the GFG hypothesis is that isolates pathogens that secrete NEs. Work starting prior to 1990 of the pathogen should vary in clear ways in their interactions defined three NEs, called ToxA, ToxB, and ToxC (reviewed in with different cultivars of the host. Such variation in GFG Lamari and Strelkov, 2010). This in turn allowed the definition systems is described as variation in ‘virulence’ and is controlled of 8 races of the pathogen, representing all possible combina- by avirulence genes. Isolates of pathogens should cause recip- tions of the 3 NEs. rocal levels of disease on different cultivars of a host: the so- ToxA is fully characterized. The monomorphic gene is pre- called quadratic check. Pathologists and breeders can then sent in about 80% of the world’s isolates (Friesen et al., 2006). develop differential lines that contain different resistance The gene encodes a small protein that induces a strong necrotic genes which can be used to monitor the virulence profile of response in wheat lines carrying the gene Tsn1 (Faris et al., the pathogen. 2010) on chromosome 5BL. Tsn1 encodes a protein with sim- In the case of biotrophic pathogens, the development of ilarity to disease resistance genes in biotrophic interactions. differentials was an essential prerequisite to the molecular clon- The interaction of Avr genes and resistance genes in biotrophic ing of the avirulence genes (Dodds et al., 2009). The conun- diseases, and interaction of HSTs and sensitivity genes in drum of why pathogens should produce gene products that necrotrophic interactions, affirms the commonality at the rendered them avirulent was solved as the (often subtle) positive base of plant pathogen interactions and justifies the general attributes of these genes were revealed (Koeck et al., 2011). term ‘effector.’ In the case of necrotrophic (and non-haustorial) patho- Wheat lines that are sensitive to ToxA are significantly more gens,the definition of clear reciprocal relationships between susceptible to ToxA-producing TS isolates (Friesen et al., 2003). pathogen isolates and host cultivars was rarely observed. It was In Australia, ToxA sensitivity is strongly associated with TS much more common to observe tonic relationships where severity (Table 3). Despite this clear relationship, markers isolates differed in aggression on all cultivars of the host. that have been available for Tsn1 were not in use by breeders. Some isolates were generally aggressive and some were less Since 2009, our laboratory has been supplying preparations of aggressive, with no significant reciprocal relationships. the ToxA protein expressed in E. coli to Australian wheat However, one group of pathogens did show reciprocal breeders. Enough ToxA to treat 30000 plants per annum has relationships: examples include species in the genera Cochlio- been delivered. Breeders use a simple infiltration test to iden- bolus, Alternaria, and Pyrenophora (Wolpert et al., 2002). This tify sensitive wheat lines (Figure 2). The test is applied to group of pathogens includes those that secreted ‘toxins’ in the primary germplasm sources and to lines throughout the breed- culture filtrate. Infiltration of the toxic preparations into culti- ing process. Plants can be grown in growth chambers, in glass vars of the hosts produced strong necrotic reactions in some houses, or in the field. Breeders can treat about 1000 plants a host plant cultivars and no responses in others. The necrotic day and can detect sensitive plants within 3–4 days. Such reactions resembled the symptoms produced by the pathogens. plants can be discarded at that stage. This process is quicker These toxins therefore became known as ‘host-specific’ or ‘host- than marker-assisted selection using leaf DNA. Since the

Table 3 Influence of NE sensitivities on field scores of current Western Australian wheat cultivars scored for tan spot and septoria nodorum

Difference in average disease score of sensitive Disease NE and insensitive lines Closest wheat marker

Tan spot ToxA 2.85 Tsn1; Xfcp623 Septoria nodorum ToxA 0.357 blotch Tox1 0.109 psp3000, fcp618, fcp624 Tox3 0.484 Cfd20, gwm234, barc130, cfd18, hbg337, gwm190

Based on Tan et al. (2014), Waters et al. (2011), and Moffat et al. (unpublished). Wheat cultivar field scores were converted to a 9-point scale (1¼very susceptible to 9¼immune). The average score of insensitive lines for each NE and disease was subtracted from the scores for the sensitive lines.

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276 AGRONOMY OF GRAIN GROWING | Necrotrophic Pathogens of Wheat

Figure 2 Infiltration of wheat lines with NE. (a) Infiltration with a needleless syringe. (b) Scoring of necrosis after a week.

cloning of Tsn1, perfect markers are also available and can be progress was made. QTL mapping for disease was undertaken used to select seeds for planting. and uncovered numerous loci, but map location precision and ToxB is also a small, secreted protein that is present in varying effect size were both low. Hence, to our knowledge, no markers copy numbers in isolates of TS (Amaike and Strelkov, 2006). were actively used by breeders.

ToxB sensitivity is encoded by the gene Tsc2 residing on 2BS There was no evidence that P. nodorum produced NE until

(Friesen and Faris, 2004) and confers additional disease suscep- 2004, when Liu et al. partially characterized Tox1 and the tibility. Isolates expressing ToxB are less common than those corresponding wheat sensitivity locus Snn1 (Liu et al., 2004). expressing ToxA (they are absent from Australia (Antoni et al., However, it took another 8 years to identify and clone Tox1 2010 )) and so the exploitation of this NE for breeding purposes (Liu et al., 2012). This finding alerted researchers to the possi- has not so far been justified. Should ToxB-expressing isolates be bility that P. nodorum, like other Pleosporales such as Alter- detected, the expressed protein could be used to distinguish naria, Cochliobolus, and Pyrenophora, might be an NE-based sensitive and insensitive wheat lines in the same way as has pathogen. When the P. nodorum genome sequence was been done for ToxA. obtained in 2005, a primary target was the identity of Tox1. ToxC is less well characterized (Effertz et al., 2002). It However, with no further information on the structure of Tox1, induces chlorosis and does not appear to be a protein. Sensi- it was the gene ToxA that stood out. Although ToxA was mis- tivity is conditioned by the gene Tsc1 on 1AS. So far, ToxC has annotated in the original P. nodorum genome sequence, RT- not been used in breeding efforts. PCR confirmed its structure as highly similar to that found in The three known NEs – ToxA, ToxB, and ToxC – cannot be P. tritici-repentis. As the physical properties of ToxA were differ- the whole story for TS. QTL mapping of disease reactions in ent from those known for Tox1, it was already clear that many wheat populations uncovers at least a dozen loci not P. nodorum, like P. tritici-repentis, was a pathogen possessing reacting to the (semi)purified effectors (Faris et al., 2013). more than one NE. Some of these QTL may represent sensitivity loci to so far Functional genomic tools for P. nodorum had been devel- undiscovered effectors. However, some of these QTL encode oped in the 1980s (Cooley et al., 1988; Solomon et al., 2003) dominant resistance, and others broad spectrum resistance, unlike P. tritici-repentis for which knockouts have only recently suggesting that other types of interactions are involved. been reported (Moffat et al., 2014). These genomic tools were

used to demonstrate the role of ToxA and Tsn1 in SNB (Friesen

et al., 2006; Liu et al., 2006). Gene deletion of ToxA reduced disease levels on ToxA-sensitive wheat lines, and ToxA expres- Septoria nodorum Blotch sion in an avirulent P. nodorum isolate conferred virulence. Unlike P. tritici-repentis, where ToxA is monomorphic, 10

forms of the protein exist in P. nodorum. These proteins exhibit Breeding for resistance to P. nodorum had been a priority in Europe until the 1990s and has remained so in Western Aus- differing levels of necrosis varying by a factor of about 30 tralia to this day. Early breeding efforts were based on prag- (Tan et al., 2012). It also appears that the gene(s) is expressed matic and laborious field scoring of breeding lines and steady at different levels in different isolates (Faris et al., 2011).

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AGRONOMY OF GRAIN GROWING | Necrotrophic Pathogens of Wheat 277

Furthermore, about 60% of a worldwide collection of (2) purification of NE; (3) identification of novel disease and P. nodorum isolates lack the ToxA gene altogether (McDonald NE QTL; and (4) marker validation and NE/marker delivery to et al., 2013 ). ToxA is present in nearly all isolates from Australia breeders. but is rare in isolates from China, Europe, and North America.

Thus, at least four factors account for the variable relationship Lateral Gene Transfer, Effector Interactions, between the presence of Tsn1 and SNB severity: the absence of and New Fungal Pathogens the gene in many isolates, the variable expression of the gene, the variable activity of the isoforms, and the presence of several Compelling evidence exists that the gene encoding ToxA was otherimportant NE interactions. acquired laterally (i.e., from a different species) by P. tritici- The deletion of the ToxA gene facilitated the isolation and repentis (Friesen et al., 2006). The disease went unnoticed by characterization of further NE. Several tools were used to identify the pathology community until 1941. TS has since become one Tox3 and later Tox1. Differential wheat lines with unique NE of the major pathogens in agriculture. A DNA region of at least sensitivities were propagated. Further strains of the pathogen 11 kb but more likely 145 kb (Manning et al., 2013) within the were chosen because of their differing NE profile and were P. tritici-repentis genome is highly similar to a genomic region sequenced. It was clear that these NEs (unlike ToxA) were in the presumed ToxA donor, P. nodorum. The ToxA gene is secreted into the culture filtrate and so protein chromatography monomorphic in the TS pathogen but highly polymorphic in was used to purify the NE. Mass spectrometry was used to identify P. nodorum, consistent with a recent history in TS. The cloning proteins in the most active fractions. Transcriptomics was used to of Tsn1 demonstrated the subtlety of these necrotrophic path- refine the annotation of genes within the genome sequences and ogens. ToxA is recognized (in a manner not yet clear) by Tsn1 to identify genes expressed in the first few days of infection when and induces a defense response. Unlike biotrophic interac- cytological studies indicated the activity of NE. Candidate genes tions, the necrosis promotes infection. The success of ToxA- were expressed in yeast and E. coli so as to acquire adequate containing TS suggests that the acquisition of a gene that quantities of single pathogen proteins. These studies identified induces necrosis in a host can be a very successful strategy for Tox3 and Tox1 (Friesen et al., 2008; Liu et al., 2012). a pathogen that can tolerate the defense response. However, Like ToxA in P. nodorum, Tox1 and Tox3 are present in the use by breeders of NE is expected to negate the advantage multiple forms and the genes are absent in some isolates accrued by the presence of these genes. Effector-assisted breed- (absent in 16% for Tox1 and 39% for Tox3). It is not yet ing thus promises to provide a sustained accrual of resistance in clear whether the different forms of Tox1 and 3 have different new cultivars leading to higher yields and reduced risk of activities or if the genes are expressed at different levels. fungicide resistance. Yet we must remain vigilant for new With the three NEs in hand, it was possible to evaluate the strains of the pathogen and even new species that evolve role of each in the wheat–P. nodorum interaction in Western in situ or arrive from overseas. Australia (Table 3). It was also possible to ablate Tox1 and Tox3 and thereby evaluate the virulence of strains lacking these NEs and to test the culture filtrate for sensitivity to NE other than ToxA, Tox1, and Tox3 (ToxA is not secreted in culture filtrates). Exercises for Revision

The results present a complex but not unexpected picture (Tan How reliable are the research methods used to estimate disease et al.,2014 ). Firstly, deletion of Tox1 and Tox3 reduced disease levels in seedling trials of cultivars sensitive to Tox1 and Tox3, data loss? Who provides the data and what biases might such performed in (the required) GM-containment conditions. Sec- people display? How are disease loss estimates used by (a) ondly, it was clear that there were no current cultivars that were farmer, (b) agrochemical industries, (c) plant breeders, (d) insensitive to all three NEs. Breeding of such a variety is a research funders, and (e) researchers? current high priority. Thirdly, it was clear that no single NE • Revise methods of QTL mapping. was a dominant factor in susceptibility, unlike the case for TS • Revise methods for map-based cloning as applied to wheat. and ToxA, and so no simple relationships exist. Instead, it How do researchers deliver markers in plant breeding of a • appears that sensitivity to any of the NE is sufficient to cause crop such as wheat? a significant level of disease. Fourthly, many cultivars were • How do breeders use markers in plant breeding of a crop sensitive to NE not present in the culture filtrate produced by such as wheat? the strain lacking ToxA, Tox1, and Tox3. We conclude that breeding for disease resistance to SNB can adopt a new strategy. In general, the order of importance in NE Exercises for Readers to Explore the Topic Further is Tox3 >ToxA>Tox1. Cultivars that are insensitive to Tox3 are very rare. However, there appears to be no obvious reason why Which omics technologies are relevant for plant pathologists? this is the case; such cultivars had no obvious deleterious properties when compared to Tox3-insensitive lines in field • Compare breeding for disease resistance to biotrophs and trials (Oliver et al., 2014). The first goal is to breed cultivars necrotrophs. lacking sensitivity to all three NEs. We predict that such lines What evolutionary pressures would effector-based breeding • would be at least as resistant as the current most resistant ones. place on necrotrophic pathogens? Numerous QTLs for SNB disease have been reported that are • How should fungicides be used by farmers given the pro- not due to the known NE. Hence, the research strategy involves gress in breeding for resistance to biotrophs and (1) disease assessment of strains lacking ToxA, Tox1, and Tox3; necrotrophs?

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Encyclopedia of Food Grains, (2016), vol. 4, pp. 273-278