Available online at www.sciencedirect.
com
Safeguarding wheat yields from cereal fungal invaders in
the postgenomic era
Francesca Minter and Diane GO Saunders
Wheat production is under constant threat from pests and
pathogens, with fungal foliar diseases causing considerable
annual yield losses. However, recent improvements in genomic
tools and resources provide an unprecedented opportunity to
enhance wheat’s resilience in the face of these biotic constraints.
Here, we discuss the impact of these advances on three key
areas of managing fungal diseases of wheat: (i) enhancing the
abundance of resistance traits available for plant breeding, (ii)
accelerating the identification of novel fungicide targets and (iii)
developing better tools for disease diagnostics and surveillance.
Embracing these new genomics-led technological innovations in
crop protection could revolutionise our wheat production system
to improve resilience and prevent yield losses.
Address
John Innes Centre, Norwich NR4 7UH, United Kingdom
Corresponding author: Saunders, Diane GO (Diane.Saunders@jic.ac.uk)
Current Opinion in Microbiology 2023, 73:102310
This review comes from a themed issue on Environmental
Microbiology
Edited by Jacob Malone and Cara Haney
For complete overview of the section, please refer to the article
collection, “Environmental Microbiology”
Available online 3 April 2023
https://doi.org/10.1016/j.mib.2023.102310
1369–5274/© 2023 The Authors. Published by Elsevier B.V. This is an
open access article under the CC BY license (http://
creativecommons.org/licenses/by/4.0/).
Introduction
Wheat is one of our oldest and most precious food crops.
It is the most widely grown cereal crop worldwide, ser­
ving as a staple food for 35% of humankind and pro­
viding over 20% of the calories and protein consumed
daily [1]. By 2031, wheat consumption is expected to
increase by 11%, but production area is set to increase by
only 3% [2]; thus, protecting wheat yields is crucial for
global food security and economic stability. However,
recent environmental, health and sociopolitical crises
have highlighted the fragility of global food production
systems [3]. For instance, the ongoing conflict in Uk­
raine has severely disrupted global wheat supplies, as
this country is the world’s fifth largest wheat exporter
www.sciencedirect.com
]]
]]]]]]
]]
[4,5]. Moreover, pests and microbial pathogens have
threatened wheat production since the dawn of agri­
culture and are currently estimated to be responsible for
average annual wheat yield losses of 21.5% [6].
Integrated approaches to disease management — using
resistant cultivars, routine application of pesticides and
agronomic practices to limit disease spread — help cir­
cumvent crop losses from biotic threats. However, the slow
pace of conventional breeding (at least 5–7 years from the
identification of new resistance traits to their deployment
in the field) [7] and the ability of pests and pathogens to
rapidly evolve and overcome introduced resistance and/or
develop tolerance to chemical treatments pose constant
challenges to disease management [8]. In addition, the
active ingredients in many pesticides pose an environ­
mental risk due to their effects on nontarget organisms.
Indeed, the broad-spectrum, nonsystemic fungicide
Chlorothalonil, which was used to control a wide range of
fungal diseases in crops, was banned by the European
Commission in 2019 due to health and environmental
concerns. Tebuconazole, which is particularly effective
against the wheat rusts (among others), is currently being
assessed for reauthorisation in Europe [9]. There is hope,
however. A flurry of newly available genomic tools and
resources provide a pathway to enhance the abundance of
resistance traits available for plant breeding, accelerate the
identification of pesticide targets and improve disease
monitoring. Here, we discuss these new tools, focusing on
advances that could markedly enhance our ability to sus­
tainably manage fungal foliar diseases, which lead to yield
losses of up to 50% in wheat [10].
The shifting landscape of resistance breeding
The most effective means of controlling wheat diseases
has been the deployment of varieties resistant to infec­
tion through the integration of partial or race-specific
resistance (R) genes. The success of the Green
Revolution in the mid-to-late 20th century exemplifies
this approach, where breeding durable wheat stem rust
resistance drove the disease to near insignificance in
many regions worldwide [11]. However, the emergence
of the Ug99 race of the wheat stem rust pathogen
(Puccinia graminis f. sp. tritici, Pgt) in 1998 in Uganda
rendered up to 80% of the world’s wheat varieties again
vulnerable to stem rust infection [12], emphasising the
need to continuously expand the R-gene inventory at
our disposal. Novel genomics techniques for cloning R
genes, including those based on variations in R- gene
Current Opinion in Microbiology 2023, 73:102310
2 Environmental Microbiology

Figure 1

Phenotyping Selection Enrichment Data analysis Candidate validation

Fungal spores R genes NLR reads
NLR
baits

High-throughput sequencing
de novo assembly of wild-type NLRs
Select/design
gDNA NLR-enriched EMS mutants
DNA Mapping to wild-type reference NLRs mutants
R genes Susceptible
gDNA Identify NLRs with conserved variants
in resistant cultivars/mutants
Resistant Resistant Enrichment
S genes Resistant
RNA dual RNA-seq data
polyA-RNA
Susceptible Compare host gene expression profiles
between resistant & susceptible cultivars
S genes RNA
polyA-RNA
Identify host genes differentially Transgenics
Resistant
expressed in susceptible cultivars
Wheat varieties Infected
Susceptible
and/or mutants plants

Current Opinion in Microbiology

Genomics-based approach for identification and validation of resistance (R) and susceptibility (S) genes. Following phenotypic characterisation of
disease susceptibility of wheat varieties and/or mutants with the pathogen of interest (‘Phenotyping’), those displaying resistant or susceptible
phenotypes are selected (‘Selection’). Next, for R-gene identification, genomic DNA (gDNA) is extracted from wheat varieties and/or mutants of
interest and a sequence bait library used to enrich for gDNA-encoding NLR R genes following variations in the RenSeq strategy. Alternatively, for S
genes, RNA is extracted from wheat varieties and/or mutants infected with the pathogen of interest and RNA enriched for poly(A) transcripts
(‘Enrichment’). High-throughput sequencing is conducted and the resulting NLR reads or dual RNA-seq data processed to identify R- and S-gene
candidates, respectively (‘Data analysis’). Publicly available EMS-induced wheat disruption mutants for the gene of interest are then selected from
public databases or transgenic mutants developed and used for subsequent validation (‘Candidate validation’).

sequence capture (RenSeq) [13] (Figure 1), have ex­
ponentially increased the number of annotated R genes
available for deployment.
Whereas traditional positional cloning is possible only
when a single R gene exists in a genetic background
susceptible to the pathogen of interest, these genomics-
based approaches have been particularly fruitful for
identifying R genes. For example, the locus responsible
for the first powdery mildew R gene described in wheat,
Pm1a, had long remained elusive due to restricted ge­
netic recombination in the area, but was recently cloned
by combining mutagenesis and RenSeq [14]. Here, a
sequence bait library was used to enrich for nucleotide-
binding, leucine-rich repeat (NLR) R genes from six
independent Pm1a disruption mutants. Following Illu­
mina sequencing and de novo assembly of the R-gene
complement, single-nucleotide polymorphisms (SNPs)
were found in a single NLR gene candidate that segre­
gated with Pm1a resistance, with Pm1a identity subse­
quently confirmed through stable transformation [14].
This exemplifies how such genomic tools can sig­
nificantly enhance R-gene identification.
But beyond the current wheat R-gene portfolio, genomic
approaches can also boost access to the vast genetic re­
sources that wild wheat relatives have to offer. For ex­
ample, a genomic region conferring resistance against Pgt
was identified in Aegilops sharonensis in 2017 using a
genome-wide association study (GWAS) [15]. Owing to
advancements in genomics, a high-quality Ae. sharonensis
genome was generated only four years later and the re­
sponsible gene, Sr62, cloned, with the tandem protein
kinase introduced into a susceptible wheat line, where it
conferred resistance to a number of Pgt races [16]. More
recently, the application of k-mer-based GWAS has fur­
ther expedited the hunt for novel R genes beyond cano­
nical NLRs in wild relatives [17]. For instance, several
discrete genomic regions that contained a diversity of
gene classes were recently identified and linked to dis­
ease resistance in Ae. tauschii by applying a k-mer-based
GWAS analysis to 242 sequenced accessions [18]. Using
such genomic-based approaches to embrace the plentiful
supply of R-gene resources in these wild wheat relatives,
will continue to inflate the diversity of R-gene archi­
tectures in the ever-expanding R-gene catalogue.
In parallel with advances in R-gene cloning methodology
over the past decade, we have also witnessed the tre­
mendous potential of precision genome editing and ge­
netic engineering to alter the landscape of resistance
breeding. R genes are typically introgressed into elite
wheat varieties through conventional breeding, which is
laborious and can lead to the cointegration of deleterious
genes through linkage drag [19]. Today, conventional
breeding goals can be accelerated via speed breeding,
where the photoperiod and temperature conditions are
tightly controlled to reduce generation times and

Current Opinion in Microbiology 2023, 73:102310 www.sciencedirect.com


expedite the resistance breeding pipeline [20]. In addi­
tion, since such conventional breeding often involves the
introduction of a single R gene, modification of the
corresponding pathogen avirulence (Avr) effector protein
can easily lead to a loss of recognition [19]. Genome
engineering has the potential to substantially expedite
the precise introgression of R genes into elite wheat
varieties singly or in tandem. For instance, a cassette of
five R genes was recently introduced into wheat through
genetic engineering, with four R genes remaining func­
tional against Pgt [21]. An alternative strategy to stacking
multiple R genes, rational design, holds great potential
for expanding single R-gene recognition spectra. For
instance, using protein structure-guided engineering of
the rice Pikp R gene, mutations targeted within the
heavy metal-associated domain expanded recognition to
multiple variants of the corresponding rice blast (Mag­
naporthe oryzae) AVR-Pik effector [22]. Another inspiring
approach as we look to the future involves integrating
nanobodies into an R-gene chassis to recognise con­
served pathogen target proteins to induce cell death,
which holds great promise as a mechanism for rational
engineering of disease resistance [23]. Such innovative
molecular approaches to enhancing R-gene recognition
specificity or repurposing an existing R-gene chassis
could drastically extend the utility of known R genes in
the resistance breeding arsenal.
Beyond the resistance-gene catalogue
An alternative strategy to deploying dominant R genes,
with potentially greater durability, is to identify and
disrupt host genes targeted by pathogens to facilitate
compatibility. Pathogens target host gene products
termed susceptibility (S) factors to support their own
establishment or colonisation and/or to modulate host
defence responses. The disruption of S genes can confer
a fundamental loss of host susceptibility [24]. One classic
example is loss of function of the mildew-resistance locus
(Mlo) in barley, which enhances powdery mildew re­
sistance [25]. The nonrace-specific resistance conferred
by the loss of Mlo has led to its widespread manipulation
in breeding pipelines since the 1980s [26]. Although the
disruption of S genes is attractive, this approach can
sometimes have deleterious effects on yield or plant
growth [24]. Hence, a large catalogue of S factors to test
is needed; the recent burst of dual RNA-seq studies of
the host–pathogen interface has started to address this
gap (Figure 1). Once candidate S factors are revealed,
methods are now available for their rapid validation,
including the analysis of publicly available ethyl me­
thanesulphonate (EMS)-induced disruption mutants for
bread and durum wheat [27] and/or the generation of
transgenic mutants. For example, a recent search for
differentially expressed genes in Puccinia striiformis f. sp.
tritici (Pst)-infected wheat leaves uncovered the S gene
Puccinia striiformis-induced protein kinase 1 (TaPsIPK1).
www.sciencedirect.com
Protecting wheat from fungal invaders Minter and Saunders 3
The Pst effector protein PsSpg1 was shown to bind to
TaPsIPK1, inducing its localisation to the nucleus and
phosphorylation of the transcription factor TaCBF1d,
thereby promoting the transcription of downstream
susceptibility-related genes [28]. By understanding the
detailed role of S genes, those with minimal impact on
plant physiology and development can be prioritised for
selection in plant resistance breeding.
Another target for resistance breeding is genes that en­
code immune regulators, as their disruption can prime
immune responses. Comparative genomics studies have
begun to accelerate the identification of these genes. For
instance, transcriptome analysis of wheat varieties with
different levels of susceptibility to Pst uncovered the
branched-chain amino acid aminotransferase gene,
TaBCAT1, encoding a positive regulator of wheat rust
susceptibility. Disrupting TaBCAT1 led to the upregu­
lation of salicylic-acid and pathogenicity-related genes,
resulting in reduced susceptibility to both Pst and Pgt
[29]. A comparative genomic analysis to identify the
WRKY transcription factor gene family in wheat identi­
fied TaWRKY10 as a regulator of jasmonic acid re­
sponses; silencing TaWRKY10 increased plant resistance
to Zymoseptoria tritici [30]. These examples highlight
how emerging genomics-led insights into fungal patho­
genicity mechanisms can also reveal new, alternative
targets for manipulation in resistance breeding.
Streamlining fungicide development through
toxicogenomics
Comparative genomic studies have also created a wealth
of insights into specific gene families linked to fungal
pathogenesis, with great potential for uncovering novel
pathogen-specific fungicide targets. Most currently de­
ployed fungicides were identified by either a natural
product-based lead discovery or random testing of li­
braries of compounds against important commercial
fungal threats [31]. The current registered fungicides
target universal cellular processes, including the in­
tegrity of the plasma membrane, respiratory func­
tions and the microtubule cytoskeleton [8]. The rapid
increase in sequenced phytopathogen genomes will fa­
cilitate the identification of genes that are conserved
across pathogenic organisms and could prove promising
as new fungicide targets. However, once a new active
ingredient has been identified, the complex and costly
road to registration begins.
The emergence of the transdisciplinary field of 'tox­
icogenomics' — the study of the cell’s response to a
toxicant at the genome, transcriptome, proteome and
metabolome levels [32]— holds great promise for ac­
celerating off-target risk assessments of fungicides.
Using an omics-based approach, mechanistic information
can be rapidly generated for nontarget organisms,
Current Opinion in Microbiology 2023, 73:102310
4 Environmental Microbiology
potentially enhancing confidence in novel active sub­
stances [33]. For instance, analysis of signatures from a
large genomic database containing gene expression
profiles for over 630 chemicals identified the mode and
mechanism of action of three structurally similar agri­
chemical triazoles (myclobutanil, propiconazole and
triadimefon) that led to hepatotoxicity in a rodent model
without the need for additional experimentation [34].
The continued expansion of omics databases for non­
target fungi and plants could widen the utility of tox­
icogenomics in agriculture for fast-tracking our
understanding of the environmental risks of emerging
chemical compounds [35].
Safeguarding resistance traits and fungicide
performance
The evolution of pathogen resistance is a continuous and
costly challenge to fungicide efficacy and the sustain­
ability of precious R-gene resources. Hence, widespread
monitoring for the evolution of fungicide resistance is
essential to guide application regimes and to potentially
extend a compound’s lifespan [36]. Ensuring that R
genes remain effective in the field also requires careful
monitoring of the corresponding pathogen Avr proteins
to rapidly identify any modifications that could indicate a
gain in virulence. Although Avr gene discovery has
generally lagged behind R-gene discovery for many of
the most destructive fungal pathogens, comparative
genomics has started to hasten Avr gene identification.
For instance, such studies led to the identification of the
first Avr proteins in Pgt (AvrSr50, AvrSr35 and AvrSr27)
[37–39] and significantly expanded the collection of
known Avr genes for the wheat powdery mildew pa­
thogen (Blumeria graminis f. sp. tritici), among others
[40]. As Avr resources continue to expand, the virulence
spectrum of pathogen isolates can be carefully mon­
itored in existing pathogen surveillance systems to gauge
the effectiveness of deployed R genes.
Large-scale population genetic studies of pathogens can
also provide insights into the mechanisms of resistance
breakdown to guide the selection of durable R genes for
introgression. For instance, a detailed population ge­
netics study of B.g. tritici showed that the durability of
the Pm17 R gene in wheat was significantly impeded by
the presence of the corresponding virulent AvrPm17
effector variants that predated Pm17 deployment [41].
With the development of portable, genomic-based di­
agnostics and surveillance techniques for complex fungal
pathogens, our ability to routinely monitor Avr mod­
ifications and the emergence of potential fungicide re­
sistance is accelerating. This includes the Mobile And
Real-time PLant disEase diagnostics approach, which
uses the portable MinION nanopore sequencer and
targeted resequencing in near-real time to monitor
changes in a Pst population [42]. The integration of
Current Opinion in Microbiology 2023, 73:102310
genomic-based diagnostic and surveillance tools into
smart farming strategies will help accelerate our re­
sponses to these ever-evolving threats to plant health,
safeguarding R-gene resources and fungicide efficacy.
Conclusions and future trends
As our understanding of plant–pathogen biology con­
tinues to accelerate in the postgenomic era, the avail­
ability of new resistance traits will markedly increase.
The use of genomic-led approaches in pesticide target
discovery and primary risk assessment could enhance
the breadth of compounds at our disposal whilst poten­
tially reducing off-target risks. When considered along­
side recent advances in pathogen surveillance
techniques, these monumental genomics-based ad­
vances have the potential to greatly enhance the resi­
lience of our wheat production system and reduce the
scale of yield losses currently caused by pests and pa­
thogens in high-production agricultural settings.
Data Availability
No data were used for the research described in the ar­
ticle.
Declaration of Competing Interest
The authors declare that they have no known competing
financial interests or personal relationships that could
have appeared to influence the work reported in this
paper.
Acknowledgements
F.M. is supported by the Biotechnology Biological Sciences Research
Council (BBSRC) Norwich Research Park Biosciences Doctoral Training
Partnership (BB/M011216/1). D.G.O.S. is supported by a European
Research Council (no. 715638) grant, the Biotechnology Biological Sciences
Research Council Institute Strategic Programmes BB/P012574/1 and BB/
P016855/1 and the John Innes Foundation.
References and recommended reading
Papers of particular interest, published within the period of review, have
been highlighted as:
•• of special interest
•• of outstanding interest
1. IDRC: Facts and Figures on Food and Biodiversity vol. 2022, IDRC
Communications, International Development Research Centre;
2010.
2. OECD/FAO. OECD-FAO: Agricultural Outlook 2022–2031. OECD
Publishing; 2022.
3. Bentley A: Broken bread - avert global wheat crisis caused by
invasion of Ukraine. Nature 2022, 603:551.
4. Bentley AR, Donovan J, Sonder K, Baudron F, Lewis JM, Voss R,
Rutsaert P, Poole N, Kamoun S, Saunders DGO, et al.: Near- to
long-term measures to stabilize global wheat supplies and
food security. Nat Food 2022, 3:483-486.
5. FAOSTAT: 2022 Food Balances Data. FAOSTAT; 2022.
www.sciencedirect.com

6. Savary S, Willocquet L, Pethybridge SJ, Esker P, McRoberts N,
Nelson A: The global burden of pathogens and pests on major
food crops. Nat Ecol Evol 2019, 3:430-439.
7. Shewry PR, Lovegrove A, Wingen LU, Griffiths S: Opinion
Exploiting genomics to improve the benefits of wheat:
prospects and limitations. J Cereal Sci 2022, 105:103444.
8. Steinberg G, Gurr SJ: Fungi, fungicide discovery and global food
security. Fungal Genet Biol 2020, 144:103476.
9. European Food Safety A, Arena M, Auteri D, Barmaz S, Bellisai G,
Brancato A, Brocca D, Bura L, Byers H, Chiusolo A, et al.: Peer
review of the pesticide risk assessment of the active substance
chlorothalonil. EFSA J 2018, 16:e05126.
10. Różewicz M, Wyzińska M, Grabiński J: The most important fungal
diseases of cereals—problems and possible solutions.
Agronomy 2021, 11:714.
11. Hodson DP: Shifting boundaries: challenges for rust monitoring.
Euphytica 2011, 179:93-104.
12. Bhavani S, Hodson DP, Huerta-Espino J, Randhawa MS, Singh RP:
Progress in breeding for resistance to Ug99 and other races of
the stem rust fungus in CIMMYT wheat germplasm. Front Agric
Sci Eng 2019, 6:210-224.
13. Andolfo G, Jupe F, Witek K, Etherington GJ, Ercolano MR, Jones
JD: Defining the full tomato NB-LRR resistance gene repertoire
using genomic and cDNA RenSeq. BMC Plant Biol 2014, 14:120.
14. Hewitt T, Muller MC, Molnar I, Mascher M, Holusova K, Simkova H,
Kunz L, Zhang J, Li J, Bhatt D, et al.: A highly differentiated region
of wheat chromosome 7AL encodes a Pm1a immune receptor
that recognizes its corresponding AvrPm1a effector from
Blumeria graminis. New Phytol 2021, 229:2812-2826.
15. Yu G, Champouret N, Steuernagel B, Olivera PD, Simmons J,
Williams C, Johnson R, Moscou MJ, Hernández-Pinzón I, Green P,
et al.: Discovery and characterization of two new stem rust
resistance genes in Aegilops sharonensis. Theor Appl Genet
2017, 130:1207-1222.
16. Yu G, Matny O, Champouret N, Steuernagel B, Moscou MJ,
•• Hernández-Pinzón I, Green P, Hayta S, Smedley M, Harwood W,
et al.: Aegilops sharonensis genome-assisted identification of
stem rust resistance gene Sr62. Nat Commun 2022, 13:1607.
A fascinating study that combined genomics, positional mapping, EMS
mutagenesis and RNAseq analysis to identify the stem rust resistance
gene Sr62, which the authors showed encodes a tandem protein kinase.
17. Sanchez-Martin J, Keller B: NLR immune receptors and diverse
types of non-NLR proteins control race-specific resistance in
Triticeae. Curr Opin Plant Biol 2021, 62:102053.
18. Gaurav K, Arora S, Silva P, Sanchez-Martin J, Horsnell R, Gao L,
Brar GS, Widrig V, John Raupp W, Singh N, et al.: Population
genomic analysis of Aegilops tauschii identifies targets for
bread wheat improvement. Nat Biotechnol 2022, 40:422-431.
19. Ellis JG, Lagudah ES, Spielmeyer W, Dodds PN: The past, present
and future of breeding rust resistant wheat. Front Plant Sci 2014,
5:641.
20. Dinglasan E, Periyannan S, Hickey LT: Harnessing adult-plant
resistance genes to deploy durable disease resistance in
crops. Essays Biochem 2022, 66:571-580.
21. Luo M, Xie L, Chakraborty S, Wang A, Matny O, Jugovich M,
•• Kolmer JA, Richardson T, Bhatt D, Hoque M, et al.: A five-
transgene cassette confers broad-spectrum resistance to a
fungal rust pathogen in wheat. Nat Biotechnol 2021, 39:561-566.
Aproof-of-concept study, illustrating the monumental potential of pre­
cision genome engineering in introducing multiple stem rust resistance
genes into wheat and the need to tailor deployment depending on re­
gional variation in the pathogen population.
22. De la Concepcion JC, Franceschetti M, MacLean D, Terauchi R,
Kamoun S, Banfield MJ: Protein engineering expands the
effector recognition profile of a rice NLR immune receptor. Elife
2019, 8:e47713.
23. Marchal C, Michalopoulou VA, Zou Z, Cevik V, Sarris PF: Show me
your ID: NLR immune receptors with integrated domains in
plants. Essays Biochem 2022, 66:527-539.
www.sciencedirect.com
Protecting wheat from fungal invaders Minter and Saunders 5
24. van Schie CC, Takken FL: Susceptibility genes 101: how to be a
good host. Annu Rev Phytopathol 2014, 52:551-581.
25. Buschges R, Hollricher K, Panstruga R, Simons G, Wolter M,
Frijters A, van Daelen R, van der Lee T, Diergaarde P, Groenendijk
J, et al.: The barley Mlo gene: a novel control element of plant
pathogen resistance. Cell 1997, 88:695-705.
26. Jørgensen IH: Discovery, characterization and exploitation of
Mlo powdery mildew resistance in barley. Euphytica 1992,
63:141-152.
27. Krasileva KV, Vasquez-Gross HA, Howell T, Bailey P, Paraiso F,
Clissold L, Simmonds J, Ramirez-Gonzalez RH, Wang X, Borrill P,
et al.: Uncovering hidden variation in polyploid wheat. Proc Natl
Acad Sci USA 2017, 114:E913-E921.
28. Wang N, Tang C, Fan X, He M, Gan P, Zhang S, Hu Z, Wang X, Yan
T, Shu W, et al.: Inactivation of a wheat protein kinase gene
confers broad-spectrum resistance to rust fungi. Cell 2022,
185:2961-2974 e2919.
29. Corredor-Moreno P, Minter F, Davey PE, Wegel E, Kular B, Brett P,
•• Lewis CM, Morgan YML, Macias Perez LA, Korolev AV, et al.: The
branched-chain amino acid aminotransferase TaBCAT1
modulates amino acid metabolism and positively regulates
wheat rust susceptibility. Plant Cell 2021, 33:1728-1747.
This study illustrates the potential of comparative RNA-seq analysis in
accelerating the identification of genes essential for supporting pa­
thogen ingress as new targets in plant resistance breeding. It also
highlighted a crucial role of branched-chain amino acid metabolism in
the rust defense response in wheat.
30. Campanaro A, Srivastava AK, Zhang C, Lee J, Millyard L,
Gatehouse AMR, Byrne E, Sadanandom A: TaWRKY10
transcription factor is a novel jasmonic acid signalling
regulator involved in immunity against Septoria tritici blotch
disease in wheat. Plant Pathol 2021, 70:1397-1408.
31. Knight SC, Anthony VM, Brady AM, Greenland AJ, Heaney SP,
Murray DC, Powell KA, Schulz MA, Spinks CA, Worthington PA,
et al.: Rationale and perspectives on the development of
fungicides. Annu Rev Phytopathol 1997, 35:349-372.
32. Alexander-Dann B, Pruteanu LL, Oerton E, Sharma N, Berindan-
Neagoe I, Modos D, Bender A: Developments in toxicogenomics:
understanding and predicting compound-induced toxicity from
gene expression data. Mol Omics 2018, 14:218-236.
33. Liu Z, Huang R, Roberts R, Tong W: Toxicogenomics: a 2020
vision. Trends Pharm Sci 2019, 40:92-103.
34. Martin MT, Brennan RJ, Hu W, Ayanoglu E, Lau C, Ren H, Wood
CR, Corton JC, Kavlock RJ, Dix DJ: Toxicogenomic study of
triazole fungicides and perfluoroalkyl acids in rat livers predicts
toxicity and categorizes chemicals based on mechanisms of
toxicity. Toxicol Sci 2007, 97:595-613.
35. Portugal J, Mansilla S, Pina B: Perspectives on the use of
toxicogenomics to assess environmental risk. Front Biosci
(Landmark Ed) 2022, 27:294.
36. Lucas JA, Hawkins NJ, Fraaije BA: The evolution of fungicide
resistance. Adv Appl Microbiol 2015, 90:29-92.
37. Chen J, Upadhyaya NM, Ortiz D, Sperschneider J, Li F, Bouton C,
Breen S, Dong C, Xu B, Zhang X, et al.: Loss of AvrSr50 by
somatic exchange in stem rust leads to virulence for Sr50
resistance in wheat. Science 2017, 358:1607-1610.
38. Salcedo A, Rutter W, Wang S, Akhunova A, Bolus S, Chao S,
Anderson N, De Soto MF, Rouse M, Szabo L, et al.: Variation in the
AvrSr35 gene determines Sr35 resistance against wheat stem
rust race Ug99. Science 2017, 358:1604-1606.
39. Upadhyaya NM, Mago R, Panwar V, Hewitt T, Luo M, Chen J,
• Sperschneider J, Nguyen-Phuc H, Wang A, Ortiz D, et al.:
Genomics accelerated isolation of a new stem rust avirulence
gene-wheat resistance gene pair. Nat Plants 2021, 7:1220-1228.
This study describes the utility of genomics in the tandem identification
of the stem rust Avr effector AvrSr27, and corresponding resistance
protein, Sr27.
40. Jaswal R, Kiran K, Rajarammohan S, Dubey H, Singh PK, Sharma
Y, Deshmukh R, Sonah H, Gupta N, Sharma TR: Effector biology
Current Opinion in Microbiology 2023, 73:102310
6 Environmental Microbiology
of biotrophic plant fungal pathogens: current advances and
future prospects. Microbiol Res 2020, 241:126567.
41. Muller MC, Kunz L, Schudel S, Lawson AW, Kammerecker S,
•• Isaksson J, Wyler M, Graf J, Sotiropoulos AG, Praz CR, et al.:
Ancient variation of the AvrPm17 gene in powdery mildew
limits the effectiveness of the introgressed rye Pm17
resistance gene in wheat. Proc Natl Acad Sci USA 2022,
119:e2108808119.
This study describes the identification of the Avr effector AvrPm17 from
the wheat powdery mildew pathogen, Blumeria graminis. In addition, the
Current Opinion in Microbiology 2023, 73:102310
authors found a number of ancient virulent alleles of AvrPm17 that
predated the introduction of Pm17 into wheat. Hence, providing insight
into the likely rapid downfall of Pm17 resistance.
42. Radhakrishnan GV, Cook NM, Bueno-Sancho V, Lewis CM,
Persoons A, Mitiku AD, Heaton M, Davey PE, Abeyo B, Alemayehu
Y, et al.: MARPLE, a point-of-care, strain-level disease
diagnostics and surveillance tool for complex fungal
pathogens. BMC Biol 2019, 17:65.
www.sciencedirect.com