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REVIEW ARTICLE
Open Access
STRATEGIC GENETIC INSIGHTS AND INTEGRATED APPROACHES FOR SUCCESSFUL MANAGEMENT
OF BLACKLEG IN CANOLA/RAPESEED FARMING
Thierry Rouxel,
Thierry Rouxel
INRAE, UR BIOGER, Université Paris-Saclay, Palaiseau, France
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Gary Peng,
Gary Peng
Saskatoon Research Centre, Agriculture and Agri-Food Canada (AAFC), Saskatoon,
Saskatchewan, Canada
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Angela Van de Wouw,
Angela Van de Wouw
* orcid.org/0000-0001-5147-0393
School of BioSciences, The University of Melbourne, Melbourne, Victoria,
Australia
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Nicholas J. Larkan,
Nicholas J. Larkan
Saskatoon Research Centre, Agriculture and Agri-Food Canada (AAFC), Saskatoon,
Saskatchewan, Canada
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Hossein Borhan,
Hossein Borhan
Saskatoon Research Centre, Agriculture and Agri-Food Canada (AAFC), Saskatoon,
Saskatchewan, Canada
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W. G. Dilantha Fernando,
Corresponding Author
W. G. Dilantha Fernando
* dilantha.fernando@umanitoba.ca
* orcid.org/0000-0002-2839-1539
Department of Plant Science, University of Manitoba, Winnipeg, Manitoba, Canada
Correspondence
W. G. Dilantha Fernando, Department of Plant Science, University of Manitoba,
Winnipeg, MB, Canada.
Email: dilantha.fernando@umanitoba.ca
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Thierry Rouxel,
Thierry Rouxel
INRAE, UR BIOGER, Université Paris-Saclay, Palaiseau, France
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Gary Peng,
Gary Peng
Saskatoon Research Centre, Agriculture and Agri-Food Canada (AAFC), Saskatoon,
Saskatchewan, Canada
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Angela Van de Wouw,
Angela Van de Wouw
* orcid.org/0000-0001-5147-0393
School of BioSciences, The University of Melbourne, Melbourne, Victoria,
Australia
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Nicholas J. Larkan,
Nicholas J. Larkan
Saskatoon Research Centre, Agriculture and Agri-Food Canada (AAFC), Saskatoon,
Saskatchewan, Canada
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Hossein Borhan,
Hossein Borhan
Saskatoon Research Centre, Agriculture and Agri-Food Canada (AAFC), Saskatoon,
Saskatchewan, Canada
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W. G. Dilantha Fernando,
Corresponding Author
W. G. Dilantha Fernando
* dilantha.fernando@umanitoba.ca
* orcid.org/0000-0002-2839-1539
Department of Plant Science, University of Manitoba, Winnipeg, Manitoba, Canada
Correspondence
W. G. Dilantha Fernando, Department of Plant Science, University of Manitoba,
Winnipeg, MB, Canada.
Email: dilantha.fernando@umanitoba.ca
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First published: 28 October 2024
https://doi.org/10.1111/ppa.14018
Thierry Rouxel and Gary Peng contributed equally to this article.
About
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* Abstract
* 1 INTRODUCTION
* 2 HISTORICAL AND CURRENT PERSPECTIVES OF CANOLA/OILSEED RAPE PRODUCTION AND
THE ASSOCIATION WITH STEM CANKER/BLACKLEG DISEASE
* 3 ONE SPECIES OR TWO? TAXONOMIC CONSIDERATIONS IN LEPTOSPHAERIA
* 4 GENETICS OF HOST–PATHOGEN INTERACTIONS
* 5 RESISTANCE GENES: THEIR CHARACTERIZATION AND APPLICATIONS
* 6 FUNGICIDES AND OTHER STRATEGIES FOR BLACKLEG MANAGEMENT
* 7 CONCLUSIONS AND FUTURE DIRECTIONS
* ACKNOWLEDGEMENTS
* Open Research
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ABSTRACT
This review describes a triumphant narrative in the battle against the
devastating plant pathogen complex, Leptosphaeria maculans and L. biglobosa, and
the success of the world's second-largest oilseed crop, canola/oilseed rape.
Emphasizing global collaborations, the article explores successfully mitigating
this destructive disease in canola/rapeseed production across Australia, Canada
and Europe. It highlights how strategies may vary between continents to adapt to
specific contexts. While initial resistance (R) genes proved effective, the
evolution of the pathogen under crop-induced disease pressure led to the
breakdown of these genes. Now, growers in these regions have been equipped with
new tools, allowing them to make informed decisions that help to keep the
disease at generally low levels. A pivotal factor in this success has been a
deepened understanding of the intricate science underlying the host–pathogen
interaction. Concerted efforts of individual laboratories and collaborative
initiatives have played an essential role in this success, including novel
methods for disease control based on extensive research that has translated into
developing highly resistant varieties, enhanced pathogen monitoring, improved
cultivar recommendation and integrated management strategies. The review
showcases many milestone advancements, including the cloning of numerous
avirulence genes within the pathogen, characterization of specific R genes, the
development of various molecular tools for monitoring both pathogen and host,
the introduction of groundbreaking disease management strategies such as R gene
labelling, rotation and stacking, and establishment of a universal pathogen
isolate collection that facilitates the exchange of information among multiple
laboratories and adds a new dimension to this triumph.
1 INTRODUCTION
Canola/oilseed rape (Brassica napus) is one of the most economically important
edible oil crops in the world, with extensive production in Canada (canola),
Australia (canola) and Europe (oilseed rape). Blackleg/stem canker disease,
caused by the fungal pathogens Leptosphaeria maculans (syn. Plenodomus lingam)
and L. biglobosa (syn. P. biglobosus), is one of the leading causes of
significant yield losses to canola/oilseed rape worldwide (Zheng et al., 2020).
While L. maculans is more damaging because it causes stem canker, L. biglobosa
can reach up to 92% disease incidence in China, where L. maculans has not been
reported (Deng et al., 2023; Fitt et al., 2006; Hao et al., 2012; Mendes-Pereira
et al., 2003). Understanding the host–pathogen interaction is essential for
developing management strategies for growers. Resistance through single
resistance genes has been successful. However, the breakdown of R genes has
presented challenges, which has led to collaborations among researchers across
continents. This review delineates the endeavours and accomplishments in
blackleg management within the canola industry across the three continents; it
illustrates how the insights garnered from extensive research have been
disseminated to growers and integrated into industry practices.
2 HISTORICAL AND CURRENT PERSPECTIVES OF CANOLA/OILSEED RAPE PRODUCTION AND THE
ASSOCIATION WITH STEM CANKER/BLACKLEG DISEASE
2.1 EUROPE
Cultivation of oilseed rape as a winter crop in Europe can be traced back to the
14th century, mainly in northern France, the Netherlands and northern Germany
(Chauvet, 2018). Initially, the oil from modest acreages served the purposes of
domestic lighting and steam engine lubrication. However, in the 19th century,
the rise of petroleum and colonial oils like peanut oil led to a significant
acreage reduction (Pinochet & Renard, 2012; Sagnier, 1920). The latter half of
the 20th century saw European decolonization efforts drive the cultivation of
oil crops towards human consumption, fostering genetic advancements and breeding
in sunflower and oilseed rape. Notably, Germany and France spearheaded the
development of new oilseed rape genotypes with reduced erucic acid and
glucosinolate content. This led to the release of the first single-low (erucic
acid) French cultivar Primor in 1973 and, subsequently, the double-low (erucic
acid and glucosinolate content) cultivar Samourai in 1989. These quality
enhancements propelled the success of oilseed rape in Europe, with acreages in
France and Germany skyrocketing from around 50,000 ha in 1960 to consistently
exceeding 1.1 million ha each in recent years (1.1 million ha sown in Germany in
2023 and 2024, 1.3 million ha in France and slightly above 1 million ha for
Poland, a country in which rapeseed cropping has dramatically increased these
last years). To date, oilseed rape is widely cropped in Europe, with France
being the EU's largest rapeseed producer (4.3 Mt in 2023), followed by Germany
(4.2 Mt) and Poland (3.7 Mt), and yields regularly above 3 t/ha
(https://agridata.ec.europa.eu/extensions/DashboardCereals/OilseedProduction.html).
Outside the EU, other important producers are the UK, Ukraine and Russia. One
other particular feature of the EU is that spring oilseed rape, which was
initially grown in northern countries such as Sweden, has now been replaced
nearly everywhere by winter oilseed rape.
As the initial hub for oilseed rape cultivation, continental Europe bore the
brunt of the initial impact of blackleg. The first epidemics were described in
the 1950s in France (Darpoux et al., 1957), with 50%–60% of the plants infected
and average yield losses of around 40% between 1964 and 1967 (Lacoste
et al., 1969). In Germany, infection incidence was up to 70% in some years
(Krüger, 1983). Breeding programmes to combat the disease were thus undertaken
rapidly, for example, in France since 1960, introducing the resistant cultivar
Ramses in 1970 and Jet Neuf in 1977, which dominated the European oilseed rape
acreages for nearly 10 years. The latter was also the genetic basis of numerous
breeding materials worldwide due to its excellent resistant traits (Pinochet &
Renard, 2012; Rimmer & Van den Berg, 1992) (see following paragraphs on breeding
history in Australia and Canada). However, the conversion to double-low
varieties in the late 1980s was also accompanied by a decline in genetic
diversity and a drastic reduction in resistance to stem canker of new varieties.
Consequently, the 1992/1993 and 1993/1994 cropping years experienced severe
epidemics of stem canker, with some western regions suffering up to 80% losses
(Ansan-Melayah et al., 1997). In Europe, despite the success of this new crop
since the 1990s, stem canker was a recurrent threat, which prompted continuous
breeding efforts towards more resistant varieties. In France, it quickly became
mandatory for new varieties to show high resistance in official trials before
being marketed commercially.
Research focused initially on fungicide treatments in Europe (Darpoux
et al., 1957), along with breeding for resistance based on mass selection in
disease nurseries. However, there was limited interaction between breeders and
plant pathologists, and the knowledge of the pathogen and its biology needed to
be improved (Rimmer & Van den Berg, 1992). Research then moved further into
studying disease epidemiology in France (Brunin, 1970a, 1970b; Lacoste
et al., 1969), with a strong impulse of the CETIOM, the technical institute in
charge of oilseed crops, demonstrating the importance of ascospores as a primary
inoculum and recommending a simple control strategy: destruction and burial of
diseased residues to prevent sexual reproduction. While the method was effective
for disease control, it added additional fieldwork for farmers and was
incompatible with conservation tillage practices. As a result, it was not widely
adopted.
In Europe, stem canker research was strongly supported by two EU-funded
projects, IMASCORE (Integrated Strategies for the Management of Stem Canker of
Oilseed Rape in Europe, led by M. H. Balesdent, INRA Versailles, France,
1996–2000) and SECURE (Stem Canker of Oilseed Rape: molecular tools and
mathematical modelling to deploy durable resistance, led by Neal Evans,
Rothamsted Research Center, UK, 2002–2006), involving partnerships from France,
Germany, the UK, Poland, Portugal and Sweden, including private seed companies.
The objectives were to achieve a better understanding of European populations of
the pathogen(s) and disease epidemiology, mine genetic resources for disease
resistance, and dissect the genetics of host–pathogen interactions based on
molecular characterization and cloning of avirulence (Avr) genes (Balesdent
et al., 2005; Evans et al., 2006).
Under these auspices, the following progress/achievements were obtained: (a) the
identification, characterization and dissection of the L. maculans–L. biglobosa
species complex; (b) the genetic elucidation of host–pathogen interactions and
identification of unusual genetic control; (c) cloning of fungal Avr genes that
were instrumental in many later studies; (d) genome sequencing of the pathogens
and hosts, as well as metatranscriptomics used to decipher the interactions; and
(e) pathogen population surveys at the European scale.
2.2 AUSTRALIA
Rapeseed production began in Australia in the mid-1960s with varieties
introduced from Canada, such as Target, Oro and Span, which proved very
susceptible to blackleg under Australian growing conditions (Salisbury
et al., 1995). While canola was recognized as an interesting cash crop, the
damage due to blackleg nearly prevented growers from growing canola in Australia
(only 2000–3200 ha grown in 1973–1974; Salisbury et al., 1995). The Victorian,
New South Wales and Western Australian state governments launched breeding
programmes in the early 1970s to address the threat, primarily for resistance to
blackleg. These breeding programmes incorporated material from 18 different
varieties that came from Canada (3), Europe (7) and Asia (8) (Cowling, 2007).
These breeding efforts led to the release of the first blackleg-resistant
varieties, Wesreo, in 1978 (Roy, 1978; Roy & Reeves, 1975) and the
canola-quality Wesroona in 1980 (Salisbury et al., 1995). Breeding efforts have
also incorporated resistance genes from brassica crops like Brassica juncea
(Cowling, 2007; Roy, 1984). Roy's work created valuable materials shared among
many research groups, eventually leading to the introduction of Rlm6, a B.
juncea resistance gene, in diverse spring or winter varieties over the next
30 years. These continuous efforts were highly successful, and in 1995,
Salisbury et al. stressed that ‘Current Australian varieties have the highest
levels of blackleg resistance of any spring canola varieties in the world’.
Canola production in Australia has increased significantly over the past
20 years, from about 1.5 Mt in 2003 to a peak of 7.9 Mt in 2022, with an average
of around 5 Mt across the past 5 years. With blackleg being a stubble-borne
disease, increased production results in increased stubble load and, therefore,
should also lead to increased severity of blackleg disease. Despite this, the
average disease severity across Australia has fallen across the same 20-year
period, with an average of 48% internal infection in the early 2000s and an
average of 32% in the past 3 years (Figure 1). Despite significant production
increases, this decrease in disease is driven by improvements in genetics,
fungicides and farming practices.
FIGURE 1
Open in figure viewerPowerPoint
Changes in canola production and blackleg disease severity in Australia across
the past 20 years. Canola production data is from the Australian Oilseeds
Federation. Data for 2023 production is an estimate. Blackleg disease severity
is represented as the percentage of internal infection at the crown for a
susceptible variety grown at eight sites each year, with no fungicide
applications. Significant drought years are highlighted as they had a
significant impact on both canola production and blackleg disease.
Farming practices have changed dramatically in Australia in the past 20 years
due to technological changes such as GPS-guided tractors for inter-row sowing.
These innovations have contributed to changes in stubble management and sowing
times. There have been significant changes in stubble conservation in Australia
with a massive shift towards no-till or zero-till practices (Umbers, 2016; Van
de Wouw, Marcroft, et al., 2021). This shift has led to the conservation of
stubble in a standing position rather than knocked over and in contact with the
soil. McCredden et al. (2017) showed that this change had resulted in altered
epidemiology of the blackleg disease, with fewer spores being released from
standing stubble, and that the spore release was also delayed. The impact of
this altered disease epidemiology remains unknown for Australian growers.
Sowing times have been significantly earlier due to the combination of
herbicide-tolerant cultivars, allowing in-crop weed control, GPS-guided
equipment, allowing precision sowing with reduced soil disturbance, and stubble
retention and hybrid seeds, allowing growers to sow into dry soil (Angus
et al., 2015; Van de Wouw, Marcroft, et al., 2021). Sowing early, and therefore
flowering early, can lead to higher yield by avoiding water stresses during the
critical period for yield development (Kirkegaard et al., 2018). Furthermore,
earlier sowing times are hypothesized to contribute to the lower levels of crown
canker severity (blackleg cankers at the crown). Spore release in Australia
occurs with each rainfall event from approximately June onwards (McGee &
Emmett, 1977). Infection of canola seedlings up to the sixth leaf stage is
generally responsible for crown canker (Marcroft et al., 2005). Crops sown early
tend to develop quickly through this vulnerable growth stage before the release
of blackleg spores, and this notion is supported by the lower levels of crown
canker severity currently being reported (Figure 1).
While earlier sowing is a possible driver towards lower crown canker severity in
Australia, this change has resulted in a change in disease epidemiology, leading
to the infection of the upper stems, upper branches, flowers and pods, resulting
in flower and pod abortion and lesions on pods, branches and upper stems, termed
upper canopy infection. Since 2010, upper canopy infection has been found in all
growing regions of Australia, with reports of up to 30% yield loss (Sprague
et al., 2017). This increase in upper canopy infection is thought to be driven
by the earlier flowering time, letting the upper canopy of the crop now be
exposed to the spore showers rather than the seedling growth stages (Sprague
et al., 2017). The change in stubble management, as described above, also plays
a role in this increased prevalence of upper canopy infection.
In Australia, there is also a significant shift in research towards
understanding how to manage yield losses associated with upper canopy infection.
Studies have already shown that major-gene resistance can control upper canopy
infection; however, when this is lacking, fungicides at the 30% bloom can help
minimize the loss associated with this form of the disease (Sprague
et al., 2017). Preliminary data has suggested that quantitative resistance (QR)
also plays a role in the impact of upper canopy infection. However, further work
is needed to understand this properly. While upper canopy infection is yet to be
reported in any other regions, these symptoms are likely to be present anywhere
when the reproductive parts of the plant are exposed to ascospores under
conducive conditions.
2.3 CANADA
Canada developed the world's first canola variety, Tower, in the late 1970s
(Stefansson & Kondra, 1975). Since then, canola acreage has surpassed everyone's
expectations and become a ‘Cinderella’ crop for many Canadian growers, reaching
8.58 million ha in 2022 (Stats Canada, 2024). However, the increase in canola
acreage has also had its share of challenges due to the impact of several
diseases, including blackleg.
By 1985, the Westar cultivar dominated canola plantings in Canada, occupying 90%
of the planted acreages (Klassen et al., 1987). This created a perfect condition
for the distribution and widespread establishment of blackleg in western Canada,
as Westar is highly susceptible to the disease. By the early 1990s, varieties
with partial blackleg resistance had been released, but no varieties showed a
high resistance level (Bansal et al., 1994). Canadian breeding programmes looked
overseas and used the Australian cultivar Maluka and doubled haploid (DH)
breeding strategies to rapidly incorporate an R gene into the first highly
resistant Canadian variety, Quantum (Stringam, Bansal, et al., 1995; Stringam,
Degenhardt, et al., 1995). Another Australian cultivar, Shiralee, was used to
produce the Canadian variety Q2 (Stringam et al., 1999), while the French
variety Jet Neuf, a valuable blackleg resistance source, was incorporated into
the pedigree of the Canadian variety Sentry (Rimmer et al., 1998). By the
mid-2000s, only 40% of registered varieties were rated blackleg-resistant.
However, the genetic basis for these resistance sources was largely unknown
(Rimmer, 2006). It was not until much later that it was found that Quantum, Q2
and Sentry all harbour the same blackleg resistance gene (Rlm3), akin to many
early blackleg-resistant varieties cultivated in Canada during the 1990s
(Larkan, Yu, et al., 2016).
The agricultural landscape and practices also changed rapidly in Canada during
this period; minimum or zero tillage was rapidly adopted by many growers.
Initial studies were conducted to understand pathogen survival, spread and
infection under these new farming practices (Guo et al., 2005, 2008). A
noticeable increase in blackleg was reported around 2010, coincidentally
exacerbating the trade dispute for Canadian canola seed export to China
(Fernando et al., 2016). The research community came together quickly to address
the challenge posed by the disease; Zhang et al. (2016) assessed Canadian
varieties but found few R genes, with Rlm3 dominating (55%) these varieties. The
pathogen population had shifted from previous years (Kutcher et al., 2010), with
97% of isolates from growers' fields carrying the virulence (Vir) allele avrLm3
(Fernando et al., 2018; Liban et al., 2016; Rashid et al., 2021). Therefore, the
R gene Rlm3 would no longer be effective.
Today, almost all canola cultivars grown in Canada carry a level of resistance
to blackleg (Zhang et al., 2016, 2017). The efficacy of genetic resistance also
corresponds well to disease levels observed during annual disease surveys in
western Canada over nearly four decades (Figure 2). The first detection of new
races (pathotypes) was reported by Chen and Fernando (2006) and Fernando and
Chen (2003). Studies on disease epidemiology were initiated later (Ghanbarnia
et al., 2011; Guo et al., 2005), under the western Canada environment and short
crop seasons relative to other jurisdictions (Ghanbarnia et al., 2009; Salam
et al., 2007). One of the highlights of these studies was the identification of
pycnidiospores as being relevant for blackleg infection in Canada, contrasting
to the previous findings in Australia (Marcroft et al., 2003) and Europe
(Brunin, 1970a, 1970b), in which only ascospores were considered the primary
inoculum.
FIGURE 2
Open in figure viewerPowerPoint
Blackleg incidence in commercial canola fields on the Canadian Prairies since
1975 based on annual disease surveys in the provinces Alberta, Saskatchewan and
Manitoba.
3 ONE SPECIES OR TWO? TAXONOMIC CONSIDERATIONS IN LEPTOSPHAERIA
In early literature, L. maculans was consistently regarded as a highly
polymorphic species; Desmazières (1849) even stated that ‘few species are so
polymorphic’, a sentiment echoed later by others when comparing various isolates
from Brassica or related species (Cunningham, 1927; Petrie, 1970; Pound, 1947).
This led to the categorization of isolates into two pathotypes referred to as
weakly/strongly parasitic or virulent/slightly virulent (Pound, 1947), among
other designations. These two groups were distinguished using (a) morphological
criteria such as the production of pigments by the weakly virulent or
non-aggressive type (West et al., 2002); (b) the host plant the isolate was from
(Petrie, 1970); (c) RFLP markers leading to the A (highly virulent) and B
(weakly virulent) terminology (Johnson & Lewis, 1990); (d) secondary metabolites
leading to the Tox+/Tox0 terminology (Balesdent et al., 1992); or (e) additional
RFLP markers complemented with soluble proteins and isozymes (Balesdent
et al., 1992; Gall et al., 1995; Koch et al., 1991) and were eventually
classified into L. biglobosa or L. maculans (Shoemaker & Brun, 2001). As an
attempt to address the polymorphic nature of the pathogen internationally, the
most significant initiative was the establishment of the International Blackleg
of Crucifers Network (IBCN) led by G. Seguin-Swartz (AAF Saskatoon, Canada) and
M. H. Balesdent and T. Rouxel (INRA Versailles, France) (Rouxel &
Séguin-Swartz, 1995), following an initial meeting during the International
Congress of Plant Pathology of Montreal in 1993. The IBCN was formed in response
to severe blackleg epidemics in Australia in the 1990s to establish an
international collection of L. maculans isolates to be maintained and shared
among researchers to accurately characterize the pathogen strains (Balesdent
et al., 2005). The IBCN network was connected through the Blackleg News Bulletin
between 1993 and 2003, as well as dedicated meetings in conjunction with
international conferences for researchers to share ideas and research
information. In response to the need to connect the community leveraging the
advancements in genomics and to address shifts in fungal populations, the IBCN
initiative was recently revitalized to create a new collection wherein all
pathogenicity and genome information is accessible to researchers worldwide (Van
de Wouw et al., 2024). The first IBCN collection also included diversified and
divergent isolates of L. biglobosa, eventually resolved with rDNA internal
transcribed spacer (ITS) sequence analysis. A total of seven subspecies were
defined that may represent valid biological species (Mendes-Pereira
et al., 2003). The diversity broadly represents geographic distributions, but
also, for rarer isolates, adaptation to wild crucifer species (Deng
et al., 2023; Gay et al., 2023; Vincenot et al., 2008; Zou, Zhang,
et al., 2019). The two most common subspecies were initially believed to be
geographically separated, with L. biglobosa ‘brassicae’ specific to the
Indo-European continent and L. biglobosa ‘canadensis’ specific to North America
(Mendes-Pereira et al., 2003). This simple view has now been discarded with
descriptions of both subspecies in other parts of the world, for example in
China where L. biglobosa ‘canadensis’ has recently been identified in northern
regions of the country (Deng et al., 2023) as well as in Australia (Van de Wouw
et al., 2008).
Tools to understand and discriminate the isolates within the L. maculans–L.
biglobosa species complex are a prerequisite to studying the genetics of
interactions, population dynamics and disease control strategies towards the
most damaging species, L. maculans (Rouxel et al., 1994). These results are
significant to Europe, where the two species are always present together
(Bousset et al., 2022; Jacques et al., 2021); they helped with better
discrimination of symptoms in the field (Bousset et al., 2022). Thus, growers
and breeders can correctly evaluate the resistance towards L. maculans in new
varieties. Due to L. maculans being the more damaging species, much of the
research has focused on this species rather than L. biglobosa. However, with the
recent reports from China as well as the prevalence in other parts of the world,
it is possible that L. biglobosa could be a concern in the future as an emerging
threat, and there would be a need to undertake dedicated research on this
species.
4 GENETICS OF HOST–PATHOGEN INTERACTIONS
Deciphering the genetics of the host–pathogen interaction has been instrumental
in breeding resistance against blackleg. Many early studies used
phenotyping-based protocols for pathogenicity or Vir assessment (Rimmer & Van
den Berg, 1992), including inoculation (a) of cotyledons with field ascospores
without wounding and scoring on cotyledons and then stem (Thurling &
Venn, 1977); (b) with ground mycelium as an inoculum (Cargeeg & Thurling, 1980);
(c) of petioles of first leaves with filter paper soaked with conidial
suspensions without wounding (Newman, 1984); and (d) of wounded leaf lamina or
cotyledons with conidial suspensions (Badawy et al., 1991; Mengistu
et al., 1991; Mithen et al., 1987). McNabb et al. (1993) critically compared
various inoculation methods concerning their correlation with field responses of
varieties; their findings, though occasionally debated, ultimately suggested
that the cotyledon inoculation provided the highest degree of precision.
Subsequently, this protocol gained popularity internationally; it enabled P. H.
Williams' group (University of Madison, United States) to identify specific
differential varieties to which groups of isolates exhibited diverse
compatibility/Vir or incompatibility/Avr (Mengistu et al., 1991).
Concurrently, the same group established robust protocols for in vitro crossings
of L. maculans (Mengistu et al., 1993), which were widely adopted later (Gall
et al., 1994; Plummer & Howlett, 1995), facilitating genetic studies targeting
pathogenicity/Vir of the fungus. Laboratory crosses between different fungal
isolates (Gall et al., 1994) demonstrated that the Avr phenotypes observed on
Quinta and Glacier were governed by monogenic control within the fungus. This
discovery paved the way for the characterization (and subsequent cloning) of two
effector-Avr genes: AvrLm1 (Ansan-Melayah et al., 1995) and AvrLm2
(Ansan-Melayah et al., 1998), demonstrating Flor's gene-for-gene interaction
between the blackleg pathogen and oilseed rape.
Through collaborations, an additional 10 Avr genes have since been genetically
characterized in L. maculans (Balesdent et al., 2001, 2002, 2005, 2013; Degrave
et al., 2021; Ghanbarnia et al., 2012; Petit-Houdenot et al., 2019; Van de Wouw
et al., 2009), with the corresponding R genes Rlm1, Rlm2, Rlm3, Rlm4, Rlm7 and
Rlm9 postulated or identified in B. napus, Rlm5 and Rlm6 in B. juncea, Rlm10 in
B. nigra and Rlm1, Rlm3, Rlm7, Rlm8, Rlm11, LepR1, LepR3 and RlmS-LepR2 in B.
rapa (Leflon et al., 2007; Neik et al., 2022; Rouxel & Balesdent, 2017) and
Rlm14 in B. oleracea (Degrave et al., 2021).
4.1 CLONING OF AVR GENES REVEALS UNUSUAL GENE-FOR-GENE INTERACTIONS
Following the genetic dissection of the interactions, the next step was to
understand the adaptation of the fungus and clone the Avr genes to develop new
tools for studying pathogen populations. Forward genetic approaches were
tedious, requiring over a decade to clone the first Avr gene, AvrLm1. This
journey began with its initial genetic characterization (Ansan-Melayah
et al., 1995) and culminated in its actual cloning (Gout, Fudal, et al., 2006).
Notably, the French sequencing institute, Genoscope, made significant
contributions by devising strategies to sequence unconventional genomic regions.
Before the genomic era, these map-based approaches enabled the cloning of
several Avr genes. For AvrLm1, using a map-based cloning strategy allowed the
identification of the genetic interval on a bacterial artificial chromosome
(BAC) contig with unusual characteristics (at the time), highlighting features
of AvrLm1 and its genomic environment. The gene is situated within a large
transposable element (TE)-rich region and codes for a small protein (205 amino
acids) containing a single cysteine residue and a signal peptide. Notably, this
gene had no homology with other sequences available in public databases. It was
later shown that these characteristics (except for cysteine enrichment) were
shared by all Avr genes subsequently cloned, with low or no expression during
axenic growth and specific induction during asymptomatic infection of B. napus
at the beginning (Rouxel et al., 2011). Indeed, only recently was the notion of
absent orthologues questioned; this shift came with the discovery of the
conservation of 3D protein structures within families of structurally related
small secreted proteins (SSPs). These proteins serve as effectors for the fungus
and, in some cases, function as Avr proteins (Lazar et al., 2022).
The L. maculans genome (reference isolate v23.1.3, also called JN3) was
sequenced in France by Genoscope under an international initiative (Europe,
Australia, United States) led by INRA-Versailles (France) and University
Melbourne (Australia). Compared to previous experiences of sequencing complex
genomes of phytopathogens, the work on the L. maculans genome benefited from an
excellent sequencing/assembly that allowed the coverage of under-represented
regions, the so-called repeat-rich AT-rich isochores (Rouxel et al., 2011),
which were often considered previously as ‘junk DNA’ unworthy of being studied.
Using L. maculans as a developmental model, Genoscope enhanced its sequencing
procedures and assembly/annotation pipelines, culminating in refining the
reference JN3 genome through high-density genetic mapping, optical mapping and
long-read sequencing to achieve chromosome-sized assembly. Additionally, the
genome of L. biglobosa was also sequenced (Dutreux et al., 2018).
This high-standard genome for L. maculans facilitated discoveries of genome
organization and evolutionary dynamics of effector/Avr genes, contributing to
establishing the two-speed genome paradigm observed in many filamentous
phytopathogens (Dong et al., 2015). This paradigm delineates gene-rich regions
from dispensable regions, characterized by degenerated transposon mosaics,
undergoing drastic evolutionary mechanisms such as repeat-induced point (RIP)
mutations while hosting genes involved in niche adaptation. Notably, the AT-rich
isochores in L. maculans harbour many effector genes, including all known Avr
genes, impacting gene regulation, accelerated evolution under R gene pressure
and diversification of sequences to generate new specificities.
Currently, 12 L. maculans Avr genes have been cloned, often in the frame of
international collaborations: AvrLm1, AvrLm2, AvrLm3, AvrLm4-7, AvrLm5-9,
AvrLm6, AvrLm10A, AvrLm10B, AvrLm11, AvrLm14, AvrLmS-Lep2 and AvrSTEE98
(Balesdent et al., 2013; Degrave et al., 2021; Fudal et al., 2007; Ghanbarnia
et al., 2015, 2018; Gout, Fudal, et al., 2006; Jiquel et al., 2021; Neik
et al., 2022; Parlange et al., 2009; Petit-Houdenot et al., 2019; Plissonneau
et al., 2016, 2018; Van de Wouw, Lowe, et al., 2014); the numbers are higher
than any other crop–pathogen system so far, comparable to what is known in the
rice–Pyricularia oryzae model (Xiao et al., 2020), making the Brassica–L.
maculans system a widely cited model system for studying R–Avr gene interactions
(Borhan et al., 2022; Rouxel & Balesdent, 2017).
With our increase in knowledge of the blackleg–Brassica pathosystem, it is
becoming clear that it no longer sits in the simple gene-for-gene model for
plant–pathogen interactions. Several discoveries of complex interactions have
now been recorded, such as AvrLm1, recognized by LepR3 and Rlm1 (Larkan
et al., 2013). Another example is the two-gene-for-one-gene interaction between
both AvrLm10A and AvrLm10B and Rlm10; both Avr genes are necessary to induce
resistance of Rlm10 (Petit-Houdenot et al., 2019; Talbi et al., 2023). The
cooperative interaction between two orthologues of AvrLm10A and AvrLm10B has
also been described in other fungal species (Talbi et al., 2023).
Dual-recognition specificities may happen with specific Avr genes, such as
AvrLm4, which was renamed AvrLm4-7, as some of its alleles can generate a
resistance response in the presence of both Rlm4 and Rlm7 (Parlange
et al., 2009), or AvrLm5-9, which induces resistance responses from both Rlm5
and Rlm9 (Ghanbarnia et al., 2018).
Another example is a ‘camouflage model’ whereby one Avr gene masks the
recognition of another by the matching resistance. First, AvrLm4-7 hides the
presence of AvrLm3 and prevents its recognition by Rlm3, even when AvrLm3 is
present and expressed (Plissonneau et al., 2016). Deletions or inactivating
mutations of AvrLm4-7 lead to unmasking and the recognition of AvrLm3, while
other mutations, such as those generating virulent isoforms of the AvrLm3
protein or isolates that contain point mutations in AvrLm4-7, escape Rlm7
resistance while maintaining the suppression of the AvrLm3 phenotype (Balesdent
et al., 2022; Plissonneau et al., 2017). These studies show that the AvrLm3
gene, once thought to be lost due to the high selection pressure caused by
widespread Rlm3-containing cultivars, is still present and expressed (Rouxel &
Balesdent, 2017). This discovery shows that R genes previously considered
ineffective may be re-used. Similarly, the presence of AvrLm4-7 masks the
recognition of AvrLm5-9 by Rlm9 (Ghanbarnia et al., 2018). The academic
significance of all this research into the gene-for-gene interactions is
amplified by the proposition that unusual gene-for-gene interactions, if so
prevalent in this system, may also occur in other plant–pathogen systems. This
highlights the need to unravel these mechanisms, equipping breeders with
pertinent information for developing robust and lasting resistance genotypes and
providing producers with effective and practical options to use such resistance.
For breeders, the recent characterization of AvrLmSTEE98, an Avr gene expressed
during stem colonization, and genetic mapping of its cognate resistance gene,
RlmSTEE98, highlighted that a gene-for-gene interaction could be involved in
limiting stem colonization and triggering partial resistance (Jiquel
et al., 2021, 2022). Examples like this will help us rethink the current
categorization of qualitative and QRs in the Brassica–L. maculans pathosystem
and open the way to identifying further gene-for-gene interactions expressed at
other plant growth stages beyond the cotyledon/leaf stage. R genes operating at
different stages are likely to be involved in QR and thus open new routes for
breeding for durable resistance.
Due to the complexity of Avr genes harboured in field isolates, crossing is the
first option to generate L. maculans isolates harbouring the minimum number of
AvrLm genes. Following a series of backcrosses, near-isogenic isolates differing
by only a single AvrLm gene may be obtained (Balesdent et al., 2002; Huang
et al., 2010; Rouxel, Willner, et al., 2003). With the advent of molecular
tools, genetic manipulation, including complementation, RNA silencing and
CRISPR-Cas9 gene editing, can now be routinely used to generate novel isogenic
isolates to identify corresponding Rlm/LepR genes in brassica genotypes for
screening genetic resources or for use in plant breeding (Balesdent
et al., 2002; Borhan et al., 2022; Ghanbarnia et al., 2012; Larkan et al., 2015;
Rouxel, Willner, et al., 2003; Zou et al., 2020).
4.2 PATHOGEN POPULATION SURVEYS
The cotyledon inoculation test and ever-evolving plant differential sets (Badawy
et al., 1991; Balesdent et al., 2005, 2023; Marcroft, Elliott, et al., 2012;
Mengistu et al., 1991) were used initially to separate the isolates into
pathogenicity groups (PGs); PG1: nonpathogenic on Westar, Glacier and Quinta;
PG2: virulent on Westar and avirulent on Glacier and Quinta; PG3: virulent on
Westar and Glacier; and PG4: virulent on all three varieties. An additional PG
(PGT), which was virulent on Westar and Quinta but avirulent on Glacier, was
described later, along with A groups (A0/A1: virulent on Lirabon, Glacier,
Quinta and Jet Neuf; A2: avirulent on Quinta only; A3: avirulent on Glacier,
Quinta and Jet Neuf; A4: avirulent on Glacier only; and NA: nonpathogenic to all
four genotypes; Badawy et al., 1991; Chen & Fernando, 2006; Mengistu
et al., 1991). Genetic identification and naming of Avr genes then were the
basis for classifying isolates as a function of the combination of Avr
specificities they harbour (also termed races; Dilmaghani et al., 2009), giving
direct information on the R genes that are efficient towards an isolate and, if
above a given percentage of avirulent isolates, against a population of the
fungus. For optimal deployment of R genes, updated knowledge of the pathogen
population structure is required, but limitations reside in the amount of
phenotyping that can be done annually. In France and Europe, large-scale surveys
were conducted in 2000–2001 (Balesdent et al., 2006; Stachowiak et al., 2006)
and in 2019–2020 (Balesdent et al., 2023), with smaller scale analyses in
between (Figure 3). These surveys indicated that L. maculans populations
displayed similar race structures throughout Europe, a finding consistent with
population genetic studies indicating the importance of sexual reproduction for
the fungus in the region, which, however, may not be the case in other parts of
the world such as North America (Dilmaghani et al., 2012; Zhang &
Fernando, 2017). European populations may be coevolving parts of a large
panmictic population (Gout, Eckert, et al., 2006), influenced by successive uses
of Rlm genes in European oilseed rape cultivars, with the absence or very low
residual presence of AvrLm alleles corresponding to the R genes used
extensively, including Rlm1, Rlm2 or Rlm4 (Rouxel & Balesdent, 2017; Figure 3).
In contrast, systematic presence of Avr alleles corresponded to the genes that
had never been used commercially (e.g., Rlm6, Rlm10, RlmS-LepR2) (Balesdent
et al., 2023; Van de Wouw, Sheedy, et al., 2022; Figure 3).
FIGURE 3
Open in figure viewerPowerPoint
Monitoring avirulent populations in France using the cotyledon-inoculation test.
Data are average values following field sampling on trap oilseed rape varieties
(i.e., devoid of Rlm genes). About 4000 isolates were phenotyped. Samplings were
taken from four locations (2017 sampling), eight locations (2010 sampling), nine
locations (2021 sampling), 10 locations (2019 sampling) or 20 locations (2000
sampling). Asterisks indicate interactions that were not studied in those years.
In Canada, initial studies using the PG system revealed the pathogen
population's evolution from exclusively PG2 to a mixture of PG2, PG3, PGT and
PG4 (Chen & Fernando, 2006; Kutcher et al., 2007). Kutcher et al. (2010)
transitioned to using differential hosts carrying a set of known R genes to
characterize the pathogen population based on the Avr profile. The study
revealed the Avr composition of the L. maculans population in western Canada
influenced by resistant canola cultivars since the early 1990s, offering
insights into the genetic basis of host–pathogen interactions in commercial
fields. In another study conducted by Kutcher et al. (2011), more than 800 L.
maculans isolates collected from nine trap plots of Westar across western Canada
in 2007 and 2008 were tested; these plots were assumed to receive pathogen
inoculum from surrounding fields, showing that AvrLm1 and AvrLep2 were at very
low levels while other Avr alleles, including AvrLm3 and AvrLm9, were present in
>50% of the isolates. In a subsequent study, Liban et al. (2016) analysed
isolates from hundreds of commercial fields gathered during disease surveys in
2010 and 2011 on a set of 13 differential brassica lines/varieties, and the
results showed a dramatic reduction in AvrLm3 and AvrLm9 relative to previous
observations (Dilmaghani et al., 2009; Kutcher et al., 2010, 2011), while AvrLm7
increased significantly. The decline in AvrLm3 might be attributable to the
extensive use of Rlm3 in Canadian cultivars (Zhang et al., 2016; Zhang &
Fernando, 2017), but the reason behind the reduction in AvrLm9 or a substantial
increase in AvrLm7 remained unexplained.
In a follow-up study of isolates collected from both Westar trap plots and
commercial fields located in the same areas during 2012–2014, similar patterns
of Avr profile were found between the two sampling methods (Soomro
et al., 2021). The results supported those of Liban et al. (2016). The Avr
pattern did not change substantially in the pathogen population between 2015 and
2017 (data not shown). These pathogen Avr analyses coincided with annual
blackleg disease surveys in western Canada; over 100 races were identified, with
much higher fungal richness and diversity than that found in other parts of the
world (Liban et al., 2016; Liu et al., 2021; Soomro et al., 2021; Zou
et al., 2018) and at least one virulent L. maculans isolate has been identified
towards each known blackleg R gene, except Rlm10.
Whilst phenotyping isolates can be used to determine the frequency of Vir in a
population, this work is tedious and low throughput as it requires each
individual to be inoculated onto a plant with the corresponding resistance gene.
With the cloning of many of the Avr genes in the blackleg–Brassica pathosystem,
we are uniquely poised to use molecular markers for Avr monitoring. Numerous
types of molecular markers have been developed for genotyping individual
isolates, which include PCR-based assays (presence/absence of bands or digestion
with restriction enzymes) through to allele-specific markers (Kompetitive
Allele-specific PCR markers; authors' unpublished data). Markers have also been
developed that allow populations of isolates to be genotyped, not just single
isolates. These include quantitative PCR and pyrosequencing approaches to look
at ascospore populations (Van de Wouw et al., 2010; Van de Wouw & Howlett, 2012)
and more recently, genome sequencing approaches such as using multiplex PCR and
MiSeq sequencing on pools of leaves with symptoms from the field (MPSeqM tool;
Gautier et al., 2023). All these markers require a thorough understanding of the
genotypes that are associated with virulent and avirulent phenotypes and the
ability to predict the interaction phenotype associated with a new allele, so
that the results can accurately be analysed to determine the frequency of
avirulent and virulent individuals. The knowledge of the specific pathosystem
must also be considered when interpreting these markers. For example, the
masking by AvrLm7 must be considered when interpreting the phenotype of isolates
based on the genotype of AvrLm3 and AvrLm9.
5 RESISTANCE GENES: THEIR CHARACTERIZATION AND APPLICATIONS
5.1 AUSTRALIA
One of the major elements in managing blackleg is the increased genetic
diversity from breeding programmes, especially in Australia and France. When
effective, major gene resistance is the most effective way to control the
disease (Geffersa et al., 2023). In Australia, 11 major R genes (Rlm1, Rlm2,
Rlm3, Rlm4, Rlm6, Rlm7, Rlm9, LepR1, LepR2, LepR3 and RlmS) are now present in
canola cultivars, a large increase from only three (Rlm3, Rlm4 and Rlm9) in the
early 2000s (Cowling, 2007; Van de Wouw, Marcroft, et al., 2021). However, the
pathogen evolves and adapts to selection pressure quickly, and as a consequence,
major gene resistance has been broken down within relatively short periods
(Sprague et al., 2006;Van de Wouw, Marcroft, et al., 2014; Van de Wouw, Sheedy,
et al., 2022). Rlm7 was ineffective in regions of Australia without varieties
carrying it being commercially grown, probably due to the dual-specificity of
the AvrLm4-7 gene in pathogen populations. In this scenario, cultivars
harbouring Rlm4 resistance were grown on a wide scale for several years, leading
to the selection of isolates that were not only virulent towards Rlm4 but also
towards Rlm7 (Van de Wouw, Sheedy, et al., 2022). With the improved
understanding of the complex interaction between various genes in the
blackleg–canola pathosystem, it was possible to explain the Rlm7 resistance
situation in Australia.
Despite the pathogen's evolutionary potential and R gene breakdowns, Australian
growers are keeping losses associated with blackleg to a minimum, mainly due to
the development of blackleg resistance groups and ongoing monitoring of the
pathogen population. All canola cultivars in Australia are characterized for
their major gene resistance using a combination of differential isolates and
molecular markers for the cloned R genes (Marcroft, Van de Wouw, et al., 2012;
Van de Wouw, Zhang, et al., 2022). Cultivars are assigned a resistance group
(Table 1), with each letter representing a different R gene. This information is
included in the Blackleg Management Guide
(https://grdc.com.au/resources-and-publications/all-publications/factsheets/2023/blackleg-management-guide)
for growers to select cultivars with different R genes for rotation in space and
time. This management system was based on the research of Marcroft, Van de Wouw,
et al. (2012), which demonstrated that disease could be minimized when R genes
are rotated to alleviate selection pressure on the pathogen population. The
effectiveness of each resistance group is monitored in 32 field sites across the
Australian canola-growing regions, and warnings are provided to growers when
resistance is being overcome (Van de Wouw, Marcroft, et al., 2014; Van de Wouw,
Sheedy, et al.,2022). This early warning system has allowed growers to change
cultivars from a different resistance group or to make fungicide application
decisions to minimize the impact of disease, preventing economic losses due to
severe blackleg (Van de Wouw, Marcroft, et al., 2014).
TABLE 1. Classification of resistance (R) genes as groups in Australia and
Canada (Van de Wouw & Howlett, 2020).
R gene Australian resistance group Canadian resistance group Rlm1/LepR3 Group A
Group A Rlm2 Group B Rlm3 Group C Group C Rlm4 Group B Group E1 Rlm5 Group G
Rlm6 Group F Rlm7 Group H Group E2 Rlm9 Group F RlmS Group S Group G LepR1 Group
D Group D LepR2 Group H
While several studies mapping blackleg quantitative trait loci (QTLs) from older
Australian varieties have suggested considerable conservation of a few major
QTLs in breeding programmes (Raman et al., 2012), the specific underlying
genetics of QR in current Australian cultivars is not publicly known. All
commercial varieties are released with a blackleg rating, reflecting the overall
resistance, considering the effect of both major-gene resistance and QR. The
ratings are provided to growers as part of the blackleg management guide, as
well as the BlacklegCM App, a decision support tool available online to growers.
Growers can then use this information to select cultivars suitable for their
growing conditions and pathogen populations in their region.
5.2 CANADA
A Blackleg Steering Committee introduced a labelling system in Canada to
identify the R genes present in canola cultivars, following the success of this
practice in Australia (Table 1). Several seed companies have voluntarily
provided the information on seed bags. This strategy was officially implemented
in the 2018 growing season. At the same time, a study was conducted to
investigate the impact of R gene rotation (Cornelsen et al., 2021; Rashid
et al., 2022), and the next phase is to introduce the R gene rotation strategy
that growers can practically do, especially for growing canola in tight
rotations where the blackleg levels have noticeably increased.
5.3 EUROPE
Rapeseed breeding took place in France very early, with a strong public–private
partnership that fostered fruitful interactions between private breeders,
technical institutes (CETIOM/Terres Inovia) and INRA scientists. In 1977, an
association to promote the breeding of oil crop (Promosol) brought together INRA
(now INRAE), Terres Inovia and a consortium of seed companies, which set
priorities and tasks in oilseed crop variety selection and implemented them
through a research fund contributed from its members to boost and coordinate
research into breeding, particularly in blackleg resistance. Terres Inovia
financially supported the research on L. maculans right from the initial work on
disease epidemiology (Lacoste et al., 1969) and disseminated the results of L.
maculans research using various extension avenues. Similarly, Promosol organizes
the annual rapeseed breeding workshops, a unique opportunity for INRA scientists
and breeders to meet.
With the need to reach a high level of resistance to register and market a
variety, efforts have rapidly been made to introduce major resistance genes that
were initially rapidly broken down (Rouxel, Penaud, et al., 2003). At the time,
Rlm genes were sequentially used in varieties with independent strategies by
breeders and a lack of information on the Rlm content of varieties to growers
(Rouxel & Balesdent, 2017). Later on, the close collaboration between
researchers and private breeders ensured rapid adoption of research findings,
leading to effective disease countermeasures and substantial market gains. For
example, the swift integration of Rlm1 resistance into rapeseed varieties in
1995, before its genetic determinism was established, resulted in the launch of
totally resistant varieties, making a breeding company the market leader in
France. However, the breakdown of Rlm1 resistance within merely 3 years
following its release prompted breeders to integrate the concept of ‘protection’
for major R genes into genotypes with high levels of QR (Brun et al., 2010),
ensuring continued field performance despite evolving pathogen populations. As a
result, some Rlm7 genotypes continue to perform well, even though pathogen
populations have become virulent in many areas. This was also facilitated by the
recent dissemination by Terres Inovia of information on the content of French
varieties in effective Rlm genes or the presence of QR exclusively disseminated
through the Myvar website (Figure 4). The dissemination of the information was a
true revolution because for a long time breeders have been very reluctant to
have this information publicized. Unfortunately, such a tool is unavailable at
the EU (or European) level due to the few common varieties between the countries
(and different registration processes) and the lack of characterization of Rlm
genes in other EU countries.
FIGURE 4
Open in figure viewerPowerPoint
An example of recommendations provided to French farmers on the use of
appropriate cultivars for specific regions via the Myvar website
(https://www.myvar.fr/) of Terres Inovia. Note that, in contrast to the practice
in Australia or Canada, the efficient resistance genes (here Rlm3, Rlm7 or RlmS)
or the exclusive presence of quantitative resistance to Leptosphaeria maculans
are indicated.
5.4 GENETICS AND GENOMICS BEHIND THE VARIETY RESISTANCE ON MAJOR GENE RESISTANCE
In Canada, the blackleg resistance genes LepR1 and LepR2 were the first R genes
identified and mapped in B. napus introgressed from B. rapa subsp. sylvestris
(Yu et al., 2005). Later LepR3 and LepR4, also originating from B. rapa subsp.
sylvestris, and BLMR1 and BLMR2 in a B. napus cultivar Surpass 400 were also
mapped (Long et al., 2011; Yu et al., 2008, 2013). Identification of B-genome
resistance and progress in introgressing it into B. napus canola has been
reported (Rashid et al., 2018). Fine mapping of R genes (Fu et al., 2019) or
finding markers linked to R genes (Rashid et al., 2018) are additional
undertakings in assisting blackleg resistance breeding in Canada. These efforts
can be traced back to the early days when a SCAR marker was developed to monitor
canola resistance against PG-3 of L. maculans (Dusabenyagasani &
Fernando, 2008). The need to breed novel blackleg resistance into Canadian
cultivars continued with private and public breeding programmes, including that
at the University of Manitoba (Duncan et al., 2020). LepR1 and LepR3 have been
used in several canola cultivars.
Following the work to categorize L. maculans isolates into pathogenicity groups
(PGs, see above), there was a concerted effort to define the resistance genes
creating the differential responses and to define a wider selection of effective
resistance sources for breeding. Researchers built on the R gene mapping
produced from winter oilseed rape in Europe (Delourme et al., 2004, 2006) and
worked to further define the R loci for effective marker-based selection in
breeding programmes and to introgress new R genes from winter germplasm into
spring-type canola. Germplasm sources incorporating resistance from B. rapa
subsp. sylvestris were used to identify, map and introgress four novel R genes,
LepR1, LepR2, LepR3 and LepR4 (Yu et al., 2005, 2007, 2008), while
collaborations with colleagues in Australia also allowed for QTL mapping studies
to define QR sources for inclusion in breeding programmes (Larkan, Raman,
et al., 2016). A set of introgression lines, each containing a single R gene
incorporated into the same susceptible background, was developed (Larkan, Yu,
et al., 2016). These lines provide unambiguous material for pathotyping (Alnajar
et al., 2022; Van de Wouw et al., 2024) and field studies (Rashid et al., 2022)
as well as in precise transcriptomic studies (Becker et al., 2019; Haddadi
et al., 2019).
Despite progress in identifying new R genes since late 1990, it was nearly two
decades later that the structure of B. napus R genes against blackleg came to
light when LepR3 was cloned (Larkan et al., 2013). LepR3 is a membrane-bound
receptor-like protein with an extracellular leucine-rich repeat (LRR-RLP).
Assuming the classic gene-for-gene interaction, AvrLep3 was considered the
putative L. maculans effector protein recognized by LepR3, though previous work
had also shown that the effector AvrLm1 triggered a hypersensitive response in
Surpass 400, leading to the assumption that the variety also contained Rlm1 (Van
de Wouw et al., 2009). Cloning LepR3 also revealed that AvrLm1 is the cognate
effector protein and the first example of the perception of one effector by two
independent and genetically unlinked R genes, Rlm1 and LepR3, in the L.
maculans–Brassica pathosystem. The knowledge from cloning the first R gene and
advances in genomics expedited the successful cloning of several additional R
genes, namely, Rlm2, Rlm9, Rlm4 and Rlm7. Rlm2 was revealed to be an allelic
variant of LepR3 (Haddadi et al., 2022; Larkan et al., 2014, 2015). Rlm4, Rlm7
and Rlm9, forming a genetically tight R gene cluster on the lower arm of
chromosome A07 of B. napus (Larkan, Yu, et al., 2016), are also cell surface
receptors, albeit belonging to the Wall-Associated-Kinase-Like (WAKL) class of R
proteins, the first discovered in Brassica species (Haddadi et al., 2022; Larkan
et al., 2020). The A07 WAKL R gene cluster varies from one to three copies in
different B. napus accessions. The remaining member, Rlm3, has recently been
cloned, with initial data suggesting its resistance phenotype expression
requires multiple paralogous WAKL genes (authors' unpublished data). Further
characterization of these WAKL proteins will enhance understanding of the
intricate R and Avr interplay governing pathogen recognition (Borhan
et al., 2022).
Both protein pull-down and yeast two-hybrid assays used to identify host plant
targets of several effector proteins were generally unsuccessful, except for the
AvrLm1 target, which was determined to be the B. napus Mitogen-Activated Protein
kinase 9 (BnMPK9) (Ma et al., 2018). Recognition of AvrLm1 activates MPK9
phosphorylation and accumulation, inducing cell death and probably paving the
way for the necrotrophic growth stage of L. maculans. It may be a challenge to
identify a cytoplasmic host target for such an apoplastic pathogen, as AvrLm1
remains the only effector protein known to date from L. maculans, with only one
cysteine residue making it more likely to be translocated to the host plant
cytoplasm. Further advances in proteomics may help identify direct or indirect
effector–R protein interaction between L. maculans and canola, facilitating the
design of novel R genes.
Work is ongoing to increase the diversity of blackleg resistance genetics in
Canadian varieties using novel resistance sources. Researchers at Agriculture &
Agri-Food Canada have screened large collections of domesticated and exotic B.
napus germplasm with well-characterized L. maculans differential isolates,
discovering two novel R genes, LepR5 and LepR6, that have been mapped to
chromosomes A01 and C03, respectively (Larkan et al., 2019). These findings also
helped to identify resistant accessions out of B. oleracea from Korea (Robin
et al., 2017) while Balesdent et al. (2013) defined the Rlm11 locus, an as-yet
undeployed R gene previously identified from B. rapa. The latter has been
introgressed into B. napus canola (authors' unpublished data;
https://canoladigest.ca/science-edition-2022/a-new-gene-for-blackleg-resistance/).
Several of these novel resistance sources have proven to be highly effective
against diverse collections of L. maculans isolates and have been provided to
Canadian and international canola breeding programmes, promising to strengthen
blackleg resistance breeding efforts worldwide.
5.5 GENETICS AND GENOMICS BEHIND THE VARIETY RESISTANCE ON QR
QR is attributed to multiple genes across several genomic regions of B. napus
(Delourme et al., 2006; Kumar et al., 2018; Rimmer, 2006), with many shared loci
found in canola cultivars (Raman et al., 2018). However, QR might be very
different between spring and winter varieties due to different cropping and
environmental conditions, including the duration of cropping. For the same
reason, they may also be different for spring types grown in Canada or
Australia. Also, the variability of the environmental conditions that winter
types experience has often led to the identification of weakly robust QTLs from
one experiment to the other (Delourme et al., 2006). Poland et al. (2009)
proposed that QR might also stem from weaker genes, reducing phytoalexin
production and/or signal transduction. For blackleg, QR may also be associated
with uncharacterized R genes or partly defeated R genes (Fopa Fomeju
et al., 2014; Jestin et al., 2011; Larkan, Raman, et al., 2016; Raman
et al., 2016, 2018), as also suggested by the AvrLmSTEE98–RlmSTEE98 interaction
(Jiquel et al., 2021). Canola cultivars with QR can still be infected by
blackleg, albeit at lower disease levels (Huang et al., 2009; Soomro, 2016).
While often referred to as adult-plant resistance, QR can also hinder infection
development in canola seedlings, limiting stem infection originating from
infected cotyledons or lower leaves (Hubbard & Peng, 2018; Schnippenkoetter
et al., 2021), explaining the general success of using QR against blackleg in
western Canada. However, in fields affected by hail injuries, QR may prove
insufficient.
In Canada, an examination of the standard hybrid cultivar 74–44 BL (Rlm3, RlmS)
involving inoculation with L. maculans isolates capable of evading these R genes
revealed moderate but consistent race-nonspecific resistance at both cotyledon
and adult-plant stages. RNA-seq analysis showed highly elevated expression of
genes involved in programmed cell death (PCD), reactive oxygen species (ROS),
signal transduction and intracellular endomembrane transport relative to a
susceptible control (Hubbard et al., 2020). ROS appeared to trigger rapid cell
death, restricting the colonization of cotyledons by L. maculans. The results
established preliminary modes of action for QR, which differ from those of
major-gene resistance such as Rlm1 and AvrLm1, where the defence response is
induced via robust activation of salicylic acid and jasmonic acid pathways (Zhai
et al., 2021). These studies offer some insights into blackleg QR in canola,
supporting the industry's ongoing efforts to improve QR.
Canadian breeders initially incorporated the QR, possibly from the French
variety Jet Neuf, in the 1990s (Rimmer et al., 1998). However, more information
is needed regarding additional sources used for ongoing QR improvements.
Selecting for QR is inherently challenging, primarily due to its operation
during an extended biotrophic phase and the reliance on extensive field trials
for identification, which can be affected by environmental conditions (Fitt
et al., 2006; Huang et al., 2016; Kumar et al., 2018). Factors like elevated
temperatures may diminish QR for some varieties (Huang et al., 2009) while not
affecting others (Hubbard & Peng, 2018). A new approach has been developed to
improve QR identification based on the growth kinetics of L. maculans in canola
measured in the amount of fungal DNA using droplet-digital PCR (ddPCR; McGregor
et al., 2019). The combination of L. maculans isolates used in the inoculation
showed proficiency in evading known R genes, with results exhibiting a
significant correlation with QR performances observed in field trials between
2019 and 2022 (data not shown). Extending this approach to quantify QR
associated with commercial canola hybrids revealed over 95% exhibiting robust
resistance, underscoring QR's pivotal role in blackleg management. This method
may also be employed to label blackleg QR in canola cultivars alongside major R
genes.
A crucial element supporting the use of QR in Canada is the longstanding public
cooperative trials for blackleg resistance conducted at multiple locations in
western Canada annually for over 30 years. The programme actively involves all
breeding companies, and the designated test sites are maintained as blackleg
nurseries, ensuring high disease pressure. The multilocation approach also
facilitates exposure to pathogen populations with diverse Vir profiles across
the region (Figure 3). This test strategy also captures changes in local
pathogen populations over time. Similar to major-gene resistance, QR would also
undergo rigorous assessment in these public trials, instilling confidence in its
efficacy in blackleg management. When combined with major gene resistance, QR
offers additional benefits by mitigating selection pressure against major R
genes (Brun et al., 2010; Delourme et al., 2014). The pivotal role of QR in
blackleg management in western Canada is unique and noteworthy; it is possibly
related to generally lighter disease pressure under current crop rotation
practices, cool and dry spring conditions inconducive for infection, and a
relatively short crop season (about 100 days) for disease infection and
development.
In Europe, and mainly France, QR has always been advised by researchers and
Terres Inovia to avoid unique reliance on major genes, famed to be of low
durability (the counterexample being Rlm7, with a very long time of efficiency
despite being widely grown; Balesdent et al., 2022). Due to the complexity of
identifying and characterizing QR, some breeders in France, following Terres
Inovia's recommendations, have opted to select exclusively for QR, which has
helped to raise the general level of resistance in winter varieties grown in
Europe (Figure 4). As a consequence, one of the most popular cultivars to-date
is a cultivar known to only have QR.
Besides major gene resistance in Australia, QR plays an essential role in
minimizing blackleg impact. Breeders effectively select for it using blackleg
nurseries where high-disease pressure is maintained by sowing directly into the
previous year's canola stubble. Under these situations, the breeding material
being screened is exposed to diverse and sexually reproducing pathogen
populations. Over time, pathogen populations at these sites have constantly
evolved, reflecting changes in the Australian population and allowing breeders
to constantly stay ahead of changing pathogen populations. The continuous
deployment of improved resistance has led to a shorter turnover of cultivars; in
the early 2000s, cultivars remained on the market for an average of 7.4 years,
which has decreased to only 4.8 years in the 2020s.
The first public genome of B. napus was sequenced by Genoscope in a broad
international consortium (Chalhoub et al., 2014), and accompanied by numerous
initiatives to sequence related species (Devisetty et al., 2014; Liu
et al., 2014; Song et al., 2021; Yang et al., 2016) and multiple genotypes of B.
napus to reach a pangenome for the species (Song et al., 2020; Zou, Mao,
et al., 2019). These genome data were instrumental for the metatranscriptomics
of L. maculans's life cycle interacting with plants and L. biglobosa (Gay
et al., 2021, 2023). This was achieved in the course of an INRA-led project and
carried out by Genoscope performing RNA-seq on samples corresponding to all
stages of L. maculans infection of its host plants, either alive or dead, under
a range of conditions (Gay et al., 2021), allowing us to identify 1200 genes, 9%
of the genes of the fungus, exclusively expressed at a specific stage or trophic
mode during the infection process. These waves of expression are strongly
enriched in genes encoding effectors and hosted in AT-isochores. The
comprehensive understanding of the L. maculans life cycle was substantially
improved by studying various B. napus genotypes with diverse levels of QR and
samples involving L. biglobosa (Gay et al., 2023).
6 FUNGICIDES AND OTHER STRATEGIES FOR BLACKLEG MANAGEMENT
Fungicide treatments against blackleg are uncommon in continental Europe where
fungicides are mostly targeted at Sclerotinia stem rot, whereas their
application varies noticeably in Australia and Canada. Fungicides effectively
reduce blackleg disease in Australia (Elliott & Marcroft, 2011; Khangura &
Barbetti, 2002; Marcroft & Potter, 2008). Their usage has surged, with recent
surveys showing that 95% of growers apply at least one fungicide per growing
season, and most apply at least two (Van de Wouw, Marcroft, et al., 2021). In
Australia, 13 different fungicides are now registered for blackleg control,
representing three modes of action: demethylation inhibitors (DMI, Group 3),
succinate dehydrogenase inhibitors (SDHI, Group 7) and the quinone outside
inhibitors (QoI, Group 11). These fungicides can be applied as seed dressings,
amended to the fertilizer or as foliar sprays at either 4- to 10-leaf or 30%
bloom growth stages. Due to broad specificity, these fungicides often also
provide control towards other diseases such as Sclerotinia stem rot (Sclerotinia
sclerotiorum), black spot (Alternaria brassicae), powdery mildew (Erysiphe spp.)
and white leaf spot (Pseudocercosphaerella capsellae).
The registration of foliar fungicides has been a game changer against blackleg
in Australia, providing growers with an in-season option to control disease.
Previously, all management decisions were made before seeding, for example,
cultivar choice, seed-dressing or fungicide-amended fertilizer at sowing and
paddock location. Once the crop was established, there were no more
opportunities to deal with the disease. When conditions are conducive to
blackleg infection, growers have this added tool under their belt to spray at 4-
to 10-leaf and 30% bloom growth stages when necessary. The blackleg monitoring
sites mentioned earlier are used to provide growers with information regarding
the effectiveness of genetics and seasonal disease conditions for additional
actions. For example, in 2016, when conditions were optimal for blackleg,
growers were advised to spray fungicides at the 4- to 10-leaf stage. Data from
agronomists suggested that this advice alone led to 0.5–1.0 t/ha yield increases
(relative to untreated fields) over an area of >0.5 million ha. Conversely, in
2017, when conditions were much drier, growers were advised that fungicides were
unnecessary due to low disease conditions.
Fungicide use has become crucial and an integral tool for Australian growers in
managing blackleg, but due to the evolutionary potential of the fungus, it also
poses a risk of fungicide resistance. Fungicide resistance has already been
detected in 15% of populations screened across Australia for DMI fungicides (Van
de Wouw et al., 2017; Van de Wouw, Scanlan, et al., 2021; Yang et al., 2020),
and detailed analysis revealed resistance frequencies as high as 32% within
specific populations, leading to field failure (Scanlan et al., 2023).
International surveys have also shown DMI resistance in countries like Czechia,
Germany and the UK (Fajemisin et al., 2022; King et al., 2024; Scanlan
et al., 2023, 2024). No resistance to the DMIs was detected in France (King
et al., 2024; Scanlan et al., 2024), and fortunately, no resistance has been
detected for SDHI or QoI fungicide classes so far (Van de Wouw, Scanlan,
et al., 2021). Fungicides will continue to play a vital role in blackleg
management in Australia. Therefore, strategies to minimize resistance evolution
to SDHI and QoI fungicides and ongoing monitoring for resistant development are
necessary. Additionally, once it occurs, strategies for managing fungicide
resistance are crucial for growers to combat blackleg disease effectively.
When blackleg crept up in western Canada in the 2010s, in-crop fungicide
treatments were recommended to mitigate the disease impact, including
azoxystrobin (Quadris), propiconazole (Tilt), pyraclostrobin (Headline) and a
premixture of propiconazole and azoxystrobin (Quilt Xcel). A 4-year study across
five locations assessed the efficacy and benefits of the treatment in relation
to crop stage and variety resistance, and the results demonstrated that all
fungicides, except propiconazole (a DMI), generally reduced the blackleg when
applied at 2- to 4-leaf stages, irrespective of cultivar resistance (Peng
et al., 2021). Late treatment at bolting proved ineffective, and two
applications at both stages did not further improve the efficacy over the early
treatment alone. Fungicide treatment yielded a slight benefit only for
susceptible cultivars with a mean disease incidence exceeding 30%. At the same
time, it showed no yield benefit on resistant or moderately resistant cultivars
despite consistent disease reductions. Based on the results, routine in-crop
fungicide application is discouraged in western Canada, where resistant canola
cultivars are prevalent. In the past decade, the overall use of fungicide on
canola has decreased by at least 50% based on the estimate of BASF Canada,
resulting in significant savings to growers each year.
However, blackleg has remained at low to moderate levels in western Canada
(Figure 2) despite the widespread use of resistant cultivars, with severe
disease reported in isolated cases each year. Drawing inspiration from Australia
on seed dressing, several studies in Canada evaluated a range of new systemic
fungicides, especially SDHI. The treatment with either fluopyram or
pydiflumetofen demonstrated efficacy against foliar infection on susceptible
canola, while the effect appeared negligible on resistant cultivars under field
conditions (Padmathilake et al., 2022; Peng et al., 2020). Nevertheless, given
the low cost and easy application, SDHI seed treatment may serve as reasonable
insurance for growers, especially for protecting against infection via wounds on
cotyledons (Huang et al., 2022).
7 CONCLUSIONS AND FUTURE DIRECTIONS
This review unfolds a compelling success story through international
collaborations in the battle against blackleg disease, offering insights for
management in sustainable canola/rapeseed production. The cloning of Avr genes
has revealed unique gene-for-gene interactions and set the stage for developing
markers essential for efficient pathogen population analysis. The adoption of
genomics, coupled with a genome-to-paddock approach, has proven instrumental in
unravelling the complex dynamics of the pathogen's behaviour. Monitoring
pathogen populations using KASP markers or MPSeqM tool provides fundamentals for
R gene deployment strategies, facilitating precise and adaptive management
practices.
Despite these successes, the war against blackleg is enduring, with the
pathogen's evolution necessitating ongoing research to stay ahead of future
epidemics and keeping in mind the possible future threat due to L. biglobosa.
Focusing on critical needs and embracing novel technologies will be crucial.
Host genetics, mainly through improved knowledge of metagenomics and gene
editing, remains a cornerstone for effective blackleg management. Tapping into
additional resources may be achieved by editing out specific pathogenicity genes
from canola varieties to develop potentially acquired disease tolerance. The
impact of climate change on the canola–blackleg pathosystem also requires our
attention, emphasizing the need for research on adaptive strategies. It has been
found that elevated temperatures negatively impact cultivars carrying major gene
resistance (Rlm6) (Huang et al., 2006). Hubbard and Peng (2018) reported that
cultivars having QR are still effective in elevated temperatures. In contrast,
Noel et al. (2022) reported that with high temperatures (25°C), the efficacy of
QR was reduced. However, more studies should be done in the future to study the
impact of temperature on qualitative and QR. Continuous monitoring of pathogen
populations is a crucial building block for blackleg resistance deployment and
adaptive management, enabling us to stay ahead of the curve in response to
pathogen population changes. Looking ahead, the integration of artificial
intelligence holds promise for generating and analysing ‘big data’ more
efficiently, providing comprehensive information on pathogen populations,
variety resistance and the outcomes of disease management practices. The
continuous interactions between research and the socio-economic world are
illustrated in this review, with different levels of recommendations for farmers
to ensure the best use of rare resources (Blackleg management guide in
Australia, labelling system in Canada, Myvar in France). The next step is to
have a global reflection between research and the socio-economic world on how to
use and disseminate new R genes to ensure they are as durable as possible. In a
case study in France, two still unreleased R genes (in Europe), Rlm6 (Chèvre
et al., 1997) and Rlm11 (Balesdent et al., 2013), were the basis for creating an
organizational innovation called Club Phoma that brings together stakeholders
for sustainable management of Rlm genes. This approach ultimately aims to
collectively manage the reasoned dissemination of these genes according to
co-designed deployment strategies, introduce them in different varieties, and
monitor deployment performance to better manage evolution of the pathogen
population. Collaborative efforts like the Club Phoma will facilitate the
efforts, aligning with the goal of sustainable agriculture.
The disease could very well spread to new areas and can be exacerbated by
climate change. South Africa and Tunisia are already experiencing blackleg,
while their canola/oilseed rape acreage is increasing. However, China is still
reporting only L. biglobosa, but it is now spreading to non-traditional areas
such as Xinjiang. As we navigate these challenges, the future appears bright for
the effective and sustainable management of blackleg on canola/rapeseed. Much
ongoing research is poised to usher in a new era for the industry.
ACKNOWLEDGEMENTS
A. Van de Wouw thanks the Grains Research and Development Corporation for
funding. W. G. D. Fernando, G. Peng, H. Borhan and N. Larkan thank the Canola
Council of Canada, SaskCanola, Alberta Canola Commission, Manitoba Canola
Growers Association, The Western Grains Research Foundation, federal (CAP and
Growing Forward 1 and 2) and provincial funding (CAP and ARDI) for funding. T.
Rouxel thanks Xavier Pinochet (Terres Inovia) for information on European
rapeseed cropping. Bioger (T. Rouxel) benefits from the support of Saclay Plant
Sciences-SPS (ANR-17-EUR-0007). All authors thank Malini Anudya Jayawardana for
proofreading and editing the manuscript.
OPEN RESEARCH
DATA AVAILABILITY STATEMENT
Data sharing is not applicable to this article as no new data were created.
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* FIGURES
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* Effect of rotation of canola (Brassica napus) cultivars with different
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canola-blackleg management toolbox
K. Rasanie E. Padmathilake, Paula S. Parks, Robert H. Gulden, Jonathan
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Plant Pathology
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© 2024 The Author(s). Plant Pathology published by John Wiley & Sons Ltd on
behalf of British Society for Plant Pathology.
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KEYWORDS
* Brassica napus
* canola/rapeseed
* disease control
* genetic resistance
* Leptosphaeria maculans
* virulence/avirulence
PUBLICATION HISTORY
* Version of Record online: 28 October 2024
* Manuscript accepted: 16 July 2024
* Manuscript revised: 08 July 2024
* Manuscript received: 06 April 2024
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