Skip to main content
NCBI home page
Molecular Plant Pathology logoLink to Molecular Plant Pathology
. 2017 Sep 20;19(4):1012–1016. doi: 10.1111/mpp.12574

One gene‐one name: the AvrLmJ1 avirulence gene of Leptosphaeria maculans is AvrLm5

Clémence Plissonneau 1, Thierry Rouxel 1, Anne‐Marie Chèvre 2, Angela P Van De Wouw 3,✉, Marie‐Hélène Balesdent 1,✉
PMCID: PMC6638039  PMID: 28661570

Summary

Leptosphaeria maculans, the causal agent of blackleg disease, interacts with Brassica napus (oilseed rape, canola) and other Brassica hosts in a gene‐for‐gene manner. The avirulence gene AvrLmJ1 has been cloned previously and shown to interact with an unidentified Brassica juncea resistance gene. In this study, we show that the AvrLmJ1 gene maps to the same position as the AvrLm5 locus. Furthermore, isolates complemented with the AvrLmJ1 locus confer avirulence towards B. juncea genotypes harbouring Rlm5. These findings demonstrate that AvrLmJ1 is AvrLm5 and highlight the need for shared resources to characterize accurately avirulence and/or resistance genes.

Keywords: avirulence, Brassica napus, canola, oilseed rape, resistance

Blackleg disease, caused by the plant pathogen Leptosphaeria maculans, is the major disease of oilseed rape (canola, Brassica napus) worldwide (Fitt et al., 2006). The L. maculans–B. napus interaction follows Flor's gene‐for‐gene scenario, whereby for each resistance gene in the host there is a corresponding avirulence gene in the pathogen (Balesdent et al., 2005; Flor, 1955). Seven avirulence genes have been cloned from L. maculans; AvrLm1, AvrLm2, AvrLm3, AvrLm4–7, AvrLm6, AvrLm11 and AvrLmJ1 (Balesdent et al., 2013; Fudal et al., 2007; Ghanbarnia et al., 2015; Gout et al., 2006; Parlange et al., 2009; Plissonneau et al., 2016; Van de Wouw et al., 2014). Conversely, at least 18 resistance genes have been reported for the L. maculans–Brassica interaction with only two cloned (Delourme et al., 2004, 2006; Larkan et al., 2013, 2015; Long et al., 2011; Rimmer, 2006; Van de Wouw et al., 2009; Yu et al., 2005, 2008). However, there has been considerable confusion in resistance gene naming with independent naming of genes by independent research groups. This is an unfortunate commonality in plant–pathogen interactions as illustrated, for example, in the rice–Magnaporthe oryzae model (Ballini et al., 2008). This is mostly a result of the difficulty in developing and sharing common sets of fixed, but adaptable, differential pathogen isolates, with an identified and fixed presence of avirulence genes, together with plant genotypes with an identified and fixed presence of resistance genes. In the case of differential isolates in particular, this is slowed down, or even made fully impossible, by import restrictions established in some parts of the world, which ban the import of biological material that could be used to demonstrate the identity of a resistance gene in geographically or genetically distant plant material. In the case of the L. maculans–Brassica interaction, independent naming of resistance genes was initially a result of the use of different parent plant genotypes, some of which corresponded to proprietary material with no easy‐to‐trace pedigree and not available to the whole community, and the generation of different genetics maps initially using markers that were difficult to transpose from one group to another [for example, random‐amplified polymorphic DNA (RAPD) and amplified fragment length polymorphism (AFLP)] (Rimmer, 2006). In addition, part of the initial identification of resistance loci was performed before the AvrLm‐Rlm gene‐for‐gene interaction was genetically identified and considered as the rule in this system, and the isolates used for the identification of resistance loci were either field populations or ill‐defined isolates in terms of avirulence gene content (Delourme et al., 2006). Nowadays, most of the groups studying the L. maculans–Brassica interaction use a common AvrLmx‐Rlmx terminology. Moreover, the generation of genetically bred isolates (including transgenic isolates) harbouring only a limited number of characterized avirulence genes, the identification of the resistance gene complement of some of the genotypes that were employed in ancient crosses using the genetically bred isolates, and the transposition of markers from one genetic map to another to confuse the locations of independently named resistance genes have allowed, with time, the reassessment of ancient studies, and have shown that many of the resistance genes previously described could be ascribed to the new terminology [e.g. LEM1, LmR1, CRLMm and CRLMrb identified in Canada or Australia and later on confused with the single Rlm4 gene (Delourme et al., 2006; Rimmer, 2006)].

Recently, Van de Wouw et al. (2014) reported the cloning of the L. maculans avirulence gene, termed AvrLmJ1, which induces a resistance response in three B. juncea (brown mustard) genotypes, including cv. Aurea. The cultivar Aurea has been described previously as harbouring two major genes for resistance, Rlm5 and Rlm6, and the cognate avirulence genes, AvrLm5 and AvrLm6, have been found to be genetically unlinked (Balesdent et al., 2002). AvrLmJ1 was identified as a gene conferring avirulence towards an unknown B. juncea resistance gene. Crosses were established between isolate IBCN18 (M1), which was virulent towards all B. juncea lines tested, and an avirulent control isolate, which allowed the mapping of the gene region conferring virulence towards B. juncea (Cozijnsen et al., 2000). Within the identified gene region, a single candidate gene, Lema_uP070880.2, within an AT‐rich region of the L. maculans genome was identified. Complementation constructs were generated with the candidate gene and, when transformed into isolate IBCN18, conferred avirulence towards the B. juncea cultivars Aurea, Stoke and Forge, confirming a role in avirulence towards B. juncea (Van de Wouw et al., 2014). AvrLm6 has been cloned previously (Fudal et al., 2007) and is distinct from AvrLmJ1. Although Van de Wouw et al. (2014) postulated that AvrLmJ1 could, in fact, be AvrLm5, the lack of B. juncea genotypes with only Rlm5 prevented them from reaching this conclusion. In the current study, we show, by two complementary approaches, that AvrLmJ1 is indeed AvrLm5.

First, to test whether AvrLmJ1 confers avirulence towards Rlm5 plant genotypes, five independent complementation isolates (IBCN18 + AvrLmJ1 #2, #3, #5, #6 and #7), generated by Van de Wouw et al. (2014), were screened for virulence towards a range of Rlm5 genotypes. Plants of B. juncea cv. Aurea usually harbour both Rlm5 and Rlm6. However, as a result of insufficient fixing of the variety, some individual plants of Aurea only contained Rlm5. The identification and selfing of some individual plants, followed by mass pollination under pollen‐proof bags, allowed the generation of S2 B. juncea lines 99.150.2.1 and 99.151.2.1 with Rlm5 only (Balesdent et al., 2002). Heterogeneous behaviour for Rlm5 was still evident in the S2 lines and, in the current study, we undertook an additional round of mass pollination in the glasshouse of individual Rlm5‐only plants to generate line 08.150.3.4 with improved homogeneous presence of Rlm5 (Table 1). For pathogenicity tests, isolates were grown on 20% V8 medium to produce conidia. Conidia (10 µL, 107 spores/mL) were inoculated onto wounded cotyledons of 10‐day‐old seedlings. Symptoms were scored at 14–21 days post‐inoculation on a 1–6 scale (Balesdent et al., 2005), with scores of 1–3 and 4–6 corresponding to avirulent and virulent phenotypes, respectively. In addition to the complementation isolates, the wild‐type isolate IBCN18 (genotype Av1‐2‐4‐7, i.e. avirulent on Rlm1, Rlm2, Rlm4 and Rlm7) and control isolates JN2 (Av5‐6‐7‐8), JN3 (Av1‐4‐5‐6‐7‐8), 19.4.24 (Av3‐5‐6‐8) and v45.30 (Av2‐7) were also used, as well as a range of control cultivars with different resistance gene content (Table 1). All isolates were virulent towards the susceptible control genotype Westar (Table 2). Isolate IBCN18 was virulent towards all genotypes harbouring the Rlm5 gene, as expected. Complementation of isolate IBCN18 with the wild‐type copy of the AvrLmJ1 gene (IBCN18 + AvrLmJ1 isolates) led to avirulence on all genotypes harbouring Rlm5. For these complementation isolates, AvrLmJ1 did not confer avirulence towards the other B. juncea resistance gene Rlm6, nor did it confer avirulence towards the B. napus resistance genes Rlm1, Rlm2, Rlm3, Rlm4 or Rlm9 (Table 2). All control isolates behaved as expected based on their avirulence genotype. These results strongly suggest that AvrLmJ1 could be the gene previously genetically identified as AvrLm5.

Table 1.

Brassica cultivars and genotypes used in this study.

Species Cultivar/genotype Resistance genes Comments References
B. napus Westar None Susceptible control
B. napus Darmor MX Rlm6, Rlm9 Addition line with the Rlm6 gene from B. juncea Balesdent et al. (2005)
B. napus 03.22.3.1 Rlm3 Balesdent et al. (2002)
B. napus Bristol Rlm2, Rlm9 Balesdent et al. (2002); Delourme et al. (2006)
B. napus Columbus Rlm1, Rlm3 Balesdent et al. (2002)
B. napus Pixel Rlm4 Parlange et al. (2009)
B. juncea Aurea Rlm5, Rlm6 Balesdent et al. (2002)
B. juncea 99.150.2.1 Rlm5 Heterogeneous for the presence of Rlm5 Balesdent et al. (2002)
B. juncea 08.150.3.4 Rlm5 An improved selection from 99.150.2.1 with homogeneous presence of Rlm5 This study
Open in a new tab

Table 2.

Pathogenicity scores of Leptosphaeria maculans isolates screened on a range of Brassica genotypes.

Isolates * Cultivar/genotype (resistance genes)
Westar † (no R genes) Aurea V95 (Rlm5, Rlm6) 99.150.2.1 (Rlm5) 08.150.3.4 (Rlm5) DarmorMX (Rlm6, Rlm9) 03.22.3.1 (Rlm3) Bristol (Rlm2, Rlm9) Pixel (Rlm4) Columbus (Rlm1, Rlm3)
IBCN18 5 ‡ 4.4 4.3 5 5 4 2.5 1.4 1.8
IBCN18 + AvrLmJ1 #2 4.9 1.7 2 2.4 5 3.7 2.9 1.3 2.7
IBCN18 + AvrLmJ1 #3 5 1.5 2 2.5 5 4.1 2.6 1.4 2.7
IBCN18 + AvrLmJ1 #5 5 1.8 1.8 2.6 5 4 2.8 1.4 2.9
IBCN18 + AvrLmJ1 #6 6 1.9 2 2.4 5 4 2.6 1.2 2.9
IBCN18 + AvrLmJ1 #7 5.2 1.9 2.1 2.1 5 4.1 2.7 1.4 2.9
JN2 5.1 2.3 1.9 2 2.1 4.8 5 5 5
JN3 5 1.6 2.9 1.5 1.6 4.8 5 1.1 2.6
19.4.24 4 1.6 2.6 2.4 1 1.3 5 5 1.7
v45.30 4.5 3.8 4.5 4.7 4.3 3.5 1.5 4 4.5
Open in a new tab

*The avirulence genotypes of wild‐type isolates are as follows: IBCN18, Av1‐2‐4‐7; JN2, Av5‐6‐7‐8; JN3, Av1‐4‐5‐6‐7‐8; 19.4.24, Av3‐5‐6‐8; v45.30, Av2‐7. Isolate IBCN18 is virulent towards genotypes harbouring Rlm5. However, when complemented with avirulence gene AvrLmJ1 (isolates IBCN18 + AvrLmJ1 #2‐7), this virulence is lost, suggesting that AvrLmJ1 confers avirulence towards resistance gene Rlm5.

†The resistance gene content (Rlm) is indicated in parentheses.

‡Symptoms were scored at 16 days post‐inoculation on a 1–6 scale (Balesdent et al., 2005), with scores 1–3 and 4–6 corresponding to avirulent and virulent phenotypes, respectively. Susceptibility symptoms (indicated by mean pathogenicity scores greater than 3.0) are highlighted in grey.

AvrLm5 was first described in a cross between JN3 (Av1‐4‐5‐6‐7‐8, the reference sequenced isolate; Rouxel et al., 2011) and v29.3.1 (Av2–7), which is a progeny of isolate IBCN18 (Balesdent et al., 2002). Seventy‐one progeny isolates were screened for avirulence towards the set of genotypes harbouring Rlm5, as described above. Virulence towards Rlm5 segregated as a single gene [p(Chi2) = 0.166]. Using the Fonzie pipeline (Bally et al., 2010), minisatellite markers were identified from the genomic sequence of SuperContig7 (SC7), where AvrLmJ1 was found (Van de Wouw et al., 2014). In addition, markers corresponding to junctions between truncated repeated elements were identified, as described previously (Gout et al., 2006), in the proximity of AvrLmJ1. Eleven markers were found to be polymorphic between parental isolates in this region (Table S1, see Supporting Information). AvrLm5 mapped between markers jcAT11 and min 7.77 (Fig. 1), where AvrLmJ1 (Lema_uP070880.2) is located. Lema_uP070880.2 displays sequence polymorphism between the two parental isolates JN3 and v29.3.1, which enabled us to genotype and map this gene in the progeny using the high‐resolution melting (HRM) method (Carpezat et al., 2014) (Figs S1 and S2, see Supporting Information). The AvrLm5 phenotype co‐segregated fully with the avirulent allelic form of AvrLmJ1 present in JN3 (Lema_uP070880.2) (Fig. 1).

Figure 1.

Figure 1

Open in a new tab

Co‐localization of AvrLmJ1 and the AvrLm5 phenotype. The genetic map of the AvrLm5 region was built from the progeny of the JN3 × v29.3.1 cross used to first identify AvrLm5. Left, cumulated genetic distances are in centimorgans. Right, markers correspond to minisatellites (min), microsatellites (srr), junctions between truncated repeated elements (jct), the AvrLmJ1 gene and the AvrLm5 phenotype.

Taken together, these data show that AvrLmJ1 co‐segregates with AvrLm5 and does indeed confer avirulence towards Rlm5; therefore, AvrLmJ1 is identical to the previously identified avirulence gene AvrLm5 (Balesdent et al., 2002, 2005). We therefore propose that AvrLmJ1 should be referred to as AvrLm5 to conform with the nomenclature used for the L. maculans–B. napus interaction. The work presented in the current study demonstrates the need for increased cooperation within research communities and common screening resources, such as plant genotypes and isolates, as the lack of access to Rlm5 genotypes prevented Van de Wouw et al. (2014) from identifying the gene cloned as AvrLm5. The cloning of AvrLmJ1 is just one example of inconsistencies in nomenclature within the community of plant–pathogen research, and such confusions have consequences not only from a scientific point of view, but also within the applied and socio‐economic communities. The same resistance gene with a different name in different parts of the world impacts on the use of resistance sources in a world of global trade and, as is the case for oilseed rape/canola breeders, in which transnational societies lead the market and may disseminate resistance sources globally. The first practical consequence is that breeders may unsustainably duplicate breeding efforts if the same gene is not recognized as identical in different breeding locations. The second is that resistance genes that have been easily defeated in one part of the world may still be introduced in other parts of the world without a knowledge of their lack of durability, simply because the genes have been given different names. In the L. maculans–B. napus system, this is illustrated by the confusion between two R genes with the same recognition specificity, Rlm1 and LepR3. Some research groups generated a distinct LepRx terminology for resistance genes, which increased confusion when the resistance gene LepR3, recognizing the AvrLm1 avirulence product, was cloned, with subsequent debates on whether LepR3 was, or was not, the previously identified Rlm1, although being located on different linkage groups of the genetic maps (Larkan et al., 2013; Rouxel and Balesdent, 2013). From a practical point of view, Rlm1, when used in France in the mid‐1990s, showed a very low durability and was defeated in only three growing seasons (Rouxel et al., 2003). From 2000 to 2003, the Surpass 400 and derivative B. napus cultivars containing B. rapa‐derived single‐gene resistance were grown on increasingly large acreages across Australia (Li et al., 2004; Sprague et al., 2006). The resistance was first assumed to be a result of the single LepR3 gene, and the increasing success of these cultivars led to the same dynamics of breakdown as observed in France with Rlm1. The last practical importance of a rigorous identification of resistance genes and resistance gene recognition specificities lies in the possibility to design durable management strategies. For example, in Australia, a ‘blackleg management guide’ (https://grdc.com.au/Resources/Factsheets/2017/03/Blackleg-Management-Guide-2017) recommends that farmers rotate in time different resistance sources to alternate selection pressures on pathogen populations. This is only possible with an accurate definition of the resistances available in the commercial cultivars.

The sharing of resources, such as mapping populations, molecular markers for the generation of maps, genotypes or isolates, may prevent inconsistencies in the future. At the recent Brassica 2016 conference, attendees representing Australia, Canada, France, the UK, China and India met to discuss this issue with the aim of resolving ambiguities in gene names through the goals of greater communication and sharing of biological resources.

Supporting information

Additional Supporting Information may be found in the online version of this article at the publisher's website:

Table S1 List and characteristics of molecular markers used to map AvrLm5.

Fig. S1 Sequence polymorphism in the gene Lema_uP070880.2 (AvrLmJ1) between parental isolates JN3 (v23.1.3) and v29.3.1.

Fig. S2 High‐resolution melting (HRM) curves of the two allelic forms of AvrLmJ1. Four dilutions of DNA, with two replicates per dilution, are shown for each isolate. Red, curves obtained for the parental isolate JN3 (v23.1.3); blue and green, curves for the v29.3.1 isolate. RFU, Relative Fluorescent Unit.

Click here for additional data file. (291.4KB, pdf)

Acknowledgements

This research was funded by the French National Research Agency project AvirLep (ANR GPLA07–024C) and the Grains Research and Development Corporation.

Contributor Information

Angela P. Van De Wouw, Email: apvdw2@unimelb.edu.au

Marie‐Hélène Balesdent, Email: marie-helene.balesdent@inra.fr.

References

  1. Balesdent, M.H. , Attard, A. , Kuhn, M.L. and Rouxel, T. (2002) New avirulence genes in the phytopathogenic fungus Leptosphaeria maculans . Phytopathology, 92, 1122–1133. [DOI] [PubMed] [Google Scholar]
  2. Balesdent, M.H. , Barbetti, M.J. , Li, H. , Sivasithamparam, K. , Gout, L. and Rouxel, T. (2005) Analysis of Leptosphaeria maculans race structure in a worldwide collection of isolates. Phytopathology, 95, 1061–1071. [DOI] [PubMed] [Google Scholar]
  3. Balesdent, M.H. , Fudal, I. , Ollivier, B. , Bally, P. , Grandaubert, J. , Eber, F. , Chèvre, A.M. , Leflon, M. and Rouxel, T. (2013) The dispensable chromosome of Leptosphaeria maculans shelters an effector gene conferring avirulence towards Brassica rapa . New Phytol. 198, 887–898. [DOI] [PubMed] [Google Scholar]
  4. Ballini, E. , Morel, J.B. , Droc, G. , Price, A. , Courtois, B. , Notteghem, J.L. and Tharreau, D. (2008) A genome‐wide meta‐analysis of rice blast resistance genes and quantitative trait loci provides new insights into partial and complete resistance. Mol. Plant–Microbe Interact. 21, 859–868. [DOI] [PubMed] [Google Scholar]
  5. Bally, P. , Grandaubert, J. , Rouxel, T. and Balesdent, M.H. (2010) FONZIE: an optimized pipeline for minisatellite marker discovery and primer design from large sequence data sets. BMC Res. Notes, 3, 322. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Carpezat, J. , Bothorel, S. , Daverdin, G. , Balesdent, M.H. and Leflon, M. (2014) Use of high resolution melting analysis to genotype the avirulence AvrLm4–7 gene of Leptosphaeria maculans, a fungal pathogen of Brassica napus . Ann. Appl. Biol. 164, 430–444. [Google Scholar]
  7. Cozijnsen, A.J. , Popa, K.M. , Purwantara, A. , Rolls, B.D. and Howlett, B.J. (2000) Genome analysis of the plant pathogenic ascomycete Leptosphaeria maculans; mapping mating type and host specificity loci. Mol. Plant Pathol. 1, 293–302. [DOI] [PubMed] [Google Scholar]
  8. Delourme, R. , Pilet‐Nayel, M.L. , Archipiano, M. , Horvais, R. , Tanguy, X. , Rouxel, T. , Brun, H. , Renard, M. and Balesdent, M.H. (2004) A cluster of major specific resistance genes to Leptosphaeria maculans in Brassica napus . Phytopathology, 94, 578–583. [DOI] [PubMed] [Google Scholar]
  9. Delourme, R. , Chèvre, A.M. , Brun, H. , Rouxel, T. , Balesdent, M.H. , Dias, J.S. , Salisbury, P. , Renard, M. and Rimmer, S.R. (2006) Major gene and polygenic resistance to Leptosphaeria maculans in oilseed rape (Brassica napus). Eur. J. Plant Pathol. 114, 41–52. [Google Scholar]
  10. Fitt, B.D.L. , Brun, H. , Barbetti, M.J. and Rimmer, S.R. (2006) World‐wide importance of phoma stem canker (Leptosphaeria maculans and L. biglobosa) on oilseed rape (Brassica napus). Eur. J. Plant Pathol. 114, 3–15. [Google Scholar]
  11. Flor, H.H. (1955) Host–parasite interactions in flax rust – its genetic and other implications. Phytopathology, 45, 680–685. [Google Scholar]
  12. Fudal, I. , Ross, S. , Gout, L. , Blaise, F. , Kuhn, M.L. , Eckert, M.R. , Cattolico, L. , Bernard‐Samain, S. , Balesdent, M.H. and Rouxel, T. (2007) Heterochromatin‐like regions as ecological niches for avirulence genes in the Leptosphaeria maculans genome: map‐based cloning of AvrLm6 . Mol. Plant–Microbe Interact. 20, 459–470. [DOI] [PubMed] [Google Scholar]
  13. Ghanbarnia, K. , Fudal, I. , Larkan, N.J. , Links, M.G. , Balesdent, M.H. , Profotova, B. , Fernando, D.W.G. , Rouxel, T. and Borhan, H. (2015) Rapid identification of the Leptosphaeria maculans avirulence gene AvrLm2 using an intraspecific comparative genomics approach. Mol. Plant Pathol. 16, 699–709. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Gout, L. , Fudal, I. , Kuhn, M.L. , Blaise, F. , Eckert, M. , Cattolico, L. , Balesdent, M.H. and Rouxel, T. (2006) Lost in the middle of nowhere: the AvrLm1 avirulence gene of the Dothideomycete Leptosphaeria maculans . Mol. Microbiol. 60, 67–80. [DOI] [PubMed] [Google Scholar]
  15. Larkan, N.J. , Lydiate, D.J. , Parkin, I.A. , Nelson, M.N. , Epp, D.J. , Cowling, W.A. , Rimmer, S.R. and Borhan, M.H. (2013) The Brassica napus blackleg resistance gene LepR3 encodes a receptor‐like protein triggered by the Leptosphaeria maculans effector AVRLM1. New Phytol. 197, 595–605. [DOI] [PubMed] [Google Scholar]
  16. Larkan, N.J. , Ma, L. and Borhan, H. (2015) The Brassica napus receptor‐like protein RLM2 is encoded by a second allele of the LepR3/Rlm2 blackleg resistance locus. Plant Biotech. J. 13, 983–992. [DOI] [PubMed] [Google Scholar]
  17. Li, H. , Damour, L. , Sivasithamparam, K. and Barbetti, M.J. (2004) Increased virulence and physiological specialisation among Western Australian isolates of Leptosphaeria maculans breaking down existing single dominant gene‐based resistance in six cultivars of Brassica napus . Brassica, 6, 1–6. [Google Scholar]
  18. Long, Y. , Wang, Z. , Sun, Z. , Fernando, D.W.G. , McVetty, P.B.E. and Li, G. (2011) Identification of two blackleg resistance genes and fine mapping of one of these two genes in a Brassica napus cultivar ‘Surpass400’. Theor. Appl. Genet. 122, 1223–1231. [DOI] [PubMed] [Google Scholar]
  19. Parlange, F. , Daverdin, G. , Fudal, I. , Kuhn, M.L. , Balesdent, M.H. , Blaise, F. , Grezes‐Besset, B. and Rouxel, T. (2009) Leptosphaeria maculans avirulence gene AvrLm4–7 confers a dual recognition specificity by the Rlm4 and Rlm7 resistance genes of oilseed rape, and circumvents Rlm4‐mediated recognition through a single amino acid change. Mol. Microbiol. 71, 851–863. [DOI] [PubMed] [Google Scholar]
  20. Plissonneau, C. , Daverdin, G. , Ollivier, B. , Blaise, F. , Degrave, A. , Fudal, I. , Rouxel, T. and Balesdent, M.H. (2016) A game of hide and seek between avirulence genes AvrLm4–7 and AvrLm3 in Leptosphaeria maculans . New Phytol. 209, 1613–1624. [DOI] [PubMed] [Google Scholar]
  21. Rimmer, S.R. (2006) Resistance genes to Leptosphaeria maculans in Brassica napus . Can. J. Plant Pathol. 28, S288–S297. [Google Scholar]
  22. Rouxel, T. and Balesdent, M.H. (2013) From model to crop plant–pathogen interactions: cloning of the first resistance gene to Leptosphaeria maculans in Brassica napus . New Phytol. 197, 356–358. [DOI] [PubMed] [Google Scholar]
  23. Rouxel, T. , Penaud, A. , Pinochet, X. , Brun, H. , Gout, L. , Delourme, R. , Schmit, J. and Balesdent, M.H. (2003) A 10‐year survey of populations of Leptosphaeria maculans in France indicates a rapid adaptation towards the Rlm1 resistance gene of oilseed rape. Eur. J. Plant Pathol. 109, 871–881. [Google Scholar]
  24. Rouxel, T. , Grandaubert, J. , Hane, J.K. , Hoede, C. , Van de Wouw, A.P. , Couloux, A. , Dominguez, V. , Anthouard, V. , Bally, P. , Bourras, S. , Cozijnsen, A.J. , Ciuffetti, L.M. , Degrave, A. , Dilmaghani, A. , Duret, L. , Fudal, I. , Goodwin, S.B. , Gout, L. , Glaser, N. , Linglin, J. , Kema, G.H. , Lapalu, N. , Lawrence, C.B. , May, K. , Meyer, M. , Ollivier, B. , Poulain, J. , Schoch, C.L. , Simon, A. , Spatafora, J.W. , Stachowiak, A. , Turgeon, B.G. , Tyler, B.M. , Vincent, D. , Weissenbach, J. , Amselem, J. , Quesneville, H. , Oliver, R.P. , Wincker, P. , Balesdent, M.H. and Howlett, B.J. (2011) Effector diversification within compartments of the Leptosphaeria maculans genome affected by Repeat‐Induced Point mutations. Nat. Commun. 2, 202. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Sprague, S.J. , Marcroft, S.J. , Hayden, H.L. and Howlett, B.J. (2006) Major gene resistance to blackleg in Brassica napus overcome within three years of commercial production in southeastern Australia. Plant Dis. 90, 190–198. [DOI] [PubMed] [Google Scholar]
  26. Van de Wouw, A.P. , Marcroft, S.J. , Barbetti, M.J. , Hua, L. , Salisbury, P.A. , Gout, L. , Rouxel, T. , Howlett, B.J. and Balesdent, M.H. (2009) Dual control of avirulence in Leptosphaeria maculans towards a Brassica napus cultivar with 'sylvestris‐derived' resistance suggests involvement of two resistance genes. Plant Pathol. 58, 305–313. [Google Scholar]
  27. Van de Wouw, A.P. , Lowe, R.G.T. , Elliott, C.E. , Dubois, D.J. and Howlett, B.J. (2014) An avirulence gene, AvrLmJ1, from the blackleg fungus, Leptosphaeria maculans, confers avirulence to Brassica juncea cultivars. Mol. Plant Pathol. 15, 523–530. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Yu, F. , Lydiate, D.J. and Rimmer, S.R. (2005) Identification of two novel genes for blackleg resistance in Brassica napus . Theor. Appl. Genet. 110, 969–979. [DOI] [PubMed] [Google Scholar]
  29. Yu, F. , Lydiate, D.J. and Rimmer, S.R. (2008) Identification and mapping of a third blackleg resistance locus in Brassica napus derived from B. rapa subsp. sylvestris. Genome, 51, 64–72. [DOI] [PubMed] [Google Scholar]

Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Supplementary Materials

Additional Supporting Information may be found in the online version of this article at the publisher's website:

Table S1 List and characteristics of molecular markers used to map AvrLm5.

Fig. S1 Sequence polymorphism in the gene Lema_uP070880.2 (AvrLmJ1) between parental isolates JN3 (v23.1.3) and v29.3.1.

Fig. S2 High‐resolution melting (HRM) curves of the two allelic forms of AvrLmJ1. Four dilutions of DNA, with two replicates per dilution, are shown for each isolate. Red, curves obtained for the parental isolate JN3 (v23.1.3); blue and green, curves for the v29.3.1 isolate. RFU, Relative Fluorescent Unit.

Click here for additional data file. (291.4KB, pdf)

Articles from Molecular Plant Pathology are provided here courtesy of Wiley

RESOURCES