Volume 231, Issue 4 p. 1301-1303
Commentary
Free Access

Quantitative resistance linked to late effectors

Claire Veneault-Fourrey

Corresponding Author

Claire Veneault-Fourrey

Laboratory of Excellence ARBRE, INRAE, UMR1136 Trees-Microbes Interactions, University of Lorraine, Nancy, F-54000 France

Authors for correspondence: emails [email protected] (CV-F); [email protected] (MR)

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Martijn Rep

Corresponding Author

Martijn Rep

Swammerdam Institute for Life Sciences, Molecular Plant Pathology, University of Amsterdam, Science Park 904, Amsterdam, 1098 XH the Netherlands

Authors for correspondence: emails [email protected] (CV-F); [email protected] (MR)

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First published: 09 June 2021
Citations: 3

This article is a Commentary on Jiquel et al. ( 2021), 231: 1510–1524.

Disease resistance is one of the most desired traits for plant breeders. Genetically, disease resistance has been described as being either ‘qualitative’ or ‘quantitative’ (Roux et al., 2014). Qualitative resistance corresponds to the presence of a matching pair of genes sufficient for complete resistance: a resistance (R) gene in the plant and an ‘avirulence’ gene in the pathogen. R genes most often encode ‘immune receptors’ capable of detecting the presence or the activity of proteins secreted by invading microbes – commonly termed effectors. An effector that is recognized by a plant immune receptor is encoded by the ‘corresponding’ avirulence gene in the pathogen. Disease resistance as a result of recognition of an effector by an immune receptor is called effector-triggered immunity (ETI). ETI plays a dominant role in protecting particular plant genotypes from specific pathogen races, and is often associated with localized cell death called the hypersentitive response (HR). By contrast, quantitative disease resistance (QDR), also known as polygenic resistance, leads to a reduction of symptoms rather that the total absence of disease. Genetically, this type of disease resistance is determined by multiple quantitative trait loci (QTL). While qualitative disease resistance can be achieved by the introgression of R genes into susceptible cultivars, QDR is much more difficult to introgress, and also to decipher at the molecular level. However, since resistance to avirulent populations of pathogenic microbes conferred by R genes is often rapidly overcome by new races of the pathogen after the release of resistant varieties in the field (Rouxel & Balesdent, 2017), new sources of resistance to the pathogen are constantly required, and quantitative resistance remains of great interest in this respect. A new paper by Jiquel et al., published in this issue of New Phytologist (2021; pp. 1510–1524), provides an elegant method to probe deeper into this issue using the Leptosphaeria maculans–Brassica napus pathosystem. Leptosphaeria maculans is a remarkable fungal pathogen in that it alternates between biotrophic and necrotrophic phases on cotyledons and leaves, followed by endophytic systemic growth in stems during the winter before another switch towards necrotrophy at the end of spring. These phases are associated with the expression of fungal effector genes in ‘waves’, with ‘early’ and ‘late’ effector genes (Gervais et al., 2017) – the latter being expressed during endophytic stem colonization (also known as ‘LmSTEEs’ for ‘Lmaculans stem-expressed effectors’). Jiquel et al. hypothesized that adult resistance may involve R genes at a late stage of infection. Early effectors were already known to cause HR if recognized by a corresponding immune effector in cotyledons (Rouxel & Balesdent, 2017). Jiquel et al. made use of this knowledge and designed an innovative strategy to identify R genes recognizing ‘late’ effectors that may contribute to adult stage resistance. Candidate effector genes of the late ‘wave’ were placed under the control of an early effector gene promoter, making it possible to screen a collection of Bnapus genotypes for resistance genes operating during stem colonization in a miniaturized cotyledon test.

‘With this elegant strategy, the authors identified and mapped a new resistance source.’

With this elegant strategy, the authors identified and mapped a new resistance source. On top of that, following CRISPR-Cas9 inactivation of the corresponding late avirulence gene in Lmaculans, they demonstrated the latter’s requirement for stem canker severity and recognition by the cognate (still unidentified) resistance gene. Jiquel et al. thereby demonstrated that adult stage resistance of oilseed rape to Lmaculans, which is a form of quantitative resistance (partial and polygenic), is at least partly dependent on gene-for-gene interactions involving fungal effectors produced during stem colonization. The overcoming of quantitative resistance by specific isolates has been observed in filamentous pathogens, for example Pyrenophora graminea (Arru et al., 2003) and Zymoseptoria tritici (Meile et al., 2018). The authors thus suggest that quantitative and qualitative resistance are not mutually exclusive and that certain instances of quantitative resistance could result from the partial or residual effect of major R genes that are partly overcome by the pathogen population. This hypothesis that partial resistance may be due, at least in part, to gene-for-gene relationships was first formulated by Parlevliet & Zadoks (1977). Earlier studies of the Bnapus–Lmaculans pathosystem mapped several putative R genes encoding nucleotide-binding leucine-rich repeat (LRR) receptors in close proximity (within 200 kb) of the significant QTL region providing adult stage resistance (Raman et al., 2018). However, none of these genes corresponds to previously characterized Bnapus resistance genes (Rlm) against Lmaculans. Clearly, the study by Jiquel et al. opens new avenues to study the genetic basis of quantitative resistance and advances work towards the identification of new sources of resistance.

Next to the elegance of the method, part of the success of this approach may be attributed to fortunate circumstances. For example, the screening was based on HR and not all R-AVR pairs provoke visible HR. The success of the method also relies on the expression of the R gene in cotyledons, whereas it recognizes the late effector in the stem. In addition, the panel of tested oilseed rape cultivars was not very diverse, with mostly European winter varieties. YUDAL, the cultivar in which the new R gene was identified, was indeed the sole spring cultivar originating from Korea. Leptosphaeria biglobosa spp. and Lmaculans spp. are found as a species complex in America, Europe and Australia with a prevalence of Lmaculans in western Europe. In Asia, Lbiglobosabrassicae’ is the sole species present (Cai et al., 2018). YUDAL may, therefore, be a cultivar with little or no co-evolutionary history with Lmaculans.

The question now arises as to the use of the identified resistance gene as a possible source of diversification of available Bnapus resistance genes against Lmaculans and its durability. In known strains of Lmaculans, LmSTEE effectors are conserved and have not experienced positive selection. The absence of polymorphisms in late effectors might be explained by a weak selection pressure on Lmaculans populations by resistance at the adult stage. This remains to be confirmed, for example by long-term monitoring of populations subjected to selection pressure from varieties carrying quantitative resistance – and without effective qualitative resistance. Nevertheless, the conservation of LmSTEE effectors in the fungal pathogen populations, while being potentially recognized by R genes, suggests that their loss has a fitness cost. Since LmSTEE genes are expressed during the endophytic phase of Lmaculans, one can wonder whether they represent an evolutionary trade-off between maintaining a role in colonization and escaping resistance gene recognition. Still, the identification of R genes recognizing such conserved effectors are more likely to confer durable resistance (Brown, 2015; Depotter & Doehlemann, 2019). In addition, a field experiment showed that quantitative resistance extends the durability of Rlm6-mediated resistance to Lmaculans (Brun et al., 2010). The selection of Bnapus cultivars combining these two types of plant resistance is therefore a priority to ensure optimal durability of major resistance genes. The increase of the repertoire of nonbypassed Bnapus Rlm genes, together with further investigation of quantitative resistance, is thus required.

The study by Jiquel et al. also invites other questions. Since Lmaculans is perhaps a rather exceptional pathogen with its long ‘endophytic’ stage, one question is how general these findings could be – is the link between late effectors and quantitative resistance unique to Lmaculans? In addition, plant microbiome studies have shown that fungal and bacterial endophytes are underestimated microbial partners of the plant. Possibly, during endophytism in general, conserved effectors may be recognized by the plant immune system. In that case, effectors of fungal endophytes may be used to identify new R genes for quantitative (adult stage) resistance. At least in the case of Lmaculans, such a conserved ‘layer’ of plant immunity could be triggered if there is no recognition of early, highly diversified effectors during cotyledon infection.

In conclusion, understanding how late and conserved effectors evolve, their roles and how they might be recognized by the plant surveillance machinery is of great and promising interest to better understand quantitative/adult stage resistance and identify novel and possibly more durable R genes, that could be used for breeding for disease resistance.

Acknowledgements

CV-F is supported by INRAE, Université de Lorraine, the French National Research Agency (ANR) as part of the ‘Investissements d'Avenir’ program (ANR-11-LABX-0002-01, Lab of Excellence ARBRE), the Genomic Science Program-US Department of Energy-Office of Science-Biological and Environmental Research as part of the Plant-Microbe Interfaces Scientific Focus Area (https://pmi.ornl.gov).