Lathyrus sativus Resistance Against the Existing and Emerging Pathogens Erysiphe pisi and E. trifolii: A Case of Commonalities or Total Discrepancy?

Powdery mildew on Lathyrus sativus (grass pea) is commonly caused by Erysiphe pisi, the causal agent of pea powdery mildew. E. trifolii could also pose an additional threat to grass pea, as it does to pea (Pisum sativum). In order to understand the potential threat and the availability of resistance sources, the response to both pathogens was analyzed on a worldwide germplasm collection of 189 grass pea accessions. Infection type and disease severity (DS) of grass pea accessions, independently inoculated with E. pisi and E. trifolii, were evaluated under controlled conditions. A wide range of responses were detected, with the previously uncharacterized partial resistance to E. trifolii in grass pea detected less frequently and uncorrelated with partial resistance against E. pisi. To test for the lack of correlation at the genetic level, an exploratory association mapping study was undertaken by statistically combining grass pea collection DS scores against both pathogens, with 5,651 previously screened genotype-by-sequencing-based single nucleotide polymorphisms (SNP). Mostly different genetic regions in grass pea were identified as being associated with the response to E. trifolii and E. pisi, anticipating an independent genetic basis that requires further validation in larger germplasm collections, with higher SNP densities. This study proposes common and unique partial resistance components against two different powdery mildews, implying the need for complementary approaches to introduce resistance to both pathogens into new grass pea varieties. The identified sources of resistance and predicted genomic targets will assist in breeding for resistance to multiple powdery mildews.

Integrating Phenotypic and Gene Expression Linkage Mapping to Dissect Rust Resistance in Chickling Pea.

Rusts are among the most important foliar biotrophic fungal diseases in legumes. Lathyrus cicera crop can be severely damaged by Uromyces pisi, to which partial resistance has been identified. Nevertheless, the underlying genetic basis and molecular mechanisms of this resistance are poorly understood in L. cicera. To prioritise the causative variants controlling partial resistance to rust in L. cicera, a recombinant inbred line (RIL) population, segregating for response to this pathogen, was used to combine the detection of related phenotypic- and expression-quantitative trait loci (pQTLs and eQTLs, respectively). RILs' U. pisi disease severity (DS) was recorded in three independent screenings at seedling (growth chamber) and in one season of exploratory screening at adult plant stage (semi-controlled field conditions). A continuous DS range was observed in both conditions and used for pQTL mapping. Different pQTLs were identified under the growth chamber and semi-controlled field conditions, indicating a distinct genetic basis depending on the plant developmental stage and/or the environment. Additionally, the expression of nine genes related to U. pisi resistance in L. cicera was quantified for each RIL individual and used for eQTL mapping. One cis-eQTL and one trans-eQTL were identified controlling the expression variation of one gene related to rust resistance - a member of glycosyl hydrolase family 17. Integrating phenotyping, gene expression and linkage mapping allowed prioritising four candidate genes relevant for disease-resistance precision breeding involved in adaptation to biotic stress, cellular, and organelle homeostasis, and proteins directly involved in plant defence.

Association Mapping of Lathyrus sativus Disease Response to Uromyces pisi Reveals Novel Loci Underlying Partial Resistance.

Uromyces pisi ([Pers.] D.C.) Wint. is an important foliar biotrophic pathogen infecting grass pea (Lathyrus sativus L.), compromising their yield stability. To date, few efforts have been made to assess the natural variation in grass pea resistance and to identify the resistance loci operating against this pathogen, limiting its efficient breeding exploitation. To overcome this knowledge gap, the genetic architecture of grass pea resistance to U. pisi was investigated using a worldwide collection of 182 accessions through a genome-wide association approach. The response of the grass pea collection to rust infection under controlled conditions and at the seedling stage did not reveal any hypersensitive response but a continuous variation for disease severity, with the identification of promising sources of partial resistance. A panel of 5,651 high-quality single-nucleotide polymorphism (SNP) markers previously generated was used to test for SNP-trait associations, based on a mixed linear model accounting for population structure. We detected seven SNP markers significantly associated with U. pisi disease severity, suggesting that partial resistance is oligogenic. Six of the associated SNP markers were located in chromosomes 4 and 6, while the remaining SNP markers had no known chromosomal position. Through comparative mapping with the pea reference genome, a total of 19 candidate genes were proposed, encoding for leucine-rich repeat, NB-ARC domain, and TGA transcription factor family, among others. Results presented in this study provided information on the availability of partial resistance in grass pea germplasm and advanced our understanding of the molecular mechanisms of quantitative resistance to rust in grass pea. Moreover, the detected associated SNP markers constitute promising genomic targets for the development of molecular tools to assist disease resistance precision breeding.

Legume Crops and Biotrophic Pathogen Interactions: A Continuous Cross-Talk of a Multilayered Array of Defense Mechanisms.

Legume species are recognized for their nutritional benefits and contribution to the sustainability of agricultural systems. However, their production is threatened by biotic constraints with devastating impacts on crop yield. A deep understanding of the molecular and genetic architecture of resistance sources culminating in immunity is critical to assist new biotechnological approaches for plant protection. In this review, the current knowledge regarding the major plant immune system components of grain and forage legumes challenged with obligate airborne biotrophic fungi will be comprehensively evaluated and discussed while identifying future directions of research. To achieve this, we will address the multi-layered defense strategies deployed by legume crops at the biochemical, molecular, and physiological levels, leading to rapid pathogen recognition and carrying the necessary information to sub-cellular components, on-setting a dynamic and organized defense. Emphasis will be given to recent approaches such as the identification of critical components of host decentralized immune response negatively regulated by pathogens while targeting the loss-of-function of susceptibility genes. We conclude that advances in gene expression analysis in both host and pathogen, protocols for effectoromics pipelines, and high-throughput disease phenomics platforms are rapidly leading to a deeper understanding of the intricate host-pathogen interaction, crucial for efficient disease resistance breeding initiatives.

Partial Resistance Against Erysiphe pisi and E. trifolii Under Different Genetic Control in Lathyrus cicera: Outcomes from a Linkage Mapping Approach.

Powdery mildew infections are among the most severe foliar biotrophic fungal diseases in grain legumes. Several accessions of Lathyrus cicera (chickling pea) show levels of partial resistance to Erysiphe pisi, the causal agent of pea powdery mildew, and to E. trifolii, a powdery mildew pathogen recently confirmed to infect pea and Lathyrus spp. Nevertheless, the underlying L. cicera resistance mechanisms against powdery mildews are poorly understood. To unveil the genetic control of resistance against powdery mildews in L. cicera, a recombinant inbred line population segregating for response to both species was used in resistance linkage analysis. An improved L. cicera genetic linkage map was used in this analysis. The new higher-density linkage map contains 1,468 polymorphic loci mapped on seven major and two minor linkage groups, covering a total of 712.4 cM. The percentage of the leaf area affected by either E. pisi or E. trifolii was recorded in independent screenings of the recombinant inbred line population, identifying a continuous range of resistance-susceptibility responses. Distinct quantitative trait loci (QTLs) for partial resistance against each pathogen were identified, suggesting different genetic bases are involved in the response to E. pisi and E. trifolii in L. cicera. Moreover, through comparative mapping of L. cicera QTL regions with the pea reference genome, candidate genes and pathways involved in resistance against powdery mildews were identified. This study extended the previously available genetic and genomic tools in Lathyrus species, providing clues about diverse powdery mildew resistance mechanisms useful for future resistance breeding of L. cicera and related species.