A successful defense of the narrow-leafed lupin against anthracnose involves quick and orchestrated reprogramming of oxidation–reduction, photosynthesis and pathogenesis-related genes

Abstract

Narrow-leafed lupin (NLL, Lupinus angustifolius L.) is a legume plant cultivated for grain production and soil improvement. Worldwide expansion of NLL as a crop attracted various pathogenic fungi, including Colletotrichum lupini causing a devastating disease, anthracnose. Two alleles conferring improved resistance, Lanr1 and AnMan, were exploited in NLL breeding, however, underlying molecular mechanisms remained unknown. In this study, European NLL germplasm was screened with Lanr1 and AnMan markers. Inoculation tests in controlled environment confirmed effectiveness of both resistance donors. Representative resistant and susceptible lines were subjected to differential gene expression profiling. Resistance to anthracnose was associated with overrepresentation of “GO:0006952 defense response”, “GO:0055114 oxidation–reduction process” and “GO:0015979 photosynthesis” gene ontology terms. Moreover, the Lanr1 (83A:476) line revealed massive transcriptomic reprogramming quickly after inoculation, whereas other lines showed such a response delayed by about 42 h. Defense response was associated with upregulation of TIR-NBS, CC-NBS-LRR and NBS-LRR genes, pathogenesis-related 10 proteins, lipid transfer proteins, glucan endo-1,3-beta-glucosidases, glycine-rich cell wall proteins and genes from reactive oxygen species pathway. Early response of 83A:476, including orchestrated downregulation of photosynthesis-related genes, coincided with the successful defense during fungus biotrophic growth phase, indicating effector-triggered immunity. Mandelup response was delayed and resembled general horizontal resistance.

Transcriptional reprogramming in sound‐treated Micro‐Tom plants inoculated with Pseudomonas syringae pv. tomatoDC3000

“…In contrast, in 1000 Hz-Pst plants at 1 dpi, a down-regulation of genes involved in tetrapyrrole and chlorophyll metabolic processes was noted, including magnesium-chelatase subunit I and D (CHLI and CHLD), and chlorophyllide a oxygenase (CAO) (Table S3). Taken together, these results suggest that SV induced a shift in the dynamic control of Chl studies have revealed a prompt down-regulation of photosynthesisrelated genes in different plant-pathogen interactions (Kretschmer et al 2019;Książkiewicz et al 2022), which is consistent with the relevance of plastids in biotic interactions and plant immunity (Littlejohn et al 2021).…”

“…Thus, the opposed regulation of Chl synthesis and degradation observed in both Pst DC3000 treatments could influence the outcome of plant disease and defense responses based on the deployment of ROS and their interactions with hormone signaling cascades. Several studies have revealed a prompt down‐regulation of photosynthesis‐related genes in different plant‐pathogen interactions (Kretschmer et al 2019; Książkiewicz et al 2022), which is consistent with the relevance of plastids in biotic interactions and plant immunity (Littlejohn et al 2021).…”

Insights into the Pathogenic Mechanisms and the Control Strat-Egies of Anthracnose in Lupins – A Comprehensive Review

“…The failure of the lupin industry to address anthracnose threats on white lupins (L. albus L.) in France (1982) and Ukraine (1983) led to subsequent outbreaks in major lupin-producing countries, including Australia, Poland, and Germany [4][5][6]. This negligence resulted in a ban on white lupin cultivation in Australia until 1998 due to its proven susceptibility and challenges in finding resistance [5,7]. The spread of the disease in Australia in 1996 prompted the development of disease management strategies, focusing on the identification of resistant plant varieties [5].…”

“…Beyond the initial basal defense line featuring physical barriers against pathogens and the continuous expression and activity of certain general defense genes, a secondary defense layer involves the activation of plant molecular signaling cascades. These cascades are initiated by the recognition of pathogenic molecules, such as microbe or pathogen-associated molecular patterns (PAMPs/MAMPs), triggering PAMPs-triggered immunity (PTI) or by secreted effector proteins, inducing effector-triggered immunity (ETI), a process dependent on the presence of R genes [7,[46][47][48][49].…”

“…A similar defense response mediated by AnMan gene, albeit delayed, proved less effective in protecting against the disease. Anthracnose resistance driven by Lanr1 gene resembles a rapid R gene response (ETI), while the AnMan gene likely imparts a horizontal response (PTI), providing a moderate level of resistance [7].…”