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Two pathogenesis-related proteins interact with leucine-rich repeat proteins to promote Alternaria leaf spot resistance in apple.

ABSTRACT: Alternaria leaf spot in apple (Malus x domestica), caused by the fungal pathogen Alternaria alternata f. sp. mali (also called A. mali), is a devastating disease resulting in substantial economic losses. We previously established that the resistance (R) protein MdRNL2, containing a coiled-coil, nucleotide-binding, and leucine-rich repeat (CC_R-NB-LRR) domain, interacts with another CC_R-NB-LRR protein, MdRNL6, to form a MdRNL2-MdRNL6 complex that confers resistance to A. mali. Here, to investigate the function of the MdRNL2-MdRNL6 complex, we identified two novel pathogenesis-related (PR) proteins, MdPR10-1 and MdPR10-2, that interact with MdRNL2. Yeast two-hybrid (Y2H) assays and bimolecular fluorescence complementation (BiFC) assays confirmed that MdPR10-1 and MdPR10-2 interact with MdRNL2 and MdRNL6 at the leucine-rich repeat domain. Transient expression assays demonstrated that accumulation of MdPR10-1 and MdPR10-2 enhanced the resistance of apple to four strains of A. mali that we tested: ALT1, GBYB2, BXSB5, and BXSB7. In vitro antifungal activity assays demonstrated that both the proteins contribute to Alternaria leaf spot resistance by inhibiting fungal growth. Our data provide evidence for a novel regulatory mechanism in which MdRNL2 and MdRNL6 interact with MdPR10-1 and MdPR10-2 to inhibit fungal growth, thereby contributing to Alternaria leaf spot resistance in apple. The identification of these two novel PR proteins will facilitate breeding for fungal disease resistance in apple.

SUBMITTER: Zhang Q

PROVIDER: S-EPMC8484663 | biostudies-literature | 2021 Oct

REPOSITORIES: biostudies-literature

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Two pathogenesis-related proteins interact with leucine-rich repeat proteins to promote Alternaria leaf spot resistance in apple.

Zhang Qiulei Q Xu Chaoran C Wei Haiyang H Fan Wenqi W Li Tianzhong T

Horticulture research 20211001 1

Alternaria leaf spot in apple (Malus x domestica), caused by the fungal pathogen Alternaria alternata f. sp. mali (also called A. mali), is a devastating disease resulting in substantial economic losses. We previously established that the resistance (R) protein MdRNL2, containing a coiled-coil, nucleotide-binding, and leucine-rich repeat (CC<sub>R</sub>-NB-LRR) domain, interacts with another CC<sub>R</sub>-NB-LRR protein, MdRNL6, to form a MdRNL2-MdRNL6 complex that confers resistance to A. mali ...[more]

PMID: 34593778

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Project description:The fungal genus Alternaria is a pan-global pathogen of > 100 crops, and is associated with the globally expanding Alternaria leaf blotch in apple (Malus x domestica Borkh.) which leads to severe leaf necrosis, premature defoliation, and large economic losses. Up to date, the epidemiology of many Alternaria species is still not resolved as they can be saprophytic, parasitic or shift between both lifestyles and are also classified as primary pathogen able to infect healthy tissue. We argue that Alternaria spp. does not act as primary pathogen, but only as a necrosis-dependent opportunist. We studied the infection biology of Alternaria spp. under controlled conditions and monitored disease prevalence in real orchards and validated our ideas by applying fungicide-free treatments in 3-years field experiments. Alternaria spp. isolates were not able to induce necroses in healthy tissue, but only when prior induced damages existed. Next, leaf-applied fertilizers, without fungicidal effect, reduced Alternaria-associated symptoms (- 72.7%, SE: ± 2.5%) with the same efficacy as fungicides. Finally, low leaf magnesium, sulphur, and manganese concentrations were consistently linked with Alternaria-associated leaf blotch. Fruit spot incidence correlated positively with leaf blotch, was also reduced by fertilizer treatments, and did not expand during storage unlike other fungus-mediated diseases. Our findings suggest that Alternaria spp. may be a consequence of leaf blotch rather than its primary cause, as it appears to colonize the physiologically induced leaf blotch. Taking into account existing observations that Alternaria infection is connected to weakened hosts, the distinction may appear slight, but is of great significance, as we can now (a) explain the mechanism of how different stresses result in colonization with Alternaria spp. and (b) substitute fungicides for a basic leaf fertilizer. Therefore, our findings can result in significant decreases in environmental costs due to reduced fungicide use, especially if the same mechanism applies to other crops.

Project description:BackgroundThe discovery and characterisation of factors governing innate immune responses in insects has driven the elucidation of many immune system components in mammals and other organisms. Focusing on the immune system responses of the malaria mosquito, Anopheles gambiae, has uncovered an array of components and mechanisms involved in defence against pathogen infections. Two of these immune factors are LRIM1 and APL1C, which are leucine-rich repeat (LRR) containing proteins that activate complement-like defence responses against malaria parasites. In addition to their LRR domains, these leucine-rich repeat immune (LRIM) proteins share several structural features including signal peptides, patterns of cysteine residues, and coiled-coil domains.ResultsThe identification and characterisation of genes related to LRIM1 and APL1C revealed putatively novel innate immune factors and furthered the understanding of their likely molecular functions. Genomic scans using the shared features of LRIM1 and APL1C identified more than 20 LRIM-like genes exhibiting all or most of their sequence features in each of three disease-vector mosquitoes with sequenced genomes: An. gambiae, Aedes aegypti, and Culex quinquefasciatus. Comparative sequence analyses revealed that this family of mosquito LRIM-like genes is characterised by a variable number of 6 to 14 LRRs of different lengths. The "Long" LRIM subfamily, with 10 or more LRRs, and the "Short" LRIMs, with 6 or 7 LRRs, also share the signal peptide, cysteine residue patterning, and coiled-coil sequence features of LRIM1 and APL1C. The "TM" LRIMs have a predicted C-terminal transmembrane region, and the "Coil-less" LRIMs exhibit the characteristic LRIM sequence signatures but lack the C-terminal coiled-coil domains.ConclusionsThe evolutionary plasticity of the LRIM LRR domains may provide templates for diverse recognition properties, while their coiled-coil domains could be involved in the formation of LRIM protein complexes or mediate interactions with other immune proteins. The conserved LRIM cysteine residue patterns are likely to be important for structural fold stability and the formation of protein complexes. These sequence-structure-function relations of mosquito LRIMs will serve to guide the experimental elucidation of their molecular roles in mosquito immunity.

Dataset Information

Two pathogenesis-related proteins interact with leucine-rich repeat proteins to promote Alternaria leaf spot resistance in apple.

Publications

Two pathogenesis-related proteins interact with leucine-rich repeat proteins to promote Alternaria leaf spot resistance in apple.

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