Plants defense mechanisms help plant to cope with pathogen infection. The valuable genetic resource of plant can be utilized to improve disease resistance. Phytopathogen exploit plant susceptibility (S)-genes to facilitate their proliferation. Disrupting these S-genes may interfere with the compatibility between host plant and the pathogen conferring broad-spectrum and durable disease resistance (Zaidi et al., 2018). The necrotrophic fungal pathogen Parastagonospora nodorum causing septoria nodorum blotch in wheat, secrete effectors that interact with plant S-gene product in an inverse gene-for-gene manner leading to host cell death and disease development (Choupannejad et al., 2024). P. nodorum benefits from cell death by hijacking host immunity responses including pathogen-associated molecular patterns (PAMPs)-triggered immunity (PTI) and the effector-triggered immunity (ETI) through the production of necrotrophic effectors resulting in necrotrophic effector triggered susceptibility (ETS) (Shi et al., 2016; Choupannejad et al., 2024). The hijacking of the molecular pathway is typically involved in resistance to biotrophic pathogens, reveals the complex nature of susceptibility and resistance in necrotrophic and biotrophic pathogen interactions with plants (Shi et al., 2016).
Pattern recognition receptors (PRRs) perceives PAMPs leading to activation of PTI (Zhou and Zhang 2020). Suppression of PTI is required as a first step by pathogen to alter the status from a nonhost into a host (Pavan et al., 2010). Adapted pathogen overcome PTI by deploying effector proteins leading to effector-triggered susceptibility (ETS). In second layer of defense plant counteract ETS through the evolution of resistance (R) genes (Jones and Dangl 2006). The plant R gene encode intracellular immune receptor NB-LRR (nucleotide-binding leucine-rich repeat) proteins which can detect pathogen effectors/avirulence (Avr) proteins that is delivered inside the plant cell triggering ETI (Jones and Dangl 2006). Many effector proteins interfere with host immune system by a multiple strategy. Effectors, however, can rapidly evolve to overcome ETI by avoiding recognition of R gene, once again leading to ETS (Jones and Dangl 2006; Keseoglou et al., 2022). The adapted pathogen deploys effector proteins to manipulate host plant S-genes, rendering plant defenses ineffective. The identification and mutation of plant S-genes exploited by the bacterial pathogen may provide crop durable and broad-spectrum resistance (Keseoglou et al., 2022). Studies on ETS propose breeding strategy: exploitation of plant S-genes for durable and broad-spectrum resistance (Pavan et al., 2010).
Plant genes that enable successful pathogen infection by suppressing host immune responses are referred to as S-genes. Three groups of S-genes act during different stages of infection (Van Schie and Takken 2014):
- Early pathogen establishment
- Modulation of host defenses
- Pathogen sustenance
Disease arises from a compatible interaction and hence inactivation/ loss of function of S-gene may result in resistance against the pathogen (Pavan et al., 2010; Van Schie and Takken 2014; Garcia-Ruiz et al., 2021). S-genes can be retained across plant species. A plethora of wheat S-genes were identified, and they revealed to regulate multiple processes, including pathogen (pre)penetration, plant immunity, pathogen sustenance and pest feeding (Li et al., 2022). S-genes can be identified and mutated by using genome engineering tools. Modifying some of the S-genes via genome editing and targeting induced local lesion in genomes (TILLING) would confer wheat broad-spectrum and durable resistance (Li et al., 2022). Another technique used is virus-induced gene silencing (VIGS), an effective method to silence gene that uses plant’s antiviral defensive mechanism to suppress the expression of specific invasive viral transcript (Zulfiqar et al., 2023). VIGS is an RNA interference (RNAi)-based technology used to transiently knock down target gene expression by utilizing modified plant viral genomes (Dommes et al., 2019).
Mutation in S-genes can lead to durable, recessively inherited and potentially broad-spectrum resistance in plants (Keseoglou et al., 2022). The Mildew resistance locus o (Mlo) was the first S-gene identified in barley. The mutation of Mlo ortholog confer strong powdery mildew resistance in many crops (Deng et al., 2020). Disabled S-genes can induce resistance phenotype resembling that of healthy plants (Sun et al., 2016). Barley mlo resistance confers total resistance against fungal penetration. The efficiency of the resistance depends on epidermal cell type, host genetic background, environmental condition and fungal genotype (Lyngkjaer et al., 2000). The barley Mlo-gene regulates several mechanisms leading to increased resistance. The resistance mechanisms involve early deposition of increased size of papilla, callose deposition, production of phenolic compounds and cell wall strengthening by cross binding (Lyngkjaer et al., 2000). Loss of function of S-genes will lead to resistance that inherit recessively in normal plants and dominantly in plant of which S-gene is silenced by using RNAi technique (Pavan et al., 2010). Resistance conferred by mutations of Mlo in barley and eIF4E in pepper are still effective in field even after 30 and 50 years of their introduction in agriculture respectively (Pavan et al., 2010).
The S-gene in barley identified as Mlo encodes a transmembrane protein and is essential for powdery mildew penetration in a wide range of monocots and dicots (Li et al., 2022). Knockout of TaMlo (the orthologue of the barley Mlo gene)using genome editing, Tilling and VIGS results in the enhanced wheat penetration resistance to Blumeria graminis f. sp. tritici (Acevedo-Garcia et al., 2016; Li et al., 2022). In barley mlo lines, resistance is associated with pleiotropic phenotypes such as deposition of callose-containing cell wall appositions, early chlorophyll decay and spontaneous mesophyll cell death, which together lead to chlorotic and necrotic leaf flecking and premature leaf senescence (Acevedo-Garcia et al., 2016). Mlo and mlo alleles control qualitatively the same apposition-based resistance mechanisms, which in the presence of the wild type of Mlo allele, is ineffective to provide protection against the fungal pathogen (Wolter et al., 1993). S-gene loss of function is an effective breeding strategy providing durable field resistance.
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