Epistasis and pleiotropy are genetic phenomenon and are the fundamental aspect of the quantitative traits. The term pleiotropy is derived from Greek words pleio, meaning “many” and tropic, which means “affecting” (Lobo 2008). Genes that affect multiple, apparently unrelated, phenotypes are called pleiotropic genes. Pleiotropy should not be confused with polygenic traits, in which multiple genes converge to result in single phenotype (Lobo 2008). Quantitative variation (traits showing continuous variation) involves epistasis and pleiotropy in plants.
Pleiotropic gene: Single gene can control more than one trait (Lobo 2008) or pleiotropy refers to as a single gene affecting two or more distinct and seemingly unrelated trait (He and Zhang 2006).
Epistasis: The interaction of genes at different loci affects trait. Epistasis is the interaction between alleles of different genes, i.e., non-allelic or intergeneric interaction, as opposed to dominance, which is interaction between alleles of the same gene, called inter-allelic or intragenic interaction (Kearsey and Pooni 2020).
Epistasis (Miko 2008):
- When two or more loci interact to create new phenotypes
- Whenever an allele at one locus masks the effect of alleles at one or more other loci
- Whenever an allele at one locus modifies the effects of alleles at one or more other loci
Immunity to disease resistance affect plant growth and development in plants. Biomass yield (i.e. grain or stover yield) in field crop is the main breeding target, usually affected by the level of disease resistance. Growth and defense trade-off is mediated by resistance (R) genes, susceptibility (S) genes and pleiotropic genes (Dwivedi et al., 2024). Epistasis and pleiotropy both contribute to complexity of trait variation in plants. Plant pathogens use host S genes to infect. Impairment of S genes can lead to recessively inherited broad-spectrum resistance to bacteria (Koseoglou et al., 2022). Disruption of S genes is a breeding strategy to confer disease resistance. S genes are implicated in many essential biological function and deletion of these genes result in undesired pleiotropic effect (Li et al., 2022). Whereas, due to their dual role in physiological processes and susceptibility, inactivation of S genes may lead to resistance along with pleiotropic effects (Koseoglou et al., 2022). Loss-of-function mutation in one such S gene the Mildew resistance Locus O (MLO) protect plant from powdery mildew infection (Kusch and Panstruga 2017; Li et al., 2022). The mlo-based resistance is an effective approach to control powdery mildew disease in many plant species (Kusch and Panstruga 2017). When MLO protein is absent, the plant is fully resistant to the virulent powdery mildew fungi (Kusch et al., 2019). Loss of S gene function can have pleiotropic effects (Garcia-Ruiz et al., 2021). Recessive S gene alleles confer resistance for example mlo allele conferring resistance to powdery mildew; rice xa13 allele providing resistance to Xanthomonas bacteria and elF4 (initiation factor) confer potyvirus resistance (Kusch and Panstruga 2017; Schmitt-Keichinger 2019; Garcia-Ruiz et al., 2021).
Powdery mildew resistant barley (Hordeum vulgare) and Arabidopsis thaliana mlo mutant plants exhibit pleiotropic phenotypes such as the formation of callose-rich cell wall appositions and early leaf chlorosis and necrosis, indicative of premature senescence (Lorek et al., 2013; Freh et al., 2024). Nitrogen deficiency induce early leaf senescence in A. thaliana (Wen et al., 2020; Fan et al., 2023; Freh et al., 2024). This nitrogen deficiency leading to early senescence in plants, is accompanied by changes in gene expression, metabolism, growth, development (Wen et al., 2020).
Few adult-plant resistance genes such as Leaf rust resistance Lr (34) and Lr67 of wheat, have pleiotropic functions and are effective against three rust (stem rust, Leaf rust and stripe rust) and powdery mildew (Sanchez-Martin and Keller 2021; Dinglasan et al., 2022). Functional allelic variation at specific genes for multiple disease resistance exists in maize (Wisser et al., 2011). Multivariate analysis of maize disease resistance suggests a pleiotropic genetic basis and involves glutathione S-transferase gene which was associated with resistance to three fungal leaf disease of maize (Wisser et al., 2011).
The additive and epistatic effect of multiple quantitative trait loci (QTL) may provide quantitative resistance to blast disease caused by Pyricularia oryzae in rice which may be comparable to that of major effect loci (Rosas et al., 2020). Three different kinds of epistasis can be distinguished with different outcome for resistance (Gallois et al., 2018):
- Positive epistasis corresponds to a more than-additive effect between resistance alleles at two QTL.
- Reciprocal sign epistasis is the combination of resistance alleles at two QTL that contributes to a higher susceptibility than the combination of two susceptibility alleles.
- Negative epistasis is intermediate, showing a less than-additive effect between resistance allele at two QTLs.
Characterizing the type of epistasis between resistance QTL is to gain an insight into the mechanisms involved and the resistance benefit expected from these epistases (Gallois et al., 2018). Epistasis is a major determinant of phenotypic variance for host plant resistance. Epistasis appears to occur predominantly between rather than within chromosomes. Wilfert and Schmid-Hempel (2008) suggest epistatic interactions is affected by segregation of chromosomes rather than by within-chromosome recombination. Indeed, the number of epistasis interactions increases with the number of chromosomes (Wilfert and Schmid-Hempel 2008).
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