Plants defense response against the plant pathogen is the ability to limit pathogen growth, which is plant resistance. Resistance and tolerance in plants are the two different strategies to deal with plant pathogens. Tolerance is the ability of plant to reduce the effect of the infection on its fitness irrespective of the pathogen’s multiplication. Diseases have negative impact on the plant. Tolerance is usually designated as either endurance or an intermediate level of observable resistance which is somewhere between immunity and full susceptibility (Schafer 1971). Schafer (1971) consider tolerance to fit into the broad concept of disease resistance such as a) escape, b) exclusion, c) host-parasite interactions following infection which leads to differing levels of disease and d) tolerance or endurance of a given level of disease. Tolerance has been defined as a limited symptom development or reduction in plant vigor or yield despite a normal virus accumulation as in susceptible cultivar (Jeger 2022).
Resistance reduces the risk of infection or multiplication, whereas tolerance does not (Pagan and Garcia-Arenal 2018). Gradually as the gene conferring disease resistance spreads through the population disease incidence reduce. Thus, gene conferring complete resistance cannot become fixed by selection in a host population and disease cannot be eliminated completely by natural selection for host resistance. Whereas, when the gene conferring disease tolerance spread through the population, disease incidence rise, increasing the evolutionary advantage of carrying the tolerance gene (Roy and Kirchner 2000). Plant resistance genes are crucial for plant defense and many a time fail to provide durable resistance. Studies indicate that there is strong balancing selection to maintain different alleles of immunity genes in wild populations of plants and that some of this diversity can be maintained for thousand of years if not millions of years (Koenig et al., 2019). Host resistance can be both general resistance as well as specific resistance, which may only be effective against a single pathogen species or genotype (Hulse et al., 2023). Plants can be resistant to virus and tolerant to the disease (Jeger 2022).
Under some condition the two strategies tolerance and resistance may be redundant. Organisms with high level of tolerance should not experience selection for resistance, because attack does not reduce fitness (organisms are tolerant). Resistance will prevent selection for tolerance, because resistant plants are not receiving attack and therefore will not benefit from the ability to withstand attack (Agrawal 2010). Theory predicts that host will evolve to maximize tolerance and resistance but not both (Montes et al., 2020).
A more tolerant host genotype will suffer a small loss in fitness per unit increase of pathogen population present within the host as compared to the less tolerant host genotype (Mikaberidze and McDonald 2020). A negative relationship between tolerance and resistance is not necessarily indicative of a metabolic tradeoff, whereby tolerance and resistance confer fitness cost. The study made by Mikaberidze and McDonald (2020) show that a tradeoff can arise via entirely different mechanism i.e. limitation in the amount of host tissue or resource available to the pathogen (or limitation in degree of fitness a host can lose because of infection). Studies propose that conditions that increase parasitism, hosts will reduce the allocation of resource to growth and will allocate more resources to reproduction, to maximize fitness under these unfavorable condition (Leventhal et al., 2014; Shukla et al., 2018).
In Arabidopsis mixed infection of Turnip mosaic virus (TuMV) and Cucumber mosaic virus (CMV) occurred in low frequency and single infections are predominant (Montes et al., 2020). It is not known which mechanism determines this infection exclusion pattern. Virus induced resource reallocation appears to be CMV specific and it is not triggered upon TuMV infection. Tolerance to TuMV is associated with changes in the length of pre-reproductive and reproductive period and CMV with resource reallocation from growth to reproduction and the tolerance to TuMV is traded-off against tolerance to CMV in a virulence-dependent manner (Montes et al., 2020). In Arabidopsis CMV and TuMV are seed transmitted.
Tolerance can be described as a stable equilibrium between the virus and its host, an interaction in which each partner not only accommodate trade-offs for survival but also receives some benefits, for example plant protection from super-infection by virulent viruses, virus infection of meristem tissues allowing vertical transmission (Paudel and Sanfacon 2018). This equilibrium which is associated with little selective pressure for the emergence of severe viral strains, is common in wild ecosystems and has implication for the management of viral disease in field (Paudel and Sanfacon 2018). Resistance reduces multiplication rate of the pathogen in the infected plant, whereas tolerance does not. These two defense strategies may lead to different outcome of plant-pathogen interactions (Pagan and Garcia-Arenal 2020). The proposed view is that resistance affects epidemic dynamics and because resistance reduces the pathogen fitness, it imposes the selection pressure on the pathogen that may lead to the resistance breaking down. The tolerance would not exert such a selection pressure and thus would be more stable (Pagan and Garcia-Arenal 2020). Tolerance enables susceptible plant to endure severe attack by rust fungus without sustaining severe losses in yield or quality (Caldwell et al., 1958). Resistance and tolerance are controlled by uncorrelated traits. Few traits in plant confer resistance by preventing contact between plant and pathogens or by reducing pathogen growth. The same or completely different host trait may increase host tolerance by reducing the effect of infection on fitness (Kover and Schaal 2002).
If the host can completely tolerate the damage caused by pathogen up to a certain replication rate, then this may result in commensalism, whereby infection causes no apparent virulence, but the original evolution of tolerance has been costly (Millner et al., 2006). Plants can tolerate infection or herbivory by increasing the chlorophyll concentration in the leaves, or increasing the size of the new leaves or the number of new branches, advancing the timing of bud break, delaying the senescence of infected tissue and increasing nutrient uptake (Roy and Kirchner 2000). Tolerance is a quantitative trait (Pagan and Garcia-Arenal 2020). It reduces the damage on the infected plant
References:
Agrawal, A. A. 2010 Current Trends in the Evolutionary Ecology of Plant Defence. Functional Ecology 25(2): 420 – 432
doi.org/10.1111/j.1365-2435.2010.01796.x
Caldwell, R. M., Schafer, J. F., Compton, L. E. and Patterson, F. 1958 Tolerance to Cereal Leaf Rusts. Science 128(3326): 714 – 715
doi: 10.1126/science.128.3326.714
Hulse, S. V., Antonovics, J., Hood, M. E. and Bruns, E. L. 2023 Specific Resistance Prevents the Evolution of General Resistance and Facilitates Disease Emergence. Journal of Evolutionary Biology 36(5): 753 – 763
doi.org/10.1111/jeb.14170
Jeger, M. J. 2022 Tolerance of Plant Virus Disease: Its Genetics, Physiological and Epidemiological Significance. Plant and Energy Security 12(6): e440
doi.org/10.1002/fes3.440
Koenig, D., Hagmann, J., Li, R., Bemm, F., Slotte, T., Neuffer, B., Wright, S. I. and Weigel, D. 2019 Long-Term Balancing Selection Drives Evolution of Immunity Genes in Capsella. eLife 8:e43606
doi.org/10.7554/eLife.43606
Kover, P. X. and Schaal, B. A. 2002 Genetic Variation for Disease Resistance and Tolerance among Arabidopsis thaliana Accessions. Special Issue Physiological and Molecular Dissection of Reproductive Stage Stress Tolerance in Crop Plants. PNAS 99(17): 11270 – 11274
doi.org/10.1073/pnas.102288999
Leventhal, G. E., Dunner, R. P. and Barribeau, S. M. 2014 Delayed Virulence and Limited Costs Promote Fecundity Compensation Upon Infection. Am. Nat. 183(4): 480 – 493
doi: 10.1086/675242
Miller, M. R., White, A. and Boots, M. 2006 The Evolution of Parasites in Response to Tolerance in their Hosts: The Good, The Bad and Apparent Commensalism. Evolution 60(5): 945 – 956
doi.org/10.1111/j.0014-3820.2006.tb01173.x
Mikabaridze, A. and McDonald, B. A. 2020 A Tradeoff between Tolerance and Resistance to a Major Fungal Pathogen in Elite Wheat Cultivars. New Phytologist 226(3): 879 – 890
doi.org/10.1111/nph.16418
Montes, N., Vijayan, V. and Pagan, I. 2020 Trade-Off between Host Tolerances to Different Pathogens in Plant-Virus Interactions. Virus Evolution 6(1): veaa019
doi.org/10.1093/ve/veaa019
Roy, B. A. and Kirchner, J. W. 2000 Evolutionary Dynamics of Pathogen Resistance and Tolerance. Evolution 54(1): 51 – 63
doi: 10.1111/j.0014-3820.2000.tb00007.x
Pagan, I. and Garcia-Arenal, F. 2018 Tolerance to Plant Pathogens: Theory and Experimental Evidence. Int. J. Mol. Sci. 19(3): 810
doi: 10.3390/ijms19030810
Pagan, I. and Garcia-Arenal, F. 2020 Tolerance of Plant to Pathogens: A Unifying View. Annu. Rev. Phytopathol. 58: 77 – 96
doi.org/10.1146/annurev-phyto-010820 – 012749
Paudel, D. B. and Sanfacon, H. 2018 Exploring the Diversity of Mechanisms Associated with Plant Tolerance to Virus Infection. Front. Plant Sci. 9: 1575
doi: 10.3389/fpls.2018.01575
Schafer, J. F. 1971 Tolerance to Plant Disease. Annu. Rev. Phytopathol. 9: 235 – 252
doi.org/10.1146/annurev.py.09.090171.001315
Shukla, A., Pagan, I. and Garcia-Arenal, F. 2018 Effective Tolerance Based on Resource. Reallocation is a Virus-Specific Defense in Arabidopsis thaliana. Mole. Plant Pathol. 19(6): 1454 – 1465
doi: 10.1111/mpp.12629
BIOLOGICAL PROCESSES- A NATURE'S GIFT 