Tolerance: the forgotten child of plant resistance

Abstract

Plant resistance against insect herbivory has greatly focused on antibiosis, whereby the plant has a deleterious effect on the herbivore, and antixenosis, whereby the plant is able to direct the herbivore away from it. Although these two types of resistance may reduce injury and yield loss, they can produce selection pressures on insect herbivores that lead to pest resistance. Tolerance, on the other hand, is a more sustainable pest management strategy because it involves only a plant response and therefore does not cause evolution of resistance in target pest populations. Despite its attractive attributes, tolerance has been poorly studied and understood. In this critical, interpretive review, we discuss tolerance to insect herbivory and the biological and socioeconomic factors that have limited its use in plant resistance and integrated pest management. First, tolerance is difficult to identify, and the mechanisms conferring it are poorly understood. Second, the genetics of tolerance are mostly unknown. Third, several obstacles hinder the establishment of high-throughput phenotyping methods for large-scale screening of tolerance. Fourth, tolerance has received little attention from entomologists because, for most, their primary interest, research training, and funding opportunities are in mechanisms which affect pest biology, not plant biology. Fifth, the efforts of plant resistance are directed at controlling pest populations rather than managing plant stress. We conclude this paper by discussing future research and development activities.

Tolerance and overcompensation to infection by Phytophthora infestans in the wild perennial climber Solanum dulcamara

“…Mechanisms of tolerance are generally poorly understood (Koch et al, 2016;Peterson et al, 2017). It has been suggested that compensation for damage caused by herbivory or pathogen infection could consist of several factors.…”

“…It has been suggested that compensation for damage caused by herbivory or pathogen infection could consist of several factors. These include increased chlorophyll concentrations, increased nutrient uptake, increased use of stored resources, delayed flowering and senescence, increased size or number of tissues such as leaves, modified phytohormone balance and altered resource allocation patterns between roots and shoots, or between growth and reproduction (Koch et al, 2016;Mitchell et al, 2016;Pagán & García-Arenal, 2018;Peterson et al, 2017;Strauss & Agrawal, 1999;Tiffin, 2000). In S. nigrum, herbivory was shown to lead to down-regulation of the hormone system and a subsequent increase in root allocation, which may favor competition with other plants following herbivory (Schmidt & Baldwin, 2009).…”

“…In future studies, it would be of great interest to explore the potential mechanism and genetics behind our result in S. dulcamara. So far, no study has identified genes contributing to variation in tolerance to pathogen infection in any organism (Medzhitov, Schneider, & Soares, 2012;Peterson et al, 2017;Soares, Teixeira, & Moita, 2017). Increased knowledge of the genetics of tolerance to pathogens in wild study systems can provide a better general understanding of the selective forces of resistance versus tolerance and their evolutionary consequences.…”

“…Identifying tolerance mechanisms could, therefore, have important implications, for the development of sustainable pest management tools for crops attacked by severe and rapidly evolving pests or pathogens (Mitchell, Brennan, Graham, & Karley, 2016;Peterson, Varella, & Higley, 2017).…”

“…In particular tolerance to herbivory has been studied extensively (Koch et al, 2016;Mitchell et al, 2016;Núñez-Farfán, Fornoni, & Valverde, 2007;Strauss & Agrawal, 1999). The study of tolerance to pests and pathogens is complicated by the difficulty of defining and quantifying tolerance (Peterson et al, 2017;Stowe et al, 2000). For example, while tolerance to infection by pathogens has been identified in a number of study species and crops (Kover & Schaal, 2002;Parker, Welham, Paveley, Foulkes, & Scott, 2004;Politowski & Browning, 1978;Simms & Triplett, 1994; see also review by Pagán & García-Arenal, 2018), the definitions used for tolerance to infection are often inconsistent (Bingham & Newton, 2009;Castro & Simón, 2016).…”