Plant Tolerance: A Unique Approach to Control Hemipteran Pests

Abstract

Plant tolerance to insect pests has been indicated to be a unique category of resistance, however, very little information is available on the mechanism of tolerance against insect pests. Tolerance is distinctive in terms of the plant's ability to withstand or recover from herbivore injury through growth and compensatory physiological processes. Because plant tolerance involves plant compensatory characteristics, the plant is able to harbor large numbers of herbivores without interfering with the insect pest's physiology or behavior. Some studies have observed that tolerant plants can compensate photosynthetically by avoiding feedback inhibition and impaired electron flow through photosystem II that occurs as a result of insect feeding. Similarly, the up-regulation of peroxidases and other oxidative enzymes during insect feeding, in conjunction with elevated levels of phytohormones can play an important role in providing plant tolerance to insect pests. Hemipteran insects comprise some of the most economically important plant pests (e.g., aphids, whiteflies), due to their ability to achieve high population growth and their potential to transmit plant viruses. In this review, results from studies on plant tolerance to hemipterans are summarized, and potential models to understand tolerance are presented.

Keywords: ROS; constitutive; hemipteran pests; inducible; model; plant tolerance; susceptibility.

FIGURE 1

Predicted interactions between ROS and plant hormones during the tolerance response. Initial response to herbivory is through the generation of ROS and the activation of basal immunity. Potential interactions between basal immunity and genotypic-dependent constitutive responses are represented with broken black lines ending in arrows. These events take place within a few hours to a few days. More ROS is generated during this immune response leading to interactions with both the constitutive and induced responses in the plant. Both the induced and constitutive responses result in changes in plant hormones. ROS by itself and plant hormones trigger ROS mitigation, which leads to redox rebalancing. Redox rebalancing restores growth. Changes in plant growth have been normally reported as a longer term (>10 days) response. Whereas it is possible that early responses could control tolerance, it would seem more likely that cellular networks controlling plant hormone levels and ROS mitigation are more likely to underpin the tolerance response.

FIGURE 2

Conceptualization of cellular changes in a tolerant phenotype. Initial aphid probing of leaves, followed by continued feeding leads to multiple plant responses. Initial perception of the pest is accompanied by a photosynthetic response in the chloroplasts, and mitigation of ROS that is likely to involve a number of cellular compartments. A consequence of these physiological changes is a repression of growth of meristems. As physiological processes return to normal, growth is reinitiated. Within chloroplasts, these changes are represented as change from dark green to light green to denote loss of functions, and from light green to dark green to indicate recovery of functions. Similarly, in the apical meristems, orange colored cells indicate a stressed state and the other colors indicate a healthy state.

FIGURE 3

Potential differences between an induced and constitutive plant tolerance response to hemipterans. A cartoon of a transverse section of monocot leaf with or without aphids is shown. In both types of predicted tolerance, there is a pre-infestation state, an infested state, followed by a sustained plant response to herbivory. (A) Induced tolerance, where there is a strong response to infestation and herbivory. (B) Constitutive tolerance, where plants have higher levels of protective mechanisms, and have a more attenuated response to hemipteran pests. (C) Plausible plant responses (arbitrary) to infestation over time. In resistant plants R (black dashed line), there is a minimal and short response due to underlying resistance mechanisms. In plants with constitutive tolerance Tc (green line), the response is present, but is more modulated and growth presumably begins sooner. For plants with induced tolerance Ti (red line), the responses to herbivory are more pronounced and last for a longer duration before reverting to conditions that permit plant growth. For susceptible plants S (blue line), there is a strong initial response to herbivory, but this response is not sustainable and the plant dies from accumulated insect damage.