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.

BackgroundAphid infestation of switchgrass (Panicum virgatum) has the potential to reduce yields and biomass quality. Although switchgrass-greenbug (Schizaphis graminum; GB) interactions have been studied at the whole plant level, little information is available on plant defense responses at the molecular level.ResultsThe global transcriptomic response of switchgrass cv Summer to GB was monitored by RNA-Seq in infested and control (uninfested) plants harvested at 5, 10, and 15 days after infestation (DAI). Differentially expressed genes (DEGs) in infested plants were analyzed relative to control uninfested plants at each time point. DEGs in GB-infested plants induced by 5-DAI included an upregulation of reactive burst oxidases and several cell wall receptors. Expression changes in genes linked to redox metabolism, cell wall structure, and hormone biosynthesis were also observed by 5-DAI. At 10-DAI, network analysis indicated a massive upregulation of defense-associated genes, including NAC, WRKY, and MYB classes of transcription factors and potential ancillary signaling molecules such as leucine aminopeptidases. Molecular evidence for loss of chloroplastic functions was also detected at this time point. Supporting these molecular changes, chlorophyll content was significantly decreased, and ROS levels were elevated in infested plants 10-DAI. Total peroxidase and laccase activities were elevated in infested plants at 10-DAI relative to control uninfested plants. The net result appeared to be a broad scale defensive response that led to an apparent reduction in C and N assimilation and a potential redirection of nutrients away from GB and towards the production of defensive compounds, such as pipecolic acid, chlorogenic acid, and trehalose by 10-DAI. By 15-DAI, evidence of recovery in primary metabolism was noted based on transcript abundances for genes associated with carbon, nitrogen, and nutrient assimilation.ConclusionsExtensive remodeling of the plant transcriptome and the production of ROS and several defensive metabolites in an upland switchgrass cultivar were observed in response to GB feeding. The early loss and apparent recovery in primary metabolism by 15-DAI would suggest that these transcriptional changes in later stages of GB infestation could underlie the recovery response categorized for this switchgrass cultivar. These results can be exploited to develop switchgrass lines with more durable resistance to GB and potentially other aphids.Electronic supplementary materialThe online version of this article (doi:10.1186/s12870-017-0998-2) contains supplementary material, which is available to authorized users.

The corn leaf aphid (CLA; Rhopalosiphum maidis) is a phloem sap-sucking insect that attacks many cereal crops, including maize (Zea mays). We previously showed that the maize inbred line Mp708, which was developed by classical plant breeding, provides enhanced resistance to CLA. Here, using electrophysiological monitoring of aphid feeding behavior, we demonstrate that Mp708 provides phloem-mediated resistance to CLA. Furthermore, feeding by CLA on Mp708 plants enhanced callose deposition, a potential defense mechanism utilized by plants to limit aphid feeding and subsequent colonization. In maize, benzoxazinoids (BX) or BX-derived metabolites contribute to enhanced callose deposition by providing heightened resistance to CLA. However, BX and BX-derived metabolites were not significantly altered in CLA-infested Mp708 plants, indicating BX-independent defense against CLA. Evidence presented here suggests that the constitutively higher levels of 12-oxo-phytodienoic acid (OPDA) in Mp708 plants contributed to enhanced callose accumulation and heightened CLA resistance. OPDA enhanced the expression of ethylene biosynthesis and receptor genes, and the synergistic interactions of OPDA and CLA feeding significantly induced the expression of the transcripts encoding Maize insect resistance1-Cysteine Protease, a key defensive protein against insect pests, in Mp708 plants. Furthermore, exogenous application of OPDA on maize jasmonic acid-deficient plants caused enhanced callose accumulation and heightened resistance to CLA, suggesting that the OPDA-mediated resistance to CLA is independent of the jasmonic acid pathway. We further demonstrate that the signaling function of OPDA, rather than a direct toxic effect, contributes to enhanced CLA resistance in Mp708.

Switchgrass, Panicum virgatum L., is being developed as a bioenergy feedstock. The potential for large-scale production has encouraged its evaluation as a host for important grass pests. Eight no-choice studies were performed for two developmental stages of two switchgrass cultivars ('Kanlow' and'Summer') and two experimental strains, K x S, and S x K produced by reciprocal mating of these cultivars followed by selection for high yield. Plants were evaluated for host suitability and damage differences to herbivory by four important cereal aphids, Sipha flava (Forbes), Schizaphis graminum (Rondani) (biotype I), Rhopalosiphum padi (L.), and Diuraphis noxia (Mordvilko). All switchgrasses were found to be unsuitable feeding and reproductive hosts to R. padi and D. noxia, which were unable to establish on the plants. However, both S. flava and S. graminum were able to establish on all switchgrasses tested. Differential levels of resistance to S. flava and S. graminum were detected among the switchgrasses by both cumulative aphid days (CAD) and plant damage ratings. Kanlow was consistently rated as highly resistant based on CAD and damage ratings for both aphid species, while Summer was consistently among the most susceptible to both aphids at both developmental stages, with relatively high damage ratings. The resistance of the K x S and S x K populations in relationship to their Summer and Kanlow parents indicted that they inherited some resistance to S. graminum and S. flava from their Kanlow parent. These studies provide valuable baseline information concerning the host suitability of switchgrass to four cereal aphids and the plant-insect interactions within a system that has been largely overlooked and indicate that there are genetic differences among switchgrass populations for resistance to some insects.

Switchgrass, Panicum virgatum L., has been targeted as a bioenergy feedstock. However, little is currently known of the mechanisms of insect resistance in this species. Here, two no-choice studies were performed to determine the categories (antibiosis and tolerance) and relative levels of resistance of three switchgrass populations (Kanlow-lowland ecotype, Summer-upland ecotype, and third generation derivatives between Kanlow×Summer plants, K×S) previously identified with differential levels of resistance to the greenbug, Schizaphis graminum (Rondani), and yellow sugarcane aphid, Sipha flava (Forbes). No-choice studies indicated that Kanlow possessed multi-species resistance, with high levels of antibiosis to both aphid species, based on aphid survival at 7 and 14 days after aphid introduction and cumulative aphid days, while K×S possessed low-to-moderate levels of antibiosis to S. flava. Further, functional plant loss indices based on plant height and biomass indicated that tolerance is an important category of resistance for Summer plants to S. graminum. These studies also indicated that Summer lacks both tolerance and antibiosis to S. flava, relative to the other switchgrasses tested, whereas K×S lack tolerance and antibiosis to S. graminum. These studies are the first attempt to analyze the categories of resistance in switchgrass and provide critical information for characterizing the biological mechanisms of resistance and improving our knowledge of the plant-insect interactions within this system.