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Simple Summary: Planthopper outbreaks in rice are associated with excessive fertilizer applications. Public research has focused on developing resistant rice to combat these outbreaks. However, to preserve ecosystem resilience, natural enemy efficacy should be maintained on resistant and susceptible rice. We examined the impact of egg parasitoids on planthoppers (Nilaparvata lugens (Stål) [BPH] and Sogatella furcifera (Horváth) [WBPH]) and a leafhopper (Nephotettix virescens (Distant) [GLH]) in field plots of resistant (IR62) and susceptible (IR64) rice under low and high nitrogen. GLH and WBPH were more abundant in low-nitrogen plots during dry (GLH) and wet (GLH, WBPH) season sampling at an early crop stage. GLH were also more abundant on IR64. Parasitoids killed between 24 and 52% of planthopper eggs during exposures in trap plants. Parasitism by Oligosita and Anagrus wasps was higher on IR64 (BPH eggs) and in high-nitrogen plots (Oligosita spp. on BPH and WBPH eggs; Anagrus spp. on BPH eggs). Parasitism by Anagrus spp. was associated with the presence of honeydew and was highest where honeydew was derived from BPH feeding on IR62; these effects were only observed under high nitrogen. Results suggest that honeydew from IR62 favors parasitoids when plants are most vulnerable (i.e., under high nitrogen), thereby countering nitrogen-induced declines in host resistance. Host plant resistance is the most researched method for the management of planthoppers and leafhoppers in tropical rice. For optimal effects, resistance should be resilient to fertilizer inputs and work in synergy with natural enemies. In field plot experiments, we examined how rice resistance and fertilizer inputs affect mortality of planthopper and leafhopper eggs by hymenopteran parasitoids. We used IR62 as a variety with resistance to Nilaparvata lugens (Stål) [BPH], Sogatella furcifera (Horváth) [WBPH] and Nephotettix virescens (Distant) [GLH], and IR64 as a susceptible control. The herbivores were more abundant during wet season sampling in low-nitrogen plots. During this study, parasitoids killed between 31 and 38% of BPH eggs and 24 and 52% of WBPH eggs during four days of field exposure. Parasitism, mainly due to Oligosita spp., was generally higher in high-nitrogen and IR64 plots. Similar densities of eggs in exposed plants suggest that these trends were mediated by semiochemicals and therefore support the Optimal Defense Hypothesis. Honeydew from BPH on IR62 had more xylem-derived wastes than honeydew on IR64. We applied honeydew from both varieties to sentinel plants. Parasitism by Anagrus spp. was higher on plants of either variety treated with honeydew derived from IR62; however, the effect was only apparent in high-nitrogen plots. Results suggest that Anagrus spp., by responding to honeydew, will counter the nitrogen-induced enhancement of planthopper fitness on resistant rice. [ABSTRACT FROM AUTHOR]

Simple Summary: The brown planthopper (Niliparvata lugens [Stål]) feeds on rice in Asia. Rice breeders have developed varieties with resistance to the planthopper; however, planthoppers quickly adapt to these varieties (called 'virulence adaptation'). We examined the potential role during adaptation of endosymbionts that are passed by the female through the egg. We adapted planthoppers by exposure to resistant rice (IR62) for >20 generations, and crossed males or females from these adapted populations with non-adapted males and females that were reared on susceptible rice. Virulent males and females contributed to the virulence of their offspring as revealed through faster development rates, higher growth rates, greater numbers of female offspring, and an increased longevity of progeny on IR62 compared to the progeny of avirulent planthoppers on IR62; however, the female contribution to virulence was greater than that of the male. Reducing densities of YLS in adult planthoppers through heat treatment reduced their capacity to gain weight on IR62, irrespective of the virulence of parents, thereby suggesting that YLS derived from the female parent play a role in the vertical transfer of virulence; however, the effects were weak and IR62 seedlings were still more affected by heat-treated planthoppers with a virulent female parent than by heat-treated planthoppers with a virulent male parent or with avirulent parents only. Virulence is a complex state with multiple underlying mechanisms, some of which are derived only from the female parent. The adaptation by planthoppers to feed and develop on resistant rice is a challenge for pest management in Asia. We conducted a series of manipulative experiments with the brown planthopper (Nilaparvata lugens (Stål)) on the resistant rice variety IR62 (BPH3/BPH32 genes) to assess behavioral and bionomic changes in planthoppers exhibiting virulence adaptation. We also examined the potential role of yeast-like symbionts (YLS) in virulence adaptation by assessing progeny fitness (survival × reproduction) following controlled matings between virulent males or females and avirulent males or females, and by manipulating YLS densities in progeny through heat treatment. We found virulence-adapted planthoppers developed faster, grew larger, had adults that survived for longer, had female-biased progeny, and produced more eggs than non-selected planthoppers on the resistant variety. However, feeding capacity—as revealed through honeydew composition—remained inefficient on IR62, even after 20+ generations of exposure to the resistant host. Virulence was derived from both the male and female parents; however, females contributed more than males to progeny virulence. We found that YLS are essential for normal planthopper development and densities are highest in virulent nymphs feeding on the resistant host; however, we found only weak evidence that YLS densities contributed more to virulence. Virulence against IR62 in the brown planthopper, therefore, involves a complex of traits that encompass a series of behavioral, physiological, and genetic mechanisms, some of which are determined only by the female parent. [ABSTRACT FROM AUTHOR]

Simple Summary: Rice in Asia is damaged by a range of sap-sucking planthoppers. For the last 50 years, the main focus for integrated management of these insects was to develop resistant rice varieties. A single, bulk phenotyping test, known as the standard seedling seedbox test (SSST) was used to inform the majority of genetics and breeding programs for planthopper-resistant rice. However, there has been much debate over the efficacy of this test. We compared results from the SSST against those from a range of other phenotyping tests to assess how antibiosis and tolerance (the ability of rice to compensate for damage) affect test results, and how phenotyping might be improved to capture information regarding plant traits that are otherwise overlooked by the SSST. Based on the efficacy and costs of different tests, we recommend that breeding programs adopt a modified seedling seedbox test (MSST) when phenotyping 100s of rice lines but that insect performance tests that assess relative changes in planthopper biomass could be adopted when phenotyping fewer lines (e.g., <100 lines). The days-to-wilt (DTW) test was found to be particularly effective in segregating resistant/tolerant lines from susceptible lines. The standard seedling seedbox test (SSST) is the most prevalent phenotyping test in research on the genetics and breeding of planthopper-resistant rice. Using 16 rice lines that included plants susceptible, resistant and tolerant to the brown planthopper (Nilaparvata lugens), we compared the SSST to modified seedling seedbox tests (MSSTs) and the days-to-wilt (DTW) test. We also conducted a series of performance tests to assess nymph survival and development; adult longevity and egg-laying; egg survival; honeydew production; and plant weight loss. We also assessed the relative costs of the different phenotyping tests to better recommend test protocols that are suitable for high-throughput phenotyping. The SSST was found to be highly robust but fails to identify late-stage resistance; tolerance; or ovicidal responses. MSSTs improved phenotyping by identifying plants with low damage from planthoppers at later growth stages. Herbivore performance tests such as population or biomass build-up tests reduce space requirements and reduce setup and evaluation costs compared with bulk tests. They can also facilitate the assessment of plant tolerance; albeit with added costs. The DTW test most clearly segregates resistant and susceptible plants, thereby facilitating gene discovery and marker-assisted selection. We recommend that bulk testing be improved by switching from the SSST to a suitable MSST and that donor variety and pre-release lines be assessed for the nature of rice–planthopper interactions using biomass build-up tests—including the DTW test. [ABSTRACT FROM AUTHOR]

Simple Summary: Plant sap-sucking insects can secrete saliva into the plant and excrete honeydew on the plant surface, which both interfere with the plant's immune system. However, knowledge about the composition of insect honeydew and the roles it plays in plant defenses is limited. In the present study, a diversity of proteins in the honeydew of two major rice pests, the brown planthopper and green rice leafhopper, were identified by way of proteomic analysis. Results revealed that the honeydew contains some insect proteins that originate from the saliva and guts, proteins that originate from plant sap via the insect digestion system as well as many bacterial proteins from insect or plant symbionts and from plant surfaces. These abundant proteins from insects, microbes and plants in the honeydew might be elicitors, effectors or self-recognized molecules for plant defenses, which provide further insights into their roles in the multitrophic interactions of plants–insects–microbes. Honeydew is a watery fluid excreted by plant sap-feeding insects. It is a waste product for the insect hosts. However, it plays important roles for other organisms, such as serving as a nutritional source for beneficial insects and bacteria, as well as elicitors and effectors modulating plant responses. In this study, shotgun LC–MS/MS analyses were used to identify the proteins in the honeydew from two important rice hemipteran pests, the brown planthopper (Nilaparvata lugens, BPH) and green rice leafhopper (Nephotettix cincticeps, GRH). A total of 277 and 210 proteins annotated to insect proteins were identified in the BPH and GRH honeydews, respectively. These included saliva proteins that may have similar functions as the saliva proteins, such as calcium-binding proteins and apolipophorin, involved in rice plant defenses. Additionally, a total of 52 and 32 Oryza proteins were identified in the BPH and GRH honeydews, respectively, some of which are involved in the plant immune system, such as Pathogen-Related Protein 10, ascorbate peroxidase, thioredoxin and glutaredoxin. Coincidentally, 570 and 494 bacteria proteins were identified from the BPH and GRH honeydews, respectively, which included several well-known proteins involved in the plant immune system: elongation factor Tu, flagellin, GroEL and cold-shock proteins. The results of our study indicate that the insect honeydew is a complex fluid cocktail that contains abundant proteins from insects, plants and microbes, which may be involved in the multitrophic interactions of plants–insects–microbes. [ABSTRACT FROM AUTHOR]