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Article

Different Maize Ear Rot Fungi Deter the Oviposition of Yellow Peach Moth (Conogethes punctiferalis (Guenée)) by Maize Volatile Organic Compounds

by
Yinhu Chen
1,†,
Jie Han
1,†,
Haiqing Yang
2,
Xiaochun Qin
1,
Honggang Guo
1,* and
Yanli Du
1,*
1
College of Bioscience and Resource Environment/Key Laboratory of Urban Agriculture (North China), Ministry of Agriculture and Rural Affairs of the People’s Republic of China, Beijing University of Agriculture, Beijing 102206, China
2
Beijing Pinggu District People’s Government Fruit Office, Beijing 101200, China
*
Authors to whom correspondence should be addressed.
†
These authors contributed equally to this work.
Agronomy 2023, 13(1), 251; https://doi.org/10.3390/agronomy13010251
Submission received: 12 December 2022 / Revised: 5 January 2023 / Accepted: 11 January 2023 / Published: 14 January 2023
(This article belongs to the Special Issue Adaptation and Responses of Insects under Abiotic, Biotic and Xenobiotic Constraints)
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Abstract

:
Yellow peach moth (Conogethes punctiferalis (Guenée), (Lepidoptera: Crambidae), YPM) and maize ear rot are important pests and diseases of maize (Zea mays L., (Poales: Poaceae)). In recent years, YPM has become the most destructive maize pest in the Huang-Huai-Hai summer maize region of China via the tunneling of larvae into maize ears. Interestingly, YPM infestation aggravates the occurrence of maize ear rot and causes heavier yield loss of maize in the field. However, few studies report whether maize ear rot would also affect the behavior of YPM. Here, we identified the effects of maize ear rot caused by four different fungi on maize ears’ volatile organic compounds (VOCs) and the cascading effects on the behavior of YPM. The current results found that mated YPM females showed a preference for mock-inoculated maize ears (MIM) or mechanically damaged maize ears (MDM) but showed repellence to Penicillium oxalicum (Eurotiales: Aspergillaceae)-infected maize ears (POM), Trichoderma asperellum (Hypocreales: Hypocreaceae)-infected maize ears (TAM), Aspergillus phoenicis (Eurotiales: Aspergillaceae)-infected maize ears (APM), Aspergillus flavus (Eurotiales: Aspergillaceae)-infected maize ears (AFM) in the oviposition selection and four-arm olfactometer experiments, indicating that VOCs emitting from fungi-infected maize ears were all repellent to mated YPM females. Further analyses showed that 57 VOCs were identified from all treatments. The partial least squares discriminant analysis (PLS-DA) displayed a separation between TAM, APM, AFM and POM, MDM, and MIM, with 24.3% and 19.1% explanation rates of the first two PLS components. Moreover, the relative quantities of eight common VOCs from different treatments were lower, and the other three common VOCs were higher in fungi-infected maize ears than those in MIM or MDM. There were also 17 unique VOCs in fungi-infected maize ears. In conclusion, these results suggested that maize ear rot negatively affected the behavior of YPM by changing both components and proportions of maize ears’ VOCs. These behavior-modifying VOCs may form the basis for the development of attractant or repellent formulations for YPM’s management in the future.

1. Introduction

In the agroecosystem, host plants are closely associated not only with herbivorous insects but also with fungi. Previous studies have demonstrated that plant-pathogenic microbes, including protists, bacteria, and fungi, can drastically modify plant metabolisms and, therefore, may have important consequences for the diversity and composition of herbivorous insect species [1,2,3,4,5,6,7,8]. Thus, it is meaningful to investigate tripartite interactions among plant-pathogenic microbes, host plants, and herbivorous insects to improve our knowledge on co-evolutionary theories of plant–fungi–insect interactions and design more effective management strategies for plant-pathogenic fungi and herbivorous insects in the agroecosystem.
Plant-pathogenic microbes have been reported as direct or indirect drivers for host plant-herbivorous insect interactions, but the outcomes of plant-pathogenic microbes on herbivorous insects’ behaviors are inconsistent. A few studies demonstrate the attraction of herbivorous insects to plant-pathogenic fungi-infected host plants, while others suggest repellence or no effect [7,8]. For example, yellow peach moth (YPM) females (Conogethes punctiferalis(Guenée), (Lepidoptera: Crambidae), YPM) were attracted to and laid more eggs on different Penicillium infected apples (Malus domestica M., (Rosales: Rosales)) than non-infected apples [9]. However, the bird cherry oat-aphids (Rhopalosiphum padi, (Hemiptera: Aphididae)) prefer uninfected over Neotypphodium-infected wild grass alpine timothy (Phleum alpinum (Poales: Poaceae)). In contrast, the beetles (Oulema melanopus, (Coleoptera: Chrysomelidae)) have no preference for Neotyphodium-infected and uninfected wild grass [10]. Given the important role of plant-pathogenic fungi, recent studies show that larval western bean cutworm (Striacosta albicosta, (Lepidoptera: Noctuidae)) and YPM infestation could significantly aggravate the occurrence of maize ear diseases and cause heavier yield loss of maize (Zea mays L., (Poales: Poaceae)) [11,12], which triggers us to explore whether maize ear disease could also affect the behavior of YPM.
Host plant volatile organic compounds (VOCs) are primary olfactory cues employed by herbivorous insects to locate and orient to food sources and oviposition sites [13,14]. Changes in the components and/or proportions of host plant VOCs caused by fungi infection could be perceived by herbivorous insects, which could then result in the behavioral responses of herbivorous insects from attractiveness to repellence or vice versa [7,15,16]. For example, the infection of Penicillium fungi alters apple fruits’ VOC profiles, including inducing 16 novel VOCs and increasing the absolute contents of ethyl hexanoate and (Z, E)-α-farnesene, which results in strong attractiveness to mated YPM females [9]. Moreover, except for host plant VOCs, VOCs from the fungus itself (Melampsora larici-populina, (Pucciniales: Melampsoraceae)) also attract herbivorous insects (Lymantria dispar, (Lepidoptera: Lymantriidae)) [5], suggesting that VOCs emitted from host plants and fungi are both olfactory signals for establishing tripartite interactions among herbivorous insects, host plants, and plant-pathogenic fungi [17,18].
The YPM is a generalist herbivorous insect that attacks more than 100 plant species, such as maize, chestnut (Castanea mollissima Blume, (Fagales: Fagaceae)), sunflower (Helianthus annuus L., (Campanulales: Compositae)), hawthorn (Crataegus pinnatifida Bunge, (Rosales: Rosales)), apple, and so on [19,20], and has become the most destructive maize pest in the Huang-Huai-Hai region of China in the last 20 years [21,22]. The YPM is a multivoltine species with three to four generations per year in North China that overwinters as diapausing larvae [23]. The larvae of YPM are typical fruit borers that infest and use maize ears as food sources and habitats to complete their life cycle in the summer maize region of China [21]. The YPM adult is a nocturnal, herbivorous insect, which feeds, oviposits, and develops primarily in buds and fruits of plants [24]. Furthermore, oviposition is an important event in the life cycle of YPM, and adult females select host plants with optimal features to lay their eggs to maximize offspring fitness [25] If oviposition is prevented, the life cycle of YPM is disrupted, and population growth can be decreased. Moreover, recent studies suggest that sex pheromones and plant-derived attractants or repellents are used as allelochemicals to selectively prevent the mating and/or oviposition behavior of YPM in the integrated pest management of YPM [26,27]. Except for YPM, maize is also affected by maize ear rot, which is one of the most prevalent and destructive diseases of maize. The maize ear rot is caused by more than 40 fungal species alone or together, such as Fusarium spp., Aspergillus spp., Trichoderma spp., and so on [28,29,30]. The incidence of maize ear rot is commonly ranged from 5% to 20% in 22 provinces in China’s fields [31]. The susceptible cultivars can be >50% incidence of maize ear rot in conducive climates, resulting in 30% to 40% yield losses [32]. For example, the incidence of Penicillium maize ear rot is about 3% to 90% in some areas of Shanxi, Shaanxi, Hebei, and Tianjin in China [33]. It is the 5% incidence of maize ear rot in Lingshui, Hainan Province, China, in 2016 [34]. Interestingly, YPM infestation significantly aggravates the occurrence of maize ear rot and causes heavier yield loss of maize [12], suggesting the strong effects of YPM on plant-pathogenic fungi (maize ear rot) and triggering us to explore the effect of maize ear rot on the behavior of YPM.
Here, we hypothesized that fungi isolated from maize ears with maize ear rot could affect the behavior of YPM by altering maize ears’ VOCs. To test this hypothesis, the following experiments were carried out: (1) the isolation and purification of fungi from maize ears with maize ear rot to identify the plant-pathogenic fungi; (2) the oviposition selection and four-arm olfactometer experiments among mock-inoculated maize ears, mechanically damaged maize ears, single fungal strain-infected maize ears, and the corresponding fungus growing in potato dextrose agar (PDA) medium to determine the effects of plant-pathogenic fungi on host plant selection behavior of mated YPM females; (3) VOCs collection and analysis of the above-mentioned treatments to clarify the effects of plant-pathogenic fungi on maize ear’ VOCs.

2. Materials and Methods

2.1. Insects

A colony of YPM was established and maintained for about 80 generations on maize ears in climate incubators (RTOP-B, Zhejiang Top Instrument Co., Ltd., Hangzhou, China) at 23 ± 1 °C, RH 75 ± 2%, 16L/8D photoperiod, and 3500 lux light intensity. Adult moths were provided with 5–8% honey solution after emergence. Apples covered with gauze pieces were provided for the oviposition of YPM in the cage. The YPM colony kept in climate incubators in the lab was mixed with the field-collected YPM on maize ears every year.

2.2. Isolation and Purification of Four Fungal Strains

Four fungal strains (SS1 strain, SS2 strain, SS3 strain, and SS4 strain) were isolated and purified from maize ears with maize ear rot using the traditional tissue separation method. The symptomatic-asymptomatic junction tissues were cut into segments (about 0.5 cm × 0.5 cm) under the horizontal-laminar airflow clean bench and were then immersed completely into 2% NaClO (Sangon biotech Co., Ltd., Shanghai, China) for 3 min and then flushed with sterilized water three times. Next, the junction tissues were immersed completely into 75% ethanol (Beijing Minda Technology Co., Ltd., Beijing, China) for 1 min and then flushed with sterilized water three times. Finally, segments were placed onto PDA (Beijing Aoboxing Biotechnology Co., Ltd., Beijing, China) (containing (g/L): potato 200; dextrose 20; agar 18) medium in Petri dishes, which were then placed in a constant temperature incubator (Shanghai Fuma Experiemental Equipment Co., Ltd., Shanghai, China) at 27 °C. After 4 times of repeated purification, a pure culture of the fungal strain was obtained.

2.3. Morphological Identification of Four Fungal Strains

The four fungal strains were identified via their micro-morphological and colony morphological characters. After growing on PDA at 27 °C for 7 days, the colony morphology of the four fungal strains was observed. The micro-morphology of the four fungal strains was observed by light microscopy (Motic BA200, Motic China Group Co., Ltd., Xiamen, China).

2.4. Molecular Identification of Four Fungal Strains

Fresh hyphae or conidia were picked and immersed into sterile water in a 1.5 mL centrifuge tube. The suspension of hyphae or conidia was then centrifuged at 10,000 r/min for 3 min. The precipitate was collected and drained with filter paper for further analysis.
Total genomic DNA was extracted directly from pure hyphae or conidia using the rapid extraction kit of fungal genomic DNA (Aidlab Biotechnologies Co., Ltd., Beijing, China) following the manufacturer’s instructions. The internal transcribed spacer region (ITS) of the ribosomal DNA (rDNA) was amplified with ITS1/ITS4 primers (ITS1: 5′-TCCGTAGGTGAACCTGCGG-3′; ITS4: 5′-TCCTCCGCTTATTGATATGC-3′) [35]. Amplification reactions were performed in a 50 μL reaction volume containing 25.0 μL 2 × Taq PCR Master Mix (Biomed, Beijing, China), 1.7 μL genomic DNA, 1.0 μL of 100 μmol primer (Sangon Biotec, Beijing), and 22.3 μL ddH2O according to the polymerase chain reaction (PCR) program described in Guo et al. [9]. To further identify the four fungal strains, phylogenetic trees based on their ITS sequences were constructed with the neighbor-joining method in Mega 7.0. Clade stabilities were estimated using bootstrap values, which were generated from 1000 replications.

2.5. Pathogenicity Test of Four Fungal Strains

The pathogenicity test was performed using a modified protocol for conidial suspensions [36]. Conidial suspensions of the four fungal strains were prepared by adding 10 mL of sterile distilled water onto 7-day-old cultures of PDA medium and swirling gently to remove the conidia. The conidial suspensions were filtered with a muslin cloth to remove the hyphae and transferred into a centrifuge tube. The conidial suspensions were adjusted to the concentrations of SS1 strain-infected maize ears (6.4 × 107 conidia/mL), SS2 strain-infected maize ears (5.6 × 108 conidia/mL), SS3 strain-infected maize ears (6.0 × 107 conidia/mL), and SS4 strain-infected maize ears (6.0 × 107 conidia/mL) with a hemocytometer (XB-K-25 type, Yuhuan precision medical instrument factory, Taizhou, China) for further pathogenicity testing.
Maize ears were sterilized with 75% (v/v) ethanol, rinsed with sterilized distilled water, and then air-dried on sterilized filter paper under the horizontal-laminar airflow clean bench. Maize ears were cut into pieces (about 80 g) and inoculated using wound inoculation methods. Eight strip-type lesions (about 5 cm length × 0.5 cm depth) were scuffed by a sterile knife at different rows of maize kernels and then inoculated with 1 mL conidial suspensions of the same fungal strain or 1 mL sterile distilled water, which served as the control. The maize ears were placed in sterilized plastic boxes (19 cm × 13 cm × 10 cm) containing 50 mL sterile distilled water to maintain humidity and cultured in a constant temperature incubator at 27 °C for 3–9 days. The symptoms of fungi-infected maize ears were recorded. All experiments were carried out under the horizontal-laminar airflow clean bench.

2.6. Maize Treatments

The YPM adult preferred to oviposit on fruits of plants, so the maize ears, but not intact plants, were selected for the following experiments. Maize ears were bought from the supermarket of the Beijing University of Agriculture (Beijing, China). It was not easy to perform the experiments with intact maize ears, so each maize ear was cut into 3–4 pieces (about 80 g/piece). The dissected maize ear pieces were firstly sterilized using 75% alcohol for 2 min and washed with sterilized distilled water under the horizontal-laminar airflow clean bench for further experiments, including oviposition selection experiments, four-arm olfactometer experiments, and VOCs collection.
Mock-inoculated maize ears (MIM): A piece of dissected maize ear (about 80 g) without fungi infection and mechanical damage was prepared as MIM. The MIMs were placed in sterilized plastic boxes (25.7 cm × 18.6 cm × 10.2 cm) and cultured 3 d at 27 °C for further experiments.
Mechanically damaged maize ears (MDM): A piece of dissected maize ear (about 80 g) was scuffed with eight strip-type lesions (about 5 cm length × 0.5 cm depth) by a sterile knife at different rows of maize kernels and then injected with 1 mL of sterilized distilled water. The MDMs were kept and cultured as MIM for further experiments.
Fungi-infected maize ears: A piece of dissected maize ear (about 80 g) was treated as MDM, except that 1 mL conidial suspension was injected instead of sterilized distilled water for Penicillium oxalicum (Sphaeropsidales: Discellaceae)-infected maize ears (POM, 6.0 × 107 conidia/mL), Trichoderma asperellum (Moniliales: Moniliales)-infected maize ears (TAM, 5.6 × 108 conidia/mL), Aspergillus phoenici (Sphaeropsidales: Discellaceae)-infected maize ears (APM, 6.0 × 107 conidia/mL), and Aspergillus flavus (Eurotiales: Trichocomaceae)-infected maize ears (AFM, 6.4 × 107 conidia/mL). The fungi-infected maize ears were kept and cultured as MIM for further experiments.

2.7. Oviposition Selection Experiments

The oviposition selection experiment was carried out to determine the effects of four fungal strains on the oviposition behavior of mated YPM females. For P. oxalicum, the dissected maize ear pieces with different treatments, including MIM, MDM, POM, and P. oxalicum strain growing in PDA medium (PPO), were separately put into two opposite plastic bowls with punched holes. The bowls were covered with wet cheesecloth and were randomly placed at each one of the four inner corners of a wood-frame cage (40 cm × 35 cm × 35 cm) with plastic gauze on the sides to allow oviposition from 10 mated YPM females. The cheesecloths were replaced every day, and the position of each treatment in one cage was changed randomly. The experiment was arranged in a randomized complete block design, with four treatments being one treatment factor. Each of the experimental units was measured for 7 days, so the data collection time (days of YPM oviposition) was the second treatment factor. Each cage was a block, and there were 20 blocks. The egg numbers on each sheet were separately counted per day. The oviposition selection rate (dependent variables) was treated as the egg numbers of one treatment per day (independent variables)/the total egg numbers of four treatments (MIM, MDM, POM, and PPO) per day.
For the other three fungal strains, the oviposition selection of mated YPM females was performed (1) among MIM, MDM, TAM, and T. asperellum strain growing in PDA medium (PTA), or (2) among MIM, MDM, APM, and A. phoenici strain growing in PDA medium (PAP), or (3) among MIM, MDM, AFM, and A. flavus strain growing in PDA medium (PAF) were performed as same as P. oxalicum strain.

2.8. Four-Arm Olfactometer Experiments

A four-arm olfactometer was used to test the behavioral responses of mated YPM females to the odors among MIM, MDM, POM, and PPO treatments according to the methods in Guo et al. [9]. The behavioral response was classified as a choice if the moth passed over 1/3 length of the arm associated with one of the four odors and stayed there for more than 30 s. Conversely, no choice was assigned if the tested moth remained in the common arm for 3 min. Females that did not make a choice within five min were not included in the statistical analysis. As a result, a total of 85 individual moths (T. asperellum), 80 individual moths (A. flavus), 84 individual moths (A. phoenici), and 82 individual moths (P. oxalicum) were used to analyze the responsive rate of females. The responsive rate of females in the four-arm olfactometer experiment was defined as the selection rate, which was calculated as the number of females that made a selection for the odor/the total number of females that made a selection for any odors offered simultaneously. For the other three fungal strains, the details were the same as the P. oxalicum strain.

2.9. VOCs Collection and Analysis

VOCs from different treatments were collected using the dynamic headspace collection method, as described in Guo et al. [9]. Briefly, two pieces of the dissected maize ear (about 80 g/piece) from each treatment or similar size PDA medium inoculated with the same fungal strain were placed into a 48.3 cm × 59.7 cm Reynolds oven bag (Reynolds Kitchens, Richmond, VA, USA). The Reynolds oven bags were bought from Amazon (https://gs.amazon.cn, access on 8 November 2022). The bag mouth was tightened with a twist tie around a glass tube (6 mm diameter, 10 cm long) filled with 50 mg of Porapark Q adsorbent (80–100 mesh, Waters Corporation of America Inc., Milford, MA, USA). At the bottom of the bag, a small hole was made and connected to a Teflon tube. The humidified and purified air was pushed into the oven bag at a rate of 450 mL/min, and the VOCs were trapped by 50 mg porapark Q adsorbent (80–100 mesh, Waters Co.). At the same time, an empty bag was prepared to identify what VOCs were in the background. The collection of VOCs lasted for 4 h from 7:30–11:30 A.M. Five replicates of each treatment were performed and collected at the same time. The trapped VOCs were eluted using 350 μL of chromatography-grade n-hexane (Fisher Scientific, 99.9%) and stored at −20 °C. For GC-MS analyses, 200 μL of eluent was subsampled, and 1 μL of n-nonyl acetate (TCI, 99.9%) was added as an internal standard.
The identification and quantification of maize’ VOCs were carried out using a Shimadzu gas chromatograph (GC) coupled to a Shimadzu mass spectrometer (MS) (GCMS-QP2010E, Japan). The GC was equipped with a DB-5MS column (30 m × 0.25 μm × 0.25 μm). Helium was used as the carrier gas with a constant flow of 36.534 cm/s. The injector temperature was 200 °C, the GC-MS transfer line temperature was 280 °C, the source 230 °C, the quadrupole 150 °C, the ionization potential 70 eV, and the scan range was 30–300 m/z. Each 1 μL sample was injected by the mode of splitless. Following injection, the column temperature was maintained at 55 °C for 1 min and then programmed at 5 °C/min to 220 °C (held for 6 min). Compounds were identified by comparing mass spectra with the NIST Standard Reference Database (Shimadzu Co., Kyoto, Japan) and quantified by their total ion abundance relative to that of the internal standard.

2.10. Statistical Analysis

The Shapiro–Wilks test and Bartlett’s test were used to check the normality of the distribution and the equality (homogeneity) of the variances of the dependent variables, respectively. Data obtained from oviposition selection experiments were analyzed with repeated-measures analysis to determine the effect of different treatments on the oviposition selection rates of mated YPM females. For P. oxalicum, the statistical model included the effect of the treatment group (MIM, MDM, POM, and PPO), days of YPM oviposition, and their interactions. The treatment group differences were subjected to a one-way analysis of variance using Duncan’s new multiple-range test at p < 0.05. Data from behavioral bioassay in four-arm olfactometer experiments were subjected to one-way analysis of variance using Duncan’s new multiple range test (p < 0.05). The other three fungal strains were also analyzed as the P. oxalicum strain. The relative quantities of VOCs were subjected to a one-way analysis of variance using Duncan’s new multiple-range test (p < 0.05). All these statistics were analyzed with SPSS 22.0 statistical software (International Business Machines Corporation, Chicago, IL, USA). The partial least squares discriminant analysis (PLS-DA) was performed with the R program (version 4.1.2) (R Foundation for Statistical Computing, Vienna, AUS). Graphs were generated in Graphpad Prism 9.0 (Graphpad software, Boston, MA, USA).

3. Results

3.1. Morphological and Molecular Identification of Maize Ear-Surface Fungi

Four fungal strains with different morphology were isolated from the surface of maize ears with maize ear rot, called SS1 strain, SS2 strain, SS3 strain, and SS4 strain. The texture of the SS1 strain was mainly dense velvet, and the central part was flocculent and flat. The colony color of the SS1 strain was yellow to green. It was light at the initial stage and slightly dark after aging (Figure 1A). The conidium of the SS1 strain was spherical (Figure 1B). The SS2 strain had concentric annular colonies with dark green on the PDA medium for 3 days. The aerial hypha of the SS2 strain was sparse (Figure 1C). The conidium of the SS2 strain was oval, and the conidium stalk with slight spiny protrusions was slender and curved (Figure 1D). The colony color of SS3 was dark brown-to-black, and its reverse side was colorless to yellow on the PDA medium (Figure 1E). The conidium was a spherical vesicle, and the conidial head color was light tan to black (Figure 1F). The SS4 strain was velutinous with fluffy and white aerial mycelium that eventually turned green on PDA medium after 3 days. The conidiophore was broom-shaped and conidium was colorless, unicellular, and ellipsoid (Figure 1G,H).
The rDNA-ITS sequences of four fungal strains were cloned for further identification. The SS1 strain (a 566 bp ITS fragment) was clustered with Aspergillus flavus ((Eurotiales: Aspergillaceae), KX067853) by a bootstrap value of 99% (Figure 1I). The SS2 strain (a 600-bp ITS fragment) was grouped with Trichoderma asperellum ((Hypocreales: Hypocreaceae), MH215551), and the SS3 strain (a 613-bp ITS fragment) was clustered with Aspergillus phoenicis ((Eurotiales: Aspergillaceae), LC360746), which was well supported by a bootstrap value of 99% (Figure 1J,K). The ITS sequences of the SS4 strain (a 561-bp ITS fragment) were 100% identical to Penicillium oxalicum isolate ((Eurotiales: Aspergillaceae), MN416225) (Figure 1L).
Combined with morphological and molecular characters, the SS1 strain was identified as A. flavus, the SS2 strain was identified as T. asperellum, the SS3 strain was identified as A. phoenicis, and the SS4 strain was identified as P. oxalicum.

3.2. The Host Preference of Mated YPM Females among MIM, MDM, Fungi-Infected Maize Ear, and the Same Fungal Strain Growing in PDA Medium

For P. oxalicum and A. phoenicis, the highest oviposition selection rates of mated YPM females were on their respective MDM treatments, followed by those on MIM. The lowest were both on fungi-infected maize ears (POM or APM) and fungi growing in PDA medium (PPO or PAP) along with the extension of infection time from the 1st to 7th day, respectively (Figure 2A,C; Table 1). For T. asperellum, the oviposition selection rate of mated YPM females was the highest on MDM from the beginning till the end (54.43%), which was significantly higher than those on MIM (31.50%), TAM (12.93%), and PTA (1.12%) (Figure 2B; Table 1). As for A. flavus, the mated YPM females preferred to lay eggs on MIM during the first three days, then showed preference to MDM in the 4th–5th days, but returned to MIM again on the 7th day. It was worth mentioning that on the first day after infection, the YPM laid much more eggs on AFM than on MDM but turned over from the second day till the end. Considering the average oviposition selection rate of 1–7 d, the oviposition selection rates on MIM (50.20%) and on MDM (39.65%) were both significantly higher than those on AFM (9.64%) and on PAF (0.51%) (Figure 2D; Table 1).
A four-arm olfactometer experiment was also prepared to test behavioral responses of mated YPM females to VOCs of different treatments. For P. oxalicum, VOCs of MDM showed the most attractiveness to mated YPM females (the selection rate of 41.19%), which was significantly higher than VOCs of MIM (the selection rate of 28.55%), PPO (the selection rate of 18.61%), and POM (the selection rate of 9.01%) (F3,12 = 12.337, p = 0.001) (Figure 3A). For T. asperellum and A. flavus, mated YPM females showed a markedly higher preference for VOCs of MIM and MDM than VOCs of fungi-infected maize ears (TAM or AFM) and fungi growing in PDA medium (PTA or PAF), respectively (Figure 3B,D). For A. phoenicis, the selection rate of mated YPM females to VOCs of MIM (36.44%) was significantly higher than that of VOCs of APM (14.72%). The selection rates of mated YPM females to VOCs of MDM (28.70%) and PAP (25.14%) were intermediate (F3,12 = 3.040, p = 0.071) (Figure 3C). These results suggested that mated YPM females showed significant repellence to the odor of fungi-infected maize ears (PPO, TAM, APM, and PAF).

3.3. VOC Profiles of Different Treatments

A total of 57 VOCs were detected in the headspace of different treatments, including 30 VOCs in MIM, 32 VOCs in MDM, 36 VOCs in POM, 24 VOCs in TAM, 34 VOCs in APM, and 24 VOCs in AFM (Table 2). According to the PLS-DA analysis based on the relative contents of all detected VOCs, the first two significant PLS components explained 24.3% and 19.1% of the total variances, respectively. It was worth mentioning that the VOCs of three fungi-infected maize ears (TAM, APM, and AFM) were clearly separated and obviously distinguishable from VOCs of POM, resembling those of MDM and MIM (Figure 4). Furthermore, there were 17 fungi-induced unique VOCs, including (E, E, E)-2,4,6-Octatrien, 2-propylheptanol, methyl benzoate, 2-pentadecanol, 5-propyltridecane in POM, benzaldehyde, 1-octen-3-one, 4-ethylanisole in TAM, 4-methoxystyrene, 3,8-dimethylundecane, 5-butylnonane in APM, 2-ethyl-cyclopentanone and butyl butyrate in AFM, 3-octanone in POM, APM, TAM, 3-octanol in TAM and APM, 3,7-dimethyldecane in TAM, APM, AFM, β-bisabolene in POM, TAM, APM, AFM. Moreover, compared with VOCs in MIM and MDM, the relative quantities of 8 common VOCs, including 2-heptanone, m-xylene, 2-heptanol, 3-(1-methylpropyl)- cyclohexene, D-limonene,2-nonanone, ethyl benzoate, and caryophyllene were decreased. The other three common VOCs (1-Octen-3-ol, 1, 3-dichlorobenzene, butylated hydroxytoluene) were increased in fungi-infected maize ears (POM, TAM, APM, AFM) (Table 1).

4. Discussion

Plants are closely associated not only with herbivorous insects but also with fungi, which leads to intimate and complex tripartite interactions. The illustration of tripartite interactions will be beneficial for designing durable ways to integrate the management of plant-pathogenic fungi and pests in agroecosystems. Here, we investigated the effects of maize ear rot caused by A. flavus, T. asperellum, A. phoenicis, and P. oxalicum on the behavior of YPM. Mated YPM females were repelled by fungi-infected maize ears (POM, TAM, APM, and AFM) but were attracted to MDM or MIM. Furthermore, compared with MIM and MDM, there were not only 17 fungi-induced unique VOCs but also a decrease in the relative contents of 8 common VOCs and an increase in the other three common VOCs in fungi-infected maize ears, indicating that plant-pathogenic fungi infection could change both components and proportions of host plant VOCs. These findings shed light on the chemical cues of plant-pathogenic fungi in modulating YPM behaviors.
The most common maize ear rot is caused by fungi in the genus Fusarium, such as Fusarium miscanthi (Tuberculariales: Tuberculariaceae), Fusarium proliferatum (Tuberculariales: Tuberculariaceae), and Fusarium verticillioides (Tuberculariales: Tuberculariaceae) [28,29,30]. Except for Fusarium spp., more than 40 fungal species, such as Aspergillus spp., Trichoderma spp., and so on, have also caused maize ear rot alone or together [37]. Similarly, four fungal strains were isolated from maize ears with maize ear rot and identified as A. flavus, T. asperellum, A. phoenicis, and P. oxalicum by morphological and molecular characters, and further confirmed by Koch’s postulates experiments in the present study. For A. flavus, it is known as one of the common and serious pathogens of maize ear rot [38]. For the other three pathogens, our results and previous documents also confirm that Trichoderma spp. and Penicillium spp. cause maize ear disease in tropical and subtropical areas of the world [39,40].
It has been reported that maize ear disease affects the preference and performance of herbivorous insects. For example, A. flavus, a main pathogen of maize ear rot, has a negative effect on maize earworm (Helicoverpa zea, (Lepidoptera: Noctuidae)) with a nearly 4-fold decrease in the infestation rate in CML322 maize [41], which resembles present results that four different fungi-infected maize ears significantly deterred mated YPM females. Interestingly, a recent study has also shown that females of Diatraea saccharalis (Lepidoptera: Pyralidae) without F. verticillioides prefer fungi-infected sugarcane plants and females with F. verticillioides prefer mock plants, suggesting that F. verticillioides gains dissemination benefits by modulating the selection behavior of D. saccharalis [42]. In fact, maize borers, such as Sesamia nonagrioides (Lepidoptera: Noctuidae) and Ostrinia nubilalis (Lepidoptera: Pyralidae), serve as vectors of maize ear rot, including Fusarium spp. and Aspergillus spp., which improves the dissemination of maize ear rot [43]. Furthermore, it has been shown that YPM infestation significantly aggravates the occurrence of maize ear rot and causes heavier yield loss of maize [44]. Therefore, further experiments will be needed to analyze the behavioral responses of YPM with pathogens of maize ear rot between fungi-infected and mock-inoculated maize ears for understanding the interactions between YPM and maize ear diseases.
Plant-pathogenic fungi alter the host plant selection behavior of herbivorous insects via modifying host plant VOCs [45,46]. Maize plants with plant growth-promoting rhizobacteria (PGPR), such as Bacillus pumilus (Bacillales: Bacillaceae) INR-7 and Bacillus mojavensis (Bacillales: Bacillaceae), emit fewer VOCs and therefore deter the oviposition of European maize borer [47]. A significant decrease in the emission of maize ears’ VOCs, including 2-heptanone, m-xylene, 2-heptanol, and so on, was also found in fungi-infected maize ears (POM, TAM, APM, AFM) in the present study. However, we also found that the relative quantities of VOCs, such as 1-octen-3-ol and 1, 3-dichlorobenzene, were higher in POM, TAM, APM, and AFM than those in MIM or MDM. This is consistent with a previous report that fungal endophyte (Neotyphodium lolii) decreases the emission of dodecane and increases the emission of 2-ethyl-1-hexanol acetate in perennial ryegrass (Lolium perenne, (Poales: Poaceae)), which in part, explains the relatively lower selection rate of African black beetles (Heteronychus arator, (Coleoptera: Scarabaeidae)) to N. lolii-infected plants [48]. Besides changes in the relative quantities of host plant VOCs, the specific VOCs induced by fungi infection can also serve as chemotaxic markers for modulating herbivorous insects’ behavior [15,49]. In the present study, some unique VOCs, including 2-propylheptanol, methyl benzoate, 3-octanone, and so on, were detected in fungi-infected maize ears (POM, TAM, APM, AFM), suggesting a potential role of changes in host plant VOCs in the repellency of mated YPM. Moreover, there are numerous examples that VOCs emitted by the fungus could enhance the attraction of lepidopteran insects to host plants [50,51,52]. Nonetheless, a few cases also suggest that fungal VOCs have an avoidant effect on the behavior of herbivorous insects [17]. VOCs from the fungus were also collected and identified in our study, in which the relative quantities of some VOCs were significantly different between fungi themselves (PPO, PTA, PAP, PAF) and corresponding fungi-infected maize ears (POM, TAM, APM or AFM).
Furthermore, some specific VOCs in the present study have been confirmed as chemotaxonomic markers in regulating herbivorous insects’ behaviors. The 2-heptanone, an important green-leaf volatile of host plants, is very attractive to the wasp Anagrus nilaparvatae (Hymenoptera: Mymaridae) at a wide range of concentrations from 0 to 500 n mol, but 2-heptanone and 2-heptanol have a repellent role in brown planthopper (Nilaparvata lugens, (Hemiptera: Delphacidae)) [53]. D-limonene of Citrus spp. Fruits are increased by Aonidiella aurantii (Hemiptera: Diaspididae) infestation and attract parasitoids Aphytis melinus (Hymenoptera: Aphelinidae) [54]. Three dominant pest species of the genus Adelphocoris (Hemiptera: Miridae), including A. suturalis, A. lineolatus, and A. fasciaticollis, are attracted to the individual compound m-xylene in field trials [55]. In contrast, the 1-octen-3-ol produced by Tricholoma matsutake (Agaricales: Tricholomataceae) repels Proisotoma minuta (Collembola: Insecta) [56]. Interestingly, the current study showed that the relative quantities of D-limonene, 2-heptanone, 2-heptanol, and m-xylene were decreased, while the relative quantity of 1-octen-3-ol was increased in fungi-infected maize ears, suggesting that those VOCs might be involved in the repellence of mated YPM females to the fungi-infected maize ears. Except for common VOCs in all treatments, the fungi-induced unique VOCs can also be important. For example, 3-octanol, a fungi-induced unique VOC in TAM and APM, has inhibitory effects on the attraction of spruce bark beetle (Ips typographus, (Coleoptera: Scolytidae)) to pheromone [57]. Methyl benzoate, a fungi-induced unique VOC in POM, exhibits repellent effects against Cimex lectularius (Hemiptera: Cimicidae) and Bemisia tabaci (Hemiptera: Aleyrodidae) [58,59]. Therefore, further experiments are needed to screen candidate active VOCs from the host plant and fungus itself that can be perceived by YPM, which can be considered as putative VOCs as attractants or repellents of YPM.
In summary, our findings demonstrated that fungi-infected maize ears emitted behavior-modifying VOCs that influence the host recognition and selection of YPM. These behavior-modifying VOCs may be used to produce attractant or repellent lures for field management of YPM in the future.

Author Contributions

Conceptualization, Y.D. and H.G.; Investigation, Y.C. and J.H.; Formal Analysis, H.G., Y.C. and J.H.; Visualization, H.G.; Writing—Original Draft Preparation, H.G.; Writing—Review & Editing, H.Y., X.Q., Y.D. and H.G.; Funding Acquisition, Y.D and H.G. All authors have read and agreed to the published version of the manuscript.

Funding

This study was supported by the science & technology fund of the Beijing Municipal Commission of Education (grant number KZ202210020027), Science Fund for Young Scholars from the Beijing University of Agriculture to H.G. Guo (grant number QNKJ202103), Beijing University of Agriculture Science and Technology innovation Sparkling support plan (grant number, BUA-HHXD2022004), and 2022 Research and Innovation ability promotion Fund for Young Scholars from the Beijing University of Agriculture to H.G. Guo (grant number, QJKC2022001).

Data Availability Statement

The data presented in this study are openly available, and the accession number will be applied after the manuscript is accepted.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Biere, A.; Tack, A.J.M. Evolutionary adaptation in three-way interactions between plants, microbes and arthropods. Funct. Ecol. 2013, 27, 646–660. [Google Scholar] [CrossRef] [Green Version]
  2. Weeraddana, C.S.; Manolii, V.P.; Strelkov, S.E.; de la Mata, A.P.; Harynuk, J.J.; Evenden, M.L. Infection of canola by the root pathogen Plasmodiophora brassicae increases resistance to aboveground herbivory by bertha armyworm, Mamestra configurata Walker (Lepidoptera: Noctuidae). Plant Sci. 2020, 300, 110625. [Google Scholar] [CrossRef] [PubMed]
  3. Eberl, F.; Hammerbacher, A.; Gershenzon, J.; Unsicker, S.B. Leaf rust infection reduces herbivore-induced volatile emission in black poplar and attracts a generalist herbivore. New Phytol. 2018, 220, 760–772. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  4. Eberl, F.; Uhe, C.; Unsicker, S.B. Friend or foe? The role of leaf-inhabiting fungal pathogens and endophytes in tree-insect interactions. Fungal Ecol. 2019, 38, 104–112. [Google Scholar] [CrossRef]
  5. Eberl, F.; Bobadilla, M.F.D.; Reichelt, M.; Hammerbacher, A.; Unsicker, S.B. Herbivory meets fungivory: Insect herbivores feed on plant pathogenic fungi for their own benefit. Ecol. Lett. 2020, 23, 1073–1084. [Google Scholar] [CrossRef]
  6. Rivera, M.J.; Pelz-Stelinski, K.S.; Martini, X.; Stelinski, L.L. Bacterial phytopathogen infection disrupts belowground plant indirect defense mediated by tritrophic cascade. Ecol Evol. 2017, 7, 4844–4854. [Google Scholar] [CrossRef]
  7. Grunseich, J.M.; Thompson, M.N.; Aguirre, N.M.; Helms, A.M. The role of plant-associated microbes in mediating host-plant selection by insect herbivores. Plants 2019, 9, 6. [Google Scholar] [CrossRef] [Green Version]
  8. Al-Naemi, F.; Hatcher, P.E. Contrasting effects of necrotrophic and biotrophic plant pathogens on the aphid Aphis fabae. Entomol. Exp. Appl. 2013, 148, 234–245. [Google Scholar] [CrossRef]
  9. Guo, H.G.; Han, C.Y.; Zhang, A.H.; Yang, A.Z.; Qin, X.C.; Zhang, M.Z.; Du, Y.L. Penicillium fungi mediate behavioral responses of the yellow peach moth, Conogethes punctiferalis (Guenée) to apple fruits via altering the emissions of host plant VOCs. Arch. Iinsect. Biochem. 2022, 110, e21895. [Google Scholar] [CrossRef]
  10. Clement, S.L.; Hu, J.; Stewart, A.V.; Wang, B.; Elberson, L.R. Detrimental and neutral effects of a wild grass-fungal endophyte symbiotum on insect preference and performance. J. Insect Sci. 2011, 11, 77. [Google Scholar] [CrossRef]
  11. Parker, N.S.; Anderson, N.R.; Richmond, D.S.; Long, E.Y.; Wise, K.A.; Krupke, C.H. Larval western bean cutworm feeding damage encourages the development of Gibberella ear rot on field corn. Pest Manag. Sci. 2017, 73, 546–553. [Google Scholar] [CrossRef] [PubMed]
  12. Yang, S.; Shi, J.; Zhang, H.; Guo, N.; Li, P.; Wang, Z.Y. Impacts of durian fruit borer Conogethes punctiferalis on yield loss of summer corn by injuring corn ears. J. Plant Prot. 2015, 42, 991–996. (In Chinese) [Google Scholar]
  13. Price, P.W.; Denno, R.F.; Eubanks, M.D.; Finke, D.L.; Kaplan, I. Insect Ecology: Behavior, Populations, and Communities; Cambridge University Press: New York, NY, USA, 2011; pp. 1–801. [Google Scholar]
  14. Davis, T.S.; Crippen, T.L.; Hofstetter, R.W.; Tomberlin, J.K. Microbial volatile emissions as insect semiochemicals. J. Chem. Ecol. 2013, 39, 840–859. [Google Scholar] [CrossRef] [PubMed]
  15. Groen, S.C.; Jiang, S.; Murphy, A.M.; Cunniffe, N.J.; Westwood, J.H.; Davey, M.P. Virus infection of plants alters pollinator preference: A payback for susceptible hosts? PLoS Pathog. 2016, 12, e1005790. [Google Scholar] [CrossRef] [Green Version]
  16. Rizvi, S.Z.; Raman, A.; Wheatley, W.M.; Cook, G. Oviposition preference and larval performance of Epiphyas postvittana (Lepidoptera: Tortricidae) on Botrytis cinerea (Helotiales: Sclerotiniaceae) infected berries of Vitis vinifera (Vitales: Vitaceae). Insect Sci. 2016, 23, 313–325. [Google Scholar] [CrossRef] [PubMed]
  17. Tasin, M.; Knudsen, G.K.; Pertot, I. Smelling a diseased host: Grapevine moth responses to healthy and fungus-infected grapes. Anim. Behav. 2012, 83, 555–562. [Google Scholar] [CrossRef]
  18. Fernandez-Conradi, P.; Jactel, H.; Robin, C.; Tack, A.J.M.; Castagneyrol, B. Fungi reduce preference and performance of insect herbivores on challenged plants. Ecology 2018, 99, 300–311. [Google Scholar] [CrossRef]
  19. Li, D.Y.; Ai, P.P.; Du, Y.L.; Sun, S.L.; Zhang, M.Z. Effects of different host plants on the development and reproduction of yellow peach moth, Conogethes punctiferalis (Guenée) (lepidoptera: Crambidae). Austral Entomol. 2015, 54, 149–153. [Google Scholar] [CrossRef]
  20. Chen, G.M.; Chi, H.; Wang, R.C.; Wang, Y.P.; Xu, Y.Y.; Li, X.D.; Yin, P.; Zheng, F.Q. Demography and uncertainty of population growth of Conogethes punctiferalis (Lepidoptera: Crambidae) reared on five host plants with discussion on some life history statistics. J. Econ. Entomol. 2018, 111, 2143–2152. [Google Scholar] [CrossRef]
  21. Wang, Z.Y.; He, K.L.; Shi, J.; Ma, S.Y. Analysis of the heavily occurrence trend of the yellow peach borer in corn and its management strategy. Plant Prot. 2016, 32, 67–69. (In Chinese) [Google Scholar]
  22. Shwe, S.M.; Prabu, S.; Chen, Y.; Li, Q.; Jing, D.; Bai, S.; He, K.; Wang, Z. Baseline susceptibility and laboratory selection of resistance to Bt Cry1Ab protein of Chinese populations of Yellow Peach Moth, Conogethes punctiferalis (Guenée). Toxins 2021, 13, 335. [Google Scholar] [CrossRef] [PubMed]
  23. Lu, J.; Wang, Z.; He, K. Research history, progresses and prospects in the yellow peach moth, Conogethes punctiferalis. Plant Prot. 2010, 36, 31–38. (In Chinese) [Google Scholar]
  24. Jia, X.J.; Wang, H.X.; Yan, Z.G.; Zhang, M.Z.; Wei, C.H.; Qin, X.C.; Ji, W.R.; Falabella, P.; Du, Y.L. Antennal transcriptome and differential expression of olfactory genes in the yellow peach moth, Conogethes punctiferalis (Lepidoptera: Crambidae). Sci. Rep. 2016, 6, 29067. [Google Scholar] [CrossRef] [PubMed]
  25. Mayhew, P.J. Herbivore host choice and optimal bad motherhood. Trends Ecol. Evol. 2001, 16, 165–167. [Google Scholar] [CrossRef]
  26. Xiao, W.; Matsuyama, S.; Ando, T.; Millar, J.G.; Honda, H. Unsaturated cuticular hydrocarbons synergize responses to sex attractant pheromone in the yellow peach moth, Conogethes punctiferalis. J. Chem. Ecol. 2012, 38, 1143–1150. [Google Scholar] [CrossRef] [Green Version]
  27. Luo, Z.; Honda, H. Olfactory and biophysical assessment of the oviposition stimulating potential of host and non-host plants for the yellow peach moth, Conogethes punctiferalis (Lepidoptera: Crambidae). Appl. Entomol. Zool. 2015, 50, 183–189. [Google Scholar] [CrossRef]
  28. Lanubile, A.; Maschietto, V.; Borrelli, V.M.; Stagnati, L.; Logrieco, A.F.; Marocco, A. Molecular basis of resistance to fusarium ear rot in maize. Front. Plant Sci. 2017, 8, 1774. [Google Scholar] [CrossRef]
  29. Shang, G.; Yu, H.; Yang, J.; Zeng, Z.; Hu, Z. First report of Fusarium miscanthi causing ear rot on maize in China. Plant Dis. 2020, 105, 1565. [Google Scholar] [CrossRef]
  30. Tahat, M.M.; Aldakil, H.; Alananbeh, K.; Salem, N.M. First report of fusarium verticillioides causing fusarium ear rot of corn in Jordan. Plant Dis. 2022. Advance online publication. [Google Scholar] [CrossRef]
  31. Wang, J.H.; Li, H.P.; Zhang, J.B.; Wang, B.T.; Liao, Y.C. First report of Fusarium maize ear rot caused by Fusarium kyushuense in China. Plant Dis. 2014, 98, 279. [Google Scholar] [CrossRef]
  32. Duan, C.X.; Wang, X.M.; Song, F.J.; Sun, S.L.; Zhou, D.N.; Zhu, Z.D. Advances in research on maize resistance to ear rot. Sci. Agric. Sin. 2015, 48, 2152–2164. [Google Scholar]
  33. Liu, S.; Wang, J.; Guo, N.; Sun, H.; Ma, H.; Zhang, H.; Shi, J. Talaromyces funiculosus, a novel causal agent of maize ear rot and its sensitivity to fungicides. Plant Dis. 2021, 105, 3978–3984. [Google Scholar] [CrossRef] [PubMed]
  34. Sun, H.; Guo, N.; Ma, H.; Liu, S.; Shi, J. First report of maize ear rot caused by Exserohilum rostratum in Hainan Province in southern China. Plant Dis. 2021, 106, 314. [Google Scholar] [CrossRef]
  35. White, T.J.; Bruns, T.; Lee, S.; Taylor, J. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In PCR Protocols: A Guide to Methods and Applications; Innis, M.A., Gelfand, D.H., Sninsky, J.J., White, T.J., Eds.; Academic Press: New York, NY, USA, 1990; pp. 315–322. [Google Scholar]
  36. Noor, N.M.; Zakaria, L. Identification and characterization of Colletotrichum spp. associated with chili anthracnose in peninsular Malaysia. Eur. J. Plant Pathol. 2018, 151, 961–973. [Google Scholar] [CrossRef]
  37. Gaikpa, D.S.; Miedaner, T. Genomics-assisted breeding for ear rot resistances and reduced mycotoxin contamination in maize: Methods, advances and prospects. Theor. Appl. Genet. 2019, 132, 2721–2739. [Google Scholar] [CrossRef] [PubMed]
  38. Reese, B.N.; Payne, G.A.; Nielsen, D.M.; Woloshuk, C.P. Gene expression profile and response to maize kernels by Aspergillus flavus. Phytopathology 2011, 101, 797–804. [Google Scholar] [CrossRef] [Green Version]
  39. Munkvold, G.P.; White, D.G. Compendium of Corn Diseases; APS:: St. Paul, MN, USA, 2016; p. 165. [Google Scholar]
  40. Sanna, M.; Pugliese, M.; Gullino, M.L.; Mezzalama, M. First report of Trichoderma afroharzianum causing seed rot on maize in Italy. Plant Dis. 2022, 106, 1982. [Google Scholar] [CrossRef]
  41. Chalivendra, S.; Huang, F.; Busman, M.; Williams, W.P.; Ham, J.H. Low aflatoxin levels in Aspergillus flavus-resistant maize are correlated with increased corn earworm damage and enhanced seed fumonisin. Front. Plant Sci. 2020, 11, 565323. [Google Scholar] [CrossRef]
  42. Franco, F.P.; Moura, D.S.; Vivanco, J.M.; Silva-Filho, M.C. Plant–insect–pathogen interactions: A naturally complex ménage à trois. Curr. Opin. Microbiol. 2017, 37, 54–60. [Google Scholar] [CrossRef]
  43. Arias-Martín, M.; Haidukowski, M.; Farinós, G.P.; Patiño, B. Role of Sesamia nonagrioides and Ostrinia nubilalis as vectors of Fusarium spp. and contribution of corn borer-resistant Bt Maize to mycotoxin reduction. Toxins 2021, 13, 780. [Google Scholar] [CrossRef]
  44. Zhang, D.Z.; Li, P.C.; Chen, X.X.; Wang, C.X.; Yu, J.F. Isolation and identification of the pathogens causing wheat common root rot in Shandong Province. J. Plant Prot. 2016, 43, 233–240. (In Chinese) [Google Scholar]
  45. Fereres, A.; Peñaflor, M.F.; Favaro, C.F.; Azevedo, K.E.; Landi, C.H.; Maluta, N.K.; Bento, J.M.; Lopes, J.R. Tomato infection by whitefly-transmitted circulative and non-circulative viruses induce contrasting changes in plant volatiles and vector behaviour. Viruses 2016, 8, 225. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  46. El-Sayed, A.M.; Ganji, S.; Unelius, C.R.; Gemeno, C.; Ammagarahalli, B.; Butler, R.C.; Hoffmann, C. Feeding volatiles of larval Sparganothis pilleriana (Lepidoptera: Tortricidae) attract hetero specific adults of the European Grapevine Moth. Environ. Entomol. 2021, 50, 1286–1293. [Google Scholar] [CrossRef] [PubMed]
  47. Disi, J.O.; Zebelo, S.; Kloepper, J.W.; Fadamiro, H. Seed inoculation with beneficial rhizobacteria affects European corn borer (Lepidoptera: Pyralidae) oviposition on maize plants. Entomol. Sci. 2018, 21, 48–58. [Google Scholar] [CrossRef]
  48. Qawasmeh, A.; Raman, A.; Wheatley, W. Volatiles in perennial ryegrass infected with strains of endophytic fungus: Impact on African black beetle host selection. J. Appl. Entomol. 2014, 139, 94–104. [Google Scholar] [CrossRef]
  49. Gong, D.; Bi, Y.; Li, Y.; Zong, Y.; Han, Y.; Prusky, D. Both Penicillium expansum and Trichothecim roseum infections promote the ripening of apples and release specific volatile compounds. Front. Plant Sci. 2019, 10, 338. [Google Scholar] [CrossRef]
  50. Honda, H.; Ishiwatari, T.; Matsumoto, Y. Fungal volatiles as oviposition attractants for the yellow peach moth, Conogethes punctiferalis (Guenée) (Lepidoptera: Pyralidae). J. Insect Physiol. 1988, 34, 205–209. [Google Scholar] [CrossRef]
  51. Cossé, A.A.; Endris, J.J.; Millar, J.G.; Baker, T.C. Identification of volatile compounds from fungus-infected date fruit that stimulate upwind flight in female Ectomyelois-Ceratoniae. Entomol. Exp. Appl. 1994, 72, 233–238. [Google Scholar] [CrossRef]
  52. Cardoza, Y.J.; Teal, P.E.A.; Tumlinson, J.H. Effect of peanut plant fungal infection on oviposition preference by Spodoptera exigua and on host searching behaviour by Cotesia arginiventris. Environ. Entomol. 2003, 32, 970–976. [Google Scholar] [CrossRef]
  53. Liao, Z.; Wang, L.; Li, C.; Cao, M.; Wang, J.; Yao, Z.; Zhou, S.; Zhou, G.; Zhang, D.; Lou, Y. The lipoxygenase gene OsRCI-1 is involved in the biosynthesis of herbivore-induced JAs and regulates plant defense and growth in rice. Plant Cell Environ. 2022, 45, 2827–2840. [Google Scholar] [CrossRef]
  54. Mohammed, K.; Agarwal, M.; Li, B.; Newman, J.; Liu, T.; Ren, Y. Evaluation of d-Limonene and β-Ocimene as attractants of Aphytis melinus (Hymenoptera: Aphelinidae), a parasitoid of Aonidiella aurantii (Hemiptera: Diaspididae) on Citrus spp. Insects 2020, 11, 44. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  55. Xiu, C.L.; Pan, H.S.; Liu, B.; Luo, Z.X.; Williams, L., 3rd; Yang, Y.Z.; Lu, Y.H. Perception of and behavioral responses to host plant volatiles for three Adelphocoris species. J. Chem. Ecol. 2019, 45, 779–788. [Google Scholar] [CrossRef] [PubMed]
  56. Sawahata, T.; Shimano, S.; Suzuki, M. Tricholoma matsutake 1-Ocen-3-ol and methyl cinnamate repel mycophagous Proisotoma minuta (Collembola: Insecta). Mycorrhiza 2008, 18, 111–114. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  57. Zhang, Q.H.; Schlyter, F.; Birgersson, G. Bark volatiles from nonhost angiosperm trees of spruce bark beetle, Ips typographus (L.) (Coleoptera: Scolytidae): Chemical and electrophysiological analysis. Chemoecology 2000, 10, 69–80. [Google Scholar] [CrossRef]
  58. Strickland, J.; Larson, N.R.; Feldlaufer, M.; Zhang, A. (2022). Characterizing repellencies of methyl benzoate and its analogs against the Common Bed Bug, Cimex lectularius. Insects 2022, 13, 1060. [Google Scholar] [CrossRef] [PubMed]
  59. Mostafiz, M.M.; Jhan, P.K.; Shim, J.K.; Lee, K.Y. (2018). Methyl benzoate exhibits insecticidal and repellent activities against Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae). PLoS ONE 2018, 13, e0208552. [Google Scholar] [CrossRef]
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Figure 1. Morphological and molecular identification of the SS1 strain, SS2 strain, SS3 strain, and SS4 strain. The morphology of the SS1 strain (A,B); The morphology of the SS2 strain (C,D); The morphology of the SS3 strain (E,F); The morphology of the SS4 strain (G,H); Phylogenetic trees of four fungal strains: SS1strain (I), SS2 strain (J), SS3 strain (K), and SS4 strain (L) with other related strains based on rDNA-ITS sequences by the neighbor-joining method. The scale bar was 50 μm (B,D,F,H)
Figure 1. Morphological and molecular identification of the SS1 strain, SS2 strain, SS3 strain, and SS4 strain. The morphology of the SS1 strain (A,B); The morphology of the SS2 strain (C,D); The morphology of the SS3 strain (E,F); The morphology of the SS4 strain (G,H); Phylogenetic trees of four fungal strains: SS1strain (I), SS2 strain (J), SS3 strain (K), and SS4 strain (L) with other related strains based on rDNA-ITS sequences by the neighbor-joining method. The scale bar was 50 μm (B,D,F,H)
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Figure 2. The oviposition selection rates of mated YPM females in oviposition behavioral experiments. P. oxalicum (A), T. asperellum (B), A. phoenicis (C), A. flavus (D). 1–7 d: Days of YPM oviposition; MIM: mock-inoculated maize ears, MDM: mechanically damaged maize ears, POM: P. oxalicum-infected maize ears, TAM: T. asperellum-infected maize ears, APM: A. phoenicis-infected maize ears, AFM: A. flavus-infected maize ears, PPO: P. oxalicum growing in PDA medium, PTA: T. asperellum growing in PDA medium, PAP: A. phoenicis growing in PDA medium, and PAF: A. flavus growing in PDA medium. Different letters indicate significant differences among the four treatments (p < 0.05).
Figure 2. The oviposition selection rates of mated YPM females in oviposition behavioral experiments. P. oxalicum (A), T. asperellum (B), A. phoenicis (C), A. flavus (D). 1–7 d: Days of YPM oviposition; MIM: mock-inoculated maize ears, MDM: mechanically damaged maize ears, POM: P. oxalicum-infected maize ears, TAM: T. asperellum-infected maize ears, APM: A. phoenicis-infected maize ears, AFM: A. flavus-infected maize ears, PPO: P. oxalicum growing in PDA medium, PTA: T. asperellum growing in PDA medium, PAP: A. phoenicis growing in PDA medium, and PAF: A. flavus growing in PDA medium. Different letters indicate significant differences among the four treatments (p < 0.05).
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Figure 3. The selection rates of mated YPM females in four-arm olfactometer experiments. P. oxalicum (A), T. asperellum (B), A. phoenicis (C), A. flavus (D). MIM: mock-inoculated maize ears, MDM: mechanically damaged maize ears, POM: P. oxalicum-infected maize ears, TAM: T. asperellum-infected maize ears, APM: A. phoenicis-infected maize ears, AFM: A. flavus-infected maize ears, PPO: P. oxalicum growing in PDA medium, PTA: T. asperellum growing in PDA medium, PAP: A. phoenicis growing in PDA medium, and PAF: A. flavus growing in PDA medium. Different letters indicate significant differences among the four treatments (p < 0.05).
Figure 3. The selection rates of mated YPM females in four-arm olfactometer experiments. P. oxalicum (A), T. asperellum (B), A. phoenicis (C), A. flavus (D). MIM: mock-inoculated maize ears, MDM: mechanically damaged maize ears, POM: P. oxalicum-infected maize ears, TAM: T. asperellum-infected maize ears, APM: A. phoenicis-infected maize ears, AFM: A. flavus-infected maize ears, PPO: P. oxalicum growing in PDA medium, PTA: T. asperellum growing in PDA medium, PAP: A. phoenicis growing in PDA medium, and PAF: A. flavus growing in PDA medium. Different letters indicate significant differences among the four treatments (p < 0.05).
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Figure 4. Partial least squares discriminant analysis (PLS-DA) of maize ears’ VOCs. MIM: mock-inoculated maize ears; MDM: mechanically damaged maize ears; POM: P. oxalicum-infected maize ears; TAM: T. asperellum-infected maize ears; APM: A. phoenicis-infected maize ears; AFM: A. flavus-infected maize ears; PPO: P. oxalicum growing in PDA medium; PTA: T. asperellum growing in PDA medium; PAP: A. phoenicis growing in PDA medium; PAF: A. flavus growing in PDA medium. P1 and P2: the first two significant PLS components.
Figure 4. Partial least squares discriminant analysis (PLS-DA) of maize ears’ VOCs. MIM: mock-inoculated maize ears; MDM: mechanically damaged maize ears; POM: P. oxalicum-infected maize ears; TAM: T. asperellum-infected maize ears; APM: A. phoenicis-infected maize ears; AFM: A. flavus-infected maize ears; PPO: P. oxalicum growing in PDA medium; PTA: T. asperellum growing in PDA medium; PAP: A. phoenicis growing in PDA medium; PAF: A. flavus growing in PDA medium. P1 and P2: the first two significant PLS components.
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Table
Table 1. Effects of fungi infection, days of YPM oviposition, and their interactions on the oviposition selection rates among different treatments by repeated-measures analysis.
Table 1. Effects of fungi infection, days of YPM oviposition, and their interactions on the oviposition selection rates among different treatments by repeated-measures analysis.
FactorP. oxalicumT. asperellumA. phoenicisA. flavus
F Valuep ValueF Valuep ValueF Valuep ValueF Valuep Value
Days0.0001.0000.0001.0000.0001.0000.0001.000
Fungi infection120.374<0.00148.759<0.00184.714<0.0013.146<0.001
Days × Fungi infection2.1980.0101.7700.0460.9330.0252.5250.003
Table
Table 2. VOCs collected from different treatments, including MIM, MDM, POM, TAM, APM, AFM, PPO, PAT, PAP, and PAF Ⅰ.
Table 2. VOCs collected from different treatments, including MIM, MDM, POM, TAM, APM, AFM, PPO, PAT, PAP, and PAF Ⅰ.
No.Compound TypeRetention Time (min)Compounds ⅡMIM ⅢMDM ⅢPOM ⅢTAM ⅢAPM ⅢAFM ⅢPPO ⅢPAT ⅢPAP ⅢPAF Ⅲ
1Alkane8.223,7-dimethyldecane1.0375 ± 0.37 4 bc1.52 ± 0.39 4 b0.9525 ± 0.25 4 bc0.34 ± 0.09 3 c 3.542 ± 0.26 3 a
2Alkane9.427Undecane45.13 ± 7.46 4 a30.198 ± 3.28 4 b3.42 ± 0.59 5 c0.89 ± 0.14 5 c 1.54 ± 0.37 4 c
3Alkane14.2695-(2-methylpropyl)nonane9.23 ± 0.92 5 b11.40 ± 1.91 5 b2.07 ± 0.32 4 b1.82 ± 0.42 5 b1367.61 ± 121.00 5 a3.66 ± 0.70 3 b0.70 ± 0.05 5 b2.19 ± 1.00 5 b
4Alkane14.2892,3,6,7-tetramethyl-Octane11.41 ± 1.81 5 a9.66 ± 0.95 4 a0.65 ± 0.14 5 b0.69 ± 0.12 4 b 1.83 ± 0.39 5 b
5Alkane14.4913,8-Dimethylundecane28.85 ± 4.29 4 a32.22 ± 2.12 4 a9.94 ± 2.40 5 b1.19 ± 0.29 4 c
6Alkane14.793Dodecane0.91 ± 0.30 5 b1.05 ± 0.30 5 b22.97 ± 2.44 5 a1.18 ± 0.26 5 b
7Alkane14.865-Butylnonane1.74 ± 0.14 4 bc4.12 ± 0.92 3 b3.85 ± 0.09 4 b2.40 ± 0.23 5 bc 2.11 ± 0.72 5 bc2.31 ± 0.10 5 bc3.33 ± 0.42 4 b11.17 ± 1.84 3 a
8Alkane15.4943-methyl-5-propylnonane 10.51 ± 2.15 5
9Alkane17.3725-Propyltridecane 1.21 ± 0.13 4
10Alkane17.395Tridecane1.84 ± 0.25 5 a1.00 ± 0.13 5 b
11Alkane19.791Eicosane 17.51 ± 2.82 5
12Alkane19.876Tetradecane 41.42 ± 5.21 5
13Alkane20.865Nonadecane 2.15 ± 0.28 5 c14.08 ± 1.37 4 c277.97 ± 39.74 5 a92.20 ± 20.59 3 b7.11 ± 0.24 3 c 11.21 ± 0.73 4 b82.21 ± 5.23 5 b50.50 ± 12.45 4 c
14Alkane22.231Pentadecane 2 ± 0.40 5 b12.10 ± 3.92 5 b148.20 ± 9.93 4 a
15Alkane24.447Hexadecane 45.48 ± 1.11 3
16Alkane24.7092,6,11,15-tetramethyl- Hexadecane 14.95 ± 1.08 5 a3.11 ± 0.20 5 b2.63 ± 0.56 3 b
17Alkene4.343Styrene 2.54 ± 0.53 5 b15.81 ± 0.57 3 a
18Alkene5.165(2E,4E,6E)-octa-2,4,6-triene 3.69 ± 0.70 5
19Alkene5.229(1R)-( + )-α-piene8.79 ± 0.20 4 d13.00 ± 0.44 4 cd21.48 ± 0.78 5 b16.67 ± 2.20 5 bc38.70 ± 4.63 4 a21.82 ± 1.90 5 b 2.64 ± 0.37 3 e
20Alkene6.523-butan-2-ylcyclohexene4.64 ± 0.14 4 a 2.03 ± 0.19 4 b1.78 ± 0.09 4 c
21Alkene7.47D-Limonene 18.75 ± 2.94 5
22Alkene7.4934-methylene-1-(1-methylethyl)bicyclo [3.1.0]hexane 1.55 ± 0.15 5 b3.54 ± 0.63 5 a
23Alkene10.7881-ethenyl-4-methoxybenzene 0.66 ± 0.15 4 b 1.63 ± 0.22 5 b3.21 ± 0.49 5 a
24Alkene17.935(4Z)-4,11,11-trimethyl-8-methylidenebicyclo [7.2.0]undec-4-ene 1.71 ± 0.25 4
25Alkene20.127β-Bisabolene 4.72 ± 1.10 5 a1.10 ± 0.30 4 c3.18 ± 0.36 4 b
26Alcohol4.4782-Heptanol14.16 ± 1.33 3 a13.93 ± 2.01 4 a0.71 ± 0.11 3 b
27Alcohol6.2071-Octen-3-ol 2.76 ± 0.25 5
28Alcohol6.6073-Octanol2.89 ± 0.67 5 b8.32 ± 1.26 5 a
29Alcohol8.1962-propylheptanol7.75 ± 0.39 3 c7.29 ± 0.63 5 c4.15 ± 0.28 5 cd 16.79 ± 2.61 5 b22.76 ± 3.94 5 a2.21 ± 0.17 5 cd2.60 ± 0.55 5 cd
30Alcohol9.322-Pentadecanol 3.00 ± 0.36 4
31Alcohol9.347Linalool 1.70 ± 0.27 5
32Alcohol10.805cis-3-nonenol 3.63 ± 0.75 5
33Aldehyde5.776Benzaldehyde 5.48 ± 3.27 5
34Aldehyde9.185(E)-non-4-enal 234.59 ± 102.11 5
35Aldehyde9.444Nonanal1.49 ± 0.53 5 b2.87 ± 0.81 4 a
36Aldehyde12.232Decanal3.53 ± 0.05 4 c19.01 ± 3.92 4 a7.01 ± 0.86 5 bc2.49 ± 0.18 5 c12.66 ± 2.66 5 b 7.06 ± 0.90 4 bcd3.11 ± 0.32 5 c 12.29 ± 0.73 5 b
37Ester4.052Isoamyl acetate 4.72 ± 0.99 4 a2.73 ± 0.34 4 b0.87 ± 0.11 4 c
38Ester4.967Methyl hexanoate3.00 ± 0.58 5 d3.41 ± 0.42 5 cd1.73 ± 0.34 5 d1.23 ± 0.18 5 d6.14 ± 1.32 5 b11.95 ± 1.65 4 a1.53 ± 0.27 5 d1.38 ± 0.13 4 d
39Ester6.636Butanoic acid, butyl ester3.14 ± 0.40 4 d4.13 ± 0.47 5 cd3.03 ± 0.15 4 d10.30 ± 1.19 5 b10.44 ± 1.42 4 b15.10 ± 1.51 5 a
40Ester9.175Benzoic acid, methyl ester 1.75 ± 0.27 5
41Ester11.275Ethyl benzoate 2.41 ± 0.18 5
42Ester16.075Malonic acid, bis(2-trimethylsilylethyl ester2.26 ± 0.24 5 c3.41 ± 0.32 5 b1.28 ± 0.16 4 c2.01 ± 0.33 4 c5.11 ± 0.56 5 a4.06 ± 0.46 5 b
43Ester30.474Ethyl palmitate 2.50 ± 0.30 5
44Ketone4.2912-Heptanone2.11 ± 0.31 5 b3.29 ± 0.48 5 bc1.60 ± 0.18 4 c7.29 ± 0.77 5 a 7.89 ± 1.09 5 a
45Ketone5.3032-ethyl-Cyclopentanone5.01 ± 1.13 5 cd2.78 ± 0.17 3 d6.14 ± 0.95 5 c3.31 ± 0.31 4 cd14.99 ± 0.71 3 a 4.93 ± 0.60 5 cd2.89 ± 0.07 5 d3.76 ± 0.86 4 c9.83 ± 1.04 4 b
46Ketone6.1921-Octen-3-one 4.24 ± 0.37 5
47Ketone6.3793-Octanone3.56 ± 0.22 4 cd6.89 ± 0.59 5 c 4.02 ± 0.5 5 cd15.04 ± 1.57 5 a10.29 ± 1.05 5 b1.73 ± 0.19 5 d2.4 ± 0.58 5 d
48Ketone6.4633-methyl-2-Heptanone4.12 ± 0.74 4 a3.79 ± 0.48 5 a0.78 ± 0.01 3 b
49Ketone9.0962-Nonanone4.01 ± 0.24 5 e6.40 ± 0.58 5 d4.16 ± 0.75 5 e10.72 ± 0.77 5 c15.13 ± 1.24 4 a13.43 ± 0.41 5 b
50Aromatic4.379m-Xylene6.69 ± 0.775 c10.53 ± 0.775 b7.30 ± 0.735 c3.97 ± 0.375 de 12.77 ± 1.435 a2.10 ± 0.544 e2.70 ± 0.484 de
51Aromatic4.833Anisole 8.32 ± 1.04 5 b15.93 ± 1.81 5 b81.49 ± 16.76 5 a13.83 ± 0.77 4 b
52Aromatic7.0171,3-Dichlorobenzene3.11 ± 1.20 5 d4.20 ± 1.09 5 d12.55 ± 1.05 4 b6.19 ± 1.62 3 cd 66.86 ± 3.15 4 a2.2 ± 0.62 5 de2.89 ± 0.99 5 de10.86 ± 1.07 3 bc11.95 ± 2.71 3 bc
53Aromatic7.984m-Diethylbenzene3.88 ± 0.15 5 b4.53 ± 0.72 5 b3.61 ± 0.59 5 b7.86 ± 0.40 5 a 8.89 ± 1.22 4 a
54Aromatic8.1431,4-Diethylbenzene7.04 ± 0.915 d10.05 ± 0.965 c10.90 ± 1.455 bc4.07 ± 0.395 de24.90 ± 1.754 a14.83 ± 3.404 b2.09 ± 0.505 de2.99 ± 0.424 de
55Aromatic9.7241-ethyl-4-Methoxybenzene4.54 ± 0.955 cd4.83 ± 0.885 cd5.23 ± 1.355 cd2.52 ± 0.65 d5.74 ± 2.765 c11.62 ± 4.714 b2 ± 0.273 d 12.75 ± 2.205 a
56Aromatic20.223Butylated Hydroxytoluene1.53 ± 0.272 b5.25 ± 0.484 a4.28 ± 0.954 a0.55 ± 0.112 b
57Others 2-Amino-m-cresol, N,O-bis(trimethylsilyl)-2.71 ± 0.214 b2.56 ± 0.395 b2.49 ± 0.145 b2.54 ± 0.075 b5.00 ± 1.005 a4.94 ± 0.514 a
Ⅰ MIM: mock-inoculated maize ears; MDM: mechanically damaged maize ears; POM: P. oxalicum-infected maize ears; TAM: T. asperellum-infected maize ears; APM: A. phoenicis-infected maize ears; AFM: A. flavus-infected maize ears; PPO: P. oxalicum growing in PDA medium; PTA: T. asperellum growing in PDA medium; PAP: A. phoenicis growing in PDA medium; PAF: A. flavus growing in PDA medium. Ⅱ Compounds are confirmed by the comparison of mass spectrum and retention time with the NIST Standard Reference Database (Shimadzu Co., Japan). Ⅲ Relative quantities are quantified by their ion abundance relative to that of the internal standard. Values are mean ± SE (n = 2~5). Values followed by different superscript numbers mean identification times in the same treatment. Different letters within the same row indicate significant differences among treatments (p < 0.05).
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Chen, Y.; Han, J.; Yang, H.; Qin, X.; Guo, H.; Du, Y. Different Maize Ear Rot Fungi Deter the Oviposition of Yellow Peach Moth (Conogethes punctiferalis (Guenée)) by Maize Volatile Organic Compounds. Agronomy 2023, 13, 251. https://doi.org/10.3390/agronomy13010251

AMA Style

Chen Y, Han J, Yang H, Qin X, Guo H, Du Y. Different Maize Ear Rot Fungi Deter the Oviposition of Yellow Peach Moth (Conogethes punctiferalis (Guenée)) by Maize Volatile Organic Compounds. Agronomy. 2023; 13(1):251. https://doi.org/10.3390/agronomy13010251

Chicago/Turabian Style

Chen, Yinhu, Jie Han, Haiqing Yang, Xiaochun Qin, Honggang Guo, and Yanli Du. 2023. "Different Maize Ear Rot Fungi Deter the Oviposition of Yellow Peach Moth (Conogethes punctiferalis (Guenée)) by Maize Volatile Organic Compounds" Agronomy 13, no. 1: 251. https://doi.org/10.3390/agronomy13010251

APA Style

Chen, Y., Han, J., Yang, H., Qin, X., Guo, H., & Du, Y. (2023). Different Maize Ear Rot Fungi Deter the Oviposition of Yellow Peach Moth (Conogethes punctiferalis (Guenée)) by Maize Volatile Organic Compounds. Agronomy, 13(1), 251. https://doi.org/10.3390/agronomy13010251

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