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Plant-Insect Interactions 2022

A special issue of International Journal of Molecular Sciences (ISSN 1422-0067). This special issue belongs to the section "Molecular Plant Sciences".

Deadline for manuscript submissions: closed (30 January 2023) | Viewed by 41460

Special Issue Editors


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Guest Editor
Department of Life Sciences and Systems Biology, University of Turin, Via Quarello 15/a, 10135 Turin, Italy
Interests: astrobiology; plant interactions with the surrounding environment; plant–insect interactions; plant responses to varying magnetic fields; metabolomics and transcriptomics of secondary plant metabolites and related genes
Special Issues, Collections and Topics in MDPI journals

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Guest Editor
Department of Life Sciences and Systems Biology, University of Turin, Via Accademia Albertina, 13-1023 Turin, Italy
Interests: plant–insect interactions; coevolution; eusociality; communication; butterflies; ants
Special Issues, Collections and Topics in MDPI journals

Special Issue Information

Dear Colleagues,

Plant–insect interactions is a fast-developing research-field that continues to increase the interest of many scientists, many of whom come from heterogeneous backgrounds. This variety reflects the complexity and the multifaceted associations from which plants and insect interactions may originate.

Mutualism, pollination, and biotrophy boost the co-evolution of plant defenses against various insect feeding strategies and the ability of insects to detoxify plant chemical defenses or to react specifically to plant compounds. The success of plants to withstand insect herbivory depends on their ability to quickly recognize and decipher the incoming signal and their ability to adequately respond to a wide array of attacking herbivores. Whilst this topic has been widely investigated, less attention has been paid to how insects use plant signals for their own advantage to detect high-quality food, to choose where to lay their eggs, or to find their prey.

Current research on plant–insect interaction has mainly focused on genomics and proteomics, which are late events induced by biotic stress. Early events, within the first seconds to minutes, are responsible for the recognition and triggering of the signal transduction pathways, preceding both genomic and proteomic responses. For both plants and insects, sensing and communication are key features that can improve fitness and that can grant survival in contrasting environments.

This Special Issue on “Plant–Insect Interactions” is open to all researchers studying this interaction at any level, from both the plant and the insect sides. Original research articles as well as review papers dealing with advancements and our current understanding of various aspects of plant–insect interactions are welcome.

Prof. Dr. Massimo Maffei
Dr. Francesca Barbero
Guest Editors

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Keywords

  • early and late plant responses to insects
  • plant immunity
  • direct and indirect defense
  • effects of insect herbivory
  • wounding or egg-laying on plants
  • systemic signaling and pathways
  • signal transduction
  • gene expression
  • metabolomics of plant‐insect interaction
  • plant-insect co-evolution
  • plant-insect sensing and communication
  • signaling in multitrophic interactions (oviposition and parasitoid strategies)
  • sequestration and use of plant natural products by insects

Published Papers (20 papers)

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20 pages, 4344 KiB  
Article
Transcriptome and Metabolome Profiling Reveal the Resistance Mechanisms of Rice against Brown Planthopper
by Qian Zhang, Tianzhu Li, Mingyang Gao, Meng Ye, Manxia Lin, Di Wu, Jianping Guo, Wei Guan, Jing Wang, Ke Yang, Lili Zhu, Yichen Cheng, Bo Du and Guangcun He
Int. J. Mol. Sci. 2022, 23(8), 4083; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms23084083 - 07 Apr 2022
Cited by 16 | Viewed by 3303
Abstract
Brown planthopper (Nilaparvata lugens Stål, BPH) is one of the most destructive insects affecting rice production. To better understand the physiological mechanisms of how rice responds to BPH feeding, we analyzed BPH-induced transcriptomic and metabolic changes in leaf sheaths of both [...] Read more.
Brown planthopper (Nilaparvata lugens Stål, BPH) is one of the most destructive insects affecting rice production. To better understand the physiological mechanisms of how rice responds to BPH feeding, we analyzed BPH-induced transcriptomic and metabolic changes in leaf sheaths of both BPH-susceptible and -resistant rice varieties. Our results demonstrated that the resistant rice reduced the settling, feeding and growth of BPH. Metabolic analyses indicated that BPH infestation caused more drastic overall metabolic changes in the susceptible variety than the resistant rice. Differently accumulated metabolites (DAMs) belonging to flavonoids were downregulated in the susceptible rice but upregulated in resistant variety. Transcriptomic analyses revealed more differentially expressed genes (DEGs) in susceptible rice than resistant rice, and DEGs related to stimulus were significantly upregulated in resistant rice but downregulated in susceptible rice. Combined analyses of transcriptome and metabolome showed that many DEGs and DAMs were enriched in phenylpropane biosynthesis, flavonoid biosynthesis, and plant hormone signal transduction. We conducted correlation analyses of DEGs and DAMs in these pathways and found a high correlation between DEGs and DAMs. Then, we found that the contents of endogenous indole 3-acetic acid (IAA) in resistant rice was lower than that of susceptible rice after BPH feeding, while the salicylic acid (SA) content was the opposite. For functional analysis, an exogenous application of IAA decreased rice resistance to BPH, but the exogenous application of SA increased resistance. In addition, biochemical assessment and quantitative PCR analysis showed that the lignin content of resistant accession was constitutively higher than in susceptible accession. By adding epigallocatechin, the substrate of anthocyanidin reductase (ANR), to the artificial diet decreased the performance of BPH. We first combined a transcriptome-metabolome-wide association study (TMWAS) on rice resistance to BPH in this study. We demonstrated that rice promoted resistance to BPH by inducing epigallocatechin and decreasing IAA. These findings provided useful transcriptomic and metabolic information for understanding the rice-BPH interactions. Full article
(This article belongs to the Special Issue Plant-Insect Interactions 2022)
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19 pages, 5249 KiB  
Article
Volatile Dimethyl Disulfide from Guava Plants Regulate Developmental Performance of Asian Citrus Psyllid through Activation of Defense Responses in Neighboring Orange Plants
by Siquan Ling, Hualong Qiu, Jinzhu Xu, Yanping Gu, Jinxin Yu, Wei Wang, Jiali Liu and Xinnian Zeng
Int. J. Mol. Sci. 2022, 23(18), 10271; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms231810271 - 07 Sep 2022
Cited by 4 | Viewed by 1742
Abstract
Intercropping with guava (Psidium guajava L.) can assist with the management of Asian citrus psyllid (ACP, Diaphorina citri Kuwayama), the insect vector of the huanglongbing pathogen, in citrus orchards. Sulfur volatiles have a repellent activity and physiological effects, as well as being [...] Read more.
Intercropping with guava (Psidium guajava L.) can assist with the management of Asian citrus psyllid (ACP, Diaphorina citri Kuwayama), the insect vector of the huanglongbing pathogen, in citrus orchards. Sulfur volatiles have a repellent activity and physiological effects, as well as being important components of guava volatiles. In this study, we tested whether the sulfur volatiles emitted by guava plants play a role in plant–plant communications and trigger anti-herbivore activities against ACP in sweet orange plants (Citrus sinensis L. Osbeck). Real-time determination using a proton-transfer-reaction mass spectrometer (PTR-MS) showed that guava plants continuously release methanethiol, dimethyl sulfide (DMS), and dimethyl disulfide (DMDS), and the contents increased rapidly after mechanical damage. The exposure of orange plants to DMDS resulted in the suppression of the developmental performance of ACP. The differential elevation of salicylic acid (SA) levels; the expression of phenylalanine ammonia lyase (PAL), salicylate-O-methyl transferase (SMT), and pathogenesis-related (PR1) genes; the activities of defense-related enzymes PAL, polyphenol oxidase (PPO), and peroxidase (POD); and the total polyphenol content were observed in DMDS-exposed orange plants. The emission of volatiles including myrcene, nonanal, decanal, and methyl salicylate (MeSA) was increased. In addition, phenylpropanoid and flavonoid biosynthesis, and aromatic amino acid (such as phenylalanine, tyrosine, and tryptophan) metabolic pathways were induced. Altogether, our results indicated that DMDS from guava plants can activate defense responses in eavesdropping orange plants and boost their herbivore resistance to ACP, which suggests the possibility of using DMDS as a novel approach for the management of ACP in citrus orchards. Full article
(This article belongs to the Special Issue Plant-Insect Interactions 2022)
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17 pages, 3087 KiB  
Article
Cajanus platycarpus Flavonoid 3′5′ Hydroxylase_2 (CpF3′5′H_2) Confers Resistance to Helicoverpa armigera by Modulating Total Polyphenols and Flavonoids in Transgenic Tobacco
by Shaily Tyagi, Maniraj Rathinam, Narasimham Dokka, Nidhee Chaudhary, Lakkakula Satish, Prasanta K. Dash, Ajit Kumar Shasany and Rohini Sreevathsa
Int. J. Mol. Sci. 2023, 24(2), 1755; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms24021755 - 16 Jan 2023
Cited by 4 | Viewed by 1604
Abstract
Pod borer Helicoverpa armigera, a polyphagus herbivorous pest, tremendously incurs crop damage in economically important crops. This necessitates the identification and utility of novel genes for the control of the herbivore. The present study deals with the characterization of a flavonoid 3′5′ [...] Read more.
Pod borer Helicoverpa armigera, a polyphagus herbivorous pest, tremendously incurs crop damage in economically important crops. This necessitates the identification and utility of novel genes for the control of the herbivore. The present study deals with the characterization of a flavonoid 3′5′ hydroxylase_2 (F3′5′H_2) from a pigeonpea wild relative Cajanus platycarpus, possessing a robust chemical resistance response to H. armigera. Though F3′5′H_2 displayed a dynamic expression pattern in both C. platycarpus (Cp) and the cultivated pigeonpea, Cajanus cajan (Cc) during continued herbivory, CpF3′5′H_2 showed a 4.6-fold increase vis a vis 3-fold in CcF3′5′H_2. Despite similar gene copy numbers in the two Cajanus spp., interesting genic and promoter sequence changes highlighted the stress responsiveness of CpF3′5′H_2. The relevance of CpF3′5′H_2 in H. armigera resistance was further validated in CpF3′5′H_2-overexpressed transgenic tobacco based on reduced leaf damage and increased larval mortality through an in vitro bioassay. As exciting maiden clues, CpF3′5′H_2 deterred herbivory in transgenic tobacco by increasing total flavonoids, polyphenols and reactive oxygen species (ROS) scavenging capacity. To the best of our knowledge, this is a maiden attempt ascertaining the role of F3′5′H_2 gene in the management of H. armigera. These interesting leads suggest the potential of this pivotal branch-point gene in biotic stress management programs. Full article
(This article belongs to the Special Issue Plant-Insect Interactions 2022)
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23 pages, 2677 KiB  
Article
Genomic Assessment of the Contribution of the Wolbachia Endosymbiont of Eurosta solidaginis to Gall Induction
by Natalie Fiutek, Matthew B. Couger, Stacy Pirro, Scott W. Roy, José R. de la Torre and Edward F. Connor
Int. J. Mol. Sci. 2023, 24(11), 9613; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms24119613 - 01 Jun 2023
Cited by 3 | Viewed by 1294
Abstract
We explored the genome of the Wolbachia strain, wEsol, symbiotic with the plant-gall-inducing fly Eurosta solidaginis with the goal of determining if wEsol contributes to gall induction by its insect host. Gall induction by insects has been hypothesized to involve the [...] Read more.
We explored the genome of the Wolbachia strain, wEsol, symbiotic with the plant-gall-inducing fly Eurosta solidaginis with the goal of determining if wEsol contributes to gall induction by its insect host. Gall induction by insects has been hypothesized to involve the secretion of the phytohormones cytokinin and auxin and/or proteinaceous effectors to stimulate cell division and growth in the host plant. We sequenced the metagenome of E. solidaginis and wEsol and assembled and annotated the genome of wEsol. The wEsol genome has an assembled length of 1.66 Mbp and contains 1878 protein-coding genes. The wEsol genome is replete with proteins encoded by mobile genetic elements and shows evidence of seven different prophages. We also detected evidence of multiple small insertions of wEsol genes into the genome of the host insect. Our characterization of the genome of wEsol indicates that it is compromised in the synthesis of dimethylallyl pyrophosphate (DMAPP) and S-adenosyl L-methionine (SAM), which are precursors required for the synthesis of cytokinins and methylthiolated cytokinins. wEsol is also incapable of synthesizing tryptophan, and its genome contains no enzymes in any of the known pathways for the synthesis of indole-3-acetic acid (IAA) from tryptophan. wEsol must steal DMAPP and L-methionine from its host and therefore is unlikely to provide cytokinin and auxin to its insect host for use in gall induction. Furthermore, in spite of its large repertoire of predicted Type IV secreted effector proteins, these effectors are more likely to contribute to the acquisition of nutrients and the manipulation of the host’s cellular environment to contribute to growth and reproduction of wEsol than to aid E. solidaginis in manipulating its host plant. Combined with earlier work that shows that wEsol is absent from the salivary glands of E. solidaginis, our results suggest that wEsol does not contribute to gall induction by its host. Full article
(This article belongs to the Special Issue Plant-Insect Interactions 2022)
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14 pages, 2508 KiB  
Article
Oligogalacturonides Enhance Resistance against Aphids through Pattern-Triggered Immunity and Activation of Salicylic Acid Signaling
by Christian Silva-Sanzana, Diego Zavala, Felipe Moraga, Ariel Herrera-Vásquez and Francisca Blanco-Herrera
Int. J. Mol. Sci. 2022, 23(17), 9753; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms23179753 - 28 Aug 2022
Cited by 5 | Viewed by 1956
Abstract
The remarkable capacity of the generalist aphid Myzus persicae to resist most classes of pesticides, along with the environmental and human health risks associated with these agrochemicals, has necessitated the development of safer and greener solutions to control this agricultural pest. Oligogalacturonides (OGs) [...] Read more.
The remarkable capacity of the generalist aphid Myzus persicae to resist most classes of pesticides, along with the environmental and human health risks associated with these agrochemicals, has necessitated the development of safer and greener solutions to control this agricultural pest. Oligogalacturonides (OGs) are pectin-derived molecules that can be isolated from fruit industry waste. OGs have been shown to efficiently stimulate plant defenses against pathogens such as Pseudomonas syringae and Botrytis cinerea. However, whether OGs confer resistance against phytophagous insects such as aphids remains unknown. Here, we treated Arabidopsis plants with OGs and recorded their effects on the feeding performance and population of M. persicae aphids. We also identified the defense mechanism triggered by OGs in plants through the analysis of gene expression and histological approaches. We found that OG treatments increased their resistance to M. persicae infestation by reducing the offspring number and feeding performance. Furthermore, this enhanced resistance was related to a substantial accumulation of callose and reactive oxygen species and activation of the salicylic acid signaling pathway. Full article
(This article belongs to the Special Issue Plant-Insect Interactions 2022)
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12 pages, 6921 KiB  
Article
The Sequence Characteristics and Binding Properties of the Odorant-Binding Protein 2 of Euplatypus parallelus to Semiochemicals
by Guangchao Cui, Xiang Zhou, Qian Wang, Kai Zhang, Lei Qin and Jixing Guo
Int. J. Mol. Sci. 2023, 24(2), 1714; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms24021714 - 15 Jan 2023
Cited by 4 | Viewed by 1199
Abstract
Euplatypus parallelus is one of the dominant rubber bark beetle species in Hainan’s rubber-planting area. Semiochemicals, including the volatiles found in rubber trees and aggregation pheromones, play an important role in the search for suitable host plants. To examine the possible functional role [...] Read more.
Euplatypus parallelus is one of the dominant rubber bark beetle species in Hainan’s rubber-planting area. Semiochemicals, including the volatiles found in rubber trees and aggregation pheromones, play an important role in the search for suitable host plants. To examine the possible functional role of highly expressed odorant-binding protein 2 of Euplatypus parallelus (EparOBP2) in the semiochemical recognition process, we cloned and analyzed the cDNA sequence of EparOBP2. The results showed that EparOBP2 contains an open reading frame (ORF) of 393 bp that encodes 130 amino acids, including a 21-amino-acid residue signal peptide at the N-terminus. The matured EparOBP2 protein consists of seven α-helices, creating an open binding pocket and three disulfide bridges. The results of the fluorescence binding assay showed that EparOBP2 had high binding ability with α-pinene and myrcene. The docking results confirmed that the interactions of α-pinene and myrcene with EparOBP2 were primarily achieved through hydrophobic interactions. This study provides evidence that EparOBP2 may be involved in the chemoreception of semiochemicals and that it can successfully contribute to the integrated management of E. parallelus. Full article
(This article belongs to the Special Issue Plant-Insect Interactions 2022)
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11 pages, 2227 KiB  
Article
JUL1, Ring-Type E3 Ubiquitin Ligase, Is Involved in Transcriptional Reprogramming for ERF15-Mediated Gene Regulation
by Junna Kawaguchi, Kaito Hayashi, Yoshitake Desaki, Abdelaziz Ramadan, Akira Nozawa, Keiichirou Nemoto, Tatsuya Sawasaki and Gen-ichiro Arimura
Int. J. Mol. Sci. 2023, 24(2), 987; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms24020987 - 04 Jan 2023
Cited by 1 | Viewed by 2026
Abstract
JAV1-associated ubiquitin ligase 1 (JUL1) is a RING-type E3 ubiquitin ligase that catalyzes ubiquitination of JAV1, a jasmonate signaling repressor, in Arabidopsis thaliana in response to herbivore attack. Here we present a new insight into the nature of JUL1 as a multi-targeting enzyme [...] Read more.
JAV1-associated ubiquitin ligase 1 (JUL1) is a RING-type E3 ubiquitin ligase that catalyzes ubiquitination of JAV1, a jasmonate signaling repressor, in Arabidopsis thaliana in response to herbivore attack. Here we present a new insight into the nature of JUL1 as a multi-targeting enzyme for not only JAV1 but also transcription factors (TFs) screened using in vitro and in vivo protein interaction assays. Reporter assays using protoplasts showed that the JUL1-interacting TFs (JiTFs), including ERF15, bZIP53 and ORA59, were involved in transcriptional activation of jasmonate-responsive PDF1.2 and abscisic acid-responsive GEA6. Likewise, assays using mutant plants suggested that the 3 JiTFs were indeed responsible for transcriptional regulation of PDF1.2 and/or GEA6, and ERF15 and ORA59 were substantially responsible for the anti-herbivore trait. In vitro protein ubiqutination assays showed that JUL1 catalyzed ubiqutination of JAV1 but not any of the TFs. This was in accord with the finding that JUL1 abolished JAV1′s interference with ERF15 function, according to the reporter assay. Moreover, of great interest is our finding that ERF15 but not bZIP53 or ORA59 serves as a scaffold for the JAV1/JUL1 system, indicating that there is narrow selectivity of the transcriptional reprogramming by the JAV1/JUL1 system. Full article
(This article belongs to the Special Issue Plant-Insect Interactions 2022)
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17 pages, 2725 KiB  
Article
Linalool Activates Oxidative and Calcium Burst and CAM3-ACA8 Participates in Calcium Recovery in Arabidopsis Leaves
by Chunyang Jiao, Junqing Gong, Zhujuan Guo, Shuwen Li, Yixin Zuo and Yingbai Shen
Int. J. Mol. Sci. 2022, 23(10), 5357; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms23105357 - 11 May 2022
Cited by 8 | Viewed by 1879
Abstract
Plants produce linalool to respond to biotic stress, but the linalool-induced early signal remains unclear. In wild-type Arabidopsis, plant resistance to diamondback moth (Plutella xylostella) increased more strongly in a linalool-treated group than in an untreated control group. H2O [...] Read more.
Plants produce linalool to respond to biotic stress, but the linalool-induced early signal remains unclear. In wild-type Arabidopsis, plant resistance to diamondback moth (Plutella xylostella) increased more strongly in a linalool-treated group than in an untreated control group. H2O2 and Ca2+, two important early signals that participated in biotic stress, burst after being treated with linalool in Arabidopsis mesophyll cells. Linalool treatment increased H2O2 and intracellular calcium concentrations in mesophyll cells, observed using a confocal microscope with laser scanning, and H2O2 signaling functions upstream of Ca2+ signaling by using inhibitors and mutants. Ca2+ efflux was detected using non-invasive micro-test technology (NMT), and Ca2+ efflux was also inhibited by NADPH oxidase inhibitor DPI (diphenyleneiodonium chloride) and in cells of the NADPH oxidase mutant rbohd. To restore intracellular calcium levels, Ca2+-ATPase was activated, and calmodulin 3 (CAM3) participated in Ca2+-ATPase activation. This result is consistent with the interaction between CAM7 and Ca2+-ATPase isoform 8 (ACA8). In addition, a yeast two-hybrid assay, firefly luciferase complementation imaging assay, and an in vitro pulldown assay showed that CAM3 interacts with the N-terminus of ACA8, and qRT-PCR showed that some JA-related genes and defense genes expressions were enhanced when treated with linalool in Arabidopsis leaves. This study reveals that linalool enhances H2O2 and intracellular calcium concentrations in Arabidopsis mesophyll cells; CAM3-ACA8 reduces intracellular calcium concentrations, allowing cells to resume their resting state. Additionally, JA-related genes and defense genes’ expression may enhance plants’ defense when treated with linalool. Full article
(This article belongs to the Special Issue Plant-Insect Interactions 2022)
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15 pages, 12170 KiB  
Article
Pollen Molecular Identification from a Long-Distance Migratory Insect, Spodoptera exigua, as Evidenced for Its Regional Pollination in Eastern Asia
by Huiru Jia, Tengli Wang, Xiaokang Li, Shengyuan Zhao, Jianglong Guo, Dazhong Liu, Yongqiang Liu and Kongming Wu
Int. J. Mol. Sci. 2023, 24(8), 7588; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms24087588 - 20 Apr 2023
Cited by 2 | Viewed by 1299
Abstract
Understanding plant-insect interactions requires the uncovering of the host plant use of insect herbivores, but such information is scarce for most taxa, including nocturnal moth species, despite their vital role as herbivores and pollinators. In this study, we determined the plant species visited [...] Read more.
Understanding plant-insect interactions requires the uncovering of the host plant use of insect herbivores, but such information is scarce for most taxa, including nocturnal moth species, despite their vital role as herbivores and pollinators. In this study, we determined the plant species visited by an important moth species, Spodoptera exigua, by analyzing attached pollen on migratory individuals in Northeast China. Pollen grains were dislodged from 2334 S. exigua long-distance migrants captured between 2019 and 2021 on a small island in the center of the Bohai Strait, which serves as a seasonal migration pathway for this pest species, and 16.1% of the tested moths exhibited pollen contamination, primarily on the proboscis. Subsequently, 33 taxa from at least 23 plant families and 29 genera were identified using a combination of DNA barcoding and pollen morphology, primarily from the Angiosperm, Dicotyledoneae. Moreover, the sex, inter-annual, and seasonal differences in pollen adherence ratio and pollen taxa were revealed. Notably, compared to previously reported pollen types found on several other nocturnal moths, we found that almost all of the above 33 pollen taxa can be found in multiple nocturnal moth species, providing another important example of conspecific attraction. Additionally, we also discussed the indicative significance of the pollen present on the bodies of migratory individuals for determining their migratory route. Overall, by delineating the adult feeding and pollination behavior of S. exigua, we advanced our understanding of the interactions of the moths with their host plants, and its migration pattern, as well as facilitated the design of (area-wide) management strategies to preserve and optimize ecosystem services that they provide. Full article
(This article belongs to the Special Issue Plant-Insect Interactions 2022)
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30 pages, 12791 KiB  
Article
Heritable Epigenomic Modifications Influence Stress Resilience and Rapid Adaptations in the Brown Planthopper (Nilaparvata lugens)
by Ayushi Gupta and Suresh Nair
Int. J. Mol. Sci. 2022, 23(15), 8728; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms23158728 - 05 Aug 2022
Cited by 6 | Viewed by 2523
Abstract
DNA methylation in insects is integral to cellular differentiation, development, gene regulation, genome integrity, and phenotypic plasticity. However, its evolutionary potential and involvement in facilitating rapid adaptations in insects are enigmatic. Moreover, our understanding of these mechanisms is limited to a few insect [...] Read more.
DNA methylation in insects is integral to cellular differentiation, development, gene regulation, genome integrity, and phenotypic plasticity. However, its evolutionary potential and involvement in facilitating rapid adaptations in insects are enigmatic. Moreover, our understanding of these mechanisms is limited to a few insect species, of which none are pests of crops. Hence, we studied methylation patterns in the brown planthopper (BPH), a major rice pest, under pesticide and nutritional stress, across its life stages. Moreover, as the inheritance of epigenetic changes is fundamentally essential for acclimation, adaptability, and evolution, we determined the heritability and persistence of stress-induced methylation marks in BPH across generations. Our results revealed that DNA methylation pattern(s) in BPH varies/vary with environmental cues and is/are insect life-stage specific. Further, our findings provide novel insights into the heritability of stress-induced methylation marks in BPH. However, it was observed that, though heritable, these marks eventually fade in the absence of the stressors, thereby suggesting the existence of fitness cost(s) associated with the maintenance of the stressed epigenotype. Furthermore, we demonstrate how 5-azacytidine-mediated disruption of BPH methylome influences expression levels of stress-responsive genes and, thereby, highlight demethylation/methylation as a phenomenon underlying stress resilience of BPH. Full article
(This article belongs to the Special Issue Plant-Insect Interactions 2022)
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18 pages, 4571 KiB  
Article
PxTret1-like Affects the Temperature Adaptability of a Cosmopolitan Pest by Altering Trehalose Tissue Distribution
by Huiling Zhou, Gaoke Lei, Yanting Chen, Minsheng You and Shijun You
Int. J. Mol. Sci. 2022, 23(16), 9019; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms23169019 - 12 Aug 2022
Cited by 12 | Viewed by 1577
Abstract
Global warming poses new challenges for insects to adapt to higher temperatures. Trehalose is the main blood sugar in insects and plays an important role in energy metabolism and stress resistance. The transmembrane transport of trehalose mainly depends on the trehalose transporter (TRET1). [...] Read more.
Global warming poses new challenges for insects to adapt to higher temperatures. Trehalose is the main blood sugar in insects and plays an important role in energy metabolism and stress resistance. The transmembrane transport of trehalose mainly depends on the trehalose transporter (TRET1). Plutella xylostella (L.) is a worldwide agricultural pest; however, the effects of the trehalose transport mechanism and trehalose distribution in tissues on the development, reproduction and temperature adaptation of P. xylostella have yet to be reported. In this study, PxTret1-like was cloned and analyzed regarding its expression pattern. It was found that the expression of PxTret1-like was affected by ambient temperature. The knockout mutation of PxTret1-like was generated using a CRISPR/Cas9 system by targeted knockout. The trehalose content and trehalase activity of mutant P. xylostella increased at different developmental stages. The trehalose content increased in the fat body of the fourth-instar P. xylostella, and decreased in the hemolymph, and there was no significant change in glucose in the fat body and hemolymph. Mutant strains of P. xylostella showed a significantly reduced survival rate, fecundity and ability to withstand extreme temperatures. The results showed that PxTret1-like could affect the development, reproduction and temperature adaptability of P. xylostella by regulating the trehalose content in the fat body and hemolymph. Full article
(This article belongs to the Special Issue Plant-Insect Interactions 2022)
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19 pages, 1735 KiB  
Review
Plant Responses to Herbivory, Wounding, and Infection
by Salma Mostafa, Yun Wang, Wen Zeng and Biao Jin
Int. J. Mol. Sci. 2022, 23(13), 7031; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms23137031 - 24 Jun 2022
Cited by 38 | Viewed by 6317
Abstract
Plants have various self-defense mechanisms against biotic attacks, involving both physical and chemical barriers. Physical barriers include spines, trichomes, and cuticle layers, whereas chemical barriers include secondary metabolites (SMs) and volatile organic compounds (VOCs). Complex interactions between plants and herbivores occur. Plant responses [...] Read more.
Plants have various self-defense mechanisms against biotic attacks, involving both physical and chemical barriers. Physical barriers include spines, trichomes, and cuticle layers, whereas chemical barriers include secondary metabolites (SMs) and volatile organic compounds (VOCs). Complex interactions between plants and herbivores occur. Plant responses to insect herbivory begin with the perception of physical stimuli, chemical compounds (orally secreted by insects and herbivore-induced VOCs) during feeding. Plant cell membranes then generate ion fluxes that create differences in plasma membrane potential (Vm), which provokes the initiation of signal transduction, the activation of various hormones (e.g., jasmonic acid, salicylic acid, and ethylene), and the release of VOCs and SMs. This review of recent studies of plant–herbivore–infection interactions focuses on early and late plant responses, including physical barriers, signal transduction, SM production as well as epigenetic regulation, and phytohormone responses. Full article
(This article belongs to the Special Issue Plant-Insect Interactions 2022)
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15 pages, 3100 KiB  
Article
Role of Acrostyle Cuticular Proteins in the Retention of an Aphid Salivary Effector
by Maëlle Deshoux, Baptiste Monsion, Elodie Pichon, Jaime Jiménez, Aránzazu Moreno, Bastien Cayrol, Gaël Thébaud, Sam T. Mugford, Saskia A. Hogenhout, Stéphane Blanc, Alberto Fereres and Marilyne Uzest
Int. J. Mol. Sci. 2022, 23(23), 15337; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms232315337 - 05 Dec 2022
Cited by 4 | Viewed by 1982
Abstract
To avoid the activation of plant defenses and ensure sustained feeding, aphids are assumed to use their mouthparts to deliver effectors into plant cells. A recent study has shown that effectors detected near feeding sites are differentially distributed in plant tissues. However, the [...] Read more.
To avoid the activation of plant defenses and ensure sustained feeding, aphids are assumed to use their mouthparts to deliver effectors into plant cells. A recent study has shown that effectors detected near feeding sites are differentially distributed in plant tissues. However, the precise process of effector delivery into specific plant compartments is unknown. The acrostyle, a cuticular organ located at the tip of maxillary stylets that transiently binds plant viruses via its stylin proteins, may participate in this specific delivery process. Here, we demonstrate that Mp10, a saliva effector released into the plant cytoplasm during aphid probing, binds to the acrostyles of Acyrthosiphon pisum and Myzus persicae. The effector probably interacts with Stylin-03 as a lowered Mp10-binding to the acrostyle was observed upon RNAi-mediated reduction in Stylin-03 production. In addition, Stylin-03 and Stylin-01 RNAi aphids exhibited changes in their feeding behavior as evidenced by electrical penetration graph experiments showing longer aphid probing behaviors associated with watery saliva release into the cytoplasm of plant cells. Taken together, these data demonstrate that the acrostyle also has effector binding capacity and supports its role in the delivery of aphid effectors into plant cells. Full article
(This article belongs to the Special Issue Plant-Insect Interactions 2022)
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18 pages, 6371 KiB  
Article
Induced Resistance Combined with RNA Interference Attenuates the Counteradaptation of the Western Flower Thrips
by Tao Zhang, Li Liu, Yulian Jia, Junrui Zhi, Wenbo Yue, Dingyin Li and Guang Zeng
Int. J. Mol. Sci. 2022, 23(18), 10886; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms231810886 - 17 Sep 2022
Cited by 6 | Viewed by 1547
Abstract
The western flower thrips, Frankliniella occidentalis Pergande, is an invasive pest that damages agricultural and horticultural crops. The induction of plant defenses and RNA interference (RNAi) technology are potent pest control strategies. This study investigated whether the anti-adaptive ability of F. occidentalis [...] Read more.
The western flower thrips, Frankliniella occidentalis Pergande, is an invasive pest that damages agricultural and horticultural crops. The induction of plant defenses and RNA interference (RNAi) technology are potent pest control strategies. This study investigated whether the anti-adaptive ability of F. occidentalis to jasmonic acid (JA)- and methyl jasmonate (MeJA)-induced defenses in kidney bean plants was attenuated after glutathione S-transferase (GST) gene knockdown. The expression of four GSTs in thrips fed JA- and MeJA-induced leaves was analyzed, and FoGSTd1 and FoGSTs1 were upregulated. Exogenous JA- and MeJA-induced defenses led to increases in defensive secondary metabolites (tannins, alkaloids, total phenols, flavonoids, and lignin) in leaves. Metabolome analysis indicated that the JA-induced treatment of leaves led to significant upregulation of defensive metabolites. The activity of GSTs increased in second-instar thrips larvae fed JA- and MeJA-induced leaves. Co-silencing with RNAi simultaneously knocked down FoGSTd1 and FoGSTs1 transcripts and GST activity, and the area damaged by second-instar larvae feeding on JA- and MeJA-induced leaves decreased by 62.22% and 55.24%, respectively. The pupation rate of second-instar larvae also decreased by 39.68% and 39.89%, respectively. Thus, RNAi downregulation of FoGSTd1 and FoGSTs1 reduced the anti-adaptive ability of F. occidentalis to JA- or MeJA-induced defenses in kidney bean plants. Full article
(This article belongs to the Special Issue Plant-Insect Interactions 2022)
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15 pages, 4513 KiB  
Article
Sogatella furcifera Saliva Mucin-like Protein Is Required for Feeding and Induces Rice Defences
by Yudi Liu, Jinyu Yi, Haokang Jia, Yutong Miao and Maolin Hou
Int. J. Mol. Sci. 2022, 23(15), 8239; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms23158239 - 26 Jul 2022
Cited by 3 | Viewed by 1390
Abstract
The white-backed planthopper (WBPH), Sogatella furcifera, is one of the most important piercing-sucking pests of rice (Oryza sativa) in Asia. Mucin-like salivary protein (SFMLP) is highly expressed in the salivary glands of WBPH, which plays an important role in WBPH [...] Read more.
The white-backed planthopper (WBPH), Sogatella furcifera, is one of the most important piercing-sucking pests of rice (Oryza sativa) in Asia. Mucin-like salivary protein (SFMLP) is highly expressed in the salivary glands of WBPH, which plays an important role in WBPH feeding. In this study, WBPH injected with dsSFMLP had difficulty in sucking phloem sap from rice plants, which significantly reduced their food intake, weight, and survival. In contrast, the knockdown of the SFMLP gene had only a marginal effect on the survival of WBPH fed an artificial diet. Further studies showed that silencing SFMLP resulted in the short and single-branched salivary sheaths secretion and less formation of salivary flanges in rice. These data suggest that SFMLP is involved in the formation of the salivary sheath and is essential for feeding in WBPH. Overexpression of the SFMLP gene in rice plants promoted the feeding of WBPH, whereas silencing the gene in rice plants significantly decreased WBPH performance. Additionally, it was found that overexpression of SFMLP in rice plants elicited the signalling pathway of SA (salicylic acid) while suppressing JA (jasmonic acid); in contrast, silencing of the SFMLP gene in rice plants showed the opposite results. This study clarified the function of SFMLP in WBPH feeding as well as mediating rice defences. Full article
(This article belongs to the Special Issue Plant-Insect Interactions 2022)
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25 pages, 4326 KiB  
Article
Assessment of the Molecular Responses of an Ancient Angiosperm against Atypical Insect Oviposition: The Case of Hass Avocados and the Tephritid Fly Anastrepha ludens
by Martín Aluja, Mirna Vázquez-Rosas-Landa, Daniel Cerqueda-García, Juan L. Monribot-Villanueva, Alma Altúzar-Molina, Mónica Ramírez-Vázquez, Olinda Velázquez-López, Greta Rosas-Saito, Alexandro G. Alonso-Sánchez, Rafael Ortega-Casas, Adrián José Enríquez-Valencia, José A. Guerrero-Analco and Enrique Ibarra-Laclette
Int. J. Mol. Sci. 2023, 24(3), 2060; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms24032060 - 20 Jan 2023
Cited by 2 | Viewed by 1842
Abstract
Anastrepha spp. (Diptera: Tephritidae) infestations cause significant economic losses in commercial fruit production worldwide. However, some plants quickly counteract the insertion of eggs by females by generating neoplasia and hindering eclosion, as is the case for Persea americana Mill., cv. Hass (Hass avocados). [...] Read more.
Anastrepha spp. (Diptera: Tephritidae) infestations cause significant economic losses in commercial fruit production worldwide. However, some plants quickly counteract the insertion of eggs by females by generating neoplasia and hindering eclosion, as is the case for Persea americana Mill., cv. Hass (Hass avocados). We followed a combined transcriptomics/metabolomics approach to identify the molecular mechanisms triggered by Hass avocados to detect and react to the oviposition of the pestiferous Anastrepha ludens (Loew). We evaluated two conditions: fruit damaged using a sterile pin (pin) and fruit oviposited by A. ludens females (ovi). We evaluated both of the conditions in a time course experiment covering five sampling points: without treatment (day 0), 20 min after the treatment (day 1), and days 3, 6, and 9 after the treatment. We identified 288 differentially expressed genes related to the treatments. Oviposition (and possibly bacteria on the eggs’ surface) induces a plant hypersensitive response (HR), triggering a chitin receptor, producing an oxidative burst, and synthesizing phytoalexins. We also observed a process of cell wall modification and polyphenols biosynthesis, which could lead to polymerization in the neoplastic tissue surrounding the eggs. Full article
(This article belongs to the Special Issue Plant-Insect Interactions 2022)
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11 pages, 1525 KiB  
Article
CALMODULIN1 and WRKY53 Function in Plant Defense by Negatively Regulating the Jasmonic Acid Biosynthesis Pathway in Arabidopsis
by Chunyang Jiao, Kaixiang Li, Yixin Zuo, Junqing Gong, Zhujuan Guo and Yingbai Shen
Int. J. Mol. Sci. 2022, 23(14), 7718; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms23147718 - 13 Jul 2022
Cited by 9 | Viewed by 1964
Abstract
Jasmonic acid (JA) is an important hormone that functions in plant defense. cam1 and wrky53 mutants were more resistant to Spodoptera littoralis than in the wild-type (WT) Arabidopsis group. In addition, JA concentration in cam1 and wrky53 mutants was higher compared with the [...] Read more.
Jasmonic acid (JA) is an important hormone that functions in plant defense. cam1 and wrky53 mutants were more resistant to Spodoptera littoralis than in the wild-type (WT) Arabidopsis group. In addition, JA concentration in cam1 and wrky53 mutants was higher compared with the WT group. To explore how these two proteins affect the resistance of Arabidopsis plants, we used a yeast two-hybrid assay, firefly luciferase complementation imaging assay and in vitro pull-down assay confirming that calmodulin 1 (CAM1) interacted with WRKY53. However, these two proteins separate when calcium concentration increases in Arabidopsis leaf cells. Then, electrophoretic mobility shift assay and luciferase activation assay were used to verify that WRKY53 could bind to lipoxygenases 3 (LOX3) and lipoxygenases 4 (LOX4) gene promoters and negatively regulate gene expression. This study reveals that CAM1 and WRKY53 negatively regulate plant resistance to herbivory by regulating the JA biosynthesis pathway via the dissociation of CAM1-WRKY53, then the released WRKY53 binds to the LOXs promoters to negatively regulate LOXs gene expression. This study reveals WRKY53′s mechanism in insect resistance, a new light on the function of WRKY53. Full article
(This article belongs to the Special Issue Plant-Insect Interactions 2022)
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6 pages, 235 KiB  
Editorial
Recent Advances in Plant–Insect Interactions
by Francesca Barbero and Massimo E. Maffei
Int. J. Mol. Sci. 2023, 24(14), 11338; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms241411338 - 12 Jul 2023
Cited by 1 | Viewed by 1224
Abstract
Plant–insect interaction is a fast-developing research field that continues to increase the interest of numerous scientists, many of whom come from heterogeneous backgrounds [...] Full article
(This article belongs to the Special Issue Plant-Insect Interactions 2022)
17 pages, 3592 KiB  
Article
Adaptation of Helicoverpa armigera to Soybean Peptidase Inhibitors Is Associated with the Transgenerational Upregulation of Serine Peptidases
by Pedro A. Velasquez-Vasconez, Benjamin J. Hunt, Renata O. Dias, Thaís P. Souza, Chris Bass and Marcio C. Silva-Filho
Int. J. Mol. Sci. 2022, 23(22), 14301; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms232214301 - 18 Nov 2022
Cited by 2 | Viewed by 1335
Abstract
Molecular phenotypes induced by environmental stimuli can be transmitted to offspring through epigenetic inheritance. Using transcriptome profiling, we show that the adaptation of Helicoverpa armigera larvae to soybean peptidase inhibitors (SPIs) is associated with large-scale gene expression changes including the upregulation of genes [...] Read more.
Molecular phenotypes induced by environmental stimuli can be transmitted to offspring through epigenetic inheritance. Using transcriptome profiling, we show that the adaptation of Helicoverpa armigera larvae to soybean peptidase inhibitors (SPIs) is associated with large-scale gene expression changes including the upregulation of genes encoding serine peptidases in the digestive system. Furthermore, approximately 60% of the gene expression changes induced by SPIs persisted in the next generation of larvae fed on SPI-free diets including genes encoding regulatory, oxidoreductase, and protease functions. To investigate the role of epigenetic mechanisms in regulating SPI adaptation, the methylome of the digestive system of first-generation larvae (fed on a diet with and without SPIs) and of the progeny of larvae exposed to SPIs were characterized. A comparative analysis between RNA-seq and Methyl-seq data did not show a direct relationship between differentially methylated and differentially expressed genes, while trypsin and chymotrypsin genes were unmethylated in all treatments. Rather, DNA methylation potential epialleles were associated with transcriptional and translational controls; these may play a regulatory role in the adaptation of H. armigera to SPIs. Altogether, our findings provided insight into the mechanisms of insect adaptation to plant antiherbivore defense proteins and illustrated how large-scale transcriptional reprograming of insect genes can be transmitted across generations. Full article
(This article belongs to the Special Issue Plant-Insect Interactions 2022)
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12 pages, 1762 KiB  
Article
The Effects of High CO2 and Strigolactones on Shoot Branching and Aphid–Plant Compatibility Control in Pea
by Hendrik Willem Swiegers, Barbara Karpinska, Yan Hu, Ian C. Dodd, Anna-Maria Botha and Christine H. Foyer
Int. J. Mol. Sci. 2022, 23(20), 12160; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms232012160 - 12 Oct 2022
Cited by 2 | Viewed by 1335
Abstract
Elevated atmospheric CO2 concentrations (eCO2) regulate plant architecture and susceptibility to insects. We explored the mechanisms underpinning these responses in wild type (WT) peas and mutants defective in either strigolactone (SL) synthesis or signaling. All genotypes had increased shoot height [...] Read more.
Elevated atmospheric CO2 concentrations (eCO2) regulate plant architecture and susceptibility to insects. We explored the mechanisms underpinning these responses in wild type (WT) peas and mutants defective in either strigolactone (SL) synthesis or signaling. All genotypes had increased shoot height and branching, dry weights and carbohydrate levels under eCO2, demonstrating that SLs are not required for shoot acclimation to eCO2. Since shoot levels of jasmonic acid (JA) and salicylic acid (SA) tended to be lower in SL signaling mutants than the WT under ambient conditions, we compared pea aphid performance on these lines under both CO2 conditions. Aphid fecundity was increased in the SL mutants compared to the WT under both ambient and eCO2 conditions. Aphid infestation significantly decreased levels of JA, isopentenyladenine, trans-zeatin and gibberellin A4 and increased ethylene precursor ACC, gibberellin A1, gibberellic acid (GA3) and SA accumulation in all lines. However, GA3 levels were increased less in the SL signaling mutants than the WT. These studies provide new insights into phytohormone responses in this specific aphid/host interaction and suggest that SLs and gibberellins are part of the network of phytohormones that participate in host susceptibility. Full article
(This article belongs to the Special Issue Plant-Insect Interactions 2022)
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