TYPE Editorial

PUBLISHED 24 September 2024

DOI 10.3389/fpls.2024.1480678

Editorial: Omics in plant-

OPEN ACCESS insect interactions
EDITED AND REVIEWED BY
Peng Wang, Shengli Jing 1*, Guangcun He 2 and Ming-shun Chen 3
Jiangsu Province and Chinese Academy of
Sciences, China 1
College of Life Sciences, Xinyang Normal University, Xinyang, China, 2 State Key Laboratory of Hybrid
*CORRESPONDENCE
Rice, College of Life Sciences, Wuhan University, Wuhan, China, 3 Hard Winter Wheat Genetics
Shengli Jing Research Unit, USDA-ARS, Manhattan, KS, United States
shljing@[Link]
KEYWORDS
RECEIVED 14 August 2024
ACCEPTED 26 August 2024
plant-insect interactions, multi-omics analysis, resistance mechanism, secondary
PUBLISHED 24 September 2024 metabolites, resistance genes

CITATION
Jing S, He G and Chen M-s (2024) Editorial:
Omics in plant-insect interactions.
Front. Plant Sci. 15:1480678.
doi: 10.3389/fpls.2024.1480678 Editorial on the Research Topic
COPYRIGHT
Omics in plant-insect interactions
© 2024 Jing, He and Chen. This is an open-
access article distributed under the terms of
the Creative Commons Attribution License
(CC BY). The use, distribution or reproduction
in other forums is permitted, provided the Insect herbivores and their host plants engage in a dynamic molecular conflict, wherein
original author(s) and the copyright owner(s) plants have evolved sophisticated defense mechanisms, while insects have developed
are credited and that the original publication
in this journal is cited, in accordance with strategies to suppress these defenses. These interactions involve intricate molecular
accepted academic practice. No use, processes that are a major focus of research, with the goal of improving pest
distribution or reproduction is permitted
control strategies.
which does not comply with these terms.
Herbivorous insects, such as piercing-sucking hemipterans and chewing
Lepidopterans, establish close associations with host plants to manipulate plant cellular
processes for feeding and reproduction (Erb and Reymond, 2019). In response, plants have
evolved complex immune systems composed of signaling pathways, resistance genes, and
secondary metabolites. This ongoing molecular arms race between plants and insects is
characterized by interactions among a diverse array of molecules from both organisms.
Plant secondary metabolites and resistance genes serve as defense mechanisms against
insect herbivory, while insects utilize detoxification enzymes and effectors to disrupt plant
defenses, enhancing their adaptation.
This Research Topic explores the complex genetic, physical, metabolic, and molecular
interactions between plants and insects, examined through advanced omics technologies such
as genomics, transcriptomics, and metabolomics. The Research Topic includes 16 original
research and review articles focusing on herbivorous insects (e.g., brown planthopper, aphids,
psyllids) and their host plants (e.g., rice, maize, cotton), which are summarized below.

Interactions between rice and brown planthopper

Eight articles in this Research Topic (one review and seven research articles) focus on
the interaction between rice (Oryza sativa L.) and the brown planthopper (Nilaparvata
lugens Stål, BPH). This interaction serves as a valuable model system for studying the
molecular mechanisms underlying plant-insect interactions. The brown planthopper is a
major pest that causes significant damage to rice crops (Cheng et al., 2013; Jing et al., 2017),
and the deployment of resistant rice varieties has proven effective in managing this pest. To
date, over 40 resistance loci and 17 resistance genes for brown planthopper have been
identified and functionally characterized (Shar et al., 2023). The molecular mechanisms of

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these resistance genes represent a key area of research. This Hu et al. performed transcriptomic analysis to understand the
Research Topic includes articles on the molecular mechanisms mechanisms behind Bph14/Bph15-conferred resistance, using near-
involving four specific resistance genes: Bph6, Bph14, Bph15, isogenic lines (NILs) of rice containing Bph14 (B14), Bph15 (B15),
and Bph30. or both Bph14 and Bph15 (B1415), compared to their recurrent
Four articles focus on Bph15, examining the specific cells and parent (RP) variety ‘Wushansimiao’. The study identified 14,492
tissues involved in resistance, the role of OsWRKY71 in Bph15- differentially expressed genes (DEGs) across the profiles, with 531
mediated resistance, the defense mechanisms against BPH DEGs common to the resistant NILs compared to the RP before and
populations with varying virulence levels, and transcriptomic after BPH feeding. The DEGs related to BPH resistance were
analysis to elucidate the mechanisms behind BPH14/BPH15- primarily enriched in defense response and oxidative stress
conferred resistance. One article investigates how indole-3-acetic pathways. Twenty-one DEGs were selected as candidate genes for
acid (IAA) negatively regulates Bph30-mediated resistance using BPH resistance based on their expression patterns and relevance
combining transcriptomic and metabolomic analyses. Two from previous research. OsPOX8.1, one of the candidate genes, was
additional articles (one review and one research) explore the validated in rice protoplasts, showing increased reactive oxygen
impact of non-coding RNAs on the interaction between rice and species (ROS) accumulation, providing insights into the defense
brown planthopper, and one article identifies BPH resistance genes mechanisms activated by BPH resistance gene pyramiding in rice.
using Genome-wide association studies (GWAS) and evaluates the Shi et al. combined transcriptomic and metabolomic analyses to
predictive ability of genomic selection for resistance to BPH. study Bph30-transgenic (Bph30T) rice plants and BPH-susceptible
Zha et al. used single-cell sequencing technology to analyze Nipponbare plants. Transcriptomic analysis revealed that many
different cell types involved in BPH resistance, comparing the differentially expressed genes (DEGs) in susceptible rice plants were
responses of leaf sheaths from susceptible (TN1) and resistant involved in plant hormone signal transduction, particularly in
(YHY15) rice varieties 48 hours after infestation. The analysis indole-3-acetic acid (IAA) signal transduction. Metabolomic
identified 14,699 cells in TN1 and 16,237 cells in YHY15, which analysis showed that differentially accumulated metabolites
were grouped into nine cell-type clusters using cell-specific marker (DAMs) in the amino acids and derivatives category were down-
genes. Significant differences were observed between the two rice regulated, while DAMs in the flavonoids category were up-
varieties in their resistance mechanisms to BPH. Further analysis regulated in resistant plants following BPH feeding. Combined
revealed that different cell types employ distinct molecular analysis indicated that flavonoid and lignin biosynthesis are
mechanisms in response to BPH, enhancing the understanding of involved in resistance, while biosynthesis of various amino acids
the molecular processes underlying rice resistance and accelerating and IAA are involved in susceptibility. The study confirmed that
the breeding of insect-resistant rice varieties. exogenous IAA application weakened Bph30-mediated BPH
Li et al. discovered that the transcription factor OsWRKY71 is resistance, demonstrating that IAA negatively regulates Bph30-
highly responsive to BPH infestation, with early-induced expression mediated resistance through the shikimate and phenylpropanoid
in Bph15 near-isogenic line (NIL) plants. OsWRKY71 localizes in metabolism pathways.
the nucleus of rice protoplasts, and its knockout in the Bph15-NIL Jing et al. summarized the roles of small RNAs in the rice-BPH
background using CRISPR-Cas9 technology resulted in interaction. Functional validation experiments indicated that these
compromised Bph15-mediated resistance. Transcriptome analysis sRNAs fine-tune plant innate immunity by integrating R gene-
indicated significant differences in the transcriptional response to mediated resistance, phytohormone signaling, callose deposition,
BPH infestation between the wrky71 mutant and the Bph15-NIL, reactive oxygen species (ROS) production, and secondary
affecting the expression of several defense-related genes. The study metabolite biosynthesis. Additionally, sRNAs are involved in key
identified three potential participants (OsSTPS2, OsEXO70J1, and aspects of BPH biology, such as metamorphosis, wing polyphenism,
RGA2) in the BPH resistance pathway mediated by OsWRKY71 in molting, and reproductive development. The study also observed
Bph15-NIL plants, highlighting the crucial role of OsWRKY71 in cross-kingdom RNAi in the rice-BPH interaction, suggesting that
Bph15-mediated resistance. sRNAs ingested by BPH while feeding on rice may regulate BPH
Yu et al. conducted miRNA and mRNA expression profiling to gene expression. These findings highlight the potential of HIGS and
investigate the differential responses of YHY15 rice to both SIGS as promising agricultural pest control strategies.
avirulent (biotype 1) and virulent (biotype Y) BPH. The study Wu et al. focused on the regulatory roles of non-coding RNAs,
found that YHY15 rice exhibited a rapid response to biotype Y BPH specifically long non-coding RNAs (lncRNAs) and circular RNAs
infestation, with significant transcriptional changes within 6 hours. (circRNAs), in Bph6-transgenic (resistant, BPH6G) and
The biotype Y-responsive genes were enriched in photosynthetic Nipponbare (susceptible, NIP) rice plants infested by brown
processes, and biotype Y BPH infestation induced more intense planthoppers. Genome-wide analysis identified 310 differentially
transcriptional responses compared to biotype 1 BPH, affecting expressed lncRNAs and 129 differentially expressed circRNAs
miRNA expression, defense-related metabolic pathways, between the resistant and susceptible rice plants. Dual-luciferase
phytohormone signaling, and multiple transcription factors. reporter assays revealed specific interactions between lncRNAs and
Callose deposition was also enhanced in biotype Y BPH-infested microRNAs (miRNAs), such as lncRNA XLOC_042442 targeting
rice seedlings, indicating a heightened defense response. These miR1846c and lncRNA XLOC_028297 targeting miR530. The study
findings provide comprehensive insights into the defense predicted that 39 lncRNAs and 21 circRNAs could interact with 133
mechanisms of resistant rice against virulent BPH populations. common miRNAs and compete for miRNA binding sites with 834

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mRNAs, implicating these mRNAs in key biological processes such Psyllid-pathogen interactions
as cell wall organization, biogenesis, developmental growth, single-
organism cellular processes, and stress responses. This study Two articles in this Research Topic focus on psyllids as vectors
provides a comprehensive identification and characterization of in vector-pathogen interactions. Li et al. examine the biochemical
lncRNAs and circRNAs in rice plants infested by BPH, laying a effects of Candidatus Liberibacter solanacearum (CLso) infection in
crucial foundation for future research on non-coding RNAs in the potato psyllids (Bactericera cockerelli), vectors of diseases such as
rice-BPH interaction. psyllid yellows, vein-greening (VG), and zebra chip (ZC). Using
Zhou et al. present a comprehensive resource on BPH resistance ultra-performance liquid chromatography tandem mass
genes and offer practical recommendations for genomic selection in spectrometry (UPLC-MS/MS), the study identified 34 metabolites
rice breeding programs. Through Genome-Wide Association related to amino acid, carbohydrate, and lipid metabolism as
Studies (GWAS), six loci were significantly associated with BPH potential biomarkers of CLso infection. Matrix-assisted Laser
resistance across three assessment criteria. Among these, two loci Desorption Ionization Mass Spectrometry Imaging (MALDI-MSI)
were novel, while others included previously identified BPH- mapped the spatial distribution of these biomarkers, revealing
resistant genes such as Bph6, Bph32, and Bph37. The accuracy of significant down-regulation of 15-keto-Prostaglandin E2 and
genomic prediction (GP) was influenced by the number of SNPs, alpha-D-Glucose in the abdomen of infected psyllids. These
training population size, and statistical models. To enhance the findings suggest mechanisms of immune suppression employed
prediction of BPH resistance, it is recommended to increase SNP by CLso to evade detection and clearance by the psyllid’s
numbers beyond 26,000, expand the training population size immune system.
beyond 737 individuals, and utilize random forest (RF) models. He et al. investigate the interactions between the Asian citrus
Optimizing these genomic selection strategies will facilitate the psyllid (ACP) and Candidatus Liberibacter asiaticus (CLas), the
development of durable BPH-resistant rice varieties, thereby causative agent of citrus greening disease. This research explores
contributing to sustainable global rice production. how different life stages of ACP influence gene expression in
response to CLas infection. RNA sequencing (RNA-seq) revealed
significant changes in gene expression, particularly in later nymphal
Aphid-mediated tritrophic interactions stages (4-5) and teneral adults. A large number of genes related to
defense mechanisms, developmental processes, and immune
Two articles in this Research Topic examine aphids as vectors in responses were found to be highly responsive to CLas infection.
tritrophic interactions. Zhao et al. investigate the effects of nitrogen Understanding these gene expressions provides insights into how
fertilization on the emission of plant volatile organic compounds ACP manages the bacterial infection and contributes to
(VOCs) that mediate interactions among maize, aphids, and disease transmission.
ladybirds. Specifically, 1-nonene was identified as a key
compound attracting ladybirds, with its release positively
correlated with the visitation rates of Harmonia axyridis. The Plant-herbivore interactions
study demonstrated that supplying 1-nonene to maize under low-
nitrogen conditions increased the attractiveness of plants to Two articles in this Research Topic focus on interactions
ladybirds, highlighting the compound’s role in tritrophic between herbivorous insects and their host plants. Liu et al.
interactions. The synthesis of 1-nonene is linked to salicylic acid investigate how insect egg deposition affects plant defenses in
(SA) and abscisic acid (ABA), indicating complex interactions willows (Salix matsudana ‘Zhuliu’). The study found that egg
within plant response mechanisms to nutrient availability and deposition by Plagiodera versicolora triggered plant defensive
pest infestation. This research enhances our understanding of responses and enhanced the plant’s ability to cope with
plant metabolic responses to nutrient levels and offers practical subsequent larval feeding. RNA-seq analysis revealed altered
insights for improving pest management and crop production. expression of genes related to stress responses and metabolic
Pandey et al. explore the influence of host plants on the gene processes. Following larval feeding, increased activity of genes
expression of the cotton aphid (Aphis gossypii Glover) when infected involved in phenylpropanoid biosynthesis and phytohormone
with the cotton leafroll dwarf virus (CLRDV). Using four host plants signaling was observed, indicating that egg deposition primes the
—cotton, hibiscus, okra, and prickly sida—the study revealed plant for heightened defense. Bioassays demonstrated that larvae
significant differences in gene expression among aphids acquiring feeding on leaves with prior egg deposition exhibited reduced
the virus from different hosts. A total of 2,942 differentially expressed performance, suggesting that the willow’s induced defenses
genes (DEGs) were identified, with varying DEG counts across hosts: effectively decrease larval survivability.
750 from cotton, 310 from hibiscus, 1,193 from okra, and 689 from Sun et al. analyze the biochemical and molecular responses of
prickly sida. Notably, more genes were overexpressed in aphids from daylilies (Hemerocallis citrina ‘Datong Huanghua’) to feeding by
cotton, hibiscus, and prickly sida, while more genes were Thrips palmi. The study found significant reductions in soluble
underexpressed in aphids from okra. These findings underscore sugar, amino acid, and free fatty acid levels in daylily leaves after T.
the complexity of vector-virus-host interactions and the pivotal palmi feeding, alongside increases in secondary metabolites like
role of host plants in influencing disease transmission. tannins, flavonoids, and phenols. Key defense enzymes, including

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peroxidase (POD), phenylalanine ammonia lyase (PAL), and review & editing. M-SC: Formal analysis, Investigation, Validation,
polyphenol oxidase (PPO), were significantly enhanced. RNA Writing – review & editing.
sequencing identified 1,894 differentially expressed genes (DEGs)
associated with T. palmi feeding, with 698 predicted as transcription
factors involved in stress responses. Weighted Gene Co-expression Funding
Network Analysis (WGCNA) highlighted 18 hub genes in key
modules, potentially crucial for regulating defense responses. The author(s) declare financial support was received for the
research, authorship, and/or publication of this article. This study
was supported by grants from the National Natural Science
Review articles on plant- Foundation of China (U1704111, and 31401732), ZHONGYUAN
YINGCAI JIHUA (ZYYCYU202012165), the Open Project
insect interactions Funding of the State Key Laboratory of Crop Stress Adaptation
and Improvement (2023KF10).
Two review articles summarize plant defenses and key insect
proteins involved in interactions with host plants. Li et al. review
current knowledge and advances in plant defenses against
Acknowledgments
whiteflies, emphasizing the role of trichomes and acylsugars as
physical barriers, and secondary metabolites and jasmonate (JA)
We thank the authors who submitted their research or review
signaling in chemical defenses. The review discusses genetic and
articles in this Research Topic for their valuable contributions and
biotechnological approaches to enhance plant resistance, including
the reviewers for their rigorous reviews. We also thank the editorial
plant-mediated RNA interference (RNAi) and ectopic expression of
board of “Omics in Plant-Insect Interactions” and the Frontiers
insecticidal proteins. These advancements are critical for developing
specialists, for their support. This manuscript was assisted by
effective and sustainable solutions for whitefly management.
ChatGPT (Version: GPT-4, Model: OpenAI GPT-4, Source of
Wang et al. highlight key areas in the study of plant-insect
Generative AI Technology: OpenAI).
interactions, focusing on the identification of insect elicitors and
effectors and their roles in activating plant defense pathways such as
jasmonic acid (JA) and salicylic acid (SA) signaling, calcium flux,
Conflict of interest
reactive oxygen species (ROS) bursts, and mitogen-activated
protein kinase (MAPK) activation. Multi-omics approaches,
The authors declare that the research was conducted in the
including genomics, transcriptomics, and proteomics, are used to
absence of any commercial or financial relationships that could be
analyze insect saliva and salivary glands. The review provides
construed as a potential conflict of interest.
insights into the complex mechanisms of attack and defense and
the roles of various elicitors and effectors in these interactions.

Publisher’s note
Author contributions All claims expressed in this article are solely those of the authors
and do not necessarily represent those of their affiliated
SJ: Conceptualization, Data curation, Formal analysis, Funding organizations, or those of the publisher, the editors and the
acquisition, Investigation, Methodology, Project administration, reviewers. Any product that may be evaluated in this article, or
Supervision, Writing – original draft, Writing – review & editing. claim that may be made by its manufacturer, is not guaranteed or
GH: Data curation, Investigation, Resources, Validation, Writing – endorsed by the publisher.

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