A tiered defensive regulatory network in tomato is revealed that integrates signal perception, hormonal regulation, metabolic reconfiguration, and ROS-mediated responses to counteract B. impatiens infestation, accompanied by sustained adaptive metabolic remodeling to withstand continuous larval feeding pressure.
Abstract
Tomato (Solanum lycopersicum) is an important agricultural crop frequently threatened by pests such as Bradysia impatiens (B. impatiens), a globally distributed sciarid fly whose larvae inflict severe damage on roots, stems, and leaves, leading to substantial yield losses. Despite its economic importance, the molecular and metabolic mechanisms underlying tomato defense against B. impatiens remain poorly understood. In this study, integrated transcriptomic and metabolomic approaches were employed to investigate the responses of tomato leaves to B. impatiens larval infestation at one week post-infestation. In our experimental system, larvae were introduced onto the soil surface and sequentially fed on stem bases (causing seedling lodging), leaves of prostrate plants, and roots. The leaf responses therefore reflect a combination of direct larval feeding on leaf tissues and systemic effects resulting from stem and root damage. Herbivory induced extensive transcriptional reprogramming, with 2,973 differentially expressed genes (DEGs) significantly enriched in pathways related to MAPK signaling, plant hormone transduction, plant-pathogen interactions, and phenylpropanoid biosynthesis. Metabolomic analysis identified 1,462 differentially accumulated metabolites, indicating significant shifts in energy metabolism, antioxidant defense systems, and the biosynthesis of defense-related compounds such as terpenoids and phenylpropanoids. Combined analyses revealed synchronized induction of α-linolenic acid metabolism and jasmonate signaling, accompanied by increased accumulation of reactive oxygen species (ROS) and upregulation of ethylene-responsive factors (ERF), bHLH, and NAC transcription factors. These findings reveal a tiered defensive regulatory network in tomato that integrates signal perception, hormonal regulation, metabolic reconfiguration, and ROS-mediated responses to counteract B. impatiens infestation. This entire defensive cascade embodies herbivory-triggered induced resistance, accompanied by sustained adaptive metabolic remodeling to withstand continuous larval feeding pressure. This study provides a comprehensive perspective on tomato plant-insect interactions and identifies potential targets for enhancing tomato resistance through molecular breeding or ecological management strategies. Notably, the hub transcription factor gene MYC, JA rate-limiting biosynthetic gene 12-oxophytodienoate reductase 3 (OPR3), α-linolenic acid-derived oxylipins and phenylpropanoid metabolites are highlighted as promising molecular biomarkers and core targets for future tomato anti-fungus gnat resistance engineering.
The stem-boring herbivore Aeolesthes induta severely threatens tea (Camellia sinensis) production, yet the systemic defense mechanisms of tea plants remain largely elusive. The unique age-dependent infestation pattern of A. induta—with minimal damage to young tea plants but infestation rates reaching 20% in 30-year-old trees and nearly 100% in ancient tea trees—necessitated field sampling from naturally infested old tea plantations rather than controlled laboratory conditions. By integrating rhizosphere microbiomics, transcriptomics, and multi-omics modeling, this study characterized the defensive regulatory networks of 30-year-old Shuixian tea cultivars under A. induta infestation. Rhizosphere microbiome analysis revealed that herbivore attack significantly reshaped the microbial community structure, reducing bacterial diversity and simplifying co-occurrence network complexity. Transcriptomic and metabolomic profiling demonstrated a precise source–sink defense allocation between host tissues. In leaves acting as the photosynthetic source, metabolic reprogramming was dominated by the systematic accumulation of soluble sugars and sugar acids for systemic energy reallocation. Concurrently, the roots acting as the metabolic sink vigorously activated the jasmonic acid (JA) signaling cascade and upregulated genes enriched in phenylpropanoid biosynthesis and alpha-linolenic acid metabolism. This molecular activation drove the substantial de novo synthesis of defensive phenolic acids, while downregulating growth-related flavonoids. Integrated network modeling further highlighted the phenylpropanoid pathway as the central regulatory node coupling transcript–metabolite fluctuations. This study constructs an integrated soil microbiome–root–leaf defense network, providing novel mechanistic insights into plant–borer interactions and a valuable foundation for future insect-resistant breeding programs in the tea industry.
Cheng-Cong Lu, Jia-Lin Zhang, Ke Chen et al.· Insects· 0 citations
The results support the use of T. harzianum as an effective bioinoculant to enhance plant growth and suppress pests, offering a sustainable alternative to synthetic agrochemicals.
Blanca A. ESQUIVEL-AYALA, Margarita Vargas-SandÓVal, M. P. Chaires-Grijalva et al.· Pest Management Science· 0 citations
Chile is a global leader in the fruit industry; however, the sector faces significant yield losses due to phytopathogens and an urgent need to reduce reliance on chemical fungicides. Induction of plant defenses and priming offer sustainable alternatives by activating the plant’s innate immune system. This study aimed to evaluate the ability of native Pseudomonas protegens strains and their formulations to trigger plant defense responses in five agronomically important fruit crops: kiwifruit (Actinidia chinensis var. deliciosa), walnut (Juglans regia), cherry (Prunus avium), blueberry (Vaccinium corymbosum), and grapevine (Vitis vinifera). Under controlled conditions, a randomized block design was implemented with four treatments, including P. protegens strains and their formulations, as well as a chemical elicitor (acibenzolar-S-methyl) as a positive control. Foliar treatments were applied, and leaf tissues were sampled at 1 day, 7 days, and 14 days post-inoculation. Transcriptional responses were quantified via qPCR using the ΔΔCt method, targeting key defense-related genes, including pathogenesis-related proteins (pr1, pr2, pr3, pr5, pr10) and enzymes of the phenylpropanoid and signaling pathways (pal, chs, ppo, lox9, glc). This study provides a molecular framework for understanding how biological inducers modulate defense-related gene expression in perennial crops. The results highlight the potential of native bacteria to be integrated into sustainable integrated pest management programs, offering an alternative strategy to trigger defense-related transcriptional activation in fruit perennial crops.
Braulio Ruíz, M. Sanz, Yerko Lovera et al.· Agronomy· 0 citations
Results suggest that the stronger resistance to P. nicotianae by X7 is associated with rapid coordination of defense-related transcription, phenylpropanoid and flavonoid metabolism, hormone signaling, and suppression of photosynthesis and primary metabolism.
Guo Li, Chang-Jiang Zhang, Bei Yu et al.· Plant physiology and biochem...· 0 citations
Verticillium dahliae is a destructive soil-borne fungus with a broad host range, and its persistence in soil complicates control. Current measures, mainly resistant cultivars and chemicals, are limited and environmentally risky, promoting biocontrol as a green alternative. Here, we investigated the biocontrol mechanisms of Bacillus velezensis L33a against V. dahliae JR2 in tomato. In vitro assays on PDA plates at 26°C for 9 d showed that L33a inhibited JR2 by 58.6%, caused hyphal malformation and disruption, and its volatile organic compounds suppressed pathogen growth. In pot experiments, tomato roots dipped in JR2 suspension (1 ×10⁶ CFU/mL) for 30 min at 7 d after transplanting and grown for 21 d achieved 60.9% control efficacy. Physiological assays indicated reduced peroxidase and catalase activities, while qPCR revealed that L33a alone upregulated JA signaling (SlJAZ1, SlMYC2, SlPI II) and antioxidant (SlCAT, SlAPX) genes, with further enhancement upon JR2 co-treatment. To track their interactions, we generated GFP-labeled JR2 and RFP-labeled L33a; dual fluorescence labeling showed that L33a endophytically colonized Arabidopsis thaliana roots and competed with JR2 for the same niche, correlating with reduced pathogen colonization. Integrated metabolomic and transcriptomic analysis further revealed that L33a treatment altered pathways related to ABC transporters, amino acid metabolism, cell wall integrity, and energy metabolism in JR2, with tyrosine metabolism significantly enriched at both levels. Collectively, these findings suggest that L33a is a promising biocontrol strain for green management of tomato Verticillium wilt.
Root knot nematodes (Meloidogyne spp.) is a major group of plant-parasitic nematode that severely reduce crop productivity by hijacking host root resources. Environmental and toxicological risks associated with chemical nematicides drive the need of eco-friendly management strategies. Therefore, a greenhouse experiment was conducted to assess the single/joint suppressive effects of Arthrobotrys oligospora and salicylic acid (SA) in tomato (Solanum lycopersicum) plants infected with Meloidogyne incognita. Compared to single treatment, combined (A. oligospora + SA) application exhibited pronounced improvement in growth, biochemical parameters, and yield attributes in nematode-infected tomatoes. The combined treatment significantly (P < 0.05) enhanced β-1,3-glucanase, phenylamine ammonia lyase (PAL), peroxidase (POD), and superoxide dismutase (SOD) activities, while significantly (P < 0.05) decreased in proline and malondialdehyde (MDA) content when compared with nematode-infected plants. The combined treatment of A. oligospora and SA significantly decreased nematode infection parameters, disease index, and reproduction factor in nematode-infected tomato. Histological analysis showed that A. oligospora reduced nematode penetration and feeding site development, whereas roots infected solely with M. incognita displayed pronounced vascular bundle damage. These findings demonstrate that the combined application of A. oligospora and SA effectively suppressed M. incognita infection and enhanced tomato defence responses under greenhouse conditions.
Abdelrahman R. Ahmed, M. Danish, Mohammad Shahid et al.· Functional Plant Biology· 0 citations
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