Plant Interactions with Viruses and Viroids: A Review of the Regulatory Roles of Secondary Metabolites and Phytohormones

Document Type : Review Paper

Authors

Mohaddeseh Sadeghi Nichkoohi

Zohreh Moradi

Department of Plant Pathology, Faculty of Crop Sciences, Sari Agricultural Sciences and Natural Resources University, Sari, Iran

10.22067/jpp.2025.94261.1239

Abstract

Introduction
Throughout the course of evolution, plants have developed remarkably sophisticated biological mechanisms that enable them to respond dynamically and effectively to a wide array of environmental and biotic stressors. Among the most formidable challenges plants face are infections by pathogenic agents, particularly viruses and viroids, which pose significant threats to plant health, productivity, and agricultural sustainability worldwide. Despite fundamental differences in their structure and mode of action, both viruses and viroids profoundly disrupt host physiological and molecular processes, leading to detrimental impacts on plant growth and defense systems.
 
Materials and Methods
This review synthesizes current knowledge on the complex interactions among viruses, viroids, and their plant hosts, focusing on the molecular crosstalk that governs secondary metabolite biosynthesis and phytohormonal regulation during infection. The information presented herein was compiled through a systematic review and analysis of relevant scientific literature, focusing on recent advancements and foundational studies in plant-pathogen interactions, molecular biology, and biochemistry. The goal was to provide a comprehensive overview of the defense mechanisms plants employ against viral and viroid infections.
 
Results and Discussion
Plant viruses, as obligate intracellular parasites, invade host cells and hijack cellular machinery to facilitate their replication and spread. This intrusion perturbs the host’s metabolic networks, altering the expression of genes involved in the biosynthesis of secondary metabolites such as alkaloids, terpenoids, and phenylpropanoids—compounds integral to plant defense. These metabolites not only serve as direct antimicrobial agents but also act as crucial modulators of signaling pathways that orchestrate defense responses and maintain cellular homeostasis. Moreover, viruses target and manipulate key plant hormonal signaling pathways involving salicylic acid, ethylene, abscisic acid, and methyl jasmonate. These phytohormones function as key regulators that modulate the delicate balance between growth and defense. Disruption of their signaling cascades manifests in a spectrum of pathological symptoms including stunted growth, chlorosis, necrosis, wilting, and characteristic mosaic leaf patterns, all of which reflect the profound physiological stress inflicted by viral invasion. In contrast, viroids—small, circular, non-coding RNA molecules—lack the capacity to encode proteins yet exert their pathogenicity through more subtle, yet no less consequential, mechanisms. By interfering with host gene expression and regulatory networks, viroids indirectly modulate the biosynthesis of defense-related metabolites and hormonal pathways. Although the mechanistic nuances of viroid pathogenicity differ from those of viruses, the resultant physiological disruptions and yield losses underscore their significance as persistent plant pathogens. Viroids—small, circular, non-coding RNAs—exert pathogenic effects through subtler mechanisms. Recent studies demonstrate that viroid infections can alter the transcriptional regulation of key biosynthetic genes involved in the production phenylpropanoids (including flavonoids and other phenolic compounds) and alkaloids—secondary metabolites that contribute significantly to structural defense, oxidative stress mitigation, and pathogen inhibition. These effects are often mediated through complex epigenetic mechanisms or RNA-based gene silencing pathways, leading to changes in enzymatic activity such as phenylalanine ammonia-lyase (PAL), chalcone synthase (CHS), and other enzymes central to the phenylpropanoid and alkaloid biosynthetic routes. Such metabolic shifts not only influence the plant’s basal immunity but also fine-tune the dynamic equilibrium between stress tolerance and physiological performance. Central to plant immunity are phytohormones, which play multifaceted roles in modulating immune responses. Notably, gibberellins and brassinosteroids exhibit dualistic functions, influencing both growth modulation and host susceptibility or resistance, whereas salicylic acid and jasmonates predominantly act as defense inducers, activating complex immune signaling networks. Ethylene’s role is more context-dependent; it may either amplify or attenuate defense responses contingent upon the specific virus involved and the physiological state of the host plant. Recent advances have illuminated the crucial involvement of certain phytohormones—such as salicylic acid, jasmonates, and brassinosteroids—in counteracting viroid infections. These hormones enhance host defenses by triggering signal transduction pathways that activate defense gene expression, thereby strengthening resistance mechanisms. This emerging evidence highlights the intricate and multilayered nature of plant immunity, underscoring the importance of hormonal regulation in maintaining a balanced and effective defense system. A hallmark of the plant’s antiviral defense is the induction of ethylene biosynthesis and activation of salicylic acid-dependent signaling pathways, culminating in systemic acquired resistance (SAR). SAR represents a long-lasting, broad-spectrum immune response that restricts pathogen proliferation beyond the initial infection site, thereby bolstering systemic immunity and fortifying plant resilience against secondary infections. Complementing these hormonal defenses, secondary metabolites serve as a critical line of defense, executing antiviral functions through diverse mechanisms including inhibition of viral replication, suppression of viral protein activity, and mitigation of oxidative damage.
 
Conclusions
The synergistic interplay between hormonal signaling and secondary metabolite production constitutes a cohesive and robust molecular defense network, the comprehensive understanding of which holds tremendous potential for the development of innovative strategies in plant disease management. This review synthesizes current knowledge on the complex interactions among viruses, viroids, and their plant hosts, focusing on the molecular crosstalk that governs secondary metabolite biosynthesis and phytohormonal regulation during infection. By elucidating these sophisticated regulatory networks, this work offers valuable insights and practical perspectives for leveraging this understanding in plant breeding programs and sustainable agriculture. The ultimate goal is to enhance crop resistance, improve yield stability, and contribute meaningfully to global food security in the face of escalating biotic stresses.
 

Keywords

Phytohormones

Plant defense response

Secondary metabolites

Viral and viroid agents

Subjects

• Virus

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Authors retain the copyright. This is an open access article distributed under Creative Commons Attribution 4.0 International License (CC BY 4.0)

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