Uncovering the multifaceted properties of 6-pentyl-alpha-pyrone for control of plant pathogens

Abstract

Some volatile organic compounds (VOCs) produced by microorganisms have the ability to inhibit the growth and development of plant pathogens, induce the activation of plant defenses, and promote plant growth. Among them, 6-pentyl-alpha-pyrone (6-PP), a ketone produced by Trichoderma fungi, has emerged as a focal point of interest. 6-PP has been isolated and characterized from thirteen Trichoderma species and is the main VOC produced, often accounting for >50% of the total VOCs emitted. This review examines abiotic and biotic interactions regulating the production of 6-PP by Trichoderma, and the known effects of 6-PP on plant pathogens through direct and indirect mechanisms including induced systemic resistance. While there are many reports of 6-PP activity against plant pathogens, the vast majority have been from laboratory studies involving only 6-PP and the pathogen, rather than glasshouse or field studies including a host plant in the system. Biopesticides based on 6-PP may well provide an eco-friendly, sustainable management tool for future agricultural production. However, before this can happen, challenges including demonstrating disease control efficacy in the field, developing efficient delivery systems, and determining cost-effective application rates must be overcome before 6-PP's potential for pathogen control can be turned into reality.

Keywords: 6-pentyl-alpha-pyrone (6-PP); Trichoderma; abiotic and biotic interactions; biopesticides; plant defense regulator; plant growth promotion; plant pathogens; sustainability.

Figure 1

Structure of 6-n-pentyl pyrone (6-PP) and variants reported in Trichoderma spp. (A) Structural representation of 6-n-pentyl-α-pyrone; the numbers in the molecule represent the position of atoms or functional groups within the molecule. The number ‘6’ indicates the position of the pentyl substituent on the six-membered pyrone ring, shown in blue. The term ‘n-pentyl’ signifies a straight-chain alkyl group containing five carbon atoms, with the numbers in the aliphatic tail highlighted in red. ‘α-pyrone’ describes the structure of the ring, specifying a six-membered heterocyclic ring with a carbonyl group (C=O) at position 2. (B–E) Variations of the molecule, including modifications in the ring structure and aliphatic side chain, are shown. These variants illustrate potential structural diversities within the 6PP molecule. The figures were modified from those reported in their original publications (Collins and Halim, 1972; Claydon et al., 1987; Parker et al., 1997; Evidente et al., 2003).

Figure 2

Abiotic and biotic interactions regulating the production of 6-pentyl-α-pyrone in Trichoderma. This hypothetical model explains at the molecular level the abiotic (sunlight) and biotic (fungivory, phytopathogens, and plants) interactions involved in regulating the biosynthesis of 6-PP and the main functions in Trichoderma interacting with plants or inhibiting phytopathogenic fungi, mechanisms both highly relevant in crop protection. Production of 6-PP is affected in mutant strains lacking in the tga1 gene encoding Gα protein (Tga1) and thus inhibiting cyclic adenosine monophosphate (cAMP) levels, the Mitogen-Activated Protein Kinase (MAPK) Tmk1 and Tmk3, the response regulator Skn7 and NADPH oxidase 1 (Nox1), 2 (Nox2), and the regulator NoxR. In filamentous fungi, the MAPK Tmk1 is regulated by MAPKK Ste7 and the last is regulated by MAPKKK Ste11, forming a cascade of at least three protein kinases. The cascade MAPKKK Ssk2 – MAPKK Pbs2 – MAPK Tmk3 is regulated by a two-component system consisting of a histidine kinase (HK) sensor, a histidine-containing phosphotransferase (Ypd1), and a response regulator (Ssk2/Skn7) (Schmoll et al., 2016). Blr1 and Blr2 form a blue-light receptor in Trichoderma (Schmoll et al., 2010). The heterotrimeric G proteins (α, β, and γ) associated with G protein-coupled receptors (GPCR) regulate cAMP synthesis from ATP by an adenylyl cyclase (AC), a second messenger which regulates protein kinase A (PKA) (Schmoll et al., 2016). Arrows (→) indicate positive regulation, activation, or induction. Bars (⊥) indicate negative regulation, repression, or inactivation.

Figure 3

Cellular processes targeted by 6-PP on plant pathogens. The figure illustrates various aspects of the interaction between 6-PP and plant pathogens. (A) A mitochondrial dysfunction may provoke ROS imbalance and affects genome integrity, leading to the programed cell dead (Apoptosis) (Liu et al., 2023; Xing et al., 2023). (B) 6-PP regulates production of mycotoxin in plant pathogens by downregulation of vel complex and fub10 genes, key players to regulate expression of the cluster Fub and synthesis of aflatoxin. (Niehaus et al., 2014; Ismaiel and Ali, 2017; Hao et al., 2023) (C) 6-PP regulates the TOR signaling pathway, impacting different development process such as growth, sporangium formation, encystment, zoospore release and pathogenicity (Wu et al., 2023). (D) Alteration of organic acids metabolism via the Krebs cycle may affect the physiology of plant pathogens. 6-PP alters metabolic pathways in plant pathogens, affecting their ability to acquire nutrients and energy for growth and survival (Jin et al., 2020).

Figure 4

Effects of 6-PP Application on Systemic Tissues. (A) Impact of two concentrations of 6-PP on metabolite accumulation in tissues of treated plants. Through metabolomic analysis, distinct accumulation patterns of various metabolites, including secondary metabolites and signalling molecules, are observed in response to the different concentrations of 6-PP. This differential accumulation suggests a dosage-dependent effect of 6-PP on plant metabolism, highlighting its potential role in modulating biochemical pathways involved in stress responses and defence mechanisms (Mazzei et al., 2016). (B) depicts the induction of salicylic acids (SA) and associated metabolites, including pathogenesis-related (PR) proteins, in different plant species following treatment with 6-PP. PRR, Pathogen Recognition Receptor.

Figure 5

Beneficial applications of 6-penty-alpha-pyrone in agriculture (A) 6-PP regulates auxin for seed germination, root formation, and enhanced plant resilience to abiotic stresses (Garnica‐Vergara et al., 2016), (B) 6-PP improves photosynthesis activity for plant growth (Comite et al., 2021), (C) 6-PP enhances plant nutrient absorption (Carillo et al., 2020), (D) 6-PP acts as an infochemical communication method to attract a beneficial wasp (Contreras-Cornejo et al., 2018), (E) 6-PP helps control plant pathogens (Kottb et al., 2015; Taha et al., 2021; Hao et al., 2023), and (F) 6-PP induces plant signal to stimulate beneficial microbiomes (Zhu et al., 2023).

Figure 6

Representation of bioconversion of 6-n-pentyl-α-pyrone (6-PP) by diverse organisms. In the top panel, the structure of 6-PP is depicted. This figure illustrates the diverse bioconversion capabilities of different organisms when exposed to 6-PP, resulting in the production of various converted molecules. These conversion products are represented by different molecules derived from 6-PP, indicated within colored squares: 6-PP converted by different fungi is represented in red (Cooney et al., 1997b; Cooney and Lauren, 1999). 6-PP converted by cell culture pine is depicted in green (Cooney et al., 2000). 6-PP converted by Streptomyces is shown in blue (Li et al., 2005).