Climate change is a complex event that consists of temperature and weather shifts, strongly impacting plant life (Janni et al., 2024). Abiotic stressors, like heat, cold and drought, have intensified in recent decades, causing detrimental effect on crop yields and making host crops more vulnerable to fungal disease onset (Sharma et al., 2023). Mycotoxins are secondary metabolites synthesized by a broad assortment of fungi. Their production is greatly impacted by climate change and warmer temperatures are increasing the distribution, abundance and co-occurrence of mycotoxin producing fungal species (Lanubile et al., 2021a; Casu et al., 2024).

Oxylipins play a pivotal role in the plant-environment interaction (Knieper et al., 2023). A literature survey was conducted to assess the scientific interest in plant oxylipins, revealing a steady increase over the last two decades (Figure 1). Indeed, literature search using the Ovid and Scopus databases on the topic “plant oxylipins” revealed a total number of 1,631 research studies between 2000 and 2024 with the peak of papers published in 2024, after applying some inclusion/exclusion criteria, i.e., excluding duplicates, including only research article published in English. Six-hundreds and sixty-five papers focused on the involvement of plant oxylipins in biotic stress, 296 on abiotic, 90 on both stresses, and 580 on other physiological processes, like germination and development. A treemap was also drawn pointing out that most papers were published on Plant Physiology (96), following by Plant Journal (93) and Plant Physiology and Biochemistry (75) (Figure 2). By scrutinizing the co-occurrence of keywords major links were revealed between oxylipins and the plant species Arabidopsis thaliana, Oryza sativa and Solanum lycopersicum (Figure 3A). Moreover, oxylipins showed connections with the signaling molecules cyclopentenones, jasmonic and salycilic acid, and implications in several physiological functions, signal transduction and plant disease responses (Figures 3B, C, respectively). Indeed, the extremely diverse chemical nature of these molecules implies their involvement in several roles. It’s well known that many oxylipins are powerful regulators of plant growth, development and interactions with biotic and abiotic stressors (Sugimoto et al., 2022). The oxylipin signaling occurs through a genetically defined signal network that is linked to several additional phytohormones, like salicylic acid, ethylene, and auxin. Therefore, jasmonates and cyclopentenone lipids, such as oxo-phytodienoic acid (OPDA and dinor OPDA), can activate or repress gene expression through the electrophilic activities of the cyclopentenone ring (Sugimoto et al., 2022).

The aim of this review is first to explore the phylogenetic relationships of the main group of enzymes participating in the biosynthesis of oxylipins considering five plant species, Arabidopsis thaliana, Oryza sativa, Zea mays, Solanum lycopersicum, and Vitis vinifera. The selection is based on their relevance in agriculture and availability of oxylipin-related gene data. The examined enzymes include the group of lipoxygenases (LOXs), allene oxide synthase (AOS) and cyclase (AOC), hydroperoxide lyase (HPL), divinyl ether synthase (DES), epoxy alcohol synthase (EAS), and peroxygenase (PXG) (Figure 4). Moreover, the contribution of oxylipins to environmental adaptation focusing on abiotic stressors, like heat, drought and waterlogging, and their role in mycotoxin production will be discussed. Lastly, the most recent genome editing interventions on the enzymes of the oxylipin pathway will be described.

Severe climatic events such as extreme heat, drought, and heavy rainfall can significantly impact plants, and call for recurrent and easily evolutionary adaptation and acclimatization. In this context, oxylipins serve as stress mitigators, reducing the impact of abiotic stressors. These lipid-derived signaling molecules modulate gene expression patterns (Taki et al., 2005; Guche et al., 2022), antioxidant activity (Yuan et al., 2017), membrane stability (Savchenko et al., 2014), and cross-talk with other hormonal pathways to fine-tune stress responses (Knieper et al., 2023). The role of oxylipins in plant responses to various abiotic challenges is explored in this section (Table 1).

How climate change affects mycotoxin contamination in edible crops was extensively reviewed by Casu et al. (2024). Plant oxylipins act as signals to modulate fungal developmental processes, including sporogenesis and biosynthesis of mycotoxins (Beccaccioli et al., 2022) (Table 2). Strong changes in oxylipin, sphingolipid, phospholipid, phytoceramide and amadori-glycated glycerophosphoethanolamine accumulation in response to fumonisin contamination and its source Fusarium verticillioides were previously reported in different maize lines and hybrids under open field conditions (Giorni et al., 2015; Righetti et al., 2021; Carbonell-Rozas et al., 2025). It was observed that ZmLOX4 gene loss of function mutation compromised resistance to F. verticillioides and fumonisin content in maize seedlings (Lanubile et al., 2021b) and ears (Guche et al., 2022) and altered ZmLOX gene expression as well as LOX enzymatic activity. Moreover, in Guche et al. (2022) work lox4 mutants were also highly susceptible to Aspergillus flavus and aflatoxin contamination. In contrast, ZmLOX4 overexpressing lines were significantly less inclined to the fungus and fumonisin contamination showing a stronger induction of 9- and 13-LOX genes along with an increased production of multiple 9-oxylipins and JA amounts (Ottaviani et al., 2026). The 9-lipoxygenase ZmLOX12 is also required to limit F. verticillioides infection in maize, indeed, lox12 loss of function mutants showed a wide fungal colonization of mesocotyls, stalks and kernels, a great amount of fumonisins and reduced levels of 12-OPDA, JA and JA-Ile and expression of JA-biosynthetic genes (Christensen et al., 2014). Contrasting findings were instead reported for the gene ZmLOX3 whose knock-out mutants were found more resistant to F. verticillioides colonization with a striking reduction of fumonisins (Gao et al., 2007; Battilani et al., 2018), but more susceptible to A. flavus and A. nidulans and aflatoxin production (Gao et al., 2009). Ogunola et al. (2017) observed that genes ZmLOX1/2, 5, 8, 9, 10 and 12 fell under previously published QTL linked to a measurable reduction of aflatoxin in maize grains in one or more mapping populations. Moreover, association mapping results revealed 28 SNPs associated with reduced aflatoxin levels that fell within or near nine of the ZmLOX genes (Ogunola et al., 2017).

The antimicrobial activity of oxylipins was also experienced directly on fungi. For instance, the deletion of three ppo genes encoding fatty acid oxygenases in A. nidulans altered spore ratios and mycotoxin sterigmatocystin production, reducing the expression of genes involved in the biosynthesis of the latter one. Additionally, the Delta ppo mutants were defective in colonization of peanut seeds and the exogenous application of seed oxylipins to Aspergillus cultures hampered fungal sporulation and mycotoxin accumulation (Tsitsigiannis and Keller, 2006). To verify whether plant LOX genes could rescue A. nidulans ppo gene functionality, ZmLOX3 was introduced into wild-type and Delta fungal strains. The expression of ZmLOX3 favored conidia and sterigmatocystin produced amount in both backgrounds (Brodhagen et al., 2008). Moreover, when peanut seeds were infected by A. nidulans Delta ppo mutants the expression of PnLOX2–3 was decreased suggesting a reciprocal oxylipin cross-talk in the Aspergillus-peanut pathosystem (Brodhagen et al., 2008). Similar findings were observed in A. ochraceus, where the AoloxA inhibition determined a different colony morphology, a delayed conidia formation, lower basal LOX activity, a limited content of 13-hydroperoxylinoleic acid and a considerable inhibition of ochratoxin A biosynthesis (Reverberi et al., 2010). Also, wheat seeds inoculated with the AoloxA mutant did not produce 9-hydroperoxylinoleic acid, known to be a crucial element in the host defense system, impairing the expression of the pathogenesis-related protein 1 (Reverberi et al., 2010). Comparable results were also found for A. flavus; indeed, silencing of the gene encoding a caleosin-like protein characterized by peroxygenase activity led to a reduced aflatoxin B₁ production in vitro, a down-regulation of aflR and aflD genes and a compromised maize seed colonization (Hanano et al., 2015). On the other hand, when caleosin/peroxygenase-derived oxylipins were applied to pxg deficient strains they reestablished the wild-type phenotype (Hanano et al., 2015). More recently, proteomics analysis highlighted the production of lipoxygenase-mediated hydroperoxy fatty acids during A. flavus–peanut interaction (Bhatnagar-Mathur et al., 2021).

Contrasting observations were instead reported for F. verticillioides, where deletion of Linoleate Diol Synthase 1 (LDS1), one of the main enzymes responsible for oxylipin generation, caused a better growth, enhanced conidia and fumonisin production as well as an improved maize cob infection of Fvlds1-deleted mutants compared to its wild-type counterpart (Scala et al., 2014). In further study, when maize kernels were infected with a F. verticillioides fumonisin-deficient mutant and its wild-type strain, an alteration of plant lipidome was reported in presence of fumonisins along with a higher production of salicylic acid and JA (Beccaccioli et al., 2021). The impact of oxylipins on mycotoxin production is also mediated through changes in plant transcriptome. In this regard, Lanubile et al. (2013) found that the response of maize kernels to fumonisin-producing and nonproducing strains of F. verticillioides was different, and a delayed and weakened activation of defense and oxidative stress-related genes was displayed by the fum1 mutant, presumably as a consequence of its reduced growth, compared to the wild-type strain. Unexpectedly, plant and fungal LOXs were up-regulated after fum1 mutant inoculation (Lanubile et al., 2013), suggesting the presence of possible alternative strategies in the association between the polyketide synthase and the LOX activities. The presence of different polyketide synthase isoforms or the production of mycotoxins by additional pathways could be explored in this regard. Taken together, the evidence suggests that oxylipins participate in multiple layers of plant–fungus interactions. In summary, plant-derived oxylipins generally act as modulators of fungal growth and mycotoxin biosynthesis, often through cross-talk with JA-dependent signaling pathways.

Recently, clustered regularly interspaced short palindromic repeats (CRISPR) and its associated Cas protein has been widely applied to further explore the role of the enzymes involved in the oxylipin pathway (Table 3). In this regard, Pathi et al. (2020) used Cas endonuclease technology approach to generate loss of function mutations in ZmLOX3. After Ustilago maydis inoculation, lox3 maize mutants showed reduced susceptibility and improved ROS accumulation implicating an enhanced defense response (Pathi et al., 2020). CRISPR/Cas9-induced knockout of OsLOX1 in rice determined diminished tolerance to drought stress associated with elevated levels of H₂O₂ and malondialdehyde, and reduced expression and activities of the antioxidant enzymes compared with the wild-type (Weng et al., 2025). The targeted knockout of barley gene isoforms LOXA and LOXC enhanced grain storability proved by significantly higher germination rates, reduced lipid peroxidation, and improved seedling growth (Zeng et al., 2025). In cucumber (Cucumis sativus L.), density of glandular trichomes was severely impaired by the site-directed mutagenesis of a CsLOX, bringing also to a lower accumulation of JA and OPDA and down-regulation of genes related to glandular trichome development (Yang et al., 2025).

Besides lipoxygenase genes, also OPR were subjected to editing by CRISPR/Cas9 system. Male sterility was obtained by mutations of OPR3 and OPR7 genes in Arabidopsis and rice, respectively (Pak et al., 2021). Moreover, Osopr7 knockout mutants showed reduced levels of endogenous JA and displayed an abnormal spikelet phenotype (You et al., 2019). Additionally, mutants for the COI-receptors that play a crucial role in the JA signaling pathway were generated in rice and maize, although with specific phenotypic effects (Table 3). It was observed that OsCOI1b gene regulates root growth and grain-size and performs similar activities with OsCOI1a in spikelet development, while OsCOI2 controls leaf senescence, male sterility, root growth, and grain size (Inagaki et al., 2023; Wang et al., 2023b). Moreover, all OsCOIs contributed to the resistance against the brown planthopper Nilaparvata lugens (Inagaki et al., 2023; Wang et al., 2023b). Similar findings were reported for ZmCOI2a and ZmCOI2b, where coi2a coi2b maize double mutant showed non-dehiscent anthers, late anther development and male sterility (Qi et al., 2022).

Even though the use of these edited plant materials has been liberalized in some countries, regulatory issues still remain in others. Recently, a window of opportunity has opened up in Europe. Indeed, the Council of the European Union and the European Parliament have reached a political agreement that maintains a dedicated category for New Genomic Techniques (NGT)-1 plants considered equivalent to conventionally bred varieties. This legislation can mark the beginning of a new era for European agriculture, allowing researchers and breeders to more efficiently translate scientific advances into sustainable agricultural solutions.

As agriculture persists in dealing with climate change challenges, there are several points that require additional investigations. This includes exploring the connection between abiotic stressors (like drought and flooding), expected to increase with global warning, and susceptibility to fungal diseases and mycotoxin production. Therefore, there is an urgent need to foster climate-resilient plants with improved resistance to biotic stress. A wide array of plant oxylipins is generated in response to multiple physiological processes and environmental acclimatization. Their production starts from the oxygenation of polyunsaturated fatty acids and proceeds with the support of several downstream oxylipin biosynthetic enzymes as CYP74 enzymes. The papers collected in this review have presented some of the recent developments in oxylipin biology with particular emphasis on those involved in environmental stress and mycotoxin contamination. Despite in the last years the numerous efforts of authors to better understand oxylipin enzymes, some important questions remain to be explored. Several technical limitations in oxylipin detection were encountered. The low abundance, extreme structural diversity and inherent instability of these compounds often deriving from complex plant matrices as well as the lack of standardized protocols and internal standards require highly sensitive LC-MS/MS instruments. Future research using advanced technologies such as the CRISPR/Cas system and further omics approaches should overcome these challenges and shed light on oxylipin signaling and cross-talk. The most promising genotypes showing favorable traits could be easily included in breeding pipelines through crosses and targeted assisted selection in order to obtain pre-breeding material. The development of next generation sequencing technologies and high throughput phenomics platform will allow a more effective exploitation of large-scale breeding populations. Moreover, the possibility of employing these molecules as potential biological agents and resistance inductors by spraying them on crops could also be explored. Further investigation into the practical application of oxylipins as biostimulants or resistance inducers could significantly contribute to sustainable crop protection.