The P. persica boasts a rich cultivation history spanning over 3000 years and is widely employed as a rootstock variety for peaches. It has demonstrated potent anti-aphid effects by inhibiting the fecundity and growth of GPAs (Verdugo et al., 2012; Wang et al., 2022). In China, peaches have been significantly affected by damages caused by M. persicae, a phloem-feeding insect that inflicts economic damage on a variety of crops (Xu, et al. 2021). The JA pathway plays a pivotal role in regulating plant resistance to insects (Wasternack and Hause, 2013). In maize, JA signaling modulates defense responses to herbivory through ZmMYC2s (Ma, et al. 2023). In tomato, PeaT1 and PeBL1 function as elicitors to activate JA-mediated defenses against aphids (Basit, et al. 2021). In soybean, JA-Ile plays a crucial role in the plant's defense against aphids (Yates-Stewart, et al. 2020). When herbivores cause local wounding, they trigger a rapid increase in newly synthesized JA. The constitutive occurrence of enzyme proteins involved in JA biosynthesis in all leaf tissues, similar to Arabidopsis (Stenzel et al., 2003), or in vascular bundles, as observed in tomato (Hause et al., 2000), can account for this immediate rise in JA levels within minutes (Mielke et al., 2011), Subsequently, starting at around 15 min after the initial damage, the transcriptional machinery responsible for the expression of LOX, AOS, AOC, OPR3, and JAZs is activated (Wasternack and Hause, 2013). In the case of peach tree (P. persica), we identified six LOX genes (LOX6, LOX2-1, LOX5-1, LOX21, LOX5, and LOX31), along with AOC1 and JMT, which are related to JA synthesis during GPA infestation. Our research has shown that these genes can be significantly induced during GPA infestation (Fig. 4B). This upregulation in the expression of genes involved in JA synthesis strongly suggests the involvement of the JA pathway in the peach plant’s response to GPA. Furthermore, the levels of JA in the plants are directly linked to the activity of these JA synthesis genes. Importantly, we observed a significant increase in JA levels during GPA infestation (Fig. 6C), and this process occurred continuously (Fig. 6D). These findings strongly indicate that the JA-mediated plant immunity continues to play a critical role in resisting GPA infestations in peach plants.
LncRNAs can serve as potential miRNA targets, thereby exerting a significant influence on miRNA activity level. In our study, we investigated the presence of GPA responsive lncRNAs that could effectively function as targets of JA-related genes and miRNAs in peach plants. We identified a total of 33 DELs as potential targets of 46 miRNAs specific to P. persica. Among these, two DEL–DEG pairs, circ16-miR482a and circ116-miR319a, were found to be associated with the JA pathway. In GPA-infested samples, we observed a significant upregulation in the expression of circ16 and circ116, while their predicted target miRNAs, miR482a and miR319a, exhibited a significant downregulation (Fig. 6A). Additionally, the target genes of these DEL–DEG pairs were significantly downregulated during GPA infestation in peach (as shown in Fig. 6B). These findings provide compelling evidence that these two DEL–DEG pairs of target genes/lncRNAs are involved in the JA pathway and play a crucial regulatory role in JA pathway during GPA infestation in peach plants.
In response to pest infestation, wounding, or pathogen attacks, the rapid synthesis of JA-Ile occurs within plant tissues. During the initial stages of this response, MYC2 serves as a central regulator, orchestrating the expression of early JA responsive genes. These genes encompass a wide range of JA responsive TFs responsible for regulation of specific branches of the JA signaling pathway. JA responsive TFs or genes are known to exhibit diverse and rapid responses to both biotic and abiotic stresses (Kazan and Manners, 2013; Wasternack and Hause, 2013) (Fig. 7). To enhance our comprehension of the architecture and regulation of the JA gene regulatory network, we conducted an enrichment analysis of DEGs and lncRNA-target genes. This analysis revealed a total of 23 GO terms related to the plant immune system process, with 3 of them ranking among the top 20 in terms of GO enrichment (Fig. 2A). Gene expression analysis further demonstrated that a majority of JA responsive genes, such as ERF1, LRR2, LRR5, LRR7, PR5, and MYC2-1, were significantly upregulated (Fig. 4D). These findings strongly suggest the activation of the JA pathway in peach trees as a response to GPA colonization. Additionally, through DEL–DEG pair interaction analysis, we identified five genes associated with JA responsive genes. Notably, LRR2 and LRR7 showed significant upregulation in the present study. Liao et al. found that lncRNAs affect the expression of miR482/2118 genes, which not only target LRRs but also impact other molecular mechanisms that influence plant resistance immunity (Shivaprasad et al., 2012; Liao et al., 2022). The miR319 family, on the other hand, represents one of the most ancient and conserved miRNA families in plants. In Arabidopsis, miR319 and TCPs are involved in JA biosynthesis (Shivaprasad et al., 2012), while in rice, virus infection reduces endogenous JA levels by inhibiting the expression of miR319 target genes, specifically TCPs (Zhang et al., 2016). In the present study, we identified three TCP genes (TCP4, TCP15, and TCP20) in peach tree that interact with the circRNA116–miR319a pair (Fig. 5B). In summary, these results collectively suggest that lncRNAs may play a significant role in altering JA metabolism in P. persica in response to GPA infestation (Fig. 7).
Aphids pose a significant challenge as major agricultural pests worldwide. For an extended period, the primary method employed to control aphids has been the use of broad-spectrum insecticides, with neonicotinoids and pyrethroids being among the most commonly utilized options. However, prolonged and extensive pesticide usage can lead to aphid resistance and environmental concerns. Recent research has shed light on the role of herbivore-induced plant volatiles (HIPVs) in safeguarding plants against herbivorous pests by activating the plants' defense system (Pickett and Pickett, 2016). Among the various HIPVs, terpenoids, a significant class, have been found to trigger repellent behavior in multiple pest species (Mithöfer, et al. 2012). JAs, which are also classified as HIPVs, have the remarkable ability to induce plants to produce toxic compounds. These compounds can directly disrupt the normal behavior of insects, compelling them to avoid infested plants altogether (Birkett, et al. 2000; Slesak, et al. 2001). Herein, we revealed that the endogenous JA content in peach trees exhibited continuous induction over a four-day period during GPA infestation (Fig. 6D). Furthermore, spray application of JA led to a significant reduction in the GPA population (Table 1). These findings in peach tree align with those of previous reports, suggesting that JA spray treatments induce resistance to economically important insect pests in crops such as wheat (El-Wakeil et al., 2010; Aslam et al., 2022). Collectively, our results provide compelling evidence that JA plays a pivotal role in inducing pest resistance in peach trees. This suggests that JA functions as a key resistance mechanism employed by peach trees to deter insect herbivores. JA holds significant potential as a sustainable and environmentally friendly biocontrol agent for effectively managing aphids in peach trees.