MdABCI17 acts as a positive regulator to enhance apple resistance to Botryosphaeria dothidea

doi:10.21203/rs.3.rs-4162250/v1

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MdABCI17 acts as a positive regulator to enhance apple resistance to Botryosphaeria dothidea

https://doi.org/10.21203/rs.3.rs-4162250/v1

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published 11 Sep, 2024

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The ATP-binding cassette (ABC) superfamily is involved in numerous complex biological processes. However, the understanding of ABCs in plant pathogen defense, particularly against Botryosphaeria dothidea (B. dothidea), remains limited. In this study, we identified MdABCI17 that plays a positive role in apple resistance to B. dothidea. Overexpression of MdABCI17 significantly enhanced the resistance of apple calli and fruits to B. dothidea. Our findings revealed that the jasmonic acid (JA) content and the expression of genes associated with JA biosynthesis and signal transduction were higher in stable MdABCI17-overexpressing apple calli than that of wild-type after inoculation with B. dothidea. Similar results were obtained for apple fruits with transient overexpression of MdABCI17. Our research indicates that MdABCI17 enhances apple resistance to B. dothidea through the JA signaling pathway. We further determined that MdABCI17 plays a crucial role in the apple’s response to JA signaling. Moreover, exogenous methyl jasmonate (MeJA) treatment significantly enhanced the effectiveness of MdABCI17 in boosting apple resistance to B. dothidea. We proposed a positive feedback regulatory loop between MdABCI17-mediated apple resistance to B. dothidea and JA signal. In summary, our study offers new insights into the role of ABC superfamily members in the control of plant disease resistance.

Apple

Botryosphaeria dothidea (B. dothidea)

MdABCI17

Pathogen defense

Pathogenic microorganisms substantially affect the growth and development of plants (Ma et al., 2021; Wang et al., 2022b). They can cause substantial losses to cash crops beyond affecting plant resource protection (Xu et al., 2022; Bellone et al., 2023; Wang et al., 2023). Thus, defending against microbial pathogens has consistently garnered attention. Reactive oxygen species (ROS) are crucial for plant immunity, affecting redox homeostasis, stress responses, and cell-to-cell signaling (Fichman et al., 2021; Iwashita et al., 2021; Mittler et al., 2022). The major forms of ROS in cells include hydrogen peroxide (H₂O₂), superoxide (O₂⁻), singlet oxygen (¹O₂), the hydroxyl radical (HO.), and various organic and inorganic peroxides (Lehmann et al., 2015; Waszczak et al., 2018; Sies and Jones, 2020). ROS play a crucial role in detecting stress, integrating various stress signals and activating plant defense mechanisms (Mittler et al., 2022). When plants experience substantial stress, active ROS are generated in the affected areas and then move to healthier parts, triggering adaptive responses that enhance the overall resistance and adaptability of plants. (Zandalinas et al., 2020a; Zandalinas et al., 2020b). This process is termed “systemic acquired acclimation” (Fichman and Mittler, 2021; Fichman et al., 2022). Numerous genes regulate disease resistance through ROS management. For instance, MebZIP3 and MebZIP5 regulate disease resistance through the biosynthesis of callose and the accumulation of H₂O₂ (Li et al., 2017), OsMESL regulates ROS-mediated broad-spectrum disease resistance in rice (Hu et al., 2021), TaAnn12 resists the invasion of pathogens by inducing the production and accumulation of ROS and callose in wheat (Shi et al., 2023), and CsbZIP90 suppresses the growth of Podosphaera xanthii by modulating ROS (Liu et al., 2024). In summary, ROS are considered vital components of the plant defense mechanism.

Jasmonic acid (JA) plays a pivotal role in plant growth, stress response, and defense mechanisms (Huang et al., 2017). As a lipid-derived plant hormone, JA and its derivatives, including its methyl ester (MeJA) and isoleucine conjugate (JA-Ile), are collectively referred to as jasmonates (Ruan et al., 2019; Wang et al., 2021a). In terms of plant disease resistance, JA plays a critical role in regulating defense responses against necrotrophic, biotrophic, and hemibiotrophic pathogens and viruses (Wasternack and Hause, 2013; Zhang et al., 2017; Wang et al., 2021a; Li et al., 2023). Numerous studies have indicated that the external application of JA, MeJA, or other JAs improves plant resistance to pathogens. For instance, exogenous JA treatment provided effective protection against Fusarium graminearum in wheat (Ameye et al., 2015), Botrytis cinerea in strawberry (Jia et al., 2016), green and blue molds in citrus (Moosa et al., 2019), Fusarium in Panax notoginseng (Liu et al., 2019), Magnaporthe oryzae in rice (Wang et al., 2021b), and Phytophthora infestans in potato (Arévalo-Marín et al., 2021). Molecular mechanisms through which JA mediates disease resistance in plants have been widely studied. Many JA signal-related genes, such as MdPIⅡ (Musetti et al., 2012), MdPR-4 (Bai et al., 2013), GhCOI1 (Seng et al., 2020), and multiple functional genes, including CATALASE2 (CAT2) (Yuan et al., 2017), GhPLP2 (Zhu et al., 2021), and GhJAZ2 (He et al., 2018), have been identified to be involved in the regulation of JA-mediated disease resistance in various plants. Thus, JA is crucial for plant disease resistance.

Apple is a vital cash crop in the horticulture industry, and extensive research has been conducted on pathogenic microorganisms affecting it. Botryosphaeria dothidea (B. dothidea) is a common pathogen causing apple ring rot, which poses substantial threat to the apple industry globally (Cui et al., 2015; Wang et al., 2018; Xin et al., 2023). B. dothidea is a widespread plant endophyte and a potential plant pathogen worldwide (Marsberg et al., 2017). The typical symptoms caused by B. dothidea include necrotic lesions that are round, oval, or irregular in shape and reddish-brown to dark brown in color, occasionally with concentric rings of dark and light brown (Dong et al., 2021). These lesions appear in the form of lenticels, graft unions, wounds, or warts on the bark of apple branches, particularly during fruit ripening and storage (Gu et al., 2020; Dong et al., 2021). Once detected, the disease spreads rapidly, leading to the rotting of branches and fruits, which can result in complete death within days. In addition to the symptomatic warts on infected branches, both the warty growths and the ring rot on fruits are referred to as apple ring rot. Recent studies have extensively explored the disease resistance pathway and molecular mechanisms underlying resistance to apple ring rot. MdERF11 (Wang et al., 2020), MdMYB73 (Gu et al., 2020), and MdPUB29 (Han et al., 2019) enhance the resistance of apple fruit to B. dothidea by regulating the salicylic acid (SA) pathway. In addition, ABA can induce the transcription of MYB30, increasing apple skin wax and thereby enhancing resistance to B. dothidea (Zhang et al., 2019). However, research on genes involved in the JA pathway’s regulation of apple ring rot resistance remains limited.

ATP-binding cassette (ABC) transporters constitute one of the largest superfamilies found in all organisms. These transporters use energy from adenosine triphosphate (ATP) to transport molecules across membranes (Beis, 2015). ABC transporter proteins are involved in plant growth and development, response to external environmental signals, and resistance to biotic and abiotic stresses (Kretzschmar et al., 2011; Geisler et al., 2017). Among the existing studies on ABC transporters, many have focused on multidrug resistance in bacteria and eukaryotic cells and a few have examined plant disease resistance; however, the role of ABC transporters in resistance to B. dothidea remains unclear. In our previous study, we identified MdABCI17, a tonoplast transporter involved in various ATP-driven transport processes (Xiang et al., 2024). In this study, we determined a positive feedback regulatory loop between MdABCI17-enhanced apple resistance to B. dothidea and the JA pathway. This finding not only broadens our understanding of the functional diversity of ABC transporter family genes but also suggests new strategies for controlling B. dothidea in plants.

Plant materials and treatments

Apple fruits are mature ‘Starking apple’ from Tianshui, Gansu Province. Apple calli were cultured on Murashige and Skoog (MS) medium. For JA treatment, calli were cultured on MS medium containing 50 µM or 100 µM JA for 15 days.

Stable transformation of apple calli, instant injection of apple fruits, and real-time quantitative PCR (RT-qPCR) analysis

The RT-qPCR analysis, stable transformation of apple calli, and the instant injection experiment of apple fruit refer to the previously described (Xiang et al., 2024). The primers are listed in supplemental table 1.

Pathogen infection assays

The incubation of Botryosphaeria dothidea (B. dothidea) as well as the pathogen infection assays of apple calli and fruits were performed according to previously reported (Zhao et al., 2024).

Determination of relative conductivity, malondialdehyde (MDA), reactive oxygen species (ROS), and phytohormones

Relative conductivity, MDA, and ROS (SOD, OFR and H₂O₂) were determined according to previously reported (Wang et al., 2022b). The levels of ABA, SA and JA were measured using the ABA (MM-088701), SA (MM-3372201), and JA (MM-013801) ELISA kit (Meimian Industrial Co., Ltd., China).

Statistical analyses

All experiments were performed using three biological replicates with three technical repetitions each. Error bars represent SD of these three biological replicates unless otherwise indicated. Asterisks indicate statistically significant differences, as determined using a Student’s t-test (*, 0.01 < P < 0.05; **, P < 0.01; n.s., no significant difference).

Overexpression of MdABCI17 significantly improves the resistance of apple calli to Botryosphaeria dothidea (B. dothidea)

To elucidate the role of MdABCI17 in resistance to B. dothidea, we generated stable MdABCI17-overexpressing apple calli (MdABCI17-OVX1/2) and subjected them to B. dothidea infection using the wild-type (WT) as a control (Fig. 1A-C). Following 6 days of B. dothidea infection, we observed smaller fungal plaque areas in MdABCI17-OVXs calli than in WT (Fig. 1A and B). Previous studies have reported the production of Reactive oxygen species (ROS) during plant immune responses (Jablonska and Tawfik, 2021; Mittler et al., 2022). Thus, we assessed the activity of superoxide dismutase (SOD) and measured the levels of oxygen free radicals (OFRs) and hydrogen peroxide (H₂O₂) in the infected calli (Fig. 1D-F). Our findings revealed lower SOD activity in MdABCI17-OVXs than in the control (Fig. 1D), along with higher levels of H₂O₂ and OFR in MdABCI17-OVXs than in the WT control (Fig. 1E and F). Overall, these results suggest that the overexpression of MdABCI17 significantly enhances the resistance of apple calli to B. dothidea.

Abscisic acid (ABA), salicylic acid (SA), and jasmonic acid (JA) play crucial roles in plant defense and immunity (Han and Kahmann, 2019). To investigate the B. dothidea resistance mechanism of MdABCI17, we simultaneously examined the involvement of the three pathways—ABA, SA, and JA—in disease resistance. Thus, we assessed the content and transcription of defense-related genes associated with ABA, SA, and JA synthesis (Fig. 1G-L). Our findings revealed an increase in JA content and the transcription of JA-responsive genes (MdLOX3.1, MdPR-4, and MdMdPI Ⅱ) compared with the WT control (Fig. 1I and L). However, no significant changes were observed in the content of SA and ABA (Fig. 1G and H) or in the transcription of SA-responsive genes (MdEDS1, MdNPR1, and MdPR1) and ABA-responsive genes (MdRAB18, MdPR-4, MdRD29A, and MdRD29B), except for the upregulation of the SA signal-related gene MdPR5 (Fig. 1J and K). In summary, these results indicate that the overexpression of MdABCI17 significantly boosts the resistance of apple calli to B. dothidea by increasing JA content and enhancing JA signal transmission.

MdABCI17 positively regulates the resistance of apple fruit to B. dothidea

Due to the prolonged juvenile period (six to eight years) in apple plants, which are perennial woody plants, obtaining stable transgenic fruits poses a significant challenge before flowering and fruit set. Therefore, we opted for direct injection of apple fruit to further validate MdABCI17’s function in enhancing apple fruit resistance to B. dothidea (Figs. 2 and 3). Initially, we utilized MdABCI17-IL60 vectors to overexpress MdABCI17 in apple fruits, with an empty vector IL60 serving as the control (Fig. 2C). As depicted in Fig. 2, we observed smaller fungal plaque areas (Fig. 2A and B), reduced SOD activity (Fig. 2D), elevated levels of OFR content (Fig. 2E) and H₂O₂ content (Fig. 2F), increased JA content (Fig. 2I), and enhanced expression of multiple genes associated with JA biosynthesis and response (Fig. 2L) in MdABCI17-IL60 apple fruits compared with the control. Conversely, ABA and SA content (Fig. 2G and 2H) as well as the expression of multiple genes related to ABA and SA biosynthesis and response (Fig. 2J and 2K) did not exhibit significant differences between MdABCI17-IL60 apple fruits and the control. These findings indicate that the overexpression of MdABCI17 significantly enhanced the resistance of apple fruits to B. dothidea by enhancing JA content and JA signal transduction.

We employed MdABCI17-TRV vectors to suppress MdABCI17 in apple fruits, with the empty vector TRV serving as the control (Fig. 3A and 3C). As shown in Fig. 3, we observed larger fungal plaque areas (Fig. 3A and 3B), increased SOD activity (Fig. 3D), decreased OFR content (Fig. 3E) and H₂O₂ content (Fig. 3F), diminished JA content (Fig. 3I), and reduced expression of multiple genes associated with JA biosynthesis and response (Fig. 3L) in MdABCI17-TRV apple fruits compared with the control. Unlike the changes observed in the aforementioned indicators, ABA and SA content (Fig. 3G and 3H) as well as the expression of multiple genes related to ABA and SA biosynthesis and response (Fig. 3J and 3K) did not differ significantly between MdABCI17-TRV apple fruits and the control. These results suggest that the suppression of MdABCI17 significantly diminishes the resistance of apple fruits to B. dothidea by reducing JA content and JA signal transduction. In summary, MdABCI17 acts as a positive regulator in enhancing apple fruit resistance to B. dothidea.

Overexpression of MdABCI17 significantly reduced the sensitivity of apple calli to JA

We established that MdABCI17 enhances apple resistance to B. dothidea by promoting JA biosynthesis and signal transduction (Figs. 1–3). Therefore, we delved deeper into the response of MdABCI17 to JA signaling. We treated MdABCI17-overexpressing calli (MdABCI17-OVX1/2) and WT calli with exogenous 50 µM and 100 µM methyl jasmonate (MeJA), respectively, and those treated with sterile water served as a control (Fig. 4). After 15 days of treatment, the growth status and fresh weight of WT calli in the control group were significantly lower than that in the groups treated with 50 µM or 100 µM MeJA (Fig. 4A and B). Similarly, the MdABCI17-overexpressing calli (MdABCI17-OVX1/2) under 50 µM or 100 µM MeJA treatment exhibited similar results compared with the control (Fig. 4A and B). However, the growth status and fresh weight of the MdABCI17-overexpressing calli (MdABCI17-OVX1/2) were significantly higher than those of WT under both MeJA treatments (Fig. 4A and B). Additionally, relative conductivity and malondialdehyde (MDA) levels, indicators of stress, were significantly lower in the MdABCI17-overexpressing calli (MdABCI17-OVX1/2) than in WT under 50 µM or 100 µM MeJA treatment (Fig. 4C and D). Furthermore, we examined the expression of genes related to JA biosynthesis and signal transduction. The RT-qPCR results revealed that under 50 µM or 100 µM MeJA treatment, the expression of MdAOC, MdAOS, and MdLOX3.1 in the MdABCI17-overexpressing calli (MdABCI17-OVX1/2) was significantly higher than in WT (Fig. 4E-F). In summary, these findings suggest that MdABCI17 plays a significant role in the apple response to JA.

MeJA treatment enhances the resistance of MdABCI17-overexpressing apple calli to B. dothidea

To further elucidate the impact of JA on enhancing apple resistance to B. dothidea via MdABCI17, we applied exogenous MeJA to MdABCI17-overexpressing calli (MdABCI17-OVX1/2) inoculated with B. dothidea, with WT calli treated with exogenous MeJA as a control. After 15 days of treatment, the fungal plaque areas of the MdABCI17-overexpressing calli (MdABCI17-OVX1/2) in the control group and the 100-µM MeJA treatment group were significantly smaller than those of the WT (Fig. 5A and B). Moreover, after MeJA treatment, the fungal plaque areas of the MdABCI17-overexpressing calli (MdABCI17-OVX1/2) were even smaller than those of the control (Fig. 5A and C). We further determined changes in ROS (SOD, OFR, and H₂O₂) and found lower SOD activity and higher levels of OFR and H₂O₂ in the MeJA-treated group (Fig. 5D-F). Overall, these results indicate that exogenous MeJA treatment significantly enhances the role of MdABCI17 in improving apple resistance to B. dothidea.

Pathogenic microorganisms pose substantial threats to plant growth, development, and survival. B. dothidea is a common fungus causing apple ring rot, resulting in substantial losses to the apple industry year-round (Tang et al., 2012). Therefore, research on B. dothidea, the pathogen responsible for apple ring rot, is warranted. In this study, we determined that the ABC transporter MdABCI17 enhanced the resistance of apple fruit to B. dothidea through the JA pathways. These findings demonstrate that MdABCI17 plays a crucial role in the regulation of plant resistance to pathogenic microorganisms.

The ABC transporter superfamily is widespread across organisms, serving diverse functions and occupying an important position. This superfamily consists of seven subfamilies, namely ABCA, ABCB, ABCC, ABCD, ABCE, ABCF, ABCG, and ABCI (Rea, 2007; Beis, 2015). Among them, the composition of members in the subfamily ABCI is relatively specific and complex. However, few studies have examined the functions of members in this subfamily. In our previous study, we isolated an ABC transporter, MdABCI17, from the vacuolar membrane protein belonging to the ABCI subfamily (Xiang et al., 2022; Xiang et al., 2024). The homologous gene of MdABCI17 in Arabidopsis is AtSTAR1 (AT1G67940) (Xiang et al., 2024). A study reported that the knockout of AtSTAR1 led to increased aluminum sensitivity and early flowering in Arabidopsis thaliana (Huang et al., 2010). Another study reported that AtSTAR1 is involved in the regulation of the phosphate deficiency response in Arabidopsis thaliana (Belal et al., 2015). Our recent study demonstrated that MdABCI17 is a positive regulator of anthocyanins in apples (Xiang et al., 2024). All the aforementioned studies indicated that MdABCI17 and its homologous genes are involved in abiotic stress and quality of plants. However, no study has examined the role of MdABCI17 in disease resistance. In this study, we determined that MdABCI17 enhanced apple resistance to B. dothidea. The functional identification of apple MdABCI17 and its homologous genes indicates the broad and complex involvement of ABC superfamily members in regulating plant life.

Microbial pathogens are classified into various types, including necrotrophic, biotrophic, and hemibiotrophic. B. dothidea is a biotrophic fungus that thrives by parasitizing live host cells for growth and reproduction (Bonito et al., 2010; Tang et al., 2012; Pel and Pieterse, 2013). Fruit and branch cankers caused by B. dothidea have led to substantial losses in both domestic and foreign cash crops, such as grapes, apples, and pistachios (Ma et al., 2001; Li et al., 2010; Tang et al., 2012). To prevent and control microbial pathogen diseases, common agricultural practices include adjusting fertilization, applying various types of pesticides, and bagging individual fruits. However, advancements in molecular biology have led to the discovery of many disease resistance mechanisms in plants. Our study demonstrated that MdABCI17 enhanced apple resistance to B. dothidea and significantly reduced the spread of canker plaques on apple calli and fruits (Fig. 1A-B, Fig. 2A-B, Fig. 3A-B, and Fig. 5A-B). Typically, after being infected by a pathogen, a plant rapidly develops resistance at the infected site (local induced resistance) and develops long-lasting resistance in healthy areas (systemic acquired resistance, SAR) (Klessig et al., 2018; Shine et al., 2019). This resistance development process in plants is complex, usually involving various resistance-related signals and substances, such as calcium (Ca²⁺), membrane potential, ROS, callose, hormones, and antioxidants (Couto and Zipfel, 2016; Fichman and Mittler, 2020; 2021; Cerqueira et al., 2023; Li and Ahammed, 2023). Thus, after observing the disease resistance mechanism of MdABCI17 against B. dothidea (Fig. 1A and B, Fig. 2A and B, Fig. 3A and B), we further explored the specific disease resistance pathways involved.

ROS play a crucial role in plant disease resistance (Sahu et al., 2022). Many disease resistance processes involve changes in ROS levels. The FliC protein elicited rapid ROS accumulation in plants expressing extracellular plant ferredoxin-like protein (Su et al., 2014). In Arabidopsis thaliana, the smd3b-1 mutant led to a reduction in early ROS production triggered by flagellin (flg22) and an increase in secondary ROS following Pseudomonas syringae pv. tomato (Pst) infection (Golisz et al., 2021). The knockout of SlMAPK3 in tomato enhanced resistance to Botrytis cinerea accompanied by ROS accumulation (Zhang et al., 2018). Furthermore, the loss of ATPb function in rice enhanced the resistance of Pijx to Magnaporthe oryzae by causing an increase in ROS production (Xiao et al., 2023). In addition, ROS can be directly regulated by resistant-related genes. The rice heavy-metal transporter OsNRAMP1 enhances broad-spectrum resistance against bacterial and fungal pathogens by modulating metal ion and ROS homeostasis (Chu et al., 2022). In wheat, TaAnn12 resisted pathogen invasion by inducing the production and accumulation of ROS and callose (Shi et al., 2023). Furthermore, in cucumbers, CsbZIP90 negatively regulated the expression of ROS-related genes and activities of ROS-related kinases to enhance resistance to Podosphaera xanthii (Liu et al., 2024). In our study, we observed a substantial change in ROS levels. We found that the total ROS content increased in MdABCI17-overexpressing apple calli (Fig. 1D-F and Fig. 5D-F) and fruits (Fig. 2D-F). This finding indicates the crucial role of ROS in MdABCI17-mediated resistance to B. dothidea. Some studies have demonstrated that the functions of ABC transporters in plants are associated with ROS. For instance, OsABCI7 interacts with HIGH CHLOROPHYLL FLUORESCENCE222 (OsHCF222) to regulate cellular ROS homeostasis for thylakoid membrane stability (He et al., 2020). ABC transporters (ABCB25 and ABCC14) in Beckmannia syzigachne contribute to mesosulfuron-methyl resistance, suggesting that ROS burst is involved in the overexpression of ABC transporter genes in these weeds (Wang et al., 2022a). Overall, the generation and propagation of ROS are complex processes. The mechanism underlying MdABCI17-mediated production and transmission of ROS is yet to be determined. In addition, whether signaling molecules other than ROS change during this disease resistance process remains unclear because stress response and resistance acquisition typically involve multiple signal changes, including ROS, calcium, and electrical signals (Shao et al., 2020; Szechynska-Hebda et al., 2022).

Phytohormones ABA, JA and SA play an important role in plant disease resistance (Han and Kahmann, 2019). ABA can induce stomatal closure to prevent the invasion of pathogenic microorganisms and activate various defense-related genes (ABR1, RAB18, and RD22), enhancing plant resistance (Choi and Hwang, 2011; Lee and Luan, 2012; Bharath et al., 2021; Singh et al., 2024). SA effectively improves the resistance of plants to many pathogenic microorganisms, including Pseudomonas syringae (Chen et al., 2022), Verticillium dahliae (Tang et al., 2019)d dothidea (Gu et al., 2020). JA is typically associated with insect resistance (Jing et al., 2021) and positively regulates plant resistance to some pathogenic microorganisms, including Xanthomonas oryzae pv.oryzae (Hui et al., 2019) and Colletotrichum camelliae (Lin et al., 2020). To further explore the disease resistance pathway of MdABCI17 against B. dothidea, we detected the content and expression of defense-related genes in response to ABA, SA, and JA in MdABCI17 transgenic apple calli and fruits after inoculation with B. dothidea. Our findings revealed significant changes in JA content and JA-responsive gene expression, whereas ABA and SA contents and their associated resistant genes demonstrated no substantial changes (Fig. 1G-L, Fig. 2G-L, and Fig. 3G-L). These results indicate that MdABCI17 resisted B. dothidea through the JA pathway. However, we observed that the SA signal-related gene MdPR-4 significantly increased in stable MdABCI17-overexpressing apple calli and decreased in transient MdABCI17-supressing apple fruits (Fig. 1K and 3K). Many studies have indicated that hormones involved in plant disease resistance pathways do not act independently (Robert-Seilaniantz et al., 2011; Long et al., 2019; Wang et al., 2021b). For instance, the inhibition of SA by JA is beneficial for the resistance of citrus to canker disease (Long et al., 2019). SIMAPK3 positively affects tomato resistance to B. cinerea through SA and JA defense signaling pathways (Zhang et al., 2018). SA notably boosts the expression of MeJA-induced PDF1.2 in the absence of AtOZF1 (Singh and Nandi, 2022). Moreover, MdPR-4 protein can inhibit hyphal growth, and its expression is regulated by both SA and JA signaling pathways (Bai et al., 2013). Our findings are similar to those of a previous study indicating that MeJA treatment significantly upregulated PR-4, PR5, and PEROXIDASE (PEROX) in wheat to defend against Fusarium graminearum (Ameye et al., 2015). MdPR-4 expression did not change in transient MdABCI17-overexpressing apple fruits, possibly due to low transient expression levels. Thus, our results combined with those of previous studies indicate that MdABCI17 may be regulated by JA signaling, enhancing the resistance of apple to ring rot. In addition, we determined that MdABCI17 responds to MeJA (Fig. 4), and MeJA treatment significantly enhanced the resistance of stable MdABCI17-overexpressing apple calli to B. dothidea (Fig. 5A-C). Many studies have reported that exogenous JA treatment effectively enhanced the resistance of plants to Fusarium (Ameye et al., 2015; Liu et al., 2019), B. cinerea (Jia et al., 2016), and Phytophthora (Arévalo-Marín et al., 2021). Taken together, these findings indicate that MdABCI17 resists B. dothidea through the JA pathway.

Secondary metabolites are considered an essential component of the defense mechanism in organisms (Akbar et al., 2023). Anthocyanins, a class of flavonoids, play a defensive role against a range of biotic stresses (Zhao et al., 2021). Overexpression of GhPAP1D in cotton increased anthocyanin accumulation and enhanced resistance to both bollworm and spite mite (Li et al., 2019). The anthocyanin-more (am) mutant exhibit higher disease resistance to Sclerotinia sclerotiorum (Liu et al., 2020). Citrus fruits infected by Penicillium digitatum (Pd) show high anthocyanin accumulation, and exogenous anthocyanin treatment can improve the disease resistance of citrus fruits to Pd (Lin et al., 2021). Combining these studies with our previous research, we found that MdABCI17 positively regulates the accumulation of anthocyanins in apple (Xiang et al., 2024). Thus, we speculate that MdABCI17 promotes anthocyanin accumulation, thereby potentially enhancing apple disease resistance.

Generally, the genes that respond to B. dothidea signals are found on the cell surface, such as the plasma membrane and cell wall. For instance, most thaumatin-like proteins in hickory (Carya cathayensis) were located in the plasma membrane following B. dothidea inoculation (Li et al., 2022). PnSN1, located in the cell wall, plays a crucial role in the resistance of Panax notoginseng to B. dothidea (Qiu et al., 2020). Our previous study revealed that MdABCI17 is localized in the vacuolar membrane, not on the cell surface. Thus, we speculate that MdABCI17 does not directly respond to B. dothidea signals. In this study, we found that ROS and JA levels changed significantly during MdABCI17-mediated enhancement of apple resistance to B. dothidea. Thus, we speculate that ROS or JA transmit signals from the outer plasma membrane or cell wall to the vacuole membrane, thus activating MdABCI17 to participate in apple resistance to B. dothidea. ROS are secondary messengers that play an important role in intracellular signaling (Marcec et al., 2019). JA can facilitate remote signal transduction under stress. JA serves as a mobile wound signal, regulated by two phloem-expressed, plasma membrane-localized jasmonate transporters, AtJAT3 and AtJAT4 (Li et al., 2020). These half-molecule ABC transporters, AtJAT3 and AtJAT4, form homo- or heterodimers that mediate cell-cell JA transport, enabling long-distance JA signal transmission in a self-propagating manner (Li et al., 2021).

Based on our finding, we summarize the mechanism through which MdABCI17 regulates apple resistance to B. dothidea (Fig. 6). MdABCI17 is significantly induced by B. dothidea infection and can directly increase the JA content by promoting the expression of JA biosynthesis-related genes (MdAOC, MdAOS, and MdLOX3.1). Subsequently, JA stimulates the expression of the JA signaling-related genes (MdPR-4 and MdPI Ⅱ), increases ROS levels (SOD, OFR, and H₂O₂), and enhances resistance to B. dothidea. In addition, with the increase in JA content and signal transduction, JA enhances the role of ABCI17 in improving apple resistance to B. dothidea. Our research not only expands the understanding of the functional diversity of the ABCI family and the hormone JA in combating apple ring rot but also offers new strategies for bolstering plant resistance to B. dothidea.

Acknowledgements

This work was supported by grants from the Key Research and Development Program of Shandong Province (2023CXGC010709), the National Key Research and Development Program of China (2023YFD2301000, 2022YFD2100102), National Natural Science Foundation of China (32122080, 32302616) and Shandong Province (ZR2023QC032).

Author contributions

D.G.H. and Q.S. conceived and designed the study. Y.X., Y.W.Z., C.K.W., and C.N.M. performed the experiments. Y.X., J.J.W., and X.B. analyzed the data. Y.X., Q.S., and D.G.H. wrote the paper. All authors discussed the results and commented on the manuscript.

Availability of data and materials

All data generated or analyzed during this study are provided in this published article and its supplementary data files.

Conﬂict of interest

The authors declare that they have no conﬂict of interest.

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MdABCI17 acts as a positive regulator to enhance apple resistance to Botryosphaeria dothidea

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