Depicting the battle between nectarine and Monilinia laxa: the fruit developmental stage dictates the effectiveness of the host defenses and the pathogen’s infection strategies

Abstract

Infections by the fungus Monilinia laxa, the main cause of brown rot in Europe, result in considerable losses of stone fruit. Herein, we present a comprehensive transcriptomic approach to unravel strategies deployed by nectarine fruit and M. laxa during their interaction. We used M. laxa-inoculated immature and mature fruit, which was resistant and susceptible to brown rot, respectively, to perform a dual RNA-Seq analysis. In immature fruit, host responses, pathogen biomass, and pathogen transcriptional activity peaked at 14–24 h post inoculation (hpi), at which point M. laxa appeared to switch its transcriptional response to either quiescence or death. Mature fruit experienced an exponential increase in host and pathogen activity beginning at 6 hpi. Functional analyses in both host and pathogen highlighted differences in stage-dependent strategies. For example, in immature fruit, M. laxa unsuccessfully employed carbohydrate-active enzymes (CAZymes) for penetration, which the fruit was able to combat with tightly regulated hormone responses and an oxidative burst that challenged the pathogen’s survival at later time points. In contrast, in mature fruit, M. laxa was more dependent on proteolytic effectors than CAZymes, and was able to invest in filamentous growth early during the interaction. Hormone analyses of mature fruit infected with M. laxa indicated that, while jasmonic acid activity was likely useful for defense, high ethylene activity may have promoted susceptibility through the induction of ripening processes. Lastly, we identified M. laxa genes that were highly induced in both quiescent and active infections and may serve as targets for control of brown rot.

Genome-Wide Association Study of Brown Rot (Monilinia spp.) Tolerance in Peach

“…Candidate gene analyses based on the 14 reliable significant QTNs reported in our study are in agreement with differentially expressed genes (DEG) reported by Balsells-Llauradó et al (2020) . Out of 146 candidate genes indicated in brown rot tolerance reported in our study ( Supplementary Table 3 ) 58 were differentially expressed in mature fruit of nectarine cultivar Venus 48 h after inoculation with M. laxa ( Balsells-Llauradó et al, 2020 ). Moreover, out of 25 candidate genes annotated in disease resistance response in our study ( Table 5 ), 8 were also reported by Balsells-Llauradó et al (2020) in mature fruit.…”

Temporal Patterns and Inter-Correlations among Physical and Antioxidant Attributes and Enzyme Activities of Apricot Fruit Inoculated with Monilinia laxa under Salicylic Acid and Methyl Jasmonate Treatments under Shelf-Life Conditions

“…Balsells-Llauradó et al [5] showed that M. laxa inoculation induced the early stage of JA biosynthesis, but a gene downregulation was detected in some cases of ripe fruit inoculated with M. laxa compared to control fruits [5]. The authors concluded that JA activity was likely useful as a plant defense signaling molecule [5]. This was in agreement with our results that MeJA increased the phenolic content, antioxidant capacity, and enzyme activities of fruits inoculated with M. laxa compared to control fruits (Figures 3 and 4).…”

“…However, some fungi can hijack the JA signaling pathway and the pathogen can cause disease [104]. Balsells-Llauradó et al [5] showed that M. laxa inoculation induced the early stage of JA biosynthesis, but a gene downregulation was detected in some cases of ripe fruit inoculated with M. laxa compared to control fruits [5]. The authors concluded that JA activity was likely useful as a plant defense signaling molecule [5].…”

“…MeJA was shown to reduce postharvest fungal diseases of fruits [34,35,39,[59][60][61], including Monilinia spp. in peach [35], sweet cherry [34,62], and in nectarine [5]. In a recent study [5], hormone and genetic analyses were also prepared for nectarine fruit infected with M. laxa, and the analyses confirmed that JA activity was likely useful for plant defense against M. laxa.…”

“…Honey is a serious fungal pathogen of stone fruit species, including apricot (Prunus armeniaca L.) [1][2][3][4][5]. The fungus can cause severe brown rot epidemics in most European stone fruit plantations [4][5][6][7][8][9][10][11]. Severe preand postharvest losses caused by M. laxa were reported in apricots [12][13][14].…”