Application of a JA-Ile Biosynthesis Inhibitor to Methyl Jasmonate-Treated Strawberry Fruit Induces Upregulation of Specific MBW Complex-Related Genes and Accumulation of Proanthocyanidins

Abstract

Fleshy fruits are an important source of anthocyanins and proanthocyanidins (PAs), which protect plants against stress, and their consumption provides beneficial effects for human health. In strawberry fruit, the application of exogenous methyl jasmonate (MeJA) upregulates anthocyanin accumulation, although the relationship between the jasmonate pathway and anthocyanin and PA biosynthesis in fruits remains to be understood. Anthocyanin and PA accumulation is mainly regulated at the transcriptional level through R2R3-MYB and bHLH transcription factors in different plant species and organs. Here, the effect of jarin-1, a specific inhibitor of bioactive JA (jasmonoyl-isoleucine, JA-Ile) biosynthesis, on anthocyanin and PA accumulation was evaluated during strawberry (Fragaria × ananassa) fruit development using an in vitro ripening system for 48 h. Also, we observed the effects of MeJA and the application of jarin-1 to MeJA-treated fruits (MeJA + jarin-1 treatment). We assessed changes of expression levels for the JA-Ile and MeJA biosynthetic (FaJAR1.2 and FaJMT), JA signaling-related (FaMYC2 and FaJAZ1), MYB-bHLH-WD40 (MBW) complex-related (FabHLH3/33, FaMYB9/10/11, and repressor FaMYB1), and anthocyanin and PA biosynthetic (FaANS, FaUFGT, FaANR, and FaLAR) genes. In addition, the promoter region of MBW complex-related MYB genes was isolated and sequenced. We found a higher redness of strawberry fruit skin and anthocyanin content in MeJA-treated fruits with respect to jarin-1-treated ones concomitant with an upregulation of FaANS and FaUFGT genes. Inversely, the PA content was higher in jarin-1- and MeJA + jarin-1-treated than in MeJA-treated fruits. MeJA + jarin-1 treatment resulted in an upregulation of FaANR and associated transcription factors such as FabHLH33 and FaMYB9/11 along with FaJMT and FaJAR1.2. Finally, we found JA-responsive elements in the promoter regions of FaMYB1/9/10/11 genes. It is proposed that PA biosynthesis-related genes can be upregulated by the application of jarin-1 to MeJA-treated fruit, thus increasing PA accumulation in strawberry.

Priming of Defense Systems and Upregulation of MYC2 and JAZ1 Genes after Botrytis cinerea Inoculation in Methyl Jasmonate-Treated Strawberry Fruits

“…To understand to some extent, the physiological and molecular mechanism underlying the defense response of MeJA-treated fruit, we analyzed changes in lignin and anthocyanin contents and defense-related gene expression in the harvested treated fruit. According to literature, MeJA treatment not only upregulated defense-related gene expression but also promoted the secondary metabolism, particularly through the activation of the phenylpropanoid pathway [16,27,28]. In this sense, we observed that M3 treatment promoted both a higher level of anthocyanin and lignin accumulation with respect to control fruits at postharvest (0 hpi) ( Figure 2).…”

“…In the M1 treatment, the absence of correlation between the FaPOD27 and FaANR expression levels with the lignin and anthocyanin accumulation patterns at 0 hpi, respectively, may be due to the participation of other genes or gene family members belonging to the phenylpropanoid pathway that we did not analyze. It has been shown that MeJA treatment upregulates most of the phenylpropanoid pathway-related genes in F. chiloensis fruits [16], and the existence of several gene family members for anthocyanin biosynthesis has been evaluated in Fragaria species [27].…”

“…In the M1 treatment, the absence of correlation between the FaPOD27 and FaANR expression levels with the lignin and anthocyanin accumulation patterns at 0 hpi, respectively, may be due to the participation of other genes or gene family members belonging to the phenylpropanoid pathway that we did not analyze. It has been shown that MeJA treatment upregulates most of the phenylpropanoid pathway-related genes in F. chiloensis fruits [16], and the existence of several gene family members for anthocyanin biosynthesis has been evaluated in Fragaria species [27]. Concerning the analysis of the changes in defense-and jasmonate (JA) pathway-related gene expression, an overall upregulation in JA biosynthesis-(FaOPR3), PR-(FaBG1-2, FaBG2-2, FaCHI2-2, and FaCHI3-1), and PGIP-(FaPGIP1) related genes was observed in both the control and MeJA treatments in response to pathogen infection (48 h-post-inoculation) (Figure 4a,d,e,g-i).…”

Recent Advances in Hormonal Regulation and Cross-Talk during Non-Climacteric Fruit Development and Ripening

“…It was reported that proanthocyanidin (PA) accumulation in developing strawberry and grape berry showed a similar pattern to JA-Ile, occurring early in fruit development and decreasing as the fruit ripens [179,180]. We observed an increase in PA content by the application of a chemical inhibitor for the key JA-Ile biosynthetic enzyme JAR1, suggesting that the JA pathway could be related to PAs biosynthesis in strawberry fruit [181].…”

Fragaria Genus: Chemical Composition and Biological Activities

“…The composition of the fruits, although representing a characteristic of each species, can be influenced by a number of factors (as presented in Table 2), including the characteristics of the cultivar [21,27,29,31,34,39,[43][44][45][46], cultivation factors, and the environmental conditions [18,27,37,38,[47][48][49][50], ripening stage [28,29,35,51], or by biotechnological approaches [52][53][54]. For example, the variation in composition of a large number of Fragaria × ananassa Duch.…”