Suppression of Cucumber Green Mottle Mosaic Virus Infection by Boron Application: From the Perspective of Nutrient Elements and Carbohydrates

Abstract

Cucumber green mottle mosaic virus (CGMMV) infection causes “blood flesh” symptoms in watermelon fruits, which severely reduces yield and edibleness. However, the growth of watermelon fruits is strongly associated with boron (B), a trace element for improving fruit quality. In this study, B-gradient hydroponic experiments (B concentration: 0, 2.86, and 5.72 mg·L–1 H3BO3) and foliar-spray experiments (B concentration: 30 and 300 mg·L–1 H3BO3) were performed. We found that the B-supplement could inhibit CGMMV infection and especially relieve “blood flesh” symptoms in watermelon fruits. The nutrient element, soluble sugar, and cell wall polysaccharide contents and their metabolism- and transport-related gene expressions were determined in leaves and fruits of the watermelons in B-gradient hydroponic and foliar-spray experiments. We found that the accumulation and metabolism of nutrients and carbohydrates in cells were disrupted by CGMMV infection; however, the B-supplement could restore and maintain their homeostasis. Additionally, we uncovered that NIP5;1 and SWEET4, induced by B-application with CGMMV infection, could majorly contribute to the resistance to CGMMV infection by regulating nutrient elements and carbohydrate homeostasis. These results provided a novel insight into the molecular mechanism of B-mediated CGMMV suppression and an efficient method of B-application for the improvement of watermelon quality after CGMMV infection.

Advances in molecular plant pathology, plant abiotic and biotic stress

“…Our laboratory has reported that leaf spraying with boron or growing in boron nutrient solution can relieve the symptoms of blood flesh disease caused by CGMMV infection in watermelon (Bi et al, 2022a). CGMMV infection affects the metabolism of carbohydrates in watermelon, and exogenous boron induces ClNIP5;1 and ClSWEET4 expression, restores and maintains their homeostasis (Bi et al, 2022a). In addition, boron can also induce watermelon resistance to CGMMV infection by regulating ROSrelated genes, such as ClCat, ClPrx and ClGST (Guo et al, 2022).…”

“…Investigations on the roles of trace elements in plant antiviral responses are still limited. Our previous studies have shown that boron can inhibit cucumber green mottle mosaic virus (CGMMV) infection in watermelon by regulating the expression levels of genes related to carbohydrate metabolism, hormone biosynthesis, cell wall catabolism and ROS burst (Bi et al, 2022a;Bi et al, 2022b;Guo et al, 2022). In this study, we demonstrated that foliar spraying of Fe inhibited PVY infection in N. tabacum, and analyzed the expression patterns of tobacco genes under four different treatments with or without PVY infection after spraying Fe or H 2 O at 1, 3, 9 days post inoculation (dpi) by full-length transcriptome and RNA-Seq analyses.…”

Transcriptomic and functional analyses reveal the molecular mechanisms underlying Fe-mediated tobacco resistance to potato virus Y infection

“…Similarly, the study on nutrient element-induced resistance to PVY infection in host plants is also conducive to improving crop yield from the perspective of PVY control. Our laboratory has reported that leaf spraying with boron or growing in boron nutrient solution can relieve the symptoms of blood flesh disease caused by CGMMV infection in watermelon ( Bi et al., 2022a ). CGMMV infection affects the metabolism of carbohydrates in watermelon, and exogenous boron induces ClNIP5;1 and ClSWEET4 expression, restores and maintains their homeostasis ( Bi et al., 2022a ).…”

“…Our laboratory has reported that leaf spraying with boron or growing in boron nutrient solution can relieve the symptoms of blood flesh disease caused by CGMMV infection in watermelon ( Bi et al., 2022a ). CGMMV infection affects the metabolism of carbohydrates in watermelon, and exogenous boron induces ClNIP5;1 and ClSWEET4 expression, restores and maintains their homeostasis ( Bi et al., 2022a ). In addition, boron can also induce watermelon resistance to CGMMV infection by regulating ROS-related genes, such as ClCat , ClPrx and ClGST ( Guo et al., 2022 ).…”

“…Investigations on the roles of trace elements in plant antiviral responses are still limited. Our previous studies have shown that boron can inhibit cucumber green mottle mosaic virus (CGMMV) infection in watermelon by regulating the expression levels of genes related to carbohydrate metabolism, hormone biosynthesis, cell wall catabolism and ROS burst ( Bi et al., 2022a ; Bi et al., 2022b ; Guo et al., 2022 ). In this study, we demonstrated that foliar spraying of Fe inhibited PVY infection in N. tabacum , and analyzed the expression patterns of tobacco genes under four different treatments with or without PVY infection after spraying Fe or H 2 O at 1, 3, 9 days post inoculation (dpi) by full-length transcriptome and RNA-Seq analyses.…”