A novel strategy for improving watermelon resistance to cucumber green mottle mosaic virus by exogenous boron application

Abstract

The molecular mode controlling cucumber green mottle mosaic virus (CGMMV)‐induced watermelon blood flesh disease (WBFD) is largely unknown. In this study, we have found that application of exogenous boron suppressed CGMMV infection in watermelon fruit and alleviated WBFD symptoms. Our transcriptome analysis showed that the most up‐regulated differentially expressed genes (DEGs) were associated with polyamine and auxin biosynthesis, abscisic acid catabolism, defence‐related pathways, cell wall modification, and energy and secondary metabolism, while the down‐regulated DEGs were mostly involved in ethylene biosynthesis, cell wall catabolism, and plasma membrane functions. Our virus‐induced gene silencing results showed that silencing of SPDS expression in watermelon resulted in a higher putrescine content and an inhibited CGMMV infection correlating with no WBFD symptoms. SBT and TUBB1 were also required for CGMMV infection. In contrast, silencing of XTH23 and PE/PEI7 (low‐level lignin, cellulose and pectin) and ATPS1 (low‐level glutathione) promoted CGMMV accumulation. Furthermore, RAP2‐3 , MYB6 , WRKY12 , H2A , and DnaJ11 are likely to participate in host antiviral resistance. In addition, a higher (spermidine + spermine):putrescine ratio, malondialdehyde content, and lactic acid content were responsible for fruit decay and acidification. Our results provide new knowledge on the roles of boron in watermelon resistance to CGMMV‐induced WBFD. This new knowledge can be used to design better control methods for CGMMV in the field and to breed CGMMV resistant watermelon and other cucurbit crops.

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

“…Here, we measured the concentrations of 10 essential nutrient elements (N, P, K, Ca, Mg, S, Fe, Zn, Cu, and B) and expressions of main genes related to nutrient element absorption and transport in watermelon leaves and fruits from different treatments (Figure ). In this study, the results of these nutrient element contents were similar or consistent with those in previous reports. − The contents of most nutrient elements and the expressions of their absorption and transport genes (i.e., NIP2;1 , NIP5;1 , BOR2 , NRT1.5 , KUP11 , and VIT1 ) were strongly associated with B treatment and/or CGMMV infection in watermelon leaves and fruits (Figure , Tables S3 and S4), which demonstrated that the nutrient element homeostasis in watermelon was indeed affected by B element and CGMMV infection.…”

“…In watermelon fruits, genes related to cell wall biosynthesis (i.e., API , CSLD3 , CESA4 , COBRA ) and cell wall modification (i.e., XTHs , PE/PEIs , and EXLA1 ) were upregulated, and wall catabolism-associated genes (i.e., BG12 and Pel13 ) were downregulated by B-application under CGMMV stress, which were consistent with the expressions of cell wall biosynthesis genes ( CesA and COBL7 ) and pectin degradation genes ( PG and PL1 ) in watermelon fruits by four treatments (Figure C). In addition, silencing XTH23 and PE/PEI7 caused more severe WBFD with lower levels of lignin, cellulose, hemicellulose, soluble pectin, and propectin in watermelon flesh . In this study, watermelon fruits in the C + H group were severely infected by CGMMV, and the contents of lignin, cellulose, hemicellulose, and pectin were also decreased (Figure B).…”

“…14 In a recent study of improving watermelon resistance to CGMMV by exogenous B-application, B content in watermelon flesh was decreased by CGMMV infection and increased by spraying boric acid solution at 30 and 45 DAP. 39 In this study, the most serious viral symptoms, the highest CGMMV accumulation, and the lowest B content were obtained in the seedling leaves with the B-deprived treatment in hydroponics experiments and the watermelon fruits treated by spraying H 2 O in foliar-spray experiments under CGMMV infection (Figures 1A−C,H−I and 2A,B), suggesting that B was associated with the resistance of watermelons to CGMMV infection. A previous study has shown that upregulation of NIP5;1 expression facilitates efficient B uptake.…”

“…As an essential trace element required for complex physiological processes in plants, B-sufficiency can alleviate the symptoms of TMV and Belladonna mottle virus infection in bean and tobacco plants, respectively, , and the symptoms resulting from B-deficiency are similar to those of GLMD caused by grapevine Pinot gris virus infection in grapevine plants . In a recent study of improving watermelon resistance to CGMMV by exogenous B-application, B content in watermelon flesh was decreased by CGMMV infection and increased by spraying boric acid solution at 30 and 45 DAP . In this study, the most serious viral symptoms, the highest CGMMV accumulation, and the lowest B content were obtained in the seedling leaves with the B-deprived treatment in hydroponics experiments and the watermelon fruits treated by spraying H 2 O in foliar-spray experiments under CGMMV infection (Figures A–C,H–I and A,B), suggesting that B was associated with the resistance of watermelons to CGMMV infection.…”

“…18 In this study, these cell wall components, as well as soluble sugar and B, showed the lowest contents in fruits of CGMMV-infected watermelon plants, which were retrieved to a large extent by B-application (Figures 2B, 3B, and 4B). In watermelon fruits, genes related to cell wall biosynthesis (i.e., API, CSLD3, CESA4, COBRA) and cell wall modification (i.e., XTHs, PE/PEIs, and EXLA1) were upregulated, and wall catabolism-associated genes (i.e., BG12 and Pel13) were downregulated by B-application under CGMMV stress, 39 which were consistent with the expressions of cell wall biosynthesis genes (CesA and COBL7) and pectin degradation genes (PG and PL1) in watermelon fruits by four treatments (Figure 4C). In addition, silencing XTH23 and PE/ PEI7 caused more severe WBFD with lower levels of lignin, cellulose, hemicellulose, soluble pectin, and propectin in watermelon flesh.…”