Cell wall polysaccharide composition of grafted ‘Liberty’ watermelon with reduced incidence of hollow heart defect

Authors: TRANDEL, MARLEE - North Carolina State University; Johanningsmeier, Suzanne; SCHULTHEIS, JONATHAN - North Carolina State University; GUNTER, CHRIS - North Carolina State University; PERKINS-VEAZIE, PENELOPE - North Carolina State University

Submitted to: Frontiers in Plant Science
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 2/4/2021
Publication Date: 3/1/2021
Citation: Trandel, M.A., Johanningsmeier, S.D., Schultheis, J., Gunter, C., Perkins-Veazie, P. 2021. Cell wall polysaccharide composition of grafted ‘Liberty’ watermelon with reduced incidence of hollow heart defect. Frontiers in Plant Science. 12:623723. https://doi.org/10.3389/fpls.2021.623723.
DOI: https://doi.org/10.3389/fpls.2021.623723

Interpretive Summary: Seedless watermelon comprise 90-95% of the U.S. market and are prone to an internal fruit disorder known as hollow heart. Hollow heart is a serious internal defect characterized by a cavity or void air space in the center of the fruit that cannot be visually distinguished from normal fruit until cut. In this study, hollow heart defect was induced on demand by limiting pollen, and the effects of grafting were studied. Although fruits with hollow heart defect can cause load rejection in the marketplace, the fruits were not compromised in quality (e.g., firmness, pH, ºBrix and total sugar) or phytonutrient content. Grafting a susceptible triploid watermelon cultivar to an interspecific hybrid rootstock both increased tissue firmness and decreased the incidence of hollow heart defect. Thirty-four cell wall polysaccharide linkages were identified in watermelon for the first time, and arabinogalacturonan I was identified as a notable polysaccharide in watermelon cell walls. Interestingly, cell wall polysaccharide composition was not directly related to the increased firmness in fruit from grafted plants. Further research is needed to understand the mechanism by which grafting prevents hollow heart in watermelon. In the meantime, grafting onto interspecific hybrid rootstock can be implemented by growers to decrease the incidence of hollow heart defects.

Technical Abstract: Grafting watermelon scions to interspecific squash hybrids has been found to increase fruit firmness. Triploid (seedless) watermelon are prone to hollow heart (HH), an internal fruit disorder characterized by a crack in the placental tissue expanding to a cavity. Although watermelon with lower tissue firmness tend to have a higher HH incidence, associated differences in cell wall polysaccharide composition are unknown. Grafting “Liberty” watermelon to “Carnivor” (interspecific hybrid rootstock, C. moschata x C. maxima) reduced HH 39% and increased tissue firmness by 3 N. Fruit with and without severe HH from both grafted and non-grafted plants were analyzed to determine differences in cell wall polysaccharides associated with grafting and HH. Alcohol insoluble residues (AIR) were sequentially extracted from placental tissue to yield water soluble (WSF), carbonate soluble (CSF), alkali soluble (ASF), or unextractable (UNX) pectic fractions. The CSF was lower in fruit with HH (24.5%) compared to those without HH (27.1%). AIRs were also reduced, hydrolyzed, and acetylated for GC-MS analysis of monosaccharide composition, and a portion of each AIR was methylated prior to hydrolysis and acetylation to produce partially methylated alditol acetates for polysaccharide linkage assembly. No differences in degree of methylation or galacturonic and glucuronic acid concentrations were found. Glucose and galactose were in highest abundance at 75.9 and 82.4 ug-mg^-1 AIR, respectively, followed by xylose and arabinose (29.3 and 22.0 ug-mg^-1). Mannose was higher in fruit with HH (p < 0.05) and xylose was highest in fruit from grafted plants (p < 0.05). Mannose is primarily found in heteromannan and rhamnogalacturonan I side chains, while xylose is found in xylogalacturonan or heteroxylan. In watermelon, 34 carbohydrate linkages were identified with galactose, glucose, and arabinose linkages in highest abundance. This represents the most comprehensive polysaccharide linkage analysis to date for watermelon, including the identification of several new linkages. However, total pectin and cell wall composition data could not explain the increased tissue firmness observed in fruit from grafted plants. Nonetheless, grafting onto the interspecific hybrid rootstock decreased the incidence of HH and can be a useful method for growers using HH susceptible cultivars.