Reduction of Fruit Load Affects Early Fruit Growth in Apple by Enhancing Carbohydrate Availability, Altering the Expression of Cell Production-related Genes, and Increasing Cell Production

Abstract

<jats:p>Carbohydrate availability is a key factor determining fruit growth in apple (<jats:italic>Malus</jats:italic> ×<jats:italic>domestica</jats:italic>) and other fruits. However, the molecular mechanisms regulating fleshy fruit growth in response to changes in carbohydrate availability are not well understood. In this study, carbohydrate availability was manipulated by reducing fruit load, and its effects on apple fruit growth, cell production and expansion, and the expression of genes associated with these processes was investigated. Reduction of fruit load during early fruit development led to a rapid increase in early fruit growth. The increase in fruit growth was associated with a transient increase in sorbitol and fructose concentrations and altered expression of <jats:italic>sorbitol dehydrogenase</jats:italic> and <jats:italic>sucrose synthase</jats:italic> genes. Increase in early fruit growth was mediated primarily by an increase in cell production. The <jats:italic>aintegumenta</jats:italic> gene, <jats:italic>MdANT1</jats:italic>, an AP2-domain transcription factor associated with the regulation of cell production and fruit growth, displayed an increase in expression by up to 5-fold during early fruit development in response to the reduction in fruit load. Additionally, multiple cell cycle genes positively associated with cell production such as the cyclins, <jats:italic>MdCYCA2;1</jats:italic>, <jats:italic>MdCYCA2;3</jats:italic>, <jats:italic>MdCYCB1;1,</jats:italic> and <jats:italic>MdCYCB2;2,</jats:italic> and the B-type <jats:italic>cyclin-dependent kinases</jats:italic>, <jats:italic>MdCDKB1;1</jats:italic>, <jats:italic>MdCDKB1;2,</jats:italic> and <jats:italic>MdCDKB2;2</jats:italic>, displayed higher expression by up to 5-fold under reduced fruit load conditions during early fruit growth. These data indicate that carbohydrate availability affects the expression of key transcription factors and cell proliferation genes, thereby regulating cell production during early fruit growth. Several genes associated with cell expansion such as the <jats:italic>expansins</jats:italic>, and <jats:italic>cobra</jats:italic> and <jats:italic>cobra-like</jats:italic> genes, also displayed altered expression in response to the reduction in fruit load. The expression of three <jats:italic>expansin</jats:italic> genes was higher under reduced fruit load conditions at maturity, a stage at which a minor increase in cell size was apparent. Together, data from this study indicate that fruit load reduction induces changes in carbohydrate availability and metabolism, which in turn affect cell production-related mechanisms, thereby enhancing early fruit growth.</jats:p>

Higher growth of the apple (Malus × domestica Borkh.) fruit cortex is supported by resource intensive metabolism during early development

“…Cortex growth during EFD was > 5fold higher than that in the pith. Majority of cortex growth during EFD is associated with rapid cell production [9,10,28]. Hence, higher cortex growth was likely achieved through greater cell production than that in the pith.…”

“…1). Fruit load reduction enhances early fruit growth by increasing cell production [9,10,28]. Hence, additional resources translocated into the fruit due to sink-removal [30,31] are allocated primarily to enhancing cell production allowing for greater cortex growth.…”

“…Growth during MFD is primarily mediated by postmitotic cell expansion [9,10,28] and likely facilitated by metabolite accumulation in the vacuole. Differential metabolic activities across fruit tissues apparent during this period were largely related to C storage (Fig.…”

“…As cell production during early development establishes a population of cells that can subsequently undergo expansion, relatively cheaply through vacuolation, growth differences established during this period may be amplified over the rest of fruit development. For example, fruit load reduction during early development enhances fruit growth by increasing cell production and this growth advantage continues through out the rest of development [27,28]. Similarly, if the cortex metabolic program facilitates preferential growth over that of the pith during early development, this may be amplified during the rest of fruit development.…”

QTL mapping and identification of SNP-haplotypes affecting yield components of Theobroma cacao L.

“…Growing vegetative tissues and harvestable organs compete for the available assimilated carbon in the translocation stream. Competition for assimilated carbon has been shown in which changes in number of fruits (fruit load) affect fruit growth, fresh weight and carbohydrate concentration in Malus domestica 18 , Citrus clementina 19 , and Actinidia Chinensis 20 . In our study, we found a significant negative correlation between DBW with all the other variables, which indicates a competition for the assimilated carbon among those harvestable organs.…”