Severe shading reduces early fruit growth in apple by Decreasing cell production and expansion

Abstract

Shading during early fruit development reduces fruit growth and initiates fruit abscission in apple (Malus × domestica). The mechanisms mediating the decline in fruit growth in response to shading are not well understood. In this study, the effects of shading during early fruit development on cell production and expansion were investigated. Additionally, the effects of shading on the expression of genes associated with carbohydrate metabolism, fruit growth, and cell production and expansion were investigated to develop a better understanding of the molecular mechanisms and to identify genes that mediate the reduction in fruit growth. Shading of isolated branches or entire trees ≈ 15 to 18 days after full bloom resulted in a sharp decline in fruit growth by 3 days after treatment. Reduction in fruit growth was consistently mediated by a decline in cell production within 3 days after treatment. Reduced fruit growth was also associated with lower cell size by 3 to 7 days after shading in two different years. These data indicate that the reduction in fruit growth as a result of shading is mediated by a reduction in cell production and expansion. The expression of two sorbitol dehydrogenase (SDH) genes, MdSDH1 and MdSDH2, was higher in the shaded fruit by up to 10-fold, suggesting an increase in SDH activity to meet the immediate respiratory demands of the developing fruit. The auxin response factor (ARF), MdARF106, displayed ≈ 3-fold higher expression in the shaded fruit, suggesting its involvement in regulating mechanisms that mediate the reduction in fruit growth. Two A2-type cyclins, MdCYCA2;2 and MdCYCA2;3, which are positively associated with cell production, displayed lower expression in the shaded fruit by up to 4.6-fold. Conversely, MdKRP4 and MdKRP5, cell cycle genes negatively associated with cell production, displayed 3.9- and 5.3-fold higher expression in the shaded fruit, respectively. Additionally, two genes associated with cell expansion, MdCOB1 (cobra1) and MdEXPA10;1 (expansin), displayed lower expression in the shaded fruit. Together, these data indicate that shading results in coordinated changes in the expression of carbohydrate metabolism-related genes, key transcription factors related to fruit growth, and genes associated with cell production and expansion. These changes may subsequently decrease the progression of the primary processes that mediate fruit growth.