Field inoculation responses of arbuscular mycorrhizal fungi versus endophytic fungi on sugar metabolism associated changes in fruit quality of Lane late navel orange

Abstract

Arbuscular mycorrhizal (AM) fungi and plants require sugars, especially during fruit ripening stage, while the underlying mechanism influencing sugar accumulation in response to AM fungi is still unclear. The objective of this study was to analyze the field inoculation response of three AM fungi (Acaulospora scrobiculata, Diversispora spurca, and D. versiformis) and an endophytic fungus (Piriformospora indica) on internal as well as external quality parameters of Lane late navel orange (Citrus sinensis) fruits, with emphasis on monosaccharide and disaccharide components and expressions of sucrose-associated enzyme genes and sugar transporter genes. Root fungal colonization rate increased by 51.2−109.6% with the inoculation of D. spurca displaying the best response after two years of field inoculation. The fungal introduction also improved the external fruit quality attributes to some extent, especially longitudinal and transverse diameter, sarcocarp weight, and fruit coloration value in response to inoculation of A. scrobiculata and P. indica. Fruit number increased in response to inoculation with D. versiformis. Although none of the four symbiotic fungi influenced the soluble solids of fruits, however fruit titratable acids registered a significant reduction leading to an increase in soluble solids-titratable acids ratio in response to A. scroblculata and D. spurca. Inoculation with A. scrobiculata and D. spurca also reduced sucrose while increased glucose, fructose, and trehalose concentrations in fruit sarcocarps, along with up-regulated expressions of CsVINV1, CsA/NINV4, and CsSWEET in fruit sarcocarps, suggesting that AM fungi played a pivotal role in sucrose transport, synthesis, and cleavage in fruits. In contrast, inoculation with P. indica only increased the sucrose and up-regulated expressions of CsSPS1 and CsSPS4 in fruit sarcocarps, implying that Pi mainly triggered the sucrose synthesis in fruits. These symbiotic fungi increased concentration of one of the three sweeteners (arabinose, xylitol and fucose) in fruit sarcocarps, with an exception of A. scrobiculata responding to an increase in the three sweeteners. These results provided strong clues that symbiotic fungi have an important role in improving the fruit size and different sugar components in citrus fruits by regulating the expression of genes related to sucrose synthesis, cleavage, and transport, with A. scrobiculata outplaying the response of other three symbiotic fungi.