Host plant-induced changes in metabolism and osmotic regulation gene expression in Diaphorina citri adults

The Asian citrus psyllid (ACP), Diaphorina citri Kuwayama (Hemiptera: Liviidae), is one of the most serious sap-sucking pests of citrus worldwide (Fan et al., 2023, Liu et al., 2023). It serves as a vector for Candidatus Liberibacter asiaticus, the causal agent of Huanglongbing (HLB) (Hosseinzadeh and Heck, 2023, Ibanez et al., 2023). The pathogen could systemically infect and weaken citrus trees, resulting in a significant decrease in fruit yield and quality and leading to serious economic losses (Lei et al., 2023). The trees infected by these pathogens may die within a few years (Ruan et al., 2015). Besides, this pest could feed on plant phloem, causing branch wilting (Chen et al., 2023). The honeydew excretion of ACP induced the occurrence of soot disease (Bin et al., 2019). ACP and CLas are thought to be native to Asia and has spread to South, Central, and North America, becoming the greatest threat to the citrus industry worldwide (Gotwald et al., 2010). To date, there is no cure for HLB management, while ACP control has become a critical strategy to prevent the spread of HLB in the field (Qureshi and Stansly, 2020).

The ACP can feed on and reproduce on various plants, especially the species of several genera, such as Citrus and Murraya, in the Rutaceae family (Paris et al., 2016). Under the unsuitable conditions of the preferred host, the weed species Ageratum conyzoides, Solanum nigrum, Praxelis clematidea, Bidens alba, Eupatorium capillifolium, and Ludwigia octovalvis around the citrus groves are the temporary hosts for ACP survival (George et al., 2020, Lu et al., 2021). Murraya exotica (L.) Millsp. is an ornamental hedge plant that serves as a suitable host for D. citri (Tsai and Liu, 2000, Cifuentes-Arenas et al., 2019). More evidence showed that the CLas titer in M. exotica and Murraya-reared ACP was inhibited compared to those in Citrus sinensis and the citrus-reared ACP (Walter et al., 2012). ‘Shatangju’ mandarin (Citrus reticulata Blanco cv. Shatangju) is a Chinese citrus specialty and native to the Sihui region of Guangdong Province, China (Wang et al., 2020). It is another host plant for ACP development and reproduction (Meng et al., 2018). No significant difference in the developmental period, juvenile survival rate, adult longevity, sex ratio, or fecundity of ACP reared on M. exotica and ‘Shatangju’ mandarin, suggesting the high suitability of these two plant species for ACP (Ren et al., 2018).

Plant phloem saps consumed by phytophagous insects, including ACP, generally have a high abundance of glucose and sucrose while being deficient in essential amino acids (Douglas, 2006). The concentration and osmotic pressure of phloem sap vary among different plants (Douglas, 2006). High intake of carbohydrates leads to an increase in osmotic pressure in insects, while insects convert excess ingested carbohydrates into long-chain oligosaccharides that are eventually excreted as honeydew (Hijaz et al., 2016). Recently, the osmoregulation mechanisms of phytophagous insects have been investigated (Jing et al., 2016, Shu et al., 2019). The primary mechanism for maintaining osmotic homeostasis is the digestion of sucrose into glucose and fructose by sucrose hydrolase in the insect gut. Aquaporin activity, indispensable for cellular water regulation, is the secondary mechanism. They facilitate the osmotic movement of water from the distal gut to the proximal midgut (stomach) and promote pressure equilibrium between the gut lumen and the hemolymph.21 In D. citri, sucrose hydrolase (DcSuh) and aquaporin (DcAQP) were proven to be involved in osmotic pressure regulation (Santos-Ortega and Killiny, 2018, Santos-Ortega and Killiny, 2021).

In this study, the contents of total sugars, sucrose, fructose, and glucose in young shoots, old leaves, and young leaves of ‘Shatangju’ mandarin and M. exotica were analyzed. The metabolome analysis was performed in the midguts of D. citri adults fed on ‘Shatangju’ mandarin and M. exotica for two weeks. In addition, the genes of the aquaporin family were identified in D. citri through the genome and transcriptome data. The mRNA expression levels of DcSuh, aquaporins, and genes involved in trehalose metabolism in adults fed on ‘Shatangju’ mandarin and M. exotica were further analyzed. Our findings provide a preliminary understanding of D. citri's host adaptive mechanism.

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