Development on Citrus medica infected with ‘Candidatus Liberibacter asiaticus’ has sex-specific and -nonspecific impacts on adult Diaphorina citri and its endosymbionts

Abstract

Huanglongbing (HLB) is a deadly, incurable citrus disease putatively caused by the unculturable bacterium, 'Candidatus Liberibacter asiaticus' (CLas), and transmitted by Diaphorina citri. Prior studies suggest D. citri transmits CLas in a circulative and propagative manner; however, the precise interactions necessary for CLas transmission remain unknown, and the impact of insect sex on D. citri-CLas interactions is poorly understood despite reports of sex-dependent susceptibilities to CLas. We analyzed the transcriptome, proteome, metabolome, and microbiome of male and female adult D. citri reared on healthy or CLas-infected Citrus medica to determine shared and sex-specific responses of D. citri and its endosymbionts to CLas exposure. More sex-specific than shared D. citri responses to CLas were observed, despite there being no difference between males and females in CLas density or relative abundance. CLas exposure altered the abundance of proteins involved in immunity and cellular and oxidative stress in a sex-dependent manner. CLas exposure impacted cuticular proteins and enzymes involved in chitin degradation, as well as energy metabolism and abundance of the endosymbiont 'Candidatus Profftella armatura' in both sexes similarly. Notably, diaphorin, a toxic Profftella-derived metabolite, was more abundant in both sexes with CLas exposure. The responses reported here resulted from a combination of CLas colonization of D. citri as well as the effect of CLas infection on C. medica. Elucidating these impacts on D. citri and their endosymbionts contributes to our understanding of the HLB pathosystem and identifies the responses potentially critical to limiting or promoting CLas acquisition and propagation in both sexes.

First report of Citrus Tristeza virus in Diaphorina citri of different nymphal and adult stages or different sexes collected from field

“…The lowest Ct value in CTV detection was 24.82 for male and 26.79 for female, while that in CLas detection was 15.40 for female and 19.05 for male. Several researchers have demonstrated that no differences in acquisiton of CLas between male and female D. citri nor in titers of the bacterium [10][11][12]. In our study, we further con rmed that no signi cant difference existed between male and female in the acquisition rates or titers of CLas and CTV.…”

Report of Citrus tristeza virus in Diaphorina citri (Hemiotera: Liviidae) insects of different sexes, color morphs, and developmental stages

“… Ning et al (2015) found that the efficiencies of acquisition and transmission of the tomato yellow leaf curl virus (TYLCV) were varied by both biotype and sex. Several other researchers have also concluded that no differences exist in the acquisition or total titer of CLas between male and female D. citri insects ( Ammar et al 2011 , Wu et al 2018 , Coates et al 2020 ). When running electrical penetration graph experiments on healthy ACPs, the effects of sex can be ignored ( Timothy and Michael 2020 ).…”

Improving Suppression of Hemipteran Vectors and Bacterial Pathogens of Citrus and Solanaceous Plants: Advances in Antisense Oligonucleotides (FANA)

“…causing the global pandemic (Bové, 2006;Sétamou et al, 2016;Wang et al, 2017a,b;Kruse et al, 2019;Ammar et al, 2020a,b). The three known Liberibacter species associated with HLB are: Candidatus Liberibacter africanus, CLaf; Candidatus Liberibacter americanus, CLam; and Candidatus Liberibacter asiaticus, CLas (Bové, 2006;Haapalainen, 2014;Wang et al, 2017a,b;Coates et al, 2020). African countries are dominated by CLaf, which is transmitted by two psyllid species, the African citrus psyllid, Trioza erytreae (Hemiptera: Triozidae) and the Asian citrus psyllid (ACP) Diaphorina citri Kuwayama (Hemiptera: Liviidae), which can transmit both CLam and CLas bacteria (Lallemand et al, 1986).…”