Bacteriocyte development is sexually differentiated in Bemisia tabaci

Li, Nana; Jiang, Shan; Lu, Kun-Yu; Hong, Ji-Sheng; Wang, Yanbin; Yan, Jin-Yang; Luan, Jing

doi:10.1016/j.celrep.2022.110613

Cited by 7 publications

(11 citation statements)

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“…S3 C and D ). This observation was consistent with the report that apoptosis and autophagy occurred in male bacteriocytes but not in females (33). Portiera and Hamiltonella titers remarkably declined only in males at this stage (Fig.…”

Section: Resultssupporting

confidence: 94%

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Subcellular niche segregation of co-obligate symbionts in whiteflies

Fujiwara

Meng

Kamagata

et al. 2022

Preprint

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Many insects contain endosymbiotic bacteria within their bodies. In multiple endosymbiotic systems comprising two or more symbionts, each of the symbionts is generally localized in a different host cell or tissue.Bemisia tabaci（Sweet potato whitefly）possesses a unique endosymbiotic system where co-obligate symbionts are localized in the same bacteriocytes. Using fluorescence in situ hybridization, we found that endosymbionts inB. tabaciMEAM1 occupy distinct subcellular habitats, or niches, within a single bacteriocyte.Hamiltonellawas located adjacent to the nucleus of the bacteriocyte, whilePortierawas present in the cytoplasm surroundingHamiltonella. Immunohistochemical analysis revealed that the endoplasmic reticulum separates the two symbionts. Habitat segregation was maintained for longer durations in female bacteriocytes. The same segregation was observed in three genetically distinctB. tabacigroups (MEAM1, MED Q1, and Asia II 6) andTrialeurodes vaporariorum, which shared a common ancestor withBemisiaover 80 million years ago, even though the coexisting symbionts and the size of bacteriocytes were different. These results suggest that the habitat segregation system existed in the common ancestor and was conserved in both lineages, despite different bacterial partners coexisting withPortiera. Our findings provide insights into the evolution and maintenance of complex endosymbiotic systems and highlight the importance of organelles for the construction of separate niches for endosymbionts.

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Section: Resultssupporting

confidence: 94%

“…are co-localized in the same bacteriocytes (31)(32)(33), suggesting possible competition between the symbionts for limited space and resources. Nevertheless, Portiera and Hamiltonella populations are large and exhibit synchronous dynamics in MEAM1 (34).…”

Section: Introductionmentioning

confidence: 99%

Subcellular niche segregation of co-obligate symbionts in whiteflies

Fujiwara

Meng

Kamagata

et al. 2022

Preprint

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“…Progressive hypervacuolation, autophagy or apoptosis and transcriptional factors are involved in bacteriocyte development or death, which can control the changes in obligate symbiont populations, in the pea aphid Acyrthosiphon pisum (Simonet et al, 2018), the cereal weevils Sitophilus spp. (Vigneron et al, 2014), the seed bug Nysius plebeius (Matsuura et al, 2015) and whiteflies (Li et al, 2022; Wang et al, 2022). Because novel‐m0780‐5p agomir‐injection reduced the titre of Portiera in whiteflies, the miRNA could be used as another way for the host to control their symbiont population.…”

Section: Discussionmentioning

confidence: 99%

“…The miRNA antagomir is the chemically modified single‐stranded miRNA that complements the miRNAs and can specifically silence the endogenous miRNAs (Krutzfeldt et al, 2005). To investigate whether overexpression or repression of novel‐m0780‐5p influences PanBC localization in whiteflies, ~800 female adult whiteflies infected with Portiera within 3–4 days after emergence were injected with 3 µ m agomir or antagomir using an Eppendorf microinjection system following a previously described method (Bao et al, 2021; Li et al, 2022; Ren et al, 2021; Wang et al, 2022). The whiteflies that were injected with 3 µ m negative control agomir were used as a negative control for agomir injection.…”

Section: Methodsmentioning

confidence: 99%

“…In China, B. tabaci MEAM1 bears Portiera and ‘ Candidatus Hamiltonella defensa’ (hereafter Hamiltonella ) in the same bacteriocytes and Rickettsia sp. (hereafter Rickettsia ) in the whole‐body cavity (Li et al, 2022; Ren et al, 2020; Wang et al, 2020). Portiera and Hamiltonella are vertically transmitted via the bacteriocytes (Luan et al, 2016, 2018).…”

Section: Introductionmentioning

confidence: 99%

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A novel microRNA regulates cooperation between symbiont and a laterally acquired gene in the regulation of pantothenate biosynthesis within Bemisia tabaci whiteflies

Sun

Liu

et al. 2022

Molecular Ecology

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Horizontally transferred genes (HTGs) play a key role in animal symbiosis, and some horizontally transferred genes or proteins are highly expressed in specialized host cells (bacteriocytes). However, it is not clear how HTGs are regulated, but microRNAs (miRNAs) are prime candidates given their previously demonstrated roles in symbiosis and impacts on the expression of host genes. A horizontally acquired PanBC that is highly expressed in whitefly bacteriocytes can cooperate with an obligate symbiont Portiera for pantothenate production, facilitating whitefly performance and Portiera titre. Here, we found that a whitefly miRNA, novel‐m0780‐5p, was up‐regulated and its target panBC was down‐regulated in Portiera‐eliminated whiteflies. This miRNA was located in the cytoplasmic region of whitefly bacteriocytes. Injection of novel‐m0780‐5p agomir reduced the expression of PanBC in whitefly bacteriocytes, while injection of novel‐m0780‐5p antagomir enhanced PanBC expression. Agomir injection also reduced the pantothenate level, Portiera titre and whitefly performance. Supplementation with pantothenate restored Portiera titre and the fitness of agomir‐injected whiteflies. Thus, we demonstrate that a whitefly miRNA regulates panBC‐mediated host–symbiont collaboration required for pantothenate synthesis, benefiting the whitefly–Portiera symbiosis. Both panBC and novel‐m0780‐5p are present in the genomes of six Bemisia tabaci species. The expression of a novel miRNA in multiple B. tabaci species suggests that the miRNA evolved after panBC acquisition, and allowed this gene to be more tightly regulated. Our discovery provides the first account of a HTG being regulated by a miRNA from the host genome, and suggests key roles for interactions between miRNAs and HTGs in the functioning of symbiosis.

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