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

Abstract

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.

Symbiosis preservation: Putative regulation of fatty acyl-CoA reductase by miR-31a within the symbiont harboring bacteriome through tsetse evolution

“…MiRNAs have emerged as potential regulators of homeostasis between insects and members of their microbiota ( Aksoy et al, 2016 ; Feng et al, 2018 , 2019 ; Mukherjee et al, 2020 ; Sun et al, 2022 ). Some miRNAs have been found to be associated with the bacteriomes in the aphid- Buchnera nutritional mutualism although the role of these miRNAs is still being evaluated ( Feng et al, 2018 , 2019 ).…”

“…Even as we expand our understanding of the functional significance of the critical tsetse- Wigglesworthia symbiosis, fundamental questions remain about how interspecies homeostasis is maintained throughout development and during energetically expensive life events such as pregnancy and trypanosome infection, as these events are associated with differences in metabolic demands. It is likely that homeostasis is coordinated by a multitude of mechanisms including epigenetic regulation mediated by microRNAs (miRNAs) ( Feng et al, 2018 , 2019 ; Sun et al, 2022 ).…”

“…MiRNAs have been implicated in nearly all biological contexts with high conservation observed across eukaryotes ( Song et al, 2004 )which eases their identification into large families based on homology. MiRNAs have additionally emerged as potential regulators of insect-bacteria homeostasis ( Zhang et al, 2015 ; Feng et al, 2018 , 2019 ; Mukherjee et al, 2020 ; Sun et al, 2022 ).…”

Vitellogenin Facilitates Associations between the Whitefly and a Bacteriocyte Symbiont

“…dsRNAs specific to whitefly JHAMT (ds JHAMT ), whitefly Vg (ds Vg ), and GFP (ds GFP ) with sizes of 713 bp, 450 bp, and 420 bp, respectively, were synthesized using a T7 RiboMAX express RNAi system kit (Promega, USA), in accordance with the manufacturer’s instructions as described previously ( 13 , 34 , 45 , 47 , 57 , 61 ).…”

“…To study the effect of the JH pathway on Vg expression and Vg localization in whiteflies, approximately 800 female adult whiteflies at day 1 after emergence were injected with 1.5 μg/μL ds JHAMT and incubated on cotton leaf disks by using a previously described method ( 13 , 45 , 47 , 57 , 61 ). Control whiteflies were injected with 1.5 μg/μL ds GFP .…”