The leaf beetle Chelymorpha alternans propagates a plant pathogen in exchange for pupal protection

Berasategui, Aileen; Breitenbach, Noa; García-Lozano, Marleny; Pons, Inès; Sailer, Brigitte; Lanz, Christa; Rodríguez, Viterbo; Hipp, Katharina; Ziemert, Nadine; Windsor, Donald M.; Salem, Hassan

doi:10.1016/j.cub.2022.07.065

Cited by 31 publications

(30 citation statements)

References 124 publications

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“…For example, rice gall dwarf virus is transmitted vertically by hitchhiking on insect sperm, thereby promoting long-term viral epidemics and persistence in nature [2]. Berasategui et al (2022) [3] found a mutualistic relationship between Chelymorpha alternans and Fusarium oxysporum, where the pupae were protected in exchange for the dissemination and propagation of the fungus. Although there is limited research on the mechanisms underlying vector-bacteria interactions.…”

Section: Discussionmentioning

confidence: 99%

“…The majority of devastating plant pathogens, including viruses and bacteria, are transmitted by insect vectors [1]. In recent decades, the interactions between vectors and pathogens have been widely studied [1][2][3][4]. However, studies on the mechanisms underlying these interactions have mainly focused on vector-virus or vector-fungus interactions; less research has been performed on vector-bacteria interactions.…”

Section: Introductionmentioning

confidence: 99%

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Adipokinetic hormone signaling mediates the enhanced fecundity ofDiaphorina citriinfected by ‘CandidatusLiberibacter asiaticus’

Li,

Holford,

Beattie

et al. 2023

Preprint

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Diaphorina citri is the primary vector of the bacterium, Candidatus Liberibacter asiaticus (C Las) associated with the severe Asian form of huanglongbing. C Las-positive D. citri are more fecund than their C Las-negative counterparts and require extra energy expenditure. Therefore, understanding the molecular mechanisms linking metabolism and reproduction is of particular importance. In this present study, we found adipokinetic hormone (Dc AKH) and its receptor (DcAKHR) were essential for increased lipid metabolism and fecundity in response to C Las infection in D. citri. Knockdown of Dc AKH and DcAKHR not only resulted in triacylglycerol accumulation and a decline of glycogen, but also significantly decreased fecundity and C Las titer in ovaries. Combined in vivo and in vitro experiments showed that miR-34 suppresses DcAKH R expression by binding to its 3'untranslated region, whilst overexpression of miR-34 resulted in a decline of DcAKH R expression and C Las titer in ovaries and caused defects that mimicked DcAKH R knockdown phenotypes. In addition, knockdown of DcAKH and DcAKHR significantly reduced juvenile hormone (JH) titer and JH signaling pathway genes in fat bodies and ovaries, including the JH receptor, methoprene-tolerant (DcMet), and the transcription factor, Kruppel homolog 1 (DcKr-h1), that acts downstream of it, as well as the egg development related genes vitellogenin 1-like (DcVg-1-like), vitellogenin A1-like (DcVg-A1-like) and the vitellogenin receptor (DcVgR). As a result, C Las hijacks AKH/AKHR-miR-34-JH signaling to improve D. citri lipid metabolism and fecundity, while simultaneously increasing the replication of C Las, suggesting a mutualistic interaction in D. citri ovaries with C Las.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Adipokinetic hormone signaling mediates the enhanced fecundity ofDiaphorina citriinfected by ‘CandidatusLiberibacter asiaticus’

Li,

Holford,

Beattie

et al. 2023

Preprint

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“…Treatments were pooled, yielding 30 caplets in each replicate. The remaining eggs were maintained under standard growth conditions (26°C and 60% relative humidity) previously described in Pons et al 8 and Berasategui et al 106 . Three larvae from each replicate were collected nine days after hatching.…”

Section: Methodsmentioning

confidence: 99%

Paleocene origin of a streamlined digestive symbiosis in leaf beetles

García-Lozano,

Henzler,

Porras

et al. 2023

Preprint

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Timing the acquisition of a beneficial microbe relative to the evolutionary history of its host can shed light on the adaptive impact of a partnership. Here, we investigated the onset and molecular evolution of an obligate symbiosis between Cassidinae leaf beetles andCandidatusStammera capleta, a γ-proteobacterium. Residing extracellularly within foregut symbiotic organs,Stammeraupgrades the digestive physiology of its host by supplementing plant cell wall-degrading enzymes. We observe thatStammerais a shared symbiont across tortoise and hispine beetles that collectively comprise the Cassidinae subfamily, despite differences in their folivorous habits. In contrast to its transcriptional profile during vertical transmission,Stammeraelevates the expression of genes encoding digestive enzymes while in the foregut symbiotic organs, matching the nutritional requirements of its host. Symbiont acquisition during the Paleocene (∼62 Mya) did not coincide with the origin of Cassidinae beetles, despite the widespread distribution ofStammeraacross the subfamily. Early-diverging lineages lack the symbiont and the specialized organs that house it. Reconstructing the ancestral state of host-beneficial factors revealed thatStammeraencoded three digestive enzymes at the onset of symbiosis, including polygalacturonase – a pectinase that is universally shared. While non-symbiotic cassidines encode polygalacturonase endogenously, their repertoire of plant cell wall-degrading enzymes is more limited compared to symbiotic beetles supplemented with digestive enzymes fromStammera. Highlighting the potential impact of a symbiotic condition and an upgraded metabolic potential,Stammera-harboring beetles exploit a greater variety of plants and are more speciose compared to non-symbiotic members of the Cassidinae.

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“…For example, the vertical transmission of rice gall dwarf virus has evolved by hitchhiking with insect sperm without disturbing sperm function, thereby facilitating long-term viral epidemics and persistence in nature (Mao et al, 2019). Berasategui et al (2022) shed light on a mutualism between Chelymorpha alternans Boheman (Coleoptera: Chrysomelidae) and Fusarium oxysporum Schlecht. emend.…”

Section: Introductionmentioning

confidence: 99%

“…Berasategui et al. (2022) shed light on a mutualism between Chelymorpha alternans Boheman (Coleoptera: Chrysomelidae) and Fusarium oxysporum Schlecht. emend.…”

Section: Introductionmentioning

confidence: 99%

Infection with ‘Candidatus Liberibacter asiaticus’ improves the fecundity of Diaphorina citri aiding its proliferation: A win‐win strategy

Nian,

Luo,

et al. 2023

Molecular Ecology

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The evolution of insect vector‐pathogen relationships has long been of interest in the field of molecular ecology. One system of special relevance, due to its economic impacts, is that between Diaphorina citri and ‘Candidatus Liberibacter asiaticus’ (CLas), the cause of the severe Asian form of huanglongbing. CLas‐positive D. citri are more fecund than their CLas‐negative counterparts, boosting opportunities for pathogens to acquire new vector hosts. The molecular mechanism behind this life‐history shift remains unclear. Here, we found that CLas promoted ovarian development and increased the expression of the vitellogenin receptor (DcVgR) in ovaries. DcVgR RNAi significantly decreased fecundity and CLas titer in ovaries, extended the preoviposition period, shortened the oviposition period and blocked ovarian development. Given their importance in gene regulation, we explored the role of miRNAs in shaping these phenotypes and their molecular triggers. Our results showed that one miRNA, miR‐275, suppressed DcVgR expression by binding to its 3' UTR. Overexpression of miR‐275 knocked down DcVgR expression and CLas titer in ovaries, causing reproductive defects that mimicked DcVgR knockdown phenotypes. We focused, further, on roles of the Juvenile Hormone (JH) pathway in shaping the observed fecundity phenotype, given its known impacts on ovarian development. After CLas infection, this pathway was upregulated, thereby increasing DcVgR expression. From these combined results, we conclude that CLas hijacks the JH signalling pathway and miR‐275, thereby targeting DcVgR to increase D. citri fecundity. These changes simultaneously increase CLas replication, suggesting a pathogen‐vector host mutualism, or a seemingly helpful, but cryptically costly life‐history manipulation.

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The leaf beetle Chelymorpha alternans propagates a plant pathogen in exchange for pupal protection

Cited by 31 publications

References 124 publications

Adipokinetic hormone signaling mediates the enhanced fecundity ofDiaphorina citriinfected by ‘CandidatusLiberibacter asiaticus’

Adipokinetic hormone signaling mediates the enhanced fecundity ofDiaphorina citriinfected by ‘CandidatusLiberibacter asiaticus’

Paleocene origin of a streamlined digestive symbiosis in leaf beetles

Infection with ‘Candidatus Liberibacter asiaticus’ improves the fecundity of Diaphorina citri aiding its proliferation: A win‐win strategy

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