Symbiosis in the green leafhopper, Cicadella viridis (Hemiptera, Cicadellidae). Association in statu nascendi?

Michalik, Anna; Jankowska, Władysława; Kot, Marta; Gołas, Aniela; Szklarzewicz, Teresa

doi:10.1016/j.asd.2014.07.005

Cited by 50 publications

(65 citation statements)

References 47 publications

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“…Sulcia, the betaproteobacterium Zinderia and a Sodalis-like symbiont) in A. quadrinotata may represent a transitional state in which the most recently acquired Sodalis-like symbiont coexists with the ancestral betaproteobacterium, which has not yet been eliminated. This hypothesis corresponds well with the findings of MICHALIK et al (2014a), which indicate that in the green leafhopper Cicadella viridis (LINNAEUS, 1758) the Sodalis-like symbiont co-resides with the bacterium Sulcia. Moreover, in C. viridis the Sodalis-like symbionts may occur in their own bacteriocytes or may co-reside in bacteriocytes with Sulcia.…”

Section: Discussionsupporting

confidence: 75%

“…Results of earlier histological studies (MÜLLER 1962, BUCHNER 1965) and more recent ultrastructural and molecular analyses , 2005, TAKIYA et al 2006, MCCUTCHEON et al 2009, MICHALIK et al 2014a, NODA et al 2012, ISHII et al 2013, KOGA et al 2013, BENNETT et al 2014, KOGA & MORAN 2014 have shown that representatives of Cicadomorpha are characterized by an enormous diversity of their symbionts. MORAN et al (2005) and KOGA et al (2013) suggested that the common ancestor of the Cicadomorpha and Fulgoromorpha acquired the bacterium Sulcia and the betaproteobacterial symbiont over 260 million years ago.…”

Section: Discussionmentioning

confidence: 99%

“…In the latter case, Sodalis-like symbionts infect cells of Sulcia resulting in the internalization of these microorganisms within the cells of Sulcia. Based on this observation, MICHALIK et al (2014a) suggested that (1) symbiosis between C. viridis and the Sodalis-like symbiont represents an association "in statu nascendi", and (2) during the evolution of C. viridis, the bacterium Sodalis replaced the bacterium Baumannia. Thus, the above facts show that the kinds of possible symbiosis in cicadomorphans are much more complex than those present in other hemipterans.…”

Section: Discussionmentioning

confidence: 99%

“…Earlier histological studies by MÜLLER (1962) andBUCHNER (1965) and more recent molecular analyses (TAKIYA et al 2006, URBAN & CRYAN 2012, ISHII et al 2013, KOGA et al 2013, MICHALIK et al 2014a have shown that Cicadomorpha and Fulgoromorpha (except Delphacidae), as a rule, harbour the obligate Bacteroidetes bacterium "Candidatus Sulcia muelleri" (hereafter Sulcia), which is accompanied by one or two bacterial species belonging to the phylum Proteobacteria. In Cicadomorpha and Fulgoromorpha all symbiotic microorganisms provide their hosts with essential amino acids (TAKIYA et al 2006, WU et al 2006, MCCUTCHEON et al 2009, MCCUTCHEON & MORAN 2010): TAKIYA et al (2006 have therefore named them "coprimary symbionts".…”

Section: Introductionmentioning

confidence: 99%

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Symbiotic microorganisms of the leafhopper Deltocephalus pulicaris (Fallén, 1806) (Insecta, Hemiptera, Cicadellidae: Deltocephalinae): molecular characterization, ultrastructure and transovarial transmission

Kobiałka¹,

Michalik²,

Walczak³

et al. 2015

Polish Journal of Entomology

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ABSTRACT. The ovaries of the leafhopper Deltocephalus pulicaris are accompanied by large organs termed bacteriomes, which are composed of numerous polyploid cells called bacteriocytes. The cytoplasm of bacteriocytes is tightly packed with symbiotic microorganisms. Ultrastructural and molecular analyses have revealed that bacteriocytes of D. pulicaris contain two types of symbionts: the bacterium "Candidatus Sulcia muelleri" and the bacterium "Candidatus Nasuia deltocephalinicola". Both symbionts are transovarially transmitted from the mother to the next generation.

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Section: Discussionsupporting

confidence: 75%

Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Symbiotic microorganisms of the leafhopper Deltocephalus pulicaris (Fallén, 1806) (Insecta, Hemiptera, Cicadellidae: Deltocephalinae): molecular characterization, ultrastructure and transovarial transmission

Kobiałka¹,

Michalik²,

Walczak³

et al. 2015

Polish Journal of Entomology

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“…After the loss of critical translation-related genes in Tremblaya, the symbiosis would persist with a bacteria within a bacterium structure because no other structure is possible. We note that Sodalis-and Arsenophonus-allied symbionts were recently suggested to sometimes reside within Sulcia cells in the leafhoppers Cicadella viridis and Macrosteles laevis (66,67). Although these studies were based only on EM imaging and not confirmed by specific probes (e.g., with FISH), it is possible that symbioses formed by bacteria taking up residence inside of degenerate symbionts with host-derived cell envelopes are not uncommon.…”

Section: Diversity Of Intra-tremblaya Symbiont Genomes Suggests Multiplementioning

confidence: 99%

Repeated replacement of an intrabacterial symbiont in the tripartite nested mealybug symbiosis

Husník

McCutcheon

2016

Proc. Natl. Acad. Sci. U.S.A.

232

279

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Stable endosymbiosis of a bacterium into a host cell promotes cellular and genomic complexity. The mealybug Planococcus citri has two bacterial endosymbionts with an unusual nested arrangement: the γ-proteobacterium Moranella endobia lives in the cytoplasm of the β-proteobacterium Tremblaya princeps. These two bacteria, along with genes horizontally transferred from other bacteria to the P. citri genome, encode gene sets that form an interdependent metabolic patchwork. Here, we test the stability of this three-way symbiosis by sequencing host and symbiont genomes for five diverse mealybug species and find marked fluidity over evolutionary time. Although Tremblaya is the result of a single infection in the ancestor of mealybugs, the γ-proteobacterial symbionts result from multiple replacements of inferred different ages from related but distinct bacterial lineages. Our data show that symbiont replacement can happen even in the most intricate symbiotic arrangements and that preexisting horizontally transferred genes can remain stable on genomes in the face of extensive symbiont turnover.Sodalis | organelle | horizontal gene transfer | scale insect

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Microbiome responses during virulence adaptation by a phloem‐feeding insect to resistant near‐isogenic rice lines

Horgan

Srinivasan

Crisol‐Martínez

et al. 2019

Ecology and Evolution

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The microbiomes of phloem‐feeding insects include functional bacteria and yeasts essential for herbivore survival and development. Changes in microbiome composition are implicated in virulence adaptation by herbivores to host plant species or host populations (including crop varieties). We examined patterns in adaptation by the green leafhopper, Nephotettix virescens, to near‐isogenic rice lines (NILs) with one or two resistance genes and the recurrent parent T65, without resistance genes. Only the line with two resistance genes was effective in reducing leafhopper fitness. After 20 generations on the resistant line, selected leafhoppers attained similar survival, weight gain, and egg laying to leafhoppers that were continually reared on the susceptible recurrent parent, indicating that they had adapted to the resistant host. By sequencing the 16s rRNA gene, we described the microbiome of leafhoppers from colonies associated with five collection sites, and continually reared or switched between NILs. The microbiomes included 69–119 OTUs of which 44 occurred in ≥90% of samples. Of these, 14 OTUs were assigned to the obligate symbiont Candidatus sulcia clade. After 20 generations of selection, collection site had a greater effect than host plant on microbiome composition. Six bacteria genera, including C. sulcia, were associated with leafhopper virulence. However, there was significant within‐treatment, site‐related variability in the prevalence of these taxa such that the mechanisms underlying their association with virulence remain to be determined. Our results imply that these taxa are associated with leafhopper nutrition. Ours is the first study to describe microbiome diversity and composition in rice leafhoppers. We discuss our results in light of the multiple functions of herbivore microbiomes during virulence adaptation in insect herbivores.

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Symbiosis in the green leafhopper, Cicadella viridis (Hemiptera, Cicadellidae). Association in statu nascendi?

Cited by 50 publications

References 47 publications

Symbiotic microorganisms of the leafhopper Deltocephalus pulicaris (Fallén, 1806) (Insecta, Hemiptera, Cicadellidae: Deltocephalinae): molecular characterization, ultrastructure and transovarial transmission

Symbiotic microorganisms of the leafhopper Deltocephalus pulicaris (Fallén, 1806) (Insecta, Hemiptera, Cicadellidae: Deltocephalinae): molecular characterization, ultrastructure and transovarial transmission

Repeated replacement of an intrabacterial symbiont in the tripartite nested mealybug symbiosis

Microbiome responses during virulence adaptation by a phloem‐feeding insect to resistant near‐isogenic rice lines

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