Reduced Levels of Membrane-Bound Alkaline Phosphatase Are Common to Lepidopteran Strains Resistant to Cry Toxins from Bacillus thuringiensis

Jurat-Fuentes, Juan Luís; Karumbaiah, Lohitash; Jakka, Siva R. K.; Ning, Changming; Liu, Chenxi; Wu, Kongming; Jackson, Jerreme; Gould, Fred; Blanco, Carlos A.; Portilla, Maribel; Perera, Omaththage P.; Adang, Michael J.

doi:10.1371/journal.pone.0017606

Cited by 147 publications

(117 citation statements)

References 70 publications

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“…sustainable in insects. For example, if ALP activity is supplied by the host, then a lower or more tissue-specific ALP activity in insects could make the parasite folate synthesis impossible (23,24). Conversely, the new host environment might have made de novo folate synthesis unnecessary, leading to its loss.…”

Section: Discussionmentioning

confidence: 99%

Gain and loss of multiple functionally related, horizontally transferred genes in the reduced genomes of two microsporidian parasites

Pombert

Selman

Burki

et al. 2012

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

106

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Microsporidia of the genus Encephalitozoon are widespread pathogens of animals that harbor the smallest known nuclear genomes. Complete sequences from Encephalitozoon intestinalis (2.3 Mbp) and Encephalitozoon cuniculi (2.9 Mbp) revealed massive gene losses and reduction of intergenic regions as factors leading to their drastically reduced genome size. However, microsporidian genomes also have gained genes through horizontal gene transfers (HGT), a process that could allow the parasites to exploit their hosts more fully. Here, we describe the complete sequences of two intermediate-sized genomes (2.5 Mbp), from Encephalitozoon hellem and Encephalitozoon romaleae. Overall, the E. hellem and E. romaleae genomes are strikingly similar to those of Encephalitozoon cuniculi and Encephalitozoon intestinalis in both form and content. However, in addition to the expected expansions and contractions of known gene families in subtelomeric regions, both species also were found to harbor a number of protein-coding genes that are not found in any other microsporidian. All these genes are functionally related to the metabolism of folate and purines but appear to have originated by several independent HGT events from different eukaryotic and prokaryotic donors. Surprisingly, the genes are all intact in E. hellem, but in E. romaleae those involved in de novo synthesis of folate are all pseudogenes. Overall, these data suggest that a recent common ancestor of E. hellem and E. romaleae assembled a complete metabolic pathway from multiple independent HGT events and that one descendent already is dispensing with much of this new functionality, highlighting the transient nature of transferred genes.evolution | genomics | parasitology

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Section: Discussionmentioning

confidence: 99%

Gain and loss of multiple functionally related, horizontally transferred genes in the reduced genomes of two microsporidian parasites

Pombert

Selman

Burki

et al. 2012

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

106

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“…3 Cry1A toxins bind to the extracellular domains of cadherin, aminopeptidase, and alkaline phosphatase in larval midgut membranes. 14,15 Disruption of Bt toxin binding to midgut receptors is the most common general mechanism of insect resistance. 9 Mutations in the genes encoding midgut cadherins that bind Cry1Ac are linked with resistance in at least three lepidopteran pests of cotton, [16][17][18] but such cadherin mutations are not the primary cause of many other cases of field-and laboratory-selected resistance.…”

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confidence: 99%

“…9,19,20 Although some aspects of the mode of action of Bt toxins remain unresolved, extensive evidence shows that after Cry1A protoxins are ingested by larvae, they are solubilized in the gut and cleaved by mid-gut proteases such as trypsin to yield activated 60-kD monomeric toxins that bind with membrane-associated receptors. 14,15 The signaling model suggests that after protease-activated monomeric toxins bind to cadherin, initiation of a magnesium-dependent signaling pathway causes cell death. 14,15 In contrast, a recent version of the pore formation model 21 proposes the following sequence of events: proteaseactivated monomers bind to glycosylphosphatidylinositol (GPI)-anchored proteins, including aminopeptidases and alkaline phosphatases.…”

mentioning

confidence: 99%

“…14,15 The signaling model suggests that after protease-activated monomeric toxins bind to cadherin, initiation of a magnesium-dependent signaling pathway causes cell death. 14,15 In contrast, a recent version of the pore formation model 21 proposes the following sequence of events: proteaseactivated monomers bind to glycosylphosphatidylinositol (GPI)-anchored proteins, including aminopeptidases and alkaline phosphatases. This interaction promotes binding of toxin monomers to cadherin, which facilitates protease cleavage of the N terminus of the toxin, including helix α-1 of domain I, inducing oligomerization of the toxin.…”

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confidence: 99%

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Efficacy of genetically modified Bt toxins against insects with different genetic mechanisms of resistance

et al. 2011

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Transgenic crops that produce Bacillus thuringiensis (Bt) toxins are grown widely for pest control, 1 but insect adaptation can reduce their efficacy. [2][3][4][5][6] The genetically modified Bt toxins Cry1AbMod and Cry1AcMod were designed to counter insect resistance to native Bt toxins Cry1Ab and Cry1Ac. 7 Previous results suggested that the modified toxins would be effective only if resistance was linked T A B A S H N I K E T A L ., N A T U R E B I O T E C H N O L O G Y 2 9 : 1 2 ( D E C E M B E R 2 0 1 1 )2 with mutations in genes encoding toxin-binding cadherin proteins. 7 Here we report evidence from five major crop pests refuting this hypothesis. Relative to native toxins, the potency of modified toxins was >350-fold higher against resistant strains of Plutella xylostella and Ostrinia nubilalis in which resistance was not linked with cadherin mutations. Conversely, the modified toxins provided little or no advantage against some resistant strains of three other pests with altered cadherin. Independent of the presence of cadherin mutations, the relative potency of the modified toxins was generally higher against the most resistant strains.The toxins produced by Bt kill some major insect pests but cause little or no harm to people and most other organisms. 8 Bt toxins have been used in sprays for decades and in transgenic plants since 1996 (ref. 6). Transgenic corn and cotton producing Bt toxins were planted on >58 million hectares worldwide in 2010 (ref. 1). The primary threat to the longterm efficacy of Bt toxins is the evolution of resistance by pests. [2][3][4][5][6] Many insects have been selected for resistance to Bt toxins in the laboratory, and some populations of at least eight crop pests have evolved resistance to Bt toxins outside of the laboratory, including two species resistant to Bt sprays and at least six species resistant to Bt crops. [2][3][4][5][6][9][10][11][12][13] The most widely used Bt toxins are crystalline proteins in the Cry1A family, particularly Cry1Ab in transgenic Bt corn and Cry1Ac in transgenic Bt cotton, which kill some lepidopteran larvae. 3 Cry1A toxins bind to the extracellular domains of cadherin, aminopeptidase, and alkaline phosphatase in larval midgut membranes. 14,15 Disruption of Bt toxin binding to midgut receptors is the most common general mechanism of insect resistance. 9 Mutations in the genes encoding midgut cadherins that bind Cry1Ac are linked with resistance in at least three lepidopteran pests of cotton, [16][17][18] but such cadherin mutations are not the primary cause of many other cases of field-and laboratory-selected resistance. 9,19,20 Although some aspects of the mode of action of Bt toxins remain unresolved, extensive evidence shows that after Cry1A protoxins are ingested by larvae, they are solubilized in the gut and cleaved by mid-gut proteases such as trypsin to yield activated 60-kD monomeric toxins that bind with membrane-associated receptors. 14,15 The signaling model suggests that after protease-activated monomeric toxins bind to ca...

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“…The most common mechanism of resistance is by the disruption of binding of Bt toxin to receptors in the mid-gut membrane. This disruption might be either due to mutations in the receptors or changes in the expression of the receptors (Fuentes et al, 2011;Tiewsiri and Wang, 2011). The resistance mechanism associated with ABC transporter loci has also been reported (Baxter et al, 2011).…”

Section: Bacterial Insecticidesmentioning

confidence: 93%

Microbial agents against Helicoverpa armigera: Where are we and where do we need to go?

Vijayabharathi¹,

Kumari²,

Gopalakrishnan³

2014

Afr. J. Biotechnol.

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Plants are prone to various biotic stresses in nature by bacteria, viruses, fungi, parasites, harmful insects and weeds. The biggest percentage loss (70%) in plants is attributed to insects. Lepidoptera is one such diversified phytophagous insect group, which include Helicoverpa armigera, a key pest of many food crops including chickpea, pigeonpea, pea, lentil, chillies, sunflower, tomato, tobacco and cotton. Controlling this insect has been a big task for farmers leading to the manufacture of a plethora of pesticides. However, over reliance on chemical pesticides has resulted in problems including safety risks, environmental contamination, outbreaks of secondary pests, insecticide resistance and decrease in biodiversity. Hence, there is an urgent need for the development of eco-friendly methods such as entomopathogens, antagonist or competitor populations of a third organism and botanicals to suppress H. armigera. Also, many compounds from microorganisms have been found to be effective in crop production, and these have a role in controlling H. armigera. The actinomycetes play an astounding role in controlling the key plant pathogens. They are the representative genera of higher microbial mass in the soil. Numerous studies have shown that these productive actino-bacteria can generate an impressive array of secondary metabolites such as antibiotics, antitumor agents, insecticides etc. This review emphasizes the mechanism behind resistance to insecticides along with actinomycetes and its potential as a biocontrol agent against H. armigera.

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Reduced Levels of Membrane-Bound Alkaline Phosphatase Are Common to Lepidopteran Strains Resistant to Cry Toxins from Bacillus thuringiensis

Cited by 147 publications

References 70 publications

Gain and loss of multiple functionally related, horizontally transferred genes in the reduced genomes of two microsporidian parasites

Gain and loss of multiple functionally related, horizontally transferred genes in the reduced genomes of two microsporidian parasites

Efficacy of genetically modified Bt toxins against insects with different genetic mechanisms of resistance

Microbial agents against Helicoverpa armigera: Where are we and where do we need to go?

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