Impact of Bt cotton on the immune system and histology of the midgut of the fall armyworm Spodoptera frugiperda (J.E. Smith) (Lepidoptera: Noctuidae)

Abstract

Despite the efficiency of transgenic plants expressing Bacillus thuringiensis (Bt) toxins as insecticides against several lepidopterans, Spodoptera frugiperda (J.E. Smith) (Lepidoptera: Noctuidae) is one species that presents low susceptibility to most Bt crops. This study investigated the effects of the Cry 1 Ac toxin expressed by Bt cotton in the midgul of S. frugiperda and its effects on the humoral and cellular immune responses. Three hypotheses were proposed and tested with contributing factors for the natural tolerance oíS. frugiperda: (i) midgut regenerative cells are activated by the CrylAc toxin, and thus renew the epithehal cells damaged by the protein, (ii) CrylAc increased production of nitric oxide or phenoloxidase in the hemolymph, and (iii) there are qualitative and quantitative variations in the hemocyte levels of S. frugiperda. Caterpillars were reared using Bt cotton (Acala 90B) and non-Bt isolines (Acala 90), from the first to the fourth instar. The Bt cotton promoted elongation of the epithehal cells in the midgut of S. frugiperda caterpillars. Hence, evidence only supported the hypothesised increase of phenoloxidase (ii) and qualitative and quantitative differences in hemocyte levels (iii) in insects that were fed with Bt and non-Bt cotton. These parameters seem to explain the low susceptibihty of S. frugiperda to CrylAc toxin and they are a viable set of responses for the evaluation of other xenobiotic factors.

Intestinal regeneration as an insect resistance mechanism to entomopathogenic bacteria

“…Moreover, no increase in ISC proliferation was detected after exposure of susceptible larvae to the Bt pesticide, suggesting that S. exigua larvae may not respond to exposure to Cry toxins by activating the gut healing response. In agreement with this observation, feeding of Spodoptera frugiperda larvae on Bt cotton producing the Cry1Ac toxin resulted in epithelial damage, which was not associated with an increase in ISCs when comparing to feeding on non-Bt cotton isoline [68]. Because diverse time points were not examined in those reports, an alternative explanation for these observations of no ISC increase is that the ISC differentiation was predominant over proliferation during the time of observation, as suggested from observations of Alabama argillacea exposed to Bt cotton [69] or exposure to Bt pesticides in susceptible and resistant strains of Plutella xylostella [70].…”

Hemocyte response to treatment of susceptible and resistant Asian corn borer (Ostrinia furnacalis) larvae with Cry1F toxin from Bacillus thuringiensis

“…Galleriae ( 54 ). Importantly, Cry1A-resistant strains of O. furnacalis ( 31 ), H. armigera ( 55 ) and S. frugiperda ( 56 ) showed higher levels of hemolymph phenoloxidase activity when exposed to Cry1A toxins compared to susceptible insects, suggestive of a potential contribution to the resistant phenotypes.…”

Analysis of Cry1Ah Toxin-Binding Reliability to Midgut Membrane Proteins of the Asian Corn Borer

“…The effectiveness of certain bioinsecticides may be correlated to the activation of proPO [ 63 ]. PO levels of Helicoverpa armigera and S. frugiperda were elevated after the larvae were exposed to Cry1Ac toxin [ 32 , 34 ]. In the event of Cry toxicity, the midgut epithelium was gradually breached by the Cry toxins.…”

“…In addition, other different proteins have been reported, such as the ATP-binding cassette (ABC—ABCC2, ABCC3 and ABCA2) transporter [ 25 , 26 , 27 , 28 ], actin, Hsp70 and V-ATPase [ 29 , 30 , 31 ]. In addition to all these membrane proteins, it was reported that immune-related proteins might also contribute to the development of resistance [ 32 , 33 , 34 , 35 , 36 ]. Recently, a study brought evidence of the possible direct binding of the Cry1Ah toxin to phenoloxidase (PO) and other immune-related proteins identified in BBMV samples extracted from susceptible and resistant strains of ACB [ 36 ].…”