Spontaneous transposition of HzSINE1 into CYP321A2 is undetectable in the field populations of Helicoverpa zea

Authors: LI, SHENGYUN - Nanjing Agricultural University; CHEN, SONG - University Of Arizona; DONG, SHUANGLIN - Nanjing Agricultural University; ZHANG, MIN - Zhengzhou University; DENG, ZHONGYUAN - Zhengzhou University; Ni, Xinzhi; HUANG, JINYONG - Zhengzhou University; LI, XIANCHUN - University Of Arizona

Submitted to: Journal of Asia-Pacific Entomology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 7/20/2021
Publication Date: 7/22/2021
Citation: Li, S., Chen, S., Dong, S., Zhang, M., Deng, Z., Ni, X., Huang, J., Li, X. 2021. Spontaneous transposition of HzSINE1 into CYP321A2 is undetectable in the field populations of Helicoverpa zea. Journal of Asia-Pacific Entomology. 24:882-888. https://doi.org/10.1016/j.aspen.2021.07.015.
DOI: https://doi.org/10.1016/j.aspen.2021.07.015

Interpretive Summary: The corn earworm is a highly polyphagous insect pest of economic importance that can feed on over one hundred reported host plant species, including major crops such as cotton, corn and soybean. Meanwhile, the corn earworm is one of the major pests controlled by insecticides and transgenic crops expressed with insecticidal proteins from a bacterium. These control measures are only partially successful, as the corn earworm has great capacity to rapidly acquire resistance to synthetic insecticides and bacterial toxins. Designing novel strategies for management of this polyphagous pest necessitates deciphering the genetic and molecular mechanisms with which the corn earworm copes with its diverse and unpredictable plant defense and insecticide challenges. Previous literature has partially elucidated the mechanisms of adaptation in this generalist herbivore to plant allelochemicals and insecticides. These include a group of 6 well-known allelochemical/insecticide-detoxifying enzymes. The 6 detoxification genes are enriched with 12 different types of transposable elements (also known as jumping genes) capable of jumping from one location to another in a living organism’s genome. By retention and accumulation of the 12 transposable elements, the allelochemical/insecticide-detoxifying enzymes from the corn earworm can gain the transposable element-introduced advantageous variations otherwise not readily available to adapt successfully to the cropping systems with a wide range of host plant allelochemicals and insecticide applications. To examine whether the insertion of one of the 12 transposable elements, i.e., HzSINE1, into the coding sequence of one of the 6 detoxification genes, i.e., CYP321A2, could result in a new adaptative protein or a non-functional detoxification enzyme, the transcripts and deduced protein isoforms as well as the constitutive and plant allelochemical-induced expression of that transposable element-inserted detoxication gene were examined. In addition, frequency of that transposable element-inserted detoxification gene allele was examined in three corn earworm strains, which include one laboratory colony, one pyrethroid -resistant strain established with the field collected larvae from Indiana, and one field population collected from Georgia. The results show that that transposable element-inserted detoxification gene allele transcribes into two different allelochemical-inducible transcripts that encode one identical heme-binding region-truncated detoxification enzyme. And that transposable element-inserted detoxification gene allele is fixed in the laboratory strain reared with xenobiotic-free artificial diets, while it is undetectable in the Georgia field population and the pyrethroid-resistant strain. These results suggest that insertion of that transposable element into the coding region of that detoxification gene results in one non-functional detoxification enzyme that can persist only in the toxin-free environment.

Technical Abstract: The enrichment of transposable elements (TEs) within allelochemical- and insecticide-metabolizing P450 alleles in Helicoverpa zea enables these P450s to gain TE-introduced adaptive variations otherwise not readily available to cope with the ever-changing and diverse xenobiotic stress factors in varying cropping systems. The critical role of each TE-inserted P450 allele depends on whether the inserted P450 allele is more adaptive than its TE-free counterpart or not. Previous study has reported a HzSINE1-inserted CYP321A2 allele in a laboratory strain of H. zea reared with xenobiotic-free artificial diets. Here we show that the HzSINE1-inserted CYP321A2 allele transcribes into two HzSINE1 sequence-containing mutant mRNA isoforms of different length that encode an identical C terminus-truncated and heme-binding region deleted non-functional P450. Nonetheless, HzSINE1 insertion does not disrupt the regulatory functional aspect of CYP321A2 since this allele is constitutively expressed and highly inducible by the allelochemicals xanthotoxin, quercetin and chlorogenic acid. Furthermore, while the HzSINE1-inserted CYP321A2 allele is fixed in the laboratory strain, the insertion is purged in the bifenthrin-resistant strain and the Georgia field population of H. zea. To sum up, the HzSINE1-inserted CYP321A2 allele represents an allelochemical-inducible non-functional P450 allele that is selected against in the field populations frequently encountering toxic plant allelochemicals and synthetic insecticides. However, such an insertion can reach fixation under the xenobiotic-free laboratory rearing conditions most likely due to random genetic drift across multiple generations.