Global challenges faced by engineered Bacillus thuringiensis Cry genes in soybean (Glycine max L.) in the twenty-first century

Abstract

The most important insect pests causing severe economic damages to soybean (Glycine max L.) production worldwide are Chrysodeixis includens (Walker, Noctuidae), Anticarsia gemmatalis (Hübner, Erebidae), Helicoverpa gelotopoeon (Dyar, Noctuidae), Crocidosema aporema (Walsingham; Tortricidae), Spodoptera albula (Walker, Noctuidae), S. cosmiodes (Walker, Noctuidae), S. eridania (Stoll, Noctuidae), S. frugiperda (Smith; Noctuidae), Helicoverpa armigera (Hübner, Noctuidae), H. zea (Boddie; Noctuidae) and Telenomus podisi (Hymenoptera,Platygastidae). Despite the success of biotech Bacillus thuringiensis (Bt)/herbicide tolerance (HT)-soybean in the past decade in terms of output, unforeseen mitigated performances have been observed due to changes in climatic events that favors the emergence of insect resistance. Thus, there is a need to develop hybrids with elaborated gene stacking to avert the upsurge in insect field tolerance to crystal (Cry) toxins in Bt-soybean. This study covers the performance of important commercial transgenic soybean developed to outwit destructive insects. New gene stacking soybean events such as Cry1Ac-, Cry1AF- and PAT-soybean (DAS-81419-2^®, Conkesta™ technology), and MON-87751-7 × MON-87701-2 × MON 87708 × MON 89788 (bearing Cry1A.105 [Cry1Ab, Cry1F, Cry1Ac], Cry2Ab, Cry1Ac) are being approved and deployed in fields. Following this deployment trend, we recommend herein that plant-mediated RNA interference into Bt-soybean, and the application of RNA-based pesticides that is complemented by other best agricultural practices such as refuge compliance, and periodic application of low-level insecticides could maximize trait durability in Bt-soybean production in the twenty-first century.

Keywords: Armyworm; Gene pyramiding; RNA inference; RNAi-based pesticides; Refuge strategy; Resistance.

Fig. 1

a World soybean production forecast summary. The production growth rate is disaggregated into area harvested and yield growth rates. We generated the graph based on prediction data generated in Masuda and Goldsmith (2009) and FAOSTAT (2012). At present, India is only producing high-yielding conventional soybean. b Emergence of destructive fall armyworm (Spodoptera frugiperda) observed in Bt-soybean farms in Vanderbijlpark, Gauteng, South Africa in 2017

Fig. 2

Molecular analysis of two Cry-protoxins (Cry1Ac and Cry1Ab) commonly introgressed in Bt-soybean. A Molecular phylogenetic analysis by maximum likelihood (ML) method and bootstrap values ≥ 50% from 1000 iterations are shown and the ML tree was rooted as previously described (Louis et al. 2014). b Three-dimensional structure of Cry1Ac (GenBank accession KKB28329.1) and CryAb (GenBank accession AEV45790.1) protoxins modeled in Phyre2 server at 90% accuracy at intensive mode. c Overall view of the functional domain of Cry1Ac or Cry1Ab

Fig. 3

a Modification of Ortega et al. (2016) depicting the strategy of pyramiding QTLs resistance with Cry1Ac-protoxin to control various soybean chewing insects. Here, Benning^{M−E−Cry1Ac} was found to be more resistant than Benning^ME and Benning^Cry1Acagainst soybean looper Chrysodeixis includens (Walker) and Southern armyworm Spodoptera eridania (Cramer). b Cry was coupled with artificial microRNAs to specifically target pests

Fig. 4

Important δ-endotoxins crystal proteins such as Cry1 (~ 130 kDa specifically target butterflies and beetles) Cry2 (~ 70 kDa specifically target butterflies and Diptera), Cry3 (~ 70 kDa specifically target beetles), and Cry4 (~ 130 kDa specifically target Diptera) (Palma et al. ; Ibrahim and Shawer 2014). Coupling PMRi with stacked Cry genes could better protect Bt-soybean against destructive insects