Abstract
Crop loss due to pests could reach as high as 70% if preventive measures with either pesticide, natural enemies, host plant resistance or other nonchemical controls are not used. Even if several conventional crop protection methods are in place, Bacillus thuringiensis (Bt)-based bioprotection of crops has been taking prominence. However, several studies documented that pests are yet developing resistance to Bt crops or Bt-based biopesticides. Hence, there is still a need to explore other alternative effective strategies that could stand on its own or could be integrated with other pest management tools. To the effect, gene pyramiding has recently been explored as a relatively sustainable alternative. Very recently some studies have been carried out to pyramid different Bt-sourced cry genes and even other genes like the one encoding for phytase enzyme. Such technique is a relatively recent advancement and one of the most important novel genetic engineering tools of the time that is yet to go mainstream, despite its untapped potential. Therefore, in this chapter, we tried to compare different crop protection strategies and make a point that gene pyramiding could be a better alternative if not the only one for sustainable pest management.
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Keywords
- Gene pyramiding
- Horizontal resistance
- Vertical resistance
- Bacillus thuringiensis
- Bt biopesticides
- Bioprotection
15.1 Introduction
Crop loss due to pests is a major concern worldwide which could reach as high as 70% if preventive measures with either pesticide, natural enemies, host plant resistance or other controls are not utilized. About 67,000 pest species damage crops, of which 9000 contribute to insect species and mites (Ibrahim and Shawer 2014). Furthermore, insects are the primary direct cause of crop losses, whereas the indirect object is by the impaired quality of the products and their roles as vectors of various plant pathogens (Kumar et al. 2006). Apart from that, crops contribute a significant part of the world food supply to maintain the growing human population (Osman et al. 2015; Oerke 2006). Most developing countries still rely on agriculture as their primary source of food. Hence, the development and protection of agriculture are very critical in sustaining the growing human population worldwide.
Crop protection could be achieved, though not sustainably, through conventional methods like application of chemical pesticides and other cultural approaches. Yet, bioprotection of crop plants from insect pests via application of natural enemies is relatively sustainable and environmentally friendly. Bacillus thuringiensis (Bt)-based technologies like Bt crops have widely been used with relative success. However, recent reports indicated that Bt crops are losing sustainability as insects pests are learning to somehow develop resistance to withstand pressure exerted by Bt crops, thereby compromising Bt crop’s resistance to pests [for further reading you may refer to a review by Feto (2016)]. Hence, the decades old ‘single-gene-Bt crop’ technology started to fail. Thus, there is a need to come up with an alternative sustainable tool to fill the void.
On the other hand, the novel Bt-based gene pyramiding could serve as an alternative to ‘single-gene-Bt crop’. Though the tool has yet to go mainstream, success has already been reported (Jain et al. 2017).
Therefore, this review will explore further on Bt as the most suitable natural source of genes that could be used to provide durable resistance in crops, since the multiple genes that make up the pyramid will render the transgene resistant to multiple pests.
Therefore, in this chapter different crop protection strategies are compared, and efforts have been made to underline that the gene pyramiding could be a better alternative if not the only one for sustainable pest management.
15.2 Prevalence of Crop Loss Worldwide
The incidence of crop loss worldwide is mainly due to insect attacks which can be as high as 70% if preventive measures are not used (Maxmen 2013). Previous reports have summarized the loss of crops to various insects and bacterial and fungal pests (Table 15.1). Most affected crops are wheat (Bahri et al. 2011), rice (Niu et al. 2017; Liu et al. 2016), cowpea (Okechukwu et al. 2010), soybean (Musser et al. 2016; Abudulai et al. 2012) and maize (Anderson et al. 2016; Grisley 1997). These crops are usually affected by pests such Xanthomonas axonopodis pv. Vignola (Xav), Nezara viridula and many more which require immediate attention.
15.3 Crop Protection Methods Against Pests
In the past, humans have searched for crops that can survive and produce under different biotic and abiotic stresses. Furthermore, farmers avoided yield loss through searching pest-resistant crops by collecting the seeds from only the highest yielding crops in their fields (Ibrahim and Shawer 2014) or through the application of chemical pesticides. Although chemical pesticides do result in reduced crop yield loss, more money is spent each year globally for inadequate control measures. Hence there is still a need to search for adequate protection of crops against pests.
15.3.1 Conventional or Traditional Methods and Its Drawbacks
Traditional crop protection method such as chemical control of pests was used as the most effective and attractive strategy in the previous century, during the 1940s and 1950s (Malav et al. 2016; Oerke 2006; Graves et al. 1999). Moreover, conventionally grown crops use more pesticides, and that represents the worst effect of chemically dependent agriculture. Although chemical pesticides are effective and had guaranteed a production increase in agriculture during the last 40 years, their continuous use is a primary cause of resistance and environmental concern (Mekonnen et al. 2017; Oerke 2006; Graves et al. 1999). These led to contamination of water and food sources, as well as the poisoning of nontarget beneficial pests and development of pests that are resistant to the chemical pesticides (Kumar et al. 2008; Scheyer et al. 2005).
Thus, the global public concern to seek alternative methods to control pests such as insects and fungal pathogens has increased due to the adverse effect of the application of chemical pesticides (Ibrahim and Shawer 2014). Furthermore, one approach could be the use of biological control methods such as biopesticides and entomopathogenic microorganisms like bacteria, fungi and viruses that include the development of technologies that would allow the insertion and functional expression of foreign genes in plant cells (Malav et al. 2016; Danny et al. 1992). Moreover, biological control reduces expenses and health hazards associated with pesticide formulations (Kouser and Qaim 2011). Hence, Bt has been used for several years as an alternative crop protection method to conventional methods.
15.3.2 Bt Biopesticide Methods
Currently, the application of Bt as a biological control method has increased crop production. Furthermore, Bt biopesticides are more effective as compared to the use of chemical pesticides which attribute more adverse effect due to contamination of the environment and food products and lead to human health problems (Tu et al. 2000). The insecticidal activity of Bt bacterium is due to the presence of the parasporal crystals (cry) which are formed during the sporulation phase of the bacterium and are assembled by the cry proteins that are expressed by the cry genes (Crickmore et al. 2017; Schnepf et al. 1998).
The Bt species has considerable variability due to the number of strains isolated around the world (Palma et al. 2014; Roh et al. 2007), the number of serotypes known to date (Roh et al. 2009) and the high number of crystal (cry) gene sequences accumulated so far. Despite the variability observed within this species, there is some uniformity in at least part, which shows some reflection on the five conserved blocks in the gene structure that is present in almost all the cry genes (De Maagd et al. 2001). Bt toxins create a heterozygous family of 74 different types of proteins (cry1–cry74) that are toxic to numerous insect pests such as lepidopteran, coleopteran, dipteran, hemipteran, some nematodes and snails’ species that cause a severe damage to economically important crops (Crickmore et al. 2017; Palma et al. 2014).
The cry toxins belonging to three domain families share similar and conserved three domain structures (Fig. 15.1) which display their differences in amino acid sequences (Pardo-Lopez et al. 2013). Also, domain I constitutes of seven α-helix clusters that are subjected to proteolytic cleavage in all three-domain cry proteins during toxin activation (Fig. 15.1). It is usually referred to as perforating domain and is located towards the N-terminus which may be responsible for toxin membrane insertion and pore formation (Ben-Dov 2014; Xu et al. 2014). Moreover, domain II or middle domain is responsible for toxin-receptor interactions, and it consists of three antiparallel β-sheets (Xu et al. 2014; Jenkins and Dean 2000). Besides, domain III which is usually referred to as the galactose-binding domain has two antiparallel β-sheet sandwiches (Fig. 15.1), which are also involved in receptor binding and pore formation (Xu et al. 2014). In addition, domain IV (Fig. 15.1) is mainly composed of alpha helices which resemble structural domains such as spectrin- or fibrinogen-binding complement inhibitor (Soberon et al. 2016).
15.3.2.1 Mechanism of Bt Biopesticides
The processing of the crystals relies on the solubilization of the toxins in the alkaline midgut of the insect pest and then activated by proteolytic digestion of the specific serine proteases (Palma et al. 2014). Interestingly, consumption of Bt toxins is found to be safe to humans because the intestinal walls of mammals do not have endotoxin receptor necessary for the toxic effect mainly due to the acidic conditions, and thus, the proteins tend to get degraded quickly in the stomach (Mekonnen et al. 2017). Some reports showed that cry gene specificity and activity could be influenced by other factors such as associated with toxin processing or stability in the insect midgut apart from the receptor binding (Jurat-Fuentes and Crickmore 2017). Moreover, cry genes are co-localized with other genes such as vegetative insecticidal proteins (vip) forming the insecticidal pathogenicity island (PAI) (Zhu et al. 2015).
15.4 Possible Challenges of Bt Toxins and Resistant Breakdown of Bt Crops
Bt has been studied for decades and is a used bacterial control agent to date. Nevertheless, several pest species have acquired field resistance to the most used Bt toxins and more severely to those included in transgenic crops (Peralta and Palma 2017). The currently used Bt toxins have not provided durable resistance due to the observed Bt resistance breakdown in the current Bt crops (Table 15.2) (Peralta and Palma 2017). An explanation for this may be due to the insects and pathogenic diversity displayed by most pests which lead to a rapid breakdown of specific resistance genes (Peralta and Palma 2017; Geffroy et al. 1999). Even though numerous reports involve the insect resistance over Bt-based formulations, field-evolved resistance has occurred which is promoted by the selective pressure applied over some insect populations (e.g. the lepidopteran Trichoplusiani) (Song et al. 2015). Furthermore, this occurs frequently in the most used Bt crops in agriculture, especially those from the first generation that express only one protein and plants that have multiple genes which have similar toxins.
Previously, some reports indicated the reduced efficacy of second-generation Bt cotton and corn harbouring cry1Ac + cry2Ab and cry1A.105 + cry2Ab against Helicoverpa zea and Spodoptera frugiperda, respectively (Table 15.2) (Santos-Amaya et al. 2015; Brévault et al. 2013). Furthermore, some authors reported on field resistance of Bt spray (Table 15.2) containing cry1C or cry1Ac observed in maize and cotton (Brévault et al. 2013; Campagne et al. 2013). Hence, there is a need in continuous search for novel Bt strains that have a broad spectrum range and could potentially circumvent the resistant issue, thus requiring the novel strategies that could anticipate the evolutionary responses of insects pests (Peralta and Palma 2017). Therefore, the best possible crop protection strategy could be pyramiding genes in such a way that could address both vertical and horizontal resistance in plants.
15.5 Transgenic Bt Crops
Genes from Bt have currently received increased attention due to their broad range of biotechnological applications, especially in agriculture for biocontrol of harmful insects and fungal pathogens (Kuddus and Ahmad 2013). These single or multiple cry-based genes could be inserted into crops, resulting in transgenic crops that are resistant to insects and fungal pathogens.
15.5.1 Single Cry-Based Bt Crops
Single cry-based Bt crops are crops incorporated with only a single cry toxin. However, single cry-based Bt crops are most likely prone to resistant breakdown than multiple cry-based Bt crops (Keshavareddy and Kumar 2018). These might be due to the pest developing resistance towards the crop mainly because the pests tend to adapt to the treatment conditions very quickly than in multiple cry-based crops. Moreover, commercialization of Bt crops such as maize, cotton and soybean worldwide has significantly reduced the application of synthetic pesticides (Keshavareddy and Kumar 2018; Ferré and Van Rie 2002). In addition, some reports showed the effective control of Bt rice such as KMD (cry1Ab), T1c-9 (cry1C) and T2A-1 (cry2A) to target lepidopteran insects (Table 15.3) including stem borers and leaf folders (Wang et al. 2016; Zheng et al. 2011; Chen et al. 2005).
15.5.2 Multiple Cry-Based Bt Crops
The multiple cry-based Bt crops are crops incorporated with two or more cry toxins. Even though multiple cry-based genes were used in transgenic crops before such as chickpea and brassica (Table 15.3), the broad-spectrum range has not been considered, or the incorporated multiple genes shared similar toxins. Hence, there is a resistant development as well (Meenakshi et al. 2011; Cao et al. 2008). Therefore, a wide range of sequences known to date is attributed to intense interest in finding novel cry proteins with alternative toxins that has a broad spectrum to manage the resistant breakdown observed in the current Bt crops (Ibrahim and Shawer 2014). These could be done with the application of Bt-based gene pyramiding as a genetic tool for inserting multiple genes that do not share the same toxins. As studies show Bt crops consisting of a single cry-based gene or multiple cry-based genes sharing the same toxins tends to be more prone to pest resistance (Keshavareddy and Kumar 2018).
15.6 Gene Pyramiding Method
Gene pyramiding is a method of assembling or stacking multiple genes to improve durable resistance in crops against insects or diseases which is crucial for stable food production. Moreover, breeding resistance crops with either single or multiple Bt-based cry genes is the most cost-effective and environment-friendly strategy for resistance management. The advantage of gene pyramiding is that it uses the same strategy as that of the pesticidal mixture to broaden the resistance spectrum in crops. In addition, if two or more resistant genes are incorporated in a crop, it is less likely for the crop to be attacked by a pathogen race resistant to both genes or for the plant to lose both genes at the same time (Meenakshi et al. 2011). Furthermore, due to biotic factors, gene pyramiding is a cost-effective and environmentally friendly method used to manage crop production. Hence it has become the most used method for developing durable resistance in crops against pests (Meziadi et al. 2016; Fukuoka et al. 2015).
Previous reports on Bt-based gene pyramiding have shown an outstanding performance against insects where Bt toxins were incorporated in rice (Ye et al. 2009; Chen et al. 2008). Moreover, the integrated genes into elite cultivars with different genetic background were introduced by sexual crossing. Hence, in field evaluations, the improved lines also showed excellent efficacy against the target insects (Liu et al. 2016; Yang et al. 2011). So recently, different types of gene pyramiding such as conventional gene pyramiding and molecular gene pyramiding are widely used to obtain durable resistance in crops (Meenakshi et al. 2011).
15.6.1 Conventional Gene Pyramiding
Conventional gene pyramiding also known as serial gene pyramiding is a method where genes are arranged in the same plant one after another. These include pedigree crossing, backcross breeding and recurrent selection (Table 15.4). The identification of sources of useful genes is very slow using traditional methods. Hence, breeders’ capability to trace the presence or absence of the target genes is limited, thus resulting in the limited number of genes incorporated into selected cultivars (Malav et al. 2016).
15.6.2 Molecular Gene Pyramiding
Molecular gene pyramiding also referred to as simultaneous gene pyramiding is a method where genes are arranged at the same time in a plant (Srivastava et al. 2017). These include marker-assisted selection and transgenic methods (Table 15.4). The differences among the two gene pyramiding methods are summarized below (Table 15.4). In addition, molecular gene pyramiding such as transgenic method is more advantageous over other pyramiding methods (Keshavareddy and Kumar 2018). Although there has been a success in Bt crop production, there are some drawbacks concerning Bt-based gene pyramiding.
15.7 Potential Challenges of Gene Pyramiding
Although gene pyramiding is a widely adopted strategy for improvement of crops against resistant effects, there are certain drawbacks associated with this strategy. In addition, the reliability of phenotyping at an individual level is minimal since the presence of target traits must first be confirmed. Phenotyping influences the inheritance model of genes for the target traits, linkage and pleiotropism between the target traits at an individual level (Malav et al. 2016; Riaz et al. 2006).
Another drawback involves the limitation of successfully pyramided transgenic crops for enhanced fungal and bacterial resistance (Summers and Brown 2013; Punja 2006; Schnepf et al. 1998). These may be due to two primary life strategies of pathogens, namely, biotrophy and necrotrophy. Thus, biotrophic pathogens essentially act as a sink for the hosts’ anabolic assimilates which keep it alive, while necrotrophic pathogens consume the hosts’ tissues as invaded. As a result, plants developed different approaches to deal with these two strategies (Summers and Brown 2013; Punja 2006) which are not obtained through genetic engineering.
Lastly, to avoid recognition by host (R) genes, the pathogen avirulence (Avr) gene undergoes strong diversifying selection or mutation (Ferry et al. 2004). The low level of pathogenic resistance by some transgenic crops coupled with a negative perception of genetic engineering-modified crops has resulted in few transgenic crops (Palma et al. 2014) being brought to the market due to the relatively small number of transgenic crops available (Mekonnen et al. 2017).
Apart from those resistant to fungal and bacterial pathogens, virus-resistant crops are not commercially available (Collinge et al. 2007). Hence, many transformation strategies have been used to increase fungal, bacterial and viral resistance in crops (Mekonnen et al. 2017). In addition, this includes introgressing R genes and introducing genes coding for antimicrobial compounds such as chitinase and glucanase enzymes that break down the fungal cell walls (chitin or glucan) and also upregulating defence pathways through promoter transfer, disarming host susceptibility genes, detoxifying pathogen virulence factors (toxins), increasing structural barriers and silencing essential pathogen genes (RNA silencing, RNA interference or RNAi) (Vincelli 2016; Collinge et al. 2007; Schnepf et al. 1998). Hence, two R genes were introgressed to develop rice cultivars resistant to bacterial blight and bacterial streak diseases in a study conducted by Zhou et al. (2008).
15.8 Conclusion and Future Prospects
The addressed reports presented insights into the fundamental basis of Bt isolates with broad spectrum, subjected to screening programmes to evaluate their insecticidal activity. The current review shows that the production and continuing development of Bt crops has been a major scientific success up to date which is deployed by the expression of Bt toxins. However, several studies documented that pests are developing resistance to Bt crops or Bt biopesticides. This situation is mostly observed in the current Bt crops that are incorporated with cry2 genes and lower. Hence, there is still a need to explore other effective strategies that could stand on its own or could be integrated with other control measures to diversify the resistance management tools.
Therefore, in this chapter, we tried to compare different crop protection strategies and make a point that gene pyramiding could be a better alternative if not the only one. These could include the involvement of pyramiding Bt toxins with other genes such as phytase, vip3 and other genes to broaden the spectrum. Another management tool could consist of the crop rotation method of cultivating Bt crops with other non-Bt crops to try and confuse the pests. However, there must be an assurance that the development of pest resistance genes does not compromise the protection of produced Bt crops. Furthermore, there are commercially available Bt crops with single or multiple toxins which reduced the application of chemical pesticides.
This review stipulated possible challenges that can inhibit the efficiency of gene pyramiding. Hence, extensive and precise phenotyping is required to counteract the difficulties in gene pyramiding. These involve the dissection of phenotypes into components that can improve the heritability, thus aiding the understanding of biological systems causing the phenotype (Varshney et al. 2005). Another strategy is phenotyping characterization of large mutagenized populations and tilling populations which could link a gene with phenotype. Apart from the challenges of gene pyramiding and current resistant breakdown in Bt crops, Bt will continue to play a significant role as a candidate bacterium for pyramiding multiple toxin genes into crops for resistant management due to its broad spectrum of resistance from the natural origin. Very recently some studies have been carried out to pyramid different Bt-sourced cry genes. Such kind of strategy is a relatively recent advancement that should be explored further.
References
Abudulai M, Salifu AB, Opare-Atakora D, Haruna M, Denwar NN, Baba II (2012) Yield loss at the different growth stages in soybean due to insect pests in Ghana. Arch Phytopathol Plant Protect 45:1796–1809
Ahmed N, Saini J, Sharma R, Seth MJHJoAR (2017) Performance of chickpea under organic and inorganic sources of nutrients at different soil moisture regimes in chickpea-okra cropping system. Himachal J Agric Res 43:23–28
Allard RW, Allard RW (1999) Principles of plant breeding. Wiley, New York
Anderson SJ, Simmons HE, French-Monar RD, Munkvold GP (2016) Susceptibility of maize inbreds and incidence of symptomless infection by the head smut pathogen, sphacelotheca reilana. Plant Health Prog 17:1–5
Bahri B, Shah S, Hussain S, Leconte M, Enjalbert J, De Vallavieille-Pope C (2011) Genetic diversity of the wheat yellow rust population in Pakistan and its relationship with host resistance. Plant Pathol 60:649–660
Ben-Dov E (2014) Bacillus thuringiensis subsp. Israelensis and its dipteran-specific toxins. Toxins 6:1222–1243
Brévault T, Heuberger S, Zhang M, Ellers-Kirk C, Ni X, Masson L et al (2013) Potential shortfall of pyramided transgenic cotton for insect resistance management. Proc Natl Acad Sci 110:5806–5811
Campagne P, Kruger M, Pasquet R, Le Ru B, Van Den Berg J (2013) Dominant inheritance of field-evolved resistance to bt corn in busseola fusca. PLoS One 8:e69675
Cao J, Zhao J-Z, Tang J, Shelton A, Earle E (2002) Broccoli plants with pyramided cry1ac and cry1c bt genes control diamondback moths resistant to cry1a and cry1c proteins. Theor Appl Genet 105:258–264
Cao J, Shelton AM, Earle ED (2008) Sequential transformation to pyramid two bt genes in vegetable indian mustard (brassica juncea l.) and its potential for control of diamondback moth larvae. Plant Cell Rep 27:479
Chen H, Tang W, Xu C, Li X, Lin Y, Zhang Q (2005) Transgenic indica rice plants harboring a synthetic cry2a∗ gene of bacillus thuringiensis exhibit enhanced resistance against lepidopteran rice pests. Theor Appl Genet 111:1330
Chen H, Zhang G, Zhang Q, Lin Y (2008) Effect of transgenic bacillus thuringiensis rice lines on mortality and feeding behavior of rice stem borers (lepidoptera: Crambidae). J Econ Entomol 101:182–189
Cheng X, Sardana R, Kaplan H, Altosaar I (1998) Agrobacterium-transformed rice plants expressing synthetic cryia (b) and cryia (c) genes are highly toxic to striped stem borer and yellow stem borer. Proc Natl Acad Sci 95:2767–2772
Collinge DB, Lund OS, Thordal-Christensen H (2007) What are the prospects for genetically engineered, disease resistant plants? In: Sustainable disease management in a european context. Springer, Dordrecht
Crickmore N. (2017) Bacillus thuringiensis Toxin Classification. In: Fiuza L., Polanczyk R., Crickmore N. (eds) Bacillus thuringiensis and Lysinibacillus sphaericus. Springer, Cham
Danny J, Llewellyn M, Brown Y, Cousins Y, Hartweck D, Last A, et al (1992) The science behind transgenic cotton plants. In: Proceedings of 6th Australian cotton conference, Broadbeach and Queensland, Australia
Datta K, Baisakh N, Thet KM, Tu J, Datta S (2002) Pyramiding transgenes for multiple resistance in rice against bacterial blight, yellow stem borer and sheath blight. Theor Appl Genet 106:1–8
De Maagd RA, Bravo A, Crickmore N (2001) How bacillus thuringiensis has evolved specific toxins to colonize the insect world. Trends Genet 17:193–199
Dhurua S, Gujar GT (2011) Field-evolved resistance to bt toxin cry1ac in the pink bollworm, pectinophora gossypiella (saunders)(lepidoptera: Gelechiidae), from India. Pest Manag Sci 67:898–903
Ferré J, Van Rie J (2002) Biochemistry and genetics of insect resistance to b acillus thuringiensis. Annu Rev Entomol 47:501–533
Ferry N, Edwards MG, Gatehouse JA, Gatehouse AM (2004) Plant–insect interactions: molecular approaches to insect resistance. Curr Opin Biotechnol 15:155–161
Feto NA (2016) Bacillus spp. and their biotechnological roles in green industry. Bacilli and Agrobiotechnology. In: Islam MT, Rahman MM, Pandey P, Jha CK, Aeron A (eds) Bacilli and Agrobiotechnology. Springer Verlag. ISBN: 978-3-319-44408-6, pp 143–162. https://doi.org/10.1007/978-3-319-44409-3
Fukuoka S, Saka N, Mizukami Y, Koga H, Yamanouchi U, Yoshioka Y et al (2015) Gene pyramiding enhances durable blast disease resistance in rice. Sci Rep 5:7773
Gahan LJ, Ma Y-T, Macgregorcoble ML, Gould F, Moar WJ, Heckel DG (2005) Genetic basis of resistance to cry1ac and cry2aa in heliothis virescens (lepidoptera: Noctuidae). J Econ Entomol 98:1357–1368
Geffroy V, Sicard D, De Oliveira JC, Sévignac M, Cohen S, Gepts P et al (1999) Identification of an ancestral resistance gene cluster involved in the coevolution process between phaseolus vulgaris and its fungal pathogen colletotrichum lindemuthianum. Mol Plant-Microbe Interact 12:774–784
Graves JB, Leonard BR, Ottea J (1999) Chemical approaches to managing arthropod pests. In: Handbook of Pest Management. Marcel Dekker, Inc, New York, pp 449–486
Grisley W (1997) Crop-pest yield loss: a diagnostic study in the Kenya highlands. Int J Pest Manag 43:137–142
Ibrahim RA, Shawer DM (2014) Transgenic bt-plants and the future of crop protection (an overview). Int J Agric Food Res 3(1):14–40
Jackson R, Bradley J Jr, Van Duyn J (2004) Performance of feral and cry1ac-selected helicoverpa zea (lepidoptera: Noctuidae) strains on transgenic cottons expressing one or two bacillus thuringiensis ssp. Kurstaki proteins under greenhouse conditions. J Entomol Sci 39:46–55
Jain D, Sunda SD, Sanadhya S, Nath DJ, Khandelwal SK (2017) Molecular characterization and pcr-based screening of cry genes from bacillus thuringiensis strains. 3 Biotech 7:4
Jenkins JL, Dean DH (2000) Exploring the mechanism of action of insecticidal proteins by genetic engineering methods. In: Genetic engineering. Springer, Boston
Jiang G, Xu C, Tu J, Li X, He Y, Zhang Q (2004) Pyramiding of insect-and disease-resistance genes into an elite indica, cytoplasm male sterile restorer line of rice, ‘minghui 63′. Plant Breed 123:112–116
Jiang F, Zhang T, Bai S, Wang Z, He K (2016) Evaluation of Bt corn with pyramided genes on efficacy and insect resistance management for the Asian corn borer in China. PLoS One 11:e0168442
Jurat-Fuentes JL, Crickmore N (2017) Specificity determinants for cry insecticidal proteins: insights from their mode of action. J Invertebr Pathol 142:5–10
Keshavareddy G, Kumar A (2018) Characterization of bt transgenic plants: a review. Int J Curr Microbiol App Sci 7:3035–3051
Kouser S, Qaim M (2011) Impact of bt cotton on pesticide poisoning in smallholder agriculture: a panel data analysis. Ecol Econ 70:2105–2113
Kuddus M, Ahmad I (2013) Isolation of novel chitinolytic bacteria and production optimization of extracellular chitinase. J Genet Eng Biotechnol 11:39–46
Kumar S, Chandra A, Pandey K (2006) Genetic transformation of lucerne (medicago sativa l.) for weevil (hypera postica) resistance. In: Extended Summaries, national seminar transfiguration crops Indian agriculture: status, risks and acceptance, Hisar, India, pp 35–37
Kumar S, Chandra A, Pandey K (2008) Bacillus thuringiensis (bt) transgenic crop: an environment friendly insect-pest management strategy. J Environ Biol 29:641–653
Liu Y, Chen L, Liu Y, Dai H, He J, Kang H et al (2016) Marker assisted pyramiding of two brown planthopper resistance genes, bph3 and bph27 (t), into elite rice cultivars. Rice 9:27
Malav AK, Chandrawat I, Chandrawat KS (2016) Gene pyramiding: an overview. Int J Curr Res Biosci Plant Biol 3:22–28
Maqbool SB, Riazuddin S, Loc NT, Gatehouse AM, Gatehouse JA, Christou P (2001) Expression of multiple insecticidal genes confers broad resistance against a range of different rice pests. Mol Breed 7:85–93
Maxmen A (2013) Crop pests: under attack. Nature 501:S15–S17
Meenakshi MA, Singh AK, Sanyal I, Altosaar I, Amla DV (2011) Pyramiding of modified cry1ab and cry1ac genes of bacillus thuringiensis in transgenic chickpea (cicer arietinum l.) for improved resistance to pod borer insect helicoverpa armigera. Euphytica 182:87
Mekonnen T, Haileselassie T, Tesfaye K (2017) Identification, mapping and pyramiding of genes/quantitative trait loci (qtls) for durable resistance of crops to biotic stresses. J Plant Pathol Microbiol 8:142
Meziadi C, Richard MM, Derquennes A, Thareau V, Blanchet S, Gratias A et al (2016) Development of molecular markers linked to disease resistance genes in common bean based on whole genome sequence. Plant Sci 242:351–357
Musser F, Catchot A Jr, Davis J, Herbert D Jr, Lorenz G, Reed T et al (2016) 2015 soybean insect losses in the southern us. Midsouth Entomologist 9:5–17
Neya BJ, Zida PE, Sereme, D, Lund OS, Traore O (2015) Evaluation of yield losses caused by cowpea aphid-borne mosaic virus (CABMV) in 21 cowpea (Vigna unguiculata (L.) Walp.) varieties in Burkina Faso. Pak J Biol Sci 18:304–313
Niu L, Mannakkara A, Qiu L, Wang X, Hua H, Lei C et al (2017) Transgenic bt rice lines producing cry1ac, cry2aa or cry1ca have no detrimental effects on brown planthopper and pond wolf spider. Sci Rep 7:1940
Oerke E-C (2006) Crop losses to pests. J Agric Sci 144:31–43
Okechukwu RU, Ekpo EJA, Okechukwu OC (2010) Seed to plant transmission of Xanthomonas campestris pv. vignicola isolates in cowpea. Afr J Agric Res 5(6):431–435
Osman G, Already R, Assaeedi A, Organji S, El-Ghareeb D, Abulreesh H, Althubiani A (2015) Bioinsecticide bacillus thuringiensis a comprehensive review. Egypt J Biol Pest Control 25:271
Palma L, Muñoz D, Berry C, Murillo J, Caballero P (2014) Bacillus thuringiensis toxins: an overview of their biocidal activity. Toxins 6:3296–3325
Pardo-Lopez L, Soberon M, Bravo A (2013) Bacillus thuringiensis insecticidal three-domain cry toxins: mode of action, insect resistance and consequences for crop protection. FEMS Microbiol Rev 37:3–22
Peralta C, Palma L (2017) Is the insect world overcoming the efficacy of bacillus thuringiensis? Toxins 9:39
Punja ZK (2006) Recent developments toward achieving fungal disease resistance in transgenic plants. Can J Plant Pathol 28:S298–S308
Riaz N, Husnain T, Fatima T, Makhdoom R, Bashir K, Masson L et al (2006) Development of indica basmati rice harboring two insecticidal genes for sustainable resistance against lepidopteran insects. S Afr J Bot 72:217–223
Roh JY, Choi JY, Li MS, Jin BR, Je YH (2007) Bacillus thuringiensis as a specific, safe, and effective tool for insect pest control. J Microbiol Biotechnol 17:547
Roh JY, Liu Q, Lee DW, Tao X, Wang Y, Shim HJ et al (2009) Bacillus thuringiensis serovar mogi (flagellar serotype 3a3b3d), a novel serogroup with a mosquitocidal activity. J Invertebr Pathol 102:266–268
Santos-Amaya OF, Rodrigues JV, Souza TC, Tavares CS, Campos SO, Guedes RN, Pereira EJ (2015) Resistance to dual-gene bt maize in spodoptera frugiperda: selection, inheritance, and cross-resistance to other transgenic events. Sci Rep 5:srep18243
Scheyer A, Graeff C, Morville S, Mirabel P, Millet M (2005) Analysis of some organochlorine pesticides in an urban atmosphere (Strasbourg, east of France). Chemosphere 58:1517–1524
Schnepf E, Crickmore N, Van Rie J, Lereclus D, Baum J, Feitelson J et al (1998) Bacillus thuringiensis and its pesticidal crystal proteins. Microbiol Mol Biol Rev 62:775–806
Soberon M, Monnerat R, Alejandra B (2016) Mode of action of cry toxins from bacillus thuringiensis and resistance mechanisms. In: Microbial toxins. Springer, Dordrecht, pp 1–13
Song X, Kain W, Cassidy D, Wang P (2015) Resistance to bacillus thuringiensis toxin cry2ab in trichoplusia ni is conferred by a novel genetic mechanism. Appl Environ Microbiol 81:5184–5195
Srivastava D, Shamim M, Kumar M, Mishra A, Pandey P, Kumar D et al (2017) Current status of conventional and molecular interventions for blast resistance in rice. Rice Sci 24:299–321
Summers R, Brown J (2013) Constraints on breeding for disease resistance in commercially competitive wheat cultivars. Plant Pathol 62:115–121
Tabashnik BE, Carrière Y (2010) Field-evolved resistance to bt cotton: bollworm in the us and pink bollworm in India. Southwest Entomol 35:417–424
Tu J, Zhang G, Datta K, Xu C, He Y, Zhang Q et al (2000) Field performance of transgenic elite commercial hybrid rice expressing bacillus thuringiensis δ-endotoxin. Nat Biotechnol 18:1101
Varshney RK, Graner A, Sorrells ME (2005) Genomics-assisted breeding for crop improvement. Trends Plant Sci 10:621–630
Vincelli P (2016) Genetic engineering and sustainable crop disease management: opportunities for case-by-case decision-making. Sustainability 8:495
Walker D, Boerma HR, All J, Parrott W (2002) Combining cry1Ac with QTL alleles from PI 229358 to improve soybean resistance to lepidopteran pests. Mol Breed 9:43–51
Wang YN, Ke KQ, Li YH, Han LZ, Liu YM, Hua HX, Peng YF (2016) Comparison of three transgenic bt rice lines for insecticidal protein expression and resistance against a target pest, chilo suppressalis (lepidoptera: Crambidae). Insect Sci 23:78–87
Xu C, Wang B-C, Yu Z, Sun M (2014) Structural insights into bacillus thuringiensis cry, cyt and parasporin toxins. Toxins 6:2732–2770
Yang Z, Chen H, Tang W, Hua H, Lin Y (2011) Development and characterisation of transgenic rice expressing two bacillus thuringiensis genes. Pest Manag Sci 67:414–422
Ye R, Huang H, Yang Z, Chen T, Liu L, Li X et al (2009) Development of insect-resistant transgenic rice with cry1c∗-free endosperm. Pest Manag Sci 65:1015–1020
Zheng X, Yang Y, Xu H, Chen H, Wang B, Lin Y, Lu Z (2011) Resistance performances of transgenic bt rice lines t2a-1 and t1c-19 against cnaphalocrocis medinalis (lepidoptera: Pyralidae). J Econ Entomol 104:1730–1735
Zhou Y, Choi Y-L, Sun M, Yu Z (2008) Novel roles of bacillus thuringiensis to control plant diseases. Appl Microbiol Biotechnol 80:563–572
Zhu X, Lei Y, Yang Y, Baxter SW, Li J, Wu Q et al (2015) Construction and characterisation of near-isogenic plutella xylostella (lepidoptera: Plutellidae) strains resistant to cry1ac toxin. Pest Manag Sci 71:225–233
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Segolela, J.C., Wokadala, O.C., Feto, N.A. (2019). Bacillus thuringiensis-Based Gene Pyramiding: a Way Forward for a Combined Horizontal and Vertical Resistance in Plant. In: Islam, M., Rahman, M., Pandey, P., Boehme, M., Haesaert, G. (eds) Bacilli and Agrobiotechnology: Phytostimulation and Biocontrol. Bacilli in Climate Resilient Agriculture and Bioprospecting. Springer, Cham. https://doi.org/10.1007/978-3-030-15175-1_15
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