Abstract
Lepidopteran borers stand out as the most destructive pests in sugarcane, leading to reductions in stalk weight, juice quality and sugar recovery. Presently, integrated pest management (IPM) systems are utilized for sugarcane borer management, employing diverse methods encompassing cropping system, chemical pesticides, behavioral manipulation, biological agents and the selection of resistant varieties. However, the effectiveness of this strategy remains controversial due to concerns about harmful residues, formulation limitations, environmental variability, labor shortages and increased input costs. Currently, multiple lines of transgenic sugarcane expressing insecticidal genes from the bacterium Bacillus thuringiensis (Bt) have been developed globally, offering the prospect of increases production with reduced pesticides application, thereby eliminating the negative effect of IPM. In Brazil, the first genetically modified sugarcane cultivars resistant to the sugarcane borer have been approved and released for commercial cultivation, shedding a bright light on a viable solution for sugarcane borers. This paper reviews borer species and distribution, the significant damage caused by sugarcane borers, current control approaches and the future effective control strategies. Additionally, this work provides comprehensive understanding on Bt sugarcane, serving as an additional tool to complement conventional sugarcane borers control resistance programs.
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Sugarcane borers species, distribution, damage worldwide
Sugarcane encounters a spectrum of biotic stressors, each with the potential to exert a substantial influence on its growth and yield. Among these stressors, lepidopteran borers are the foremost destructive pests in the major sugarcane-growing regions, including Brazil, India, China, the USA, South Africa, Indonesia, Reunion Island, Mexico, Iran, Colombia and Papua New Guinea (Nikpay et al. 2015). To better protect sugarcane from borer attacks, understanding the species, distribution and damage worldwide is of paramount importance.
Sugarcane borers species
Globally, sugarcane is susceptible to attacks by various insects from orders such as Lepidoptera, Homoptera, Coleoptera, Hemiptera, Orthoptera, and Isoptera (Yoseph and Desmond 2009). Lepidoptera borers represent significant pests in almost all sugarcane-planting countries. Approximately 50 species of Lepidoptera borers, including the genera Chilo, Diatraea, Sesamia, Argyroploce, Tryporyza, Scirpophaga, Eoreuma, Telchin and Eldana, have been documented attacking sugarcane (Fig. 1), mainly belonging to the Pyralidae, Crambidae, Noctuidae and Tortricidae families (Long and Hensley 1972; Kfir et al. 2002).
One notable sugarcane borers belongs to the genus Chilo, which is classified under the Crambidae and was previously categorized under Pyralidae. Species within the genus Chilo initiate damaged by causing 'dead-heart' in sugarcane shoots and subsequently feed on the internal stem tissue. These damages result in a significant reduction in sugarcane yield, potentially leading to total crop failure (Guan et al. 2012). Chilo infuscatellus, commonly referred to as the early shoot borer, causes damage to the crop in its early stages, leading to a subsequent reduction in yield. This species can survive year-round in mild climates (David et al. 1986; Narasimhan et al. 2001; Srikanth et al. 2009; Omkar 2018). Another significant sugarcane borer in this genus is the internode spotted borer, Chilo sacchariphagus, known for typically attacking plants aged 3–7 months. It exerts a more substantial impact on cane yield than sucrose yield (Waterhouse 2007; Bezuidenhout et al. 2008). The third species, C. venosatus, is also a noteworthy sugarcane borer, contributing to substantial economic losses (Liu et al. 2012; Hu et al. 2017; Fang et al. 2018). The fourth species, C. tumidicostalis, primarily inflicts damage to the crop after internode formation (Long and Hensley 1972). The fifth species, stalk borer C. auricilius, has young larvae that bore into shoots and canes by cutting holes and forming galleries in the stalk (Jaipal 1996), impairing growth and causing losses in cane yield and sugar recovery (Nesbitt et al. 1986).
Concerning borers within the Diatraea genus, their primary impact is on sugarcane in the Americas. In this genus, Diatraea saccharal is a prominent pest prevalent in the Western Hemisphere (Box and Harold 1931; Long and Hensley 1972; Reagan et al. 1972; Cristofoletti et al. 2018). Additionally, species like D. albicrinella, D. busckella, D. tabernella, D. centrella, D. indigenella, D. lineolata, D. considerate and D. magnifactella have been documented as sugarcane attackers (Long and Hensley 1972; Vejar-Cota et al. 2008; Vargas et al. 2015; Solis and Metz 2016).
The pink borers species in the Sesamia genus lead to a significant reduction in sugar recovery (Okamoto et al. 1999; Nikpay et al. 2014). Among these species, Sesamia cretica and S. nonagrioides are widely distributed in all sugarcane-growing areas, infesting sugarcane at all stages of growth (Jamshidnia et al. 2010; Nikpay et al. 2017). S. grisescens, on the other hand, can cause substantial damage to sugarcane in a few countries (Young et al. 1992). Additionally, larvaes of S. inferens bore into the aboveground parts of sugarcane seedlings (Luo et al. 2014). S. nonagrioides, also known as the corn borer, is another species within the Sesamia genus that causes severe damage to sugarcane (Fantinou et al. 2003).
Apart from the borer species from Chilo, Diatraea and Sesamia, some species of other genera also attack sugarcane. For example, larvaes of Argyroploce schistaceana inflict damage to both underground and surficial parts of sugarcane, causing a significant increase in population density and ultimately resulting in losses in cane yield and sugar (Luo et al. 2014; Zhang et al. 2019a). Larvaes of Tryporyza intacta bore into the seedlings, causing 'dead-heart' and reducing the number of tillers (Wei et al. 2012, 2014). Scirpophaga nivella imparts a characteristic 'bunchy top' appearance to the plant (Long and Hensley 1972). The Mexican rice borer, Eoreuma loftini, is an invasive sugarcane borer causing severe damage (Meagher et al. 1994; Showler et al. 2011). The giant cane borer, Telchin licus, caused severe damage to sugarcane (Almeida et al. 2007; Triana et al. 2020), mainly in Central and South America. The African sugarcane stalk borer, Eldana saccharina, attacks mature sugarcane (Girling 1978) and is the most destructive pest in South African (Keeping 2006), with the first description dating back to 1865 from sugarcane in Sierra Leone (Atkinson and Carnegie 1989; Bosque-Pérez and Mareck 1991; Ngwuta 2015).
Sugarcane borers distribution
Sugarcane borers, particularly species within the genera Chilo and Sesamia, stand out as the predominant and highly damaging pests affecting sugarcane in cane-growing countries globally, with the exception of Australia and Fiji (Sallam 2006). Each geographical region possesses its distinctive pest fauna. Old World regions, including African and Asia, host a variety of Chilo and Sesamia species (Long and Hensley 1972). Conversely, New World regions, such as the Americas, are primarily populated by Diatraea species (Long and Hensley 1972).
The sugarcane internode spotted borer, Chilo sacchariphagus, originally emerged in Asia but has subsequently disseminated to various sugarcane-producing countries and islands worldwide, encompassing central Asia, India, Korea, China, Indonesia, Malaysia, Sri Lanka, Thailand, Vietnam, Madagascar, Mauritius, Mozambique and South Africa (Cao et al. 2011; Ghahari et al. 2009; Nibouche et al. 2019; CABI 2022). The early shoot borer, C. infuscatellus, constitutes a notable pest with an extensive range spanning from the Philippines to Afghanistan, encompassing central Asia, India, Korea, China, Indonesia, Malaysia, Thailand, Uzbekistan, Vietnam, Russia and Papua New Guine (Narasimhan et al. 2001; CABI 2022). Another destructive pest, the stalk borer C. auricilius, is present in Eastern and Southeastern Asia, including Bangladesh, Bhutan, China, India, Indonesia, Malaysia, Myanmar, and other regions, as well as, northern Australia (Khanna et al. 1957; Nesbitt et al. 1986; Jaipal 1996; CABI 2022). C. tumidicostalis is a serious pest in some states of India, such as Assam, West Bengal, and the eastern part of Bihar, as well as in Bangladesh and Nepal (Neupane 1990). C. venosatus is primarily distributed in South China, Swaziland, Australia, Brazil, India, the Antilles, and Central and South America (He 2009; Liu et al. 2012 Fang et al. 2018).
Borers belonging to the genus D. are acknowledged as severe pests of sugarcane in the Americas (White et al. 2001). D. saccharalis, in particular, is a significant sugarcane pest across the American continent, spanning Antigua and Barbuda, Barbados, Belize, Costa Rica, Cuba, Haiti, Honduras, Mexico, Montserrat, Argentina, Bolivia, Brazil, Colombia, Ecuador, Guyana, Peru, Suriname, Uruguay and Venezuela (CABI 2022). This borer has posed a significant and enduring threat to the sugar industry in Brazil and America (Box and Harold 1931; Reagan et al. 1972 Vargas et al. 2015; Almeida et al. 2007; Sidhu 2013). It also represents a significant challenge in Cuba, Peru, Puerto Rico, Jamaica, Trinidad, Mexico, Colombia and America (Long and Hensley 1972; Solis and Metz 2016). Crambid stalk borer species, including Diatraea considerata, D. magnifactella, are distributed in Mexico (Vejar-Cota et al. 2008). In Colombia, various Diatraea species, including D. albicrinella, D. busckella, D. tabernella D. centrella, D. indigenella and D. lineolata, have been reported to attack sugarcane (Solis and Metz 2016). D. centralla is the primary sugarcane borer in Guyana and Trinidad (Long and Hensley 1972).
The pink borer, Sesamia inferens, has been identified as a sugarcane borer in various countries, including Bangladesh, Bhutan, Cambodia, China, India, Indonesia, Japan, Nepal, Pakistan, the Philippines, Singapore, Thailand, Papua New Guinea, the Solomon Islands and others (Young et al. 1992; Okamoto et al. 1999; CABI 2022). The other two species from the Sesamia genera, S. cretica and S. nonagrioides, are distributed in all sugarcane-growing areas (Jamshidnia et al. 2010). The corn borer, S. nonagrioides, is found throughout southern Europe, North Africa, and the Middle East (Fantinou et al. 2003; CABI 2022). S. calamistis and E. saccharina are the two major sugarcane borers found exclusively in South Africa (Long and Hensley 1972; CABI 2022). The pink stem borer, Sesamia spp., is also the most destructive pest of sugarcane in Southwest Iran (Nikpay et al. 2014; CABI 2022). S. cretica is an important borer of sugarcane, maize and sorghum in Africa, the Middle East, Southern Europe, Egypt, and Mediterranean, including Sudan, Somalia, Kenya, Cameroon and Ethiopia (Temerak and Negm 2009; Goftishu et al. 2016; CABI 2022). S. grisescens is exclusively distributed in Papua New Guinea (Young et al. 1992; CABI 2022).
Apart from the three aforementioned genera of sugarcane borers, there are additional generas specific to Asia, Africa and Americas. In Asia, the white borer A. schistaceana is prevalent in sugarcane-growing areas in China and is considered highly detrimental in Mauritius (Young et al. 1992) and also distributed in Madagascar, Indonesia, Japan, Malaysia, Philippines, Sri Lanka and Vietnam (CABI 2022). S. excerptalis is identified as a prominent sugarcane borer in Thailand (Young et al. 1992) and is frequently found across various regions, including Bangladesh, China, India, Indonesia, Japan, Malaysia, Myanmar, Nepal, Pakistan, the Philippines, Singapore, South Korea, Thailand, Vietnam, Australia, Papua New Guinea and the Solomon Islands (CABI 2022). S. nivella is identified as a species that inflicts significant economic damage in India, Java and Indonesia (Long and Hensley 1972; Angerilli et al. 1998). Moreover, it is commonly found across several regions, including Bangladesh, Brunei, China, India, Indonesia, Malaysia, Myanmar, Nepal, Pakistan, the Philippines, Singapore, Sri Lanka, Thailand, Vietnam, Australia, Fiji, New Caledonia and Papua New Guinea (CABI 2022). The Guangxi sugarcane area hosts various sugarcane borers, including A. schistaceana and T. intact Snellen (Li et al. 2016a, b). In the Americas, the Mexican rice borer, E. loftini, was initially discovered on sugarcane in the Lower Rio Grande Valley of Texas, USA, in the early 1980s and has subsequently spread to sugarcane-growing regions in Louisiana (Showler et al. 2011; Vanweelden et al. 2015; Wilson et al. 2015a). The sugarcane borer, T. intacta, is a severe pest in Southeast Asian countries and South China, causing significant damage, particularly in recent years (Wei et al. 2014). In 2008, the giant cane borer T. licus was initially recorded in Sao Paulo, the largest sugarcane-growing state in Brazil. It has subsequently spread across all sugarcane areas and is currently invading the central and southern regions of this country (Almeida et al. 2007). The African sugarcane stalk borer, E. saccharina, is acknowledged as the most destructive pest in South Africa, where it not only infests numerous wetland sedges (Atkinson and Carnegie 1989; Keeping 2006), but is also widely distributed in Angola, Benin, Botswana, Burkina Faso, Burundi, Cameroon, Chad, Congo, Equatorial Guinea, Eswatini, Ethiopia, Gabon, Gambia, Ghana, Guinea, Guinea-Bissau, Kenya, Liberia, Madagascar, Malawi, Mali, Mozambique, Niger, Nigeria, Rwanda, Senegal, Seychelles, Sierra Leone, Somalia, Sudan, Tanzania, Togo, Uganda, Zambia, Zimbabwe and Saudi Arabia (CABI 2022).
In the major sugarcane production regions, namely Asia, South America, and their neighboring areas, a greater variety of borer species indicate a significant occurrence of pests. In contrast, Australia and Europe exhibit fewer borer species (Fig. 2). This phenomenon is partly attributed to the relatively small total area of sugarcane in these two regions. However, it may also be linked to their effective pest control measures. The diversity of borer species in various regions may also be influenced by the local climate, ecological environment, and insect species composition. To prevent the spread and proliferation of insect pests, effective control of invasive species is a crucial strategy for every country, particularly those with border regions.
Economic loss caused by borers
Yield losses linked to most borers species are primarily attributed to reductions in crop before the formation of young shoots and to reductions in stalk weight and juice quality after internodes formation has commenced (Long and Hensley 1972). The infestation index, represented by the percentage of bored internodes, stands as a reliable parameter for predicting yield losses (Milligan et al. 2003). Ellis et al. (Ellis et al. 1960) concluded that the occurrence of internodes bored per unit weight of cane consistently correlates with sugar loss more effectively than estimates of the number of bored internodes or stalks. However, some researchers have also highlighted the impact of borer damage on juice quality (Holloway and Haley 1928). Thus, the damage caused by different species of borers has been assessed based on various methods of measurement. For example, Chilo infuscatellus can survive the winter in mild climates, and attacks the ratooning seedlings, resulting in the occurrence of 28.6 percent dead hearts (Srikanth et al. 2009), determined by the ratio of damaged seedlings to total seedlings. Meanwhile, larvaes of C. venosatus feed inside the sugarcane stem, resulting in a production loss of 25 percent (w/w) (Liu et al. 2012), measured by assessing the bored rate of the sugarcane and estimating the sugar production loss.
Based on various calculations, the losses attributed to borers were estimated. In Brazil, D. saccharalis larvae bored an average of 25.77 percent and 19.01 percent of the internodes during the sugarcane-growing seasons of 2010 and 2011, respectively. Percentage of bored internodes (D. saccharalis) ranged from 3.7 to 27.7% in the 2018 plant cane and 2019 first ratoon trials in in Louisiana, the USA (Salgado et al. 2022). Sucrose yield significantly decreased with the increasing internodes infestation, resulting in estimated sugar yield losses of 8.83 percent and 19.80 percent per 1 percent bored internodes for the first and second seasons, respectively (Rossato et al. 2013). Additionally, an approximately 0.5 percent reduction in sugar yield per acre was observed for each 1 percent of bored internodes after D. saccharalis infestation (Long and Hensley 1972).
In India, losses in sugarcane yield and sucrose content due to C. tumidicostalis have been estimated to range from 8.2 to 12.6 percent and 10.7 to 48.6 percent, respectively, in Bihar (Khanna et al. 1957). And these borers result in cane yield losses of 8 to 10 percent at the farmer's level and sugar recovery losses of 10 to 15 percent in sugar processing (Jasmine et al. 2012).
In China, about 40 percent of sugarcane is annually damaged by borers, leading to yield losses ranging from 10 to 25 percent (Li et al. 2016a, b). In China, researches observed that sugarcane borer could cause cane loss of 2625–7950 kg/ha, representing 3.2–9.4% of cane production when borer damage rate was 5–20% and 9960–13,537.5 kg/ha, accounting for 11.7–15.9% when borer incidence was 25–35% (Zhang et al. 2019b). Pests occurred significantly in Xianggui sugarcane area of China, where the average borer-damaged strain was 46.54%, the average yield loss was 14.89%, and the average sucrose content loss was as high as 1.12%. The estimated results of economic damage caused by pests revealed that the agricultural losses amounted to 467 million yuan (about 60.31 million dollars), industry losses reached 856 million yuan (about 119.72 million dollars), and the national financial losses were 51million yuan (Xie et al. 2020).
In Louisiana, damages caused by D. saccharalis were estimated to cause losses of up to 28 percent of cane weight per acre in a susceptible cultivar ('CP 44–101') (Hensley and Long 1969). However, it is crucial to note that economic losses associated with E. loftini in Louisiana sugarcane may reach as high as 220 million US dollars when the insect becomes fully established in the state (Meagher et al. 1994). The crambid stalk borer, D. considerata, causes annual losses of up to 10 million US dollars in Mexico (Vejar-Cota et al. 2008). Mexican rice borers, E. loftini, damage 20 percent of sugarcane internodes in that region, resulting in losses of 575 USD/ha (Meagher et al. 1994), and the total annual losses throughout the region are estimated to be between 10 and 20 million USD (Hardke et al. 2011). These diverse instances underscore the significant economic impact. Under the conditions of the Cauca River Valley in Colombia, economic losses attributed to Diatraea spp. are estimated at 143 kg of sucrose for each percent of bored internodes (Vargas et al. 2013). In Papua New Guinea, between January and June 1987, 70 percent of the total commercial planting in Ramu suffered moderate-to-severe damage by S. grisescens, leading to an 18 percent loss in sugar production (Young et al. 1992). The crop losses caused by E. saccharina in South African sugarcane have been estimated at a 0.1-percent yield loss for every 1 percent of damaged stalks (Smaill and Carnegie 1979).
In Indonesia, the economic losses of sugarcane caused by S. nivella can amount to as much as 50 percent (Angerilli et al. 1998). Simultaneously, the proportion of stalks damaged by C. sacchariphagus and C. auricilius reached 40 percent, leading to an approximate biomass yield reduction of 12.5 t/ha (19.2 percent) (Goebel et al. 2014).
Moreover, the damage inflicted by its larvaes is pervasive, manifesting at all stages of plant development. In addition, the entrance holes crafted by these borers not only serve as gateways for their but also provide avenues for secondary phytopathogenic fungi, thereby intensifying the potential impact on the crop (Rossato et al. 2013).
In general, bores damage results in 10–30% reduction in sugarcane yield, corresponding to the losses of one-fifth (calculated as an average of 20%) of the land allocated for sugarcane cultivation annually, thereby representing a substantial and noteworthy losses. Consequently, the developed and implementation of novel technologies to mitigate borer damage represent a critically important and formidable undertaking for sugarcane-producing economies worldwide.
Current integrated pest management (IPM) strategy on control on sugarcane bores
Integrated pest management (IPM) is an ecological strategy for pest control designed to suppress pest populations below the economic threshold level (ETL). Presently, IPM systems for managing the sugarcane borer encompass the manipulation of cropping system, the use of chemical pesticides, behavioral manipulation, biological control, and the selection of resistant varieties (Fig. 3).
Cropping system
The cropping system have long been acknowledged as the fundamental line of defense against pests in sugarcane cultivation practices. These practices encompass intercropping, planting clean seed canes, the removal of crop residues and damaged plants, fertilization, the manipulation of planting dates, and other specific tillage methods (Hensley 1971; Jaipal 2000; Kfir et al. 2002) (Fig. 4).
Intercropping is a valuable cultivation practice that can reduce pest damage, while simultaneously increasing income. However, it is important to avoid intercropping sugarcane with similar crops from the same family, Graminae, such as maize, sorghum and rice, to prevent the spread of pests between these crops. Alternatively, intercropping sugarcane with legumes such as soybean, mung bean, green manure crops, peanut, as well as vegetables such as tomatoes, hot peppers and cabbage, can establish an ecological balance conducive to the survival of natural enemies, thereby enhancing pest control (Zeng 2004).
The use of clean seed canes is instrumental in reducing the risk of pest infestation and enhancing both cane yield and quality. It is imperative to refrain from using canes sourced from fields severely impacted by pests (Tan et al. 2003). Moreover, common practices such as pre-harvest burning and the timely mechanical removal of borer-infested shoots or egg masses have been widely employed to curtail in-field pest populations and minimize damage (Jaipal 2000; Ma et al. 2014). The application of silicon (Si) fertilizer has proven effective in mitigating borer infestations by delaying the penetration of early instar larvaes into the stalks, resulting in increased larval mortality and reduced weight lost (Kvedaras and Keeping 2007). Additionally, the choice of planting date can significantly impact D. saccharalis populations in sugarcane, with early-planted sugarcane displaying greater susceptible to borers, consequently leading to heightened infestations (Beuzelin et al. 2011).
Moreover, performing low cutting during cane harvest proves effective in eliminating the majority of overwintering pests. Conversely, continuous sugarcane cultivation in the same field can result in an overabundance of overwintering borers, asynchronous borer development, and ultimately, substantial damage (Tan et al. 2003). Additional practices such as earthing up and propping cane stalks prevent lodging have been demonstrated to be effective measures in reducing stalk borer (Jaipal 2000).
However, it is essential to acknowledge that certain cultivation practices have been abandoned due to their low control efficiency, labor shortages and escalating input costs (Hensley 1971). Despite these challenges, the integration of a combination of cultivation control practices, tailored to the specific conditions of each sugarcane cultivation area, remains crucial for effective and sustainable pest management.
Chemical pesticide control
When the level of economic injury reaches 6–12% of damaged internodes for D. saccharalis, the necessity for action and the application of insecticides is recommended (White et al. 2008). Novaluron, an inhibitor of chitin synthesis, has demonstrated noteworthy reductions in D. saccharalis infestations, resulting in a 6.3–14.5-fold decrease in bored internodes. Moreover, the pyrethroid gamma-cyhalothrin has proven effective in safeguarding sugarcane against D. saccharalis infestations (Beuzelin et al. 2010). In studies conducted in Louisiana, insecticides such as Esfenvalerate, Cyfluthrin + Azinphos-methyl, Lambda-cyhalothrin, Tebufenozide and Esfenvalerate + Acephate have demonstrated efficacy against D. saccharalis. Particularly, they have shown a strong fit for the chemical management of the pest (Rodriguez et al 2001; Cherry et al. 2015). Similarly, insecticides such as Flubendiamide, ß-cyfluthrin, Novaluron and Chlorantraniliprole have proven effective in reducing D. saccharalis injury, achieving reductions ranging from 39.1 to 99.4% (Reay-Jones et al. 2005). Chlorantraniliprole and Flubendiamide have demonstrated high effectiveness in the management of E. loftini (Wilson et al. 2017). In China, insecticides including Carbofuran granules and Bisalfap granules have been extensively employed for controlling sugarcane borer (Chen 1998). Granular pesticides such as Sevidol granules, Lindane and Carbofuran have been utilized for controlling of the early shoot borer, C. infuscatellus, a significant pest in the sugarcane fields of Tamil Nadu, India (Narasimhan et al. 2001).
Despite the demonstrated effectiveness of numerous insecticides in mitigating sugarcane borer infestations, the indiscriminate application of these chemicals has resulted in adverse outcomes. These include the persistence of harmful residues, the development of pest resistance, resurgence of pests, environmental damage and the emergence of secondary pests (Reagan et al. 1972; Singh et al. 2015). Challenges such as inadequate penetration of insecticides, the protection of later instars and pupae within stalks, and the inability to apply foliar treatments in a timely manner during peak periods of adult emergence or oviposition pose substantial obstacles to the effectiveness of insecticide treatments (Bennett 1971; Reagan et al. 1972). To address these issues, novel application techniques and formulations need to be explored and implemented.
Behavioral manipulation
Considering the potential adverse effects of pesticides, behavioral management and biological control are regarded as alternative supplementary technologies for controlling sugarcane borer.
Insects respond to a variety of chemical cues, including pheromones employed for mate attraction and allelochemicals used to locate host plants and identify plants under attack by herbivores. The utilization of sex pheromones serves as a valuable method for monitoring moth population levels of borers, providing essential information for timing insecticide applications and diminishing the fertility of wild females through mating disruption techniques (Van Rensburg et al. 1985; Narasimhan et al. 2001). The complexity of insect pheromones necessitates careful consideration of the formulation employed, particularly for successful trapping. For instance, the pheromone of C. infuscatellus has been identified as Z-II hexadecenol and Z-II Hexadecenal (Narasimhan et al. 2001). While the sex pheromones of C. venosatus consist of a mixture of major components (Z13–18:AC, Z11–16:AC, and Z13–18:OH), only one sex pheromone component (Z11–16:OH) has been identified from C. infuscatellus (Fang et al. 2018). Pheromone-trapping techniques have proven successfully in detecting the presence of C. sacchariphagus Bojer in sugarcane in Mozambique sugarcane fields (Way et al. 2004). The female sex pheromone of the sugarcane borer, C. sacchariphagus, comprises two compounds, (Z)-13-octadecenyl acetate (I) and (Z)-13-octadecen-l-ol (II). Traps baited with combinations of these components successfully captured male C. sacchariphagus moths, with the 7:1 ratio performing similar to a virgin female moth (Trials 1980). In field trials, a blend of (Z)-8-tridecenyl acetate, (Z)-9-tetradecenyl acetate and (Z)-10-pentadecenyl acetate in an 8:4:1 ratio proved highly attractive for trapping male C. auricilius (Nesbitt et al. 1986). Studies have showed that a combination of (Z)-9-tetradecenol with (Z)-9-tetradecenyl acetate, with the most effective composition being 75:25, as an enticing attractant for male S. cretica (Donegani 1977). In Guangxi, China, control experiments utilizing the sex pheromone of C. infuscatellus on 5333 ha of sugarcane fields achieved a control effect of 82.48%, with the rate of attacked plants being less than 5% (Zeng 2004). Synthetic pheromone blends for C. suppressalis, C. indicus and C. auricilius have demonstrated satisfactory attractiveness to male moths in the field (Beevor et al. 1990). Three potential pheromone components, hexadecenal (l6Ald), (E)-l1-hexadecenal (E11-l6Ald) and (Z)-l1-hexadecenal (Zl1-16Ald), have been identified from Scirpophaga nivella and Diatraea saccharalis (Angerilli et al. 1998; Dam et al. 2023). Field tests using traps baited with a 3-component blend revealed it as the most attractive synthetic pheromone combination (Angerilli et al. 1998). The sex pheromone produced by females of Sesamia nonagrioides is a blend comprising Z-l1-hexadecenyl acetate (Z-11-16: Ac), Z-11-hexadecenal (Z-11-16: Ald), Z11-hexadecenol (Z-11-16: OH) and dodecyl acetate (12: AC) (Babilis and Mazomenos 1992). Despite the absence of recorded pheromone traps for Sesamia nonagrioides in the field, studies have identified. (Z)-13-octadecenyl acetate (I), (Z)-ll-hexadecenyl acetate (II) and (Z)-13-octadecenal (III) in an approximate ratio of 8:1:1.3 as equally attractive to the natural pheromone extracted from the female E. loftini moths (Shaver et al. 1988). Likewise, a two-component blend of (9Z, 11E)-hexadeca-9,1-dienal and (11Z)-hexadec-11-enal, in an approximate ratio of 10:1, has demonstrated comparable attractiveness to the natural pheromone extracted from the female D. saccharalis pheromone glands (Kalinová et al. 2005). The effectiveness of the D. saccharalis pheromone in reducing sugarcane borer damage has also been reported (Hensley 1973).
Trap crops are plant strategically cultivated to attract insects, serving as a protective measure for target crops against pest attacks. Extensive testing have been conducted on trap crops, with numerous instances of successful commercial application in various crops documented (Hokkanen and T 1991; Shelton and Nault 2004; Jacob et al. 2021). The utilization of trap crops extends to sugarcane borer management. In field conditions, small sugarcane plots surrounded by a row of Erianthus arundinaceus (Retz.) Jeswiet have demonstrated reduced stalk borer damage, leading to decreased larval survival and development compared to sugarcane (Hokkanen and T 1991; Shelton and Badenes-Perez 2006; Nibouche and Tibère 2010), and E. arundinaceus 28NG7 has been identified as a potential trap crop for controlling C. sacchariphagus, and larger commercial field trials have substantiated its efficiency in diminishing C. sacchariphagus damage on sugarcane (Nibouche et al. 2012).
Push–pull strategies encompass the manipulation of insect pests and their natural enemies by incorporating stimuli that render the protected target unattractive or unsuitable to the pests (push), while simultaneously exert a pulling force on the pest, guiding it toward an alternative crop or trap (pull), from which the pests are subsequently removed (Cook et al. 2007). Maize (Zea mays) is identified as a suitable attractive plant (Schexnayder et al. 2001), while Melinis minutiflora and Cyperus dives serve as repellent plant for certain borers (Conlong and Rutherford 2009) and are also attractive to parasitoids of these pests, such as Xanthopimpla stemmator (Conlong and Kasl 2000). When intercropped with sugarcane, M. minutiflora can reduce E. saccharina populations in sugarcane by up to 50% and diminish damage to sugarcane by up to 75% (Barker et al. 2006). Additionally, Bt maize functions as a 'dead-end trap crop' due to the toxic effect of the cry1Ab protein on E. saccharina larvae, potentially mitigating borer damage on sugarcane (Keeping et al. 2010). Recently, MON 95379 Bt maize as a new tool to manage sugarcane borer (D. saccharalis) in South America (Horikoshi et al. 2022).
Regrettably, the utilization of pheromone to diminish stem borers infestation and enhance sugarcane crop production has made little progress thus far (Campion and Nesbitt 1983). The advancement of semiochemical components is frequently impeded by constraints in formulation and delivery technology, mainly stemming from the small and specialized market. Inadequate knowledge and components may result in control breakdowns, jeopardizing the robustness and reliability of pest management approaches. Attaining a comprehensive understanding of the behavioral and chemical ecology of host-pest interactions and the impacts of these strategies on beneficial organisms necessitate substantial research efforts.
Biological control
In Integrated Pest Management (IPM) strategies for sugarcane borers, biocontrol plays a pivotal role. Biocontrol agents mainly encompass entomopathogenic microorganisms, parasitoids and natural enemies (Fig. 5).
Entomopathogenic microorganisms, encompassing bacteria, viruses, fungi, have found commercially applications as biological agents. Notably, among bacteria, Bt (B. thuringiensis) stands out as a well-known classical biological agent (Sanahuja et al. 2011). Diverse Bt strains (HD133 cryAa, cry1Ab, cry1C; HD559; GM7 cry1Aa, cry1Ab, and cry1B; GM10 cry1Aa, cry1Ab, cry1Ac, and cry1C; GM34 cry1Aa, cry1Ab, and cry1Ac; S76 cryAa, cry1Ab, cryAc, cry2Aa, and cry2Ab) and pure proteins have demonstrated efficacy in killing D. saccharalis (Hernández-Velázquez et al. 2012; Daquila et al. 2021). In South Africa, novel control strategies for E. saccharina have been developed using the sugarcane endophyte Gluconacetobacter diazotrophicus carrying Bt cry1Ac genes (Theo and Gustav 2013). Glasshouse trials revealed that sugarcane treated with Pseudomonas fluorescens carrying the Bt gene exhibited increased resistance to E. saccharina damage compared to untreated sugarcane (Herrera et al. 1994). In field trials, B. thuringiensis Berliner reduced D. saccharalis damage by up to 75%, although it has not yet been adopted for commercial production (Legaspi et al. 2000; Showler 2016).
Viruses infecting insects have garnered great attention as biological control agents, owing to their specificity toward insect populations and minimal impact environment impact. An endemic granulovirus (GV) extracted from larvae of the sugarcane borer, Diatraea saccharalis (DisaGV), originally discovered in the USA, was introduced to Brazil as an effort to control sugarcane borers (Alves 1986). In India, natural occurrences of two GVs infecting larvae of C. infuscatellus (ChinGV) and C. sacchariphagus (ChsaGV) were widely distributed in Tamil Nadu (Easwaramoorthy and Jayaraj 1987). Additionally, viruses such as Anticarsia gemmatalis MNPV (AgMNPV), Trichoplusia ni MNPV (TnMNPV) and AgMNPV-D10 have demonstrated lethal effects on D. saccharalis (Hernández-Velázquez et al. 2012). These viruses provide potential insights for practical use in the biological control of sugarcane borer.
The field of entomopathogenic fungi has emerged as a promising avenue for researching the biological control of insect pests in sugarcane plants. The entomopathogenic fungi Beauveria bassiana and Metarhizium anisopliae have displayed significant potential as biocontrol agents against the sugarcane borer, D. saccharalis. Field experiments conducted in Brazil showed that the application of M. anisopliae resulted in a commendable mortality rate of above 50% for D. saccharalis. Similarly, in India, M. anisopliae exhibited efficacy against C. indicus (Easwaramoorthy et al. 2001). Eight strains of M. anisopliae displayed high virulence against C. venosatus in China (Liu et al. 2012). Furthermore, M. anisopliae has demonstrated potential as a pathogen for S. inferens (Varma and Tandan 1996). In India, B. bassiana caused mortality rates of 69% to 76% in C. infuscatellus larvae (Sivasankaran et al. 1990). Laboratory studies have also indicated the pathogenicity of B. bassiana against S. inferens and S. grisescens (Varma and Tandan 1996; Sweet 1994). Other entomopathogenic fungi such as Hirsutella nodulosa, Isaria tenuipes, and I. farinosa, Cordyceps species have been studied on D. saccharalis, S. inferens and C. indicus, E. saccharina (Varma and Tandan 1996; Assefa et al. 2010; Hernández-Velázquez et al. 2012). Moreover, Fusarium oxysporum has exhibited pathogenicity against S. inferens (Varma and Tandan 1996). Additionally, Nosema sp., a microsporidium causing 'white larvae' disease, has impeded large-scale production of borers on sugarcane (Inglis et al. 2015).
Biocontrol programs have also utilized parasitoids on egg, larva and pupa, to manage sugarcane borers (Table 1). Sixteen known species of parasitoids target the larva-pupa stage of the sugarcane borer (Chen 1998). Insect parasitoids such as Trichogramma spp. and Cotesias spp. have demonstrated effectiveness in controlling the egg and larval stages of moth borers (Goebel et al. 2014; Roldán et al. 2020; Molter et al. 2023). For example, in Brazil, releases of Trichogramma galloi Zucchi and Cotesia flavipes have been employed to handle Diatraea spp. infestations, resulting in a substantial 60% reduction in pest populations (Parra et al. 2014). C. flavipes is also a pivotal agent in managing D. saccharalis in South Texas (Fuchs et al. 1979; Parra et al. 2014). Lixophaga diatraeae has demonstrated effectiveness in controlling D. saccharalis in Louisiana, with a noteworthy 75% parasitization rate recorded in the 1954 season (Posnock 2016). In Colombia, the tachinid flies Lydella minense or Billaea claripalpis are released when previous crop damage exceeds 2.5–5% (Vargas et al. 2015). Sturmiopsis inferens, a tachinid fly, serves as a crucial larval parasitoid of shoot borer (C. infuscatellus), stalk borer (C. auricilius), Gurdaspur borer (Acigona steniellus) and pink borer (S. inferens) (David et al. 1988). Releases of S. inferens against C. infuscatellus in India resulted in parasitism rates of 23.3% to 21.0% (Srikanth et al. 2009). T. busseolae, an egg parasitoid wasp, has demonstrated high parasitism rates of approximately 50% on the eggs of sugarcane borers, S. intacta and C. sacchariphagus (Nagarkatti and Nair 1973; Jamshidnia et al. 2010; Qin et al. 2018). Goniozus natalensis shows promise as a parasitoid for biologically controlling E. saccharina infestations in sugarcane, resulting in a 60% reduction in crop damage (Hearne et al. 1994). The pupa parasitoid Xanthopimpla stemmator Thunberg has been widely reared and released against E. saccharina in South African (Conlong 1994). In Açucareira de Moçambique, releases of X. stemmator led to reductions in C. sacchariphagus populations ranging from 31.3 to 90% across different trial sites (Conlong and Goebel 2002) (Table 1).
Biological control through predation by natural enemies plays a significant role in managing sugarcane borers (Meagher et al. 1998). Predators such as ants, earwigs, ground beetles, spiders, wireworms, lady beetles, mites and soldier beetles are considered crucial in controlling sugarcane borers in Louisiana (Negm and Hensley 1969). The red imported fire ant (Solenopsis invicta) emerges as a dominant natural enemy of D. saccharalis in Louisiana sugarcane fields (Beuzelin et al. 2010). Pheidole spp. ants also serve as abundant predators on sugarcane borers (Cherry et al. 2015). Spiders (Araneae) play a significant role as egg predators of D. saccharalis and hold second importance within the natural enemy complex (Ali and Reagan 1986). Among the spiders, Lycosa poonaensis and Palystes sp. stand out as the most voracious species, consuming 1.6 borer larvae and 2.2 borer adults per day respectively, indicating their effectiveness in controlling sugarcane borer (Technol 2001a). Ground beetles (Coleoptera: Carabidae), tiger beetles (Coleoptera: Carabidae: Cicindelinae), rove beetles (Coleoptera: Staphylinidae), click beetles (Coleoptera: Elateridae), and earwigs (Dermaptera) are also acknowledged as important natural enemies on D. saccharalis in Louisiana (Negm and Hensley 1967, 1969).
Fluctuations in biological control can arise due to geographical and seasonal variations, along with the presence of hyperparasitoids, which may undermine the effectiveness of this strategy (Gitahy et al. 2007). Moreover, the environmental instability of entomopathogenic microorganisms hinders their augmentative use in controlling sugarcane borers. Therefore, further in-depth research is still required in this field to achieve widespread application.
Host plant resistance
In the realm of diseases and pests’ control, the paramount approach is plant resistance, prove to be both highly and economically prudent. The selection of resistant sugarcane varieties is commonly achieved through the application of conventional breeding techniques. Resistance to borers in sugarcane manifests in leaves or stems, impeding or retarding larval ingress into the stalks (Kvedaras et al. 2007). Traits linked to leave, such as narrow leaves, leaf shedding, erect leaves, long leaf spindles, low leaf senescence, and those related to stems, including high fiber content, light stalk color, heavy wax coating, thin stalks, high vigor, high juice content, and rind hardness and epicuticular wax composition, have served as criteria for ranking entries based on their resistance to borers (Long and Hensley 1972; Ngwuta 2015; Reagan and Mulcahy 2019; de Mello et al. 2020; Wartha et al. 2022; Penn and Read 2023). The selection of numerous resistant sugarcane cultivars has been facilitated by these pivotal resistance traits. Exemplary varieties, including N21, N24, L 99-226, L 01-299, HoCP 04-838, L 01-283, Ho 12-615, SP803280, SP813250, RB867515 and SP891115, have exhibited resistance traits in either the stem or leaves, leading to a diminished rate of borer larvae and substantial height gain in stalks (Kvedaras et al. 2009; Tomaz et al. 2017; Reagan and Mulcahy 2019). In India, varieties such as Co 243, 281, 285, 312, 356, 421, 449, 453, 527, 617, 650, 775, 853, 975, 1007, 1048, 1049, 1157, 6239, 6402, 6403, 6507, 6508, 6510, 6610, Cos 673, 729, BO17, 54, 70 and 99 have demonstrated a low incidence of infestation by C. infuscatellus (David et al. 1986). Among these, Co 1007, 1236, 7302, 7303, S-5/75, S-38/76, E 92 and E 168 (David et al. 1986), as well as Co 356 and 513 are acknowledged for their resistance to Chilo auricilius in India. Additionally, Co 243, 453 and 617 display a lower susceptible to Chilo tumidicostalis (Negm and Hensley 1969). Furthermore, the determination of the percentage of bored internodes and the relative survival of larval within the stalk have been employed to select sugarcane varieties exhibiting resistance to the Mexican rice borer, Eoreuma loftini (Wilson et al. 2015b; Salgado et al. 2022). The evaluation of sugarcane resistance to the African sugarcane borer, E. saccharina, involves the measurement of the length of bored stalks, the count of bored internodes, and the quantification of surviving larvae and pupae in terms of both number and weight (Keeping 2006).
The incorporation of introgressions from wild relatives species plays a pivotal role in enhancing resistance and tolerance to various biotic and abiotic stresses, as well as obtaining desirable agronomic traits, including increased yields (Prescott-Allen 1986; Singh et al. 2020; Meena et al. 2020). Nevertheless, the effective selection of elite varieties with resistance to borers through introgression poses challenges, given the highly time-consuming and labor-intensive nature of the selection process. The selection of desired clones necessitates three stages on a large population before they can proceed to regional evaluation trials (Meena et al. 2020). To confer resistance to Lepidopteran stalk borers, transgenic sugarcane lines expressing genes like the Cry protein, proteinase inhibitor, or lectin have been successfully developed (Srikanth et al. 2011). This approach holds promise in effectively suppressing borers, offering substantial benefits to sugarcane production.
Status of transgenic sugarcane
Genes used for GM sugarcane
Significant endeavors have been devoted to the development of genetically modified sugarcane harboring desired traits. For example, transgenic sugarcane plants have been employed for the production of sorbitol, gentiobiose, and gentiobiitol (Chong et al. 2010a,b), cellobiohydrolases (CBH I and CBH II) (Harrison et al. 2011), bacterial endoglucanase (Harrison et al. 2014), 2G ethanol (Bewg et al. 2016), and other valuable alternative products (Petrasovits et al. 2012; Barros et al. 2013; Zale 2016). Furthermore, numerous genetically modified sugarcanes exhibiting resistance to both biotic and abiotic stresses have been successfully developed. Diverse genes have been integrated into sugarcane genomes, encompassing a bacterial toxin degradation gene (Zhang et al. 1999), virus resistance genes (Ingelbrecht et al. 1999; Butterfield et al. 2002; McQualter et al. 2004; Gilbert et al. 2005, 2009; Zhu et al. 2011; Guo et al. 2015), bovine pancreatic trypsin inhibitor gene (Christy et al. 2009), several insect resistance genes (Arencibia et al. 1997; Enríquez and G. 2000; Falco and Silva-Filho 2003; Weng et al. 2006; Kalunke et al. 2009; Arvinth et al. 2010; Weng et al. 2011; de Oliveira et al. 2022), herbicide resistance genes (Enríquez-Obregón et al. 1998; Christell et al. 2013), and tolerance to drought and salinity genes (Molinari et al. 2010; Reis et al. 2014; Kumar et al. 2014) (Table 2).
The prosperous commercialization of transgenic crops hinges on the stable and uniform expression of introduced traits across successive generations, coupled with their agronomic performance comparable to elite commercial cultivars (Anderson and Birch 2012). Prominent transgenic crops, including soybean (Padgette et al. 1995), rice (Duan et al. 1996) and corn (Fearing et al. 1997; Chen et al. 2008; Paz et al. 2010), have exhibited these characteristics. Nonetheless, transgenic sugarcane populations manifest considerable genetic variability (Joyce et al. 1998; Gilbert et al. 2005; Vickers et al. 2005a), and somaclonal variation may occur to varying degrees in transgenic sugarcane due to the prolonged period in tissue culture during the transformation process. Hence, a comprehensive field assessment of transgenic events is imperative to identify elite and commercially valuable events. However, there have been limited field assessments of transgenic sugarcanes, as evidenced by studies conducted by several scientists (Arencibia et al. 1999; Leibbrandt and Snyman 2003; Lakshmanan et al. 2005; Vickers et al. 2005a; Gilbert et al. 2009; Weng et al. 2011; Basnayake et al. 2012).
Gallo-Meagher and Irvine presented the initial documentation of stable expression of a transgenic trait-herbicide resistance in successive generations of sugarcane (Gallo-Meagher and Irvine 1996). Subsequent to that milestone, stable transgene expression has been observed in relation to virus and insect resistance (Joyce et al. 1998; Gilbert et al. 2009; Weng et al. 2011), herbicide resistance (Weng et al. 2011), polyphenol oxidase activity (Vickers et al. 2005b), sorbitol (Chong et al. 2010b) and isomaltulose accumulation (Basnayake et al. 2012). Contradictory results have emerged from certain analyses of the agronomic performance of transgenic sugarcane. Arencibia et al. (1999) demonstrated that majority of transgenic events resistant to stalk borers exhibited agronomic traits akin to those of the untransformed parent clone. In field trials spanning three years, Leibbrandt and Snyman (2003) and Gilbert et al. (2005) similarly concluded that stable transgene expression and agronomic performance equivalent to that of parent clones were attained. Nonetheless, Vickers et al. (2005a) observed that the majority of transgenic events exhibited substantial yield reduction in contrast to the parent clone, with no impact on sugar content and purity. In summary, numerous beneficial genes have been successfully integrated into sugarcane, yielding the desired traits. No significant technical bottlenecks impede the generation of transgenic sugarcane. Nevertheless, more key tools are necessary to make transgenic events more efficient and available for commercial use.
Sugarcane transformation methods
The production of transgenic sugarcane depends on reliable genetic transformation techniques. Presently, the two predominant methods for sugarcane transformation are biolistic and agrobacterium-based approaches (Manickavasagam et al. 2004; Zhangsun et al. 2007; Joyce et al. 2014; Mayavan et al. 2015). These methods involve the use of embryogenic callus induced from immature top stalks (Taparia et al. 2012a; Fouad et al. 2015). The regeneration of transformed plants has been accomplished through diverse approaches, including direct and indirect organogenesis or somatic embryogenesis (Arencibia et al. 1998), (Manickavasagam et al. 2004; Attia et al. 2005; Lakshmanan 2006), (Eldessoky et al. 2011; Taparia et al. 2012b). Various methods have demonstrated differing efficiencies in generating regenerative embryogenic calli. The application of a biolistic-based transformation approach, coupled with a bioreactor-based micro-propagation system, has proven successful in transforming twelve elite cane genotypes, achieving transformation efficiencies of up to 39% (Ramasamy et al. 2018). Nevertheless, these methods may be time-consuming and labor-intensive. In addressing these challenges, researchers have investigated tissue culture-free plant transformation methods mediated by A. tumefaciens, involving sugarcane axillary buds, stem cuttings, or seeds (Manickavasagam et al. 2004; Mayavan et al. 2013, 2015).
The promoter stands out as the most important element influencing the expression of transformed genes. To mitigate the risk of transgene silencing in multigene transformations and attain superimposed traits in transgenic crops, employing promoters with diverse expression patterns is highly desirable (Peremarti et al. 2010; Zeevi et al. 2012). Among several promoters, ubiquitin promoters have surfaced as a promising option for the constitutive expression of transgenes in sugarcane (Lakshmanan et al. 2005). These promoters have demonstrated a significant enhancement in transgene expression levels compared to other promoters, including the CaMV 35S promoter, rice actin Act1 promoter, and synthetic Emu promoter (Mcelroy et al. 1991; Last et al. 1991). Ubiquitin promoters encompass those derived from Cauliflower mosaic virus (CaMV), Rice tungro bacilliform virus (RTBV), Commelina yellow mottle virus, Taro bacilliform virus, Banana streak virus (BSV), and Sugarcane bacilliform virus (SCBV) (Kay et al. 1987; Medberry and Olszewski 1992; Bhattacharyya-Pakrasi et al. 1993; Chen et al. 1996; Peer et al. 2001; Tzafrir et al. 1998; Schenk et al. 1999). The Ubi-1 promoter has proven effective in producing stable transgenic sugarcane lines (Falco and Silva-Filho 2003). In a recent development, transgenic sugarcane plants expressing two genes encoding proteinase inhibitors under the control of the maize ubiquitin promoter (pUbi-1) were created, leading to a substantial retardation of Diatraea saccharalis feeding on the transgenic sugarcane leaf tissues (Falco and Silva-Filho 2003). Similar to Ubi-1, sugarcane ubi4 has demonstrated heat shock inducibility in stable transformed sugarcane callus lines, whereas sugarcane ubi9 did not exhibit such inducibility in transgenic sugarcane plants (Wei et al. 2003). In contrast, another promoter, SCBV21, exhibited 1.8- and 2.4-fold higher transient expression of EYFP (Enhanced Yellow Fluorescent Protein) compared to the standard maize ubiquitin 1 (Ubi1) and Cauliflower mosaic virus 35S promoters, respectively, in sugarcane young leaf segments (Gao et al. 2017). Additional functional promoters in sugarcane encompass sugarcane dirigent and o-methyltransferase from putative defense and fiber biosynthesis-related genes, maize phosphoenolpyruvate carboxylase, and sugarcane loading stem gene (Damaj et al. 2010; Harrison et al. 2011; Moyle and Birch 2013).
Another critical factor influencing exogenous gene expression and performance is the GC content and codon usage pattern of target gene (Estruch et al. 1997). Earlier studies have shown that GC-rich regions are more transcriptionally active in plants and animals, whereas AT-rich regions can hinder transcription (Scott et al. 1998; Herbert and Rich 1999; Vinogradov 2003). Hence, designing synthetic copies of exogenous genes with elevated GC contents has the potential to enhance translational efficiency (Rocher et al. 1998Rouwendal et al. 1997; Liu 2009; Jackson et al. 2013; Mudge et al. 2013). In the development of strongly insect-resistant sugarcane, the cry1Ac gene underwent modification to create a synthetic version, referred to as s-cry1Ac. This involved increasing the GC content of the coding region from the original 37.4% to 47.5% based on the sugarcane codon usage pattern. Consequently, this modification enhances the protein expression level of s-cry1Ac in transgenic sugarcane plants by twofold to threefold (Weng et al. 2006). Transgenic sugarcane lines harboring the modified cry1Ac gene with an evaluated GC content (54.8%) yielded approximately fivefold higher levels of cry1Ac protein (up to 50 ng cry1Ac protein per mg soluble proteins) compared to those expressing the partially modified s-cry1Ac (GC% = 47.5%) (Weng et al. 2011). These m-cry1Ac transgenic sugarcane lines demonstrated enhanced resistance to insect attacks compared to s-cry1Ac transgenic sugarcane plants (Weng et al. 2011).
The creation of transgenic plants with stacked multiple genes is typically accomplished through the cross between different transgenic plants (Cao et al. 2002; Datta et al. 2002; Zhao et al. 2003) or by retransformation with multiple genes (Jobling et al. 2002; Carlo et al. 2003; Singla-Pareek et al. 2003; Qi et al. 2004). However, researchers have devised a fast and cost-effective method that entails inserting a single transferred DNA (T-DNA) containing multiple genes into a plant at the same site of the genome within one transformation cycle (Slater et al. 1999; Bohmert et al. 2000, 2002). Despite its advantages, the T-DNA approach has its limitations, including the size of the T-DNA and potential uneven gene expression among different genes (Jones et al. 1987; Peach and Velten 1991).
Besides, various studies have reported that factors, including the transgene copy number, developmental regulation, and transcriptional or post-transcriptional mechanisms, can influence transgene stability in transgenic sugarcane plants (Wei et al. 2003; Robert et al. 2010; Mudge et al. 2009). Hence, further improvements are necessary to overcome these limitations (Poirier et al. 2000; Goderis et al. 2002; Thomson et al. 2002). Encouragingly, long-term transgene expression consistency and the T-DNA insert stability have been successfully achieved in multiple cycles of field-propagated sugarcane (Caffall et al. 2017). Moreover, transgenic sugarcane parents that exhibit stable inheritance of transgenes can be effectively utilized in breeding programs (Butterfield et al. 2002), indicating a high likelihood of successful commercialization of transgenic sugarcane.
Progress, advantages and limitations of Bt sugarcane
The status of Bt crops
Bacillus thuringiensis (Bt) Cry toxins, recognized biological agents employed for insect pests control (Gómez 2007), are synthesized as crystal inclusions, hence acquiring the designation Cry toxins. Presently, a total of 166 cry genes have been documented, classifying their respective cry proteins divided into 30 groups and several subgroups (Barboza-Corona 1998).
Genetically modified (GM) plants incorporating Bt genes have undergone swift adoption since their commercial introduction in 1996 (Dively et al. 2016). Various crops, such as maize, cotton, soybean, rice, potato, brinjal, tomato and sugarcane, have been genetically modified with Bt genes (Xiao and Wu 2019). The global cultivation area of Bt crops has witnessed a substantial surge, escalating from 1.1 million hectares in 1996 to approximately 178 million hectares annually across 28 countries at present (Venugopal and Dively 2017). Bt corn, cotton and soybean collectively constitute over 99% of this total area (Venugopal and Dively 2017), with a cumulative surpassing of 830 million hectares planted with Bt crops globally up to the present moment.
Cry toxins exhibit toxic activity against various insect species (Miyasono et al. 1994; Bradley et al. 1995; Schnepf et al. 1998). Their mode of action involves solubilization and proteolytic processing in the insect midgut. The proteins bind to receptor molecules located in the apical cells of the brush border membrane, leading to their insertion and the formation of a pore (Hfte and Whiteley 1989; Bravo 1997; Schnepf et al. 1998). The specificity of these crystals to insects relies on the proteins’ affinity to binding receptor molecules and the environmental conditions within the insect midgut (Van et al. 1990; Bravo et al. 1992) (Fig. 6). Cry toxins have exhibited substantial insecticidal activity against Lepidopterans, Coleopterans and mosquitoes (Gómez et al. 2007).
In addition to Cry proteins, different types of Bt crops have been engineered to produce vegetative insecticidal proteins (Vip) (Mahon et al. 2012; Bernardi 2015; Chakroun et al. 2016; Sharon et al. 2016; Wei et al. 2017). The increasing adoption of Bt crops reflects growers’ high satisfaction with their performance. Bt crops have demonstrated outstanding effectiveness in controlling Coleopteran, Lepidopteran and some Hemipteran insect pests (Carrière et al. 2003; Wu et al. 2008; Hutchison et al. 2010; Downes et al. 2017; Xiao and Wu 2019; Girón-Calva et al. 2020). By diminishing reliance on conventional chemical pesticides, Bt crops provide an alternative and sustainable strategy for pest management (Betz et al. 2000).
Progress of Bt sugarcane
Due to the large and complex genome, selecting sugarcane cultivars with desired agronomic traits by conventional breeding program is a time- and labor-consuming procedure (Cheavegatti-Gianotto et al. 2011; Souza et al. 2011). Consequently, direct gene transformation is being employed as a promising approach to introduce important traits into sugarcane (Ye et al. 2016). The enhancement of insect resistance in transgenic sugarcane has been achieved through the transformation of cry1A(b) (Arencibia et al. 1997, 1999; Arvinth et al. 2010; Zhi et al. 2017), GNA (Sétamou et al. 2002; Zhangsun et al. 2007), cry1Aa3 (Kalunke et al. 2009), cry1Ac (Weng et al. 2006, 2011; Gao et al. 2016a, b; Dessoky et al. 2021; Salgado et al. 2022), cry2A (Gao et al. 2018), Vip3A (Riaz et al. 2020), and proteinase inhibitor (Nutt et al. 2001; Falco and Silva-Filho 2003) (Iqbal et al. 2021)(Table 3). Field trials of insect-resistant transgenic sugarcane have revealed that most lines exhibit agronomic traits similar or less favorable than those of non-transgenic varieties (Arencibia et al. 1999; Zhi et al. 2017). Notably, concerning borer resistance, the creation of sugarcane cultivars ROC16 and YT79-177 by introducing of a modified cry1Ac gene through particle bombardment resulted in about 62% of transgenic plants being resistant to borer in both greenhouse and field trials (Weng et al. 2011). Furthermore, the Bt insecticidal gene Cry1Ab and the glyphosate-tolerant gene EPSPS were inserted into a single transferred DNA fragment along with the selection marker gene PMI and introduced into sugarcane using agrobacterium-mediated transformation, leading to the development of robust borer-resistant lines (Wang et al. 2017). Additionally, a gene encoding the Bacillus thuringiensis Cry1a(b) protein has been found to confer sugarcane resistance to Diatraea saccharalis under both laboratory and field conditions (Technol 2001b). Therefore, the insertion of insect-resistant genes into sugarcane holds great promise as a strategy for controlling sugarcane borers.
It is worth noting that having low copy-number exogenous genes are considered to be beneficial for plant improvement (Dai et al. 2001). For example, a single copy of Cry1Ab or Cry1Ac in sugarcane can provide effective protection against borers (Arvinth et al. 2010; Weng et al. 2011). Additionally, transgenic sugarcane lines with a medium copy number of the cry1Ac gene have also shown significantly higher resistance to sugarcane borers while maintaining a similar yield to control lines (Gao et al. 2016a, b). However, there was a statistically significant negative correlation between the copy number of the cry2A gene and the percentage of borer-infested plants (Gao et al. 2018). The gene balance hypothesis suggests that a correlation between transgene copy number and gene expression levels, but in reality, the relationship is complex (Dai et al. 2001; Coate et al. 2016). Moreover, the correlation between the cry1Ac protein abundance and cry1Ac gene copies varied among different transgenic lines from various varieties(Zhou et al. 2018). Therefore, in practical plant improvement, it is necessary to screen a large population of transgenic lines to identify individuals with stable expression patterns that are appropriate for an aimed trait, while avoiding adverse agronomic changes that may arise from chance mutations or quasi-stable epigenetic changes during tissue culture (Graham et al. 2011; Yu et al. 2011).
Commercialized Bt sugarcane
During 2022, the total global area under GM crop cultivation reached approximately 202.2 million hectares, the planting area of GM crops accounted for about 12% of the total arable land area, reflecting an increase of 3.3%. The number of countries approved to cultivate GM crops increased to 29, and 71 countries and regions approved the commercial application of GM products (Li et al. 2023). Transgenic crops with herbicide tolerance (HT) and pest resistance (Bt) have been widely used in recent years. According to the statistics of the United States Department of Agriculture (USDA), in 2022, the share of Bt cotton accounted for about 89%, and Bt corn climbed to 84% of the GM crops. However, the plantation area of transgenic sugarcane is 100,000 hm2. So far, a total of 7 GM sugarcane events, which confer insect resistance (against Lepidoptera), have been developed for approval (ISAAA 2019, 2022). In Brazil, the foremost sugarcane producer and primary sugar exporter, genetically modified (GM) sugarcane varieties resistant to the sugarcane borer (Diatraea saccharalis), have obtained approval and been introduced for commercial cultivation. Brazil stands as the sole and pioneering country to introduce Bt sugarcane to the market. These varieties CTC 20 Bt, CTC 9001 Bt and CTC 93309–4 Bt express not only the cry1Ab protein, but also the neomycin phosphotransferase type II (NptII) protein used as a selection marker during the transformation process (Kennedy et al. 2018). Regarding health issue, the major concern for people is regarding GM crops. Investigations into the presence of foreign DNA and protein in sugar produced from these sanctioned GM sugarcane varieties have demonstrated the absence of heterologous DNA or Bt protein in the clarified juice, ethanol or raw sugar. This suggests their elimination or degradation during the processing of this GM variety (Cheavegatti-Gianotto et al. 2018).
Advantages of Bt crops
Biotechnology provides potent tools capable of substantially enhancing agricultural productivity and efficiency, concurrently tackling diverse challenges. Utilizing biotechnology enables the reduction of excessive insecticide use, leading to sustainable economic and ecological benefits (James 2010). For instance, Bt cotton has exhibited notable outcomes, including a 50% decrease in insecticide usage and a 31% surge in crop yields in China and India. This has resulted in a significant boost in cotton income, totaling US$11.9 billion (James 2011). In addition to direct economic benefits, reports indicate indirect advantages such as heightened employment, household income and diminished poverty (Subramanian and Qaim 2009; Raybould and Quemada 2010; Shankar and Thirtle 2010; Carpenter 2010). Substantial research suggests that the adoption of Bt crops has substantially decreased insecticide application in numerous countries (Carpenter 2010). On a global scale, genetically modified (GM) crops have augmented yields by 22%, diminished pesticide usage by 37%, and mitigated environmental impact, including an 18% reduction in insecticide and herbicide use (Raman 2017).
Cry proteins, expressed by Bt crops, have been shown to possess high specificity toward target pests, thereby presenting minimal risk to non-target species due to their narrow spectrum of activity (Romeis et al. 2006; Lareesa et al. 2008; Li et al. 2014). Reports confirm that the widespread adoption of Bt cotton has indeed yielded a positive impact on pest populations (Wu et al. 2008; Qiao et al. 2016; Qiao et al. 2017). Thus, Bt crops play a role in enhancing the overall sustainability and health of agroecosystems by fostering a more balanced and resilient ecosystem (Marvier et al. 2007); Naranjo et al. 2008; Naranjo 2011; Lu et al. 2012; Li et al. 2016a, b; Wei et al. 2018). As a result, this fosters more effective pest control and reduces reliance on broad-spectrum insecticides.
Bt crops contribute to food quality by mitigating pest damage, preventing not only yield losses but also preserving quality (Miller 2008), (Li et al. 2016a, b). Pesticide residues are a significant concern regarding food quality, given their potential adverse effects on health through the direct consumption of foods containing toxic residues (Anilkumar et al. 2008; Usha et al. 2011; Nag and Raikwar 2011). Bt crops can decrease the dependence on chemical insecticides, thereby reducing pesticide residues in crops. This contributes to heightened food safety and quality by minimizing the potential health risks associated with pesticide exposure (Abedullah et al. 2014).
Due to its unique characteristics, such as vegetative propagation, sugarcane minimizes the likelihood of gene flow and potential environmental impacts associated with transgenic varieties. Additionally, sugar derived from sugarcane, undergoing high-temperature and crystallization processes, is considered a low-risk product in terms of both food and environmental safety (Qaiser et al. 2011). Several biosafety reports have been conducted on transgenic sugarcane lines to assess their safety and potential environmental effects (Gilbert et al. 2005). Specifically, studies on Cry1Ac transgenic sugarcane have demonstrated that it does not have a significant impact on microbial diversity in the rhizosphere soil and enzyme activities within a single crop season (Zhou et al. 2016). These findings suggest that Bt sugarcane has the potential to be utilized for effective insect pest management in sugarcane fields without significant adverse effects on the environment.
In summary, Bt crops function as a valuable tool for enhancing food and feed quality by decreasing pesticide residues, mitigating health risks linked to pesticide exposure, and advocating for safer and healthier agricultural practices.
Issues and solution of Bt crops
The emergence of pest resistance poses a significant challenge to the sustainability of Bt transgenic technology (Heckel 2012; Pardo-López et al. 2013; Dively et al. 2016; Sharon et al. 2016). The development of resistance in pest populations can lead to a reduction in the efficacy of Bt crops for pest control on a global scale (Tabashnik et al. 2013; Bruce et al. 2014). Additionally, there are reports of cross-resistance between Cry proteins in cotton pest insects (Anilkumar et al. 2008; Unnithan et al. 2015), emphasizing the urgency of resistance management (Mchughen 2012). To tackle these challenges, one commonly utilized approach is the high-dose refuge strategy. This approach involves planting Bt crops with high levels of toxin expression to suppress the population of resistant pests, while simultaneously growing 'refuge' plants that do not produce Bt toxins. These refuge plants offer a habitat for susceptible pests, allowing for their survival and mating with any resistant insects, thus maintaining a low frequency of resistant alleles (Roush 1997; Liu and Tabashnik 1997; Dively et al. 2016).
In addition to the high-dose refuge strategy, early detection of resistance is crucial. This involves conducting baseline susceptibility tests to determine the susceptibility of pest populations to Bt toxins and to identify the genetic basis underlying their resistance, (Paolino and Gassmann 2017; Wei et al. 2017). Identifying resistant individuals or populations early on enables the implementation of appropriate management strategies to mitigate resistance evolution and preserve the efficacy of Bt crops. Overall, these strategies are essential to delaying the evolution of resistance and maintaining the long-term effectiveness of Bt transgenic technology.
Conclusion and future perspectives
Lepidopteran borers, by causing reductions in stalk weight, juice quality and sugar recovery, are the most destructive pests in sugarcane. Currently, the use of chemical pesticides can severely damage human health and ecosystem functioning, compromising the sustainability of plant protection. Thus, the objective for scientists is reducing the use of chemical pesticides, thereby minimizing environmental impact without compromising crop yields. Biological agents, such as aphids and fungi, have been studied and other novel technologies, including application of cropping system, behavioral manipulation and the selection of resistant varieties, have been identified to effectively reduce sugarcane borer damages in laboratory conditions. However, the effectiveness of this strategy has been hampered by harmful residues, limitations in formulation, environmental variability, labor shortages, and increased input costs. Furthermore, the life cycle of the sugarcane borer typically lasts for two months, with 4–6 overlapping generations occurring each year. Given that the sugarcane borer primarily feeds within sugarcane stalks, managing it with foliar insecticides or other biological agents is challenging and requires careful timing to coincide with larval eclosion. Consequently, the effectiveness of biological control activities against the pest is impeded, and most of these technologies are challenging to implement in the field.
Transgenic Bt sugarcane, achieved through the introduction of genes encoding Cry proteins, has effectively enhanced sugarcane's resistance to insect damage, as evidenced by studies conducted by scientists (Kalunke et al. 2009; Arvinth et al. 2010; Wu et al. 2010; Weng et al. 2011; Gao et al. 2016a, b). A lot of successful commercial examples can be also found in Bt corn and Bt cotton, which have shown increased profits and decreased yield losses, so developing Bt sugarcane is a viable solution for sugarcane borers.
Further studies can focus on these aspects:
There is still a need for improvement in IPM strategy to control sugarcane borers. The development of innovative biological products, including microorganisms and metabolites, screening additional chemical pesticides, employing chemical ecology strategies, identifying novel cultural management approaches, and breeding resistant varieties, will enhance the resistance of sugarcane to attacks by borers. Investigating the effectiveness of various combinations of control strategies in 'IPM' is crucial for achieving effective control of sugarcane borers, albeit with significant challenges.
The implementation of these tactics depended on an enhanced understanding of the systematics, biology and ecology of the pests. Investigating the lifespan and feeding habits is crucial for determining the optimal timing of pesticide and other agent applications. Additionally, Geographic Information Systems (GIS), remote sensing, and semiochemicals for detecting damage and monitoring populations offer significant opportunities for IPM.
The success of this initiative relies on the collaborative efforts of researchers, technology-transfer specialists, and commercial partners to ensure the effective translation of research into practical use. Current practices in IPM should be evaluated within the context of IPM programs, with a focus on compatibility and consideration of ecological, environmental, and economic consequences. The efficacy of new control strategies should be assessed by farmers, ensuring consistent profitability and security for growers and sugarcane millers.
Promising biotechnological advances with excellent potential are poised to significantly enhance the control of sugarcane borers. Exploring the feasibility and advantages of stacking multiple genes within a single transferred DNA (T-DNA) fragment holds the potential to simplify genetic engineering and enhance the effectiveness of pest resistance (Xiao and Wu 2019). Thus, the future management of lepidopteran pests will encompass the integration of transgenic crops with various novel Bt genes. Additional research should concentrate on utilizing or developing more robust genetic modification techniques, including genome editing technology and efficient genetic transformation, for the development of crops with enhanced resistance traits against sugarcane borers.
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Acknowledgements
This work was supported by the Science and Technology Major Project of Guangxi (AA22036003), the Natural Science Foundation of Guangxi (2021GXNSFBA075010), the Science and Technology Major Project of Guangxi (AB22035028 and AA22117002), the Natural Science Foundation of Guangxi (2023GXNSFAA026453), the National Natural Science Foundation of China (32360247), the Fundamental Research Fund of Guangxi Academy of Agriculture Sciences (2021YT010), the earmarked fund for CARS (CARS-170206).Yunnan Provincial Seed Industry Joint Laboratory Project (202205AR070001-09).
Funding
This work was supported by the Science and Technology Major Project of Guangxi (AA22036003), the Natural Science Foundation of Guangxi (2021GXNSFBA075010), the Science and Technology Major Project of Guangxi (AB22035028 and AA22117002), the Natural Science Foundation of Guangxi (2023GXNSFAA026453), the National Natural Science Foundation of China (32360247), the Fundamental Research Fund of Guangxi Academy of Agriculture Sciences (2021YT010), the earmarked fund for CARS (CARS-170206).Yunnan Provincial Seed Industry Joint Laboratory Project (202205AR070001-09).
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A-MLS-LW and D-LH did conceptualization; A-ML, FL, MW, Z-LC, C-XQ, Y-RL, Y-QP and D-LH gave methodology; A-ML, Z-LC and D-LH did writing—original draft preparation; S-LW and D-LH performed writing—review and editing; S-LW and D-LH supervised the study; D-LH administrated the project and did funding acquisition. All authors have read and agreed to the published version of the manuscript.
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Li, AM., Chen, ZL., Liao, F. et al. Sugarcane borers: species, distribution, damage and management options. J Pest Sci (2024). https://doi.org/10.1007/s10340-024-01750-9
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DOI: https://doi.org/10.1007/s10340-024-01750-9