The efficacy of disease resistance genes in plants decreases over time because of the selection of virulent pathogen genotypes. A key goal of crop protection programs is to increase the durability of the resistance conferred by these genes. The spatial and temporal deployment of plant disease resistance genes is considered to be a major factor determining their durability. In the literature, four principal strategies combining resistance genes over time and space have been considered to delay the evolution of virulent pathogen genotypes: cultivars mixture, rotation, landscape deployment, pyramiding. We reviewed this literature with the aim of determining which deployment strategy results in the greatest durability of resistance genes. Although theoretical and empirical studies comparing deployment strategies of more than one resistance gene are very scarce, they suggest that the overall durability of disease resistance genes can be increased by combining their presence in the same plant (pyramiding). Retrospective analyses of field monitoring data also suggest that the pyramiding of disease resistance genes within a plant is the most durable strategy. By extension, we suggest that the combination of disease resistance genes with other practices for pathogen control (pesticides, farming practices) may be a relevant management strategy to slow down the evolution of virulent pathogen genotypes.

/pdf/combining-selective-pressures-to-enhance-the-durability-of-4jl7nu8i1i.pdf

Combining Selective Pressures to Enhance the Durability of Disease Resistance Genes

Transgenic crop pyramids producing two or more Bacillus thuringiensis (Bt) toxins that kill the same insect pest have been widely used to delay evolution of pest resistance. To assess the potential of pyramids to achieve this goal, we analyze data from 38 studies that report effects of ten Bt toxins used in transgenic crops against 15 insect pests. We find that compared with optimal low levels of insect survival, survival on currently used pyramids is often higher for both susceptible insects and insects resistant to one of the toxins in the pyramid. Furthermore, we find that cross-resistance and antagonism between toxins used in pyramids are common, and that these problems are associated with the similarity of the amino acid sequences of domains II and III of the toxins, respectively. This analysis should assist in future pyramid design and the development of sustainable resistance management strategies.

Optimizing pyramided transgenic Bt crops for sustainable pest management

BACKGROUND
Cases of western corn rootworm (WCR) field-evolved resistance to Cry3Bb1 and other corn rootworm (CRW) control traits have been reported. Pyramid products expressing multiple CRW traits can delay resistance compared to single trait products. We used field studies to assess the pyramid CRW corn products, SmartStax (expressing Cry3Bb1 and Cry34Ab1/Cry35Ab1) and SmartStax PRO (expressing Cry3Bb1, Cry34Ab1/Cry35Ab1 and DvSnf7), at locations with high WCR densities and possible Cry3Bb1 resistance, and to assess the reduction in adult emergence attributable to DvSnf7 and other traits. Insect resistance models were used to assess durability of SmartStax and SmartStax PRO to WCR resistance.

RESULTS
SmartStax significantly reduced root injury compared to non-CRW-trait controls at all but one location with measurable WCR pressure, while SmartStax PRO significantly reduced root injury at all locations, despite evidence of Cry3Bb1 resistance at some locations. The advantage of SmartStax PRO over SmartStax in reducing root damage was positively correlated with root damage on non-CRW-trait controls. DvSnf7 was estimated to reduce WCR emergence by approximately 80–95%, which modeling indicated will improve durability of Cry3Bb1 and Cry34Ab1/Cry35Ab1 compared to SmartStax.

CONCLUSION
The addition of DvSnf7 in SmartStax PRO can reduce root damage under high WCR densities and prolong Cry3Bb1 and Cry34Ab1/Cry35Ab1 durability. © 2017 Society of Chemical Industry

/pdf/evaluation-of-smartstax-and-smartstax-pro-maize-against-2vadrhp6cj.pdf

Evaluation of SmartStax and SmartStax PRO maize against western corn rootworm and northern corn rootworm: efficacy and resistance management.

BACKGROUND
Transgenic maize (Zea mays L.) event TC1507 (Herculex® I insect protection), expressing Cry1F δ-endotoxin derived from Bacillus thuringiensis var. aizawai, was commercialized in 2003 in the Americas. Spodoptera frugiperda (J.E. Smith) (Lepidoptera: Noctuidae) susceptibility to Cry1F was monitored annually across several regions in Argentina using diagnostic concentration bioassays. Reduced performance of TC1507 maize against S. frugiperda was reported in 2013. A resistant population was established in the laboratory and the dominance of Cry1F resistance was characterized. RESULTS: During 2012–2015, high-survivorship of several populations was observed in the resistance monitoring program. Reciprocal crosses of a Cry1F-resistant population with a Cry1F-susceptible population were evaluated to calculate effective dominance (DML) based on mortality levels observed at 100 µg/ml Cry1F. Two additional dominance levels (DLC and DEC) were calculated using lethal (LC50) or effective concentration (EC50) derived from concentration-response bioassays. Estimates indicated that Cry1F resistance in S. frugiperda in Argentina was either highly-recessive (DML=0.005) or incompletely recessive (DLC < 0.26 and DEC<0.19).

CONCLUSION
This study is the first documented confirmation and characterization of S. frugiperda Cry1F field-evolved resistance in Argentina. The resistance to Cry1F in S. frugiperda populations collected in Argentina, is autosomal and incompletely recessive similar to the resistance reported in Brazil.

https://onlinelibrary.wiley.com/doi/pdf/10.1002/ps.4776

Characterization of field-evolved resistance to Bacillus thuringiensis-derived Cry1F δ-endotoxin in Spodoptera frugiperda populations from Argentina.

Transgenic plants have been widely adopted by growers to manage the western corn rootworm, Diabrotica virgifera virgifera LeConte, in field corn. Because of reduced efficacy in some Nebraska fields after repeated use of Cry3Bb1-expressing hybrids, single plant bioassays were conducted in 2012 and 2013 to characterize the susceptibility of western corn rootworm populations to the rootworm-active proteins Cry3Bb1, mCry3A, and Cry34/35Ab1. Results demonstrate that there are heritable differences in susceptibility of Nebraska western corn rootworm populations to rootworm-active Bt traits. Proportional survival and corrected survival data coupled with field histories collectively support the conclusion that a level of field resistance to Cry3Bb1 has evolved in some Nebraska populations in response to selection pressure and that cross-resistance exists between Cry3Bb1 and mCry3A. There was no apparent cross-resistance between Cry34/35Ab1 and either Cry3Bb1 or mCry3A. The potential implications of these results on current and future corn rootworm management strategies are discussed.

/pdf/susceptibility-of-nebraska-western-corn-rootworm-coleoptera-2ytab7k6kz.pdf

Susceptibility of Nebraska Western Corn Rootworm (Coleoptera: Chrysomelidae) Populations to Bt Corn Events

Studies were conducted across the southern United States to characterize the efficacy of multiple Bacillus thuringiensis (Bt) events in a field corn, Zea mays L., hybrid for control of common lepidopteran and coleopteran pests. Cry1F protein in event TC1507 and Cry1A.105 + Cry2Ab2 proteins in event MON 89034 were evaluated against pests infesting corn on above-ground plant tissue including foliage, stalks, and ears. Cry34Ab1/Cry35Ab1 proteins in event DAS-59122-7 and Cry3Bb1 in event MON 88017 were evaluated against the larvae of Mexican corn rootworm, Diabrotica virgifera zeae Krysan and Smith, which occur below-ground. Field corn hybrids containing Cry1F, Cry1A.105 + Cry2Ab2, Cry34Ab1/Cry35Ab1, and Cry3Bb1 insecticidal proteins (SmartStax) consistently demonstrated reductions in plant injury and/or reduced larval survivorship as compared with a non-Bt field corn hybrid. Efficacy provided by a field corn hybrid with multiple Bt proteins was statistically equal to or significantly better than corn hybrids containing a single event active against target pests. Single event field corn hybrids provided very high levels of control of southwestern corn borer, Diatraea grandiosella (Dyar), lesser cornstalk borer, Elasmopalpus lignosellus (Zeller), and fall armyworm, Spodoptera frugiperda (J.E. Smith), and were not significantly different than field corn hybrids with multiple events. Significant increases in efficacy were observed for a field corn hybrid with multiple Bt events for sugarcane borer, Diatraea saccharalis (F.), beet armyworm, Spodoptera exigua (Hubner), corn earworm, Helicoverpa zea (Boddie), and Mexican corn rootworm. Utilization of field corn hybrids containing multiple Bt events provides a means for managing insect resistance to Bt proteins and reduces non-Bt corn refuge requirements.

https://bioone.org/journals/journal-of-economic-entomology/volume-105/issue-5/EC12155/Evaluation-of-Corn-Hybrids-Expressing-Cry1F-Cry1A105-Cry2Ab2-Cry34Ab1-Cry35Ab1/10.1603/EC12155.pdf

Evaluation of corn hybrids expressing Cry1F, cry1A.105, Cry2Ab2, Cry34Ab1/Cry35Ab1, and Cry3Bb1 against southern United States insect pests.

Commercial field corn (Zea mays L.) hybrids transformed to express some or all of the lepidopteran insect-resistant traits present in SmartStax corn hybrids were evaluated for insecticidal efficacy against a wide range oflepidopteran corn pests common to the northern United States, during 2008 to 2011 at locations in 15 states. SmartStax hybrids contain a pyramid of two Bacillus thuringiensis (Bt) derived events for lepidopteran control: event TC1507 expressing Cry1F protein and MON 89034 expressing CrylA.105 + Cry2Ab2. These studies focused on characterization of the relative efficacy of each event when expressed alone or in combination, and compared with non-Bt hybrid. Corn hybrids containing pyramided insecticidal proteins Cry1F + Cry1A.105 + Cry2Ab2 (SmartStax) consistently showed reduced plant feeding damage by a wide range of lepidopteran larvae compared with single event and non-Bt hybrids. Corn hybrids expressing TC1507 or MON 89034 as single or pyramided events were consistently efficacious against Ostrinia nubilalis (Hubner). SmartStax hybrids had less injury from Agrotis ipsilon (Hufnagel) and Striacosta albicosta (Smith) than corn hybrids containing only event MON 89034 but were not more efficacious than single event TC1507 hybrids. Corn hybrids with event MON 89034 provided better control of Helicoverpa zea (Boddie), than event TC1507 alone. Spodoptera frugiperda (J.E. Smith) efficacy was higher for hybrids with pyramid events and single events compared with the non-Bt hybrids. The spectra of activity of events TC1507 and MON 89034 differed. The combination of TC1507 + MON 89034 provided redundant control of some pests where the spectra overlapped and thereby are expected to confer a resistance management benefit.

https://bioone.org/journals/journal-of-economic-entomology/volume-107/issue-1/EC12448/Efficacy-of-Pyramided-Bt-Proteins-Cry1F-Cry1A105-and-Cry2Ab2-Expressed/10.1603/EC12448.pdf

Efficacy of Pyramided Bt Proteins Cry1F, Cry1A.105, and Cry2Ab2 Expressed in SmartStax Corn Hybrids Against Lepidopteran Insect Pests in the Northern United States

Studies were conducted across nine U.S. states, over 5 yr, to characterize the efficacy of transgenic corn (Zea mays L.) hybrids producing insecticidal proteins derived from Bacillus thuringiensis (Bt) for control of western corn rootworm, Diabrotica virgifera virgifera Le Conte. Hybrids tested had the same genetic background, contained one of two single events (DAS-59122-7 expressing Cry34Ab1/Cry35Ab1 or MON 88017 expressing Cry3Bb1) or a pyramid consisting of both rootworm-active events (SmartStax traits) and were compared with a non-Bt near isoline. Frequency analyses of root feeding data showed that hybrids containing both events sustained less root damage (0–3 node injury scale) than hybrids containing either event alone. The levels of root protection provided by MON 88017 and DAS-59122-7 were not different from each other. Efficacy was also evaluated based on consistency of protection, based on the proportion of plants with root ratings of either ≤0.25 or <1.00 on the node injury scale. The...

https://bioone.org/journals/journal-of-economic-entomology/volume-106/issue-2/EC12392/Evaluation-of-Corn-Hybrids-Expressing-Cry34Ab1-Cry35Ab1-and-Cry3Bb1-Against/10.1603/EC12392.pdf

Evaluation of Corn Hybrids Expressing Cry34Ab1/Cry35Ab1 and Cry3Bb1 Against the Western Corn Rootworm (Coleoptera: Chrysomelidae)

Since 2003, rootworm-protected transgenic corn has been commercially deployed in the United States as a principal method of control of western corn rootworm, Diabrotica virgifera virgifera LeConte. Durability of this technology depends partly on larval mortality (“dose”) exerted by the traits, but density-dependent mortality can confound calculations of dose. Research reported here examined the effects of density-dependent mortality on adult emergence and estimates of trait dose. At sites in Illinois and Indiana, western corn rootworm eggs were infested at four densities on non-Bt corn and at a single density on corn hybrids with transgenic events MON 88017 (VT Triple PRO), DAS-59122-7 (Herculex Insect Protection), and MON 88017 × DAS-59122-7 (SmartStax corn). Beetles were collected weekly in large emergence cages. Density-dependent mortality and the effect of Bt traits were examined using percent survival from egg to adult, sex ratio, and beetle mass. Beetle emergence from Bt treatments was very low, and percent survival from non-Bt treatments was greatest at the lowest egg density (410 eggs per row-meter). Therefore, emergence from the lowest infestation density on non-Bt corn was used to estimate the effective dose of the Bt treatments. Sex ratio and beetle mass were unaffected by density-dependent effects and were not consistently affected by Bt traits. Dose was estimated at 97.4–99.3% for MON 88017, 98.8–99.9% for DAS-59122-7, and 99.7–100.0% for MON 88017 × DAS-59122-7. This study confirms the need to account for density-dependent mortality when estimating dose of corn rootworm protection events even at relatively low egg infestation densities.

/pdf/effects-of-bt-corn-and-egg-density-on-western-corn-rootworm-2b51ttupui.pdf

W. H. Hendrix

Papers

Evaluation of corn hybrids expressing Cry1F, cry1A.105, Cry2Ab2, Cry34Ab1/Cry35Ab1, and Cry3Bb1 against southern United States insect pests.

Efficacy of Pyramided Bt Proteins Cry1F, Cry1A.105, and Cry2Ab2 Expressed in SmartStax Corn Hybrids Against Lepidopteran Insect Pests in the Northern United States

Evaluation of Corn Hybrids Expressing Cry34Ab1/Cry35Ab1 and Cry3Bb1 Against the Western Corn Rootworm (Coleoptera: Chrysomelidae)

Effects of Bt Corn and Egg Density on Western Corn Rootworm (Coleoptera: Chrysomelidae) Adult Emergence and Estimation of Effective Bt Dose.