Andrew F. Roberts, Ph.D. Deputy Director, CERA. September 19, 2013
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1 Risk assessment and regulation of RNAi Pesticides in the context of GE plants and the regulation of novel plant breeding techniques in the United States Andrew F. Roberts, Ph.D. Deputy Director, CERA September 19, 2013
2 Contents of the talk What is RNAi? Molecular mechanism Applications in GE plants Review of the ERA Paradigm Conference: Problem Formulation for the ERA of RNAi Plants Objective and approach Case Studies Results of the conference Implications for Regulation of New Plant Breeding Techniques in the USA
3 What is RNAi? Credit: V. Vance Set of processes mediated by small regulatory RNAs Sequence-specific RNA degradation Some are inducible responses to defend against invasive nucleic acids (e.g. defense mechanisms in plants against plant viruses) Some are endogenous pathways used to control gene expression
4 RNAi is an important biological phenomenon Credit: V. Vance Ancient pathways present in virtually all eukaryotic organisms Different names for the same thing: Plants - post-transcriptional gene silencing (PTGS) Fungi - quelling Animals - RNA interference (RNAi) Silencing pathways share genetic requirements and biochemical features Triggered by double stranded RNA (dsrna)
5 Why is RNAi useful to plant breeders? Credit: V. Vance A powerful genetic tool Can be induced experimentally using transgene constructs that make dsrna Once silencing is triggered, any RNA with homology to the target RNA is destroyed Major biotechnology implications A way to turn off gene expression in a sequence-specific way
6 Applications of RNAi in the plant sciences Credit: G. Heck Example transgenic RNAi traits in development Modified oil composition Potato starch composition (e.g., Amflora) Decaffeinated coffee Reduced lignin alfalfa Increased essential amino acids in corn Nematode resistant soybean Reduced phytate sorghum
7 Approved (presumptive) RNAi plants Event Crop Trait ERA Approval (Country, Year) FlavrSavr Tomato Delayed softening USA (1992) Mexico (1995) Japan (1996) ZW-20 Squash Virus resistance USA (1994) CZW-3 Squash Virus resistance USA (1996) 55-1/63-1 Papaya Virus resistance USA (1996) RBMT15-101, SEMT15-02, SEMT15-15 Potato Virus resistance (+ Bt) USA (1999) Canada (1999) RBMT21-129, RBMT21-350, RBMT Potato Virus resistance (+Bt) USA (1998) Canada (1999) Vector Tobacco Reduced nicotine USA (2002) C5 Plum Virus resistance USA (2007) X17-2 Papaya Virus resistance USA (2009) DP Soybean Modified seed fatty acid content Canada (2009) USA (2010)
8 A brief explanation of the generalized ERA paradigm for GE plants Trait Plant Environment Comparative Assessment Conducted on a case by case basis Considers Characteristics of the Plant, Introduced Trait and Receiving Environment As well as their interactions Makes use of the concept of Familiarity
9 There is no international standard for ERA of GE plants, but Countries consider similar broad protection goals and potential for harm, including: Potential for the GE plant to be a weed of agriculture or invasive of natural habitats Potential for gene flow to related species that might become weeds of agriculture or invasive of natural habitats Potential to adversely impact non-target organisms or biodiversity The types of data collected to address these are also generally similar: Phenotypic characterization/comparison Laboratory toxicology / feeding studies Observations from field trials Differences in decision making typically stem from Differences in tolerance to risk and uncertainty Differences at the Policy/Political level NOT fundamental differences in ERA methodology
10 Conference: Problem Formulation for the ERA of RNAi Plants June 1-3, 2011 in Washington, D.C. Organized by CERA Funded by the National Institute for Food and Agriculture (NIFA), USDA Biotechnology Risk Assessment Research Grants Program (BRAG) Tri-partite conference organizing committee Conference of 40 scientists: regulators, academics, private sector, NGOs
11 Why? RNAi represents a substantially different technology than traditional genetic engineering (i.e. the introduction of genes encoding proteins which mediate phenotype) No protein produced Highly dependent on nucleic acid sequence May or may not be a donor organism It is important to have a deliberate examination of how the ERA paradigm being used for GE plants can be applied to new technologies
12 RNAi conference objectives To share information about current applications of RNA interference to produce novel, transgenic plants To explore if problem formulation for RNAi plants leads to new or additional risk hypotheses when compared with non-rnai plants expressing similar traits Scientific exchange not a policy discussion
13 Conference focused on four case studies Participants were asked to: Identifying risk scenarios whereby the introduction of a GE plant with an RNAi trait might have an adverse impact on a protection goal Identifying testable hypotheses related to risk scenarios Case Studies Insect resistant maize Nematode resistant soybean Nutritionally enhanced sorghum Reduced allergen soybean
14 Relevant Protection Goals USEPA: No unreasonable adverse effects upon man or the environment No non-target organism affected No gene flow leading to enhanced weediness and altered exposure scenario No environmental fate leading to altered exposure scenario USDA APHIS: No potential risks to agriculture and the environment No increase in disease and pest susceptibilities No increase in weediness characteristics No increase in weediness of sexually compatible plants No increase in harm to other organisms (beneficial, threatened and endangered species) No plant pest effects from changes in cultivation practices
15 Case Study 1: Insect-resistant RNAi maize Plant Cell 21-24mers Ingestion (uptake) Corn Rootworm Cell Dicer dsrna Credit: J. Masucci Dicer 21-24mers dsrna 5 cap RISC mrna cleavage recognition AAAAA Stable IR transgene target gene target gene November 2007, Volume 25, pp
16 Case Study 2: Soybean Cyst Nematode Resistant Soybean Credit: B. Matthews Currently under development by USDA Agricultural Research Service Soybean Cyst Nematode The major pest of soybean in the U.S. No chemical control available (legal and effective) Goal Develop soybean resistant to all SCN genotypes (and other nematodes) using RNAi gene silencing Approaches Turn off critical nematode genes and proteins important to nematode survival using RNAi targeted to nematode genes with essential functions
17 Case Study 3: Nutritionally Enhanced Sorghum Credit: J. Anderson Reduced-phytate (phytic acid) Phosphorous storage complex Binds zinc and iron Decreases bioavailability
18 Nutritionally Enhanced Sorghum Credit: J. Anderson One approach to reduce phytate is through RNAi suppression of the myo-inositol kinase gene X Reduced Source: Buchanan et al., Biochemistry and Molecular Biology of Plants. 2000
19 Case Study 4: Reduced Allergen Content Soybean Credit: E. Herman Soybean contains many allergens P34 is the primary human neonatal allergen Transgenic Soy has been produced using RNAi to eliminate P34 protein Beta beta-conglycinin Glycinin acidic chain Gly m Bd 30k/P34 Agglutinin Kunitz TI Alpha beta-conglycinin Napin-type 2S albumin Alpha prime beta-conglycinin Glycinin A5A4B3 Lipoxygenase Sucrose binding protein Dehydrin Basic 7S globulin Glycinin basic chain
20 What did we do? Participants were divided into four breakout groups Working independently Each group was asked to work on two of the four case studies Risk Scenarios (pathway to harm) Risk Hypotheses Information/Data that would be useful to corroborate or refute the hypotheses The work of two groups were then combined for each case study Plenary then reconvened to go over the results and identify points of consensus
21 Points of consensus from the RNAi conference The paradigm currently applied to the environmental risk assessment of genetically engineered plants is adequate for the assessment of RNAi plants.
22 This Paradigm is Robust and Broadly Applicable Trait Plant Environment Comparative Assessment Conducted on a case by case basis Considers Characteristics of the Plant, Introduced Trait and Receiving Environment As well as their interactions Makes use of the concept of Familiarity
23 Points of consensus from the RNAi conference No plausible risk hypotheses were identified that can be considered unique to RNAi mechanisms when compared to other GE plants with similar traits. The same tests and protocols that are used for evaluating other GE plants will be sufficient for testing RNAi plants, including plants expressing pesticidal traits.
24 Points of consensus from the RNAi conference The use of RNAi technologies allows for the use of alternative informative tests, such as bioinformatic analyses, to address certain risk questions. For plants expressing pesticidal dsrnas, bioinformatics can be applied to characterize potential susceptibility of relevant NTO species. The accumulation of bioinformatic data that defines thresholds for activity spectra based on shared sequence identity will reduce the need for NTO testing.
25 Points of consensus from the RNAi conference Baseline data about environmental fate of dsrna will be broadly useful for future exposure analyses
26 Implications for Regulation of New Breeding Techniques in the USA
27 Implications for Regulation of New Breeding Techniques in the USA Coordinated Framework Policy Statement U.S. agencies will regulate the products of biotechnology in accordance with their authorities under existing safety regulations USDA Plant Protection Act FDA Federal Food Drug and Cosmetic Act (FFDCA) US EPA Federal Insecticide, Fungicide and Rodenticide Act (FIFRA) FFDCA (Pesticide residues in food)
28 USDA Regulation of New Plant Breeding Techniques Plant Protection Act Regulations (7 CFR 340) Defines plant pest A regulated article must meet two requirements Produced using genetic engineering (recombinant DNA techniques) AND Donor organism, recipient organism, vector, vector agent, is a plant pest OR Is an unclassified organism the Administrator determines is a plant pest or has reason to believe is a plant pest
29 US EPA FIFRA Regulates the use of pesticides through a registration process Plant incorporated protectants (PIPs) are considered pesticides Bt proteins Virus resistance (RNAi mediated) EPA regulates the pesticide, not the plant EPA will be holding a Scientific Advisory Panel meeting to discuss RNAi pesticides in October
30 US FDA Regulates food safety Primarily post-market safety authority Novel foods are subject to a voluntary consultation process (premarket) Consultation is voluntary Safety is mandatory
31 The U.S. will continue regulating under the Coordinated Framework For RNAi Plants USDA will likely regulate RNAi plants with sequences from pests US EPA will regulate any pesticidal RNAs FDA will continue to have oversight over food safety voluntary consultation process is likely to be requested by developers of GE plants with RNAi mediated phenotypes
32 Acknowledgements Slides from: Vicki Vance - University of South Carolina Greg Heck Monsanto Company Alan Gray - Centre for Ecology and Hydrology, UK Jim Musucci Monsanto Company Ben Matthews USDA ARS Jennifer Anderson Pioneer Eliot Herman (Danforth Center) University of Arizona
33 Thank You!
34 Developments since the conference Zhang et el Report evidence that micro RNA (mirna) from rice can be found in human and mouse tissue Evidence suggesting that this mirna might regulate gene transcription both in vitro in human cells and in vivo in mice This result is surprising, and captured a lot of attention But does it impact the results of the conference? I think the answer is no
35 Risk Hypothesis for Mammalian Consumption of dsrna Risk Scenario Consumption of dsrna in food leads to harm (death or illness) The mechanism may be different than for GE plants expressing protein, but the assessment endpoint is the same Similar to pesticides with different mode of action Further, the same tests currently used to assess GE plants should be sufficient to address risk from an RNAi plant Toxicity testing (dsrna) Feeding studies
36 Verbatim Consensus Points The paradigm currently applied to the environmental risk assessment of genetically engineered plants is adequate for the assessment of RNAi plants. No plausible risk hypotheses were identified that can be considered unique to RNAi mechanisms when compared to other GE plants with similar traits. The same tests and protocols that are used for evaluating other GE plants will be sufficient for testing RNAi plants, including plants expressing pesticidal traits. The use of RNAi technologies allows for the use of alternative informative tests, such as bioinformatic analyses, to address certain risk questions. For plants expressing pesticidal dsrnas, bioinformatics can be applied to characterize potential susceptibility of relevant NTO species. The accumulation of bioinformatic data that defines thresholds for activity spectra based on shared sequence identity will reduce the need for NTO testing. Baseline data about environmental fate of dsrna will be broadly useful for future exposure analyses
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