Source: UNIVERSITY OF CALIFORNIA, RIVERSIDE submitted to NRP
THREAT ASSESSMENT AND RESISTANCE CHARACTERIZATION OF A NOVEL ECOTYPE OF WOOLLY APPLE APHID
Sponsoring Institution
National Institute of Food and Agriculture
Project Status
ACTIVE
Funding Source
Reporting Frequency
Annual
Accession No.
1027495
Grant No.
2021-51181-35866
Cumulative Award Amt.
$789,141.00
Proposal No.
2021-07723
Multistate No.
(N/A)
Project Start Date
Sep 1, 2021
Project End Date
Aug 31, 2025
Grant Year
2021
Program Code
[SCRI]- Specialty Crop Research Initiative
Recipient Organization
UNIVERSITY OF CALIFORNIA, RIVERSIDE
(N/A)
RIVERSIDE,CA 92521
Performing Department
Botany and Plant Sciences
Non Technical Summary
The global apple industry, and especially the U.S. organic sector, depend on apple rootstocks that are resistant to diseases and insects, especially the woolly apple aphid (WAA). The main resistance factor used against WAA has remained viable for decades; however, an emerging ecotype was found in a global hub for rootstock export to overcome this resistance, threatening the viability of apple production. Large-scale replanting, reduced yields, and additional barriers to market entry alongside increased management costs will occur should this aphid invade without knowing how to manage it. Our international team has confirmed the breakdown of resistance in the field, identified what genes in rootstock provide resistance to typical WAA, and developed a plan to assess the threat of this ecotype and other WAA populations to current apple production while characterizing how resistance failed. Specifically, we will identify what genes allow this new ecotype to overcome rootstock resistance, determine if this ecotype or others with the same capacity to adapt occur across North American growing regions, and incorporate this knowledge into screens of current and breeding of new rootstocks to advance pest management. These results will provide growers with regionally specific risk assessment, the means to manage emerging and longstanding WAA genotypes, and novel understanding of how aphids adapt to host plants. This project addresses the legislatively mandated focus areas of Research in plant breeding, genetics, and genomics, Efforts to identify and address threats from pests, and New innovations and technology.
Animal Health Component
45%
Research Effort Categories
Basic
45%
Applied
45%
Developmental
10%
Classification

Knowledge Area (KA)Subject of Investigation (SOI)Field of Science (FOS)Percent
2011110106033%
2113110106067%
Goals / Objectives
Our preliminary results show that an emerging ecotype of WAA can overcome R5+ rootstocks, the main WAA management tool used solely by organic producers and employed throughout the US by conventional producers. This ecotype emerged in a hub of global export, suggesting invasion and resistance failure is imminent. Our previous work on R5+ resistance has identified the chromosomal region for both major and minor resistance genes, and we now have candidate genes underlying R5- resistance. However, our data also indicate a gene-for-gene interaction may play a role in resistance, setting the stage for regional management challenges. We have identified plant immune (resistance) genes in both R5+ and wild relatives and have unreleased genotypes that vary in these genes but remain untested against WAA. We have also identified other plant physiological and developmental processes that play a role in the resistance phenotype, possibly providing a means for enhanced (cross) resistance against other aphids and pathogens. We have predicted and begun characterization of WAA effectors shared with other aphids and have candidates that likely underlie the emerging ecotype's ability to overcome resistance. Until now, WAA performance assays have been the only means to assess rootstock resistance, with few studies attempting characterize resistance phenotypes or the molecular mechanisms underlying resistance for any Er loci. Understanding the fundamental processes that underlie WAA colonization and host immune responses are crucial for predicting the efficacy and durability of resistance in the field. Thus, we propose to:• Identify gene presence and expression that allow a new WAA ecotype to overcome rootstock resistance in Europe• Assess presence of the emerging ecotype (Obj. 1) and overall WAA genetic diversity across North American growing regions.• Identify plant genes that interact with WAA genes of interest from the emerging ecotype (Obj. 1 and 2) to advance rootstock development.
Project Methods
To reveal what new (or missing) genes and enhanced gene expression enable resistance to be overcome, we will use a combination of DNA and RNA sequencing of plants and insects across a resistance spectrum. For gene discovery and sequence polymorphism analysis, individuals with a reciprocal resistance phenotype will be collected and allowed to feed on R5+ and R5- plants to confirm performance. Two pools of each genotype will be collected (one for archive) and DNA will be extracted and shipped to UCR as part of the international survey of WAA genetics. To resolve the plant molecules linked to the resistance phenotype and test if overexpression enables performance, individuals will be colonized on a R5+ rootstock and a R5- rootstock alongside a local genotype that performs opposite on these genotypes. Age synchronized aphids (n=25 per plant) will be allowed to feed over time with both aphid and plant tissues collected for transcriptome profiling at 2 and 7d. Aphid feeding sites will be quickly excised and flash frozen and aphids will be collected and pooled per plant making four biological replicates/pools per genotype x time designation. All samples will be flash frozen and stored at -80C prior to extraction. RNA will be extracted following manufactured protocols. Extracted samples will be sent to a fee-based sequencing facility and raw reads will be cleaned and aligned each to their respective genome to generate gene counts.Differential expression between genotypes will be assessed using EdgeR with statistical contrasts made for general patterns (e.g., time, aphid, genotype) and genotype specific patterns. We will also construct a baseline constitutive R5+ gene expression profile and assess interactions with time to detect genes linked to constitutive and induced resistance in both R5+ and R5- plants and to normalize for changes in time. We will also compare plant gene expression to an unpublished Robusta 5 genome to manually curate novel genes not found in M. domestica genomes.To identify what gene absence or presence may underlie its resistance phenotype, DNA (collected in Obj 1) will be compared to WAA populations across the major growing regions from both cultivated and wild hosts. To leverage a whole genome resequencing approach, insect samples will be collected from commercial and research orchards and nurseries throughout Europe (n≥15), Canada (n≥15), and across the major growing regions in the U.S. (n≥300). Insects will also be sampled from wild hosts near orchards when present, and chosen on the basis of apple production density and degree of geographic isolation, with a goal to sample the widest possible area. Samples will be both targeted and opportunistic. Field collections will occur over two years. Samples will be collected, maintained in refrigeration (on ice), and then preserved in 95% alcohol back at the lab. Samples will be stored at -20C prior to shipping to UCR and then DNA extracted and prepped for Illumina NovaSeq at the UCR core facilities. Sequencing will target >30x coverage for all samples and nucleotide polymorphisms (SNPs) will be identified using standard bioinformatics analyses.To identify the specific plant genes that interact with WAA genes of interest we will employ two complementary protein interaction assays and screen newly developed rootstocks for resistance. For the Y2H-BiFC protein interaction pipeline candidate effectors defined in Obj. 1 and 2 will be screened against protein products of an apple cDNA library in a yeast-two hybrid assay as in with modifications. Here, WAA effector genes (excluding signal peptide) will be PCR amplified from cDNA and the amplified genes will be cloned into a gateway cloning vector and then recombined and transformed into yeast. Next, plant candidate genes will be PCR amplified from apple cDNA and cloned into a complementary vector using the gateway recombination technique, and subsequently screened for potential interactions. To validate the apple resistance-related proteins that interact with WAA effector proteins during the Y2H, a Bimolecular Fluorescence Complementation (BiFC) approach for direct protein-protein interaction will be used. The genes will be transferred from the previously prepared entry clones into gateway compatible BiFC destination vectors. Both insect and plant vectors (plasmids) containing target candidate genes will be transformed into apple protoplasts and visualized for YFP signals to detect protein interaction under confocal laser scanning microscope. For additional validation, the same vectors will be transformed into agrobacterium strain GV3101 followed by inoculation into Nicotiana benthamiana leaves. After incubation in dark for 2-3 days, transformed leaves from N. benthamiana plants will be observed for YFP signals under confocal microscope.Protoplasts from young apple leaves will be harvested where 20-25 days old leaves from in-vitro cultivated apple plants will be collected and cut into small slices of 1 mm. Leaf slices will be digested in Cell-wall digestion enzyme solution (macerozyme R-10 (0.15% (wt/vol)), cellulase R-10 (1% (wt/vol)), and hemicellulose (1.5% (wt/vol)) in 20 mM MES, supplemented with 0.5 M mannitol, 20 mM KCl, and 10 mM CaCl2, and vacuum infiltrated for 20-30 min followed by gentle shaking (40 rpm) in dark at room temperature overnight. Samples will be washed and protoplasts will be filtered through nylon mesh before centrifugation. Following resuspension in a sucrose solution. The supernatant will be discarded. and protoplasts will be washed again. The viability and density of apple protoplasts will be determined using a haemocytometer. Isolated protoplasts used in interaction assays will be incubated at room temperature overnight and examined under fluorescence microscope for YFP signals.To increase short-term tangible results from this proposal, we will also perform enhanced WAA-rootstock screens each summer. Unreleased rootstocks derived from parents Robusta 5, G.16, and several wild species that feature resistance to WAA have been or will be genotyped with high resolution SNP chips for discovery of the physical location of additional genetic effectors that modulate resistance to WAA. Diverse regional collections of WAA from the Northeast U.S. (where diversity is predicted to be highest) will be allowed to freely colonize rootstocks used in performance trials with successful genotypes sequenced for DNA (as in Obj. 2) to link insect genetic patterns with performance and diverse host plant genotypes.

Progress 09/01/23 to 08/31/24

Outputs
Target Audience:We delivered numerous extension and outreach talks to WA, MI, NY, and PA growers at state and county level engagements to introduce people to the project and solicit for areas of interest to sample insects. In various labs undergraduates, including from underrepresented groups were involved in research. One postdoctoral researcher and two graduate students in the PI lab worked on the system processing samples for molecular analyses. Changes/Problems:During 2022-2023 the postdoctoral union negotiated a new contract with UC that increased salaries. This was not planned for in the budget and there is no additional funding to offset this, so components of Obj 3 are being adjusted to ensure completion of most of the project. The original PD transferred operation of this award to a new PD (January 2024) and a graduate student has begun work on the data analysis. What opportunities for training and professional development has the project provided? Nothing Reported How have the results been disseminated to communities of interest?We delivered numerous extension and outreach talks to WA, MI, NY, and PA growers at state and county level engagements to introduce people to the project and solicit for areas of interest to sample insects. In various labs undergraduates, including from underrepresented groups were involved in research. One postdoctoral researcher and two graduate students in the PI lab worked on the system processing samples for molecular analyses. What do you plan to do during the next reporting period to accomplish the goals?Data analysis for Obj 1 and Obj 2 will begin by Fall 2024 with manuscript preparation ongoing. Obj 3 will begin Fall 2024 based on findings from Obj 1 and 2.

Impacts
What was accomplished under these goals? In year 3, we submitted all DNA samples for sequencing to examine the genetic differences in the European genotype able to overcome resistance (Obj 1). The RNAseq experiment to profile resistant breaking genotypes was also completed and samples submitted. Insect performance of the glasshouse trials largely mirrored field trials and confirmed the resistance breaking trait is present in different populations in Europe (Obj 1). Isoform level data were returned and are currently being analyzed. Insect samples collected in 2022 were extracted and a subsample sequenced at low coverage to verify sequence integrity relative to quality of extractions. All samples from 2022 were assessed for metadata (host genotype, geography, etc) and additional sampling was completed in 2023, amassing ~400 replicates. All samples were extracted, confirmed of high quality (reextracted if not) and submitted for sequencing. Half the samples have been returned and the other half are expected by the end of summer (Obj 2). The protein interaction pipeline was completed (in 2023) for two known aphid effectors (Obj 3) and is in draft to merge with sequencing data in publication. This assay revealed the WAA armet protein does not bind to the same plant target as in other species, but that the ortholog of Me10 does bind to a similar 14-3-3 protein. Thus, even with effectors shared with other aphids, the WAA targets different suites of apple proteins for successful interactions. Once the remaining sample sequences are generated, the final data analysis will begin (Obj 1 and 2) prior to proceeding with the protein interaction assays.

Publications


    Progress 09/01/22 to 08/31/23

    Outputs
    Target Audience:We delivered numerous extension and outreach talks to WA, MI, NY, and PA growers at state and county level engagements to introduce people to the project and solicit for areas of interest to sample insects. In various labs undergraduates, including from underrepresented groups were involved in research. One postdoctoral researcher and two graduate students in the PI lab worked on the system processing samples for molecular analyses. Changes/Problems:During 2022-2023 the postdoctoral union negotiated a new contract with UC that increased salaries. This was not planned for in the budget and there is no additional funding to offset this, so components of Obj 3 are being adjusted to ensure completion of most of the project. What opportunities for training and professional development has the project provided? Nothing Reported How have the results been disseminated to communities of interest?We delivered numerous extension and outreach talks to WA, MI, NY, and PA growers at state and county level engagements to introduce people to the project and solicit for areas of interest to sample insects. In various labs undergraduates, including from underrepresented groups were involved in research. One postdoctoral researcher and two graduate students in the PI lab worked on the system processing samples for molecular analyses. What do you plan to do during the next reporting period to accomplish the goals?Obj 1 samplesare all collectedand being processed. Sequencing will be scheduled for Fall 2023 with analysis and manuscript preparation by summer 2024. Obj 2 samples are largely (~75% collected and extracted for sequencing). Additional samples will be collected Fall 2023, process and submitted by winter 2024, and analyzed for a manuscript by summer 2024. Obj 3 is awaiting data and samples from 2023 prior to being scheduled.

    Impacts
    What was accomplished under these goals? In year 2, we collected and prepared additional insect genotypes for sequencing to examine the genetic differences in the European genotype able to overcome resistance (Obj 1). The RNAseq experiment to profile resistant breaking genotypes was conducted. Insect performance of the glasshouse trials largely mirrored field trials and confirmed the resistance breaking trait is present in different populations in Europe (Obj 1). Both plant and insect samples are currently being processed for sequencing in Fall 2023. Insect samples collected in 2022 were extracted and sequenced at low coverage to verify sequence integrity relative to quality of extractions. All samples from 2022 are processed and once archived samples are extracted, sequencing will be scheduled (Fall 2023) (Obj 2). Based on metadata (cultivar and scion type) additional samples are currently being scouted for and collected to establish ample sample size for genotype specific comparisons. These samples will be processed, sequenced and combined with prior data in winter 2024. The protein interaction pipeline was completed for two known aphid effectors (Obj 3). This revealed apple proteins targeted by these effectors and provided new insight into how the same aphid effector proteins target different host proteins across host species. A manuscript is in draft.

    Publications


      Progress 09/01/21 to 08/31/22

      Outputs
      Target Audience:We delivered numerous extension and outreach talks to WA, MI, NY, and PA growers at state and county level engagements to introduce people to the project and solicit for areas of interest to sample insects. Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided?Undergraduates including from underrepresented groups were involvedin research and extension activities, oriented to the project, and shadowed researchers or helped with sampling. A postdoctoral scientist was oriented to the apple-aphid system and is conducting molecular analyses. How have the results been disseminated to communities of interest? Nothing Reported What do you plan to do during the next reporting period to accomplish the goals?DNA is collected and awaiting sequencing (Obj 1). Upon analysis we will have targets for resistance screening via protein interaction assays (Obj 3). The experimental design is established and will proceedfor RNAseq of resistant interactions (Obj 1) next summer.Samples are in hand for population genotyping (Obj 2) and will be sequenced fall/winter 2023. Preliminary analyses will determine cultivars and regions to target for sampling in year 2.

      Impacts
      What was accomplished under these goals? We collected and prepared insect DNA for sequencing to verify the genetic difference in the genotype able to overcome resistance (Obj 1). RNAseq experimental setup was explored, troubleshot, and will commence in 2023. Timing was optimizedto balance aphid population growth and containment with naturally occurring parasitoid populations that limit experimental approaches. Upwards of 200 viable insect samples were collected from across North America and Europe (Obj 2). Samples will be processed, sequenced and linked to metadata this fall 2022. Targeted collections based on this year's sampling will occur as planned in 2023. Tissues of both aphids and plants were collected and processed to generate cDNA for protein interaction screening (Obj 3). Three genes shared among hemiptera are currently being profiled to establish the bioassay and analysis pipeline (Obj 3).

      Publications