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ARS Home Northeast Area Ithaca, New York Robert W. Holley Center for Agriculture & Health Emerging Pests and Pathogens Research Research





- Wang, Xiaohong
- Hansen, Zachariah
- 2023
- 2022
- Publications
- Plant Diseases (303)

Research Project: Biology and Management of Invasive Plant Pathogens Affecting Potato and Soybean **Location:
                            Emerging Pests and Pathogens Research** 2023 Annual Report **Objectives**
                                

Objective 1: Identify and characterize soybean cyst nematode (SCN) populations in newly detected regions in New York. (NP303, C1, PS1B)

Objective 2: Discover and characterize genes and proteins regulating the interactions between potato and its associated pathogens. (NP303, C2, PS2A)
   Sub-Objective 2.A: Characterize AIM-containing effector protein-encoding genes from PCN and their associated host proteins contributing to nematode parasitism or virulence. 
   Sub-Objective 2.B: Investigate a role of autophagy in potato diseases caused by other invasive potato pathogens.

Objective 3: Investigate novel or improved strategies to manage potato cyst nematodes and/or other invasive potato pathogens. (NP303, C3, PS3A)
   Sub-Objective 3.A:  Determine the resistance of breeding potato clones as well as wild potato clones to G. rostochiensis pathotypes.
   Sub-Objective 3.B: Clone the novel R gene present in the broad-spectrum resistant clone Y1-5.
    Sub-Objective 3.C: Determine the resistance of wild potato clones to G. pallida. **Approach**
                                

In general, nematodes and other invasive pathogens of potato and soybean crops cause severe yield loss, and effective control measures are often lacking. In addition, most nematicides are no longer available; thus alternative control strategies for emerging nematode species and pathotypes are critically needed. New plant biotechnologies will likely provide the basis for the development of novel methods of controlling nematode and other invasive pathogens, but the success of these methods will be dependent upon a complete understanding of the fundamental mechanisms of host-pathogen interactions. One approach is to identify and characterize soybean cyst nematode (SCN) populations in newly detected regions in New York. An extensive statewide SCN survey in NY will be condicted and soli samples will be analyzed to determine SCN population densities. A modified HG type test will be used to determine the virulence phenotypes of selected SCN pouplations. The data on SCN population density and virulence diversity will be used to develop recommendations on SCN management in New York. A second approach is to discover and characterize genes and proteins regulating the interactions between potato and its associated pathogens. AIM-containing effector protein-encoding genes from potato cyst nematodes (PCN) that potentially target the host autophagy machinery will be cloned and characterized by multiple technologies to better understand the function of these effectors in nematode parasitism and virulence. The third approach is to investigate novel or improved strategies to manage potato cyst nematodes and/or other invasive potato pathogens. Working with potato breeders we will continue to use bioassays to evaluate breeding clones and wild potato germplasm for nematode resistance. We will conduct nematode phenotyping of the Y1-5 F1 population and use a RenSeq approach coupled with long-read PacBio SMRT sequencing to identify the novel resistance gene(s) present in the wild potato clone Y1-5. Conceptually novel information on the population dynamics of nematode and other invasive pests of potato and soybean crops, and on host–pathogen interactions will aid in the development of new effective biologically-based disease control strategies. Novel genes and germplasm for disease resistance that are identified will accelerate resistance breeding in potatoes and disease resistant cultivars developed through conventional breeding and genetic engineering can be transferred readily to customers. **Progress Report**
                                

Objective 1: Identify and characterize soybean cyst nematode (SCN) populations in newly detected regions in New York. (NP303, C1, PS1B)

The soybean cyst nematode (SCN) continues to rank as the number one yield-limiting pathogen of soybean, causing over $1.5 billion in yield losses annually in the United States. SCN continues to spread as soybean acreage expands. Since its first detection in New York in 2016, SCN has already been spread to more than 30 counties. If SCN is left unmanaged, population densities and the potential for yield reduction will keep increasing. Unfortunately, SCN problems are often neglected in fields since aboveground symptoms of plant damage and yield loss may not be readily visible. Thus, regular monitoring of SCN population densities and virulence phenotypes is essential for developing management plans based on the use of resistant cultivars. In collaboration with Cornell Cooperation Extension educators, researchers in Ithaca have received and analyzed thirty-nine soil samples collected from soybean fields in New York. The soil analysis showed that four field samples contained nematode cysts. We further conducted the bioassay test to verify the nematode species. The results showed that none of the four cyst samples could reproduce on a susceptible soybean plant, indicating that the cysts recovered from the four soybean fields are not soybean cyst nematode. In summary, our results indicated that the surveyed thirty-nine soybean fields in New York may not have SCN infestation or have an SCN infestation level that is below detection.   

Objective 2: Discover and characterize genes and proteins regulating the interactions between potato and its associated pathogens. (NP303, C2, PS2A)

Sub-Objective 2.A: Characterize AIM-containing effector protein-encoding genes from PCN and their associated host proteins contributing to nematode parasitism or virulence. 

Potato cyst nematodes (PCN; Globodera rostochiensis and G. pallida) are among the most devastating plant pathogens that pose serious threats to food security globally. PCN delivers a mixture of secretory proteins known as effectors into host root cells to induce disease. Understanding how nematode effectors function in host root cells is necessary for developing effective and sustainable means for nematode control. We previously cloned and functionally characterized a novel NMAS1 (Nematode Manipulator of Autophagy System 1) effector gene from PCN. We found that NMAS1 effectors use a conserved sequence to target ATG8 (autophagy-related protein 8) proteins in potato (Solanum tuberosum). Targeting potato ATG8 proteins by NMAS1 effectors was found to affect the immune function of host autophagy, thereby helping promote nematode parasitism. A paper describing the results of this work has been published in a high-impact journal. Our studies have continued to identify additional host targets of NMAS1 effectors. Using a proteomics approach, two potato proteins, StATG20 (autophagy-related protein 20) and StCHMP1 (CHARGED MULTIVESICULAR BODY PROTEIN 1) were identified as candidate host targets of NMAS1 effectors. Protein-protein interaction assays further confirmed that NMAS1 can specifically interact with StATG20 or StCHMP1 in plant cells. We also used Arabidopsis atg20 mutants to evaluate the role of ATG20 protein in nematode parasitism. We found that atg20 mutants have enhanced resistance to nematode infection, indicating that modulating the function of ATG20 protein by NMAS1 effectors is required for nematode parasitism. A better understanding of the molecular interaction between NMAS1 and ATG20 may help develop novel resistance in potatoes against PCN. In addition, we found that PCN encodes a group of effectors that contain putative sequences capable of targeting the host autophagy machinery. We have cloned several of these effector genes from G. rostochiensis (golden nematode) and initiated the functional study of these effector genes. Understanding the function of this unique group of effectors, which potentially target host autophagy, will not only provide new knowledge on the molecular basis of nematode parasitism but may also suggest means for developing novel and durable nematode resistance in potatoes. 

Sub-Objective 2.B: Investigate a role of autophagy in potato diseases caused by other invasive potato pathogens.

Work was not conducted because of a vacant SY position.

Objective 3: Investigate novel or improved strategies to manage potato cyst nematodes and/or other invasive potato pathogens. (NP303, C3, PS3A)

Sub-Objective 3.A:  Determine the resistance of breeding potato clones as well as wild potato clones to G. rostochiensis pathotypes.

The research program in Ithaca is one of only two programs in the U.S. authorized to conduct research on potato cyst nematodes (PCN; golden nematode and pale cyst nematode), pests of regulatory concern. One of the key factors that have contributed to the success of golden nematode (GN) quarantine in New York is the availability of potato cultivars with resistance to GN. Researchers in Ithaca, New York, continued the collaboration with potato breeders at Cornell University and other major U.S. potato breeding programs to evaluate potato breeding clones for resistance against GN. A total of 158 breeding clones were screened using marker tests and pot bioassays; 67 of them showed resistance to the Ro1 pathotype of GN, and 6 of them showed resistance to the Ro2 pathotype of GN. These clones will be retested for GN resistance multiple times and further evaluated in fields by university collaborators until they may be released as a GN-resistant cultivar. We also evaluated 15 existing European cultivars and identified 3 cultivars (Toronto, Maria Huanca, and Morene) that showed strong Ro2 resistance. These resistant cultivars may serve as an alternative tool for Ro2 control in New York. Additionally, we reevaluated a group of wild potato clones and confirmed that many of them offer strong resistance to GN Ro2. 

Sub-Objective 3.B: Clone the novel R gene present in the broad-spectrum resistant clone Y1-5.

The wild potato clone Y1-5 of Solanum brevicaule was previously identified as offering strong resistance to both species of potato cyst nematodes (golden nematode and pale cyst nematode). A mapping population derived from Y1-5 as a resistant parent was generated for downstream mapping and cloning of the novel resistance gene(s) present in Y1-5. Studies this year focused on determining the resistance/susceptibility of the offspring of Y1-5 to nematode infection (referred to as genotyping) using bioassays. The phenotypic data are being collected and will be used to guide downstream discovery of candidate resistance genes.  

Sub-Objective 3.C: Determine the resistance of wild potato clones to G. pallida.
We previously identified a group of wild potato clones that showed strong resistance to the Ro2 pathotype of the golden nematode (Globodera rostochiensis).

We conducted bioassays to determine their resistance to G. pallida (pale cyst nematode), a pest that is only found in Idaho. Our results showed that seven of the clones exhibited strong resistance to G. pallida. These seven wild potato clones (PI 473011, PI 205407 and PI 275143 of Solanum brevicaule, PI 275152 and PI 218221 of S. boliviense, and PI 473311 and PI 320332 of S. vernei) offer robust and broad-spectrum nematode resistance. They represent valuable germplasm that can be introduced to potato breeding programs to develop potatoes with novel and durable nematode resistance or used in genetic crosses to discover new nematode resistance genes. **Accomplishments**
                                

1. A joint effort resulted in the release of a new resistant potato cultivar. Potato cyst nematodes (PCN; golden nematode and pale cyst nematode) are devastating pests for U.S. potato production, which is valued at $4.6 billion. Utilizing host resistance is the most effective and sustainable approach for PCN control. ARS researchers in Ithaca, New York, in collaboration with scientists at Cornell University, have developed and released a new golden nematode resistant potato cultivar named ‘Bliss’. This new cultivar can serve as an effective tool for golden nematode control and eradication in the U.S. It can also be utilized by potato breeders as parent material in genetic crosses to develop more resistant cultivars. **Review Publications**
                            *Chen, S., Cui, L., Wang, X. 2021. A plant cell wall-associated kinase encoding gene is dramatically downregulated during nematode infection of potato. Plant Signaling and Behavior. 17(1):e2004026. https://doi.org/10.1080%2F15592324.2021.2004026.*
                                *Chen, S., Mitchum, M., Wang, X. 2022. Characterization and response of two potato receptor-like kinases to cyst nematode infection. Plant Signaling and Behavior. 17:1. https://doi.org/10.1080/15592324.2022.2148372.*
                                *Dejong, W.S., Halseth, D.E., Plaisted, R.L., Wang, X., Perry, K.L., Qu, X., Paddock, K.M., Falise, M., Christ, B.J., Porter, G.A. 2023.  Lehigh, a variety with yellow flesh and resistance to the golden cyst nematode and common scab. American Journal of Potato Research. 100:163-168. https://doi.org/10.1007/s12230-022-09900-4.*
                                *Wang, X., Yang, H., Veronneau, P., Thurston, D., Mimee, B. 2021. Genome resources of two pathotypes of the potato cyst nematode Globodera rostochiensis from New York. Phytopathology. https://doi.org/10.1094/PHYTO-09-20-0403-A.*
                                *Chen, J., Chen, S., Xu, C., Yang, H., Achom, M., Wang, X. 2023.  A key virulence effector from cyst nematodes targets host autophagy to promote nematode parasitism. New Phytologist. 237:1374-1390. https://doi.org/10.1111/nph.18609.*
                                *Dejong, W., Halseth, D.E., Plaisted, R.L., Wang, X., Perry, K.L., Qu, X., Paddock, K.M., Falise, M., Christ, B.J., Porter, G.A. 2020. Waneta, a variety with excellent chip color out of cold storage, long tuber dormancy, and resistance to the Golden Cyst Nematode. American Journal of Potato Research. 97:580-585. https://doi.org/10.1007/s12230-020-09806-z.*


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