Predator-Prey Interactions and Co-Evolution Between Carnivorous Fungi and the Nematode C. elegans

Nematodes are the most abundant animals on earth and many species are parasitic, causing diseases in human, animals and plants that result in more than a billion infections worldwide and > USD$80 billions loss annually. Drug resistance is an emerging problem. Hardy gastrointestinal nematodes displaying multidrug resistance to all three basic classes of anthelmintics (benzimidazoles, macrocyclic lactones and imidazothiazoles) have appeared around the world. Thus, new treatments or methods to control these parasites are urgently needed. Nematodes rely on elaborate networks of chemical signaling to communicate with each other and to interact with other species, including predators such as carnivorous fungi that have independently evolved within different lineages of the fungal kingdom. The predatorprey relationship between nematophagous fungi and nematodes makes them an ideal system to study inter-species communication and predator-prey co-evolution. We have established molecular and genetic tools to study the molecular interactions between the nematode-trapping fungi and the oyster mushroom with the model nematode C. elegans. We apply systematic approaches, combining genetics, genomics, molecular biology, cell biology, biochemistry, neurobiology, imaging analyses, computational modeling and chemical analyses to focus on the following questions:

1. Molecular mechanisms of nematode-sensing and trap morphogenesis in the nematode-trapping fungi
2. Molecular mechanisms of nematode-adhesion and penetration in nematode-trapping fungi
3. Evolution of the predatory behavior in Nematode-trapping fungi
4. Identification of the Nematocidal compounds in Pleurotus mushrooms
5. Molecular mechanisms of the development of specialized nematode-killing structure in Pleurotus
6. Neuronal basis of C. elegans behavior in response to fungal predators
7. Evolution of the behavior of C. elegans in response to fungal predators

• Education
• Achievements & Honors
• Selected publications
• Lab members

• PDF, 2010-2015, Division of Biology and Biological Engineering, California Institute of Technology
• Ph.D., 2008-2010, Department of Molecular Genetics and Microbiology, Duke University
• MS, 2003, Department of Plant Pathology and Microbiology, National Taiwan University
• BS, 2001, Department of Plant Pathology and Microbiology, National Taiwan University

• 2022, Academia Sinica Early-Career Investigator Research Achievement Award
• 2022, Taiwan Outstanding Women in Science Young Talent Award. Wu Chien-Shiung Education Foundation and L’Oréal Taiwan
• 2021, Biomedical Young Scientist Award, Tie-Te Lee Biomedical Foundation
• 2020, EMBO Young Investigator Program
• 2019, EMBO Global Investigator Network
• 2018, Taiwan Foundation for Advancement of Outstanding Scholarship Yong Scholars’ Creativity Award
• 2014, NIH/NIGMS Pathway to Independence (PI) K99 Award
• 2008, Genetics Society of America, DeLill Nasser Award

1. Ching-Han Lee, Yi-Yun Lee, Yu-Chu Chang, Wen-Li Pon, Sue-Ping Lee, Niaz Wali, Takehito Nakazawa, Yoichi Honda, Jiun-Jie Shie, Yen-Ping Hsueh (2023) A carnivorous mushroom paralyzes and kills nematodes via a volatile ketone. SCIENCE ADVANCES 18 Jan 2023 Vol 9, Issue 3.
2. Sheng-An Chen, Hung-Che Lin, Yen-Ping Hsueh (2022) The cAMP-PKA pathway regulates prey sensing and trap morphogenesis in the nematode-trapping fungus Arthrobotrys oligospora. G3 Genes|Genomes|Genetics 12, jkac217 (Cover)
3. Sheng-An Chen, Hung-Che Lin, Frank C Schroeder, Yen-Ping Hsueh (2021) Prey sensing and response in a nematodetrapping fungus is governed by the MAPK pheromone response pathway. Genetics 217: jyaa008.
4. Tsung-Yu Huang, Yi-Yun Lee, Guillermo Vidal-Diez de Ulzurrun, Yen-Ping Hsueh (2021) Forward genetic screens identified mutants with defects in trap morphogenesis in the nematode-trapping fungus Arthrobotrys oligospora. G3 11: jkaa022.
5. Yi-Yun Lee, Guillermo Vidal-Diez de Ulzurrun, Erich M Schwarz, Jason E Stajich, Yen-Ping Hsueh (2021) Genome sequence of the oyster mushroom Pleurotus ostreatus strain PC9. G3 11: jkaa008.
6. Ching-Ting Yang, Guillermo Vidal-Diez de Ulzurrun, A Pedro Gonçalves, Hung-Che Lin, Ching-Wen Chang, Tsung-Yu Huang, Sheng-An Chen, Cheng-Kuo Lai, Isheng J Tsai, Frank C Schroeder, Jason E Stajich, Yen-Ping Hsueh (2020) Natural diversity in the predatory behavior facilitates the establishment of a robust model strain for nematode- trapping fungi. PNAS 117: 6762-6770.
7. Ching-Han Lee, Han-Wen Chang, Ching-Ting Yang, Niaz Wali, Jiun-Jie Shie, Yen-Ping Hsueh (2020) Sensory cilia as the Achilles heel of nematodes when attacked by carnivorous mushrooms. PNAS 117: 6014-6022.
8. Guillermo Vidal-Diez de Ulzurrun, Tsung-Yu Huang, Ching-Wen Chang, Hung-Che Lin, Yen-Ping Hsueh (2019) Fungal feature tracker (FFT): A tool for quantitatively characterizing the morphology and growth of filamentous fungi. PLoS Comput Biol. 15: e1007428.
9. Yen-Ping Hsueh, Matthew R Gronquist, Erich M Schwarz, Ravi David Nath, Ching-Han Lee, Shalha Gharib, Frank C Schroeder, Paul W Sternberg (2017) Nematophagous fungus Arthrobotrys oligospora mimics olfactory cues of sex and food to lure its nematode prey. eLife 6: e20023.