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Professor, Molecular Biosciences & Bioengineering, University of Hawaii 2019-current
Chair & Professor, Molecular Biosciences & Bioengineering, University of Hawaii 2011-2019
Professor, Molecular Biosciences & Bioengineering, University of Hawaii 2006-2011
Visiting Professor, Molecular & Cellular Biology, University of Colorado 2005-2006

Projects :

Minor Crops Papaya Pests and Diseases, USDA-Research Services
"Using CRISPR-CAS for creating disease resistance in Papaya"
"Bioengineering Papaya for Resistance to Phytophthora palmivora”

National Science Foundation, MCB-Cellular Biology Program
"Functional genomics of the protein disulfide isomerase gene family: Unraveling protein folding  and redox-regulatory networks".

National Science Foundation, Major Research Instrumentation.
"Acquisition of Instrumentation for Transmission Electron Microscopy at the University of Hawaii"

USDA-Research Services  Papaya Pests and Diseases, USDA-Research Services 
“Characterization and Cloning of Pathogen-Inducible Genes and Promoters to Improve Resistance of Papaya to Fungal Disease”

Courses Offered:

MBBE 304  Biotechnology: Science and Ethical Issues (3 credits)
Introduction to the concepts, goals, impacts, socio-ethical issues, controversies, and consequences of biotechnology using real-life case studies of cloning, stem cells, GMO foods, DNA fingerprinting, gene therapy, genetic engineering and pharmaceuticals. (Cross-listed as BIOL 304); Pre:  BIOL 171 (concurrent) or consent.

MBBE 499/699 Directed Research (1-4 credits)
Research experience training in the methods of plant molecular and cellular biology, genetics, biochemistry, genomics.

Research Interests :

My lab's research emphasizes two general areas: 1) basic research exploring the function of plant cells at the molecular level in response to heat stress; and 2) the application of plant biotechnology to solve practical problems faced by local agriculture, such as papaya and pineapple. In the first area, we are elucidating the intriguing molecular mechanisms that regulate plant growth and productivity in response to heat stress. This involves the characterization of protein-protein interactions and protein-membrane dynamics involved in secretory protein folding in both in vitro and live cells.  We utilize a combination of advanced molecular, cellular, genetic, and biophysical methods applied to the model plant, Arabidopsis thaliana. For example, we have been measuring fluorescence resonance energy transfer (FRET) between fluorophore fusions of interacting proteins using state-of-the-art confocal laser microscopy (Fluorescence lifetime imaging). These proteins are modified by site-directed mutagenesis to identify residues involved in the protein-protein interactions.

Studies on secretory protein synthesis and folding in the endoplasmic reticulum (ER) focus on a class of enzymes designated as the protein disulfide isomerases (PDI). We have found that PDIs play roles in the protection of pollen from heat stress, the accumulation of proteins in seeds, the nutritional value of grain, and the secretory trafficking of proteins to other compartments in plants. We have used PDI-specific antisera, electron microscopy and immunolabeling as well as green fluorescent protein fused to PDIs, to localize the proteins to sub-cellular membranes and organelles of leaf, embryo and root cells. We have located PDIs in the ER, vacuole, chloroplast, golgi and apoplasm.  Reverse genetics are being used to identify the phenotypes of PDI knockouts. Yeast-two hybrid analyses, co-immunoprecipitation and FRET experiments are used to identify and study proteins that interact with PDIs. Complementation of protein folding mutants of E. coli and yeast and protein folding assays  distinguish between isomerase, reduction and oxidation functions.

  In the second area of research, our primary goals are to decrease the use of pesticides in agriculture by developing pest and disease resistant plants. We contribute the tools of molecular biology in collaborative research that uses biotechnology (such as gene editing) to improve anthuriums, papaya, and pineapple. In papaya, we are developing plants that are resistant to the pathogen, Phytophthora palmivora.  In Anthuriums, we investigate the genetic manipulation of aging and senescence. In pineapple, we study the biochemistry of protease inhibitors. A genomics approach is being used to isolate and characterize comprehensive sets of tissue-specific genes from tropical fruit crops. Detailed expression and regulation analyses and tissue-specific promoter isolation are being undertaken.

Our lab also sponsors community college and undergraduate research training funded by various federal grants. We have brought community college and UH-Manoa faculty and students together to gain hands-on experience in molecular biology research. They work as teams on experimental problems using state-of-the-art molecular biological, bioinformatic, cellular, genomic and biochemical approaches.

Recent Publications :

•  Elias, M.J., Hasley, J., Tian, M. and Christopher, D.A. (2023) Development of a Mesophyll Protoplast-Based System for Gene Editing of Papaya. In Vitro Cell Developmental Biology-Plant. https://doi.org/10.1007/s11627-023-10373-1 
• • Carrillo, R.M. and Christopher, D.A. (2022) Development of a GFP biosensor reporter for the unfolded protein response-signaling pathway in plants: Incorporation of the bZIP60 intron into the GFP gene. Plant Signaling & Behavior, 17(1): 8 pp. https://doi.org/10.1080/15592324.2022.2098645
• • Carrillo, R.M., Feldeverd, E., Christopher, D.A. (2021) The use of fluorescent protein fusions to monitor the unfolded protein response and protein foldase-substrate interactions in plant protoplasts. In: "The Unfolded Protein Response: Methods and Protocols." (Robert P. Torrado, Ed.) Springer-Nature Humana Press, Methods in Molecular Biology.
• • Feldeverd, E., Porter, B.W., Yuen, C.Y.L, Iwai, K.,Carrillo, R., Smith, T., Barela, C., Wong, K., Wang, P.-F., Kang, B.-H., Matsumoto, K., Christopher, D.A (2020) The Arabidopsis Protein Disulfide Isomerase Subfamily M Isoform, PDI9, Localizes to the Endoplasmic Reticulum and Influences Pollen Viability and Proper Formation of the Pollen Exine During Heat Stress. Frontiers in Plant Science.11:610052. doi: 10.3389/fpls.2020.610052
• • Yuen, C.Y.L, Wang, P.-F., Kang, B.-H., Matsumoto, K., Christopher, D.A. 2017. A Non-Classical Member of the Protein Disulfide Isomerase Family, PDI7, of Arabidopsis thaliana, Localizes to the cis-Golgi and Endoplasmic Reticulum Membranes. Plant & Cell Physiology, 58: 1103–1117. (Cover Feature).
• • Shimshock, R.G. and Christopher, D.A. 2017. Genetic Manipulation of Stilbene Composition in Plants to Enhance Pathogen Resistance. (In: Stilbene Derivatives Applications and Research, S. Henderson, Ed.), Nova Science Publishers, NY. pp. 23-48.
• • Yuen, C.Y.L, Shek, R., Kang, B.-H., Matsumoto, K., Cho, E.-J., Christopher, D.A. 2016. Arabidopsis protein disulfide isomerase-8 is a type I endoplasmic reticulum transmembrane protein with thiol-disulfide oxidase activity. BMC Plant Biology, 16:181-196.
• • Yuen, C.Y.L, Wong, K., Christopher, D.A. 2016. Phylogenetic characterization and promoter expression analysis of a novel hybrid protein disulfide isomerase/cargo receptor subfamily unique to plants and chromalveolates. Molecular Genetics Genomics, 291: 455–469.
• • Chinnasri, B. Sipes, B.S., Borsics T., Christopher, D.A. (2016) Induction of pathogenesis-related gene 1 (PR-1) by acibenzolar-s-methyl application in pineapple and its effect on reniform nematodes (Rotylenchulus reniformis). Agricultural & Natural Resources, 50:368–373.
• • Teixeira da Silva, J.A., Dobra´nszki, J., Zeng, S.J. , Winarto, B., Lennon, A.M., Jaufeerally-Fakim, Y., Christopher, D.A. (2015) Genetic transformation and molecular research in Anthurium: progress and prospects. Plant Cell Tissue & Organ Culture, 123:205–219.
• • Hilario, L.C., Shimshock, R., Ng, Cheryl, Bingham, J.-P., Christopher, D.A. 2015 Screening Carica papaya native promoters driving stilbene synthase expression in Arabidopsis thaliana for resveratrol glucoside (piceid) synthesis. Plant Biotechnology Reports, 9: 307-317.
• • Hilario, L.C., Christopher, D.A. 2015. Improved Agrobacterium-mediated transformation of Carica papaya cultivar ‘Kapoho’ from embryogenic cell suspension cultures. In Vitro Cellular & Developmental Biology-Plant 51: 580-587. http://dx.doi.org/10.1007/s11627-015-9719-4.
• • Porter, B.W., Yuen, C.Y.L, Christopher, D.A. 2015. Dual protein trafficking to secretory and non-secretory cell compartments: Clear or double vision? Plant Science, 234: 174-179.
• • Porter, B.P., Christopher, D.A. and Zhu, Y.J. 2014. Genomics of Papaya Disease Resistance. In: Genetics and Genomics of Papaya. Ming R and Moore PH (eds). Springer Science and Business Media, New York.
• • Hilario, L.C., Porter, B.W., Zhu, Y.J., Christopher, D.A. 2014. Identification and Characterization of Papaya (Carica papaya, L.) Promoters by Heterologous Expression as eGFP Fusions in Arabidopsis thaliana. Tropical Plant Biology 7:85-99.
• • Yuen, C.Y.L, Matsumoto, K.O., Christopher, D.A. 2013. Variation in the subcellular localization and protein folding activity among Arabidopsis thaliana homologs of PDI. Biomolecules 3:848-869.
• • Yuen, C.Y.L, Christopher, D.A. 2013. The group IV-A cyclic nucleotide-gated channels, CNGC19 and CNGC20, localize to the vacuole membrane in A. thaliana. AoB Plants 5: doi:10.1093/aobpla/plt012
• • Cho, E.J., Yuen, C.Y., Kang, B-H.,Ondzighi, C., Staehelin, L. A., Christopher, D.A. (2011) Protein disulfide isomerase-2 of Arabidopsis mediates protein folding and localizes to both the secretory pathway and nucleus, where it interacts with maternal effect embryo arrest factor. Molecules and Cells 32:459-75.
• • Yuen, C.Y.L and Christopher, D.A. 2010. The role of cyclic nucleotide-gated channels in cation nutrition and abiotic stress. (In: “Ion Channels and Plant Stress Responses, V. Demidchik & F. Maathuis eds),Springer-Verlag, Berlin-Heidelberg, Germany, pp. 137-158.
• • Guo, K.M., Babourina, O., Christopher, D.A., Borsics, T., Rengel, Z. (2010) The cyclic nucleotide-gated channel AtCNGC10 transports Ca2+ and Mg2+ in Arabidopsis. Physiologia Plantarum 139:303-312.
• • Neuteboom L.W., Matsumoto K.O., Christopher D.A. (2009) An extended AE-rich N-terminal trunk in secreted pineapple cystatin enhances inhibition of fruit bromelain and is post-translationally removed during ripening. Plant Physiology 151:515-527 (Cover Feature).
• • Porter B.W., Y.J. Zhu, Christopher, DA (2009) Carica papaya genes regulated by Phytophthora palmivora: A new system for comparative genomics of compatible Phytophthora-plant interactions. Tropical Plant Biology 2:84–97.
• • Porter, B.W., Zhu, Y.J., Webb, D.T., Christopher, D.A. 2009. Novel thigmomorphogenetic responses in Carica papaya: Touch decreases anthocyanin levels and stimulates petiole cork outgrowths. Annals of Botany 103:847-858.
• • Ondzighi, C.A., Christopher, D.A., Cho, E.J., Chang, S.C., Staehelin, L.A. 2008. Arabidopsis Protein Disulfide Isomerase-5 Inhibits Cysteine Proteases during Trafficking to Vacuoles before Programmed Cell Death of the Endothelium in Developing Seeds. The Plant Cell 20:2205-2220.
• • Lu, D-P, Christopher, DA (2008) Light enhances the unfolded protein response as measured by BiP2 gene expression and the secretory GFP-2SC marker in Arabidopsis. Physiologia Plantarum 134:360–368.
• • Lu, D-P, Christopher, DA (2008) Endoplasmic reticulum stress activates the expression of a sub-group of protein disulfide isomerase genes and AtbZIP60 modulates the response in Arabidopsis thaliana. Molecular Genetics & Genomics 280:199-210.
• • Guo, K.M., Babourina, O., Christopher, D.A., Borsics, T., Rengel, Z. (2008) The cyclic nucleotide-gated channel, AtCNGC10, influences salt tolerance in Arabidopsis. Physiologia Plantarum 134: 499-50
• • Porter, BW, Aizawa, KS, Zhu, YJ, Christopher DA (2008) Differentially expressed and new non-protein-coding genes from a Carica papaya root transcriptome survey. Plant Science 174:38-50 (2008).
• • Ming, R et al. (2008) Genome of the transgenic tropical fruit tree papaya (Carica papaya L.) Nature 452:991-995 • Lu, D.-P., Christopher, D.A. 2008. The effect of irradiance and redox-modifying reagents on the 52 kDa protein disulfide isomerase of Arabidopsis chloroplasts. Biologia Plantarum 52: 42-48.
• • D. A. Christopher, Borsics T, Yuen CYL, Ullmer W, Andème-Ondzighi C, Andres ML, Kang BH, Staehelin L.A. (2007) The cyclic nucleotide-gated cation channel AtCNGC10 traffics from the ER via Golgi vesicles to the plasma membrane of Arabidopsis root and leaf cells. Biomedical Central Plant Biology 7(48): 1471-2229. http://www.biomedcentral.com/1471-2229/7/48
• • T. Borsics, D. Webb, C. Ondzighi, L.A. Staehelin, D. A. Christopher, The cyclic nucleotide-gated calmodulin-binding channel AtCNGC10 localizes to the plasma membrane and influences numerous growth responses and starch accumulation in Arabidopsis thaliana. Planta 225:563-573 (2007).
• • Lau, T.S.L., Eno, E., Goldstein, G., Smith, C. Christopher, D.A. (2006) Ambient levels of UV-B in Hawaii combined with nutrient deficiency decrease photosynthesis in near-isogenic maize lines varying in leaf flavonoids: Flavonoids decrease photoinhibition in plants exposed to UV-B. Photosynthetica, 44: 394-403.
• • Lu D-P, Christopher, DA (2006) Immunolocalization of a protein disulfide isomerase to Arabidopsis thaliana chloroplasts and its association with starch biogenesis. Intl. J. Plant Sciences 167(1):1-9.
• • D.-P. Lu and D.A. Christopher, Analysis of isoforms of protein disulfide isomerase in plants by immuno-microscopy.” Microscopy & Microanalysis, 11(S2):1160-1161, (2005).
• • X.L. Li, T. Borsics, H.M. Harrington, D.A. Christopher, Arabidopsis AtCNGC10 rescues potassium channel mutants of E. coli, yeast and Arabidopsis and is regulated by calcium/calmodulin and cyclic GMP in E. coli. Functional Plant Biology, 32:643-653 (2005).
• • D.M. Hayden and D.A. Christopher, Characterization of senescence-associated gene expression and senescence-dependent and -independent cysteine proteases differing in microsomal processing in Anthurium, Plant Science, 166:779-790, (2004).
• • D.A. Christopher, Photosensory Pathways Regulating Chloroplast Gene Expression, (In: Handbook of Photochemistry & Photobiology, M.S.A. Abdel-Mottaleb & H.S. Nalwa, eds), American Scientific Publishers, 4:249-268, (2003).
• • Publications prior to 2003 excluded.
•  
• Recent Conference Presentations
• • Tian, M., Elias, M.J., Hasley, J., Dinulong, R-J., and Christopher, D.A. (2023) Genome editing of papaya. American Society of Plant Biologists, Aug. 2-6, 2023, Savannah, GA.
• • Carrillo, R., Albertson, A., and Christopher, D.A. (2023) Protein Disulfide Isomerase-9 modulates cellular stress in Arabidopsis through two mechanisms: Protein folding and via interaction with the master regulator, IRE1. American Society of Plant Biologists, Aug. 2-6, 2023, Savannah, GA .

• • Christopher, D.A., Feldeverd, E., Carrillo, R., Matsumoto, K.O. (2021) Studies on Protein Disulfide Isomerase to Develop Plant Tolerance to Heat Stress. Plant Science for Climate Emergency; June 7-9, 2021. • Carrillo, R., Christopher, D.A. (2021) Protein Disulfide Isomerase 9 modulates cellular stress in plants through interaction with the master regulator, IRE1. American Society of Plant Biologists WORLDWIDE SUMMIT, July 19-23, 2021
• • Yuen, CYL, Matsumoto, KO, Shek, R. Carrillo, R, Christopher, DA (2019) Variations in the structure, subcellular localization and protein folding activity of evolutionary diverse protein disulfide isomerases in Arabidopsis thaliana. American Society of Plant Biologists, Aug. 3-7, 2019, San Jose, CA
• • Yuen, C.Y.L, Wang, P.-F., Kang, B.-H, Matsumoto, K., Christopher, D.A. 2017. A Non-classical Member of the Protein Disulfide Isomerase Family, PDI7 of Arabidopsis thaliana, Cycles Between the cis-Golgi and Endoplasmic Reticulum Membranes. Cell Biology, American Society of Plant Biologists, June 24-27, 2017, Honolulu, HI.
• • Christopher, D.A. , Yuen, C.Y.L, Kang, B.-H., Matsumoto, K., Shek, R., 2016. The Arabidopsis Protein Disulfide Isomerases-7 and -8 are Transmembrane Proteins of the cis-Golgi and Endoplasmic Reticulum: Oxidase and Secretory Functions. SPEAKER Concurrent Symposium 20: Cell Biology, American Society of Plant Biologists, July 9-13, 2016, Austin, TX.
• • Yuen, CYL, Matsumoto, KO, Kang, B-H, Christopher, DA (2015) PDI7, a Novel Membrane-bound Member of the Protein Disulfide Isomerase Family, Localizes to the Cis-Golgi Cisternae and Endoplasmic Reticulum in Arabidopsis Thaliana. (700-023-Z ), American Society of Plant Biologists, July 25-30, 2015, Minneapolis, MN.
• • Hilario, LC, Christopher, DA (2015) Comparative functional identification and analysis of Carica papaya promoters in the model system Arabidopsis thaliana revealed post-transcriptional regulation of gene expression. 20th Plant Biology Symposium (Plant Stress-Omics in a Changing Climate), Penn State University. May 13-16, 2015.
• • Shimshock, R, Hilario, LC, Bingham, JP, Christopher, DA (2015) Biochemical analysis of the antimicrobial resveratrol glucoside in transgenic papaya calli differentially expressing the stilbene synthase gene controlled by three native papaya promoters. Annual Meeting of the American Society of Plant Biologists, July 25-30, 2015 Minneapolis, MN.