Education

Research Description

My lab is interested in elucidating novel roles of vesicular trafficking in innate immunity and nutrient-deficiency responses. We focus on host clathrin-coated vesicle (CCV) components with novel roles in innate immune signaling, responses to Pseudomonas syringae pathogenic bacteria and iron (Fe) deficiency responses. This research interest has been ignited by my cross-disciplinary postdoctoral training in protein trafficking in plants (Prof. Natasha Raikhel, DOE Plant Research Lab, Michaigan State University, E. Lansing, MI, USA), sterol requirement in yeast endocytosis (Prof. Howard Riezman, Biozentrum, Basel, Switzerland) and syntaxin phosphorylation in plant immune signaling against pathogenic fungi (Cf-9/Avr9) (Prof. Jonathan Jones, Sainsbury Laboratory, Norwich, England).

The plasma membrane (PM) provides a critical interface between eukaryotic cells and their environment to control cellular responses. In the model plant Arabidopsis, the cellular mechanisms and molecular machineries regulating the PM proteome for effective immune responses and nutrient deficiency responses remain largely elusive. One strategy that cells use to control the protein composition of the PM is trafficking of cargo proteins to and from the PM by vesicular trafficking. Vesicular trafficking is the movement of cargo proteins from one organelle to another in form of small, membrane bound vesicles.

We utilize the plant immune receptor FLAGELLIN SENSING 2 (FLS2) that detects bacterial flagellin or its active peptide-derivative flg22. We and others have shown that FLS2 needs to reside at the PM to perceive flg22 for effective immune responses. A multifaceted vesicle trafficking network is essential for ensuring that FLS2 localizes correctly to its site of function (the PM) and in the correct abundance.

My lab focusses on identifying components of the clathrin-coated vesicle (CCV) network with novel roles in immune signaling and/or trafficking of FLS2 and other proteins with immune functions to and from the cell surface. Our efforts center on CCV components that function in endocytosis and secretion from the PM and the trans-Golgi network, respectively. To address these questions, we use a combination of interdisciplinary techniques including biochemical, cell biological, proteomic, metabolomics, genetic, molecular biological and live-cell imaging approaches. By identifying novel roles for dynamin-related proteins, epsin and clathrin components, our lab has advanced the limited understanding of the identity and role(s) of vesicle components that function in immune responses and/or trafficking of FLS2.

Recently, we have expanded our work from assessing roles of CCV components in flg22-signaling from the model plant Arabidopsis into the field-to-table crop maize. Furthermore, we discovered CCV components that govern Fe-deficiency responses in Arabidopsis, likely by modulating communication between the site at which Fe-deficiency is sensed (leaves) and the site at which Fe is taken up from the soil (root epidermis). We are also deciphering how plants utilize CCV components to help integrate Fe-deficiency and innate immune responses. As a large proportion of the world population rely on plants as their food source for the micronutrient Fe,  our long-term goals are to increase yield and nutritional value of crop species to improve food security and human health.

Our projects are currently funded by

1. NSF-Plant Biotic Interaction Grant #2220951 “MCA-Delineating molecular components and mechanisms of bacterial flagellin-induced immune responses in maize”. (May 2023-April 2026) PI, 90% effort (Co-PIs: Paula McSteen, David Braun).
2. NSF – Division of Environmental Biology Grant #2217322 “IntBIO: Defining how plants integrate abiotic and biotic stress signals to coordinate changes in plasma membrane proteomes throughout the organism”. (Sep 2022-Aug 2025) Co-PI, 30% effort (PI, Scott Peck, Co-PI David Mendoza-Cozatl).
3. MU CAFNR Joy of Discovery “Towards understanding how protein trafficking modulates iron (Fe) uptake and allocation in model and crop plants” (Jan 2022-Dec 2023) PI; 40% effort (Co–PIs, Scott Peck, David Mendoza-Cozatl).

Notable Honors and Service

• Recipient, 2023 CAFNR-Outstanding Graduate Mentor Award, MU (April 2023)
• Recipient, 2021 CAFNR-Outstanding Undergraduate Advisor Award, MU (Spring 2022)
• Ann K. Covington Award for Outstanding Mentoring, Univ. of Missouri (April 2018)
• Outstanding Undergraduate Research Mentor Award, Univ. of Missouri (April 2018)
• Mentor for four “American Society of Plant Biologists (ASPB)- Summer Undergraduate Research Fellowships (SURF)” students (Summers 2014, 2016, 2022, 2023)
• Outstanding Undergraduate Mentor Award – Biochemistry, Univ. of Missouri (April 2015)
• EMBO Long Term Fellowship, Sainsbury Laboratory, Norwich, England (Feb. 2001- Jan. 2003)
• Human Frontier Science Program Fellowship, Biozentrum, Univ. of Basel, Basel, Switzerland (Oct. 1998 – Sep. 2000)
• EMBO Short Term Fellowship, Technical Univ. of Graz, Graz, Austria (March 1999)
• Fulbright Scholarship, Michigan State University, DOE-PRL, East Lansing, USA (Sep. 1989 – Aug. 1990)

Selected Publications

Ekanayake G, Leslie ME, Smith JM, Heese A (2023) Arabidopsis Dynamin-Related Protein AtDRP2A contributes to late flg22-signaling and effective immunity against Pseudomonas syringae bacteria. Molecular Plant-Microbe Interaction (MPMI) 36 (4) 201–20.  PMID: 36653183. [PubMed]

Mason KN, LaMontagne-Mueller ED, Sauer M, Heese A (2023) Arabidopsis clathrin adaptor EPSIN1 but not MODIFIED TRANSPORT TO THE VACOULE1 contributes to effective plant immunity against pathogenic Pseudomonas bacteria. Plant Signal Behav 2023 18(1):2163337. PMID: 36603596. [PubMed]

Dahhana DA, Reynolds GD, Cárdenasa JJ, Johnson A, Eeckhoutb D, Vanga N, Ypermanb K, Hwang I, Heese A, De Jaeger G, Friml J, Van Damme D, Pane J, Bednarek SY. (2022) Proteomic Characterization of Isolated Arabidopsis Clathrin-Coated Vesicles Reveals Evolutionarily Conserved and Plant Specific Components. The Plant Cell 34(6):2150-2173. PMID: 35218346. [PubMed]

Mc Gowan G, Ekanayake G, Ingle R#, Heese A# (2022) Novel roles for Arabidopsis dynamin-related proteins DRP1A and DRP2B in resistance against Botrytis cinerea fungal infection. Plant Signal Behav 17(1):2129296. PMID: 36200597. [PubMed]

Ekanayake G, Smith JM, Jones KB, Stiers HM, Robinson SJ, Lamontagne ED, Kostos PH, Cornish PV, Bednarek SY, Heese A# (2021). DYNAMIN-RELATED PROTEIN DRP1A functions with DRP2B in plant growth, flg22-immune responses and endocytosis. Plant Physiology 185: 1986-2002. PMID: 33564884. [PubMed]

Ma X, Claus LAN, Leslie ME, Tao K, Wu Z, Liu J, Yu X, Li B, Zhou J, Savatin DV, Peng J, Tyler BM, Heese A, Russinova E, He P, Shan L. (2020). Ligand-induced monoubiquitination of BIK1 regulates plant immunity. Nature. 2020 May;581(7807):199-203. doi: 10.1038/s41586-020-2210-3. Epub 2020 Apr 22. PMID: 32404997 [PubMed]

Collins CA, LaMontagne ED, Anderson JC, Ekanayake G, Clarke AS, Bond LN, Salamango DJ, Cornish PV, Peck SC, Heese A. (2020). EPSIN1 Modulates the Plasma Membrane Abundance of FLAGELLIN SENSING2 for Effective Immune Responses. Plant Physiol. 2020 Apr;182(4):1762-1775. doi: 10.1104/pp.19.01172. Epub 2020 Feb 24. PMID: 32094305 [PubMed]

Mason KN, Ekanayake G, Heese A. (2020). Staining and automated image quantification of callose in Arabidopsis cotyledons and leaves. Methods Cell Biol. 2020;160:181-199. doi: 10.1016/bs.mcb.2020.05.005. Epub 2020 Jun 16.PMID: 32896315 [PubMed]

Ekanayake G, LaMontagne ED, Heese A. (2019). Never Walk Alone: Clathrin-Coated Vesicle (CCV) Components in Plant Immunity. Annu Rev Phytopathol. 57:387-409. doi: 10.1146/annurev-phyto-080417-045841. [PubMed]

LaMontagne ED, Heese A. (2017). Trans-Golgi network/early endosome: a central sorting station for cargo proteins in plant immunity. Curr Opin Plant Biol. 40:114-121. doi: 10.1016/j.pbi.2017.08.012. Review. [PubMed]

Leslie ME, Heese A. (2017). Quantitative Analysis of Ligand-Induced Endocytosis of FLAGELLIN-SENSING 2 Using Automated Image Segmentation. Methods Mol Biol. 1578:39-54. doi: 10.1007/978-1-4939-6859-6_4. [PubMed]

Collins CA, Leslie ME, Peck SC, Heese A. (2017). Simplified Enrichment of Plasma Membrane Proteins from Arabidopsis thaliana Seedlings Using Differential Centrifugation and Brij-58 Treatment. Methods Mol Biol. 1564:155-168. doi: 10.1007/978-1-4939-6813-8_13. [PubMed]

Leslie ME, Rogers SW, Heese A. (2016). Increased callose deposition in plants lacking DYNAMIN-RELATED PROTEIN 2B is dependent upon POWDERY MILDEW RESISTANT 4. Plant Signal Behav. 11(11):e1244594. [PubMed]

Smith JM, Leslie ME, Robinson SJ, Korasick DA, Zhang T, Backues SK, Cornish PV, Koo AJ, Bednarek SY, Heese A. (2014). Loss of Arabidopsis thaliana Dynamin-Related Protein 2B reveals separation of innate immune signaling pathways. PLoS Pathog. 10(12):e1004578. doi: 10.1371/journal.ppat.1004578. eCollection 2014 Dec. [PubMed]

Leslie ME, Heese A. (2014). A re-elicitation assay to correlate flg22-signaling competency with ligand-induced endocytic degradation of the FLS2 receptor. Methods Mol Biol. 1209:149-62. doi: 10.1007/978-1-4939-1420-3_12. [PubMed]

Smith JM, Heese A. (2014). Rapid bioassay to measure early reactive oxygen species production in Arabidopsis leave tissue in response to living Pseudomonas syringae. Plant Methods. 10(1):6. doi: 10.1186/1746-4811-10-6. [PubMed]

Smith JM, Salamango DJ, Leslie ME, Collins CA, Heese A. (2014). Sensitivity to Flg22 is modulated by ligand-induced degradation and de novo synthesis of the endogenous flagellin-receptor FLAGELLIN-SENSING2. Plant Physiol. 164(1):440-54. doi: 10.1104/pp.113.229179. Erratum in: Plant Physiol. 2017 Aug;174(4):2549. [PubMed]

Lu D, Lin W, Gao X, Wu S, Cheng C, Avila J, Heese A, Devarenne TP, He P, Shan L. (2011). Direct ubiquitination of pattern recognition receptor FLS2 attenuates plant innate immunity. Science. 332(6036):1439-42. doi: 10.1126/science.1204903. [PubMed]

Backues SK, Korasick DA, Heese A, Bednarek SY. (2010). The Arabidopsis dynamin-related protein2 family is essential for gametophyte development. Plant Cell. 22(10):3218-31. doi: 10.1105/tpc.110.077727. [PubMed]

Korasick DA, McMichael C, Walker KA, Anderson JC, Bednarek SY, Heese A. (2010). Novel functions of Stomatal Cytokinesis-Defective 1 (SCD1) in innate immune responses against bacteria. J Biol Chem. 285(30):23342-50. doi: 10.1074/jbc.M109.090787. [PubMed]

Shan L, He P, Li J, Heese A, Peck SC, Nürnberger T, Martin GB, Sheen J. (2008). Bacterial effectors target the common signaling partner BAK1 to disrupt multiple MAMP receptor-signaling complexes and impede plant immunity. Cell Host Microbe. 4(1):17-27. doi: 10.1016/j.chom.2008.05.017. [PubMed]

Heese A, Hann DR, Gimenez-Ibanez S, Jones AM, He K, Li J, Schroeder JI, Peck SC, Rathjen JP. (2007). The receptor-like kinase SERK3/BAK1 is a central regulator of innate immunity in plants. Proc Natl Acad Sci U S A. 104(29):12217-22. [PubMed] This paper was highlighted in Science STKE (Jul 2007; tw269).

Mentoring Statement & Achievements

As a MU faculty, I advise and mentor postdoctoral fellows, graduate and undergraduate students in two capacities: as an academic advisor and as a research advisor. Independent of my role, my goals are for each student and postdoc to become confident, self-reliant and self-reflective, so that s/he can reach her/his full potential as a student in Biochemistry, CAFNR and MU. I strive to provide a stimulating, challenging and inclusive environment that allows for academic, scientific and personal growth of each student. I listen carefully to each person’s interests, ambitions and career goals as such knowledge allows me to tailor my mentoring and training efforts towards advancing the skills and potentials of the individual mentee. In addition to training them in authentic bench research, critical thinking and data analysis, I mentor them in preparing successful fellowship and graduate school applications, preparing & presenting posters at (inter)national meetings.

Undergraduates: I have hosted and served as a research mentor for 23 undergraduate students from diverse socio-economic background including females, rural MO, minorities, identifying as LGBTQ, and first-generation college students. My research undergraduates have achieved the following honors and accomplishments under my mentorship and research training:

• 9 different undergrads are co-authors on publications in high-impact journals [J Biol Chem (undergrad is first author), The Plant Cell, Plant Phys, PLOS Path, Plant Sign & Behav]
• 9 National Awards/Fellowships by 6 different undergrads: 1 NSF-Graduate Research Fellowship; 1 female Goldwater Scholarship recipient, 4 American Society of Plant Biologists-Summer Undergrad Research Fellowship (ASPB SURF); 2 – Outstanding Poster Award, Annual Biomedical Research Conference for Minority Students (ABRCMS); 2 NSF-funded travel awards to attend international conference in Europe.
• > 20 poster presentations by 8 different undergrads at 11 (inter)national scientific conferences; >30 poster presentations by 18 different undergrads at local MU forums; 48 MU Awards and Research Fellowships by 15 different undergrads including 4 MU Academic Distinction Awards; 7 Outstanding Undergraduate Honor’s Thesis-Biochemistry, 4 NIH IMSD-EXPRESS fellowships, 6 Freshmen Research in Plants Fellowships (FRIPS), 13 CAFNR Undergrad Research Internships, 6 Life Sciences Undergraduate Research Opportunity Fellowships, 5 “First Place” Poster awards at Life Sciences Week, 1 Outstanding Freshman Discovery Fellow Award; 1 MU Chancellor Award.
• Accepted into PhD, Master, Dentistry, Physical Therapy, Pharmacy & Medical School programs [U Michigan, Cornell Univ, Univ Wisconsin, WashU, The Saint Louis Univ, MU, Rush-Chicago, MO Stowers); or obtained jobs as research technicians (MO Stowers, Sigma).

Postdocs and Graduate students: I have hosted and mentored 2 postdocs, 7 PhD students and 2 visiting Master students, and I have provided professional training resulting in these achievements:

• First and coauthors on 13 different publications including in Nature, Plant Physiology, MPMI and PLOS Pathogens
• >15 talks at international conferences including ASPB Plant Biology, PANAM Plant Membrane Workshop, Plant Cell Dynamics Meetings, and Interface between Abiotic & Biotic Stress Responses and Redox/ROS IPG Symposia
• >15 talks at local seminar series or regional meetings including Summer CROPS Webinar Series, Local Auxin Meeting, IPG Plant Talks, Midwestern ASPB Meetings
• Presented > 50 posters at >20 different (inter)national, regional and local meetings.
• Awarded >20 travel grants to attend (inter)national meetings.
• Awarded fellowships to conduct research in PI’s lab including NSF-Graduate Research Fellowship, NIH-Initiative for Maximizing Student Development (IMSD), MU Life Sciences Fellowship, Wayne L. Ryan Graduate Fellowship
• Obtained postdoctoral positions at Univ. Wisconsin-Madison and Ohio State Univ; positions as Assistant Professor at Drury Univ (MO), Marian Univ (IN) and as research scientists in industry at Eurofins (PA), Elemental Enzymes (MO), Ely Lilly (IN).

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