Ohio University | College of Arts and Sciences | Department of Environmental and Plant Biology

Porter Hall 315 | Athens OH 45701 | Tel 740 593 1126 | Fax 740 593 1130

Allan M. Showalter

Professor

Department Chair

Ph.D., Rutgers University, 1983

Molecular Biology and Biochemistry

Porter Hall 504

740 593 1135

Other Websites

Showalter Lab & Graduate Students

Faculty Research Focus Areas

Plant Cell Wall Biotechnology

Courses

PBIO 450/550 (Biotechnology and Genetic Engineering)
MCB 720 (Molecular Biology)
MCB 730 (Molecular and Cellular Biology Laboratory)
PBIO 427/527 (Molecular Genetics)
BIOL 101 (Principles of Biology)
PBIO 691 (Seminar)
Plant Cell Wall Club

Departmental Service

Graduate Committee

Professional Service

Full Curriculum Vitae (click here)
Chair (2009-2011) and Vice-Chair (2007-2009), Ohio Plant Biotechnology Consortium
Executive Committee (2001-present), Ohio Plant Biotechnology Consortium
Executive Committee (2004-2007), American Society of Plant Biologists
Midwest Section representative (2004-2007), American Society of Plant Biologists
Chair (2003-04) and Vice-Chair (2002-03), American Society of Plant Biologists (Midwest Section)
Invited Session Organizer and Speaker at the International Botanical Congress in Melbourne (2011)
Member, American Association for the Advancement of Science
Member, American Society of Plant Biologists
Member, Sigma Xi
Member, Ohio Plant Biotechnology Consortium

Research Program Summary

STRUCTURE, EXPRESSION AND FUNCTION OF PLANT CELL WALL PROTEINS
Research in my lab is directed at elucidating the structure, expression, and function of the superfamily of hydroxyproline-rich glycoproteins (HRGPs) found in plant cell walls. HRGPs represent the major protein components of the plant cell surface (i.e., the plant cell wall and plasma membrane) and include the arabinogalactan-proteins (AGPs), extensins (EXTs), proline-rich proteins (PRPs), and solanaceous lectins. Using a variety of molecular biology techniques, we have isolated and characterized a number of cDNA and genomic clones encoding these cell surface proteins. Moreover, we have used these clones as molecular probes to examine the regulated expression of these genes during development and in response to various stress conditions such as wounding, pathogen infection, and drought. Biochemical studies are underway to determine the molecular interactions that these proteins undergo once deposited at the cell surface. Current efforts to alter the expression of these HRGPs in plants using a variety of techniques (antisense RNA, RNA interference, insertional mutagenesis, overexpression, expression of fusion proteins) in transgenic plants is also underway in order to elucidate their expression, molecular interactions, and functions. We have expressed a GFP-arabinogalactan-protein fusion in transgenic plants and used it to demonstrate that this particular arabinogalactan-protein is attached to the outer leaflet of the plasma membrane via a glycosylphosphatidylinositol (GPI) lipid anchor. We have also established a link between arabinogalactan-proteins and programmed cell death in plants. Our recent work makes use of the genetic model plant, Arabidopsis thaliana, in which we are studying various AGP mutants to elucidate AGP function and also isolating the enzymes (and the genes) responsible for glycosylating AGPs and other HRGPs. Our research on arabinogalactan-proteins uses many experimental approaches (i.e., molecular genetics, molecular biology, biochemistry, functional genomics, cell biology, plant physiology) and is supported by NSF and USDA grants.

BIOINFORMATICS OF PLANT CELL WALL PROTEINS
Research in my lab also uses a a bioinformatic approach to the identification and characterization of plant cell wall hydroxyproline-rich glycoproteins (HRGPs). Initially, Arabidopsis was used as the model organism for this work; now other plant genomes/proteomes are being examined. This bioinformatics work complements the lab bench work that we do on HRGPs and relates to the evolution of the HRGP superfamily and to the evolution of plants.

MOLECULAR ADAPTATIONS OF HALOPHYTES TO SALINE ENVIRONMENTS
Another project in the lab involves examining the molecular adaptations of halophytes to saline environments. Here, Atriplex prostrata, a plant that thrives in saline environments, is being examined with respect to its physiological and molecular responses to growth under various salt concentrations. We are particularly interested in the role which glycinebetaine plays as an osmoprotectant. Consequently, we have cloned the genes that encode the pathway for the synthesis of glycinebetaine for the purpose of genetically engineering crop plants to survive in saline soils.

Selected References

Showalter, A.M. (1993) Structure and function of plant cell wall proteins. Plant Cell 5, 9-23. PDF

Li, S. and A.M. Showalter (1996) Cloning and developmental/stress-regulated expression of a gene encoding a tomato arabinogalactan protein. Plant Molecular Biology 32, 641-652. PDF

Wang, L.-W., A.M. Showater, and I.A. Ungar (1997) Effect of salinity on growth, ion content and cell wall chemistry in Atriplex prostrata Boucher. Amer. J. Bot. 84, 1247-1255. PDF

Khan, M.A., I.A. Ungar, A.M. Showalter, and H. Dewald (1998) NaCl-induced accumulation of glycinebetaine in four subtropical halophytes from Pakistan. Physiol. Plant. 102, 487-492. PDF

Khan, M.A., I.A. Ungar, and A.M. Showalter (1999) Effects of salinity on growth, ion content, and osmotic relations in Halopyrum mucronatum (L.) Stapf. J. Plant Nutr. 22, 191-204. PDF

Gao, M., M.J. Kieliszewski, D.T.A. Lamport, and A.M. Showalter (1999) Isolation, characterization, and immunolocalization of a novel, modular tomato arabinogalactan-protein corresponding to the LeAGP-1 gene. Plant J. 18, 43-55. PDF

Gao, M. and A.M. Showalter (1999) Yariv reagent treatment induces programmed cell death in Arabidopsis cell cultures and implicates arabinogalactan-protein involvement. Plant J. 19, 321-331. PDF

Gao, M. and A.M. Showalter (2000) Immunolocalization of LeAGP-1, a modular arabinogalactan-protein, reveals its developmentally regulated expression in tomato. Planta 210, 865-874. PDF

Khan, M.A., I.A. Ungar, and A.M. Showalter (2000) Effects of salinity on growth, water relations and ion accumulation of the subtropical perennial halophyte, Atriplex griffithii Moq. var. stocksii. Annals of Botany 85, 225-232. PDF

Khan, M.A., I.A. Ungar, and A.M. Showalter (2000) The effect of salinity on the growth, water status, and ion content of a leaf succulent perennial halophyte, Suaeda fruticosa (L.) Forssk. Journal of Arid Environments 45, 73-84. PDF

Showalter, A.M., M. Gao, M.J. Kieliszewski, and D.T.A. Lamport (2000) Characterization and localization of a novel tomato arabinogalactan-protein (LeAGP-1) and the involvement of arabinogalactan-proteins in programmed cell death. In Cell and Developmental Biology of Arabinogalactan-Proteins, (E. A. Nothnagel, A. Bacic, and A. E. Clarke, eds.), Kluwer Academic/Plenum Publishers: New York, pp. 61-70. PDF

Khan, M.A., I.A. Ungar, and A.M. Showalter (2000) Effects of sodium chloride treatments on growth and ion accumulation of the halophyte Haloxylon recurvum. Communications in Soil Science and Plant Analysis 31, 2763-2774. PDF

Stratford, S., W. Barnes, D.L. Hohorst, J.G. Sagert, R. Cotter, A. Golubiewski, A.M. Showalter, S. McCormick, and P. Bedinger (2001) A leucine-rich repeat region is conserved in pollen extensin-like (Pex) genes in monocots and dicots. Plant Mol. Biol. 46, 43-56. PDF

Lu, H., M. Chen, and A.M. Showalter (2001) Developmental expression and perturbation of arabinogalactan-proteins during seed germination and seedling growth in tomato. Physiologia Plantarum 112, 442-450. PDF

Showalter A.M. (2001) Arabinogalactan-proteins: structure, expression, and function. Cellular and Molecular Life Sciences 58, 1399-1417. PDF

Showalter A.M. (2001) Introduction: plant cell wall proteins. Cellular and Molecular Life Sciences 58, 1361-1362. PDF

Zhao Z., L. Tan, A.M. Showalter, D.T.A. Lamport, and M. Kieliszewski (2002) Tomato LeAGP-1 arabinogalactan-protein purified from transgenic tobacco corroborates the Hyp contiguity hypothesis. Plant Journal 31, 431-444. PDF

Chaves I., A. Regalado, M. Chen, C. Ricardo and A.M. Showalter (2002) Programmed cell death induced by (b-D-galactosyl)3 Yariv reagent in Nicotiana tabacum BY-2 suspension-cultured cells. Physiologia Plantarum 116, 548-553. PDF

Sun, W., Z.D. Zhao, M.C. Hare, M.J. Kieliszewski, and A.M. Showalter (2004) Tomato LeAGP-1 is a plasma membrane-bound glycosylphosphatidylinositol-anchored arabinogalactan-protein. Physiologia Plantarum 120, 319-327. PDF

Wang, L.-W. and A.M. Showalter (2004) Cloning and salt-induced, ABA-independent expression of choline mono-oxygenase in Atriplex prostrata. Physiologia Plantarum 120, 405-412. PDF

Sun, W., M.J. Kieliszewski, and A.M. Showalter (2004) Overexpression of tomato LeAGP-1 arabinogalactan-protein promotes lateral branching and hampers reproductive development. Plant Journal 40, 870-881. PDF

Sun, W., J. Xu, J. Yang, M.J. Kieliszewski, and A.M. Showalter (2005) The lysine-rich arabinogalactan-protein subfamily in Arabidopsis: gene expression, glycoprotein purification and biochemical characterization. Plant and Cell Physiology 46, 975-984. PDF

Khan, M.A., I.A. Ungar, and A.M. Showalter (2005) Salt stimulation and tolerance in an intertidal stem-succulent halophyte. Journal of Plant Nutrition 28, 1365-1374. PDF

Wang, L.-W., A.M. Showalter, and I.A. Ungar (2005) Effects of intraspecific competition on growth and photosynthesis of Atriplex prostrata. Aquatic Botany 83, 187-192. PDF

Lamport, D.T.A., M.J. Kieliszewski, and A.M. Showalter (2006) Salt stress upregulates periplasmic arabinogalactan proteins: using salt stress to analyse AGP function. New Phytologist 169, 479-492. PDF

Sardar, H., J. Yang, and A.M. Showalter (2006) Molecular interactions of arabinogalactan- proteins (AGPs) with cortical microtubules and actin in bright yellow 2 (BY-2) tobacco cultured cells. Plant Physiology 142, 1469-1479. PDF

Yang J., H.S. Sardar, K.R. McGovern, Y. Zhang, and A.M. Showalter (2007) A lysine-rich arabinogalactan-protein in Arabidopsis is essential for plant growth and development, including cell division and expansion. Plant Journal 49, 629-640. PDF

Sardar H. and A.M. Showalter (2007) A cellular networking model involving interactions among glycosylphosphatidylinositol (GPI)-anchored plasma membrane arabinogalactan proteins (AGPs), microtubules and F-actin in tobacco BY-2 cells. Plant Signaling and Behavior 2, 8-9. PDF

Yang J. and A.M. Showalter (2007) Expression and localization of AtAGP18, a lysine-rich arabinogalactan-protein in Arabidopsis. Planta, 226, 169-179. PDF

Xu, J., L. Tan, D.T.A. Lamport, A.M. Showalter, and M.J. Kieliszewski (2008) The O-Hyp glycosylation code in tobacco and Arabidopsis and a proposed role of Hyp-glycans in secretion. Phytochemistry 69, 1631-1640. PDF

Wu Y., M. Williams., S. Bernard, A. Driouich, A.M. Showalter, and A. Faik. (2010) Functional identification of two non-redundant Arabidopsis α(1,2)fucosyltransferases specific to arabinogalactan-proteins. J. Biol. Chem. 285, 13638–13645. PDF

Showalter, A.M., B. Keppler, J. Lichtenberg, D. Gu, and L.R.Welch (2010) A bioinformatics approach to the identification, classification, and analysis of hydroxyproline-rich glycoproteins. Plant Physiol. 153, 485-513. PDF

B. Keppler and A.M. Showalter (2010) IRX14 and IRX14-LIKE, two glycosyl transferases involved in glucuronoxylan biosynthesis and drought tolerance in Arabidopsis. Molecular Plant 3, 834-841. PDF

Liang, Y., A. Faik, M. Kieliszewski, L. Tan, W.-L. Xu, and A.M. Showalter (2010) Identification and characterization of in vitro galactosyltransferase activities involved in arabinogalactan-protein glycosylation in tobacco and Arabidopsis. Plant Physiol. 154, 632-642. PDF

Yang, J. and A.M. Showalter (2010) Subcellular localization of a classical arabinogalactan-protein from Arabidopsis. Journal of Fuzhou University (Natural Science) 38, 753-757. PDF

Zhang, Y., J. Yang, A.M. Showalter (2011) AtAGP18 is localized to the plasma membrane and functions in plant growth and development. Planta, 233, 675–683. PDF

Yang, J., Y. Zhang, Y. Liang, A.M. Showalter (2010) Expression analyses of AtAGP17 and AtAGP19, two lysine-rich arabinogalactan-proteins, in Arabidopsis. Plant Biology, 13, 431-438. PDF

Zhang, Y., J. Yang, A.M. Showalter (2011) AtAGP18, a lysine-rich arabinogalactan protein in Arabidopsis thaliana, functions in plant growth and development as a putative co-receptor for signal transduction. Plant Signaling and Behavior 6, 855-857. PDF

Much of this research was supported by the National Science Foundation (NSF) under grants IBN-0110413 and IBN-9727757; however, “any opinions, findings, and conclusions or recommendations expressed in this material are those of the author (s) and do not necessarily reflect the views of the National Science Foundation.”

Textbooks

See Courses section above. Click on the relevant course to open the course homepage and then click on the syllabus to see the most recent textbook being used for the course.

Funding

United States Department of Agriculture (USDA)
National Science Foundation (NSF)
Ohio Plant Biotechnology Consortium (OPBC)
Ohio University

Current and Recent Research Projects

Isolation and characterization of the enzymes and genes responsible for glycosylating arabinogalactan-proteins (AGPs) and other hydroxyproline-rich glycoproteins (HRGPs).
A bioinformatics approach to the identification, classification, and analysis of plant cell wall HRGPs.
Isolation and characterization of genes encoding tomato and Arabidopsis AGPs.
Molecular, cellular, biochemical, and physiological characterization of genetic mutants in AGP genes and AGP glycosyltransferase genes to elucidate AGP function.
Molecular interactions and function of LeAGP-1, a modular plasma membrane AGP in tomato.
GFP-AGP fusion protein expression in transgenic plants for purification/characterization of native AGPs.
Cloning and characterization of the betaine aldehyde dehydrogenase and choline monooxygenase genes from the halophyte Atriplex prostrata.
Programmed cell death in plants and the role of AGPs in this process.

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