Robert W. Roberson

Associate Professor
Robert W. Roberson
Phone: (480) 965-8618
Office: LSE 527
Education: PhD, University of Georgia
Curriculum Vitae: roberson_r.pdf
Faculty Group: Cellular & Molecular
Expertise: Microscopy

Dr. Roberson joined ASU in 1989. He is also the Director of the Life Sciences Electron Microscope Facility. He received a Ph.D. from the Department of Plant Biology at the University of Georgia.

Fungal Biology

Dr. Roberson’s fungal biology research has been focused primarily on answering questions regarding how polarized cell growth of fungal hyphae is maintained.  The result is polarized steady state growth of an apically expanding tubular-shaped cell that can, upon specific external or internal signaling, undergo morphogenesis giving rise to a plethora of functional structures such as sexual and asexual reproductive structures and symbiotic/pathogenic structures such as appressoria, haustoria, and arbuscula.  In order to better understand polarized hyphal growth and how the processes that sustain it are switched to those that result in morphological change, his group focuses attention on the organization, behavior, and function of cytoskeleton elements (microtubules, filamentous actin) and their associated proteins.  Their method of data collection is through documentation of cellular dynamics, protein localization, and cytoplasmic order using basic and advanced bioimaging methods (light microscopy - live-cell imaging, wide-field epifluorescence, laser scanning confocal, total internal reflected fluorescence (TIRF), computer enhanced imaging; transmission electron microscope - cryofixation preparation, immuno-cytochemistry approaches, serial section reconstruction analysis and electron tomography).

Research performed by Roberson’s group has led to a number of significant observations that have broadened our understanding of the biology of fungal hyphae.  One of their most surprising observations was that hyphae of the aquatic fungus Allomyces macrogynus possess an apical collection of vesicles and unique proteins that form a Spitzenkörper (= apical body, a structure unique to the fungi common in most terrestrial fungi, but never before seen in this or any other aquatic fungus).  Like terrestrial fungi, the Allomyces Spitzenkörper is involved in regulating rates and direction of cell growth, but unlike other Spitzenkörper it functions as a cytoplasmic microtubule organizing center (MTOC); a role dominated primarily by the centrosomes/spindle pole bodies in other eukaryotes and fungi.  Interestingly, the Spitzenkörper all other fungi examined to date do not function as MTOCs.  Later work on Allomyces led to additional interesting discoveries, for example, microtubule nucleating sites anchored to the nuclear envelope and the roles of microtubules and actin in maintaining cytoplasmic order, regulating intracellular motility, and establishing membrane organization and biogenesis events during the cell cycle of A. macrogynus.

Through a productive and ongoing collaboration with researchers at the Centro de Investigacion Cientifica y de Educaion Superior de Ensenada, BC (CICESE), Ensenada, Baja California, México; primarily with Drs. Rosa Mouriño-Pérez, Meritxell Riquelme, and Salomon Bartnicki-García,  great progress has been made in using molecular techniques for live-cell imaging experiments in the model organism Neurospora crassa.  One of the highlights of this work was their documentation of microtubule dynamic instability and the discovery that microtubules polymerize at faster rates in N. crassa than in any other eukaryotic organism!  Interestingly, strains deficient in microtubule molecular motor have rates of microtubule polymerization and depolymerization that were significantly reduced relative to wild type, suggesting a role for molecular motors in regulating the dynamics of microtubules.

Additional research in Roberson’s lab deals with elucidation fungal evolution.  Here, the group is using bioimaging methods to examine certain subcellular characters (e.g., Spitzenkörper organization and presence, cytoskeletal organization, MTOCs, septal characteristics, nuclear division) in hyphal tip cells of selected groups of understudied fungi that are seen as being important in elucidating evolutionary relationships. Understand cytoplasmic structure can provide powerful insights not only into the biology of cells, but the organism as a whole. Some of the larger questions that are being asked include:  What are the unique characteristics of the three-dimensional structure of the apex in fungi that have Spitzenkörper verses those that do not and are they applicable to phylogenetic analysis?  What are the precise mechanisms of Spitzenkörper function and the processes regulating its assembly and disassembly?  What is the lineage of Spitzenkörper evolution? Are there specific advantages the Spitzenkörper provides to growing septate hyphae that are absent from non-septate hyphae?  How common are Spitzenkörper in other under-studied taxa?

Cyanobacteria and Biofuels

In collaboration with Dr. Wim Vermaas (ASU), Roberson is very much involved with using the above mentioned visualization and analysis methods (with the addition of high-resolution cryo-field emission scanning electron microscopy) in studies of cytoplasmic order of the model cyanobacterium Synechocystis sp. PCC 6803.  Coupled with strong molecular and genetic approaches, Synechocystis is ideal organism for detailed structural studies to elucidate the biogenesis and organization of thylakoid membranes, cell wall architecture and compositional function, and photosystem function.  The information gained not only is valuable for understanding the fundamental cell biology of cyanobacteria, but also for advancements in biofuels technology where Synechocystis sp. PCC 6803 is playing a prominent role.

Selected Publications in Peer Reviewed Journals

Echauri Espinosa RO, Callejas-Negrete OA, Roberson RW, Bartnicki-García S, Mouriño-Pérez RR. Coronin a smooth modulator of endocytosis and tip growth in Neurospora crassa. (In preparation).

Bentivenga SP, Kumar KA, Kumar L, Roberson RW, McLaughlin DJ. Cellular organization in germ tube tips of Gigaspora. (In preparation).

Kumar A, Crow TK, Wennblom JT, Abril M, Letcher PM, Blackwell M, Roberson RW, McLaughlin DJ. 2011. An ontology of fungal subcellular traits. American Journal of Botany 98: 1504-1510.

Ho CK, Hotta T, Guo F, Roberson RW, Lee YJ, Liu B. 2011. Interaction of anti-parallel microtubules in the phragmoplast is mediated by the microtubule-associated protein MAP65-3 in Arabidopsis. Plant Cell 23: 2909-2923.

Riquelme M, Yarden O, Bartnicki-García S, Bowman B, Castro-Longoria E, Free SJ, Fleissner A, Freitag M, Lew RR, Mourino-Pérez R, Plamann M, Rasmussen C, Richthammer C, Roberson RW, Sanchez-Leon E, Seiler S, Watters MK. 2011. The architecture and development of Neurospora crassa hyphae - model cells for polarized growth.  Fungal Biology 115: 446-474.

Roberson RW, Saucedo B, MacLean D, Propster J, Unger B, Oneil TA, Parvanehgohar K, Cavanaugh C, Lowry D. 2011. The hyphal tip structure of Basidiobolus sp.: a zygomycete fungus of uncertain phylogeny.  Fungal Biology 115: 485-492

Amicucci A, Balestrini R, Kohel A, Barbieri E, Saltarelli R, Faccio A, Roberson RW, Bonfante P, Stocchi V.  2011.  Hyphal and cytoskeleton polarization in Tuber melanosporum: a genomic and cellular analysis. Fungal Genetics and Biology 48:561-572

Sánchez-León E, Verdín J, Freitag M, Roberson RW, Bartnicki-García S, Riquelme M. 2011. Traffic of chitin synthase 1 (CHS-1) to the Spitzenkörper and developing septa in hyphae of Neurospora crassa: actin dependence and evidence of distinct microvesicle populations. Eukaryotic Cell 10: 683-695

Uchida M, Mouriño-Pérez RR, Roberson RW.  2010. Total internal reflection fluorescence microscopy of fungi. Fungal Biology Reviews 24:132-136

Flynn CR, Cheung-Flynn J, Smoke CC, Lowry D, Roberson RW, Sheller MR, Brophy C.  2010. Internalization and intracellular trafficking of a PTD-conjugated anti-fibrotic peptide, AZX100, in human dermal keloid fibroblasts.  Journal of Pharmaceutical Sciences 99: 3100-3121

Delgado-Álvarez DL, Callejas-Negrete OA, Gómez , Freitag M, Roberson RW, Smith LG, Mouriño-Pérez RR. 2010. Visualization of F-actin localization and dynamics with live cell markers in Neurospora crassa. Fungal Genetics and Biology 47: 573-586

Hohmann-Marriott, M.F., Roberson, R.W. 2009. Exploring photosynthesis by electron tomography. Photosynthesis Research. 102:177–188.

Ramos-García, S.L., Roberson, R.W., Freitag, M., Bartnicki-García, S., Mouriño-Pérez, R.R. 2009. Role of cytoplasmic bulk flow and microtubule-related motor proteins in nuclear displacement in growing hyphae of Neurospora crassa. Eucaryotic Cell. 8:1880-1890).

Bates, S.T., Roberson, R.W. and Desjardin, D.E. 2008. Arizona gasteroid fungi I: Lycoperdaceae (Agaricales, Basidiomycota). Fungal Diversity. 37:153-207.

Köhli, M., Galati, V., Boudier, V., Roberson, R.W., Philippsen, P. 2008. Growth-speed correlated localization of exocyst and polarisome components in growth zones of Ashbya gossypii hyphal tips. Journal of Cell Science. 121:3803-3814.

Maho Uchida, R. R. Mouriño-Pérez, Michael Freitag, Salomon Bartnicki-García, Roberson, R.W. 2008. Microtubule dynamics and the role of molecular motors in Neurospora crassa. Fungal Genetics and Biology. 45:683-692

Hohmann-Marriott, M.F., Uchida, M., van de Meene, A.M.L., Garret, M., Hjelm, B.E., Kokoori, S., Roberson, R.W. 2006. Electron tomography and its application to revealing fungal ultrastructure: Tansley Review. New Phytologist. 172:208-220.

Mouriño-Pérez, R.R., Roberson, R.W ., Bartnicki-García, S. 2006. Microtubule dynamics and organization during hyphal branching in Neurospora crassa . Fungal Genetics and Biology 43:389-400.

van de Meen A., Hohmann-Marriott M.F., Vermaas W.F.J., Roberson R.W. 2006. The three-dimensional structure of the cyanobacterium Synechocystis sp. PCC 6803. Archives of Microbiology 184:259-270.

Hohmann-Marriott, M.F., Sharp, W.P., Blankenship, R.E., Roberson, R.W. 2005. Digital position determination system for electron microscopy. Microscopy Techniques and Methods. 67:106-111.

Mohamed, H.E., Van de Meene, A.M.L., Roberson, R.W., Vermaas, W. 2005. Myxoxanthophyll is required for normal cell wall structure and thylakoid organization in the cyanobacterium Synechocystis sp. strain PCC 6803. Journal of Bacteriology 187:6883-6892.

Hohmann-Marriott, M.F. Blankenship, R.E., Roberson, R.W . 2005. The ultrastructural of Chlorobium tepitum chlorosomes revealed by electron microscopy. Photosynthesis Research 86:145-154.

Uchida, M. , Roberson, R.W. , Chun, S., Kim, D. 2005. In vivo effects of the fungicide ethaboxam on microtubule integrity in Phytophthora infestans . Pest Manag Sci. 61:787-792.

Harris , S.D. , Read, N.D., Roberson, R.W ., Shaw, B., Seiler, S., Plamann, M., Momany, M. 2004. Spitzenkörper meets polarisome: microscopy, genetics, and genomics converge. Eukaryotic Cell 4:225-229.

Lowry, D.L., Fisher, K.F., Roberson, R.W. 2004. Functional necessity of the cytoskeleton during cleavage membrane development and zoosporogenesis in Allomyces macrogynus . Mycologia 96:211-218.

Riquelme M., McDaniel, D.P., Bartnicki-García S., Roberson R.W. 2002. The effect of ropy-1 mutation on cytoplasmic organization in mature hyphae of Neurospora crassa . Fungal Genetics and Biology 37:171-179.

Woyke T., Winkelmann G., Roberson R.W. Pettit, G.R., Pettit R.K. 2002. Three-dimensional visualization of microtubules during the Cryptococcus neoformans cell cycle and effects of auristatin PHE. Antimicrobial Agents and Chemotherapy 46:3802-3808.

Pettit R.K., Hamel E., Verdier-Pinard P., Roberson R.W . , Hazen K.C., Pettit G.R., Crews L.C. 2002. Antifungal and cancer cell growth inhibitory activities of 1-(3, 4, 5 -trimethoxyphenyl)-2-nitroethylene. Mycosis 45:65-74.

McDaniel, D.P., Roberson, R.W . 2000. Intracellular motility and mechanisms of control during hyphal tip growth in Allomyces . Fungal Genetics and Biology 31:223-234.

Fisher, K.E., Lowry, D.S. Roberson, R.W . 2000. Cytoplasmic cleavage in zoosporangia of Allomyces macrogynus . Journal of Microscopy 198:260-270.

Lowry, D.S., Fisher, K.E., Roberson, R.W. 1998. Establishment and maintenance of nuclear position during zoospore formation in Allomyces macrogynus : roles of the cytoskeleton. Fungal Genetics and Biology 24:34-44.

McDaniel D.P, Roberson, R.W. 1998. γ-Tubulin is a component of the Spitzenkörper and centrosomes in hyphal tip cells of Allomyces macrogynus . Protoplasma 203:118-123.

Roberson, R.W. , Tucker, B., Pettit, G.R. 1998. Microtubule depolymerization in Uromyces appendiculatus by three new antineoplastic drugs: combretastatin A-4, dolastatin 10 and halichondrin B. Mycological Research 102:378-382 .

McNally, H.A., Kozicki, M.N., Roberson, R.W. , Whidden, T.K. 1997. Electrical Characterization of Uromyces germ tubes grown on integrated circuit substrates. Journal of Vacuum Science andTechnology. 15:779-783.

Roberson, R.W. 1992. The actin cytoskeleton in hyphal cells of Sclerotium rolfsii . Mycologia 84 41-51.

Roberson, R.W. , Luttrell E.S., Fuller M.S. 1990. Mycoparasitisum of teliospores of the smut fungus Ustilago bullata by an oomycete. Canadian Journal of Botany . 68:2415-2421.

Fuller, M.S., Roberson, R.W. , Gisi, U. 1990. Effects of the sterol biosynthesis inhibitor cyproconazole on hyphal tip cells of Sclerotium rolfsii . III A cytochemical study. Pesticide Biochemistry and Physiology 36:115-126.

Roberson, R.W. , Fuller, M.S. 1990. Effects of the sterol biosynthesis inhibitor cyproconazole on hyphal tip cells of Sclerotium rolfsii. II An electron microscopic study. Experimental Mycology 14:124-135

Mims, C.W., Roberson, R.W. , Richardson , E.A. 1988. Ultrastructure of freeze-substituted and chemically fixed basidiospores of Gymnosporangium juniperi - virginianae . Mycologia 80:356-364.

Publications In Edited Books

McLaughlin DJ, Kumar TKA, Blackwell M, Letcher P, Roberson R.W. 2011. Subcellular Structure and Biochemical Characters in Fungal Phylogeny. In: McLaughlin DJ, McLaughlin EG, Lemke PA (eds). The Mycota VII Systematics and Evolution Part B. Springer-Verlag, New York. (In preparation)

Uchida M, Mouriño-Pérez RR, Roberson RW. 2010. Live-cell imaging of microtubule dynamics in leading hyphae of Neurospora crassa. In: Sharon A. (ed), Molecular and Cell Biology Methods for Fungi. The Humana Press Inc. Totowa, New Jersey, USA, 638:259-268

Roberson R.W., Abril M, Blackwell M., Letcher P, McLaughlin DJ, Mouriño-Pérez RR, Riquelme M, Uchida M. 2010. Hyphal Structure, Chapter 2. In: Cellular and Molecular Biology of Filamentous Fungi.. Borkovich K, Ebbole D (eds). ASM Press, Washington, D.C. (pp. 8 - 27)

Hohmann-Marriott, M., van de Meene, A. Roberson, R.W . 2006. Electron tomography: Advances in Photosynthesis. Biophysical techniques in photosynthesis (Volume II), Series Editor Govindjee, J. Matysik and T. J. Aartsma (in press), Kluwer Academic Publishers.

Roberson, R.W. , Chandler , D.E. 1998. Rapid freezing and deep etching of cells and molecules. In : Cell Biology: A Laboratory Handbook. Eds . D. Spector, R. Goldman, and L. Leinwand. Cold Spring Harbor Laboratory Press, Cold Spring Harbor , New York . (pp.129.1-129.23).

Roberson, R.W. 1991. The hyphal tip cell of Sclerotium rolfsii : cytological observations. In : Fungal Cell Wall and Immune Response. Pp. 27-37. Eds. J.P. Latge and D. Boucias. NATO Scientific Series, Springer-Verlag , Berlin , Heidelberg .

Howard, W., Roberson, R.W. 1987. Pythium : sexual reproduction. Pp 92-93. In : Zoosporic Fungi in Teaching and Research. Eds . M.S. Fuller and A. Jaworski. Southeastern Publishing Corp.

Roberson, R.W. , Howard, W. 1987. Pythium : asexual reproduction. Pp 90-91. In : Zoosporic Fungi in Teaching and Research. Eds . M.S. Fuller and A. Jaworski. Southeastern Publishing Corp.

Books Published

Chandler DE, Roberson RW. 2009. Bioimaging: Current Concepts in Light and Electron Microscopy. Jones and Bartlett, Boston, MA.

Additional links