Professor Maria Hrmova

Professor Maria Hrmova
 Position Professor
 Org Unit School of Agriculture, Food and Wine
 Email maria.hrmova@adelaide.edu.au
 Telephone +61 8 8313 7160
 Location Floor/Room 2 36 ,  Plant Genomics Centre ,   Waite
  • Qualifications

    ·     Bachelor of Science (BSc) in Biochemistry, Comenius University, Czecho-Slovakia

    ·     Master of Science (MSc) in Biochemistry, Comenius University, Czecho-Slovakia

    ·     Doctor of Philosophy (PhD) in Biochemistry, Comenius University and Slovak University of Technology, Czecho-Slovakia

    ·     Doctor Scientiarum (DrSci) in Chemistry, Comenius University, Slovak Republic

  • Awards & Achievements

    ELECTED MEMBER OF THE LEARNED SOCIETY OF SLOVAK ACADEMY OF SCIENCES

    I was elected a member of the Society, which supports the development of science, spreads scientific knowledge, debates the ethical questions of research, declares clear positions on the problems and norms of science and technology, influences the direction of research in Slovak Republic, and honourably represents the Slovak Academy of Sciences. The Learned Society established in 1949 has 112 members and is an equivalent to the Australian Academy of Science.

  • Research Interests

    My expertise is in the multidisciplinary field of structural biochemistry and biophysics. My tasks are to investigate molecular mechanisms that underpin the function of plant proteins in three major areas: 

    (i)           PLANT TRANSPORT PROTEINS UNDERLYING ELEMENTAL SOIL TOXICITY TOLERANCE

    My laboratory is focused on the structural and functional properties of plant borate and HKT (High-affinity Potassium Transporter) Na+/K+ transporters, and on orthodox and multifunctional aquaporins. By combining in silico and in vitro methods, we discovered that borate transporters mediate Na+-dependent anion transport and exhibit channel-like characteristics. This work was published in Plant Cell, one of the highest-ranking journals in the plant science field. 

    With HKT transporters, we designed a model for Na+-exclusion in rice and explained that variations in salt tolerance can be explained by transcription, alternative splicing and a protein structure. We also clarified a long-standing question, how the structural variations in wheat HKT proteins underpin differences in Na+ transport capacity; this work was highlighted on the front cover of Cellular and Molecular Life Sciences.

    (ii)          TRANSCRIPTION FACTORS INVOLVED IN THE REGULATION OF PLANT RESPONSES TO DROUGHT

    We perform extensive 3D molecular modelling studies of transcription factors in complex with DNA cis-elements, such as bZIP, HDZip, DREB, ERF, NFY-YB, CBF and MYB, and validate these DNA-binding properties in vitro. We engineered wheat transcription factor variants and in the breakthrough science, using genetically engineered plants, we showed that these modifications changed DNA recognition and plant responses to drought and frost. Our work has been highlighted on the front covers of Plant Biotechnology Journal, Plant Molecular Biology and Journal of Experimental Botany.

    (iii)         CATALYTIC MECHANISMS OF ENZYMES INVOLVED IN PLANT DEVELOPMENT

    We focus on exohydrolytic enzymes to define their catalytic mechanisms at the atomic levels. We solved the crystal structure of a plant exohydrolase with a non-covalently trapped glucose product, but the glucose displacement mechanism, and how it is linked to the catalytic cycle remained unanswered. Using high-resolution X-ray crystallography, enzyme kinetics, mass spectrometry, NMR spectroscopy and multi-scale 3D molecular modelling, we revealed the new catalytic mechanism that we coined ‘”substrate-product assisted processive catalysis”. Here, upon productive substrate binding near the active site, entrapped glucose modifies its binding patterns and evokes the formation of a temporary lateral cavity, which serves as a conduit for glucose departure to allow for the next catalytic cycle. This path enables efficient catalysis via multiple hydrolytic events without the enzyme losing contact with oligo- or polysaccharides. This discovery has significance in biotechnology to engineer enzymes that could be used efficiently outside of biological systems. This work was published in Nature Communications. 

    Press Release to this article can be seen here.

    A movie illustrating the discovered catalytic mechanism can be seen here.

  • Research Funding

    Research in my group has been funded by the Australian Research Council, by the Grains Research & Development Corporation, the South Australian Government, the Waite Research Institute of the University of Adelaide, DuPont Pioneer and by the Australian Synchrotron Research Program. The latter is supported by the Commonwealth of Australia under the Major National Research Facilities Program. 

     

    Expertise for Media Contact

    
    

    Categories

    Science & Technology, Biotechnology

    Expertise

    Biochemistry and biophysics; biotechnology and applications; carbohydrate and protein chemistry; enzyme mechanisms; genomics and genetic engineering; transport proteins; transcription factors; protein structure; 3D protein modelling; molecular mechanisms of plant abiotic stress tolerance.

  • Publications

    We have published over 140 peer-reviewed articles and lodged patents on mechanisms explaining plant abiotic stress tolerance and enzyme catalysis. Our papers have appeared in the top-tier journals Nature Communications, Science, American Chemical Society, Biotechnology Advances, Plant Cell and Current Opinion in Plant Biology. Our papers received ~5,500 citations and 18 papers were featured on front covers. Our key articles are:

    RECENTLY RELEASED ARTICLES:

    Streltsov VA, Luang S, Peisley A, Varghese JN, Ketudat Cairns JR, Fort S, Hijnen M, Tvaroška I, Ardá A, Jiménez-Barbero J, Alfonso-Prieto M, Rovira C, Mendoza F, Tiessler-Sala L, Sánchez-Aparicio S-E, Rodríguez-Guerra J, Lluch JM, Maréchal J-D, Masgrau L, Hrmova M* (2019) Discovery of processive catalysis by an exo-hydrolase with a pocket-shaped active site. Nature Communications 10 (1), 2222; DOI: https: //doi.org/10.1038/s41467-019-09691-z. *Corresponding author.  

    Yang Y, Al-Baidhani HHHJ, Harris J, Riboni M, Li Y, Mazonka I, Bazanova N, Chirkova L, Hussain SS, Hrmova M*, Haefele S, Lopato S, Kovalchuk N (2019) DREB/CBF expression in wheat and barley using the stress-inducible promoters of HD-Zip I genes: impact on plant development, stress tolerance and yield. Plant Biotechnology Journal; doi: 10.1111/pbi.1325.*Corresponding author.

    Kovalchuk N, Wu W, Bazanova N, Reid N, Singh R, Shirley N, Eini O, Johnson A, Langridge P, Hrmova M*, Lopato S (2019) Wheat wounding-responsive HD-Zip IV transcription factor GL7 is predominantly expressed in grain and activates expression of defensins. Plant Molecular Biology 101, 41-61. Correction to Figure 8: Plant Molecular Biology 101, 63-64. *Corresponding author.

    Stratilová B, Firáková Z, Klaudiny J, Šesták S, Kozmon S, Strouhalová D, Garajová S, Ait-Mohand F, Horváthová A, Farkaš V, Stratilová E, Hrmova M* (2019) Engineering the acceptor substrate specificity in the xyloglucan endotransglycosylase TmXET6.3 from nasturtium seed (Tropaeolum majus L.). Plant Molecular Biology 100, 181-197. *Corresponding author.

    Hrmova M*, Gilliham M (2018) Plants fighting back: to transport or not to transport, this is a structural question. Current Opinion in Plant Biology 46, 68-76. *Corresponding author.

    OTHER KEY ARTICLES:

    Xu B, Waters S, Byrt CS, Plett D, Tyerman SD, Tester M, Munns R, Hrmova M*, Gilliham M* (2018) Structural variations in wheat HKT1;5 underpin differences in Na+ transport capacity. Cellular and Molecular Life Sciences 75, 1133-1144. Featured on the front cover. *Co-corresponding authors.

    Bi H, Shi J, Kovalchuk N, Luang S, Bazanova N, Chirkova L, Zhang D, Shavrukov Y, Stepanenko A, Tricker P, Langridge P, Hrmova M*, Lopato S, Borisjuk N* (2018) Overexpression of the TaSHN1 transcription factor in bread wheat leads to leaf surface modifications, improved drought tolerance and no yield penalty under controlled growth conditions. Plant Cell & Environment 41, 2549-2566*Co-corresponding authors.

    Luang S, Hrmova M* (2017) Structural basis of the permeation function of plant aquaporins. In: Plant Aquaporins, Series Signaling and Communication in Plants, Subtitle: From Transport to Signaling (Chaumont F, Tyerman SD, eds), pp 1-28. Springer Verlag, Berlin, Heidelberg, London, ISBN 978-3-319-49393-0. Invited review. *Corresponding author.

    Nagarajan Y, Rongala J, Luang S, Singh A, Shadiac N, Hayes J, Sutton T, Gilliham M, Tyerman SD, McPhee G, Voelcker NH, Mertens HDT, Kirby NM, Lee J-G, Yingling YG, Hrmova M* (2016) A barley efflux transporter operates in a Na+-dependent manner, as revealed through a multidisciplinary platform. Plant Cell 28, 202-218. *Corresponding author.

    Li B, Evrard A, Qiu J, Johnson AAT, Baumann U, Birnbaum KD, Hrmova M, Mayo GM, Jha D, Henderson S, Tester M, Gilliham M*, Roy SJ* (2016) Identification of a stelar-localised transport protein that facilitates root-to-shoot transfer of chloride in Arabidopsis. Plant Physiology 170, 1014-1029. *Co-corresponding authors.

    Waters S, Gilliham M, Hrmova M* (2013) Plant high affinity potassium (HKT) transporters involved in salinity tolerance: structural insights to probe differences in ion selectivity. International Journal of Molecular Sciences 14, 7660-7680. *Corresponding author.

    Cotsaftis O, Plett D, Shirley N, Tester M, Hrmova M* (2012) A two-staged model of Na+ exclusion in rice explained by 3D modeling of HKT transporters and alternative splicing. PLoS ONE 7, e39865. *Corresponding author.

    Schnurbusch T, Hayes J, Hrmova M, Baumann U, Ramesh SA, Tyerman SD, Langridge P, Sutton T* (2010) Boron toxicity tolerance in barley through reduced expression of the multifunctional aquaporin, HvNIP2;1. Plant Physiology 153, 1706-1715. *Corresponding author.

    (ii)          TRANSCRIPTION FACTORS INVOLVED IN THE REGULATION OF PLANT RESPONSES TO DROUGHT

    Yang Y, Luang S, Harris J, Riboni M, Li Y, Bazanova N, Hrmova M*, Haefele S, Kovalchuk N, Lopato S (2018) Overexpression of the class I homeodomain transcription factor TaHDZipI-5 increases drought and frost tolerance in transgenic wheat. Plant Biotechnology Journal 16, 1227-1240. *Corresponding author.

    Luang S, Sornaraj P, Bazanova N, Jia W, Eini O, Hussain SS, Kovalchuk N, Agarwal P, Hrmova M*, Lopato S (2018) TabZIP2 from wheat is a part of the signalling pathway that mobilises plants to respond to nutrient starvation under drought. Plant Molecular Biology 96, 543-561. *Corresponding author.

    Bi H, Luang S, Li Y, Bazanova N, Borisjuk N, Hrmova M*, Lopato S (2017) Wheat drought-responsive WXPL transcription factors regulate cuticle biosynthesis genes. Plant Molecular Biology 94,15-32. Featured on the front cover. *Corresponding author.

    Bi H, Luang S, Li Y, Bazanova N, Morran S, Song Z, Perera MA, Hrmova M*, Borisjuk N, Lopato S (2016) Identification and characterisation of wheat drought responsive MYB transcription factors involved in the regulation of cuticle biosynthesis. Journal of Experimental Botany 67, 5363-5380. Featured on the front cover. *Corresponding author.

    Kovalchuk N, Chew W, Sornaraj P, Borisjuk N, Yang N, Singh R, Bazanova N, Shavrukov Y, Guendel A, Munz E, Borisjuk L, Langridge P, Hrmova M*, Lopato S (2016) The homeodomain transcription factor TaHDZipI-2 from wheat regulates frost tolerance, flowering time and spike development in transgenic barley. New Phytologist 211, 671-687. *Corresponding author.

    Harris JC, Sornaraj P, Taylor M, Bazanova N, Baumann U, Lovell B, Langridge P, Lopato S, Hrmova M* (2016) Molecular interaction of the γ-Clade Homeodomain-Leucine Zipper class I transcription factors during the wheat response to water deficit. Plant Molecular Biology 90, 435-452. Featured on the front cover. *Corresponding author.

    Sornaraj P, Luang S, Lopato S, Hrmova M* (2016) Basic leucine zipper (bZIP) transcription factors involved in abiotic stresses: A molecular model of a wheat bZIP factor and implications of its structure and function. Biochimica et Biophysica Acta - General Subjects 1850, 46-56. *Corresponding author.

    Amalraj A, Luang S, Kumar M, Sornaraj P, Eini O, Kovalchuk N, Bazanova N, Li Y, Yang N, Eliby S, Langridge P, Hrmova M*, Lopato S (2016) Change of function of the wheat stress-responsive transcriptional repressor TaRAP2.1L by repressor motif modification. Plant Biotechnology Journal 14, 820-832. *Corresponding author.

    Yadav D, Shavrukov Y*, Bazanova N, Chirkova L, Borisjuk N, Kovalchuk N, Ismagul A, Parent B, Hrmova M, Langridge P, Lopato S (2015) Constitutive over-expression of the TaNF-YB4 gene in transgenic wheat significantly improves grain yield. Journal of Experimental Botany 66, 6635-6650. *Corresponding author.

    Li M*, Lopato S, Hrmova M, Pickering M, Shirley N, Koltunow AM, Langridge P (2014) Expression patterns and protein structure of a lipid transfer protein END1 from Arabidopsis. Planta 240, 1319-1334. *Corresponding author.

    Lopato S*, Borisjuk N, Langridge P, Hrmova M (2014) Endosperm transfer cell-specific genes and proteins: structure, function and applications in biotechnology. Frontiers in Plant Science 5, article 64, 1-14. *Corresponding author.

    Borisjuk N*, Hrmova M*, Lopato S* (2014) Transcriptional regulation of cuticle biosynthesis. Biotechnology Advances 32, 526-540. *Co-corresponding authors.

    Hrmova M*, Lopato S (2014) Enhancing abiotic stress tolerance in plants by modulating properties of stress responsive transcription factors. In: Genomics of Plant Genetic Resources (Tuberosa R, Graner A, Frison E, eds), Volume 2, Part II: Crop productivity, food security and nutritional quality, pp 291-316. Springer Verlag, Netherlands, ISBN 978-94-007-7574-9. Invited review. *Corresponding author.

    (iii)         CATALYTIC MECHANISMS OF ENZYMES INVOLVED IN PLANT DEVELOPMENT

    Tankrathok A, Iglesias-Fernández J, Williams RJ, Pengthaisong S, Baiya S, Hakki Z, Robinson RC, Hrmova M, Rovira C, Williams SJ, Ketudat Cairns JR (2015) A single glycosidase harnesses different transition state conformations for hydrolysis of mannosides and glucosides. American Chemical Society: Catalysis, 5, 6041-6051.

    Kaewthai N, Harvey AJ, Hrmova M, Brumer H, Ezcurra I, Teeri TT, Fincher GB (2010) Recombinant expression of a diversity of barley XTH genes in the yeast Pichia pastoris. Plant Biotechnology 27, 251-258.

    Vaaje-Kolstad G, Farkaš V, Hrmova M, Fincher GB (2010) Xyloglucan xyloglucosyl transferases from barley (Hordeum vulgare L.) bind oligomeric and polymeric xyloglucan molecules in their acceptor binding sites. Biochimica et Biophysica Acta - General Subjects 1800, 674-684.

    Vaaje-Kolstad G, Farkas V, Fincher GB, Hrmova M (2010) Barley xyloglucan xyloglucosyl transferases bind xyloglucan-derived oligosaccharides in their acceptor binding regions in multiple conformational states. Archives of Biochemistry and Biophysics 496, 61-68

    Luang S, Hrmova M, Ketudat Cairns JR (2010) High-level expression of barley β-d-glucan exohydrolase HvExoI from a codon-optimized cDNA in Pichia pastoris. Protein Expression and Purification 73, 9098.

    Luang S, Ketudat Cairns JR, Streltsov VA, Hrmova M (2010) Crystallisation of wild-type and variant forms of a recombinant β-d-glucan glucohydrolase from barley (Hordeum vulgare L.) by macroseeding with wild-type native microcrystals and preliminary X-ray analysis. International Journal of Molecular Sciences 11, 27592769.

    Hrmova M, Farkas V, Harvey AJ, Lahnstein J, Wischmann B, Kaewthai N, Ezcurra I, Teeri TT, Fincher GB (2009) Substrate specificity and catalytic mechanism of a xyloglucan xyloglucosyl transferase HvXET6 from barley (Hordeum vulgare L.). FEBS Journal 276, 437-456.

    Kuntothom T, Raab M, Tvaroška I, Fort S, Pengthaisong S, Cañada FJ, Calle L, Jiménez-Barbero J, Ketudat Cairns JR, Hrmova M (2010) Binding of β-d-glucosides and β-d-mannosides by rice and barley β-d-glycosidases with distinct substrate specificities. Biochemistry (USA) 49, 8779-8793.

    Hrmova M, Fincher GB (2009) Plant and microbial enzymes involved in the depolymerisation of (1,3)-β-d-glucans and related polysaccharides. In: Chemistry, Biochemistry and Biology of (1,3)-β-d-Glucans and Related Polysaccharides, Academic Press, Elsevier Inc, San Diego, USA, 677 pp, 16 color plates (Bacic T, Fincher GB, Stone BA, eds), pp 119-170. Invited review. Featured on the front cover.

    Hrmova M, Farkas V, Lahnstein J, Fincher GB (2007) A barley xyloglucan xyloglucosyl transferase covalently links xyloglucan, cellulosic substrates and (1,3;1,4)-β-d-glucans. Journal of Biological Chemistry 282, 12951-12962.

    Burton RA, Wilson SM, Hrmova M, Harvey AJ, Shirley NJ, Stone BA, Newbigin EJ, Medhurst A, Bacic A, Fincher GB (2006) Cellulose synthase-like CslF genes mediate the synthesis of cell wall (1,3;1,4)-β-d-glucans. Science 311, 1940-1942.

    Hrmova M, Streltsov VA, Smith BJ, Vasella A, Varghese JN, Fincher, GB (2005) Structural rationale for low nanomolar binding of transition state mimics to a family GH3 β-d-glucan glucohydrolase from barley. Biochemistry (USA) 44, 16529-16539.

    Hrmova M, De Gori R, Smith BJ, Vasella A, Varghese JN, Fincher GB (2004) Three-dimensional structure of the barley β-d-glucan glucohydrolase in complex with a transition-state mimic. Journal of Biological Chemistry 279, 4970-4980.

    Lee RC, Hrmova M, Burton RA, Lahnstein J, Fincher GB (2003) An α-l-arabinofuranosidase and a β-d-xylosidase from barley: purification, characterization and primary structures. Journal of Biological Chemistry 278, 5377-5387.

    Hrmova M, Imai T, Rutten SJ, Fairweather JK, Pelosi L, Bulone V, Driguez H, Fincher GB (2002) Barley (1,3)-β-d-glucan endohydrolase mutants synthesise crystalline (1,3)-β-d-glucans. Journal of Biological Chemistry 277, 30102-30111.

    Hrmova M, De Gori R, Smith BJ, Fairweather JK, Driguez H, Varghese JN, Fincher GB (2002) Structural basis for broad substrate specificity in higher plant β-d-glucan glucohydrolases. Plant Cell 14, 1033-1052. Featured on the front cover.

    Hrmova M, Varghese JN, DeGori R, Smith BJ, Driguez H, Fincher GB (2001) Catalytic mechanisms and reaction intermediates along the hydrolytic pathway of plant β-d-glucan glucohydrolase. Structure 9, 1005-1016.

    Varghese JN, Hrmova M, Fincher GB (1999) Three-dimensional structure of a barley β-d-glucan exohydrolase, a family 3 glycosyl hydrolase. Structure 7, 179-190.

    Hrmova M, MacGregor EA, Biely P, Stewart RS, Fincher GB (1998) Substrate binding and catalytic mechanism of a barley β-d-glucosidase/(1,4)-β-d-glucan exohydrolase. Journal of Biological Chemistry 273, 11134-11143.

    Hrmova M, Harvey AJ, Wang J, Shirley NJ, Jones GP, Høj PB, Fincher GB (1996) Barley β-d-glucan exohydrolases with β-d-glucosidase activity. Purification and determination of primary structure from a cDNA clone. Journal of Biological Chemistry 271, 5277-5286.

    Hrmova M, Garrett TPJ, Fincher GB (1995) Subsite affinities and disposition of catalytic amino acids in the substrate-binding region of barley 1,3-β-d-glucanases. Journal of Biological Chemistry 270, 14556-14563.

    (iv)         PROTEIN TECHNOLOGIES AND COMMENTARIES

    Zieleniecki J, Nagarajan Y, Waters S, Rongala J, Thompson V, Hrmova M*, Köper I* (2016) Cell-free synthesis of a functional membrane transporter into a tethered bilayer lipid membrane. American Chemical Society: Langmuir 32, 2445-2449. *Co-corresponding authors.

    Shadiac N, Nagarajan Y, Waters S, Hrmova M* (2013) The close allies in membrane protein research: cell-free synthesis and nanotechnology. Molecular Membrane Biology 30, 229-245. *Corresponding author.

    Periasamy A, Shadiac N, Amalraj A, Garajová S, Nagarajan Y, Waters S, Mertens HD, Hrmova M* (2013) Cell-free protein synthesis of membrane (1,3)-β-d-glucan (curdlan) synthase: co-translational insertion in liposomes and reconstitution in nanodiscs. Biochimica et Biophysica Acta - Biomembranes 1828, 743-757. *Corresponding author.

    Kosik O, Auburn RP, Stratilova E, Garajova S, Hrmova M, Farkas V (2010) Polysaccharide micro-arrays for screening of transglycosylase activities in plant extracts. Glycoconjugate Journal 27, 79-87.

    Kaiser BN, Hrmova M (2010) A glimpse at regulation of nitrogen homeostasis. Structure 18, 1395-1397. Invited commentary.

    Montel E, Hrmova M, Fincher GB, Driguez H, Cottaz S (2009) A chemoenzymatic route to conjugatable β-(1,3)-glucan oligosaccharides. Australian Journal of Chemistry 62, 575-584.

    Farrokhi N, Hrmova M, Burton RA, Fincher GB (2009) Heterologous and cell free expression systems. In: Plant Genomics, Humana Press Inc, Totowa, USA (Somers D, Langridge P, Gustafson P, eds). Methods in Molecular Biology 513, 175-198. Invited review.

    Hrmova M, Fincher GB (2009) Functional genomics and structural biology in the definition of gene function. In: Plant Genomics, Humana Press Inc, Totowa, USA (Somers D, Langridge P, Gustafson P, eds). Methods in Molecular Biology 513, 199-227. Invited review.

    Hrmova M, Stone BA, Fincher GB (2010) High-yield production, refolding and molecular modelling of the catalytic module of (1,3)-β-d-glucan (curdlan) synthase from Agrobacterium sp. Glycoconjugate Journal 27, 461-476.

    Hrmova M, Fincher GB (2001) Structure-function relationships of β-d-glucan endo- and exohydrolases from higher plants. Plant Molecular Biology 47, 73-91. Invited review.

     

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Entry last updated: Friday, 13 Sep 2019

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