PLANT HORMONAL REGULATORY NETWORKS

Group leader: Stephan Pollmann - Assistant Professor

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Plants have to cope with ever-changing and sometimes adverse environmental conditions. In order to deal with these circumstances, they have developed a wealth of developmental solutions to shape their body plan and optimize their metabolism in response to given environmental demands. In the first place, such responses rely upon and, likewise, witness the remarkable developmental flexibility of plants, including permanent meristematic activity, de novo organogenesis, and the enormous capacity for regeneration. However, coordinated plant growth and development as well as appropriate plant stress responses require an efficient communication not only of single cells, but rather of whole tissues. As with animals, plants use a limited number of hormonal compounds to accomplish this task. To date, we know that the plant life cycle, from germination till reproduction, is controled by a highly complex network of low abundant signaling molecules, referred to as phytohormones. The existence of such compounds has already been proposed more than 120 years ago, by the famous plant physiologists Charles Darwin (1880) and Julius von Sachs (1887). Already back then, they have been convinced that coordinated morphogenesis and functionality of multi-cellular organisms has to rely on transmissible signals that are transported within the plant cormus.

Indole-3-acetic acid (IAA) is the major naturally occurring auxin and one of the major growth factors in plants. It is recognized to be involved in virtually all aspects of plant growth and differentiation, e.g. the promotion of shoot elongation, the induction of cambial cell division, the maintenance of apical dominance, and the induction of lateral and adventitious root formation. In the past decades, evidence has accumulated both emphasizing the physiological importance of auxins in the context of coordinating plant development and describing the molecular mode of auxin action. However, although IAA constitutes a rather simple molecule, sharing major structural features with the proteinogenic amino acid L-tryptophan, the biosynthesis of IAA remains elusive.

One major research line of our group concerns auxin biosynthesis and its regulation in the model plant Arabidopsis thaliana. Over the past, experimental proof has been provided that auxin biosynthesis in this species is realized by a small number of alternative pathways, each of them designated for an intermediate that is a hallmark of the pathway (Fig. 1).

Figure 1. Presumptive pathways of IAA biogenesis in plants. The IAOx pathway that is seemingly restricted to IG-producing plant species is given in the grey box. In the middle, the TAM pathway is shown (dark blue), followed by the IPyA (orange) and the IAM pathway (green), respectively, further left. A tryptophan-independent pathway (light blue) of IAA formation is added on the left boarder of the scheme. Dashed lines indicate assumed reaction steps for which the corresponding enzymes have yet to be identified. Enzymes are abbreviated as follows: AAO, arabidopsis aldehyde oxidase 1; AMI1, amidase 1; CYP71A13, cytochrome P450 monooxygenase 71A13; CYP79B2/B3, cytochrome P450 monooxygenase 79B2/B3; NIT, nitrilase; TAA1, tryptophan aminotransferase of Arabidopsis 1; TAR, tryptophan amonotransferase related; TDC, tryptophan decarboxylase; YUC, YUCCA. (Lehmann et al., 2010)

 

Thus far, one Trp-independent and four Trp-dependent pathways for auxin biosynthesis have been proposed. These are the indole-3-acetaldoxime (IAOx)-pathway, the tryptamine (TAM)-pathway, the indole-3-pyruvic acid (IPA)-pathway, and the indole-3-acetamide (IAM)-pathway. As yet, none of the proposed pathways is fully disclosed with respect to the catalyzed reaction steps and the enzymes involved. Due to the obious gaps in the pathways, the functional redundancy, and the tissue and plant specific variations in expression patterns of the identified components, the relevance of each of these pathways is difficult to assess.

Our previous work provided evidence that led us to suggest that one route of auxin formation takes it course via the intermediate IAM, a compound proven to be endogenous to Arabidopsis and several other plant species. In the following, we succeeded in identifying and characterizing the first plant IAM hydrolase (AMI1) from Arabidopsis, capable of catalyzing the conversion of IAM to IAA (for review see: Pollmann et al., 2006, Lehmann et al., 2010).

AMI1 is located in the cytoplasm (Fig. 2), assumed to be the main locus of IAA biosynthesis. Judged by its primary amino acid composition and homology to other well-characterized enzymes (Fig. 3), AMI1 is considered as a member of the amidase signature family that comprises enzymes that can be found widespread in nature, catalyzing a diverse range of different reactions. To date, more than twenty AMI1-like proteins from both monocot and dicot plant species have been identified (Mano et al., 2010; Lehmann et al., 2010), suggesting a conserved and likely important function of AMI1-like enzymes. Currently, our focus is on the elucidation of the role of AMI1-mediated IAA formation and on how AMI1 integrates into the already deciphered framework of auxin biosynthesis in plants. Furthermore, we are interested in the regulation of auxin biosynthesis. To tackle these objectives, we use a combination of genetic, molecular biological, protein biochemical, cell biological, and mass spectromerical techniques.

Figure 2. The picture shows a confocal laser scanning microscopical image of an Arabidopsis pavement cell, co-transformed with an AMI1:GUS:GFP-construct and a nuclear control, CRY2:DsRed. AMI1 is obviously localized in the cytoplasm. (Pollmann et al., 2006)

Figure 3. Structural modeling of amidase 1 from Arabidopsis thaliana. The side chains of the putative catalytic residues are shown. The Lys36, Ser113, Ser137 triad is highlighted in blue. (Neu et al., 2007)

 

In a second research line that has been started not long ago, we are interested in plant hormone cross-talk and phytohormone-mediated processes, especially with respect to plant stress responses. As an example, we recently described a wound- and environmental stress-induced aromatic L-amino acid decarboxylase (TyrDC1) that specifically catalyzes the conversion of L- tyrosine to tyramine. It is not yet entirely clear what physiological function can be attributed to TyrDC1 and tyramine, respectively. However, the latter could serve as a precusor for several interesting secondary metabolites, including phenolic cell wall constituents, jasmonate derivatives, and catecholeamines.

Central to this project is the investigation of molecular mechanisms that contribute to stress perception and integration, leading to approriate plant responses. The cross-talk between auxins and oxylipins and the relationship between plant stress and growth responses are particular concerns of this work. As with the first research line, we use a combination of genetic, phenotypic, metabolomic, and biochemical methods in order to answer physiological questions turning up in this project.

 
 

Representative Publications

Loba, VC; Alonso, M-MP; Pollmann, S. 2017. "Monitoring of crosstalk between jasmonate and auxin in the framework of plant stress responses of roots", p. 175-185. In T. Dandekar and M. Naseem (eds.), Auxins and Cytokinins in Plant Biology: Methods and Protocols. Springer New York, New York, NY. DOI: 10.1007/978-1-4939-6831-2_15".

Lehmann, T; Janowitz, T; Sánchez-Parra, B; Alonso, M-MP; Trompetter, I; Piotrowski, M; Pollmann, S. 2017. "Arabidopsis NITRILASE 1 contributes to the regulation of root growth and development through modulation of auxin biosynthesis in seedlings". Frontiers in Plant Science. DOI: 10.3389/fpls.2017.00036".

Loba, VC; Pollmann, S. 2017. "Highly sensitive salicylic acid quantification in milligram amounts of plant tissue", p. 221-229. In J. Kleine-Vehn and M. Sauer (eds.), Plant Hormones: Methods and Protocols. Springer New York, New York, NY. DOI: 10.1007/978-1-4939-6469-7_18".

Silva-Navas, J; Moreno-Risueño, MA; Manzano, C; Téllez-Robledo, B; Navarro-Neila, S; Carrasco, V; Pollmann, S; Gallego, FJ; del Pozo, JC. 2016. "Flavonols mediate root phototropism and growth through regulation of proliferation-to-differentiation transition". Plant Cell. DOI: 10.1105/tpc.15.00857".

Zhu, J; Bailly, A; Zwiewka, M; Sovero, V; di Donato, M; Ge, P; Oehri, J; Aryal, B; Hao, P; Linnert, M; Burgardt, N; Lücke, C; Weiwad, M; Michel, M; Weiergräber, OH; Pollmann, S; Azzarello, E; Mancuso, S; Ferro, N; Fukao, Y; Hoffmann, C; Wedlich-Söldner, R; Friml, J; Thomas, C; Geisler, M. 2016. "TWISTED DWARF1 mediates the action of auxin transport inhibitors on actin cytoskeleton dynamics". Plant Cell. DOI: 10.1105/tpc.15.00726".

Boex-Fontvieille, E; Rustgi, S; Von Wettstein, D; Pollmann, S; Reinbothe, S; Reinbothe, C. 2016. "Jasmonic acid protects etiolated seedlings of Arabidopsis thaliana against herbivorous arthropods". Plant Signaling & Behavior. DOI: 10.1080/15592324.2016.1214349".

Boex-Fontvieille, E; Rustgi, S; von Wettstein, D; Pollmann, S; Reinbothe, S; Reinbothe, C. 2016. "An ethylene-protected Achilles’ heel of etiolated seedlings for arthropod deterrence". Frontiers in Plant Science. DOI: 10.3389/fpls.2016.01246".

Wilcoxen, J; Arragain, S; Scandurra, AA; Jimenez-Vicente, E; Echavarri-Erasun, C; Pollmann, S; Britt, RD; Rubio, LM. 2016. "Electron paramagnetic resonance characterization of three iron–sulfur clusters present in the nitrogenase cofactor maturase NifB from Methanocaldococcus infernus". Journal of the American Chemical Society. DOI: 10.1021/jacs.6b03329".

de Marchi, R; Sorel, M; Mooney, B; Fudal, I; Goslin, K; Kwasniewska, K; Ryan, PT; Pfalz, M; Kroymann, J; Pollmann, S; Feechan, A; Wellmer, F; Rivas, S; Graciet, E. 2016. "The N-end rule pathway regulates pathogen responses in plants". Scientific Reports. DOI: 10.1038/srep26020".

Springer, A; Kang, C; Rustgi, S; von Wettstein, D; Reinbothe, C; Pollmann, S; Reinbothe, S. 2016. "Programmed chloroplast destruction during leaf senescence involves 13-lipoxygenase (13-LOX)". Proceedings of the National Academy of Sciences of the United States of America. DOI: 10.1073/pnas.1525747113".

Król, P; Igielski, R; Pollmann, S; Kępczyńska, E. 2015. "Priming of seeds with methyl jasmonate induced resistance to hemi-biotroph Fusarium oxysporum f.sp. lycopersici in tomato via 12-oxo-phytodienoic acid, salicylic acid, and flavonol accumulation". Journal of Plant Physiology. DOI: 10.1016/j.jplph.2015.01.018".

Corrales, A-R; Nebauer, SG; Carrillo, L; Fernández-Nohales, P; Marqués, J; Renau-Morata, B; Granell, A; Pollmann, S; Vicente-Carbajosa, J; Molina, R-V; Medina, J. 2014. "Characterization of tomato Cycling Dof Factors reveals conserved and new functions in the control of flowering time and abiotic stress responses". Journal of Experimental Botany. DOI: 10.1093/jxb/ert451".

Corrales, R; Carrillo, L; Nebauer, SG; Renau-Morata, B; Sánchez-Perales, M; Fernández-Nohales, P; Marqués, J; Granell, A; Pollmann, S; Vicente-Carbajosa, J; Molina, RV; Medina, J. 2014. "Salinity assay in Arabidopsis". Bio-protocol. DOI:

Renau-Morata, B; Sánchez-Perales, M; Medina, J; Molina, RV; Corrales, R; Carrillo, L; Fernández-Nohales, P; Marqués, J; Pollmann, S; Vicente-Carbajosa, J; Granell, A; Nebauer, SG. 2014. "Salinity assay in tomato". Bio-protocol. DOI:

Hentrich, M; Bottcher, C; Duchting, P; Cheng, Y; Zhao, Y; Berkowitz, O; Masle, J; Medina, J; Pollmann, S. 2013. "The jasmonic acid signaling pathway is linked to auxin homeostasis through the modulation of YUCCA8 and YUCCA9 gene expression". Plant Journal. DOI: 10.1111/tpj.12152".

Hentrich, M; Sánchez-Parra, B; Pérez Alonso, M-M; Carrasco Loba, V; Carrillo, L; Vicente-Carbajosa, J; Medina, J; Pollmann, S. 2013. "YUCCA8 and YUCCA9 overexpression reveals a link between auxin signaling and lignification through the induction of ethylene biosynthesis". Plant Signaling & Behavior. DOI: 10.4161/psb.26363".

Grossmann K, Christiansen N, Looser R, Tresch S, Hutzler J, Pollmann S, Ehrhardt T. 2012. "Physionomics and metabolomics – two key approaches in herbical mode of action discovery". Pest Manag Sci. 68(4): 494-504.

Kamimoto, Y., Terasaka, K., Hamamoto, M., Takanashi, K., Fukuda, S., Shitan, N., Sugiyama, A., Suzuki, H., Shibata, D., Wang, B., Pollmann, S., Geisler, M., Yazaki, K. 2012. Arabidopsis ABCB21 is a Facultative Auxin Importer/Exporter Regulated by Cytoplasmic Auxin Concentration. Plant & Cell Physiology 53(12):2090-2100.

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