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Publications - Molecular Signal Processing

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Printed publications

Wasternack, C. & Feussner, I. The oxylipin pathways: biochemistry and function. Annu Rev Plant Biol (2018) DOI: 10.1146/annurev-arplant-042817-040440

Plant oxylipins form a constantly growing group of signaling molecules that comprise oxygenated fatty acids and metabolites derived therefrom. In the last decade, the understanding of biosynthesis, metabolism, and action of oxylipins, especially jasmonates, has dramatically improved. Additional mechanistic insights into the action of enzymes and insights into signaling pathways have been deepened for jasmonates. For other oxylipins, such as the hydroxy fatty acids, individual signaling properties and cross talk between different oxylipins or even with additional phytohormones have recently been described. This review summarizes recent understanding of the biosynthesis, regulation, and function of oxylipins.
Publications

Wasternack, C A plant's balance of growth and defense – revisited. New Phytol 215, 1291-1294, (2017) DOI: 10.1111/nph.14720

The sessile lifestyle of plants requires a permanent and efficient adjustment to environmental stresses caused by biotic factors, such as pathogens and herbivores, or abiotic factors, such as drought and salt. Any defense responses, however, are costly, and investment into defense leads to reduced growth. These plant growth–defense tradeoffs, with simultaneous activation of defense and maintenance of growth, are critical for crop breeding. For some stresses, such as wounding by herbivores, the cost–benefit ratio in the growth–defense tradeoff has been tested in native populations; a costly jasmonic acid (JA)-induced defense response has been shown, which is down-regulated when the defense is not required (Baldwin, 1998). JA is the central player in many stress responses: inhibition of root growth, photosynthesis, and leaf growth (Zhang & Turner, 2008), induction of defense proteins, formation of secondary compounds active in defense and defense upon bacterial infection are JA-induced processes with consequences for growth (Wasternack & Hause, 2013; reviewed in Havko et al., 2016).
This article is a Commentary on Major et al., 215: 1533–1547.
Publications

Bürstenbinder, K., Mitra, D. & Quegwer, J.  Functions of IQD proteins as hubs in cellular calcium and auxin signaling: a toolbox for shape formation and tissue-specification in plants? Plant Signal Behav 12 , e1331198, (2017) DOI: 10.1080/15592324.2017.1331198

Ca2+ ions play pivotal roles as second messengers in intracellular signal transduction, and coordinate many biological processes. Changes in intracellular Ca2+ levels are perceived by Ca2+ sensors such as CaM/CML proteins, which transduce Ca2+ signals into cellular responses by regulation of diverse target proteins. Insights into molecular functions of CaM targets are thus essential to understand the molecular and cellular basis of Ca2+ signaling. During the last decade, IQD proteins emerged as the largest class of CaM targets in plants with mostly unknown functions. In the March issue of Plant Physiology, we presented the first comprehensive characterization of the 33-membered IQD family in Arabidopsis thaliana. We showed, by analysis of the subcellular localization of translational GFP fusion proteins, that most IQD members label MTs, and additionally often localize to the cell nucleus or to membranes, where the recruit CaM Ca2+ sensors. Important functions at MTs are supported by altered MT organization and plant growth in IQD gain-of-function lines. Because IQD proteins share structural hallmarks of scaffold proteins, we propose roles of IQDs in the assembly of macromolecular complexes to orchestrate Ca2+ CaM signaling from membranes to the nucleus. 
Printed publications

Gantner, J., Ilse, T., Ordon, J., Kretschmer, C., Gruetzner, R., Loefke, C., Dagdas, Y., Buerstenbinder, K., Marillonnet, S. & Stuttmann, J. Peripheral infrastructure vectors and an extended set of plant parts for the modular cloning system. bioRxiv (2017) DOI: 10.1101/237768

Standardized DNA assembly strategies facilitate the generation of multigene constructs from collections of building blocks in plant synthetic biology. A common syntax for hierarchical DNA assembly following the Golden Gate principle employing Type IIs restriction endonucleases was recently developed, and underlies the Modular Cloning and GoldenBraid systems. In these systems, transcriptional units and/or multigene constructs are assembled from libraries of standardized building blocks, also referred to as phytobricks, in several hierarchical levels and by iterative Golden Gate reactions. This combinatorial assembly strategy meets the increasingly complex demands in biotechnology and bioengineering, and also represents a cost-efficient and versatile alternative to previous molecular cloning techniques. For Modular Cloning, a collection of commonly used Plant Parts was previously released together with the Modular Cloning toolkit itself, which largely facilitated the adoption of this cloning system in the research community. Here, a collection of approximately 80 additional phytobricks is provided. These phytobricks comprise e.g. modules for inducible expression systems, different promoters or epitope tags, which will increase the versatility of Modular Cloning-based DNA assemblies. Furthermore, first instances of a "peripheral infrastructure" around Modular Cloning are presented: While available toolkits are designed for the assembly of plant transformation constructs, vectors were created to also use coding sequence-containing phytobricks directly in yeast two hybrid interaction or bacterial infection assays. Additionally, DNA modules and assembly strategies for connecting Modular Cloning with Gateway Cloning are presented, which may serve as an interface between available resources and newly adopted hierarchical assembly strategies. The presented material will be provided as a toolkit to the plant research community and will further enhance the usefulness and versatility of Modular Cloning.

Printed publications

Gantner, J., Ilse, T., Ordon, J., Kretschmer, C., Gruetzner, R., Loefke, C., Dagdas, Y., Buerstenbinder, K., Marillonnet, S. & Stuttmann, J. Peripheral infrastructure vectors and an extended set of plant parts for the modular cloning system.  bioRxiv (2017) DOI: 10.1101/237768

Standardized DNA assembly strategies facilitate the generation of multigene constructs from collections of building blocks in plant synthetic biology. A common syntax for hierarchical DNA assembly following the Golden Gate principle employing Type IIs restriction endonucleases was recently developed, and underlies the Modular Cloning and GoldenBraid systems. In these systems, transcriptional units and/or multigene constructs are assembled from libraries of standardized building blocks, also referred to as phytobricks, in several hierarchical levels and by iterative Golden Gate reactions. This combinatorial assembly strategy meets the increasingly complex demands in biotechnology and bioengineering, and also represents a cost-efficient and versatile alternative to previous molecular cloning techniques. For Modular Cloning, a collection of commonly used Plant Parts was previously released together with the Modular Cloning toolkit itself, which largely facilitated the adoption of this cloning system in the research community. Here, a collection of approximately 80 additional phytobricks is provided. These phytobricks comprise e.g. modules for inducible expression systems, different promoters or epitope tags, which will increase the versatility of Modular Cloning-based DNA assemblies. Furthermore, first instances of a "peripheral infrastructure" around Modular Cloning are presented: While available toolkits are designed for the assembly of plant transformation constructs, vectors were created to also use coding sequence-containing phytobricks directly in yeast two hybrid interaction or bacterial infection assays. Additionally, DNA modules and assembly strategies for connecting Modular Cloning with Gateway Cloning are presented, which may serve as an interface between available resources and newly adopted hierarchical assembly strategies. The presented material will be provided as a toolkit to the plant research community and will further enhance the usefulness and versatility of Modular Cloning.
Publications

Abel, S. Phosphate scouting by root tips. Curr Opin Plant Biol. 39, 168-177, (2017) DOI: 10.1016/j.pbi.2017.04.016

Chemistry assigns phosphate (Pi) dominant roles in metabolism; however, it also renders the macronutrient a genuinely limiting factor of plant productivity. Pi bioavailability is restricted by low Pi mobility in soil and antagonized by metallic toxicities, which force roots to actively seek and selectively acquire the vital element. During the past few years, a first conceptual outline has emerged of the sensory mechanisms at root tips, which monitor external Pi and transmit the edaphic cue to inform root development. This review highlights new aspects of the Pi acquisition strategy of Arabidopsis roots, as well as a framework of local Pi sensing in the context of antagonistic interactions between Pi and its major associated metallic cations, Fe3+ and Al3+.
Printed publications

Krägeloh, T., Cavalleri, J. M. V., Ziegler, J., Sander, J., Terhardt, M., Breves, G. & Cehak, A. Identification of hypoglycin a binding adsorbents as potential preventive measures in co-grazers of atypical myopathy affected horses. Equine Vet J. (2017) DOI: 10.1111/evj.12723

Summary

Background

Intestinal absorption of hypoglycin A (HGA) and its metabolism are considered major prerequisites for atypical myopathy (AM). The increasing incidence and the high mortality rate of AM urgently necessitate new therapeutic and/or preventative approaches.

Objectives

To identify a substance for oral administration capable of binding HGA in the intestinal lumen and effectively reducing the intestinal absorption of the toxin.

Study design

Experimental in vitro study.

Methods

Substances commonly used in equine practice (activated charcoal composition, di-tri-octahedral smectite, mineral oil and activated charcoal) were tested for their binding capacity for HGA using an in vitro incubation method. The substance most effective in binding HGA was subsequently tested for its potential to reduce intestinal HGA absorption. Jejunal tissues of 6 horses were incubated in Ussing chambers to determine mucosal uptake, tissue accumulation, and serosal release of HGA in the presence and absence of the target substance. Potential intestinal metabolism in methylenecyclopropyl acetic acid (MCPA)-conjugates was investigated by analysing their concentrations in samples from the Ussing chambers.

Results

Activated charcoal composition and activated charcoal were identified as potent HGA binding substances with dose and pH dependent binding capacity. There was no evidence of intestinal HGA metabolism.

Main limitations

Binding capacity of adsorbents was tested in vitro using aqueous solutions, and in vivo factors such as transit time and composition of intestinal content, may affect adsorption capacity after oral administration.

Conclusions

For the first time, this study identifies substances capable of reducing HGA intestinal absorption. This might have major implications as a preventive measure in cograzers of AM affected horses but also in horses at an early stage of intoxication.

Publications

Liu, S., Ziegler, J., Zeier, J., Birkenbihl, R. P. & Somssich, I. E. Botrytis cinerea B05.10 promotes disease development in Arabidopsis by suppressing WRKY33-mediated host immunity. Plant, Cell Environ. 40(10), 2189-2206, (2017) DOI: 10.1111/pce.13022

The large WRKY transcription factor family is mainly involved in regulating plant immune responses. Arabidopsis WRKY33 is a key transcriptional regulator of hormonal and metabolic processes towards Botrytis cinerea strain 2100 infection and is essential for resistance. In contrast to B. cinerea strain 2100, the strain B05.10 is virulent on wild-type (WT) Col-0 Arabidopsis plants highlighting the genetic diversity within this pathogen species. We analysed how early WRKY33-dependent responses are affected upon infection with strain B05.10 and found that most of these responses were strongly dampened during this interaction. Ectopic expression of WRKY33 resulted in complete resistance towards this strain indicating that virulence of B05.10, at least partly, depends on suppressing WRKY33 expression/protein accumulation. As a consequence, the expression levels of direct WRKY33 target genes, including those involved in the biosynthesis of camalexin, were also reduced upon infection. Concomitantly, elevated levels of the phytohormone abscisic acid (ABA) were observed. Molecular and genetic studies revealed that ABA negatively influences defence to B05.10 and effects jasmonic acid/ethylene (JA/ET) and salicylic acid (SA) levels. Susceptibility/resistance was determined by the antagonistic effect of ABA on JA, and this crosstalk required suppressing WRKY33 functions at early infection stages. This indicates that B. cinerea B05.10 promotes disease by suppressing WRKY33-mediated host defences.
Books and chapters

White, M. D., Klecker, M., Hopkinson, R. J., Weits, D. A., Mueller, C., Naumann, C., O’Neill, R., Wickens, J., Yang, J., Brooks-Bartlett, J. C., Garman, E. F., Grossmann, T. N., Dissmeyer, N. & Flashman, E. Plant cysteine oxidases are dioxygenases that directly enable arginyl transferase-catalysed arginylation of N-end rule targets Nature Commun 8, 14690, (2017) DOI: 10.1038/ncomms14690

Crop yield loss due to flooding is a threat to food security. Submergence-induced hypoxia in plants results in stabilization of group VII ETHYLENE RESPONSE FACTORs (ERF-VIIs), which aid survival under these adverse conditions. ERF-VII stability is controlled by the N-end rule pathway, which proposes that ERF-VII N-terminal cysteine oxidation in normoxia enables arginylation followed by proteasomal degradation. The PLANT CYSTEINE OXIDASEs (PCOs) have been identified as catalysts of this oxidation. ERF-VII stabilization in hypoxia presumably arises from reduced PCO activity. We directly demonstrate that PCO dioxygenase activity produces Cys-sulfinic acid at the N terminus of an ERF-VII peptide, which then undergoes efficient arginylation by an arginyl transferase (ATE1). This provides molecular evidence of N-terminal Cys-sulfinic acid formation and arginylation by N-end rule pathway components, and a substrate of ATE1 in plants. The PCOs and ATE1 may be viable intervention targets to stabilize N-end rule substrates, including ERF-VIIs, to enhance submergence tolerance in agriculture.
Publications

Dong, H., Dumenil, J., Lu, F.-H., Na, L., Vanhaeren, H., Naumann, C., Klecker, M., Prior, R., Smith, C., McKenzie, N., Saalbach, G., Chen, L., Xia, T., Gonzalez, N., Seguela, M., Inze, D., Dissmeyer, N., Li, Y. & Bevan, M. W. Ubiquitylation activates a peptidase that promotes cleavage and destabilization of its activating E3 ligases and diverse growth regulatory proteins to limit cell proliferation in Arabidopsis Gen. Dev 31, 197-208, (2017) DOI: 10.1101/gad.292235.116

The characteristic shapes and sizes of organs are established by cell proliferation patterns and final cell sizes, but the underlying molecular mechanisms coordinating these are poorly understood. Here we characterize a ubiquitin-activated peptidase called DA1 that limits the duration of cell proliferation during organ growth in Arabidopsis thaliana. The peptidase is activated by two RING E3 ligases, Big Brother (BB) and DA2, which are subsequently cleaved by the activated peptidase and destabilized. In the case of BB, cleavage leads to destabilization by the RING E3 ligase PROTEOLYSIS 1 (PRT1) of the N-end rule pathway. DA1 peptidase activity also cleaves the deubiquitylase UBP15, which promotes cell proliferation, and the transcription factors TEOSINTE BRANCED 1/CYCLOIDEA/PCF 15 (TCP15) and TCP22, which promote cell proliferation and repress endoreduplication. We propose that DA1 peptidase activity regulates the duration of cell proliferation and the transition to endoreduplication and differentiation during organ formation in plants by coordinating the destabilization of regulatory proteins. 
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