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Publikation

Wasternack, C.; How Jasmonates Earned their Laurels: Past and Present J. Plant Growth Regul. 34, 761-794, (2015) DOI: 10.1007/s00344-015-9526-5

The histories of research regarding all plant hormones are similar. Identification and structural elucidation have been followed by analyses of their biosynthesis, distributions, signaling cascades, roles in developmental or stress response programs, and crosstalk. Jasmonic acid (JA) and its derivatives comprise a group of plant hormones that were discovered recently, compared to auxin, abscisic acid, cytokinins, gibberellic acid, and ethylene. Nevertheless, there have been tremendous advances in JA research, following the general progression outlined above and parallel efforts focused on several other “new” plant hormones (brassinosteroids, salicylate, and strigolactones). This review focuses on historical aspects of the identification of jasmonates, and characterization of their biosynthesis, distribution, perception, signaling pathways, crosstalk with other hormones and roles in plant stress responses and development. The aim is to illustrate how our present knowledge on jasmonates was generated and how that influences current efforts to extend our knowledge.
Publikation

Ried, M. K.; Antolín-Llovera, M.; Parniske, M.; Spontaneous symbiotic reprogramming of plant roots triggered by receptor-like kinases eLife 3, e03891, (2014) DOI: 10.7554/eLife.03891

Symbiosis Receptor-like Kinase (SYMRK) is indispensable for the development of phosphate-acquiring arbuscular mycorrhiza (AM) as well as nitrogen-fixing root nodule symbiosis, but the mechanisms that discriminate between the two distinct symbiotic developmental fates have been enigmatic. In this study, we show that upon ectopic expression, the receptor-like kinase genes Nod Factor Receptor 1 (NFR1), NFR5, and SYMRK initiate spontaneous nodule organogenesis and nodulation-related gene expression in the absence of rhizobia. Furthermore, overexpressed NFR1 or NFR5 associated with endogenous SYMRK in roots of the legume Lotus japonicus. Epistasis tests revealed that the dominant active SYMRK allele initiates signalling independently of either the NFR1 or NFR5 gene and upstream of a set of genes required for the generation or decoding of calcium-spiking in both symbioses. Only SYMRK but not NFR overexpression triggered the expression of AM-related genes, indicating that the receptors play a key role in the decision between AM- or root nodule symbiosis-development.
Publikation

Maldonado-Bonilla, L. D.; Eschen-Lippold, L.; Gago-Zachert, S.; Tabassum, N.; Bauer, N.; Scheel, D.; Lee, J.; The Arabidopsis Tandem Zinc Finger 9 Protein Binds RNA and Mediates Pathogen-Associated Molecular Pattern-Triggered Immune Responses Plant Cell Physiol. 55, 412-425, (2014) DOI: 10.1093/pcp/pct175

Recognition of pathogen-associated molecular patterns (PAMPs) induces multiple defense mechanisms to limit pathogen growth. Here, we show that the Arabidopsis thaliana tandem zinc finger protein 9 (TZF9) is phosphorylated by PAMP-responsive mitogen-activated protein kinases (MAPKs) and is required to trigger a full PAMP-triggered immune response. Analysis of a tzf9 mutant revealed attenuation in specific PAMP-triggered reactions such as reactive oxygen species accumulation, MAPK activation and, partially, the expression of several PAMP-responsive genes. In accordance with these weaker PAMP-triggered responses, tzf9 mutant plants exhibit enhanced susceptibility to virulent Pseudomonas syringae pv. tomato DC3000. Visualization of TZF9 localization by fusion to green fluorescent protein revealed cytoplasmic foci that co-localize with marker proteins of processing bodies (P-bodies). This localization pattern is affected by inhibitor treatments that limit mRNA availability (such as cycloheximide or actinomycin D) or block nuclear export (leptomycin B). Coupled with its ability to bind the ribohomopolymers poly(rU) and poly(rG), these results suggest involvement of TZF9 in post-transcriptional regulation, such as mRNA processing or storage pathways, to regulate plant innate immunity.
Publikation

Budiharjo, A.; Chowdhury, S. P.; Dietel, K.; Beator, B.; Dolgova, O.; Fan, B.; Bleiss, W.; Ziegler, J.; Schmid, M.; Hartmann, A.; Borriss, R.; Transposon Mutagenesis of the Plant-Associated Bacillus amyloliquefaciens ssp. plantarum FZB42 Revealed That the nfrA and RBAM17410 Genes Are Involved in Plant-Microbe-Interactions PLOS ONE 9, e98267, (2014) DOI: 10.1371/journal.pone.0098267

Bacillus amyloliquefaciens ssp. plantarum FZB42 represents the prototype of Gram-positive plant growth promoting and biocontrol bacteria. In this study, we applied transposon mutagenesis to generate a transposon library, which was screened for genes involved in multicellular behavior and biofilm formation on roots as a prerequisite of plant growth promoting activity. Transposon insertion sites were determined by rescue-cloning followed by DNA sequencing. As in B. subtilis, the global transcriptional regulator DegU was identified as an activator of genes necessary for swarming and biofilm formation, and the DegU-mutant of FZB42 was found impaired in efficient root colonization. Direct screening of 3,000 transposon insertion mutants for plant-growth-promotion revealed the gene products of nfrA and RBAM_017140 to be essential for beneficial effects exerted by FZB42 on plants. We analyzed the performance of GFP-labeled wild-type and transposon mutants in the colonization of lettuce roots using confocal laser scanning microscopy. While the wild-type strain heavily colonized root surfaces, the nfrA mutant did not colonize lettuce roots, although it was not impaired in growth in laboratory cultures, biofilm formation and swarming motility on agar plates. The RBAM17410 gene, occurring in only a few members of the B. subtilis species complex, was directly involved in plant growth promotion. None of the mutant strains were affected in producing the plant growth hormone auxin. We hypothesize that the nfrA gene product is essential for overcoming the stress caused by plant response towards bacterial root colonization.
Publikation

Bosch, M.; Wright, L. P.; Gershenzon, J.; Wasternack, C.; Hause, B.; Schaller, A.; Stintzi, A.; Jasmonic Acid and Its Precursor 12-Oxophytodienoic Acid Control Different Aspects of Constitutive and Induced Herbivore Defenses in Tomato Plant Physiol. 166, 396-410, (2014) DOI: 10.1104/pp.114.237388

The jasmonate family of growth regulators includes the isoleucine (Ile) conjugate of jasmonic acid (JA-Ile) and its biosynthetic precursor 12-oxophytodienoic acid (OPDA) as signaling molecules. To assess the relative contribution of JA/JA-Ile and OPDA to insect resistance in tomato (Solanum lycopersicum), we silenced the expression of OPDA reductase3 (OPR3) by RNA interference (RNAi). Consistent with a block in the biosynthetic pathway downstream of OPDA, OPR3-RNAi plants contained wild-type levels of OPDA but failed to accumulate JA or JA-Ile after wounding. JA/JA-Ile deficiency in OPR3-RNAi plants resulted in reduced trichome formation and impaired monoterpene and sesquiterpene production. The loss of these JA/JA-Ile -dependent defense traits rendered them more attractive to the specialist herbivore Manduca sexta with respect to feeding and oviposition. Oviposition preference resulted from reduced levels of repellant monoterpenes and sesquiterpenes. Feeding preference, on the other hand, was caused by increased production of cis-3-hexenal acting as a feeding stimulant for M. sexta larvae in OPR3-RNAi plants. Despite impaired constitutive defenses and increased palatability of OPR3-RNAi leaves, larval development was indistinguishable on OPR3-RNAi and wild-type plants, and was much delayed compared with development on the jasmonic acid-insensitive1 (jai1) mutant. Apparently, signaling through JAI1, the tomato ortholog of the ubiquitin ligase CORONATINE INSENSITIVE1 in Arabidopsis (Arabidopsis thaliana), is required for defense, whereas the conversion of OPDA to JA/JA-Ile is not. Comparing the signaling activities of OPDA and JA/JA-Ile, we found that OPDA can substitute for JA/JA-Ile in the local induction of defense gene expression, but the production of JA/JA-Ile is required for a systemic response.
Publikation

Antolín-Llovera, M.; Petutsching, E. K.; Ried, M. K.; Lipka, V.; Nürnberger, T.; Robatzek, S.; Parniske, M.; Knowing your friends and foes - plant receptor-like kinases as initiators of symbiosis or defence New Phytol. 204, 791-802, (2014) DOI: 10.1111/nph.13117

The decision between defence and symbiosis signalling in plants involves alternative and modular plasma membrane‐localized receptor complexes. A critical step in their activation is ligand‐induced homo‐ or hetero‐oligomerization of leucine‐rich repeat (LRR)‐ and/or lysin motif (LysM) receptor‐like kinases (RLKs). In defence signalling, receptor complexes form upon binding of pathogen‐associated molecular patterns (PAMPs), including the bacterial flagellin‐derived peptide flg22, or chitin. Similar mechanisms are likely to operate during the perception of microbial symbiont‐derived (lipo)‐chitooligosaccharides. The structurally related chitin‐oligomer ligands chitooctaose and chitotetraose trigger defence and symbiosis signalling, respectively, and their discrimination involves closely related, if not identical, LysM‐RLKs. This illustrates the demand for and the challenges imposed on decision mechanisms that ensure appropriate signal initiation. Appropriate signalling critically depends on abundance and localization of RLKs at the cell surface. This is regulated by internalization, which also provides a mechanism for the removal of activated signalling RLKs. Abundance of the malectin‐like domain (MLD)‐LRR‐RLK Symbiosis Receptor‐like Kinase (SYMRK) is additionally controlled by cleavage of its modular ectodomain, which generates a truncated and rapidly degraded RLK fragment. This review explores LRR‐ and LysM‐mediated signalling, the involvement of MLD‐LRR‐RLKs in symbiosis and defence, and the role of endocytosis in RLK function.
Publikation

Antolín-Llovera, M.; Ried, M. K.; Parniske, M.; Cleavage of the SYMBIOSIS RECEPTOR-LIKE KINASE Ectodomain Promotes Complex Formation with Nod Factor Receptor 5 Curr. Biol. 24, 422-427, (2014) DOI: 10.1016/j.cub.2013.12.053

Plants form root symbioses with fungi and bacteria to improve their nutrient supply. SYMBIOSIS RECEPTOR-LIKE KINASE (SYMRK) is required for phosphate-acquiring arbuscular mycorrhiza, as well as for the nitrogen-fixing root nodule symbiosis of legumes [1] and actinorhizal plants [2, 3], but its precise function was completely unclear. Here we show that the extracytoplasmic region of SYMRK, which comprises three leucine-rich repeats (LRRs) and a malectin-like domain (MLD) related to a carbohydrate-binding protein from Xenopus laevis [4], is cleaved to release the MLD in the absence of symbiotic stimulation. A conserved sequence motif—GDPC—that connects the MLD to the LRRs is required for MLD release. We discovered that Nod factor receptor 5 (NFR5) [5, 6, 7, 8] forms a complex with the SYMRK version that remains after MLD release (SYMRK-ΔMLD). SYMRK-ΔMLD outcompeted full-length SYMRK for NFR5 interaction, indicating that the MLD negatively interferes with complex formation. SYMRK-ΔMLD is present at lower amounts than MLD, suggesting rapid degradation after MLD release. A deletion of the entire extracytoplasmic region increased protein abundance, suggesting that the LRR region promotes degradation. Curiously, this deletion led to excessive infection thread formation, highlighting the importance of fine-tuned regulation of SYMRK by its ectodomain.
Publikation

Jayaweera, T.; Siriwardana, C.; Dharmasiri, S.; Quint, M.; Gray, W. M.; Dharmasiri, N.; Alternative Splicing of Arabidopsis IBR5 Pre-mRNA Generates Two IBR5 Isoforms with Distinct and Overlapping Functions PLOS ONE 9, e102301, (2014) DOI: 10.1371/journal.pone.0102301

The INDOLE-3-BUTYRIC ACID RESPONSE5 (IBR5) gene encodes a dual specificity phosphatase that regulates plant auxin responses. IBR5 has been predicted to generate two transcripts through alternative splicing, but alternative splicing of IBR5 has not been confirmed experimentally. The previously characterized ibr5-1 null mutant exhibits many auxin related defects such as auxin insensitive primary root growth, defective vascular development, short stature and reduced lateral root development. However, whether all these defects are caused by the lack of phosphatase activity is not clear. Here we describe two new auxin insensitive IBR5 alleles, ibr5-4, a catalytic site mutant, and ibr5-5, a splice site mutant. Characterization of these new mutants indicates that IBR5 is post-transcriptionally regulated to generate two transcripts, AT2G04550.1 and AT2G04550.3, and consequently two IBR5 isoforms, IBR5.1 and IBR5.3. The IBR5.1 isoform exhibits phosphatase catalytic activity that is required for both proper degradation of Aux/IAA proteins and auxin-induced gene expression. These two processes are independently regulated by IBR5.1. Comparison of new mutant alleles with ibr5-1 indicates that all three mutant alleles share many phenotypes. However, each allele also confers distinct defects implicating IBR5 isoform specific functions. Some of these functions are independent of IBR5.1 catalytic activity. Additionally, analysis of these new mutant alleles suggests that IBR5 may link ABP1 and SCFTIR1/AFBs auxin signaling pathways.
Publikation

Grubb, C. D.; Zipp, B. J.; Kopycki, J.; Schubert, M.; Quint, M.; Lim, E.-K.; Bowles, D. J.; Pedras, M. S. C.; Abel, S.; Comparative analysis of Arabidopsis UGT74 glucosyltransferases reveals a special role of UGT74C1 in glucosinolate biosynthesis Plant J. 79, 92-105, (2014) DOI: 10.1111/tpj.12541

The study of glucosinolates and their regulation has provided a powerful framework for the exploration of fundamental questions about the function, evolution, and ecological significance of plant natural products, but uncertainties about their metabolism remain. Previous work has identified one thiohydroximate S‐glucosyltransferase, UGT74B1, with an important role in the core pathway, but also made clear that this enzyme functions redundantly and cannot be the sole UDP‐glucose dependent glucosyltransferase (UGT) in glucosinolate synthesis. Here, we present the results of a nearly comprehensive in vitro activity screen of recombinant Arabidopsis Family 1 UGTs, which implicate other members of the UGT74 clade as candidate glucosinolate biosynthetic enzymes. Systematic genetic analysis of this clade indicates that UGT74C1 plays a special role in the synthesis of aliphatic glucosinolates, a conclusion strongly supported by phylogenetic and gene expression analyses. Finally, the ability of UGT74C1 to complement phenotypes and chemotypes of the ugt74b1‐2 knockout mutant and to express thiohydroximate UGT activity in planta provides conclusive evidence for UGT74C1 being an accessory enzyme in glucosinolate biosynthesis with a potential function during plant adaptation to environmental challenge.
Publikation

Flores, R.; Gago-Zachert, S.; Serra, P.; Sanjuán, R.; Elena, S. F.; Viroids: Survivors from the RNA World? Annu. Rev. Microbiol. 68, 395-414, (2014) DOI: 10.1146/annurev-micro-091313-103416

Because RNA can be a carrier of genetic information and a biocatalyst, there is a consensus that it emerged before DNA and proteins, which eventually assumed these roles and relegated RNA to intermediate functions. If such a scenario—the so-called RNA world—existed, we might hope to find its relics in our present world. The properties of viroids that make them candidates for being survivors of the RNA world include those expected for primitive RNA replicons: (a) small size imposed by error-prone replication, (b) high G + C content to increase replication fidelity, (c) circular structure for assuring complete replication without genomic tags, (d) structural periodicity for modular assembly into enlarged genomes, (e) lack of protein-coding ability consistent with a ribosome-free habitat, and (f) replication mediated in some by ribozymes, the fingerprint of the RNA world. With the advent of DNA and proteins, those protoviroids lost some abilities and became the plant parasites we now know.
  • Die Leibniz-Gemeinschaft
  • Digitalisierung in der Landwirtschaft
  • Martin-Luther Universität Halle
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