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Publikation

García, M. L.; Bó, E. D.; da Graça, J. V.; Gago-Zachert, S.; Hammond, J.; Moreno, P.; Natsuaki, T.; Pallás, V.; Navarro, J. A.; Reyes, C. A.; Luna, G. R.; Sasaya, T.; Tzanetakis, I. E.; Vaira, A. M.; Verbeek, M.; ICTV Report Consortium, .; Corrigendum: ICTV Virus Taxonomy Profile: Ophioviridae J. Gen. Virol. 99, 949-949, (2018) DOI: 10.1099/jgv.0.001093

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Publikation

García, M. L.; Bó, E. D.; da Graça, J. V.; Gago-Zachert, S.; Hammond, J.; Moreno, P.; Natsuaki, T.; Pallás, V.; Navarro, J. A.; Reyes, C. A.; Luna, G. R.; Sasaya, T.; Tzanetakis, I. E.; Vaira, A. M.; Verbeek, M.; ICTV Report Consortium, .; ICTV Virus Taxonomy Profile: Ophioviridae J. Gen. Virol. 98, 1161-1162, (2017) DOI: 10.1099/jgv.0.000836

The Ophioviridae is a family of filamentous plant viruses, with single-stranded negative, and possibly ambisense, RNA genomes of 11.3–12.5 kb divided into 3–4 segments, each encapsidated separately. Virions are naked filamentous nucleocapsids, forming kinked circles of at least two different contour lengths. The sole genus, Ophiovirus, includes seven species. Four ophioviruses are soil-transmitted and their natural hosts include trees, shrubs, vegetables and bulbous or corm-forming ornamentals, both monocots and dicots. This is a summary of the International Committee on Taxonomy of Viruses (ICTV) Report on the taxonomy of the Ophioviridae, which is available at http://www.ictv.global/report/ophioviridae.
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

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

Den Herder, G.; Yoshida, S.; Antolín-Llovera, M.; Ried, M. K.; Parniske, M.; Lotus japonicus E3 Ligase SEVEN IN ABSENTIA4 Destabilizes the Symbiosis Receptor-Like Kinase SYMRK and Negatively Regulates Rhizobial Infection Plant Cell 24, 1691-1707, (2012) DOI: 10.1105/tpc.110.082248

The Lotus japonicus SYMBIOSIS RECEPTOR-LIKE KINASE (SYMRK) is required for symbiotic signal transduction upon stimulation of root cells by microbial signaling molecules. Here, we identified members of the SEVEN IN ABSENTIA (SINA) E3 ubiquitin-ligase family as SYMRK interactors and confirmed their predicted ubiquitin-ligase activity. In Nicotiana benthamiana leaves, SYMRK–yellow fluorescent protein was localized at the plasma membrane, and interaction with SINAs, as determined by bimolecular fluorescence complementation, was observed in small punctae at the cytosolic interface of the plasma membrane. Moreover, fluorescence-tagged SINA4 partially colocalized with SYMRK and caused SYMRK relocalization as well as disappearance of SYMRK from the plasma membrane. Neither the localization nor the abundance of Nod-factor receptor1 was altered by the presence of SINA4. SINA4 was transcriptionally upregulated during root symbiosis, and rhizobia inoculated roots ectopically expressing SINA4 showed reduced SYMRK protein levels. In accordance with a negative regulatory role in symbiosis, infection thread development was impaired upon ectopic expression of SINA4. Our results implicate SINA4 E3 ubiquitin ligase in the turnover of SYMRK and provide a conceptual mechanism for its symbiosis-appropriate spatio-temporal containment.
Publikation

Antolín-Llovera, M.; Ried, M. K.; Binder, A.; Parniske, M.; Receptor Kinase Signaling Pathways in Plant-Microbe Interactions Annu. Rev. Phytopathol. 50, 451-473, (2012) DOI: 10.1146/annurev-phyto-081211-173002

Plant receptor-like kinases (RLKs) function in diverse signaling pathways, including the responses to microbial signals in symbiosis and defense. This versatility is achieved with a common overall structure: an extracytoplasmic domain (ectodomain) and an intracellular protein kinase domain involved in downstream signal transduction. Various surfaces of the leucine-rich repeat (LRR) ectodomain superstructure are utilized for interaction with the cognate ligand in both plant and animal receptors. RLKs with lysin-motif (LysM) ectodomains confer recognitional specificity toward N-acetylglucosamine-containing signaling molecules, such as chitin, peptidoglycan (PGN), and rhizobial nodulation factor (NF), that induce immune or symbiotic responses. Signaling downstream of RLKs does not follow a single pattern; instead, the detailed analysis of brassinosteroid (BR) signaling, innate immunity, and symbiosis revealed at least three largely nonoverlapping pathways. In this review, we focus on RLKs involved in plant-microbe interactions and contrast the signaling pathways leading to symbiosis and defense.
Bücher und Buchkapitel

Vaira, A. M.; Gago-Zachert, S.; Garcia, M. L.; Guerri, J.; Hammond, J.; Milne, R. G.; Moreno, P.; Morikawa, T.; Natsuaki, T.; Navarro, J. A.; Pallas, V.; Torok, V.; Verbeek, M.; Vetten, H. J.; Family - Ophioviridae (King, A. M. Q., et al., eds.). 743-748, (2012) DOI: 10.1016/B978-0-12-384684-6.00060-4

This chapter focuses on Ophioviridae family whose sole member genus is Ophiovirus. The member species of the genus include Citrus psorosis virus (CPsV), Freesia sneak virus(FreSV), Lettuce ring necrosis virus (LRNV), and Mirafiori lettuce big-vein virus (MiLBVV).The single stranded negative/possibly ambisense RNA genome is divided into 3–4 segments, each of which is encapsidated in a single coat protein (43–50 kDa) forming filamentous virions of about 3 nm in diameter, in shape of kinked or probably internally coiled circles of at least two different contour lengths. Ophioviruses can be mechanically transmitted to a limited range of test plants, inducing local lesions and systemic mottle. The natural hosts of CPsV, ranunculus white mottle virus (RWMV), MiLBVV, and LRNV are dicotyledonous plants of widely differing taxonomy. CPsV has a wide geographical distribution in citrus in the Americas, in the Mediterranean and in New Zealand. FreSV has been reported in two species of the family Ranunculacae from Northern Italy, and in lettuce in France and Germany. Tulip mild mottle mosaic virus (TMMMV) has been reported in tulips in Japan. LRNV is closely associated with lettuce ring necrosis disease in The Netherlands, Belgium, and France, and FreSV has been reported in Europe, Africa, North America and New Zealand.
Publikation

Schilling, S.; Wasternack, C.; Demuth, H.-U.; Glutaminyl cyclases from animals and plants: a case of functionally convergent protein evolution Biol. Chem. 389, (2008) DOI: 10.1515/BC.2008.111

Several mammalian peptide hormones and proteins from plant and animal origin contain an N-terminal pyroglutamic acid (pGlu) residue. Frequently, the moiety is important in exerting biological function in either mediating interaction with receptors or stabilizing against N-terminal degradation. Glutaminyl cyclases (QCs) were isolated from different plants and animals catalyzing pGlu formation. The recent resolution of the 3D structures of Carica papaya and human QCs clearly supports different evolutionary origins of the proteins, which is also reflected by different enzymatic mechanisms. The broad substrate specificity is revealed by the heterogeneity of physiological substrates of plant and animal QCs, including cytokines, matrix proteins and pathogenesis-related proteins. Moreover, recent evidence also suggests human QC as a catalyst of pGlu formation at the N-terminus of amyloid peptides, which contribute to Alzheimer's disease. Obviously, owing to its biophysical properties, the function of pGlu in plant and animal proteins is very similar in terms of stabilizing or mediating protein and peptide structure. It is possible that the requirement for catalysis of pGlu formation under physiological conditions may have triggered separate evolution of QCs in plants and animals.
Publikation

Schilling, S.; Stenzel, I.; von Bohlen, A.; Wermann, M.; Schulz, K.; Demuth, H.-U.; Wasternack, C.; Isolation and characterization of the glutaminyl cyclases from Solanum tuberosum and Arabidopsis thaliana: implications for physiological functions Biol. Chem. 388, 145-153, (2007) DOI: 10.1515/BC.2007.016

Glutaminyl cyclases (QCs) catalyze the formation of pyroglutamic acid at the N-terminus of several peptides and proteins. On the basis of the amino acid sequence of Carica papaya QC, we identified cDNAs of the putative counterparts from Solanum tuberosum and Arabidopsis thaliana. Upon expression of the corresponding cDNAs from both plants via the secretory pathway of Pichia pastoris, two active QC proteins were isolated. The specificity of the purified proteins was assessed using various substrates with different amino acid composition and length. Highest specificities were observed with substrates possessing large hydrophobic residues adjacent to the N-terminal glutamine and for fluorogenic dipeptide surrogates. However, compared to Carica papaya QC, the specificity constants were approximately one order of magnitude lower for most of the QC substrates analyzed. The QCs also catalyzed the conversion of N-terminal glutamic acid to pyroglutamic acid, but with approximately 105- to 106-fold lower specificity. The ubiquitous distribution of plant QCs prompted a search for potential substrates in plants. Based on database entries, numerous proteins, e.g., pathogenesis-related proteins, were found that carry a pyroglutamate residue at the N-terminus, suggesting QC involvement. The putative relevance of QCs and pyroglutamic acid for plant defense reactions is discussed.
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