Martin-Luther-Universität Halle-Wittenberg

Plant Nutrition 2019

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Prof. Dr. Edgar Peiter

Research interests

  • Membrane transport
  • Calcium signalling
  • Manganese nutrition
  • Stress responses
  • Symbiotic nitrogen fixation

Publications

Articles in peer-reviewed journals

Bhattacharyya S, Giridhar M, Meier B, Peiter E, Vothknecht UC, Chigri F (2023). Global transcriptome profiling reveals root- and leaf-specific responses of barley (Hordeum vulgare L.) to H2O2. Frontiers in Plant Science 14, 1223778.

Manh MB, Ost C, Peiter E, Hause B, Krupinska K, Humbeck K (2023). WHIRLY1 acts upstream of ABA-related reprogramming of drought-induced gene expression in barley and affects stress-related histone modifications. International Journal of Molecular Sciences 24, 6326.

Alejandro S, Meier B, Hoang MTT, Peiter E (2023). Cation Diffusion Facilitators of Beta vulgaris reveal diversity of metal handling in dicotyledons. Plant, Cell and Environment 46, 1629-1652.

Kabir AH, Ela EJ, Bagchi R, Rahman MA, Peiter E, Lee K-W (2023). Nitric oxide acts as an inducer of Strategy-I responses to increase Fe availability and mobilization in Fe-starved broccoli (Brassica oleracea var. oleracea). Plant Physiology and Biochemistry 194, 182-192.

Seppelt R, Klotz S, Peiter E, Volk M (2022). Agriculture and food security under a changing climate: An underestimated challenge. iScience 25, 105551.

He J, Yang B, Hause G, Rössner N, Peiter-Volk T, Schattat M, Voiniciuc C, Peiter E (2022). The trans-Golgi-localized protein BICAT3 regulates subcellular manganese allocation and matrix polysaccharide biosynthesis. Plant Physiology 190, 2579-2600.

Olt P, Alejandro S, Fermum J, Ramos E, Peiter E, Ludewig, U (2022). The vacuolar transporter LaMTP8.1 detoxifies manganese in leaves of Lupinus albus. Physiologia Plantarum174, e13807.

Fu D, Zhang Z, Wallrad L, Wang Z, Höller S, Ju C, Schmitz-Thom I, Huang P, Peiter E, Kudla J, Wang C (2022). Ca2+-dependent phosphorylation of NRAMP1 by CPK21 and CPK23 facilitates manganese uptake and homeostasis in Arabidopsis. Proceedings of the National Academy of Sciences of the USA 119, e2204574119.

Oliveira-Garcia E, Aliyeva-Schnorr L, De Oliveira Silva A, El Din Ghanem S, Thor K, Peiter E, Deising HB (2022). The small Ras superfamily GTPase Rho4 of the maize anthracnose fungus Colletotrichum graminicola is required for β-1,3-glucan synthesis, hyphal cell wall integrity, and full virulence. Journal of Fungi 8, 997.

Giridhar M, Meier B, Imani J, Kogel K-H, Peiter E, Vothknecht UC,  Chigri F (2022). Comparative analysis of stress-induced calcium signals  in the crop species barley and the model plant Arabidopsis thaliana. BMC Plant Biology 22, 447.

Cai Y, Lehmann F, Peiter E, Chen S, Zhu J, Hinderberger D, Binder WH (2022). Bergman cyclization of main-chain enediyne polymers for enhanced DNA-cleavage. Polymer Chemistry 13, 3412-3421.

Steinfurth K, Börjesson G, Denoroy P, Eichler-Löbermann B, Gans W, Heyn J, Hirte J, Huyghebaerth B, Jouany C, Koch D, Merbach I, Mokry M, Mollier A, Morel C, Panten K, Peiter E, Poulton PR, Reitz T, Holton Rubæk G, Spiegel H, van Laak M, von Tucher S, Buczko U (2022). Thresholds of target phosphorus fertility classes in European fertilizer recommendations in relation to critical soil test phosphorus values derived from the analysis of 55 European long-term field experiments. Agriculture, Ecosystems and Environment 332, 107926.

Höller S, Küpper H, Brückner D, Garrevoet J, Spiers K, Falkenberg G, Andresen E, Peiter E (2022). Overexpression of METAL TOLERANCE PROTEIN8 reveals new aspects of metal transport in Arabidopsis thaliana seeds. Plant Biology 24, 23-29.

He J, Rössner N, Hoang MTT, Alejandro S, Peiter E (2021). Transport,  functions, and interactions of calcium and manganese in plant organellar  compartments. Plant Physiology 187, 1940-1972.

Kailasam S, Peiter E (2021). A path toward concurrent biofortification and cadmium mitigation in plant-based foods. New Phytologist 232, 17-24.

Malabarba J, Meents A, Reichelt M, Scholz S, Peiter E, Rachowka J, Konopka-Postupolska D, Wilkins K, Davies J, Oelmüller R, Mithöfer A (2021). ANNEXIN1 mediates calcium-dependent systemic defense in Arabidopsis plants upon herbivory and wounding. New Phytologist 231, 243-254.

Alejandro S, Höller S, Meier B, Peiter E (2020). Manganese in plants: from acquisition to subcellular allocation. Frontiers in Plant Science 11, 300.

Lange M, Peiter E (2020). Calcium transport proteins in fungi: the phylogenetic diversity of their relevance for growth, virulence, and stress resistance. Frontiers in Microbiology 10, 3100.

Rissel D, Peiter E (2019). Poly(ADP-ribose) polymerases in plants and their human counterparts: parallels and peculiarities. International Journal of Molecular Sciences 20, 1638.

Wiegmann M, Thomas WTB, Bull HJ, Flavell AJ, Zeyner A, Peiter E, Pillen K, Maurer A (2019). Wild barley serves as a source for biofortification of barley grains. Plant Science 283, 83-94.

Frank J, Happeck R, Meier B, Hoang MTT, Stribny J, Hause G, Ding H, Morsomme P, Baginsky S, Peiter E (2019). Chloroplast-localized BICAT proteins shape stromal calcium signals and are required for efficient photosynthesis. New Phytologist 221, 866-880.

van Laak M, Klingenberg U, Peiter E, Reitz T, Zimmer D, Buczko U (2018). The equivalence of the Calcium-Acetate-Lactate and Double-Lactate extraction methods to assess soil phosphorus fertility. Journal of Plant Nutrition and Soil Science 181, 795–801.

Tavares RG, Lakshmanan P, Peiter E, O’Connell A,  Caldana C, Vicentini R, Sérgio JS, Menossi M (2018). ScGAI is a key  regulator of culm development in sugarcane. Journal of Experimental Botany 69, 3823-3837.

Ding H, He J, Wu Y, Wu X, Ge C, Wang Y, Zhong S, Peiter E, Liang J, Xu W (2018). Tomato mitogen-activiated protein kinase SlMPK1 targeting the serine/proline-rich protein SlSPR1 functions as a negative regulator in high temperature stress. Plant Physiology 177, 633-651.

Robbins C, Thiergart T, Hacquard S, Garrido-Oter R, Gans W, Peiter E, Schulze-Lefert P, Spaepen S (2018). Root-associated bacterial and fungal community profiles of Arabidopsis thaliana are robust across contrasting soil P levels. Phytobiomes 2, 24-34.

Andresen E, Peiter E, Küpper H (2018). Trace metal metabolism in plants. Journal of Experimental Botany 69, 909-954.

Buczko U, van Laak M, Eichler-Löbermann B, Gans W, Merbach I, Panten K, Peiter E, Reitz T, Spiegel H, von Tucher S (2018). Re-evaluation of the yield responses to phosphorus fertilization based on meta-analyses of long-term field experiments. Ambio 47 (Suppl. 1), S50-S61.

Eroglu S, Giehl R, Meier B, Takahashi M, Terada Y, Ignatyev K, Andresen E, Küpper H, Peiter E, von Wirén N (2017). Metal Tolerance Protein 8 mediates manganese homeostasis and iron re-allocation during seed development and germination. Plant Physiology174, 1633-1647.

Rissel D, Heym PP, Peiter E (2017). A yeast growth assay to characterize plant poly(ADP-ribose) polymerase (PARP) proteins and inhibitors. Analytical Biochemistry 527, 20-23.

Müller A, Ngwene B, Peiter E, George E (2017). Quantity and distribution of arbuscular mycorrhizal fungal spore formation within dead roots. Mycorrhiza 27, 201-210.

Rissel D, Heym PP, Thor K, Brandt W, Wessjohann LA, Peiter E (2017). No silver bullet: Canonical Poly(ADP-Ribose) Polymerases  (PARPs) are no universal factors of abiotic and biotic stress resistance  of Arabidopsis thaliana. Frontiers in Plant Science 8, 59.

Peiter E (2016). The ever-closer union of signals: Propagating waves of calcium and ROS are inextricably linked. Plant Physiology 172, 3-4.

Lange M, Weihmann F, Schliebner I, Horbach R, Deising HB, Wirsel SGR, Peiter E (2016). The Transient Receptor Potential (TRP) channel family in Colletotrichum graminicola: a molecular and physiological analysis. PLOS ONE 11, e0158561.

Lange M, Peiter E (2016). Cytosolic free calcium dynamics as related to hyphal and colony growth in the filamentous fungal pathogen Colletotrichum graminicola. Fungal Genetics and Biology 91, 55-65.

Zhao Y, Yan H, Happeck R, Peiter-Volk T, Xu H, Zhang Y, Peiter E, van Oostende C, Whiteway M, Jiang L (2016). Rch1 is a negative regulator of cytosolic calcium homeostasis and positively regulated by calcineurin in budding yeast. European Journal of Cell Biology 95, 164-174.

Schilling G, Eißner H, Schmidt L, Peiter E (2016). Yield formation of five crop species under water shortage and differential potassium supply. Journal of Plant Nutrition and Soil Science 179, 234-243.

Eroglu S, Meier B, von Wirén N, Peiter E (2016). The vacuolar manganese transporter MTP8 determines tolerance to iron deficiency-induced chlorosis in Arabidopsis. Plant Physiology 170, 1030-1045.

Kiep V, Vadassery J, Lattke J, Maaß, J-P, Boland W, Peiter E, Mithöfer A (2015). Systemic cytosolic Ca2+ elevation is activated upon wounding and herbivory in Arabidopsis. New Phytologist 207, 996-1004.

Thor K, Peiter E (2014). Cytosolic calcium signals elicited by the pathogen-associated molecular pattern flg22 in stomatal guard cells are of an oscillatory nature. New Phytologist 204, 873-881.

Lange M, Oliveira-Garcia E, Deising HB, Peiter E (2014). A modular plasmid system for protein co-localization and bimolecular fluorescence complementation in filamentous fungi. Current Genetics 60, 343-350.

Rissel D, Losch J, Peiter E (2014). The nuclear protein Poly(ADP-ribose) polymerase 3 (AtPARP3) is required for seed storability in Arabidopsis thaliana. Plant Biology 16, 1058-1064.

Zörb C, Senbayram M, Peiter E (2014). Potassium in agriculture - status and perspectives. Journal of Plant Physiology 171, 656-669.

Lange M, Müller C, Peiter E (2014). Membrane-assisted culture of fungal mycelium on agar plates for RNA extraction and pharmacological analyses. Analytical Biochemistry 453, 58-60.

Demaegd D, Foulquier F, Colinet A-S, Gremillon L, Legrand D, Mariot P, Peiter E, van Schaftingen E, Matthijs G, Morsomme P (2013). A newly characterized Golgi-localized family of proteins is involved in calcium and pH homeostasis in yeast and human cells. Proceedings of the National Academy of Sciences USA 110, 6859-6864.

Peiter E (2011). The plant vacuole: emitter and receiver of calcium signals. Cell Calcium 50, 120-128.

Ülker B, Peiter E, Dixon DP, Moffat C, Capper R, Bouché N, Edwards R, Sanders D, Knight H, Knight MR (2008). Getting the most out of publicly available T-DNA insertion lines. The Plant Journal 56, 665-677.

Peiter E, Sun J, Heckmann AB, Venkateshwaran M, Riley BK, Otegui MJ, Edwards A, Freshour G, Hahn MG, Cook DR, Sanders D, Oldroyd GED, Downie JA, Ané J-M (2007). The Medicago truncatula DMI1 protein modulates cytosolic Ca2+ signaling. Plant Physiology 145, 192-203.

Peiter E, Montanini B, Gobert A, Pedas P, Husted S, Maathuis FJM, Blaudez D, Chalot M, Sanders D (2007). A secretory pathway-localized cation diffusion facilitator confers plant manganese tolerance. Proceedings of the National Academy of Sciences USA 104, 8532-8537.

Peiter E, Fischer M, Sidaway K, Roberts SK, Sanders D (2005). The Saccharomyces cerevisiae Ca2+ channel Cch1pMid1p is essential for tolerance to cold stress and iron toxicity. FEBS Letters 579, 5697-5703.

Peiter E, Maathuis FJM, Mills LN, Knight H, Pelloux J,Hetherington AM, Sanders D (2005). The vacuolar Ca2+-activated channel TPC1 regulates germination and stomatal movement. Nature 434, 404-408.

Peiter E, Yan F, Schubert S (2004). Amino acid export from infected cells of Vicia faba root nodules: Evidence for an apoplastic step in the infected zone. Physiologia Plantarum 122, 107-114.

Peiter E
, Schubert S (2003). Sugar uptake and proton release by protoplasts from the infected zone of Vicia faba L. nodules: evidence against apoplastic sugar supply of infected cells. Journal of Experimental Botany 54, 1691-1700.

Peiter E, Imani J, Yan F, Schubert S (2003). A novel procedure for gentle isolation and separation of intact infected and uninfected protoplasts from the central tissue of Vicia faba L. nodules. Plant, Cell and Environment 26, 1117-1126.

Hartmann K, Peiter E, Koch K, Schubert S, Schreiber L (2002). Chemical composition and ultrastructure of broad bean (Vicia faba L.) nodule endodermis in comparison to the root endodermis. Planta 215, 14-25.

Peiter E, Yan F, Schubert S (2001). Proteoid root formation of Lupinus albus L. is triggered by high pH of the root medium. Journal of Applied Botany 75, 50-52.

Peiter E, Yan F, Schubert S (2001). Lime-induced growth depression in Lupinus species: Are soil pH and bicarbonate involved? Journal of Plant Nutrition and Soil Science 164, 165-172.

Abd-Alla MH, Koyro H-W, Yan F, Schubert S, Peiter E (2000). Functional structure of the indeterminate Vicia faba L. root nodule: implications for metabolite transport. Journal of Plant Physiology 157, 335-343.

Peiter E, Yan F, Schubert S (2000). Are mineral nutrients a critical factor for lime intolerance of lupins? Journal of Plant Nutrition 23, 617-635.

Book chapters

Seppelt R, Klotz S, Peiter E, Volk M (2022). Landwirtschaft in einer heißen Welt. In: Klaus Wiegand (ed.). Drei Grad mehr. Oekom Verlag, München, Germany. ISBN 978-3-96238-369-5. pp. 55-78.

Peiter E (2014). Mineral requirement and insufficiencies.
In: G-J Krauss, DH Niess (eds.). Ecological Biochemistry - Environmental and Interspecies Interactions. Wiley-VCH, Weinheim, Germany. ISBN 978-3-527-31650-2. pp. 209-222.


CV

since 2008Professor of Plant Nutrition at MLU Halle-Wittenberg
2002-2007Postdoctoral Research Fellow, Biology Department, University of York (UK)
2002Dr.agr., Justus Liebig University of Giessen (Germany)
1997-2002Postgraduate Research Fellow, Institute of Plant Nutrition, Justus Liebig University of Giessen
1997Diplom-Ingenieur sc. agr., University of Hohenheim (Germany)
1994-1997Graduate studies in Crop Science, University of Hohenheim
1993-1994Visiting student, University College of Wales, Aberystwyth (UK)
1991-1993Undergraduate studies in Agricultural Sciences, University of Hohenheim

Awards

2004Dissertation Award, German Society of Plant Nutrition

Research biography

My past and current research as a plant scientist has revolved around the interaction of plants with their abiotic and biotic environment, with an emphasis on plant nutrition.

  • Graduate period

After having acquired a strong background in agronomy during undergraduate studies at the University of Hohenheim (Germany), I spent a year at the University College of Wales at Aberystwyth (UK), focusing mainly on aspects of plant (eco‑)physiology and soil chemistry. Since plant-soil relationships were also the main emphasis of my subsequent graduate studies in Crop Science at the University of Hohenheim, my Diploma project addressed the poorly understood mechanism of growth depression of lupins by alkaline soil conditions. Lupins are a promising high-protein pulse crop. However, their absolute requirement for acidic soils is a major drawback. We were able to show that mineral element toxicities or deficiencies (including iron) are not a major factor in growth depression by soil alkalinity. Furthermore, we demonstrated that not high pH per se, but rather an increased buffering capacity is detrimental to lupin root development on alkaline soils, presumably acting via a mechanism involving carboxylate metabolism. An interesting by-product of these studies was the finding that high pH and buffering capacity interfere in the induction and development of proteiod roots of Lupinus albus, which are highly efficient in the acquisition of phosphate from infertile soils.

  • Postgraduate period

After graduation I directed my interest to transport processes in symbiotic nitrogen fixation. Low-input cropping systems in developing countries and "organic" farming practices largely rely on nitrogen input through legumes, which harbour N2-fixing bacteria in root nodules. Despite the importance of N2 fixation, it is poorly understood how metabolites move within nodules. Because the mode of transport is believed to be crucial for the efficiency of symbiotic N­2 fixation we first investigated the morphology of indeterminate nodules with respect to transport pathways. Those histological studies revealed a high symplastic connectivity between vascular bundles and infected cells and the presence of two endodermal barrier layers in the nodule cortex. A combination of microscopic and advanced analytical techniques further revealed novel features of the nodule vascular endodermis (e.g. polarity of suberin lamellae formation), of the outer nodule endodermis (e.g. extremely high suberin content and localised passage cells), and of the nodule outer cortex (e.g. high triterpenoid content). Transport of metabolites within the central tissue of the nodule may involve loading and unloading of cells via transporters in the plasma membrane. To determine transport activity, a novel protocol for isolation and separation of protoplasts from the central nodule tissue was developed. This enabled us to obtain highly purified fractions of intact infected and uninfected cells. Infected protoplasts, in contrast to non-infected ones, did not actively accumulate sugars, indicating that infected cells rely on uninfected cells for carbon supply. Studies on excised infected tissue and protoplasts further revealed an apoplastic step in amino acid export from infected cells and a retrieval system located in uninfected cells.

  • Postdoctoral period

As postdoctoral research fellow at the Biology Department of the University of York I focussed on cation transport across biological membranes. A central theme of my work was the molecular basis of calcium transport and signalling. Calcium serves as a universal second messenger not only in plants, but in all higher organisms. A wide variety of stimuli (e.g., biotic and abiotic stresses) trigger elevations of cytosolic free calcium that evoke stimulus-specific downstream responses. Generation of these calcium signals is effected through opening of Calcium-permeable ion channels that catalyse a flux of calcium into the cytosol from the extracellular space or from intracellular stores.

A vacuolar calcium-permeable channel
Although many classes of calcium-permeable channels have been characterised electrophysiologically in plant membranes, the molecular identity of the proteins underlying these currents is largely obscure. We therefore aimed to identify plant calcium channel proteins using a candidate gene approach. Database searches revealed a plant membrane protein, TPC1, which is homologous to the yeast Cch1 protein and to the pore-forming subunit of animal voltage-gated calcium channels. Expression of TPC1 in a yeast mutant deleted in a plasma membrane calcium channel (cch1Dmid1D) partially restored calcium influx, indicating TPC1 may be a calcium channel. Using GFP fusion and immunological methods, we demonstrated that TPC1 is targeted to the vacuolar membrane in plants. Subsequent electrophysiological analysis demonstrated that the TPC1 gene encodes a class of calcium-dependent calcium release channel that has been known from numerous electrophysiological studies as the Slow Vacuolar (SV) channel. SV channels are ubiquitous in plant vacuoles, where they form the dominant cation conductance. We showed that a tpc1 knockout mutant lacks functional SV channel activity and is defective in both abscisic acid-induced repression of seed germination and in the response of stomata to extracellular calcium. These findings unequivocally demonstrated for the first time a critical role of intracellular Ca2+ release channels in physiological processes of plants.

Role of calcium channels in yeast
Besides being a tool for heterologous expression, yeast is an excellent eucaryotic model system and has been used to dissect a number of signalling and developmental pathways present in higher eukaryotes. A characterisation of the cch1Dmid1D yeast mutant revealed a role of the Cch1Mid1 Ca2+ channel in survival of various environmental stresses, such as iron toxicity and low temperature. This was the first demonstration that iron stress induces a calcium influx, which is essential for cell survival. We further showed that iron sensitivity of the yeast mutant is not due to excessive iron uptake, but rather linked to an increased oxidative poise during iron stress. Our findings on the yeast system are likely to have implications for biomedical research (Iron toxicity is involved in various neurodegenerative diseases.) and also for plant science (Iron toxicity occurs on waterlogged soils).

Calcium signalling in nodulation
A well-described calcium-dependent process is the initiation of nodules on legume roots. In this symbiotic interaction, bacteria-derived Nod factors induce regular calcium spikes in and around the nucleus. Those calcium spikes are decoded by a calcium- and calmodulin-dependent kinase, and are essential for downstream processes leading to the development of a nodule. Previously the DMI1 gene (DOESN`T MAKE INFECTIONS1) had been shown to be required for the generation of Nod factor-induced calcium spikes. By examining full-length and truncated versions of this gene we were able to show that DMI1 is able to regulate calcium channels in both plants and yeast through an unknown mechanism.

Manganese detoxification
Manganese shares many similarities with calcium and may be able to interfer in calcium signalling. Furthermore, manganese toxicity is a major problem for plant growth on acidic soils. However, cellular mechanisms that facilitate growth in such conditions have not been clearly delineated. We have identified a member of the Cation Diffusion Facilitator (CDF/MTP) family, MTP11, from Arabidopsis and poplar that is able to restore manganese tolerance to a manganese-hypersensitive yeast mutant. In accord with a presumed function of this protein in manganese tolerance, Arabidopsis mtp11 mutants are hypersensitive to elevated levels of manganese, whereas plants overexpressing MTP11 are hypertolerant. Imaging of MTP11-EYFP fusions demonstrated that MTP11 localizes neither to the plasma membrane nor to the vacuole, but to a punctate endomembrane compartment that largely coincides with a Golgi marker. Golgi-based manganese accumulation might therefore result in manganese tolerance through vesicular trafficking and exocytosis. In accord with this, Arabidopsis mtp11 mutants exhibit enhanced manganese concentrations in shoots and roots. These findings provide strong evidence that Golgi-mediated exocytosis comprises a conserved route for heavy metal tolerance in plants. Our improved understanding of the molecular mechanisms underlying manganese tolerance may form a basis for the design of manganese-tolerant crops.

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