Publications

The John Innes Centre Publications Repository contains details of all publications resulting from our researchers.

The repository also includes Open Access publications, which can be identified by the icons found on search results.

 Green open access publications are marked by the PDF icon. Click on the publication title, or the PDF icon, and read a pre-print PDF version of the publication.  Gold open access publications have the gold open padlock icon. You can read the full version of these papers on the publishing journal’s website without a subscription. 

The creation of this publications repository was funded by BBSRC.

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Abstract

Calcium ions are predicted to be key signaling entities during biotic interactions, with calcium signaling forming an established part of the plant defense response to microbial elicitors and to wounding caused by chewing insects, eliciting systemic calcium signals in plants. However, the role of calcium in vivo during biotic stress is still unclear. This protocol describes the use of a genetically-encoded calcium sensor to detect calcium signals in plants during feeding by a hemipteran pest. Hemipterans such as aphids pierce a small number of cells with specialized, elongated sucking mouthparts, making them the ideal tool to study calcium dynamics when a plant is faced with a biotic stress, which is distinct from a wounding response. In addition, fluorescent biosensors are revolutionizing the measurement of signaling molecules in vivo in both animals and plants. Expressing a GFP-based calcium biosensor, GCaMP3, in the model plant Arabidopsis thaliana allows for the real-time imaging of plant calcium dynamics during insect feeding, with a high spatial and temporal resolution. A repeatable and robust assay has been developed using the fluorescence microscopy of detached GCaMP3 leaves, allowing for the continuous measurement of cytosolic calcium dynamics before, during, and after insect feeding. This reveals a highly-localized rapid calcium elevation around the aphid feeding site that occurs within a few minutes. The protocol can be adapted to other biotic stresses, such as additional insect species, while the use of Arabidopsis thaliana allows for the rapid generation of mutants to facilitate the molecular analysis of the phenomenon.

Vincent T. R., Avramova M., Canham J., Higgins P., Bilkey N., Mugford S. T., Pitino M., Toyota M., Gilroy S., Miller A. J., Hogenhout S., Sanders D. (2017)

Interplay of plasma membrane and vacuolar ion channels, together with BAK1, elicits rapid cytosolic calcium elevations in Arabidopsis during aphid feeding.

Plant Cell (Epub ahead of print) Epub ahead of print

Publisher's version: 10.1105/tpc.17.00136

ID: 56585

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Abstract

A transient rise in cytosolic calcium ion concentration is one of the main signals used by plants in perception of their environment. The role of calcium in the detection of abiotic stress is well documented; however, its role during biotic interactions remains unclear. Here, we use a fluorescent calcium biosensor (GCaMP3) in combination with the green peach aphid (Myzus persicae) as a tool to study Arabidopsis thaliana calcium dynamics in vivo and in real time during a live biotic interaction. We demonstrate rapid and highly-localised plant calcium elevations around the feeding sites of M. persicae, and by monitoring aphid feeding behaviour electrophysiologically we demonstrate that these elevations correlate with aphid probing of epidermal and mesophyll cells. Furthermore, we dissect the molecular mechanisms involved, showing that interplay between the plant defence co-receptor BRASSINOSTEROID INSENSITIVE-ASSOCIATED KINASE 1 (BAK1), the plasma membrane ion channels GLUTAMATE RECEPTOR-LIKE 3.3 and 3.6 (GLR3.3 and GLR3.6) and the vacuolar ion channel TWO-PORE CHANNEL 1 (TPC1) mediate these calcium elevations. Consequently, we identify a link between plant perception of biotic threats by BAK1, cellular calcium entry mediated by GLRs, and intracellular calcium release by TPC1 during a biologically relevant interaction.

Menguer P., Vincent T., Miller A. J., Brown J. K. M., Vincze E., Borg S., Holm P. B., Sanders D., Podar D. (2017)

Improving zinc accumulation in barley endosperm using HvMTP1, a transition metal transporter.

Plant Biotechnology Journal (Plant Biotechnol J. 2017 Apr 24. doi: 10.1111/pbi.12749. [Epub ahead of print]) doi: 10.1111/pbi.12749

Publisher's version: 10.1111/pbi.12749

ID: 56109

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Abstract

Zinc (Zn) is essential for all life forms, including humans. It is estimated that around two billion people are deficient in their Zn intake. Human dietary Zn intake relies heavily on plants, which in many developing countries consists mainly of cereals. The inner part of cereal grain, the endosperm, is the part that is eaten after milling but contains only a quarter of the total grain Zn. Here we present results demonstrating that endosperm Zn content can be enhanced through expression of a transporter responsible for vacuolar Zn accumulation in cereals. The barley (Hordeum vulgare) vacuolar Zn transporter HvMTP1 was expressed under the control of the endosperm-specific D-hordein promoter. Transformed plants exhibited no significant change in growth but had higher total grain Zn concentration, as measured by ICP-OES, compared to parental controls. Compared with Zn, transformants had smaller increases in concentrations of Cu and Mn but not Fe. Staining grain cross-sections with the Zn-specific stain DTZ revealed a significant enhancement of Zn accumulation in the endosperm of two of three transformed lines, a result confirmed by ICP-OES in the endosperm of dissected grain. Synchrotron X-ray fluorescence analysis of longitudinal grain sections demonstrated a redistribution of grain Zn from aleurone to endosperm. We argue that this proof-of-principle study provides the basis of a strategy for biofortification of cereal endosperm with Zn. This article is protected by copyright. All rights reserved.

Abstract

Nuclear-associated Ca(2+) oscillations mediate plant responses to beneficial microbial partners--namely, nitrogen-fixing rhizobial bacteria that colonize roots of legumes and arbuscular mycorrhizal fungi that colonize roots of the majority of plant species. A potassium-permeable channel is known to be required for symbiotic Ca(2+) oscillations, but the calcium channels themselves have been unknown until now. We show that three cyclic nucleotide-gated channels in Medicago truncatula are required for nuclear Ca(2+) oscillations and subsequent symbiotic responses. These cyclic nucleotide-gated channels are located at the nuclear envelope and are permeable to Ca(2+) We demonstrate that the cyclic nucleotide-gated channels form a complex with the postassium-permeable channel, which modulates nuclear Ca(2+) release. These channels, like their counterparts in animal cells, might regulate multiple nuclear Ca(2+) responses to developmental and environmental conditions.

Patron N. J., Orzaez D., Marillonnet S., Warzecha H., Matthewman C., Youles M., Raitskin O., Leveau A., Farré G., Rogers C., Smith A., Hibberd J., Webb A. A., Locke J., Schornack S., Ajioka J., Baulcombe D. C., Zipfel C., Kamoun S., Jones J. D., Kuhn H., Robatzek S., Van Esse H. P., Sanders D., Oldroyd G., Martin C., Field R., O'Connor S., Fox S., Wulff B., Miller B., Breakspear A., Radhakrishnan G., Delaux P. M., Loqué D., Granell A., Tissier A., Shih P., Brutnell T. P., Quick W. P., Rischer H., Fraser P. D., Aharoni A., Raines C., South P. F., Ané J. M., Hamberger B. R., Langdale J., Stougaard J., Bouwmeester H., Udvardi M., Murray J. A., Ntoukakis V., Schäfer P., Denby K., Edwards K. J., Osbourn A., Haseloff J. (2015)

Standards for plant synthetic biology: a common syntax for exchange of DNA parts.

New Phytologist (208) 13-9

Publisher's version: 10.1111/nph.13532

ID: 55372

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Abstract

Inventors in the field of mechanical and electronic engineering can access multitudes of components and, thanks to standardization, parts from different manufacturers can be used in combination with each other. The introduction of BioBrick standards for the assembly of characterized DNA sequences was a landmark in microbial engineering, shaping the field of synthetic biology. Here, we describe a standard for Type IIS restriction endonuclease-mediated assembly, defining a common syntax of 12 fusion sites to enable the facile assembly of eukaryotic transcriptional units. This standard has been developed and agreed by representatives and leaders of the international plant science and synthetic biology communities, including inventors, developers and adopters of Type IIS cloning methods. Our vision is of an extensive catalogue of standardized, characterized DNA parts that will accelerate plant bioengineering.

Patron N. J., Orzaez D., Marillonnet S., Warzecha H., Matthewman C., Youles M., Raitskin O., Leveau A., Farré G., Rogers C., Smith A., Hibberd J., Webb A. A., Locke J., Schornack S., Ajioka J., Baulcombe D. C., Zipfel C., Kamoun S., Jones J. D., Kuhn H., Robatzek S., Van Esse H. P., Sanders D., Oldroyd G., Martin C., Field R., O'Connor S., Fox S., Wulff B., Miller B., Breakspear A., Radhakrishnan G., Delaux P. M., Loqué D., Granell A., Tissier A., Shih P., Brutnell T. P., Quick W. P., Rischer H., Fraser P. D., Aharoni A., Raines C., South P. F., Ané J. M., Hamberger B. R., Langdale J., Stougaard J., Bouwmeester H., Udvardi M., Murray J. A., Ntoukakis V., Schäfer P., Denby K., Edwards K. J., Osbourn A., Haseloff J. (2015)

Standards for plant synthetic biology: a common syntax for exchange of DNA parts.

New Phytologist (208) 1319

Publisher's version: 10.1111/nph.13532

ID: 51594

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Abstract

Inventors in the field of mechanical and electronic engineering can access multitudes of components and, thanks to standardization, parts from different manufacturers can be used in combination with each other. The introduction of BioBrick standards for the assembly of characterized DNA sequences was a landmark in microbial engineering, shaping the field of synthetic biology. Here, we describe a standard for Type IIS restriction endonuclease-mediated assembly, defining a common syntax of 12 fusion sites to enable the facile assembly of eukaryotic transcriptional units. This standard has been developed and agreed by representatives and leaders of the international plant science and synthetic biology communities, including inventors, developers and adopters of Type IIS cloning methods. Our vision is of an extensive catalogue of standardized, characterized DNA parts that will accelerate plant bioengineering.

Abstract

Wheat, like many other staple cereals, contains low levels of the essential micronutrients iron and zinc. Up to two billion people worldwide suffer from iron and zinc deficiencies, particularly in regions with predominantly cereal-based diets. Although wheat flour is commonly fortified during processing, an attractive and more sustainable solution is biofortification, which requires developing new varieties of wheat with inherently higher iron and zinc content in their grains. Until now most studies aimed at increasing iron and zinc content in wheat grains have focused on discovering natural variation in progenitor or related species. However, recent developments in genomics and transformation have led to a step change in targeted research on wheat at a molecular level. We discuss promising approaches to improve iron and zinc content in wheat using knowledge gained in model grasses. We explore how the latest resources developed in wheat, including sequenced genomes and mutant populations, can be exploited for biofortification. We also highlight the key research and practical challenges that remain in improving iron and zinc content in wheat.

Schroeder J. I., Delhaize E., Frommer W. B., Guerinot M. L., Harrison M. J., Herrera-Estrella L., Horie T., Kochian L. V., Munns R., Nishizawa N. K., Tsay Y. F., Sanders D. (2013)

Using membrane transporters to improve crops for sustainable food production.

Nature (497) 60-6

Publisher's version: 10.1038/nature11909

ID: 41951

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Podar D., Scherer J., Noordally Z., Herzyk P., Nies D., Sanders D. (2012)

Metal selectivity determinants in a family of transition metal transporters.

Journal of Biological Chemistry (287) 3185-96

Publisher's version: 10.1074/jbc.M111.305649

ID: 39956

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Dodd A. N., Kudla J., Sanders D. (2010)

The language of calcium signaling.

Annual Review of Plant Biology (61) 593-620

Publisher's version: 10.1146/annurev-arplant-070109-104628

ID: 47313

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Abstract

Ca(2+) signals are a core regulator of plant cell physiology and cellular responses to the environment. The channels, pumps, and carriers that underlie Ca(2+) homeostasis provide the mechanistic basis for generation of Ca(2+) signals by regulating movement of Ca(2+) ions between subcellular compartments and between the cell and its extracellular environment. The information encoded within the Ca(2+) transients is decoded and transmitted by a toolkit of Ca(2+)-binding proteins that regulate transcription via Ca(2+)-responsive promoter elements and that regulate protein phosphorylation. Ca(2+)-signaling networks have architectural structures comparable to scale-free networks and bow tie networks in computing, and these similarities help explain such properties of Ca(2+)-signaling networks as robustness, evolvability, and the ability to process multiple signals simultaneously.

Dodd A. N., Kudla J., Sanders D. (2010)

The language of calcium signalling

Annual Reviews in Plant Biology (61) 593-620

ID: 38108

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Uelker B., Peiter E., Dixon D. P., Moffat C., Capper R., Bouche N., Edwards R., Sanders D., Knight H., Knight M. R. (2008)

Getting the most out of publicly available T-DNA insertion lines

Plant Journal (56) 665-677

ID: 38109

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Whiteman S. A., Nuhse T. S., Ashford D. A., Sanders D., Maathuis F. J. M. (2008)

A proteomic and phosphoproteomic analysis of Oryza sativa plasma membrane and vacuolar membrane

Plant Journal (56) 146-156

ID: 38110

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Whiteman S. A., Serazetdinova L., Jones A. M. E., Sanders D., Rathjen J., Peck S. C., Maathuis F. J. M. (2008)

Identification of novel proteins and phosphorylation sites in a tonoplast enriched membrane fraction of Arabidopsis thaliana

Proteomics (8) 3536-3547

ID: 38111

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Palmgren M. G., Clemens S., Williams L. E., Kraemer U., Borg S., Schjorring J. K., Sanders D. (2008)

Zinc biofortification of cereals: problems and solutions

Trends in Plant Science (13) 464-473

ID: 38112

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Peiter E., Montanini B., Gobert A., Pedas P., Husted S., Maathuis F. J. M., Blaudez D., Chalot M., Sanders D. (2007)

A secretory pathway-localised cation diffusion facilitator confers plant manganese tolerance

Proceedings of the National Academy of Sciences of the United States of America (104) 8532-8537

ID: 38117

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Dodd A. N., Gardner M. J., Hotta C. T., Hubbard K. E., Dalchau N., Love J., Assie J. M., Robertson F. C., Jakobsen M. K., Goncalves J., Sanders D., Webb A. A. R. (2007)

The Arabidopsis circadian clock incorporates a cADPR-based feedback loop

Science (318) 1789-1792

ID: 38114

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Peiter E., Sun J., Heckmann A. B., Venkateshwaran M., Riely B. K., Otegui M. S., Edwards A., Freshour G., Hahn M. G., Cook D. R., Sanders D., Oldroyd G. E. D., Downie J. A., Ane J. M. (2007)

The Medicago trunculata DMI1 protein modulates cytosolic calcium signaling

Plant Physiology (145) 192-203

ID: 38115

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Gobert A., Park G., Amtmann A., Sanders D., Maathuis F. J. M. (2006)

Arabidopsis thaliana cyclic nucleotide gated channel 3 forms a non-selective ion transporter involved in germination and cation transport

Journal of Experimental Botany (57) 791-800

ID: 38119

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Moscatiello R., Mariani P., Sanders D., Maathuis F. J. M. (2006)

Transcriptional analysis of calcium-dependent and calcuim-independent signalling pathways induced by oligogalacturonides

Journal of Experimental Botany (57) 2847-2865

ID: 38120

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Cerana M., Bonza M. C., Harris R., Sanders D., De Michelis M. I. (2006)

Abscisic acid stimulates the expression of two isoforms of plasma membrane Ca2+-ATPase in Arabidopsis thaliana seedlings

Plant Biology (8) 572-578

ID: 38122

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Peiter E., Maathuis F. J. M., Mills L. N., Knight H., Pelloux J., Hetherington A. M., Sanders D. (2005)

The vacuolar Ca2+-activated channel TPC1 regulates germination and stomatal movement

Nature (434) 404-408

ID: 38123

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Peiter E., Fischer M., Sidaway K., Roberts S. K., Sanders D. (2005)

The Saccharomyces cerevisiae Ca2+ channel Cch1pMid1p is essential for tolerance to cold stress and iron toxicity

FEBS Letters (579) 5697-5703

ID: 38124

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