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Transcriptional and post-translational regulation of Arabidopsis b-amylase 1 during drought stress

English title Transcriptional and post-translational regulation of Arabidopsis b-amylase 1 during drought stress
Applicant Santelia Diana
Number 147074
Funding scheme Project funding
Research institution Molekulare Pflanzenphysiologie Institut für Pflanzenbiologie Universität Zürich
Institution of higher education University of Zurich - ZH
Main discipline Biochemistry
Start/End 01.05.2013 - 31.07.2016
Approved amount 228'960.00
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All Disciplines (2)

Discipline
Biochemistry
Molecular Biology

Keywords (6)

redox regulation; b-amylase; Drought stress; ABA; starch-maltose; Arabidopsis thaliana

Lay Summary (German)

Lead
Als Antwort auf Trockenstress können Pflanzen Stärkereserven der Blätter in lösliche Zucker umwandeln. Dies erzeugt Energie und führt zur Akkumulation von osmoprotektiven Substanzen, was zusammen die negativen Effekte von Trockenheit auf Wachstum und Ertrag verringert. Die b-amylase 1 (BAM1) von Arabidopsis ist ein Schlüsselenzym dieses stress-induzierten Stärkeabbaus. Das Forschungsziel ist die Identifikation der Kontrollmechanismen der BAM1 Aktivität als Antwort auf Trockenstress.
Lay summary

Transkriptionelle und post-translationale Regulation der b-Amylase 1 aus Arabidopsis unter Trockenstress

Eines der grössten Probleme der Landwirtschaft ist die globale Wasserknappheit, die durch die wachsende Weltbevölkerung und dem Klimawandel verschärft wird. Damit Erträge stabil bleiben ist daher die Entwicklung von salz- und trockenstress resistenten Kulturpflanzen notwendig. Um die negativen Effekte von Stress auf Wachstum und Ertrag zu vermindern, können Pflanzen Stärkereserven in lösliche Zucker umwandeln, was den zentralen Kohlenstoffmetabolismus aufrecht erhält und so zum einen osmoprotektive Substanzen (vor allem Saccharose und Maltose) generiert und zum anderen den pflanzlichen Energiebedarf deckt. Vor kurzem konnten wir zeigen dass die b-Amylase 1 (BAM1) von Arabidopsis, welche Maltose vom nichtreduzierten Ende der Glucanketten der Stärke abspaltet ein Schlüsselenzym im Stress-induzierten Abbau von Stärke ist. Die molekularen Mechanismen, die die BAM1 Aktivität unter Stressbedingungen induzieren sind allerdings weiterhin unbekannt.

Unser Fokus liegt auf der Identifizierung der Kontrollmechanismen der BAM1 Aktivität unter Stressbedingungen. Dabei werden wir die Signalkaskade, die die BAM1 Transkription aktiviert, sowie post-translationale Regulierungsmechanismen untersuchen. Weiterhin werden wir die funktionelle Interaktion mit anderen Enzymen des Stärkeabbaus untersuchen.

Diese Untersuchungen haben das Potenzial neue Faktoren zu identifizieren die Stresssignale mit der Kontrolle des Kohlenhydratstoffwechsels verknüpfen. Veränderungen dieser Faktoren können ein Werkzeug sein um komplexe Stoffwechselwege zu beeinflussen. Mit diesen Untersuchungen an der Modellpflanze Arabidopsis wird es möglich sein auch wirtschaftlich interessante Pflanzen zügig zu verbessern.

Direct link to Lay Summary Last update: 30.04.2013

Responsible applicant and co-applicants

Employees

Publications

Publication
beta-amylase 1 (BAM1) degrades transitory starch to sustain proline biosynthesis during drought stress
Zanella Martina, Borghi Gian Luca, Pirone Claudia, Thalmann Matthias, Pazmino Diana, Costa Alex, Santelia Diana, Trost Paolo, Sparla Francesca (2016), beta-amylase 1 (BAM1) degrades transitory starch to sustain proline biosynthesis during drought stress, in JOURNAL OF EXPERIMENTAL BOTANY, 67(6), 1819-1826.
Blue Light Induces a Distinct Starch Degradation Pathway in Guard Cells for Stomatal Opening
Horrer Daniel, Fluetsch Sabrina, Pazmino Diana, Matthews Jack S. A., Thalmann Matthias, Nigro Arianna, Leonhardt Nathalie, Lawson Tracy, Santelia Diana (2016), Blue Light Induces a Distinct Starch Degradation Pathway in Guard Cells for Stomatal Opening, in CURRENT BIOLOGY, 26(3), 362-370.
Regulation of Leaf Starch Degradation by Abscisic Acid Is Important for Osmotic Stress Tolerance in Plants
Thalmann Matthias, Pazmino Diana, Seung David, Horrer Daniel, Nigro Arianna, Meier Tiago, Koelling Katharina, Pfeifhofer Hartwig W., Zeeman Samuel C., Santelia Diana (2016), Regulation of Leaf Starch Degradation by Abscisic Acid Is Important for Osmotic Stress Tolerance in Plants, in PLANT CELL, 28(8), 1860-1878.
Rethinking Guard Cell Metabolism
Santelia Diana, Lawson Tracy (2016), Rethinking Guard Cell Metabolism, in PLANT PHYSIOLOGY, 172(3), 1371-1392.
Starch Turnover and Metabolism during Flower and Early Embryo Development
Hedhly Afif, Vogler Hannes, Schmid Marc W., Pazmino Diana, Gagliardini Valeria, Santelia Diana, Grossniklaus Ueli (2016), Starch Turnover and Metabolism during Flower and Early Embryo Development, in PLANT PHYSIOLOGY, 172(4), 2388-2402.
Mechanistic Insights into Glucan Phosphatase Activity against Polyglucan Substrates
Meekins David A., Raththagala Madushi, Auger Kyle D., Turner Benjamin D., Santelia Diana, Koetting Oliver, Gentry Matthew S., Kooi Craig W. Vander (2015), Mechanistic Insights into Glucan Phosphatase Activity against Polyglucan Substrates, in JOURNAL OF BIOLOGICAL CHEMISTRY, 290(38), 23361-23370.
New insights into redox control of starch degradation
Santelia Diana, Trost Paolo, Sparla Francesca (2015), New insights into redox control of starch degradation, in CURRENT OPINION IN PLANT BIOLOGY, 25, 1-9.
Arabidopsis thaliana AMY3 Is a Unique Redox- regulated Chloroplastic alpha-Amylase
Seung David, Thalmann Matthias, Sparla Francesca, Abou Hachem Maher, Lee Sang Kyu, Issakidis-Bourguet Emmanuelle, Svensson Birte, Zeeman Samuel C., Santelia Diana (2013), Arabidopsis thaliana AMY3 Is a Unique Redox- regulated Chloroplastic alpha-Amylase, in JOURNAL OF BIOLOGICAL CHEMISTRY, 288(47), 33620-33633.
Starch as a determinant of plant fitness under abiotic stress
Thalmann Matthias, Santelia Diana, Starch as a determinant of plant fitness under abiotic stress, in New Phytologist.

Collaboration

Group / person Country
Types of collaboration
Prof. Francesca Sparla, University of Bologna, Department of Experimental Evolutionary Biology Italy (Europe)
- in-depth/constructive exchanges on approaches, methods or results
- Publication
- Exchange of personnel
Prof. Sam Zeeman, ETH Zürich Switzerland (Europe)
- Publication
- Research Infrastructure
Dr. Bruno Mueller/Institute of Plant Biology, University of Zürich Switzerland (Europe)
- in-depth/constructive exchanges on approaches, methods or results
- Research Infrastructure

Scientific events

Active participation

Title Type of contribution Title of article or contribution Date Place Persons involved
Invited spekaer, by Prof. Felik Kessler, Master seminar University of Neuchatel Individual talk Starch metabolism in guard cells 13.10.2016 Neuchatel, Switzerland Santelia Diana;
Invited speaker by Dr. John Lunn, Max Planck Institute of Molecular Plant Physiology Individual talk Starch metabolism in guard cells 24.08.2016 Potsdam-Golm, Germany Santelia Diana;
Gordon Research Conference “Salt and Water Stress in Plants” Talk given at a conference Mechanistic insights into the adaptive plasticity of plant starch metabolism 29.05.2016 Les Diablerets, Switzerland Santelia Diana;
SwissPlant2016 Talk given at a conference Mechanistic insights into the adaptive plasticity of plant starch metabolism 25.01.2016 Les Diablerets, Switzerland Santelia Diana;
6th World Gene Convention Talk given at a conference The biology of a-amylase 3 and its potential industrial applications 13.11.2015 Qingdao, China Santelia Diana;
Workshop on “Plant Development and Drought stress” by the American Society of Plant Biologists Talk given at a conference Abscisic acid-induced starch degradation confers osmotic stress tolerance in Arabidopsis 01.11.2015 Asilomar, United States of America Santelia Diana;
Invited speaker by Prof. Mike Blatt, University of Glasgow, Institute of Molecular, Cell and Systems Biology Individual talk The unique features of starch metabolism in guard cells and its influence on stomatal movements 09.10.2015 Glasgow, Great Britain and Northern Ireland Santelia Diana;
ASPB Conference Minisymposium Talk given at a conference Starch Degradation Induced by Abscisic Acid Confers Resistance to Osmotic Stress in Arabidopsis thaliana 27.07.2015 Minneapolis, Minnesota, United States of America Thalmann Matthias;
Invited speaker by Prof. Francesco Licausi, Scuola Normale Superiore di Pisa, Institute of Life Sciences Individual talk The unique features of starch metabolism in guard cells and its influence on stomatal movements 04.06.2015 Pisa, Italy Santelia Diana;
Invited speaker by Prof. Uwe Sonnewald, University of Erlangen, Department of Biology Individual talk Blue light induces a unique starch degradation pathway in guard cell chloroplasts to promote stomatal opening 27.03.2015 Erlangen, Germany Santelia Diana;
Plant Biology Winter School 2015 Talk given at a conference ABA triggers a unique pathway of starch degradation in leaves to confer plant tolerance to water deficit 26.02.2015 Bertinoro, Italy Santelia Diana;
Invited speaker by Prof. Tracy Lawson/Christine Raines, University of Essex, Department of Biological Sciences Individual talk Mechanism and regulation of starch degradation in Arabidopsis guard cells and its influence on stomatal opening 14.11.2014 Colchester, Great Britain and Northern Ireland Santelia Diana;
Gordon Research Conference “Salt and Water Stress in Plants” Talk given at a conference Mechanism and regulation of starch degradation in Arabidopsis guard cells and its influence on stomatal opening 03.08.2014 Sunday River Resort (Newry, ME), United States of America Santelia Diana;
Invited speaker by Prof. Hartwig W. Pfeifhofer Individual talk Drought Stress in Mesophytes 27.05.2014 Graz, Austria Thalmann Matthias;
Invited speaker by Prof. Francesca Sparla, University of Bologna, Department of Experimental Evolutionary Biology Individual talk Mechanism and regulation of starch degradation in Arabidopsis guard cells and its influence on stomatal opening 23.04.2014 Bologna, Italy Santelia Diana;
Invited speaker by Prof. Luis Lopez Molina, University of Geneva, Department of Plant Biology Individual talk The role of starch metabolism in drought stress tolerance 22.01.2014 Geneva, Switzerland Santelia Diana;
ALAMY_5 Talk given at a conference The Arabidopsis AtAMY3 is a unique redox-regulated chloroplastic a-amylase 20.10.2013 Smolenice Castle , Slovakia Santelia Diana;


Associated projects

Number Title Start Funding scheme
185241 Rewiring starch metabolism for plant environmental adaptation 01.10.2019 Project funding
166539 Mechanistic insights into the adaptive plasticity of plant starch metabolism 01.08.2016 Project funding
171682 PSC Creative Camps for Youth 01.04.2017 Agora
164086 Imaging of Deep-Lying Tissues with Enhanced Resolution and Sensitivity to Study Plant Development 01.12.2015 R'EQUIP
139645 Arabidopsis guard cell carbon metabolism in response to drought stress 01.02.2012 Marie Heim-Voegtlin grants

Abstract

One of the major challenges facing agriculture today is the global water shortage caused by increasing world population and worldwide climate change. The Intergovernmental Panel on Climate Change (IPCC) has concluded that elevated greenhouse gas concentrations are likely to lead to the general drying of the subtropics by the end of this century, creating widespread drought stress in agriculture (IPCC, 2007). Drought and salinity stress threaten the productivity of most field crops. In general, the primary response of plants to water deficit is the inhibition of shoot growth, allowing cellular essential solutes to be diverted from growth requirements to stress-related functions. However, since this growth arrest decreases plant size and hence limits yield potential, the development of crop plants able to withstand salt and drought stress is critical for yield stability.There is increasing evidence that the rapid mobilization of the starch reserve in the leaves in response to stress represents a short-term mechanism of survival, which aids plant fitness. The degradation of starch into soluble sugars sustains the central carbon metabolism in the production of osmoprotectans (sucrose and maltose) and energy generation, limiting the negative effects of stress on plant growth and yield. Thus, the pathway of starch degradation represents an emerging target for genetic engineering of drought stress tolerance. We have recently obtained solid evidence that the Arabidopsis ß-amylase 1 (BAM1), which releases maltose from the exposed nonreducing ends of glucan chains in starch, is a key enzyme involved in the stress-induced degradation of starch in the light. On the contrary, BAM1 is not required for normal nighttime leaf starch degradation when plants are grown under standard conditions. Among the different Arabidopsis ß-amylase isoforms (nine in total), BAM1 is unique in that it displays a very peculiar gene expression profile and is the only one to be redox regulated, possibly explaining why BAM1 has a critical role in starch metabolism only under certain conditions. Up till now, however, the molecular mechanisms that integrate such a multiple level of regulation are poorly characterized and their physiological relevance for BAM1 function in planta has not been investigated. The research we propose will focus on the characterization, at the molecular and biochemical level, of the mechanisms driving BAM1 activity in response to stress, including transcriptional regulation, post-translational modifications, and the functional interaction of BAM1 with other proteins of the starch degradation pathway. The work described in this proposal will take a combination of in vivo and in vitro approaches. The identification of Trans-regulatory elements involved in BAM1 transcriptional regulation will mainly take advantage of the Arabidopsis protoplasts transactivation assay, in combination with other standard methods, such as electrophoresis mobility shift assay and chromatin immunoprecipitation. In addition, we will generate a set of transgenic plants and multiple bam1 mutant combinations for in depth molecular phenotyping, including the analysis of carbon partitioning by “pulse-chase” 14CO2-labelling experiments, starch and sugars accumulation, gene expression levels and enzyme activities. These investigations have the potential to identify, for the first time, novel factors linking stress signaling and the control of carbohydrate metabolism. The manipulation of these factors is a powerful tool for bioengineering complex metabolic pathways in plants.
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