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Mechanistic insights into the adaptive plasticity of plant starch metabolism

English title Mechanistic insights into the adaptive plasticity of plant starch metabolism
Applicant Santelia Diana
Number 166539
Funding scheme Project funding
Research institution Institut für Integrative Biologie Departement Umweltsystemwissenschaften ETH Zürich
Institution of higher education ETH Zurich - ETHZ
Main discipline Biochemistry
Start/End 01.08.2016 - 30.09.2019
Approved amount 471'426.00
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All Disciplines (2)

Discipline
Biochemistry
Molecular Biology

Keywords (7)

osmotic stress; phosphoproteomics; guard cells; starch; circadian clock; b-amylase; ABA

Lay Summary (Italian)

Lead
L’amido e’ una delle piu’ abbondanti forme di riserva di carboidrati. L’amido nelle foglie e’ normalmente sintetizzato durante il giorno e degradato durante le notte per sostenere il metabolismo e la crescita della pianta quando la fotosintesi non e’ attiva. La sintesi e la degradazione dell’amido sono molto sensisibili ai cambiamenti nell’ambiente esterno e presentano delle caratteristiche specifiche a seconda del tipo di cellula e tessuto in cui l’amido si trova. L’obiettivo di questa ricerca e’ di rivelare il meccanismo e la regolazione della sintesi e degradazione dell’amido nei diversi tessuti della pianta e in risposta a diversi stimoli ambientali, nonché la sua influenza sulla produttività della pianta e la tolleranza a stress.
Lay summary

L’amido e’ sintetizzato nel plastidi dei tessuti fotosintetici e non fotosintetici, ma il suo metabolismo e la sua funzione dipendono del tipo di tessuto in cui l’amido di trova e dalle condizioni ambientali esterne. Nelle cellule di guardia che circondano i pori stomatici che controllano lo scambio di acqua ed anidride carbonica con l’ambiente esterno, l’amido viene mobilizzato nel giro di pochi minuti, cosi’ aiutando a generare acidi organici e zuccheri che promuovono l’incremento del turgore cellulare e l’apertura degli stomi. Nel resto della foglia, l’amido si accumula generalmente durante il giorno e viene metabolizzato durante la notte per sostenere il metabolismo della pianta. In responsa  a stress osmotico, le piante degradano molto rapidamente l’amido per generare zuccheri solubili che funzionano come protettori osmotici limitando gli effetti negativi dello stress sulla crescita e la produttività della pianta.

Questa abilità di modificare il metabolismo dell’amido a seconda dei bisogni della pianta dipende principalmente dalla diversificazione a livello funzionale tra i membri della famiglia delle b-amilasi (BAM). BAM e’ la piu’ importante idrolasi implicata nella degradazine dell’amido. Il nostro obiettivo principale e’ di identificare i meccanismi molecolari che determinano la specializzazione delle BAM, e la loro influenza sulla funzione delle BAM nel metabolismo dell’amido nei diversi tipi cellulari e in risposta a diversi stimuli ambientali.
Siccome BAM sono molto conservate tra le diverse specie di piante, la nostra ricerca avrà delle implicazioni molto piu’ ampie per la generazione di piante con elevata capacità di adattamento a condizioni ambientali estreme, permettendo di estendere la coltivazioni in terre al momento inaccessibili, assicurando una sufficiente provvigione di cibo per la crescente popolazione mondiale.

Direct link to Lay Summary Last update: 14.12.2016

Responsible applicant and co-applicants

Employees

Publications

Publication
Glucose uptake to guard cells via STP transporters provides carbon sources for stomatal opening and plant growth
Flütsch Sabrina, Nigro Arianna, Conci Franco, Fajkus Jiří, Thalmann Matthias, Trtílek Martin, Panzarová Klára, Santelia Diana (2020), Glucose uptake to guard cells via STP transporters provides carbon sources for stomatal opening and plant growth, in EMBO reports, 21(8), e49719.
Peeling back the layers of crassulacean acid metabolism: functional differentiation between Kalanchoë fedtschenkoi epidermis and mesophyll proteomes
Abraham Paul E., Hurtado Castano Natalia, Cowan‐Turner Daniel, Barnes Jeremy, Poudel Suresh, Hettich Robert, Flütsch Sabrina, Santelia Diana, Borland Anne M. (2020), Peeling back the layers of crassulacean acid metabolism: functional differentiation between Kalanchoë fedtschenkoi epidermis and mesophyll proteomes, in The Plant Journal, 103(2), 869-888.
Guard Cell Starch Degradation Yields Glucose for Rapid Stomatal Opening in Arabidopsis
Flütsch Sabrina, Wang Yizhou, Takemiya Atsushi, Vialet-Chabrand Silvere R. M., Klejchová Martina, Nigro Arianna, Hills Adrian, Lawson Tracy, Blatt Michael R., Santelia Diana (2020), Guard Cell Starch Degradation Yields Glucose for Rapid Stomatal Opening in Arabidopsis, in The Plant Cell, 32(7), 2325-2344.
The evolution of functional complexity within the β-amylase gene family in land plants
Thalmann Matthias, Coiro Mario, Meier Tiago, Wicker Thomas, Zeeman Samuel C., Santelia Diana (2019), The evolution of functional complexity within the β-amylase gene family in land plants, in BMC Evolutionary Biology, 19(1), 66-66.
Salinity in Autumn-Winter Season and Fruit Quality of Tomato Landraces
Moles Tommaso Michele, de Brito Francisco Rita, Mariotti Lorenzo, Pompeiano Antonio, Lupini Antonio, Incrocci Luca, Carmassi Giulia, Scartazza Andrea, Pistelli Laura, Guglielminetti Lorenzo, Pardossi Alberto, Sunseri Francesco, Hörtensteiner Stefan, Santelia Diana (2019), Salinity in Autumn-Winter Season and Fruit Quality of Tomato Landraces, in Frontiers in Plant Science, 10, 1078.
The Thioredoxin-Regulated α-Amylase 3 of Arabidopsis thaliana Is a Target of S-Glutathionylation
Gurrieri Libero, Distefano Luca, Pirone Claudia, Horrer Daniel, Seung David, Zaffagnini Mirko, Rouhier Nicolas, Trost Paolo, Santelia Diana, Sparla Francesca (2019), The Thioredoxin-Regulated α-Amylase 3 of Arabidopsis thaliana Is a Target of S-Glutathionylation, in Frontiers in Plant Science, 10, 933.
Quantification of Starch in Guard Cells of Arabidopsis thaliana
Flütsch Sabrina, Distefano Luca, Santelia Diana (2018), Quantification of Starch in Guard Cells of Arabidopsis thaliana, in BIO-PROTOCOL, 8(13), e2920.

Collaboration

Group / person Country
Types of collaboration
Prof. Atsushi Takemiya, University of Yamaguchi Japan (Asia)
- in-depth/constructive exchanges on approaches, methods or results
- Publication
- Exchange of personnel
Dr. Claudia Jonak, Gregor Mendel Institute of Molecular Plant Biology, Vienna Austria (Europe)
- in-depth/constructive exchanges on approaches, methods or results
- Publication
Prof. Francesca Sparla, University of Bologna Italy (Europe)
- in-depth/constructive exchanges on approaches, methods or results
- Publication
Prof. Tracy Lawson, University of Essex Great Britain and Northern Ireland (Europe)
- in-depth/constructive exchanges on approaches, methods or results
- Publication
Prof. Mike Blatt, University of Glasgow Great Britain and Northern Ireland (Europe)
- in-depth/constructive exchanges on approaches, methods or results
- Publication
- Exchange of personnel

Scientific events

Active participation

Title Type of contribution Title of article or contribution Date Place Persons involved
Photobiology 2019 Talk given at a conference Blue-light-induced guard cell starch degradation is required for fast stomatal opening kinetics 25.08.2019 Barcelona, Spain Santelia Diana;
Keystone Symposia meeting on Climate Change-Linked Stress Tolerance in Plants Talk given at a conference Blue light-induced guard cell starch degradation for fast stomatal opening kinetics 13.05.2019 Hannover, Germany Flütsch Sabrina;
IPMB2018 conference Talk given at a conference Sugar transport to guard cells is required for stomatal opening and plant growth 05.08.2018 Montpellier, France Santelia Diana;
ASPB conference Talk given at a conference Sugar transport to guard cells is required for stomatal opening and plant growth 14.07.2018 Montreal, Canada Santelia Diana;
“Abiotic Stress Tolerance” conference Talk given at a conference Rewiring starch metabolism for abiotic stress tolerance 05.07.2018 Vienna, Austria Santelia Diana;
Gordon Research Conference “Salt and Water Stress in Plants” Talk given at a conference Discussion leader 03.06.2018 Waterville, United States of America Santelia Diana;
Gordon Research Conference “CO2 assimilation in plants from Genome to Biome”. Talk given at a conference Guard cell starch metabolism as a bottleneck for efficient stomatal control 30.04.2017 Lucca, Italy Flütsch Sabrina; Santelia Diana;


Self-organised

Title Date Place
TriNational Arabidopsis meeting 10.04.2019 ETH Zurich, Switzerland
Chloroplast Metabolism and Photosynthesis 26.06.2017 Neuchatel, Switzerland

Knowledge transfer events

Active participation

Title Type of contribution Date Place Persons involved


Associated projects

Number Title Start Funding scheme
147074 Transcriptional and post-translational regulation of Arabidopsis b-amylase 1 during drought stress 01.05.2013 Project funding
185241 Rewiring starch metabolism for plant environmental adaptation 01.10.2019 Project funding

Abstract

Starch is the most abundant form in which plants store carbohydrate. Starch serves functions that range over timescales from minutes to years, according to the cell-type from which it is derived. In guard cells, which border the stomatal pores that control water and carbon dioxide exchange with the environment, starch can be mobilized within minutes, helping to generate organic acid and sugars to increase guard cell turgor and promote stomatal opening. In the rest of the leaf, starch typically accumulates gradually during the day and is metabolized at night to support metabolism. Starch is intimately integrated with plant biology. Rearrangements of starch metabolism occur in response to changes in day length, light intensity, water deficit or extreme temperatures in a cell type-specific manner, such that carbon supply is ultimately optimized to sustain continued growth under changing environmental conditions. Such adaptive plasticity of starch metabolism is a key plant survival strategy. During phase I of this SNF project, we made a new fundamental discovery on how the ability of the plant to adjust starch turnover to the need of the individual cells depends upon sub-functionalization amongst the chloroplastic members of the Arabidopsis b-amylase (BAM) gene family. BAM is the main starch-degrading enzyme. We showed that BAM1 and BAM3 are active under different conditions and in a cell-type specific manner. We identified important upstream components affecting BAM activity, demonstrating that an intricate network of differential transcriptional and post-translational regulation underpins BAM isoform sub-functionalization. This ground breaking and exclusive findings present yet only the tip of the iceberg. Urgent research is needed to expand the frontiers in our knowledge on BAM isoform sub-functionalization and its impact on plant survival under changing environmental conditions. We propose pioneering innovative approaches, ranging from guard cell phosphoproteomics, high-resolution analytical imaging and in vivo radioisotope labelling of protein synthesis and turnover in a mix that is rather unique for my laboratory and will allow us to unravel the underlying molecular mechanisms of such a remarkable adaptive plasticity of starch metabolism in plants. Given that BAM are highly conserved in plants, our work will encourage further investigations on the influence of starch adaptive plasticity on plant survival in the environment in plants with commercial value. This ultimately will have broader implications for the generation of plants with high adaptation to extreme weather conditions, allowing extending the cultivation in fallow lands to ensure food security in the face of the expanding world’s population.
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