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Chlorophyll breakdown: catabolite modification and transport, and the relation to stoma function and cell death signalling

English title Chlorophyll breakdown: catabolite modification and transport, and the relation to stoma function and cell death signalling
Applicant Hörtensteiner Stefan
Number 149389
Funding scheme Project funding (Div. I-III)
Research institution Institut für Pflanzen- und Mikrobiologie Universität Zürich
Institution of higher education University of Zurich - ZH
Main discipline Botany
Start/End 01.05.2014 - 30.06.2017
Approved amount 490'967.00
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Keywords (5)

transport; cell death; catabolite modification; leaf senescence; chlorophyll breakdown

Lay Summary (German)

Lead
Das Projekt untersucht verschiedene Aspekte des Chlorophyllabbaus, der während der Blattalterung in Pflanzen auftritt.
Lay summary

Während der Blattalterung und der Reifung von vielen Früchten bauen Pflanzen Chlorophyll zu einer Klasse von linearen tetrapyrrolischen Pigmenten, sogenannten Phyllobilinen, um. Der Abbau von Chlorophyll beinhaltet eine komplexe Reihe von biochemischen Schritten und erfordert den zellulären Transport verschiedener Abbauprodukte vom Chloroplasten zur Vakuole. Obwohl die meisten der am Chlorophyllabbau beteiligten Enzyme in den letzten Jahren molekular identifiziert werden konnten, bestehen weiterhin unterschiedliche offene Fragen, die innerhalb dieses Forschungsprojekts bearbeitet werden. Diese betreffen einige enzymatische Schritte, den subzellulären Phyllobilintransport und offene Fragen zur Regulation des gesamten Abbauweges.

Direct link to Lay Summary Last update: 19.05.2014

Responsible applicant and co-applicants

Employees

Publications

Publication
Characterization of the pheophorbide a oxygenase/phyllobilin pathway of chlorophyll breakdown in grasses
Das Aditi, Christ Bastien, Hörtensteiner Stefan (2018), Characterization of the pheophorbide a oxygenase/phyllobilin pathway of chlorophyll breakdown in grasses, in Planta, 248(4), 875-892.
A liquid chromatography-mass spectrometry platform for the analysis of phyllobilins, the major degradation products of chlorophyll in Arabidopsis thaliana.
Christ Bastien, Hauenstein Mareike, Hörtensteiner Stefan (2016), A liquid chromatography-mass spectrometry platform for the analysis of phyllobilins, the major degradation products of chlorophyll in Arabidopsis thaliana., in The Plant journal : for cell and molecular biology, 88(3), 505-518.
A Role for TIC55 as a Hydroxylase of Phyllobilins, the Products of Chlorophyll Breakdown during Plant Senescence
Hauenstein Mareike, Christ Bastien, Das Aditi, Aubry Sylvain, Hörtensteiner Stefan (2016), A Role for TIC55 as a Hydroxylase of Phyllobilins, the Products of Chlorophyll Breakdown during Plant Senescence, in The Plant Cell, 28(10), 2510-2527.
Pheophytinase Knockdown Impacts Carbon Metabolism and Nutraceutical Content Under Normal Growth Conditions in Tomato.
Lira Bruno Silvestre, Rosado Daniele, Almeida Juliana, de Souza Amanda Pereira, Buckeridge Marcos Silveira, Purgatto Eduardo, Guyer Luzia, Hörtensteiner Stefan, Freschi Luciano, Rossi Magdalena (2016), Pheophytinase Knockdown Impacts Carbon Metabolism and Nutraceutical Content Under Normal Growth Conditions in Tomato., in Plant & cell physiology, 57(3), 642-53.
Down-regulation of tomato PHYTOL KINASE strongly impairs tocopherol biosynthesis and affects prenyllipid metabolism in an organ-specific manner.
Almeida Juliana, Azevedo Mariana da Silva, Spicher Livia, Glauser Gaétan, vom Dorp Katharina, Guyer Luzia, del Valle Carranza Andrea, Asis Ramón, de Souza Amanda Pereira, Buckeridge Marcos, Demarco Diego, Bres Cécile, Rothan Christophe, Peres Lázaro Eustáquio Pereira, Hörtensteiner Stefan, Kessler Félix, Dörmann Peter, Carrari Fernando, Rossi Magdalena (2016), Down-regulation of tomato PHYTOL KINASE strongly impairs tocopherol biosynthesis and affects prenyllipid metabolism in an organ-specific manner., in Journal of experimental botany, 67(3), 919-34.
Arabidopsis NAC016 promotes chlorophyll breakdown by directly upregulating STAYGREEN1 transcription.
Sakuraba Yasuhito, Han Su-Hyun, Lee Sang-Hwa, Hörtensteiner Stefan, Paek Nam-Chon (2016), Arabidopsis NAC016 promotes chlorophyll breakdown by directly upregulating STAYGREEN1 transcription., in Plant cell reports, 35(1), 155-66.
A Dioxobilin-Type Fluorescent Chlorophyll Catabolite as a Transient Early Intermediate of the Dioxobilin-Branch of Chlorophyll Breakdown in Arabidopsis thaliana.
Süssenbacher Iris, Hörtensteiner Stefan, Kräutler Bernhard (2015), A Dioxobilin-Type Fluorescent Chlorophyll Catabolite as a Transient Early Intermediate of the Dioxobilin-Branch of Chlorophyll Breakdown in Arabidopsis thaliana., in Angewandte Chemie (International ed. in English), 54(46), 13777-81.
Hydroxymethylated Dioxobilins in Senescent Arabidopsis thaliana Leaves: Sign of a Puzzling Biosynthetic Intermezzo of Chlorophyll Breakdown.
Süssenbacher Iris, Kreutz Christoph R, Christ Bastien, Hörtensteiner Stefan, Kräutler Bernhard (2015), Hydroxymethylated Dioxobilins in Senescent Arabidopsis thaliana Leaves: Sign of a Puzzling Biosynthetic Intermezzo of Chlorophyll Breakdown., in Chemistry (Weinheim an der Bergstrasse, Germany), 21(33), 11664-70.
Reexamination of chlorophyllase function implies its involvement in defense against chewing herbivores.
Hu Xueyun, Makita Satoru, Schelbert Silvia, Sano Shinsuke, Ochiai Masanori, Tsuchiya Tohru, Hasegawa Shigeaki F, Hörtensteiner Stefan, Tanaka Ayumi, Tanaka Ryouichi (2015), Reexamination of chlorophyllase function implies its involvement in defense against chewing herbivores., in Plant physiology, 167(3), 660-70.
Water deficit induces chlorophyll degradation via the 'PAO/phyllobilin' pathway in leaves of homoio- (Craterostigma pumilum) and poikilochlorophyllous (Xerophyta viscosa) resurrection plants.
Christ Bastien, Egert Aurélie, Süssenbacher Iris, Kräutler Bernhard, Bartels Dorothea, Peters Shaun, Hörtensteiner Stefan (2014), Water deficit induces chlorophyll degradation via the 'PAO/phyllobilin' pathway in leaves of homoio- (Craterostigma pumilum) and poikilochlorophyllous (Xerophyta viscosa) resurrection plants., in Plant, cell & environment, 37(11), 2521-31.
Arabidopsis STAYGREEN-LIKE (SGRL) promotes abiotic stress-induced leaf yellowing during vegetative growth.
Sakuraba Yasuhito, Kim Dami, Kim Ye-Sol, Hörtensteiner Stefan, Paek Nam-Chon (2014), Arabidopsis STAYGREEN-LIKE (SGRL) promotes abiotic stress-induced leaf yellowing during vegetative growth., in FEBS letters, 588(21), 3830-7.
Chlorophyll degradation: the tocopherol biosynthesis-related phytol hydrolase in Arabidopsis seeds is still missing.
Zhang Wei, Liu Tianqi, Ren Guodong, Hörtensteiner Stefan, Zhou Yongming, Cahoon Edgar B, Zhang Chunyu (2014), Chlorophyll degradation: the tocopherol biosynthesis-related phytol hydrolase in Arabidopsis seeds is still missing., in Plant physiology, 166(1), 70-9.
Different mechanisms are responsible for chlorophyll dephytylation during fruit ripening and leaf senescence in tomato.
Guyer Luzia, Hofstetter Silvia Schelbert, Christ Bastien, Lira Bruno Silvestre, Rossi Magdalena, Hörtensteiner Stefan (2014), Different mechanisms are responsible for chlorophyll dephytylation during fruit ripening and leaf senescence in tomato., in Plant physiology, 166(1), 44-56.
Arabidopsis STAY-GREEN2 is a negative regulator of chlorophyll degradation during leaf senescence.
Sakuraba Yasuhito, Park So-Yon, Kim Ye-Sol, Wang Seung-Hyun, Yoo Soo-Cheul, Hörtensteiner Stefan, Paek Nam-Chon (2014), Arabidopsis STAY-GREEN2 is a negative regulator of chlorophyll degradation during leaf senescence., in Molecular plant, 7(8), 1288-302.
Delayed degradation of chlorophylls and photosynthetic proteins in Arabidopsis autophagy mutants during stress-induced leaf yellowing.
Sakuraba Yasuhito, Lee Sang-Hwa, Kim Ye-Sol, Park Ohkmae K, Hörtensteiner Stefan, Paek Nam-Chon (2014), Delayed degradation of chlorophylls and photosynthetic proteins in Arabidopsis autophagy mutants during stress-induced leaf yellowing., in Journal of experimental botany, 65(14), 3915-25.
Hydroxymethylated phyllobilins: a puzzling new feature of the dioxobilin branch of chlorophyll breakdown.
Süssenbacher Iris, Christ Bastien, Hörtensteiner Stefan, Kräutler Bernhard (2014), Hydroxymethylated phyllobilins: a puzzling new feature of the dioxobilin branch of chlorophyll breakdown., in Chemistry (Weinheim an der Bergstrasse, Germany), 20(1), 87-92.

Collaboration

Group / person Country
Types of collaboration
Prof. B. Kräutler, University of Innsbruck Austria (Europe)
- in-depth/constructive exchanges on approaches, methods or results
- Publication
- Research Infrastructure
- Exchange of personnel
Prof. S. Baginsky, University of Halle Germany (Europe)
- in-depth/constructive exchanges on approaches, methods or results
- Research Infrastructure
Prof. E. Martinoia, Univeristy of Zurich Switzerland (Europe)
- in-depth/constructive exchanges on approaches, methods or results
Dr. Y. Eyal, The Volcani Center Israel (Asia)
- in-depth/constructive exchanges on approaches, methods or results
Dr. C. Ringli, University of Zurich Switzerland (Europe)
- in-depth/constructive exchanges on approaches, methods or results
Prof. N.-C. Paek, Seoul University Korean Republic (South Korea) (Asia)
- in-depth/constructive exchanges on approaches, methods or results
- Publication

Scientific events

Active participation

Title Type of contribution Title of article or contribution Date Place Persons involved
3rd Natural Pigments Conference for South-East Asia Talk given at a conference Chlorophyll breakdown during leaf senescence 22.08.2016 Malang, Indonesia Hörtensteiner Stefan;
Gordon Research Conference on “Chemistry and Biology of Tetrapyrroles” Poster An LC-MS platform for the analysis of phyllobilins, the major degradation products of chlorophyll, in Arabidopsis thaliana 17.07.2016 Salve Regina University, Providence, United States of America Hörtensteiner Stefan;
Yamada Conference on “Dynamics and Regulation of Photosynthesis” Talk given at a conference Chlorophyll breakdown: complexity of chlorophyll catabolite modification 02.11.2015 Nara, Japan Hörtensteiner Stefan;
11th International Conference on “Tetrapyrrole Photoreceptors in Photosynthetic Organisms” Talk given at a conference Chlorophyll breakdown: complexity of chlorophyll catabolite modification 12.10.2015 Hagrashim, Israel Hörtensteiner Stefan;
Gruppenseminar Individual talk Biochemical and molecular analysis of chlorophyll breakdown during plant senescence 24.04.2015 Laimburg, Italy Hörtensteiner Stefan;
7th European Plant Senescence Workshop Talk given at a conference Catabolite modification during chlorophyll breakdown in senescing plants 13.11.2014 Sonderberg, Denmark Peter Noemi; Hörtensteiner Stefan;
Gordon Research Conference on “Mitochondria and Chloroplasts” Talk given at a conference Catabolite modification during chlorophyll breakdown in plants 10.07.2014 Il Ciocco Resort, Luca, Italy Hörtensteiner Stefan;


Associated projects

Number Title Start Funding scheme
132603 Chlorophyll breakdown: analysis of fruit ripening, evolution and regulation 01.01.2011 Project funding (Div. I-III)
157884 Supercritical fluid chromatography tandem mass spectrometry as a new analytical tool for plant sciences 01.06.2015 R'EQUIP
172977 Diversity and evolution of the PAO/phyllobilin pathway of chlorophyll breakdown 01.07.2017 Project funding (Div. I-III)

Abstract

1. Project summary1.1. Background. Chlorophyll (Chl) degradation during leaf senescence and fruit ripening leads to the formation of colorless linear tetrapyrroles. Early reactions of breakdown within plastids are the removal of the hydrophobic phytol chain of Chl by pheophytinase and a porphyrin ring opening reaction, catalyzed by pheophorbide a oxygenase (PAO), that defines the linear tetrapyrrole structure found in the subsequent catabolites. Before import into the vacuole, where they ultimately accumulate, these catabolites are modified at defined positions, e.g. by a commonly occurring hydroxylation at the C8-2 position. 1.2. Working hypothesis. Even though Chl breakdown is rather well understood, different aspects of the pathway, such as catabolite transport within the cell and the mechanism of hydroxylation, are largely unknown. In addition, certain phenotypes of Chl catabolic mutants indicate that Chl breakdown may be related to guard cell function as well as possibly being involved in retrograde signaling. Thus, the following questions can be raised:- What are the molecular transport systems that transport Chl catabolites from plastids to the vacuole?- By which mechanism/enzyme are Chl catabolites hydroxylated?- Is there a link between Chl breakdown and guard cell function?- How does light-independent cell death occur in PAO mutants?1.3. Specific aims. This proposal addresses different aspects of Chl breakdown and has the following aims:- Elucidating the molecular mechanism of Chl catabolite export from plastids- Elucidating the molecular mechanism of Chl catabolite import into the vacuole- Characterizing Chl catabolite hydroxylation- Analyzing whether Chl breakdown plays a role in stomata function- Analyzing light-independent cell death regulation in PAO mutants1.4. Methods. Performing the experiments proposed here involves a variety of molecular, biochemical and analytical methods, such as (i) mutant identification, crossing and analysis, (ii) production of transgenic plants, (iii) expression and enzymatic analysis of enzymes, (iv) chromatographic methods, (v) pigment and protein identification and/or structure analysis techniques, and (vi) confocal microscopy.1.5. Expected value of the proposed project. This proposal addresses a few important aspects of Chl breakdown. The elucidation of transporters will provide molecular insight into intracellular transport mechanism of Chl catabolites and will possibly also elucidate the unknown mechanism of chloroplast export of phytochromobilin, the phytochrome chromophor. Recently, stomata were recognized as being important sites for regulating leaf senescence. The planned research will add to this by elucidating whether/to what extent Chl breakdown in guard cells is important. Finally, this proposal aims at elucidating a cell death signaling mechanism that is related to Chl breakdown and may be triggered by a plastid-localized breakdown intermediate. Thus, the results of this part may add to the highly interesting field of retrograde signaling.
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