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Diversity and evolution of the PAO/phyllobilin pathway of chlorophyll breakdown

English title Diversity and evolution of the PAO/phyllobilin pathway of chlorophyll breakdown
Applicant Zipfel Cyril
Number 172977
Funding scheme Project funding
Research institution Institut für Pflanzen- und Mikrobiologie Universität Zürich
Institution of higher education University of Zurich - ZH
Main discipline Botany
Start/End 01.07.2017 - 30.06.2022
Approved amount 856'592.00
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Keywords (6)

evolution; leaf senescence; seed maturation; pathway diversity; chlorophyll breakdown; phyllobilin

Lay Summary (German)

Lead
Lead: Das Projekt untersucht biochemische, molekulare und evolutionäre Aspekte des Chlorophyllabbaus, der während der Blattalterung und Fruchtreife in Pflanzen auftritt.
Lay summary

Während der Blattalterung und der Reifung von vielen Früchten bauen Pflanzen Chlorophyll zu einer Klasse von linearen tetrapyrrolischen Stoffen, sogenannten Phyllobilinen, ab. Der Abbau von Chlorophyll beinhaltet eine komplexe Reihe von biochemischen Reaktionen, die man in zwei Abschnitte einteilen kann, und erfordert den zellulären Transport der Phyllobiline vom Chloroplasten zur Vakuole. Obwohl die meisten der am Chlorophyllabbau beteiligten Enzyme in den letzten Jahren molekular identifiziert werden konnten, bestehen offene Fragen in Bezug auf (i) einige enzymatische Schritte des zweiten Teils des Abbauweges, (ii) Modulationen des Abbaus in unterschiedlichen Geweben einer Pflanze, (iii) den Grad der Variabilität des Abbaus innerhalb der Angiospermen und (iv) den evolutionären Ursprung und die phylogenetische Diversität der Enzyme des Abbaus. Das Ziel dieses Projekts ist es, diese Fragen zu klären.

Direct link to Lay Summary Last update: 16.06.2017

Responsible applicant and co-applicants

Employees

Publications

Publication
Evolution of chlorophyll degradation is associated with plant transition to land
Schumacher Isabel, Menghini Damian, Ovinnikov Serguei, Hauenstein Mareike, Fankhauser Niklaus, Zipfel Cyril, Hörtensteiner Stefan, Aubry Sylvain (2022), Evolution of chlorophyll degradation is associated with plant transition to land, in The Plant Journal, 109(6), 1473-1488.
De novo transcriptome assembly data of the marine bioluminescent dinoflagellate Pyrocystis lunula
Menghini Damian, Aubry Sylvain (2021), De novo transcriptome assembly data of the marine bioluminescent dinoflagellate Pyrocystis lunula, in Data in Brief, 37, 107254-107254.
An evergreen mind and a heart for the colors of fall
Aubry Sylvain, Christ Bastien, Kräutler Bernhard, Martinoia Enrico, Thomas Howard, Zipfel Cyril (2021), An evergreen mind and a heart for the colors of fall, in Journal of Experimental Botany, 72(13), 4625-4633.
Pheophorbide a May Regulate Jasmonate Signaling during Dark-Induced Senescence
Aubry Sylvain, Fankhauser Niklaus, Ovinnikov Serguei, Pružinská Adriana, Stirnemann Marina, Zienkiewicz Krzysztof, Herrfurth Cornelia, Feussner Ivo, Hörtensteiner Stefan (2020), Pheophorbide a May Regulate Jasmonate Signaling during Dark-Induced Senescence, in Plant Physiology, 182(2), 776-791.
Subcellular localization of chlorophyllase2 reveals it is not involved in chlorophyll degradation during senescence in Arabidopsis thaliana
Hu Xueyun, Jia Ting, Hörtensteiner Stefan, Tanaka Ayumi, Tanaka Ryouichi (2020), Subcellular localization of chlorophyllase2 reveals it is not involved in chlorophyll degradation during senescence in Arabidopsis thaliana, in Plant Science, 290, 110314-110314.
The C-terminal cysteine-rich motif of NYE1/SGR1 is indispensable for its function in chlorophyll degradation in Arabidopsis
Xie Zuokun, Wu Shengdong, Chen Junyi, Zhu Xiaoyu, Zhou Xin, Hörtensteiner Stefan, Ren Guodong, Kuai Benke (2019), The C-terminal cysteine-rich motif of NYE1/SGR1 is indispensable for its function in chlorophyll degradation in Arabidopsis, in Plant Molecular Biology, 101(3), 257-268.
Cryptic chlorophyll breakdown in non-senescent green Arabidopsis thaliana leaves
Süssenbacher Iris, Menghini Damian, Scherzer Gerhard, Salinger Kathrin, Erhart Theresia, Moser Simone, Vergeiner Clemens, Hörtensteiner Stefan, Kräutler Bernhard (2019), Cryptic chlorophyll breakdown in non-senescent green Arabidopsis thaliana leaves, in Photosynthesis Research, 142(1), 69-85.
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.
Mutations in the Arabidopsis ROL17/isopropylmalate synthase 1 locus alter amino acid content, modify the TOR network, and suppress the root hair cell development mutant lrx1
Schaufelberger Myriam, Galbier Florian, Herger Aline, de Brito Francisco Rita, Roffler Stefan, Clement Gilles, Diet Anouck, Hörtensteiner Stefan, Wicker Thomas, Ringli Christoph (2019), Mutations in the Arabidopsis ROL17/isopropylmalate synthase 1 locus alter amino acid content, modify the TOR network, and suppress the root hair cell development mutant lrx1, in Journal of Experimental Botany, 70(8), 2313-2323.
Chlorophyll breakdown—Regulation, biochemistry and phyllobilins as its products
Hörtensteiner Stefan, Hauenstein Mareike, Kräutler Bernhard (2019), Chlorophyll breakdown—Regulation, biochemistry and phyllobilins as its products, Elsevier, Advances in Botanical Research, 213-271.
Inhibition of bacteriochlorophyll biosynthesis in the purple phototrophic bacteria Rhodospirillumrubrum and Rhodobacter capsulatus grown in the presence of a toxic concentration of selenite
Kessi Janine, Hörtensteiner Stefan (2018), Inhibition of bacteriochlorophyll biosynthesis in the purple phototrophic bacteria Rhodospirillumrubrum and Rhodobacter capsulatus grown in the presence of a toxic concentration of selenite, in BMC Microbiology, 18(1), 81-81.
Contribution of Untargeted Metabolomics for Future Assessment of Biotech Crops
Christ Bastien, Pluskal Tomáš, Aubry Sylvain, Weng Jing-Ke (2018), Contribution of Untargeted Metabolomics for Future Assessment of Biotech Crops, in Trends in Plant Science, 23(12), 1047-1056.
The wheat ABC transporter Lr34 modifies the lipid environment at the plasma membrane
Deppe Johannes P., Rabbat Ritta, Hörtensteiner Stefan, Keller Beat, Martinoia Enrico, Lopéz-Marqués Rosa L. (2018), The wheat ABC transporter Lr34 modifies the lipid environment at the plasma membrane, in Journal of Biological Chemistry, 293(48), 18667-18679.
Molecular Mechanisms Preventing Senescence in Response to Prolonged Darkness in a Desiccation-Tolerant Plant
Durgud Meriem, Gupta Saurabh, Ivanov Ivan, Omidbakhshfard M. Amin, Benina Maria, Alseekh Saleh, Staykov Nikola, Hauenstein Mareike, Dijkwel Paul P., Hörtensteiner Stefan, Toneva Valentina, Brotman Yariv, Fernie Alisdair R., Mueller-Roeber Bernd, Gechev Tsanko S. (2018), Molecular Mechanisms Preventing Senescence in Response to Prolonged Darkness in a Desiccation-Tolerant Plant, in Plant Physiology, 177(3), 1319-1338.
Catalytic and structural properties of pheophytinase, the phytol esterase involved in chlorophyll breakdown
Guyer Luzia, Salinger Kathrin, Krügel Undine, Hörtensteiner Stefan (2018), Catalytic and structural properties of pheophytinase, the phytol esterase involved in chlorophyll breakdown, in Journal of Experimental Botany, 69(4), 879-889.
The biochemistry and molecular biology of chlorophyll breakdown
Kuai Benke, Chen Junyi, Hörtensteiner Stefan (2018), The biochemistry and molecular biology of chlorophyll breakdown, in Journal of Experimental Botany, 69(4), 751-767.
Chlorophyll and Chlorophyll Catabolite Analysis by HPLC
Das Aditi, Guyer Luzia, Hörtensteiner Stefan (2018), Chlorophyll and Chlorophyll Catabolite Analysis by HPLC, Springer New York, New York, NY, 223-235.
Non-specific activities of the major herbicide-resistance gene BAR
Christ Bastien, Hochstrasser Ramon, Guyer Luzia, Francisco Rita, Aubry Sylvain, Hörtensteiner Stefan, Weng Jing-Ke (2017), Non-specific activities of the major herbicide-resistance gene BAR, in Nature Plants, 3(12), 937-945.
Isolation and Detection of the Chlorophyll Catabolite Hydroxylating Activity from Capsicum annuum Chromoplasts
Hauenstein Mareike, Hörtensteiner Stefan (2017), Isolation and Detection of the Chlorophyll Catabolite Hydroxylating Activity from Capsicum annuum Chromoplasts, in BIO-PROTOCOL, 7(18), e2561.
Isolation and Detection of the Chlorophyll Catabolite Hydroxylating Activity from Capsicum annuum Chromoplasts
Hauenstein Mareike, Hörtensteiner Stefan (2017), Isolation and Detection of the Chlorophyll Catabolite Hydroxylating Activity from Capsicum annuum Chromoplasts, in BIO-PROTOCOL, 7(18), https://do.

Collaboration

Group / person Country
Types of collaboration
Ryouichi Tanaka, University of Hokkaido Japan (Asia)
- in-depth/constructive exchanges on approaches, methods or results
- Publication
Kräutler Bernhard, Universität Innsbruck Austria (Europe)
- in-depth/constructive exchanges on approaches, methods or results
- Publication
Benke Kuai, Fudan University China (Asia)
- in-depth/constructive exchanges on approaches, methods or results
- Publication
Beat Keller, UZH Switzerland (Europe)
- in-depth/constructive exchanges on approaches, methods or results
- Publication
Diana Santeria, UZH Switzerland (Europe)
- in-depth/constructive exchanges on approaches, methods or results
- Publication
Christoph Ringli, UZH Switzerland (Europe)
- in-depth/constructive exchanges on approaches, methods or results
- Publication
Ivo Feussner, Universität Göttingen Germany (Europe)
- in-depth/constructive exchanges on approaches, methods or results
- Publication
Tsanko Gechev, CPSBB, Plovdiv Bulgaria (Europe)
- in-depth/constructive exchanges on approaches, methods or results
- Publication
Jing-Ke Weng, Massachusetts Institute of Technology United States of America (North America)
- 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
9th International Symposium on Plant Senescence Talk given at a conference Evolutionary aspects of chlorophyll breakdown 01.04.2019 Berlin, Germany Menghini Damian; Schumacher Isabel;
Swiss Plant meeting Poster Chlorophyll breakdown: complexity of chlorophyll catabolite modification 31.01.2018 Meiringen, Switzerland Aubry Sylvain;


Communication with the public

Communication Title Media Place Year
Media relations: radio, television Blattverfärbung SRF1, Schweiz Aktuell German-speaking Switzerland 2017

Associated projects

Number Title Start Funding scheme
163504 Molecular mechanisms of abiotic stress-induced senescence in plants 01.05.2015 ERA-CAPS
183310 Ion Mobility Mass Spectrometry to Unscramble Complex Biological Samples 01.09.2019 R'EQUIP
149389 Chlorophyll breakdown: catabolite modification and transport, and the relation to stoma function and cell death signalling 01.05.2014 Project funding
132603 Chlorophyll breakdown: analysis of fruit ripening, evolution and regulation 01.01.2011 Project funding

Abstract

The so-called PAO/phyllobilin pathway of chlorophyll breakdown consists of two parts. First, chlorophyll is converted to a primary fluorescent chlorophyll catabolite (pFCC) with PHEOPHORBIDE A OXYGENASE (PAO) as the key enzyme. In the second part, pFCC is modified by different enzymes to ultimately produce a species-specific variety of final chlorophyll degradation products, so-called phyllobilins, which accumulate in the vacuole of senescent cells. Phyllobilins have been identified from more than twenty angiosperm species, mostly in senescent leaves. Accordingly, it has been considered that the PAO/phyllobilin pathway is highly conserved within higher plants. Even though almost all enzymatic steps of the first part of the PAO/phyllobilin pathway have been elucidated in the past, there are open questions regarding (i) the conservation of the pathway in different tissues within a given species, (ii) the degree of pathway diversity among different angiosperm species, including the molecular identity of several phyllobilin-modifying enzymes, and (iii) the evolutionary origin and phylogenetic distribution and diversity of the enzymes of the pathway. This proposal aims to address some of these aspects by answering the following questions:- How can tissue-specific differences in phyllobilin formation be explained?- How diverse is the occurrence of phyllobilins within photosynthetic organisms?- How widely distributed and how similar are the enzymes that catalyze PAO/phyllobilin pathway reactions?- What is the molecular identity of so far unknown activities within the pathway?To answer these questions, a variety of molecular, biochemical and analytical methods will be used. These include (i) analysis of enzyme activities, (ii) classical protein purification, (iii) production of transgenic plants by classical T-DNA- and CRISPR/Cas9-based methods and their analysis, (iv) phyllobilin analysis by liquid chromatography-mass spectrometry, (v) genome-wide association studies and (vi) bioinformatics- and proteomics-based identification of candidate proteins.Breakdown of chlorophyll is a physiological process that has a broad impact for daily life; among other aspects it is relevant for the food industry, for example the shelf life of leafy vegetables and fruits, and for the amenity sector, for example turf grass systems. With this in mind, it seems surprising that the mechanism of chlorophyll breakdown so far mainly focused on a few angiosperm model species. This proposal aims to get a better picture about the extent of existence and variability of the PAO/phyllobilin pathway within the lineage of oxygenic photosynthetic organisms and about its evolutionary origin.
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