Dokument: Establishment of C 4 Photosynthesis in Ontogeny and Evolution
| Titel: | Establishment of C 4 Photosynthesis in Ontogeny and Evolution | |||||||
| Weiterer Titel: | Etablierung der C4-Photosynthese während Ontogenese und Evolution | |||||||
| URL für Lesezeichen: | https://docserv.uni-duesseldorf.de/servlets/DocumentServlet?id=36948 | |||||||
| URN (NBN): | urn:nbn:de:hbz:061-20160122-162629-3 | |||||||
| Kollektion: | Dissertationen | |||||||
| Sprache: | Englisch | |||||||
| Dokumententyp: | Wissenschaftliche Abschlussarbeiten » Dissertation | |||||||
| Medientyp: | Text | |||||||
| Autor: | M. Sc Denton, Alisandra [Autor] | |||||||
| Dateien: |
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| Beitragende: | Prof. Dr. Weber, Andreas P. M. [Gutachter] Prof. Dr. Rose, Laura [Gutachter] | |||||||
| Stichwörter: | C4 photosynthesis, evolution, gene duplication, transcriptome | |||||||
| Dewey Dezimal-Klassifikation: | 500 Naturwissenschaften und Mathematik » 580 Pflanzen (Botanik) | |||||||
| Beschreibungen: | Many plant species harbor an adaptive photosynthetic trait known as C4 photosynthesis.
The C4 cycle is a biochemical pump that concentrates CO2 in the vicinity of the central carbon fixing enzyme Rubisco, suppressing the fixation of O2 and thereby photorespiration. This is highly advantageous for C4 plants because photorespiration is energetically costly and results in a net loss of carbon. Further, C4 plants show increased water-use efficiency, as they are more able to modulate stomatal opening and closing and maintain a sufficient CO2 concentration near Rubisco; and increased nitrogen use efficiency, as they can reduce the amount of nitrogen that must be invested in the extremely abundant Rubisco protein. These characteristics result in a strong selective advantage for C4 species in hot and arid environments. The C4 trait is found in many high-biomass producing crop plants, including maize, sorghum, and sugar cane. Therefore, there is strong interest in engineering C4 photosynthesis into crop plants of the ancestral C3 photosynthetic type. A fully integrated C4 photosynthetic trait requires complex modifications to support the CO2 concentrating C4 cycle. In most species with C4 photosynthesis, CO2 is initially fixed in the exterior mesophyll (M) tissue and then pumped into interior bundle sheath (BS) tissue, where the CO2 is released and then re-fixed by Rubisco. Extensive changes in anatomy are required, both to reduce diffusional distances for the metabolites of the C4 cycle and to take advantage of the concentrated CO2 . These changes include an increased vein density, enlarged bundle sheath cells, increased organelle content in bundle sheath cells, and modifications to the BS cell wall that reduce diffusive escape of CO2 . C4 photosynthesis requires specialization of function between M and BS cells, notably with the Calvin- Benson-Bassham (CBB) cycle and the photorespiratory cycle restricted primarily to the BS. Further common changes include the restriction of photosystem II to M tissue, and the establishment of redox shuttles to balance energy between the two tissue types. The high complexity of the C4 trait leads to both evolutionary questions and engineering challenges. The evolution of C4 photosynthesis is particularly intriguing, because despite the high complexity and lack of master regulator, C4 photosynthesis evolves in a vhighly convergent fashion. A step wise model summarizes a commonly observed path to C4 photosynthesis, starting with genetic and anatomical preconditioning, and proceeding to the establishment of a photorespiratory pump and later the up-regulation and optimization of the cycle. Three manuscripts examine what facilitates the evolution of C4 photosynthesis, with findings consistent with, but providing additional detail to the standing model for C4 evolution. In Denton et al. (in preparation), we elucidated how duplication contributes to the C4 trait in maize, beyond the core C4 genes. Paralogs with functions relevant to anatomical specialization, including cell wall and auxin response, showed specific patterns of divergence in immature tissue. Paralogs with functions relevant to energy balance, namely 3 out of the 4 ATP consuming enzymes in the CBB and photorespiratory cycles, showed complementary expression in mature M and BS tissue. Further BS or M tissue specificity was related to duplication level on a genome wide scale. In Denton et al. (2013) we reviewed recent progress in understanding anatomical preconditioning factors, such as BS cell size and dense vein spacing, and their advantages in hot and arid environments. Finally, in Heckmann et al. (2013) we modeled and cross checked the evolutionary progression from C3 to fully integrated C4 biochemistry. Establishment of the C4 photosynthetic anatomy occurs not in mature but in developing tissues, and a full mechanistic understanding of the C4 trait requires comparative ontogenies. Two manuscripts in this thesis generate and analyze comparative ontogeny data. Denton et al. (in preparation) compares BS and M tissues in maize leaf development, and showed, in addition to tissue specific paralogs, transcriptional regulators with early tissue specificity. Kuelahoglu et al. (2014), compares leaf ontogeny in closely related C3 and C4 Cleomaceae species, and finds a link between transcription and anatomy for both enlarged BS and dense vein spacing in the C4 species. The enlarged BS correlated with a higher BS ploidy level and down-regulation of a key endoreduplication inhibiting transcription factor in the C4 species. The increased vein formation in the C4 species appears to be facilitated by a delay in tissue differentiation observed at both the transcriptional and anatomical level. Taken together, the manuscripts in this thesis have contributed to understanding the natural evolutionary path towards C4 photosynthesis and provided insight into the mechanisms and details of a fully integrated C4 trait.In vielen Pflanzenarten findet sich das adaptive Merkmal, das als C4-Syndrom bekannt ist. Der C4-Zyklus beinhaltet eine biochemische Pumpe, die CO2 in der Naehe des wesentlichen Kohlenstoff-fixierenden Enzyms Rubisco anreichert und dadurch die Fixierung von O2 und somit die Photorespieration unterdrueuckt. Dies ist von großem Vorteil fuer C4-Pflanzen, da die Photorespiration energieaufwendig ist und in einem NettoVerlust von Kohlenstoff resultiert. Darueberhinaus weisen C4-Pflanzen eine erhoehte Wassernutzungseffizienz auf, da sie besser dazu in der Lage sind, das Offnen und Schließen der Stomata zu regulieren und eine ausreichende CO2-Konzentration um Rubisco aufrechtzuerhalten. Außerdem verfuegen sie ueber eine effizientere Stickstoffnutzung, da weniger Stickstoff in die Produktion von Rubisco investiert werden muss. Diese Eigenschaften schlagen sich in einem starken selektiven Vorteil fuer C4-Spezies in heißen und trockenen Umgebungen nieder. Das C4-Syndrom kommt in vielen Nutzpflanzen vor, die grosse Mengen an Biomasse produzieren, darunter Mais, Sorghum und Zuckerrohr. Aus diesem Grund besteht ein grosses Interesse daran, Nutzpflanzen mit dem ancestralen C3-Typ der Photosynthese zur Nutzung der C4-Photosynthese zu modifizieren. Zur vollstaendigen Integration des C4-Photosyntheseweges bedarf es komplexer Modifikationen, um den CO2-Konzentrations-Zyklus zu unterstuetzen. In den meisten C4-Spezies wird CO2 zuerst im aeusseren Mesophyll-Gewebe (M) fixiert und anschliessend in die inneren Buendelscheidenzellen (BS) gepumpt, wo CO2 freigesetzt und durch Rubisco re-fixiert wird. Umfangreiche Anderungen in der Anatomie sind noetig, um Diffusionswege der Metaboliten des C4-Zyklus zu reduzieren und um Nutzen aus der CO2-Konzentration ziehen zu koennen. Diese Anderungen beinhalten eine erhoehte Blattaderdichte, vergroesserte Buendelscheidenzellen, eine erhoehte Anzahl von Organellen in den Buendelscheidenzellen und Modifikationen der BS-Zellwand, die den Austritt von CO2 durch Diffusion reduzieren. C4 Photosynthese erfordert die funktionelle Spezialisierung von M- und BS-Zellen, insbesondere eine Beschraenkung des Calvin-Benson-Bassham-Zyklus (CBB) und des photorespirativen Zyklus primaer auf das BS-Gewebe. Weitere verbreitete Anpassungen beinhalten die Beschraenkung des Photosystem II zum M-Gewebe und die Etablierung von Redox-Shuttles, um Energie zwischen den beiden Geweben auszugleichen. Die hohe Komplexitaet der C4-Photosynthese fuehrt sowohl zu Fragen ihrer Evolution als auch zu technischen Herausforderungen. Die Evolution der C4-Photosynthese ist dadurch besonders faszinierend, dass sie – trotz ihrer so hohen Komplexitaet und Abwesenheit eines Master-Regulator-Gens – mehrfach unabhaengig evolutionaer hochgradig konvergent entstanden ist. Ein schrittweises Modell fasst einen oft beobachteten Weg zur C4-Photosynthese zusammen, ausgehend von genetischer und anatomischer Praekonditionierung, ueber die Etablierung der photorespiratorischen Pumpe und anschliessender Hochregulierung und Optimierung des Zyklus. Drei der Manuskripte dieser Arbeit beschaeftigen sich mit den Voraussetzungen der Evolution der C4-Photosynthese. Die hier gewonnen Erkenntnisse decken sich mit den bestehenden Modellen und ergaenzen sie um zusaetzliche Details. In Denton et al. (in preparation) erlaeutern wir, wie Genduplikationen, ueber die Haupt-C4-Gene hinaus, zum C4-Syndrom in Mais beitragen. Paraloge, die eine fuer die anatomische Spezialisierung wichtige Funktion haben, wie etwa Zellwand- oder Auxin-Response-Funktion, zeigten spezifische Divergenzmuster in jungen Geweben. Drei der vier ATP-verbrauchenden Enzyme des CBB- und des photorespiratorischen Zyklus sind Paraloge mit Funktionen die fuer den Energieausgleich wichtig sind und, zeigten komplementaere Expression in voll entwickeltem M- und BS-Gewebe. Darueberhinaus hing die BS- bzw. M-Spezifitaet mit dem Duplikationsgrad auf genomweiter Ebene zusammen. In Denton et al. (2013) haben wir die juengsten Fortschritte und Erkenntisse aus dem Bereich der Praekonditionierung, wie etwa BS-Zellgroesse, hohe Blattaderdichte, und die Vorteile in heissen und trockenen Umgebungen, analysiert. Abschliessend modellierten und ueberprueften wir in Heckmann et al. (2013) den evolutionaeren Verlauf ausgehend von einem C3-Zustand zur vollstaendig integrierten C4-Biochemie und fanden. Die Errichtung der C4-photosynthetischen Anatomie findet nicht in vollentwickelten, sondern in sich entwickelnden Geweben statt; zu einem vollen mechanistischen Verstaendnis sind vergleichende Studien der Ontogenese erforderlich. Zwei der Manuskripte dieser Arbeit generierten und analysierten solche vergleichende Ontogenese-Daten. Den- ton et al. (in preparation) vergleicht BS- und M-Gewebe waehrend der Entwicklung des Mais-Blattes und zeigte, zusaetzlich zu gewebespezifischen Paralogen, Transkriptionsreglatoren mit frueher Gewebe-Spezifitaet. Kuelahoglu et al. (2014) vergleicht die Blatt-Ontogenese zwischen zwei nahe verwandten C3- und C4-Cleomaceae-Spezies und findet eine Verbindung zwischen Transkription und Anatomie fuer vergroesserte BS und hohe Blattaderdichte in den C4-Spezies. Die vergroesserten BS in den C4-Spezies korrelierten mit hoeheren BS-Ploiditaetsstufen und der Herunterregulation eines Transkriptionsfaktors, der eine Schluesselrolle in der Inhibition der Endoreduplikation spielt. Die vergroesserte Blattaderdichte scheint durch eine Verzoegerung der Gewebedifferenzierung ermoeglicht zu sein, welche auf transkriptionaler und anatomischer Ebene beobachtet werden konnte. Zusammengenommen tragen die Manuskripte in dieser Arbeit zum Verstaendnis ueber die fuer die Entwicklung der C4-Photosynthese noetigen Schritte bei und bieten Einblicke in die Mechanismen und Details des vollstaendig integrierten C4-Syndroms | |||||||
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| Lizenz: |  Urheberrechtsschutz | |||||||
| Fachbereich / Einrichtung: | Mathematisch- Naturwissenschaftliche Fakultät » WE Biologie » Biochemie der Pflanzen | |||||||
| Dokument erstellt am: | 22.01.2016 | |||||||
| Dateien geändert am: | 22.01.2016 | |||||||
| Promotionsantrag am: | 21.04.2015 | |||||||
| Datum der Promotion: | 22.07.2015 |
