Krome, Kristin (2008)
Interactions in the rhizosphere: Plant responses to bacterivorous soil protozoa.
Technische Universität Darmstadt
Dissertation, Erstveröffentlichung
Kurzbeschreibung (Abstract)
Plant growth promotion by bacterivorous soil protozoa is generally assigned to an improved nitrogen supply due to the mobilisation of nitrogen fixed in bacterial biomass. However, there is evidence that protozoa may also stimulate plant growth by non-nutrient effects with the phytohormone auxin (indole-3-acetic acid; IAA) being likely involved. This PhD Thesis was performed to investigate morphological, physiological and transcriptional responses of plants to soil protozoa and to assess the involvement of nitrogen and plant hormones in the protozoa-induced plant growth promotion. In the first experiment (Chapter 2) modifications of root architecture and internal auxin metabolism of Lepidium sativum and Arabidopsis thaliana due to the presence of a diverse soil bacterial community and the protozoan species Acanthamoeba castellanii were analysed. Soil bacteria enhanced concentrations of conjugated IAA in L. sativum shoots without affecting root architecture, whereas soil bacteria plus A. castellanii increased free bioactive IAA concentrations and root branching. The results indicate that soil protozoa stimulate root foraging via affecting plant internal modifications of auxin metabolism and thus enable enhanced nutrient capture and plant growth. However, despite increased root branching, A. thaliana reporter plants for auxin and cytokinin did not respond to auxin but to cytokinin. Since soil protozoa increased nitrate concentrations in the rhizosphere the results suggest that nitrate caused an accumulation of cytokinin in the plant and interacted with its hormonal antagonist auxin, which finally induced increased root branching. In the second experiment (Chapter 3) a defined laboratory system using A. thaliana as model plant was designed allowing to investigate effects of interactions between a diverse soil bacterial community and A. castellanii on plant performance in detail. Soil bacteria and protozoa increased growth of A. thaliana already three days past plant inoculation (dpi) with the effects of protozoa exceeding those of bacteria only. The immediate growth response was accompanied by an increased carbon but not nitrogen allocation. However, three days later protozoa enhanced ammonium availability and plant uptake of nitrogen from organic material, which presumably was responsible for prolonged vegetative growth and increased seed production. The results suggest that A. thaliana sensed the upcoming mobilization of nitrogen presumably by changes in rhizosphere signalling and initiated carbon fixation and root carbon allocation which payed off later by increased nutrient capture and strongly increased plant reproduction. In the third experiment (Chapter 4) transcriptional changes of A. thaliana genes involved in plant signalling and stress response as well as nitrogen responsive genes were investigated by performing a DNA array and quantitative real time PCR. Nitrogen responsive genes were not immediately regulated by soil protozoa, but later ammonium responsive genes were up-regulated supporting the results obtained in the experiment reported in Chapter 3. Transcription analysis further demonstrated that soil protozoa down-regulate defence mechanisms in plant roots, but induce plant defence in plant shoots. This suggests that soil protozoa inhibit detrimental soil bacteria by selective grazing leading to a reduced defence in roots and thus reduced investment in secondary metabolite production. Improved nutrient and energy status of A. thaliana may be responsible for increased shoot growth in presence of protozoa despite plant defence concurrently being enhanced. Overall, the results suggest that the effect of protozoa on plant growth in fact initially may not be caused by increased nitrogen availability. Rather, the plants appear to anticipate the subsequent up-coming nitrogen mobilization due to changes in rhizosphere signalling and increase carbon assimilation and allocation to roots resulting in strongly increased plant growth and seed production, i.e. plant fitness. Further, protozoa-mediated reduction in detrimental bacteria may have contributed to increased plant growth by saving costs for secondary metabolite production. Notably, the induction of plant defence in shoots by protozoa was not associated with reduced plant growth but rather the opposite, suggesting that due to increasing nitrogen supply protozoa enable plants to invest in defence in shoots and in parallel increase plant growth and reproduction.
| Typ des Eintrags: |
Dissertation
|
| Erschienen: |
2008 |
| Autor(en): |
Krome, Kristin |
| Art des Eintrags: |
Erstveröffentlichung |
| Titel: |
Interactions in the rhizosphere: Plant responses to bacterivorous soil protozoa |
| Sprache: |
Englisch |
| Referenten: |
Scheu, Prof. Stefan ; Warzecha, Prof. Heribert ; Pfeifer, Prof. Felicitas ; Kolmar, Prof. Harald |
| Publikationsjahr: |
20 Juli 2008 |
| Ort: |
Darmstadt |
| Verlag: |
Technische Universität |
|
Datum der mündlichen Prüfung: |
30 Mai 2008 |
| URL / URN: |
urn:nbn:de:tuda-tuprints-10554 |
| Kurzbeschreibung (Abstract): |
Plant growth promotion by bacterivorous soil protozoa is generally assigned to an improved nitrogen supply due to the mobilisation of nitrogen fixed in bacterial biomass. However, there is evidence that protozoa may also stimulate plant growth by non-nutrient effects with the phytohormone auxin (indole-3-acetic acid; IAA) being likely involved. This PhD Thesis was performed to investigate morphological, physiological and transcriptional responses of plants to soil protozoa and to assess the involvement of nitrogen and plant hormones in the protozoa-induced plant growth promotion. In the first experiment (Chapter 2) modifications of root architecture and internal auxin metabolism of Lepidium sativum and Arabidopsis thaliana due to the presence of a diverse soil bacterial community and the protozoan species Acanthamoeba castellanii were analysed. Soil bacteria enhanced concentrations of conjugated IAA in L. sativum shoots without affecting root architecture, whereas soil bacteria plus A. castellanii increased free bioactive IAA concentrations and root branching. The results indicate that soil protozoa stimulate root foraging via affecting plant internal modifications of auxin metabolism and thus enable enhanced nutrient capture and plant growth. However, despite increased root branching, A. thaliana reporter plants for auxin and cytokinin did not respond to auxin but to cytokinin. Since soil protozoa increased nitrate concentrations in the rhizosphere the results suggest that nitrate caused an accumulation of cytokinin in the plant and interacted with its hormonal antagonist auxin, which finally induced increased root branching. In the second experiment (Chapter 3) a defined laboratory system using A. thaliana as model plant was designed allowing to investigate effects of interactions between a diverse soil bacterial community and A. castellanii on plant performance in detail. Soil bacteria and protozoa increased growth of A. thaliana already three days past plant inoculation (dpi) with the effects of protozoa exceeding those of bacteria only. The immediate growth response was accompanied by an increased carbon but not nitrogen allocation. However, three days later protozoa enhanced ammonium availability and plant uptake of nitrogen from organic material, which presumably was responsible for prolonged vegetative growth and increased seed production. The results suggest that A. thaliana sensed the upcoming mobilization of nitrogen presumably by changes in rhizosphere signalling and initiated carbon fixation and root carbon allocation which payed off later by increased nutrient capture and strongly increased plant reproduction. In the third experiment (Chapter 4) transcriptional changes of A. thaliana genes involved in plant signalling and stress response as well as nitrogen responsive genes were investigated by performing a DNA array and quantitative real time PCR. Nitrogen responsive genes were not immediately regulated by soil protozoa, but later ammonium responsive genes were up-regulated supporting the results obtained in the experiment reported in Chapter 3. Transcription analysis further demonstrated that soil protozoa down-regulate defence mechanisms in plant roots, but induce plant defence in plant shoots. This suggests that soil protozoa inhibit detrimental soil bacteria by selective grazing leading to a reduced defence in roots and thus reduced investment in secondary metabolite production. Improved nutrient and energy status of A. thaliana may be responsible for increased shoot growth in presence of protozoa despite plant defence concurrently being enhanced. Overall, the results suggest that the effect of protozoa on plant growth in fact initially may not be caused by increased nitrogen availability. Rather, the plants appear to anticipate the subsequent up-coming nitrogen mobilization due to changes in rhizosphere signalling and increase carbon assimilation and allocation to roots resulting in strongly increased plant growth and seed production, i.e. plant fitness. Further, protozoa-mediated reduction in detrimental bacteria may have contributed to increased plant growth by saving costs for secondary metabolite production. Notably, the induction of plant defence in shoots by protozoa was not associated with reduced plant growth but rather the opposite, suggesting that due to increasing nitrogen supply protozoa enable plants to invest in defence in shoots and in parallel increase plant growth and reproduction. |
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Alternatives oder übersetztes Abstract: |
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Alternatives Abstract | Sprache |
|---|
Die Förderung von Pflanzenwachstum durch bakterivore Bodenprotozoen wird meist mit einer Mobilisierung von festgelegtem Stickstoff aus bakterieller Biomasse erklärt. Es existieren jedoch auch Hinweise dafür, dass das Pflanzenhormon Auxin (Indol-3-Essigsäure; IAA) an der Pflanzenwachstumsförderung durch Protozoen beteiligt ist. In der vorliegenden Doktorarbeit wurden morphologische, physiologische und transkriptionale Pflanzenreaktionen auf bakterivore Bodenprotozoen untersucht. In einem ersten Experiment (Kapitel 2) wurde die Wirkung von Bodenbakterien und der Bodenamöbe Acanthamoeba castellanii auf die Wurzelmorphologie und den Auxinmetabolismus von Lepidium sativum und Arabidopsis thaliana analysiert. Bodenbakterien erhöhten die Konzentration an konjugiertem IAA ohne die Wurzelmorphologie zu beeinflussen. Die zusätzliche Anwesenheit von A. castellanii hingegen führte zu einer erhöhten Konzentration an freiem IAA sowie zu einer vermehrten Bildung von Lateralwurzeln. Bodenprotozoen steigern demnach die Ausdehnung des Wurzelsystems durch Veränderungen des pflanzlichen Auxin-metabolismus und ermöglichen so eine verbesserte Ausbeutung von Nährstoffen. Obwohl A. castellanii ebenfalls eine erhöhte Lateralwurzelbildung in A. thaliana induzierte, reagierten die Reporterpflanzen ARR5::GUS und DR5::GUS nicht auf Auxin, jedoch auf den Auxinantagonisten Cytokinin. Möglicherweise war hierfür eine erhöhte Nitratverfügbarkeit verantwortlich, da Nitrat zu einer Akkumulation von Cytokinin führt. Zur Durchführung des zweiten Experiments (Kapitel 3) wurde ein definiertes Laborsystem mit A. thaliana entwickelt, welches die detaillierte Untersuchung von Interaktionen zwischen Bodenbakterien und A. castellanii auf das Pflanzenwachstum erlaubt. Bodenbakterien sowie A. castellanni steigerten das Pflanzenwachstum bereits drei Tage nach der Inokulation, wobei der Einfluss von A. castellanii denjenigen der Bodenbakterien übertraf. Die Wachstumssteigerung ging mit einer erhöhten Kohlenstoff-, aber nicht Stickstoffaufnahme einher. Später erhöhten die Bodenprotozoen jedoch die Ammoniumverfügbarkeit, was vermutlich zu einer Verlängerung der vegetativen Wachstumsphase und erhöhten Reproduktion von A. thaliana führte. Die Ergebnisse legen nahe, dass A. thaliana die bevorstehende Stickstoffmobilisierung antizipiert und mit einer Erhöhung des Spross- und Wurzelwachstums reagiert. Die damit verbundene Vergrößerung der Wurzel ermöglicht später die vermehrte Aufnahme von Stickstoff, welches eine erhöhte Reproduktion bedingt. In dem dritten Experiment (Kapitel 4) wurde der Einfluss von A. castellanii auf transkriptionale Veränderungen in A. thaliana mittels eines DNA arrays und quantitativer real time PCR untersucht. Die Initiierung einer Wachstumssteigerung durch A. castellanii war zunächst nicht mit einer Veränderung der Genexpression von stickstoffinduzierbaren Genen verbunden. Später wurden jedoch Gene der Ammoniumassimilation hoch reguliert, welches die Ergebnisse aus Kapitel 3 bestätigt. Die Transkriptionsanalyse zeigte weiterhin, dass durch Bodenprotozoen Abwehrmechanismen in der Wurzel reduziert, im Spross jedoch induziert werden. Möglicherweise reduziert A. castellannii die Besiedlung der Wurzeln mit pflanzenschädigenden Bodenbakterien durch Beweidung, welches eine verminderte Abwehr und somit eine Reduktion der Investitionen in den pflanzlichen Sekundärmetabolismus in der Wurzel ermöglicht. Der allgemein verbesserte Nährstoff- und Energiestatus der Pflanze könnte dafür verantwortlich sein, dass sowohl Wachstum als auch Abwehr im Spross gesteigert wurden. Zusammenfassend deuten die Ergebnisse daraufhin, dass der positive Effekt von Bodenprotozoen auf das Pflanzenwachstum nicht nur durch eine erhöhte Stickstoffverfügbarkeit verursacht wird. Vielmehr scheinen die Pflanzen die Stickstoffmobilisierung über Signalstoffe in der Rhizosphere wahrzunehmen und steigern bereits vorher Spross- und Wurzelwachstum, was die Nährstoffaufnahme verbessert und das Pflanzenwachstum sowie die Reproduktion erhöhen. Die Reduktion von schädlichen Bodenbakterien durch Bodenprotozoen und die damit verbundene Reduktion von induzierter Abwehr in den Wurzeln haben vermutlich zu dem gesteigerten Pflanzenwachstum beigetragen. Die Abwehrinduktion im Spross führte nicht zu einer Reduktion von Pflanzenwachstum, was darauf hindeutet, dass die verbesserte Stickstoff- und Energieversorgung eine gleichzeitige Investition in Abwehr sowie in Wachstum ermöglicht. | Deutsch |
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| Freie Schlagworte: |
Soil protozoa, Arabidopsis thaliana, Soil bacteria, Auxin, gene expression, Plant growth, Acanthamoeba castellanii, Induced defence, microarray |
| Schlagworte: |
| Einzelne Schlagworte | Sprache |
|---|
| Bodenprotozoen, Arabidopsis thaliana, Bodenbakterien, Auxin, Genexpression, Pflanzenwachstum, Microarray | Deutsch |
|
| Sachgruppe der Dewey Dezimalklassifikatin (DDC): |
500 Naturwissenschaften und Mathematik > 590 Tiere (Zoologie) |
| Fachbereich(e)/-gebiet(e): |
10 Fachbereich Biologie |
| Hinterlegungsdatum: |
17 Okt 2008 09:23 |
| Letzte Änderung: |
05 Mär 2013 09:27 |
| PPN: |
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| Referenten: |
Scheu, Prof. Stefan ; Warzecha, Prof. Heribert ; Pfeifer, Prof. Felicitas ; Kolmar, Prof. Harald |
|
Datum der mündlichen Prüfung / Verteidigung / mdl. Prüfung: |
30 Mai 2008 |
| Schlagworte: |
| Einzelne Schlagworte | Sprache |
|---|
| Bodenprotozoen, Arabidopsis thaliana, Bodenbakterien, Auxin, Genexpression, Pflanzenwachstum, Microarray | Deutsch |
|
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