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Transport of oxygen in roots of rice (Oryza
sativa L.) and of water in developing grape
berries (Vitis vinifera L.)
Inaugural-Dissertation
zur Erlangung des Doktorgrades
der Fakultät Biologie, Chemie und Geowissenschaften
der Universität Bayreuth
von
Lukasz Kotula
aus Rybnik, Polen
Bayreuth, im Juni 2009II
Die vorliegende Arbeit wurde am Lehrstuhl für Pflanzenökologie der Universität
Bayreuth unter der Leitung von Prof. Dr. E. Steudle durchgeführt und entstand im
Zeitraum von Oktober 2003 bis Juni 2009.
1. Gutachter: Prof. Dr. E. Steudle
2. Gutachter: Prof. Dr. E . Komor
Tag der Einreichung: 03.06.2009
Tag der mündlichen Prüfung: 29.09.2009
Prüfungsausschuss:
Prof. Dr. S. Clemens (Vorsitz)
Prof. Dr. E. Steudle
Prof. Dr. E. KomorMatzner
Prof. Dr. S. Liede-Schumann
Vollständiger Abdruck der von der Fakultät für Biologie, Chemie und
Geowissenschaften der Universität Bayreuth genehmigten Dissertation zur Erlangung
des Grades eines Doktors der Naturwissenschaften (Dr. rer. nat.)III
This dissertation is submitted as a “Cumulative Thesis” that covers four (4)
publications; three (3) printed articles and one (1) submitted article. In order to clarify
the publications, they are listed below.
Printed articles:
1. Kotula L, Steudle E. 2009. Measurements of oxygen permeability coefficients of
rice ( Oryza sativa L.) roots using a new perfusion technique. Journal of
Experimental Botany 60, 567-580. (Publications - Chapter 1)
2. Kotula L, Ranathunge K, Schreiber L, Steudle E. 2009. Functional and
chemical comparison of apoplastic barriers to radial oxygen loss in roots of rice
(Oryza sativa L.) grown in aerated or deoxygenated solution. Journal of
Experimental Botany 60, 2155-2167. (Publications - Chapter 2)
3. Tyerman SD, Tilbrook J, Pardo C, Kotula L, Sullivan W, Steudle E. 2004.
Direct measurements of hydraulic properties in developing berries of Vitis vinifera
L. cv Shiraz and Chardonay. Australian Journal of Grape Wine Research 10, 170-
181. (Publications - Chapter 4)
Article in press:
1. Kotula L, Ranathunge K, Steudle E. 2009. Apoplastic barriers effectively block
oxygen permeability across outer cell layers of rice roots under deoxygenated
conditions: roles of apoplastic pores and of respiration. New Phytologist,
submitted. (Publications - Chapter 3)
Other printed article which is not part of this dissertation:
1. Ranathunge K, Kotula L, Steudle E, Lafitte R. 2004. Water permeability and
reflection coefficient of the outer part of young rice roots are differently affected
by closure of water channels (aquaporins) or blockage of apoplastic pores. Journal
of Experimental Botany 55, 433-447.
(this article was part of my master thesis completed at the University of Silesia,
Katowice, Poland)IV
Declaration of the self-contribution of research articles
This thesis is completed with four research articles, which include different research
work. Most of the research work in was carried out by myself independently at the
Department of Plant Ecology, University of Bayreuth under the supervision of Prof.
Dr. E. Steudle.
In Chapter 1, all experimental work and writing of the manuscript was conducted by
myself.
In Chapter 2, most of the experiments were conducted by myself. The biochemical
analysis of rice roots were carried out in co-operation with Dr. Kosala Ranathunge
and Prof. Dr. Lukas Schreiber at the University of Bonn. As a guest in Prof.
Schreiber’s laboratory, I participated in the analysis. I drafted the manuscript, which
was completed after discussion with the co-authors.
In Chapter 3, all experimental work was conducted by myself. I drafted the
manuscript, which was completed after discussion with co-authors.
In Chapter 4, I have participated in experiments on hydraulic conductance of grape-
berry pedicel during my stay in the laboratory of Prof. Dr. Stephen Tyerman at the
School of Agriculture and Wine, University of Adelaide, Australia.
All published articles can be downloaded from the web-side:
http://www.old.uni-bayreuth.de/departments/planta/research/steudle/index.htmlV
Acknowledgements
In the first place, I would like to express my gratitude to Prof. Dr. Ernst Steudle for
his supervision and excellent guidance during my PhD. His critical advises, patience
and experience have been essential for the accomplishment of this work. I am also
grateful to him for providing me the opportunity of many research visits in distinct
labs all over the world throughout my study.
I am grateful to Dr. Renee Lafitte (International Rice Research Institute Manila,
Philippines), for co-operation within the BMZ-project No. 2000.7860.0-001.00, which
supported initial stages of my work.
I am very grateful to Prof. Lukas Schreiber (University of Bonn, Germany) for
enabling me to work in his lab and for his valuable suggestions and discussions of my
results. I thank Professor Stephen Tyerman (University of Adelaide, Australia) for
inviting me to study water relations of grape berries in Adelaide. I have profited a lot
from both stays.
I would like to thank Prof. Carol Peterson (University of Waterloo, Ontario, Canada)
for her excellent teaching of plant anatomy during her various stays in Bayreuth. I
thank Prof. Tim Colmer (University of Western Australia, Perth, Australia) for
introducing me into technique for measuring ROL and for his suggestions and
advises. The valuable help of Dr. Hermann Heilmeier (Technical University, Freiberg,
Germany) concerning statistical analysis is gratefully acknowledge.
Many thanks go to Dr. Kosala Ranathunge (University of Bonn, Germany). I enjoyed
working with him from the beginning of my stay in Bayreuth and learnt a lot. I am
grateful for his never-ceasing help and continuous friendship.
I thank Burkhard Stumpf for his great technical assistance during my stay in
Bayreuth, and for creating a friendly and pleasant atmosphere in the lab and beyond.
I would like to thank past and present lab members for their great company: Alaina,
Ankur, Bogus, Carlos, Chris, Ewa, Hagen, Qing, Ola, Soenghee, Suigi, Yangmin.
Thanks go in particular to Thorsten for his great help in German translations.VI
Finally, my gratitude goes to my parents and brother for their encouragement. I would
like to give my special thanks to my wife Asia, whose patience and support enabled
me to complete this work.VII
Table of contents
I. Detailed Summary ......................................................................................1
1. General Introduction .............................................................................................3
2. Background ............................................................................................................6
2.1. Transport of oxygen in rice roots: effects of anaerobic conditions…......6
2.1.1. Rice: importance, cultivation, and morphology............................. .......6
2.1.2. Waterlogging...........................................................................................8
2.1.3. Adaptations to waterlogging and aeration of roots................................10
2.1.4. The barrier to ROL vs root water uptake..............................................16
2.2. Transport of water in grape berries………………..……………………..18
2.2.1. Structure of grape-berry………………………………………...…....18
2.2.2. Grape berry development……………………………………….……19
2.2.3. Transport of water into the grape berry…............................................20
3. Aims of Research..................................................................................................21
4. Materials and Methods........................................................................................24
4.1. Transport of oxygen in rice roots: effects of anaerobic conditions……24
4.1.1. Plant material and growth conditions………….................……………24
4.1.2. Measurements of root porosity……………...................................……24
4.1.3. Histochemical detection of apoplastic barriers in the OPR……........…24
4.1.4. Biochemical analyses of apoplastic barriers in the OPR…………..…..25
4.1.5. Measurements of radial oxygen loss (ROL) from roots of intact
plants………………………………………………………………….25
4.1.6. Responses of ROL to an increased O concentration around2
the shoot…………………………………………………………….25
4.1.7. Measurements of oxygen permeability coefficient of rice root
segments...............................................................................................26VIII
4.1.8. Blockage of apoplastic pores in the OPR………………….....………..28
4.1.9. Treatment with 0.1 N HCl (pH = 1) to kill living cells in the OPR…...28
4.2. Transport of water in developing grape berries…………….......……..28
4.2.1. Fruit material…………………………………...……………….......…28
4.2.2. Pressure probe measurements.................................................................28
5. Results and Discussion.........................................................................................30
5.1. Transport of oxygen in rice roots: effects of anaerobic conditions.........30
5.1.1. Growth of rice plants in aerated or deoxygenated solution....................30
5.1.2. Porosity of adventitious roots of rice grown in aerated or
deoxygenated solution..........………...........………….........................30
5.1.3. Histochemical detection of the apoplastic barriers in the OPR
of rice grown in aerated or deoxygenated conditions...........................31
5.1.4. Amounts of suberin and lignin in the OPR of rice grown in
aerated or deoxygenated conditions......................................................32
5.1.5. Radial O loss (ROL) from intact adventitious roots of rice2
grown in aerated or stagnant solution...................................................33
5.1.6. Responses of ROL to increased O concentration around the shoot......342
5.1.7. Oxygen permeability coefficient of the OPR of plants grown
in aerated or stagnant solution.............................................................35
5.1.8. Oxygen permeability coefficient of the OPR after blocking
the apoplast with precipitated salts crystals.........................................38
5.1.9. Oxygen permeability of the OPR after killing the root
segments with 0.1 N HCl......................................................................39
5.2. Transport of water in developing grape berries........................................39
5.2.1. Hydraulic conductance of berries of Vitis vinifera L.
cv. Shiraz and Chardonnay…………………...…….............................39
6. General conclusion...............................................................................................41IX
6.1. Transport of oxygen in roots of rice: effects of anaerobic conditions...........41
6.2. Transport of water in developing grape berries.............................................42
7. Short summary.....................................................................................................43
7.1. Transport of oxygen in roots of rice: effects of anaerobic conditions...........43
7.2. Transport of water in developing grape berries.............................................45
8. References.............................................................................................................46
II. Publications...................................................................................................55
1. Measurements of oxygen permeability coefficients of rice (Oryza sativa L.)
roots using a new perfusion technique..........…………………………..............57
2. Functional and chemical comparison of apoplastic barriers to radial
oxygen loss in roots of rice (Oryza sativa L.) grown in aerated or
deoxygenated solution..........................................................................................91
3. Apoplastic barriers effectively block oxygen permeability across
outer cell layers of rice roots under deoxygenated conditions:
roles of apoplastic pores and of respiration.....................................................121
4. Direct measurement of hydraulic properties in developing berries
of Vitis vinifera L. cv Shiraz and Chardonnay................................................141
5. Summary.............................................................................................................173
5.1. Radial oxygen flow in rice (Oryza sativa L.) roots: effects of anaerobic
conditions and the role of apoplastic barriers..............................................173
5.2. The hydraulic properties in developing berries of Vitis vinifera L
cv. Shiraz and Chardonnay...........................................................................176
6. Zusammenfassung..............................................................................................177
6.1. Radialer Sauerstofffluss in Reiswurzeln (Oryza sativa L.):
der Einfluss anaerober Bedingungen und apoplastischer Barrieren…...….177
6.2. Die hydraulischen Eigenschaften von sich entwickelnden
Beeren von Vitis vinifera L. cv. Shiraz and Chardonnay……………...…..180
Erklärung..................................................................................................................183X

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