Identification of Cis- and Trans-regulatory factors controlling the expression of the C4 phosphoenolpyruvate carboxylase gene of the C4 dicot Flaveria trinervia [Elektronische Ressource] / vorgelegt von Meryem Akyildiz

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• Biologie

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• Publié par: heinrich-heine-universitat_dusseldorf
• Publié le: 01 janvier 2007
• Nombre de lectures: 21
• Langue: English
• Poids de l'ouvrage: 60 Mo

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Identification of Cis- and Trans-Regulatory Factors Controlling
the Expression of the C Phosphoenolpyruvate Carboxylase Gene4
of the C Dicot Flaveria trinervia4
Inaugural-Dissertation
zur
Erlangung des Doktorgrades der
Mathematisch-Naturwissenschaftlichen Fakultät
der Heinrich-Heine Universität Düsseldorf
vorgelegt von
Meryem Akyildiz
aus Duisburg
Düsseldorf im Juli 2007Aus dem Institut für Entwicklungs- und Molekularbiologie der Pflanzen
der Heinrich-Heine-Universität Düsseldorf
Gedruckt mit der Genehmigung der
Mathematisch-Naturwissenschaftlichen Fakultät der
Heinrich-Heine-Universität Düsseldorf
Referent: Prof. Dr. P. Westhoff
Koreferent: Prof. Dr. G. Groth
Tag der mündlichen Prüfung: 24.09.2007Die hier vorgelegte Dissertation habe ich eigenständig und ohne unerlaubte Hilfe angefertigt.
Die Dissertation wurde in der vorgelegten oder in ähnlicher Form noch bei keiner anderen
Institution eingereicht. Ich habe bisher keine erfolglosen Promotionsversuche unternommen.
Düsseldorf, den 02.07.2007I
Contents
I. General Introduction…………………………………………..…….…...… 1
I.1 C Photosynthesis………………………………………………..…………....… 14
I.2 The Evolution of C Photosynthesis.…………..…..………..………................. 64
I.3 The Phosphoenolpyruvate Carboxylase………………………………………. 12
I.4 The Cis-Regulatory Modules Required in the Expression of the
ppcA Phosphoenolpyruvate Carboxylase Gene
in the Genus Flaveria…………………………………………………………… 14
II. Objectives……………………………………………………………………... 19
III. Theses………………………………………………………………………….. 20
IV.1 Summary………………………………………………………………..…….. 21
IV.2 Zusammenfassung………………………………………………………..…. 23
V. Literature……………………………………………………………….…….. 25
Acknowledgment/ Danksagung……………………………………………….…. 33
Manuscripts………………………………………………………………………….. 34
1) Udo Gowik, Janet Burscheidt, Meryem Akyildiz, Ute Schlue, Maria Koczor, Monika
Streubel and Peter Westhoff (2004). Cis-regulatory elements for mesophyll-specific
gene expression in the C plant Flaveria trinervia, the promoter of the C4 4
phosphoenolpyruvate carboxylase gene. The Plant Cell 16: 1077-1090.
2) Meryem Akyildiz, Udo Gowik, Maria Koczor, Monika Streubel and Peter Westhoff
(2007). Evolution and function of a cis-regulatory module for mesophyll-specific
gene expression in the C dicot Flaveria trinervia. Submitted to Plant Cell for4
publication.II
3) Meryem Akyildiz, Ming Chang Tsai, Claus Seidel and Peter Westhoff (2007). Basic
leucine zipper proteins interact with MEM1, the mesophyll specificity cis-
regulatory element of the C phosphoenolpyruvate carboxylase gene of Flaveria4
trinervia.I. General Introduction 1
I. General Introduction
I.1 C Photosynthesis4
Photosynthesis is the physico-chemical process by which plants, algae and photosynthetic
bacteria use light energy to drive the synthesis of organic compounds. In plants, algae and
certain types of bacteria, the photosynthetic process results in the release of molecular
oxygen and the removal of carbon dioxide (CO ) from the atmosphere that is used to2
synthesize carbohydrates. Based on the number of carbon compounds in the first stable
molecule, formed from the carbon dioxide fixation process, land plants can be divided into
two major photosynthetic types, namely C and C .3 4
In plants with C photosynthesis the fixation of carbohydrates is catalyzed by the3
enzyme ribulose-1,5-bisphosphate carboxylase oxygenase in which carbon dioxide is
combined with a five-carbon sugar, ribulose 1,5-bisphosphate, to yield two molecules of a
three-carbon compound, 3-phosphoglycerate, hence the name C photosynthesis. However,3
in low atmospheric carbon dioxide concentrations C photosynthesis is impaired by the lack3
of carbon dioxide as a substrate in addition to photorespiration (Furbank & Badger, 1983;
Ogren, 1984; Furbank & Taylor, 1995; von Caemmerer & Furbank, 2003). At low CO2
concentrations ribulose-1,5-bisphosphate is oxygenated by the oxygenating function of
ribulose-1,5-bisphosphate carboxylase oxygenase producing one molecule of 3-
phosphoglycerate and one molecule of phosphoglycolate (Andrews and Lorimer, 1987).
Phosphoglycolate is metabolically useless and toxic if it accumulates in the cell. The
conversion of phosphoglycolate to useful metabolites is therefore essential for land plants.
During this metabolic process, called photorespiration, CO and NH are produced and ATP2 3
and reducing equivalents are consumed, thus making photorespiration a wasteful process
(Furbank & Taylor, 1995) resulting in the loss of 25% of the carbon entering the pool of
phosphoglycolate molecules (Ogren, 1984; Leegood et al., 1995). As a result water- and
nitrogen-use efficiencies are low (Black, 1973; Ehleringer & Monson, 1993).
C plants assimilate atmospheric carbon dioxide through a sophisticated addition to4
the ancient C photosynthetic pathway. This enables C plants to cope well with high3 4
temperatures, high light intensities, drought and increased salinity. Important crop plants like
maize, sugar cane and sorghum belong to this photosynthetic type. The high photosynthetic
capacity of C plants is due to their unique mode of carbon assimilation which involves two4
different photosynthetic cell types, mesophyll and bundle-sheath cells. Recently thisI. General Introduction 2
paradigm, the requirement of two photosynthetic active cell types in the C photosynthesis4
cycle, was disproved by the identification of single-celled C photosynthesis (Voznesenskaya4
et al., 2001; Voznesenskaya et al., 2002; Edwards et al., 2004). However, this single-celled
C photosynthesis is an exceptional case rather than representing a common type of C4 4
photosynthesis.
In C photosynthesis, atmospheric carbon dioxide is first hydrated to bicarbonate4
-(HCO ) by the enzyme carbonic anhydrase (Hatch & Burnell, 1990; Badger & Price, 1994)3
in the cytosol of mesophyll cells and subsequently fixed into the C acid oxaloacetate with4
the three-carbon substrate phosphoenolpyruvate through the enzyme phosphoenolpyruvate
carboxylase (PEPC) (Figure 1). Oxaloacetate is rapidly reduced to malate in the mesophyll
chloroplasts by NADP-malate dehydrogenase or transaminated to aspartate in the cytosol by
glutamate-aspartate aminotransferase, depending on the C acid-decarboxylating mechanism4
of C plants (Hatch, 1987). These C compounds are then transported to the bundle-sheath4 4
cells where they are decarboxylated to release carbon dioxide by one of the three
decarboxylation enzymes: NADP-malic enzyme, NAD-malic enzyme or PEP carboxykinase
(Kanai &Edwards, 1999). The consequence of this decarboxylation is that carbon dioxide is
concentrated within the bundle-sheath cells. The released carbon dioxide is re-assimilated by
the bundle-sheath-specific enzyme ribulose-1,5-bisphosphate carboxylase/oxygenase in the
reductive pentose phosphate pathway (Calvin cycle) (Hatch, 1987; Dai et al., 1993; Furbank
& Taylor, 1995). The decarboxylation reaction also leaves pyruvate, which is transported
back to the mesophyll cells and phosphorylated, in a reaction catalysed by the pyruvate
orthophosphate dikinase enzyme, to regenerate phosphoenolpyruvate at the cost of a
phosphorus group and one ATP molecule.I. General Introduction 3
Figure 1. Schematic presentation of the CO concentrating mechanism in the NADP-malic enzyme type2
C plant Flaveria trinervia (Hatch, 1987).4
CA: carbonic anhydrase; GAA: glutamate-aspartate aminotransferase; MDH: NADP-malate dehydrogenase;
ME: NADP-malic enzyme; PEPC: phosphoenolpyruvate carboxylase; PEP: phosphoenolpyruvate; PPDK:
pyruvate phosphate dikinase; RUBISCO: ribulose-1,5-bisphosphate carboxylase oxygenase.
As a consequence of this carbon dioxide concentration, also referred to as CO2
pump, in the chloroplasts of bundle-sheath cells ribulose-1,5-bisphosphate
carboxylase/oxygenase operates in C plants at high carbon dioxide/oxygen ratios. The4
competitive inhibition of the carboxylating function of ribulose-1,5-bisphosphateby oxygen, which becomes prominent at higher temperatures, is
largely excluded and C plants show drastically reduced rates of photorespiration. The CO4 2
pump ensures high rates of photosynthesis even at low atmospheric carbon dioxide
concentrations, thus C plants are capable to limit the opening of their stomata and thereby4
minimize water loss through transpiration. As the carbon dioxide pump delivers saturating
carbon dioxide concentrations to the site of ribulose-1,5-bisphosphate carboxylase/oxygenase
high photosynthetic rates are maintained with three to six times less enzyme than is required
in C species. This is reflected in a higher nitrogen use efficiency (Ehleringer & Monson,3
1993; Long, 1999).I. General Introduction 4
To achieve an effective CO concentration mechanism in the C photosynthesis the2 4
distance between mesophyll and bundle-sheath cells has to decline to allow for rapid
diffusion of metabolites (Raghavendra, 1980; Ehleringer et al., 1997). The latter is
accomplished by reducing the interveinal distance. Thus the C leaves are highly4
vascularized, with veins often separated by as few as four photosynthetic active mesophyll
cells (Nelson & Langdale, 1992). The leaf thickness is limited in C eudicot plants and is4
usually smaller than in the leaves of C plants (Hattersley, 1992; McKown &am