Abstract
Sulfur metabolite levels and sulfur metabolism have been studied in a significant number of herbaceous and woody plant species. However, only a limited number of datasets are comparable and can be used to identify similarities and differences between these two groups of plants. From these data, it appears that large differences in sulfur metabolite levels, as well as the genetic organization of sulfate assimilation and metabolism do not exist between herbaceous plants and trees. The general response of sulfur metabolism to internal and/or external stimuli, such as oxidative stress, seems to be conserved between the two groups of plants. Thus, it can be expected that, generally, the molecular mechanisms of regulation of sulfur metabolism will also be similar. However, significant differences have been found in fine tuning of the regulation of sulfur metabolism and in developmental regulation of sulfur metabolite levels. It seems that the homeostasis of sulfur metabolism in trees is more robust than in herbaceous plants and a greater change in conditions is necessary to initiate a response in trees. This view is consistent with the requirement for highly flexible defence strategies in woody plant species as a consequence of longevity. In addition, seasonal growth of perennial plants exerts changes in sulfur metabolite levels and regulation that currently are not understood. In this review, similarities and differences in sulfur metabolite levels, sulfur assimilation and its regulation are characterized and future areas of research are identified.
Key words
Adenosine 5′-phosphosulfate reductase (APR) - cell differentiation - compartmentation - cysteine - genetic engineering - glutathione - methionine - plant development - protein - ozone - oxidative stress - sulfate - sulfate assimilation - transgenic poplar.
References
(Fagus sylvatica) and Norway spruce (Picea abies) trees in a mixed forest stand.
Plant Biology.
(2007);
9
227-241
(Populus tremula × P. alba) overexpressing enzymes involved in glutathione synthesis.
Planta.
(1997);
203
362-372
Arabidopsis .
Plant Cell.
(2004);
16
2448-2462
(Picea abies) and pine (Pinus sylvestris ) needles.
Physiologia Plantarum.
(1998);
104
248-254
Picea abies [Karst] L.).
Journal of Experimental Botany.
(1996);
47
1025-1032
2 in soybean.
Journal of Experimental Botany.
(2005);
56
2139-2151
Phaseolus vulgaris cultivars under ozone stress.
Phyton - Annales Rei Botanicae.
(2005);
45
279-293
2 and assimilatory sulfate reduction in beech leaves.
Physiologia Plantarum.
(1983);
59
313-318
Spinacia oleracea L.) to ozone measured by gas exchange, chlorophyll a fluorescence, antioxidant systems, and lipid peroxidation.
Photosynthetica.
(2004);
42
23-29
Arabidopsis genes required for cell proliferation at the root tip.
Plant Physiology.
(1995);
107
365-376
2 and O3 .
Oecologia.
(2006);
147
143-154
cad2-1, of Arabidopsis thaliana is deficient in γ-glutamylcysteine synthetase.
The Plant Journal.
(1998);
16
73-78
2 S as sulphur source for sulphur deprived Brassica oleracea L.
Botanica Acta.
(1997);
110
411-419
2 O2 , ethylene and salicylic acid.
New Phytologist.
(2005);
168
351-364
Picea abies [L] Karst) exposed to drought and ozone.
Water, Air and Soil Pollution.
(1994);
78
153-168
Allium cepa L., a species with a potential sink capacity for secondary sulfur compounds.
Journal of Experimental Botany.
(2004);
55
1821-1830
Picea abies .
Plant Physiology.
(1978);
61
119-121
Arabidopsis .
Journal of Microscopy.
(2000);
198
162-173
(Picea abies) and beech (Fagus sylvatica) trees.
New Phytologist.
(1998);
138
275-285
Populus leaves.
Plant Physiology.
(1991);
96
650-655
2 and troposphere O3 .
New Phytologist.
(2005);
167
633
Arabidopsis trichome cells.
Proceedings of the National Academy of Sciences of the USA.
(2000);
97
11108-11113
Phaseolus vulgaris L).
New Phytologist.
(1993);
124
617-625
15 N and total N in Fagus sylvatica and associated mycorrhizal fungi.
Plant Biology.
(2007 a);
9
242-252
(Fagus sylvatica) under elevated O3 in a free air exposure system.
Plant Biology.
(2007 b);
9
215-226
2 O2 - combination of enzyme catalysis with a subsequent non-enzymatic reaction step.
Journal of Biological Chemistry.
(2006);
281
6884-6888
(Populus tremula × P. alba) of wild type and overexpressing γ-glutamylcysteine synthetase in the cytosol.
Journal of Experimental Botany.
(2004 a);
55
837-845
(Populus tremula × P. alba) leaves.
Journal of Experimental Botany.
(2000);
51
1077-1088
Zinnia Cells and Arabidopsis roots.
Plant Cell Physiology.
(2005);
46
1757-1765
Zinnia elegans .
Plant Cell Physiology.
(2001);
42
673-676
Fagus sylvatica under experimental free-air ozone exposure.
Environmental Pollution.
(2005);
137
476-482
Sulfur nutrition of deciduous trees at different environmental growth conditions. Davidian, J.-C., Grill, D., De Kok, L. J., Stulen, H., Hawkesford, M. J., Schnug, E., and Rennenberg, H., eds. Sulfur Transport and Assimilation in Plants: Regulation, Interaction, Signaling. Leiden; Backhuys Publishers (2003): 111-119
2 S or SO2 : does atmospheric sulfur affect the “inter-organ” regulation of sulfur nutrition.
Botanica Acta.
(1995);
108
41-46
2 S.
Plant Physiology.
(2000);
124
461-473
Arabidopsis thaliana .
Plant Physiology.
(1995 b);
107
1067-1073
Arabidopsis thaliana are phytochelatine deficient.
Plant Physiology.
(1995 a);
107
1059-1066
Fagus sylvatica L.) trees.
Plant Biology.
(2007);
9
253-264
Arabidopsis thaliana .
Photosynthesis Research.
(2005);
86
491-508
Arabidopsis and beyond.
Annals of Botany.
(2006);
97
479-495
Zea mays .
Plant Biology.
(2001);
3
24-31
Lemna minor .
Plant Physiology.
(2002);
130
1406-1413
Physcomitrella patens revives an old route of sulfate assimilation.
Journal of Biological Chemistry.
(2002);
277
32195-32201
Arabidopsis .
Plant Physiology.
(2000);
122
737-746
Picea abies trees.
Tree Physiology.
(1998);
18
1-9
Sulfate uptake by mycorrhizal (Laccaria laccata) and non-mycorrhizal roots of beech (Fagus sylvatica) trees. Cram, W., De Kok, L. J., Stulen, I., Brunold, C., and Rennenberg, H., eds. Sulfur Metabolism in Higher Plants. Leiden; Backhuys Publishers (1997 b): 165-168
Fagus sylvatica L.) roots.
Journal of Experimental Botany.
(1997 a);
48
1431-1438
Ethylen and jasmonate as regulators of cell death in desease resistance. Sandermann, H., ed. Molecular Ecotoxicology of Plants. Berlin, Heidelberg; Springer Verlag (2004): 75-109
4
2- uptake in intact canola. The role of phloem-translocated glutathione.
Plant Physiology.
(1996);
111
147-157
2 and/or pO3 on C-, N-, and S-metabolites in the leaves of juvenile beech and spruce differ between trees grown in monoculture and mixed culture.
Plant Physiology and Biochemistry.
(2005);
43
147-154
Arabidopsis thaliana .
Physiologia Plantarum.
(1994);
92
322-328
Arabidopsis is higly controlled by adenosine 5′-phosphosulfate reductase.
Nature Genetics.
(2007);
Fagus sylvatica L.) leaves: seasonal variations and responses to changing ozone concentrations in air.
Plant, Cell and Environment.
(1996);
19
321-328
Plantago major : apoplastic and symplastic antioxidant status.
New Phytologist.
(1999);
141
253-263
Met25 gene of Saccharomyces cerevisiae exhibited enhanced levels of cysteine and glutathione and increased tolerance to oxidative stress.
Amino Acids.
(2006);
30
185-194
2 concentration: ozone exclusion and detoxification.
New Phytologist.
(1997);
137
275-284
Arabidopsis roots by two-photon laser scanning microscopy.
Journal of Microscopy.
(2000);
198
174-181
Arabidopsis suspension culture cells.
Plant Physiology.
(2002);
130
1927-1937
in vivo measurements of glutathione in Arabidopsis cells.
The Plant Journal.
(2001);
27
67-78
Curcurbita pepo plants.
Protoplasma.
(2004);
223
213-219
Arabidopsis root quiescent center.
Plant Cell.
(2005);
17
1908-1925
Arabidopsis thaliana : mechanism of strong interaction of light intensity with flowering.
Plant Cell Physiology.
(2004);
45
1-8
Arabidopsis thaliana .
Plant Cell Physiology.
(2001);
42
524-530
Arabidopsis mutant that overaccumulates O-acetyl-L‐Ser.
Plant Physiology.
(2004);
136
3209-3222
Fagus sylvatica L.).
Plant Biology.
(2005);
7
670-676
Arabidopsis rcd1 mutant reveals opposite roles for ethylene and jasmonate signaling pathways in regulating superoxide-dependent cell death.
Plant Cell.
(2000);
12
1849-1862
2 O2 detoxification in elongating leaf bases of ryegrass: effect of inhibition of glutathione reductase activity on foliar regrowth.
Physiologia Plantarum.
(2002);
116
406-415
Pinus sylvestris L.) from three SO2 -polluted field sites in eastern Germany.
New Phytologist.
(1994);
127
571-577
Fagus sylvatica L.) trees: seasonal changes in the axial distribution of sulfur compounds.
Tree Physiology.
(1994);
14
541-548
Arabidopsis .
Plant Physiology.
(2004);
136
3784-3794
Brassica napus .
Planta.
(2002);
214
965-969
Arabidopsis root are under mechanistically different forms of redox control.
Proceedings of the National Academy of Sciences of the USA.
(1997);
94
2745-2750
Arabidopsis .
The Plant Journal.
(2005);
44
653-668
Populus × canadensis “robusta”).
Canadian Journal of Botany.
(1994 b);
72
347-351
Picea abies [Karst.] L.).
Journal of Experimental Botany.
(1994 a);
45
457-462
Long term effects of naturally elevated CO2 , H2 S and SO2 on sulfur allocation in Quercus . Cram, W. J., De Kok, L. J., Stulen, I., Brunold, C., and Rennenberg, H., eds. Sulphur Metabolism in Higher Plants. Leiden; Backhuys Publishers (1997): 289-291
Quercus ilex L. at natural CO2 springs acclimates sulfur, nitrogen and carbohydrate metabolism of the progeny to elevated p CO2 .
Plant, Cell and Environment.
(2002);
25
1715-1727
Picea abies L.).
Journal of Experimental Botany.
(1992);
43
1243-1250
Quercus robur L.).
Plant and Soil.
(2002);
242
291-297
2 on sulphur nutrition of young pedunculate oak (Quercus robur L.) trees.
Plant, Cell and Environment.
(1996);
19
418-426
(Populus tremula × P. alba) over-expressing glutathione synthetase or glutathione reductase.
Trees.
(2002);
16
262-273
(Populus tremula × P. alba) overexpressing glutathione synthetase.
The Plant Journal.
(1995);
7
141-145
Arabidopsis accessions and its relevance to ethylene synthesis.
Planta.
(2003);
216
552-560
(Vaccinium myrtillus) in response to trace gases (CO2 , O3 ) and nitrogen fertilization.
Physiologia Plantarum.
(1997);
101
192-198
2 and O3 on antioxidative and photoprotective defense systems in needles of ponderosa pine.
Biologia Plantarum.
(2004 a);
48
543-548
Arabidopsis thaliana expressing 5′-adenylylsulfate reductase from Pseudomonas aeruginosa .
The Plant Journal.
(2002);
32
879-889
2 on the activity of adenosine 5′-phosphosulfate sulfotransferase from spruce trees (Picea abies) in fumigation chambers and under field conditions.
Physiologia Plantarum.
(1986);
67
235-241
Arabidopsis thaliana : adenosine 5′-phosphosulfate reductase is more susceptible to negative control by thiols than ATP sulphurylase.
The Plant Journal.
(2002);
31
729-740
ROOT MERISTEMLESS1/CADMIUM SENSITIVE2 gene defines a glutathione-dependent pathway involved in initiation and maintenance of cell division during postembryonic root development.
Plant Cell.
(2000);
12
97-109
Cucurbita maxima .
Plant Physiology and Biochemistry.
(2001);
39
121-127
2 S in the shoot and sulphate uptake by the roots of curly kale (Brassica oleracea) .
Physiologia Plantarum.
(2000);
109
443-449
2 S as sulfur source for Brassica oleracea : consequences for the activity of the enzymes of the assimilatory sulphate reduction pathway.
Plant Physiology and Biochemistry.
(2001);
39
425-432
Pinus cembra L. needles as affected by ozone exposure.
Biologia Plantarum.
(2001);
44
225-232
Arabidopsis era.
Trends in Plant Science.
(2002);
7
263-270
Arabidopsis transgenic plants with altered glutathione levels.
Plant Physiology.
(2001);
126
564-574
Populus tremuloides differing in sensitivity to ozone in the field.
New Phytologist.
(1999 a);
141
411-421
Populus tremuloides to dynamic ozone exposure under controlled environmental conditions.
New Phytologist.
(1999 b);
143
305-313
1 Dedicated to Prof. Dr. L. Bergmann at the occasion of his 80th birthday.
heinz.rennenberg@ctp.uni-freiburg.de
Guest Editor: T. Rausch
