Abstract
Heteroblastic Eucalyptus (Eucalyptus globulus L.) leaves were characterized for their functional diversity examining photosynthesis and photosynthesis limitations, transpiration, and the emission of isoprene and monoterpenes. In vivo and combined analyses of gas-exchange, chlorophyll fluorescence, and light absorbance at 830 nm were made on the adaxial and abaxial sides of juvenile and adult leaves. When adult leaves were reversed to illuminate the abaxial side, photosynthesis and isoprene emission were significantly lower than when the adaxial side was illuminated. Monoterpene emission, however, was independent on the side illuminated and similarly partitioned between the two leaf sides. The abaxial side of adult leaves showed less diffusive resistance to CO2 acquisition by chloroplasts, but also lower ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco) activity, than the adaxial leaf side. In juvenile leaves, photosynthesis, isoprene, and monoterpene emissions were similar when the adaxial or abaxial side was directly illuminated. In the abaxial side of juvenile leaves, photosynthesis did not match the rates attained by the other leaf types when exposed to elevated CO2 , which suggests the occurrence of a limitation of photosynthesis by ribulose bisphosphate (RuBP) regeneration. Accordingly, a reduced efficiency of both photosystems and a high non-radiative dissipation of energy was observed in the abaxial side of juvenile leaves. During light induction, the adaxial side of juvenile leaves also showed a reduced efficiency of photosystem II and a large non-radiative energy dissipation. Our report reveals distinct functional properties in Eucalyptus leaves. Juvenile leaves invest more carbon in isoprene, but not in monoterpenes, and have a lower water use efficiency than adult leaves. Under steady-state conditions, in adult leaves the isobilateral anatomy does not correspond to an equal functionality of the two sides, while in juvenile leaves the dorsiventral anatomy does not result in functional differences in primary or secondary metabolism in the two sides. However, photochemical limitations may reduce the efficiency of carbon fixation in the light, especially in the abaxial side of juvenile leaves.
Key words
Eucalyptus
- fluorescence - isoprene - monoterpenes - heteroblastic leaves - photochemistry - photosynthesis (limitations).
References
1
Bilger W., Bjorkmann O..
Relationship among violaxanthin deepoxidation, thylakoid membranes conformation, non-photochemical chlorophyll fluorescence quenching in leaves of cotton (Gossypium hirsutum L.).
Planta.
(1994);
193
238-246
2
Chameides W. L., Lindsay R. W., Richardson J., Kiang C. S..
The role of biogenic hydrocarbons in urban photochemical smog: Atlanta as a case study.
Science.
(1988);
241
1473-1475
3
Delfine S., Alvino A., Zacchini M., Loreto F..
Consequences of salt stress on diffusive conductances, Rubisco characteristics and anatomy of spinach leaves.
Australian Journal of Plant Physiology.
(1998);
25
395-402
4
Demmig-Adams B., Adams W. W..
Photoprotection and other responses of plants to high light stress.
Annual Review of Plant Physiology and Plant Molecular Biology.
(1992);
43
599-626
5
Demmig-Adams B., Adams W. W., Barker D. H., Logan B. A., Bowling D. R., Verhoeven A. S..
Using chlorophyll fluorescence to assess the fraction of absorbed light allocated to thermal dissipation of excess excitation.
Physiologia Plantarum.
(1996);
98
253-264
6
Endo T., Kawase D., Sato F..
Stromal over-reduction by high light stress as measured by decreases in P700 oxydation by far-red light and its physiological relevance.
Plant Cell Physiology.
(2005);
46
775-781
7
Fall R., Monson R. K..
Isoprene emission rate in relation to stomatal distribution and stomatal conductance.
Plant Physiology.
(1992);
100
987-992
8
Farquhar G. D., von Caemmerer S., Berry J. A..
A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species.
Planta.
(1980);
149
78-90
9 Genty B., Harbinson J.. Regulation of light utilization for photosynthetic electron transport. Baker, N. R., ed. Photosynthesis and the Environment. Dordrecht; Kluwer (1997): 67-99
10
Genty B., Briantais J.-M., Baker N. R..
The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence.
Biochimica et Biophysica Acta.
(1989);
990
87-92
11
Guenther A. B., Monson R. K., Fall R..
Isoprene and monoterpene emission rate variability: observations with eucalyptus and emission rate algorithm development.
Journal of Geophysical Research.
(1991);
96
10799-10808
12
Harbinson J., Genty B., Baker N. R..
Relationship between the quantum yield of photosystems I and II in pea leaves.
Plant Physiology.
(1989);
90
1029-1034
13
He C., Murray F., Lyons T..
Monoterpene and isoprene emissions from 15 Eucalyptus species in Australia.
Atmospheric Environment.
(2000);
34
645-655
14
James S. A., Bell D. T..
Leaf morphological and anatomical characteristics of heteroblastic Eucalyptus globulus spp. Globulus (Myrtacee).
Australian Journal of Botany.
(2001);
49
259-269
15
James S. A., Bell D. T..
Leaf orientation, light interception and stomatal conductance of Eucalyptus globulus spp. globulus leaves.
Tree Physiology.
(2000);
20
815-823
16
James S. A., Smith W. K., Vogelmann T. C..
Ontogenetic differences in mesophyll structure and chlorophyll distribution in Eucalyptus globulus spp. Globulus (Myrtacee).
American Journal of Botany.
(1999);
86
198-207
17
Johnson E. D..
A comparison of the juvenile and adult leaves of Eucalyptus globulus .
New Phytologist.
(1926);
25
202-212
18
Lawler I. R., Stapley J., Foley W. J., Eschler B. M..
Ecological example of conditioned flavour aversion in plant-herbivore interactions: effect of terpenes of Eucalyptus leaves on feeding by common ringtail and brushtail possums.
Journal of Chemical Ecology.
(1999);
25
401-415
19
Lichtenthaler H. K., Schwendler J., Disch A., Rohmer M..
Biosynthesis of isoprenoids in higher plant chloroplasts proceeds via a mevalonate-independent pathway.
FEBS Letters.
(1997);
400
271-274
20
Loreto F., Velikova V..
Isoprene produced by leaves protects the photosynthetic apparatus against ozone damage, quenches ozone products, and reduces lipid peroxidation of cellular membranes.
Plant Physiology.
(2001);
127
1781-1787
21
Loreto F., Nascetti P., Graverini A., Mannozzi M..
Emission and content of monoterpenes in intact and wounded needles of the Mediterranean pine Pinus pinea .
Functional Ecology.
(2000);
14
589-595
22
Loreto F., Ciccioli P., Cucinato A., Brancaleoni E., Frattoni M., Tricoli D..
Influence of environmental factors and air composition on the emission of α-pinene from Quercus ilex leaves.
Plant Physiology.
(1996);
110
267-275
23
Loreto F., Di Marco G., Tricoli D., Sharkey T. D..
Measurements of mesophyll conductance, photosynthetic electron transport and alternative electron sinks of field grown wheat leaves.
Photosynthesis Research.
(1994);
41
397-403
24
Miyake C., Shinkazi Y., Miyata M., Tomizawa K..
Enhancement of cyclic electron flow around PSI at high light and its contribution to the induction of non-photochemical quenching of Chl fluorescence in intact leaves of tobacco plants.
Plant Cell Physiology.
(2004);
45
1426-1433
25
Pieruschka R., Schurr U., Jahnke S..
Lateral gas diffusion inside leaves.
Journal of Experimental Botany.
(2005);
56
857-864
26
Schreiber U., Klughammer C., Neubauer C..
Measuring P700 absorbance changes around 830 nm with a new type of pulse modulation system.
Zeitschrift für Naturforschung Teil C.
(1988);
43
686-698
27
Sharkey T. D., Yeh S..
Isoprene emission from plants.
Annual Review of Plant Physiology and Plant Molecular Biology.
(2001);
52
407-436
28
Sharkey T. D., Singsaas E. L..
Why plants emit isoprene.
Nature.
(1995);
374
769
29
Van Kooten O., Snel J. F. H..
The use of chlorophyll fluorescence nomenclature in plant stress physiology.
Photosynthesis Research.
(1990);
25
147-150
30
Weis E., Lechtenberg D..
Fluorescence analysis during steady-state photosynthesis.
Philosophical Transcripts of the Royal Society of London, Section B.
(1989);
323
253-268
31
Wong S.-C., Cowan I. R., Farquhar G. D..
Leaf conductance in relation to rate of CO2 assimilation.
Plant Physiology.
(1985);
78
826-829
V. Velikova
Institute of Plant Physiology Bulgarian Academy of Sciences
Acad. G. Bonchev Street, Bl. 21
1113 Sofia
Bulgaria
Email: violet@bio21.bas.bg
Editor: H. Rennenberg