Transitions in Photosynthetic Parameters of Midvein and Interveinal Regions of Leaves and Their Importance During Leaf Growth and Development

Abstract

The areal development of photosynthetic efficiency and growth patterns in expanding leaves of two different dicotyledonous species - Coccoloba uvifera and Sanchezia nobilis - was investigated by imaging both processes repeatedly over 32 days. Measurements were performed using combined imaging systems for chlorophyll fluorescence and growth, with the same spatial resolution. Significant differences in potential quantum yield of photosynthesis (F_v/F_m), a parameter indicating the functional status of photosystem II, were found between midvein and interveinal tissue. Although base-tip gradients and spatial patchiness were observed in the distribution of relative growth rate, neither midvein nor interveinal tissue showed such patterns in F_v/F_m. In young leaves, F_v/F_m of the midvein was higher than F_v/F_m of interveinal tissue. This difference declined gradually with time, and upon cessation of growth, F_v/F_m of interveinal regions exceeded those of midvein tissue. Images of chlorophyll fluorescence quenching showed that ΔF/F_m′ in the different tissues correlated with F_v/F_m, indicating that, in these uniformly illuminated leaves, transitions in photosynthetic electron transport activity follow those of predawn quantum efficiency. We explore the implications of these observations during leaf development, discuss effects of sucrose delivery from veins to interveinal areas on relative rates of photosynthetic development in these tissues, and propose that the initially higher photosynthetic activity in the midvein compared to the intervein tissues may supply carbohydrates and energy for leaf growth processes.

Key words

Chlorophyll fluorescence - imaging - spatio-temporal dynamics - pattern formation - Coccoloba uvifera - Sanchezia nobilis.

References

• 1 Avery G. S.. Structure and development of tobacco leaves.  American Journal of Botany. (1933);  20 565-592
• 2 Baker N. R., Oxborough K., Lawson T., Morison J. I. L.. High resolution imaging of photosynthetic activities of tissues, cells and chloroplasts in leaves.  Journal of Experimental Botany. (2001);  52 615-621
• 3 Bilger W., Schreiber U., Bock M.. Determination of the quantum efficiency of photosystem II and of non-photochemical quenching of chlorophyll fluorescence in the field.  Oecologia. (1995);  102 425-432
• 4 Croxdale J. G., Omasa K.. Patterns of chlorophyll fluorescence kinetics in relation to growth and expansion in cucumber leaves.  Plant Physiology. (1990);  93 1083-1088
• 5 Daley P. F., Raschke K., Ball J. T., Berry J. A.. Topography of photosynthetic activity of leaves obtained from video images of chlorophyll fluorescence.  Plant Physiology. (1989);  90 1233-1238
• 6 Dengler N. G., Dengler R. E., Donnelly P. M., Filosa M. F.. Expression of the C₄ pattern of photosynthetic enzyme accumulation during leaf development in Atriplex rosea (Chenopodiaceae).  American Journal of Botany. (1995);  82 318-327
• 7 Edwards G. E., Baker N. R.. Can CO₂ assimilation in maize leaves be predicted accurately from chlorophyll fluorescence analysis?.  Photosynthesis Research. (1993);  37 89-102
• 8 Edwards G. E., Furbank R. T., Hatch M. D., Osmond C. B.. What does it take to be C₄? Lessons from the evolution of C₄ photosynthesis.  Plant Physiology. (2001);  125 46-49
• 9 Esau K.. Plant Anatomy. New York; Wiley (1965)
• 10 Evans J. R., Vogelmann T. C.. Profiles of ¹⁴C fixation through spinach leaves in relation to light absorption and photosynthetic capacity.  Plant, Cell and Environment. (2003);  26 547-560
• 11 Gamalei Y. V.. Assimilate transport and partitioning in plants: approaches, methods, and facets of research.  Russian Journal of Plant Physiology. (2002);  49 16-31
• 12 Genty B., Briantais J. M., Baker N. R.. The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence.  Biochemica and Biophysica Acta. (1989);  990 87-92
• 13 Genty B., Meyer S.. Quantitative mapping of leaf photosynthesis using chlorophyll fluorescence imaging.  Australian Journal of Plant Physiology. (1994);  22 277-284
• 14 Gerendas J., Schurr U.. Physicochemical aspects of ion relations and pH regulation in plants: a quantitative approach.  Journal of Experimental Botany. (1999);  50 1101-1114
• 15 Haritatos E., Ayre B. G., Turgeon R.. Identification of phloem involved in assimilate loading in leaves by the activity of the galactinol synthase promoter.  Plant Physiology. (2000);  123 929-937
• 16 Hibberd J. M., Quick P. W.. Characteristics of C₄ photosynthesis in stems and petioles of C₃ flowering plants.  Nature. (2002);  415 451-454
• 17 Kinsman E. A., Pyke K. A.. Bundle sheath cells and cell-specific plastid development in Arabidopsis leaves.  Development. (1998);  125 1815-1822
• 18 Koch K. E.. Carbohydrate-modulated gene expression in plants.  Annual Review of Plant Physiology and Plant Molecular Biology. (1996);  47 509-540
• 19 Lichtenthaler H. K., Lang M., Sowinska M., Heisel F., Miehé J. A.. Detection of vegetation stress via a new high resolution fluorescence imaging system.  Journal of Plant Physiology. (1996);  148 599-612
• 20 Liu Y., Dengler N. G.. Bundle sheath and mesophyll cell differentiation in the C₄ dicotyledon Atriplex rosea: Quantitative ultrastructure.  Canadian Journal of Botany. (1994);  72 644-657
• 21 Lu C. M., Zhang J. H.. Photosynthetic CO₂ assimilation, chlorophyll fluorescence and photoinhibition as affected by nitrogen deficiency in maize plants.  Plant Science. (2000);  151 135-143
• 22 Maxwell K., Johnson G. N.. Chlorophyll fluorescence - a practical guide.  Journal of Experimental Botany. (2000);  51 659-668
• 23 Meng Q., Siebke K., Lippert P., Baur B., Mukherjee U., Weis E.. Sink-source transition in tobacco leaves visualized using chlorophyll fluorescence imaging.  New Phytologist. (2001);  151 585-595
• 24 Nedbal L., Soukupová J., Kaftan D., Whitmarsh J., Trtílek M.. Kinetic imaging of chlorophyll fluorescence using modulated light.  Photosynthesis Research. (2000);  66 3-12
• 25 Nelson T., Dengler N.. Leaf vascular pattern formation.  The Plant Cell. (1997);  9 1121-1135
• 26 Osmond C. B., Daley P. F., Badger M. R., Lüttge U.. Chlorophyll fluorescence quenching during photosynthetic induction in leaves of Abutilon striatum Dicks. infected with Abutilon mosaic virus, observed with a field-portable imaging system.  Botanica Acta. (1998);  111 390-397
• 27 Osmond C. B., Kramer D., Lüttge U.. Reversible, water stress-induced non-uniform chlorophyll fluorescence quenching in wilting leaves of Potentilla reptans may not be due to patchy stomatal responses.  Plant Biology. (1999);  1 618-624
• 28 Poethig R. S., Sussex I. M.. The developmental morphology and growth dynamics of tobacco leaf.  Planta. (1985);  165 158-169
• 29 Rascher U., Hütt M. T., Siebke K., Osmond C. B., Beck F., Lüttge U.. Spatio-temporal variations of metabolism in a plant circadian rhythm: the biological clock as an assembly of coupled individual oscillators.  Proceedings of the National Academy of Sciences USA. (2001);  98 11801-11805
• 30 Rascher U., Lüttge U.. High-resolution chlorophyll fluorescence imaging serves as a non-invasive indicator to monitor the spatio-temporal variations of metabolism during the day-night cycle and during the endogenous rhythm in continuous light in the CAM-plant Kalanchoë daigremontiana. .  Plant Biology. (2002);  4 671-681
• 31 Roberts A. G., Santa Cruz S., Roberts I. M., Prior D. A. M., Turgeon R., Oparka K. J.. Phloem unloading in sink leaves of Nicotiana benthamiana: comparison of a fluorescent solute with a fluorescent virus.  The Plant Cell. (1997);  9 1381-1396
• 32 Rolfe S. A., Scholes J. D.. Quantitative imaging of chlorophyll fluorescence.  New Phytologist. (1995);  131 69-79
• 33 Schmundt D., Stitt M., Jähne B., Schurr U.. Quantitative analysis of the local rates of growth of dicot leaves at a high temporal and spatial resolution, using image sequence analysis.  The Plant Journal. (1998);  16 505-514
• 34 Schreiber U., Bilger W.. Progress in chlorophyll fluorescence research: major developments during the past years in retrospect.  Proceedings in Botany. (1993);  53 151-173
• 35 Schreiber U., Bilger W., Neubauer C.. Chlorophyll fluorescence as a nonintrusive indicator for rapid assessment of in vivo photosynthesis. In Ecological Studies, Vol. 100. Berlin, Heidelberg, New York; Springer-Verlag (1994): 49-70
• 37 Siebke K., Weis E.. Assimilation images of leaves of Glechoma hederacea: analysis of non-synchronous stomata related oscillations.  Planta. (1995 a);  196 155-165
• 38 Siebke K., Weis E.. Imaging of chlorophyll-a-fluorescence in leaves: Topography of photosynthetic oscillations in leaves of Glechoma hederacea. .  Photosynthesis Research. (1995 b);  45 225-237
• 39 Siffel P., Santrucek J., Lang M., Braunova Z., Simkova M., Synkova H., Lichtenthaler H. K.. Age dependence of photosynthetic activity, chlorophyll fluorescence parameters and chloroplast ultrastructure in aurea and green forms of Nicotiana tabacum Su/su mutant.  Photosynthetica. (1993);  29 81-94
• 40 Vaughn M. W., Harrington G. N., Bush D. R.. Sucrose-mediated transcriptional regulation of sucrose symporter activity in the phloem.  Proceedings of the National Academy of Sciences USA. (2002);  99 10876-10880
• 41 Vogelmann T. C., Evans J. R.. Profiles of light absorption and chlorophyll within spinach leaves from chlorophyll fluorescence.  Plant, Cell and Environment. (2002);  25 1313-1323
• 42 Walter A., Schurr U.. Spatial variability of leaf development, growth and function. Marshall, B. and Roberts, J., eds. Leaf Development and Canopy Growth. Sheffield; Sheffield Academic Press (2000): 96-118
• 43 Walter A., Feil R., Schurr U.. Restriction of nyctinastic movements and application of tensile forces on leaves affects diurnal patterns of expansion growth.  Functional Plant Biology. (2002);  29 1247-1258
• 44 Wright K. M., Roberts A. G., Martens H. J., Sauer N., Oparka K. J.. Structural and functional vein maturation in developing tobacco leaves in relation to AtSUC2 promoter activity.  Plant Physiology. (2003);  131 1555-1565

Section Editor: M. C. Ball