Developmental stages of delayed-greening leaves inferred from measurements of chlorophyll content and leaf growth
Andrzej Stefan Czech A B , Kazimierz Strzałka B , Ulrich Schurr A and Shizue Matsubara A CA Institut Phytosphäre, ICG-3, Forschungszentrum Jülich, 52425 Jülich, Germany.
B Wydział Biochemii, Biofizyki i Biotechnologii, Uniwersytet Jagielloński, ul. Gronostajowa 7, 30-387 Kraków, Poland.
C Corresponding author. Email: s.matsubara@fz-juelich.de
Functional Plant Biology 36(7) 654-664 https://doi.org/10.1071/FP09035
Submitted: 11 February 2009 Accepted: 20 April 2009 Published: 2 July 2009
Abstract
Chlorophyll (Chl) accumulation and leaf growth were analysed in delayed-greening leaves of Theobroma cacao (L.) to examine whether these parameters are correlated during leaf development and can be used as non-destructive indicators of leaf developmental stages. There was a clear correlation between Chl content and leaf relative growth rate (RGR) and between Chl content and percentage of full leaf expansion (%FLE) under different growth conditions. Five distinct developmental phases were defined according to the correlation between these parameters and corroborated by data from the analyses of leaf growth (epidermal cell size and specific leaf area) or photosynthetic properties (maximal PSII efficiency, CO2 assimilation and non-structural carbohydrate contents). The five phases were characterised by rapid leaf expansion by cell division (I), pronounced cell expansion (II), development of photosynthetic capacity concomitant with reinforcement of leaf structure (III), and maturation (IV and V). The transition from cell division to cell expansion happened uniformly across the leaf lamina between phase I and II; the sink-to-source transition was found between phase III and IV. These results demonstrate coordinated development of photosynthetic machinery and leaf structure in delayed-greening leaves and provide a simple and non-invasive method for estimation of leaf developmental stages in T. cacao.
Additional keywords: chloroplast development, leaf development, leaf expansion, leaf growth, photosynthesis, Theobroma cacao.
Acknowledgements
The work of ASC at the Institut Phytosphäre (ICG-3) was supported by a Forschungszentrum Jülich scholarship.
Abo-Hamed S,
Collin HA, Hardwick K
(1983) Biochemical and physiological aspects of leaf development in cocoa (Theobroma cacao L.) VII. Growth, orientation, surface structure and water loss from developing flush leaves. New Phytologist 95, 9–17.
| Crossref | GoogleScholarGoogle Scholar |
Acevedo E,
Fereres E,
Hsiao TC, Henderson DW
(1979) Diurnal growth trends, water potential, and osmotic adjustment of maize and sorghum leaves in the field. Plant Physiology 64, 476–480.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Avery GS
(1933) Structure and development of the tobacco leaf. American Journal of Botany 20, 565–592.
| Crossref | GoogleScholarGoogle Scholar |
Baker NR, Hardwick K
(1973) Biochemical and physiological aspects of leaf development in cocoa (Theobroma cacao) I. Development of chlorophyll and photosynthetic activity. New Phytologist 72, 1315–1324.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Baker NR, Hardwick K
(1975) Biochemical and physiological aspects of leaf development in cocoa (Theobroma cacao) III. Changes in soluble sugar content and sucrose synthesizing capacity. New Phytologist 75, 519–524.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Baker NR,
Hardwick K, Jones P
(1975) Biochemical and physiological aspects of leaf development in cocoa (Theobroma cacao) II. Development of chloroplast ultrastructure and carotenoids. New Phytologist 75, 513–518.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Boardman NK
(1977) Comparative photosynthesis of sun and shade plants. Annual Review of Plant Physiology 28, 355–377.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Boussiba S, Richmond AE
(1980) C-Phycocyanin as a storage protein in the blue-green alga Spirulina platensis. Archives of Microbiology 125, 143–147.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Cai Z-Q,
Slot M, Fan Z-X
(2005) Leaf development and photosynthetic properties of three tropical tree species with delayed greening. Photosynthetica 43, 91–98.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Fujita Y
(1996) Protochlorophyllide reduction: a key step in the greening of plants. Plant & Cell Physiology 37, 411–421.
|
CAS |
PubMed |
Givnish TJ
(1988) Adaptation to sun and shade: a whole-plant perspective. Australian Journal of Plant Physiology 15, 63–92.
| Crossref | GoogleScholarGoogle Scholar |
Gould KS,
Kuhn DN,
Lee DW, Oberbauer SF
(1995) Why leaves are sometimes red. Nature 378, 241–242.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Ho LC,
Hurd RG,
Ludwig LJ,
Shaw AF,
Thornley JHM, Withers AC
(1984) Changes in photosynthesis, carbon budget and mineral content during the growth of the first leaf of cucumber. Annals of Botany 54, 87–101.
|
CAS |
Jones MGK,
Outlaw WH, Lowry OH
(1977) Enzymatic assay of 10–7 to 10–14 moles of sucrose in plant tissues. Plant Physiology 60, 379–383.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Koike T
(1990) Autumn coloring, photosynthetic performance and leaf development of deciduous broad-leaved trees in relation to forest succession. Tree Physiology 7, 21–32.
| PubMed |
Kursar TA, Coley PD
(1992a) Delayed greening in tropical leaves: an antiherbivore defense? Biotropica 24, 256–262.
| Crossref | GoogleScholarGoogle Scholar |
Kursar TA, Coley PD
(1992b) Delayed development of the photosynthetic apparatus in tropical rain-forest species. Functional Ecology 6, 411–422.
| Crossref | GoogleScholarGoogle Scholar |
Lai I-L,
Scharr H,
Chavarría-Krauser A,
Küsters R,
Wu J-T,
Chou C-H,
Schurr U, Walter A
(2005) Leaf growth dynamics of two congener gymnosperm tree species reflect the heterogeneity of light intensities given in their natural ecological niche. Plant, Cell & Environment 28, 1496–1505.
| Crossref | GoogleScholarGoogle Scholar |
Landhäusser SM, Lieffers VJ
(2003) Seasonal changes in carbohydrate reserves in mature northern Populus tremuloides clones. Trees (Berlin) 17, 471–476.
| Crossref | GoogleScholarGoogle Scholar |
Lebedev N, Timko MP
(1998) Protochlorophyllide photoreduction. Photosynthesis Research 58, 5–23.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Li J-Y,
Liu X-H,
Cai Q-S,
Gu H,
Zhang S-S,
Wu Y-Y, Wang C-J
(2008) Effects of elevated CO2 on growth, carbon assimilation, photosynthate accumulation and related enzymes in rice leaves during sink-source transition. Journal of Integrative Plant Biology 50, 723–732.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Lichtenthaler HK,
Ač A,
Marek MV,
Kalina J, Urban O
(2007) Differences in pigment composition, photosynthetic rates and chlorophyll fluorescence images of sun and shade leaves of four tree species. Plant Physiology and Biochemistry 45, 577–588.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Marini RP, Barden JA
(1981) Seasonal correlations of specific leaf weight to net photosynthesis and dark respiration of apple leaves. Photosynthesis Research 2, 251–258.
| Crossref | GoogleScholarGoogle Scholar |
Matsubara S,
Hurry V,
Druart N,
Benedict C,
Janzik I,
Chavarría-Krauser A,
Walter A, Schurr U
(2006) Nocturnal changes in leaf growth of Populus deltoides are controlled by cytoplasmic growth. Planta 223, 1315–1328.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Miyazawa S-I, Terashima I
(2001) Slow development of leaf photosynthesis in an evergreen broad-leaved tree, Castanopsis sieboldii: relationships between leaf anatomical characteristics and photosynthetic rate. Plant, Cell & Environment 24, 279–291.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Miyazawa S-I,
Satomi S, Terashima I
(1998) Slow leaf development of evergreen broad-leaved tree species in Japanese warm temperate forests. Annals of Botany 82, 859–869.
| Crossref | GoogleScholarGoogle Scholar |
Miyazawa S-I,
Makino A, Terashima I
(2003) Changes in mesophyll anatomy and sink–source relationships during leaf development in Quercus glauca, an evergreen tree showing delayed leaf greening. Plant, Cell & Environment 26, 745–755.
| Crossref | GoogleScholarGoogle Scholar |
Pearcy RW
(1990) Sunflecks and photosynthesis in plant canopies. Annual Review of Plant Physiology and Plant Molecular Biology 41, 421–453.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Poethig RS, Sussex IM
(1985) The cellular parameters of leaf development in tobacco: a clonal analysis. Planta 165, 170–184.
| Crossref | GoogleScholarGoogle Scholar |
Porra RJ,
Thompson WA, Kriedemann PE
(1989) Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy. Biochimica et Biophysica Acta 975, 384–394.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Radyuk MS, Homan NM
(2002) Discrete character of the development of the photosynthetic apparatus in greening barley leaves. Photosynthesis Research 72, 117–122.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Schmundt D,
Stitt M,
Jähne B, Schurr U
(1998) 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 16, 505–514.
| Crossref | GoogleScholarGoogle Scholar |
Smith AM, Stitt M
(2007) Coordination of carbon supply and plant growth. Plant, Cell & Environment 30, 1126–1149.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Solymosi K,
Martinez K,
Kristóf Z,
Sundqvist C, Böddi B
(2005) The effect of prolonged etiolation inside the cabbage (Brassica oleracea L. cv. capitata) head and the greening of the different leaf layers. Acta Biologica Szegediensis 9, 227–228.
Walter A, Schurr U
(2005) Dynamics of leaf and root growth – endogenous control versus environmental impact. Annals of Botany 95, 891–900.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Walter A,
Feil R, Schurr U
(2002) Restriction of nyctinastic movements and application of tensile forces to leaves affects diurnal patterns of expansion growth. Functional Plant Biology 29, 1247–1258.
| Crossref | GoogleScholarGoogle Scholar |
Walter A,
Roggatz U, Schurr U
(2003) Expansion kinetics are an intrinsic property of leaf development and are scaled from cell to leaf level at different nutrient availabilities. Plant Biology 5, 642–650.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Watling JR,
Robinson SA,
Woodrow IE, Osmond CB
(1997) Responses of rainforest understorey plants to excess light during sunflecks. Australian Journal of Plant Physiology 24, 17–25.
| Crossref | GoogleScholarGoogle Scholar |
Whatley JM
(1992) Plastid development in distinctively coloured juvenile leaves. New Phytologist 120, 417–426.
| Crossref | GoogleScholarGoogle Scholar |
Wiese A,
Christ MM,
Virnich O,
Schurr U, Walter A
(2007) Spatio–temporal leaf growth patterns of Arabidopsis thaliana and evidence for sugar control of the diel leaf growth cycle. New Phytologist 174, 752–761.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Wobus U, Weber H
(1999) Sugars as signal molecules in plant seed development. Biological Chemistry 380, 937–944.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Woodall GS,
Dodd IC, Stewart GR
(1998) Contrasting leaf development within the genus Syzygium. Journal of Experimental Botany 49, 79–87.
| Crossref | GoogleScholarGoogle Scholar |
CAS |