TRANSLOCATION INTO MATURE LEAVES-THE EFFECT OF GROWTH PATTERN
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1 New Phytol (1977) 78, TRANSLOCATION INTO MATURE LEAVES-THE EFFECT OF GROWTH PATTERN BY STELLA L. THROWER Department of Biology, The Chinese University of Hong Kong, Hong Kong {Received 3 September 1976) SUMMARY In rosette plants, import of labelled assimilate by mature leaves is a normal part of the translocation pattern. Following elongation and loss of the rosette habit with the onset of flowering, the translocation pattern becomes that typical of elongate plants, characterised by lack of movement into mature leaves. INTRODUCTION A very precise pattern of movement of labelled assimilate from a source leaf upward into other fully expanded leaves has been described by Jones, Martin and Porter (1959) and by Joy (1964). Many other workers have stressed the lack of movement of assimilate into any but actively growing young organs or developing reproductive parts. No-one who has used the autoradiographic technique over a period of time for visualizing translocation of label within plants can have failed to notice the occasional, slight and seemingly random movement of labelled photosynthate into mature leaves. In certain species, movement of label from a source leaf down the stem into normally 'non-importing' healthy leaves can be induced by aphid infestation (Wu and Thrower, 1973), by sink limitation (Thrower, 1974), by the combined effect of darkening and benzyladenine treatment, (Quinlan and Weaver, 1969) or by herbicide treatment (Leonard, Bayer and Glenn, 1966). During an investigation into the physiology of yield of the local vegetable, Choi Sum {Brassica parachinensis Bailey), it was observed that the changing growth pattern was accompanied by a changing translocation pattern. When young, the main axis is very short and the plant is functionally a rosette. Following flower initiation, the main axis elongates and, at anthesis, the plant has an erect main stem (30-50 cm) with leaves along its length and a terminal inflorescence. At the rosette stage, movement into the mature leaves consistently occurred. In the elongate stage, the more usual pattern involving lack of such movement was the constant picture. These observations prompted the following investigation into the translocation pattern both in B. parachinensis and in other plants of similar habit. MATERIALS AND METHODS Experimental plants. Brassica parachinensis, lettuce (Lactuca sativa L. 'Burpee Bibb'), Swiss chard (Beta vulgaris L. var. cicla (L) Miq.), Tsit Gwa (Benincasa hispida (Thunb.) Cogn. var. chieh-qua How) and radish (Raphanus sativus L. 'Half-long Rose') were grown under glasshouse conditions with natural light. Seeds were sown in 5-in. plastic pots in coarse 361
2 362 STELLA L. THROWER sand and thinned after germination to one plant per pot except where otherwise stated. Plants were watered daily with nutrient solution (Hewitt, 1952). Beta vulgaris, Benincasa hispida and Raphanus sativus were used in the rosette stage only;brassicaparachinensis and Lactuca sativa were used in both the rosette and flowering stages. ^'^C feeding. The leaf to be treated was sealed with petroleum jelly into a Perspex box, into the base of which a glass tube with a side-arm containing a removeable syringe was fitted. *'*C-sodium bicarbonate solution in the base of the glass tube reacted with excess lactic acid delivered from the syringe to generate approximately 20 /ici of ^"^COj. Experiments were conducted in the open air on sunny days. Assessment of movement. At the end of the 2-h feeding period, the source leaf was cut off and the remainder of the plant dissected into separate leaves, stem and roots. Plant parts were placed in presses, oven-dried at 40 C and placed on X-ray film for 5 days. RESULTS In all species at the rosette stage, the autoradiographs showed heavy labelling in the apex above the source leaf and below the source leaf in the root, and moderate to light labelling in all mature leaves, both above and below the source leaf (See Plate 1 iox Lactuca sativa and Brassica parachinensis.) The possibility of *'*C02 leakage was investigated by feeding one plant of 5. parachinensis in a pot of three. Leaves of unfed plants were as near or nearer to the feeding box as were leaves of the experimental plant. Expanded, unfed leaves of the experimental plant contained considerable label whereas no label could be demonstrated in leaves of the control plants. Autoradiographs of B. parachinensis and Lactuca sativa in the flowering stage showed heavy labelling of the source leaf, but only moderate labelling of stem, root and, in Brassica parachichensis, the apex. Mature leaves either above or below the source did not import detectable amounts of label (Plate 2). The distribution of activity is that usually reported for plants with an elongated stem. DISCUSSION Movement of assimilate into mature leaves under normal conditions has been the subject of little direct investigation. It does, however, arise continually as a peripheral effect in studies directed towards elucidation of other aspects of translocation. Examples from the literature show that such movement has been reported from a wide spectrum of plant forms and species. These range from fruit trees (Quinlan, 1965; Kriedemann, 1968, 1969) to annual crop plants such as tomato (Khan and Sagar, 1966, 1967, 1969a, b) and legumes (Lucas, Milbourn and Whitford, 1976; and many others); from climbing plants such as grape vine (Quinlan and Weaver, 1969) to rosette plants such as sugar beet (Joy, 1964); and include ferns (Whittle, 1964), gymnosperms (Gordon and Larson, 1968) monocotyledons (Palmer, Heichel and Musgrave, 1973; and many others) and many species of dicotyledons. Before it can be assumed that the activity found in mature leaves is evidence of translocation into them, it is necessary to consider the possible processes whereby mature
3 Translocation into mature leaves 363 leaves may acquire label. The immediate origin of such label may be either within the plant or external to it. External sources include labelled carbon dioxide lost from the fed leaf by respiration or by lateral transfer through mesophyll spaces and loss through the stomata during spotfeeding, with subsequent re-assimilation by the leaves of the experimental plant. Within the plant, there may be lateral movement of assimilate already travelling in the phloem either into cauline bundles via vascular anastomoses or into the xylem system with subsequent distribution via the transpiration stream. Furthermore, labelled carbon which reaches the root may be used in amino acid synthesis and again re-distributed via the transpiration system. In the experiments reported here, the source leaf was contained in a closed system throughout the experimental period and no uptake of label by adjacent control plants occurred. It can thus be assumed that the activity demonstrated in expanded leaves did not originate from an external source. Before any further conclusions can be drawn, experimental work is required to discover the form of the label in expanded leaves, whether sugar or amino acid; and whether it enters them via the phloem or in the transpiration stream. These aspects, along with an investigation of the vascular anatomy, are the subjects of current work. REFERENCES GORDON, J.C. & LARSON, P.R. (1968). Seasonal course of photo-synthesis, respiration and distribution of '''C in youngpmws resinosa trees as related to wood formation. PI. Physiol., Lancaster, 43, HEWITT, E.J. (1952). Sand and Water Culture Methods Used in the Study of Plant Nutrition. Commonwealth Agricultural Bureaux, England. JONES, H., MARTIN, R.V. & PORTER, H.K. (1959). Translocation of '"carbon in tobacco following assimilation of '"carbon dioxide by a single leaf. Ann. Bot., 23, 493. JOY, K.W. (1964). Translocation in sugar-beet. I. Assimilation of '"CO, and distribution of materials from leaves. 7. exp. Bot., 15,485. KHAN, A.A. & SAC.AR, G.R. (1966). Distribution of C'"-labelled products of photosynthesis during the commercial life of the tomato cro'p. Ann. Bot., 30, 727. KHAN, A.A. & SAGAR, G.R. (1967). Translocation in tomato: The distribution of the products of photosynthesis of the leaves of a tomato plant during the phase of fruit production. Hort. Res., 7,61. " KHAN, A.A. & SAGAR, G.R. (1969a). Alteration of the pattern of distribution of photosynthetic products in the tomato by manipulation of the plant. Ann. Bot., 33, 753. KHAN, A.A. & SAGAR, G.R. (1969b). Changing patterns of distribution of the products of photosynthesis in the tomato plant with respect to time and to the age of the leaf. Ann. Bot., 33, 763. KRIEDEMANN, P.E. (1968). '"C translocation patterns in peach and apricot shoots. Aust. J. agric. Res., 19,775. KRIEDEMANN, P.E. (1969). '"C translocation in orange plants. y4wsf. /. agric. Res., 20, 291. LEONARD, O.A., BAYER, D.E. & GLENN, R.K. (1966). Translocation of herbicides and assimilates in red maple and white ash. Bot. Gaz., 127, 193. LUCAS, E.O., MILBOURN, G.M. & WHITl ORD, P.N. (1976). The translocation of '"C photosynthate from leaves and pods in Phaseolus vulgaris. Ann. appl. Biol, 83, 285. PALMER, A.F.E., HEICHEL, G.H. & MUSGRAVE, R.B. (1973). Patterns of translocation, respiratory loss, and redistribution of '"C in maize labelled after tlowering. Crop Science, 13, 371. QUINLAN, J.D. (1965). The pattern of distribution of '"carbon in a potted apple rootstock following assimilation of '"carbon dioxide by a single leaf. Rep. E. Mailing Res. Sta., 117. OUINLAN, J.D. & WEAVER, R.J. (1969). Influence of benzyladenine, leaf darkening, and ringing on movement of '"C-labelled assimilates into expanded leaves of Vitis vinifera L. PL Physiol., Lancaster, 44, THROWER, S.L. (1974). Sink limitation and import of assimilate into mature leaves. New Phytoi., 73, 685. WHITTLE, CM. (1964). Translocation in Pteridium. Ann. Bot., 28, 331. WU, A. & THROWER, L.B. (1973). Translocation into mature leaves. PL Cell PhysioL, 14, 1225.
4 364 STELLA L. THROWER EXPLANATION OF PLATES PLATE 1 Movement of assimilate in rosette plants. LHS: plant parts. RHS: autoradiographs illustrating movement of label into mature leaves. Nos. 1 and 2. Brassica parachinensis. Nos. 3 and 4. Lactuca sativa. Control plants not receiving direct '"CO^ feeding indicated by 'Con.' S indicates source leaf; S + 1, S + 2 er seq. indicate successive leaves developed above the source leaf; S 1, S 2 er seq. leaves below. PLATE 2 Movement of assimilate in elongate plants. LHS: plant parts. RHS: autoradiographs illustrating lack of movement of label into mature leaves. Nos. 5 and 6. Brassica parachinensis. Nos. 7 and 8-leaves and Nos. 9 and 10- stems and roots of one plant of Lactuca sativa. Stems have been split longitudinally so appear duplicated. Legend as for Plate 1.
5 THE NEW PHYTOLOGIST, 78, 2 PLATE I STELLA I>. THROWER Ti?^Ar5LOCy4T/OA/' /ivto MATURE LEAVES (facing p. 364)
6 THE NEW PHYTOLOGIST, 78, 2 PLATE 2 9 *. 10 FELLA L. THROWER Ti^^A^^LOC^T/OiV INTO MATURE LEAVES
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