Received: 12 June 1995 Accepted: 6 September 1995
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1 Annals of Botany 77: 63 70, 996 Sylleptic Shoot Formation in Young Apple Trees Exposed to Various Soil Temperature and Air Humidity Regimes in Three Successive s of the Growing Season J. TROMP Research Station for Fruit Growing, Brugstraat 5, 4475 AN Wilhelminadorp, The Netherlands Received: June 995 Accepted: 6 September 995 Under otherwise controlled conditions, the effect of two soil temperatures ( and C) and two air humidities (50 and 90%) applied during three successive periods of 6 weeks (starting at the beginning of the growing season) on sylleptic shoot production of young apple trees was evaluated during the first year of growth. The treatment effects were mainly reflected on sylleptic growth; the growth of the main shoot was much less influenced. In I sylleptic growth tended to be reduced at C. In II it responded greatly to the soil temperature in I resulting in a much stronger sylleptic growth at than at C. However, the actual soil temperature in II was not of any importance. In III growth activity was low and there were no treatment effects. High humidity favoured sylleptic growth in I at the soil temperature of C but not at C, but in II the reverse was found. Humidity did not affect syllepsis in III. The various treatments greatly affected the distribution of sylleptic shoots along the main shoot. The ability to grow out into sylleptic shoots was restricted to buds in a certain stage of development. The results are discussed in terms of a negative feed back mechanism between shoot and root growth which controls sylleptic growth. 996 Annals of Botany Company Key words: Malus pumila Mill., apple, syllepsis, branching, soil temperature, air humidity. INTRODUCTION In fruit trees, lateral buds of growing shoots usually do not leaf out. However, in early summer lateral buds may grow into sylleptic shoots when the supply of nutrients and water is abundant, a condition that is satisfied in nurseries for fruit trees in the first year after bud-grafting. The natural ability for syllepsis is generally small (Cody, Larsen and Fritts, 985; Popenoe and Barritt, 988; Volz, Gibbs and Popenoe, 994; Wertheim and Estabrooks, 994) and differs markedly between various cultivars of fruit trees (Wertheim, 978). In addition, since strong year-to-year variations in the degree of syllepsis occur, environmental factors may also play an important role. Recently, in studies done under completely controlled conditions, it was shown that lateral shoot formation of young apple trees was much better at high than at low air humidity and, broadly speaking, increased with soil temperature in the range of 7 8 C (Tromp, 99a, b). In addition, soil temperature clearly affected the distribution of sylleptic shoots along the main shoot. In the experiments of Tromp (99a, b) the various humidity and soil temperature conditions were applied during the whole growing season. In the present two experiments young apple trees were exposed to two different air humidities and soil temperatures during three successive periods of about 6 weeks. An attempt is made to answer the question whether these factors are especially important in a specific phase of the growing season. In addition, attention will be paid to what happens in each period with respect to $.00 0 extension of already present sylleptic shoots s. number and outgrowth of new shoots, and to the distribution of sylleptic shoots along the main axis. MATERIAL AND METHODS In Jan. 99 (expt ) and 993 (expt ) -year-old apple rootstocks M.9 (Malus pumila Mill.) bud-grafted with cvs Rode Boskoop and Elstar were planted into 3-l plastic pots containing enriched pot soil. Half-way through each experiment every tree received extra nutrients in the form of the slow-release fertilizer Osmocote. Budding height was about 0 cm; at planting the rootstocks were cut back to cm above the bud. At the beginning of February, the trees of each cultivar were divided into four (expt ) or eight (expt ) groups of 4 trees each and transferred to four (expt ) or two (expt ) identical controlled-environment rooms. In each room one (expt ) or two (expt ) temperaturecontrolled Wisconsin tanks were available, each tank could accommodate 8 trees (4 of each cultivar) in three rows of nine or ten trees. Tree spacing within and between rows was cm. The trees of the two cultivars were intermixed at random. During the next 4 weeks in each room, air and soil temperature were gradually increased from 0 to 0 C (air) and to about 5 C (soil). The rooms were illuminated by high-pressure sodium lamps (Philips SON-T, 400 W) giving an irradiance of Wm at about 70 cm above soil level. Day length was 4 h. The trees were watered as needed, and control was maintained by weighing the pots. 996 Annals of Botany Company Downloaded from by guest on 3 December 08
2 64 Tromp Sylleptic Shoot Formation in Young Apple Trees Experiment Starting at the beginning of Mar. 99 at the mouse-ear stage of bud development, the four groups of trees of each cultivar were exposed to low ( C) or high ( C) soil temperature for three successive periods of about 40 d each. The treatments were --, --, --, and - -. Day night temperature and relative humidity (RH) were C and about 90%, respectively. Experiment Again starting at the beginning of March (993) when the expanding buds started to open ( mouse-ear stage), at a soil temperature of C and of C four groups of trees of each cultivar were exposed to low (L, 50 55%) or high (H, about 90%) RH for three successive periods of about 40 d each, resulting in the following four treatments: LLL, HLL, LHL, and LLH, at each of the two soil temperatures. Day night air temperature was 0 C throughout the experiment. Measurements and statistical analysis Every weeks, the length of the main shoot and the length and position (number from graft union) of each individual sylleptic shoot were recorded. At the end of the third period when shoot growth had ceased, internodes were counted and mean internode length was calculated. The data were subjected to analysis of variance followed by the Student-Newman-Keuls multiple range test for pairwise comparisons between the treatment means. RESULTS Since, broadly speaking, Rode Boskoop and Elstar behaved similarly, not all data are provided for both cultivars. Experiment For both cultivars, the effect of treatments was mainly reflected in differences in sylleptic growth, and to a TABLE. Growth of the main shoot (cm per tree) in each of three successi e periods of about 40 d (starting at bud opening) of c s Rode Boskoop and Elstar at four soiltemperature regimes. Experiment Rode Boskoop Elstar Soil temp. ( C) I II III I II III b 8 9a 4b 65 b 34 b 6 5a b 6 6a 3 9a 6 6b 4 3a 0 4a a 46 0b 6 6b 53 4a 46 5b 6 6a a 43 6b 6 6b 54 9a 47 5b 4 8a Within columns, values followed by a different superscript letter differ significantly (P 0 05). TABLE. Sylleptic growth (cm per tree) and number of newly formed sylleptic shoots in each of three successi e periods of about 40 d of c s Rode Boskoop and Elstar at four soiltemperature regimes. Further growth (cm per tree) of the shoots already formed in I is indicated in parentheses. Experiment Growth Number of sylleptic shoots Soil temp. ( C) I II III I II III Rode Boskoop a 4a ( 4) 0 0a 6 4a 0 0a a 0 0a (0 0) 0 a 6 6a 0 0a a 04 b (48 3) a 3 8a 9b a 5 9b (6 0) 0 9a 5 0a 4b 0 0 Elstar a 49 a (43 6) 6 4a 5 4a 0 4a 6a a a ( ) 5 8a 5 6a 0 0a 0 6a a 78 b (99 ) 0 a 3 5a 5 3b 0 0a a 8 7b (88 8) 8 4a 4 7a 5 9b 0 3a For each cultivar, within columns, values followed by a different superscript letter differ significantly (P 0 05). lesser degree in differences in growth of the parent shoot (Tables and ). In both cultivars, the high soil temperature given in I enhanced growth of the main shoot in that period, but it reduced growth in II (Table ). Growth in II did not respond to differences in temperature in that period. Apart from the low value at regime -- for Rode Boskoop, growth in III was the same at the various regimes. The various treatments did not affect mean internode length (data not given). With respect to sylleptic shoot formation, the pattern found for growth, expressed in cm, was similar to that for shoot number. Although the data strongly suggest that in I sylleptic growth was reduced at the soil temperature of C, the differences were not significant (Table ). There was a very pronounced carry-over effect of the temperature given in I on growth in II, resulting in a much stronger growth at than at C. The actual temperature in II was not of any importance. In III growth activity was low; the data suggest a slight growth stimulation for Elstar at C. For II I calculated the share of sylleptic growth that accounted for further growth of the sylleptic shoots already formed in I (Table, values in brackets). In treatments -- and --, the growth in II was almost completely the growth of old shoots. New shoot formation hardly occurred, as the data for shoot number show. In contrast, when root temperature was low in I (-- and --) a great part of growth in II was the outgrowth of new shoots. Without exception, the sylleptic shoots appeared acropetally and all shoots originated from buds. To study the distribution of the sylleptic growth along the axis, for each successive section of five nodes (starting at the graft union) Downloaded from by guest on 3 December 08
3 Tromp Sylleptic Shoot Formation in Young Apple Trees Number of shoots >40 FIG.. Final number of sylleptic shoots per five-node segment per tree counted from the graft union of Elstar at four soil temperature regimes. Experiment., --;, --; 3, --; 4, --;, I;, II;, III. Shoot growth (cm) >40 FIG.. Final sylleptic shoot growth per five-node segment per tree counted from the graft union of Elstar at four soil temperature regimes. Experiment. For explanation of symbols, see Fig.. Downloaded from by guest on 3 December 08 the newly emerged shoots in each period were counted and, in addition, total growth ( new shoots shoots already formed in a previous period) was calculated. There was no essential difference in behaviour between Rode Boskoop and Elstar. Therefore, the data for Elstar only are given (Figs and ). Sylleptic growth in I is restricted to the lower part of the main shoot (buds 6 5). The higher soil temperature in that period (-- and --) led to more shoots and a greater total shoot length in segment 5. When soil temperature was high in I no further shoots emerged in II (Fig. ); sylleptic growth was restricted to the extension of shoots already present (Fig. ). In contrast, the low soil temperature in I was reflected in a considerable increase of sylleptic growth (number of shoots as well as total shoot length) in segments 6 0, 5 and 6 30 in II. Increased growth in the lower segments mainly concerned old shoots. It should be noted that the actual soil temperature
4 66 Tromp Sylleptic Shoot Formation in Young Apple Trees TABLE 3. Growth of the main shoot (cm per tree) in each of three successi e periods of about 40 d (starting at bud opening) of c s Rode Boskoop and Elstar at four relati e humidity (RH) regimes (L 50%, H 90%) and two soil temperatures. Experiment TABLE 4. Sylleptic growth (cm per tree) and number of newly formed sylleptic shoots in each of three successi e periods of 40 d (starting at bud opening) of c. Rode Boskoop at four relati e humidity (RH) regimes (L 50%, H 90%) and two soil temperatures. Experiment Rode Boskoop Elstar RH Soil temp. regime ( C) I II III I II III LLL 49 a 33 5c 5 9b 34 4a 36 4b 43 4bc HLL 5 4a 30 4bc 9bc 38 9ab 34 0b 43 8bc LHL 48 8a 40 0d 8bc 38 3ab 4 4c a LLH 49 4a 33 9c 3 bc 39 4ab 37 5b 3 9ac LLL 50 9a 8 ab 4 ac 37 5ab 35 8b 8 ac HLL 55 6a 4 6a 6a 43 b 9 6a 4 9a LHL 5 3a 35 4c 6 3ac 39 ab 38 6b 3a LLH 5 4a 7 4ab 5 6ac 4 6b 33 9b 8 9ac Within columns, values followed by different superscript letters differ significantly (P 0 05). in II was not of any importance (cf. -- with - -, and -- with --). Sylleptic growth in III was slight; it was mainly restricted to a few new shoots higher up the main shoot in the treatments wherein soil temperature was high in I. The actual soil temperature in III was irrelevant. Experiment Again, the effect of the various treatments mainly concerned the sylleptic shoot growth and to a lesser degree the growth of the main shoot (Tables 4 and 5). Humidity did not affect growth of the main shoot in I (Table 4). High humidity in II favoured growth in both cultivars in that period (except for Elstar at C) but reduced it in III in Elstar, especially at the low soil temperature. Comparison of regimes LLH and LLL shows that humidity was not effective in III. Mean internode length again was not influenced by treatments (data not given). In general, the sylleptic growth and the number of shoots affected by the various treatments closely followed the same pattern for Rode Boskoop and Elstar (Tables 4 and 5). Sylleptic growth was stimulated at high RH in I at the soil temperature of C but not at C. In contrast, in II sylleptic growth was enhanced considerably at high humidity at C but did not respond to differences in humidity at C. There was again no effect of humidity on sylleptic growth in III. Apart from treatment HLL- for Rode Boskoop where in II growth and shoot number tended to be reduced, no carry-over effect occurred. In s I and II, in both cultivars, growth of the main shoot was the same at the two soil temperatures, but seemed to be reduced somewhat at C in III (Table 3). Similarly, apart from regime HLL, soil temperature did not influence sylleptic growth and the number of shoots in Growth Number of sylleptic shoots RH Soil temp. regime ( C) I II III I II III LLL 8 a 73 b 38 b 6ab 7b 0 4a HLL 9 7a 43 0ab 33 0ab 3ab a 0 3a LHL 5 a 5 c 38 4b 0 9ab 5 5c 0 a LLH 4 6a 65 b 48 6b 0 5a 8b 0a LLL 6 6a 5 9a 0 3a ab 0 8a 0 3a HLL 3 3b 9 9a 6 a 8b 0 a 0 a LHL 8 9a 3 0a 0 a ab 0 9a 0 4a LLH 9 6a 4 a 6 6a 3ab 0 a 0 a Within columns, value followed by different superscript letters differ significantly (P 0 05). TABLE 5. Sylleptic growth (cm per tree) and number of newly formed sylleptic shoots in each of three successi e periods of 40 d (starting at bud opening) of c. Elstar at four relati e humidity (RH) regimes (L 50%, H 90%) and two soil temperatures. Experiment Growth Number of sylleptic shoots RH Soil temp. regime ( C) I II III I II III LLL 4 a 7 a 4 9b 0 6a 0 6a a HLL 8 9a 39 6a 3 ab 4a 0a a LHL 7 9a 04 b 76 c 4a 5 6b a LLH 7 a 37 a 8 3ab 0 9a 0a 0 4a LLL 7 8a 3 8a 0 a 0 9a 0 a 0 a HLL b 33 9a 6 9a 4a 0 4a 0 0a LHL 5 8a 6 8a 6 0a 0 6a 0 4a 0 0a LLH 6 5a 9 4a 5 6a 0 9a 0 0a 0 a Within columns, values followed by different superscript letters differ significantly (P 0 05). I (Tables 4 and 5). In general, in s II and III there was also hardly any effect of temperature for Elstar, but for Rode Boskoop lower values were found at the high soil temperature. Again, all sylleptic shoots originated from buds, and they emerged acropetally. Similarly, as for expt, the distribution of sylleptic growth over the main axis for the different periods was calculated. Data for Elstar at the soil temperature of C only are given (Figs 3 and 4). As might be expected (the main shoot was still short), sylleptic growth in I was restricted to the lower few sections. The high humidity was not effective; the differences in number of Downloaded from by guest on 3 December 08
5 Tromp Sylleptic Shoot Formation in Young Apple Trees 67 3 Number of shoots FIG. 3. Final number of sylleptic shoots per five-node segment per tree counted from the graft union of Elstar at four air humidity regimes (L 50%, H 90%) at a soil temperature of C. Experiment., LLL;, HLL; 3, LHL; 4, LLH;, I;, II;, III. shoots were by chance. In II, very few shoots emerged in section 6 0, but in bud range 30 a rapid outgrowth of new shoots occurred, especially when humidity was high (LHL, Fig. 3). The stimulating effect of high humidity in II also becomes clear when total shoot length is considered (Fig. 4). The increase of sylleptic growth in segment 6 0 was from shoots that already grew out in the previous period, but the increase higher up concerned newly emerged as well as old shoots. Apart from a few shoots in sections 6 30 and 3 35, in III hardly any new shoots were added. The increase in shoot growth was mainly from already existing shoots, and was most marked when humidity was high in the previous period. DISCUSSION In the present experiments, a stimulation of sylleptic growth in some period was nearly always associated with a stimulation of growth of the main shoot. This observation is not new, Champagnat (96) has already stated that sylleptic branching usually occurs in periods when the growth vigour of the parent shoot is highest. This positive relationship between syllepsis and growth vigour of the parent shoot has been further reported for a number of woody perennials, e.g. Myrsine floridana (Wheat, 980), Tsuga canadensis (Powell, 99) and peach (Page s, Ge nard and Kervella, 993). Very recently, in a detailed study on sylleptic branching in peach, Ge nard, Page s and Kervella (994) found that branching probability on the one hand, and node emergence rate and internode length of the parent shoot on the other, were closely positively correlated. The aforegoing observations are difficult to reconcile with the hormonal version of the apical dominance concept, which just assumes an inhibiting effect of the apical growing point of the main shoot on lateral growth (Cline, 99). It seems more plausible that some common factor controls sylleptic growth and growth of the parent shoot independently of each other. Actually, the present results rather support the nutritive theory of apical dominance, which attributes a decisive role to the internal competition for water, mineral elements, and carbohydrates between the lateral buds and the parent shoot (Cline, 99). In this view, when both nutrient and water supply are satisfied, growth of the main shoot and sylleptic growth will not affect each other. With respect to the influence of soil temperature the situation is complicated. When applied in the first 6 weeks after leafing out, the high soil temperature favoured growth in expt and, provided RH was high, also in expt. This positive effect of higher soil temperatures is well-known (Cooper, 973; Bowen, 99) and was also found for apple (Carlson, 965; Tromp, 978, 984). However, in expt, sylleptic growth in II was not affected by the actual soil temperature, but it greatly depended on the preceding temperature. In III, sylleptic growth had slowed down and did not respond to treatments. As a result, surprisingly, as can easily be seen in Tables 4 and 5, total sylleptic growth at C markedly exceeded that at C. In a similar experiment using the same apple cultivars, Tromp (99b) found, broadly speaking, that sylleptic growth increased with soil temperature in the range of 7 8 C, but in Elstar growth vigour at C was clearly lower than at 4 C. To explain the present effects of soil temperature on branching, we support the hypothesis suggested by Goodwin, Gollnow and Letham (978) that root factors are involved in lateral bud growth. There is ample reason to attribute an important role to cytokinins produced in the growing root tips in that respect. Application of cytokinins to lateral buds favours their outgrowth (Cline, 99; King and Van Staden, 988). Distinct qualitative differences in cytokinins were found by Skene and Kerridge (967) between xylem sap from grapevines grown at 0 and 30 C. Downloaded from by guest on 3 December 08
6 68 Tromp Sylleptic Shoot Formation in Young Apple Trees 3 Number of shoots FIG. 4. Final sylleptic shoot growth per five-node segment per tree counted from the graft union of Elstar at four air humidity regimes (L 50%, H 90%) at a soil temperature of C. Experiment. For explanation of symbols see Fig. 3. Tromp and Ovaa (994) found hardly any influence of soil temperature (6 and 0 C) on cytokinin concentration in xylem sap of apple, but they concluded that, due to the strongly reduced total leaf area (less transpiration) at 6 C, the cytokinin flux must have been much higher at 0 than at 6 C. Since in the present experiments at planting only a few roots were present, a rapid new root growth must have occurred in I, especially at the higher root temperature. As a consequence, sylleptic shoots grew out in that period. At C, the time taken to reach a certain root development and to produce sufficient cytokinins to favour shoot outgrowth will be extended, leading to a delay in sylleptic growth until somewhere in II. It is surprising that the effect of soil temperature is restricted to a relatively short period and is not extended over a longer period even when exposure of the stimulating factor is continued as in the -- treatment. The most plausible explanation is that shoot and root growth control each other via some negative feed back mechanism, implying that the shoot growth induced by the developing root system inhibits further root growth. In its turn, the reduced root growth prevents the outgrowth of new sylleptic shoots. In this reasoning, after some rest period a second flush of sylleptic growth might have occurred. This did not happen in the present experiment, but in a similar experiment done at a higher air temperature Tromp (993) found two flushes of sylleptic growth. The periodicity in root growth as assumed here is supported by observations of Head (966, 967) and Atkinson and Wilson (980), that root growth was reduced when shoot growth was most vigorous. They found two peaks in root growth, one in late spring and a second in mid-summer. The factor responsible for the reduction of root growth by growing shoots may be auxin. Very recently, Bangerth (994) showed for bean plants that the cytokinin concentration in xylem sap was controlled by a basipetally directed auxin flow. It is not clear why the actual temperature in II was not relevant for shoot growth. It may be suggested that, in line with the foregoing discussion, the inhibition issued by the growing shoots outstripped the effect of soil temperature. Alternatively, the positive effect of the higher temperature on root development may be counterbalanced by the increased demand for assimilates by root respiration. Moving now to the effect of humidity, the enhanced shoot growth at high humidity, as shown in the present study, is consistent with data for a large number of plant species (Hoffman, 979) including apple (Tromp and Oele, 97; Tromp and Van Vuure, 993) but, as found in expt, an interaction with soil temperature may occur. Apart from one earlier study on apple by Tromp (99a), there seems to be no further data on the effect of air humidity on syllepsis for woody perennials, but the present data are in line with observations for some herbaceous plants (McIntyre, 977; Hunter, Hsiao and McIntyre, 985; McIntyre and Hsiao, 990). McIntyre (987) suggested that at high humidity water potential and turgor are increased, which would trigger the lateral buds from inhibition. The observation that in the HLL treatment in I, growth being stimulated only at the soil temperature of C, fits in with the view given in the foregoing that at C early in the season root growth activity limits shoot growth. It may be assumed that in II at C, root development no longer inhibits shoot growth, which explains the growth stimulation at high humidity (LHL). This stimulation failed to occur at high soil temperature which may be due to the supposed enhancement of respiration as discussed before. This argument may also explain the weaker shoot growth at C in III. However, it remains obscure why high humidity in III (treatment LLH) did not favour sylleptic growth. Ge nard et al. (994) found that the readiness to form sylleptic shoots decreased later in the season, which they Downloaded from by guest on 3 December 08
7 Tromp Sylleptic Shoot Formation in Young Apple Trees 69 attributed to the gradually decreasing photoperiod. In our experiments, the number of sylleptic shoots formed in III usually remained behind that in the previous periods, but since the photoperiod was the same throughout, some endogenous factor may be involved, originating in e.g. ageing leaves. In addition, it should be realized that the ability to form sylleptic shoots later in the season may be reduced because part of the carbohydrates and nutrients needed were used up in the further growth of already existing shoots. For example, as Table shows for Elstar, sylleptic growth in treatments -- and -- in II exceeded that of -- and -- in I, but a marked proportion concerned shoots already formed in I; the number of new shoots was the same as in I. In the similar situation for Rode Boskoop, the number of shoots grown out in II was much lower than in I, whereas growth in cm did not differ much. In view of the ample supply of fertilizer, it is not very likely that the decrease in sylleptic shoot formation is due to mineral deficiency. How far mutual shading of the trees (increasing with time) was of any importance in this respect is a matter of conjecture. The distribution of sylleptic shoots along the main axis greatly depended on the period in which their outgrowth occurred. Stimulation of sylleptic growth in I in expt (-- and --, Fig. ) and in expt (HLL, Fig. 3) was restricted to the lower sections because, at that time, the greater part of the main axis had not yet formed. However, the increase in sylleptic shoots in II mainly occurred above node 5 (expt ) or 0 (expt ); in expt hardly any new shoots were formed in the 6 5 range. Similarly, the few shoots that grew out in III were mainly found in the higher sections. On the other hand, buds near the main growing tip, i.e. very young buds never grew out into sylleptic shoots. Apparently, each bud passes a critical period in which it is able to respond to outgrowthinducing factors. It may be reasoned that whether outgrowth actually occurs is controlled by the balance between, on the one hand, the degree of rest increasing with bud age, and on the other hand the strength of the inducing factor. As a consequence, the position of sylleptic growth along the main axis was determined by the time that the inducing factor became manifest, as is clearly shown in the present experiments. Very young buds may be inhibited by the growing shoot tip; they reach the critical phase after a certain distance from the tip is exceeded. It should be stressed that the effect of the various treatments mainly concerned the distribution of the sylleptic shoots and much less the distribution of the amount of growth. For example, unlike the situation for shoot number, growth in II included for the greater part the further extension of shoots in the bud range 6 5 that emerged in I. In summary, sylleptic growth was assumed to be mainly controlled by a negative feedback mechanism between shoot and root growth. High humidity favoured sylleptic growth under conditions of sufficient root growth but, since our soil-temperature experiment was only done at high air humidity, it remains to be seen how far the effect of soil temperature on syllepsis is dependent on air humidity. It is questionable whether the phenomenon of apical dominance is an important factor in sylleptic shoot formation in the present experiments. ACKNOWLEDGEMENTS I thank Mr C.A.R.Ro mer for extensive technical assistance and Dr S.J.Wertheim for critical reading of the text. LITERATURE CITED Atkinson D, Wilson SA The growth and distribution of fruit tree roots: some consequences for nutrient uptake. In: Atkinson D, Jackson JE, Sharples RO, Waller WM. Mineral nutrition of fruit trees. London: Butterworth, Bangerth F Response of cytokinin concentration in the xylem exudate of bean (Phaseolus ulgaris L.) plants to decapitation and auxin treatment, and relationship to apical dominance. Planta 94: Bowen GD. 99. Soil temperature, root growth, and plant function. In: Waisel Y, Eshel A, Kafkafi U, eds. Plant roots, the hidden half. New York: Marcel Dekker Inc., Carlson RF Responses of Malling Merton clones and Delicious seedlings to different root temperatures. Proceedings of the American Society for Horticultural Science 86: Champagnat P. 96. Dominance apicale. Tropismes, e pinastie. Encyclopedia of Plant Physiology 6: Cline GC. 99. Apical dominance. Botanical Re iew 57: Cody CA, Larsen FE, Fritts R Jr Induction of lateral branches in tree fruit nursery stock with propyl 3-t-butylphenoxy acetate (M&B 5, 05) and Promalin (GA ) 6-benzyladenine. Scientia Horticulturae 6: 8. + Cooper AJ Root temperature and plant growth. Commonwealth Bureau of Horticulture and Plantation Crops, Research Review No. 4. Ge nard M, Page s L, Kervella J Relationship between sylleptic branching and components of parent shoot development in the peach tree. Annals of Botany 74: Goodwin PB, Gollnow BI, Letham DS Phytohormones and growth correlations. In: Letham DS, Goodwin PB, Higgins TJV, eds. Phytohormones and related compounds: a comprehensi e treatise. II. Amsterdam: Elsevier-North Holland Biomedical Press, Head GC Estimating seasonal changes in the quantity of white unsuberized roots on fruits trees. Journal of Horticultural Science 4: Head GC Effects of seasonal changes in shoot growth on the amount of unsuberized root on apple and pear trees. Journal of Horticultural Science 4: Hoffman GJ Humidity. In: Tibbitts TW, Kozlowsky TT, eds. Controlled en ironments guidelines for plant research. New York: Academic Press, 4 7. Hunter JH, Hsiao AI, McIntyre GI Some effects of humidity on the growth and development of Circium ar ense. Botanical Gazette 46: King RA, Van Staden J Differential responses of buds along the shoot of Pisum sati um to isopentenyladenine and zeatin application. Plant Physiology and Biochemistry 6: McIntyre GI Environmental control of lateral bud growth in the sunflower (Helianthus annuus). Canadian Journal of Botany 55: McIntyre GI The role of water in the regulation of plant development. Canadian Journal of Botany 65: McIntyre GI, Hsiao AI The role of expanded leaves in the correlative inhibition of axillary buds in milkweed (Asclepias syriaca). Canadian Journal of Botany 68: Page s L, Ge nard M, Kervella, J Analyse quantitative du de veloppement ve ge tatif du syste me ae rien de jeunes pe chers (Prunus persica L. Batsch). Agronomie 3: Popenoe J, Barritt BH Branch induction by growth regulators and leaf removal in Delicious apple nursery stock. 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8 70 Tromp Sylleptic Shoot Formation in Young Apple Trees Powell GR. 99. Preformed and neoformed extension of shoots and sylleptic branching in relation to shoot length in Tsuga canadensis. Trees 5: Skene KGM, Kerridge GH Effect of root temperature on cytokinin activity in root exudate of Vitis inifera. Plant Physiology 4: Tromp J The effect of root temperature on the absorption and distribution of K, Ca and Mg in three rootstock clones of apple budded with Cox s Orange Pippin. Gartenbauwissenschaft 43: Tromp J Flower-bud formation in apple as affected by air and root temperature, air humidity, light intensity and day length. Acta Horticulturae 49: Tromp J. 99a. Lateral shoot formation in apple in the first year after budding as affected by air humidity and soil temperature. Acta Horticulturae 3: 4 5. Tromp J. 99b. The effect of soil temperature on lateral shoot formation and flower-bud formation in apple in the first year after budding. Journal of Horticultural Science 67: Tromp J Lateral shoot formation and flower-bud formation in apple in the first year after budding as affected by air temperature and exposure to red light. Journal of Horticultural Science 68: Tromp J, Oele J. 97. Shoot growth and mineral composition of leaves and fruits of apple as affected by relative air humidity. Physiologia Plantarum 7: Tromp J, Ovaa JC Spring cytokinin of xylem sap of apple at two root temperatures. Sciencia Horticulturae 57: 6. Tromp J, Van Vuure J Accumulation of calcium, potassium and magnesium in apple fruits under various conditions of humidity. Physiologia Plantarum 89: Volz RK, Gibbs HM, Popenoe J Branch induction on apple nursery trees: effects of growth regulators and defoliation. New Zealand Journal of Crop and Horticultural Science : Wertheim SJ Manual and chemical induction of side-shoot formation in apple trees in the nursery. Scientia Horticulturae 9: Wertheim SJ, Estabrooks EN Effect of repeated sprays of 6- benzyladenine on the formation of sylleptic shoots in apple in the fruit-tree nursery. Scientia Horticulturae 60: Wheat D Sylleptic branching in Myrsine floridana (Myrticaceae). American Journal of Botany 67: Downloaded from by guest on 3 December 08
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