Scientia Horticulturae 82 (1999) 217±226
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1 Scientia Horticulturae 82 (1999) 217±226 Photoperiod and temperature effect on growth of strawberry plant (Fragaria ananassa Duch.): development of a morphological test to assess the dormancy induction Fabien Robert a,*, Georgette Risser b, Gilles PeÂtel a a Physiologie InteÂgreÂe de l'arbre Fruitier (Unite associeâe INRA Bioclimatologie-Universite Blaise Pascal) 24, avenue des Landais, F AubieÁre Cedex, France b INRA, Station d'ameâlioration des Plantes MaraõÃcheÁres, BP 94, Montfavet Cedex, France Accepted 24 March 1999 Abstract At the end of summer, the diminution of photoperiod and temperature cause a decrease of vegetative growth and the dormancy of strawberry plants. Although the decrease in vegetative growth can be measured morphologically, no test is able to evaluate the decrease in growth potential (i.e. during the dormancy induction) nor its possible influence on vegetative growth. On the one hand, to estimate this influence biometrically, we have correlated photoperiod and temperature decreases with the vegetative growth decrease of some strawberry cultivars observed in the field. Results have confirmed the major role of photoperiod, temperature and the effect of growth potential decrease on vegetative growth. Moreover, the results showed that the decrease of vegetative growth was an early event at the end of summer which depended upon strawberry cultivar. On the other hand, we have measured petiole length under standard climatic conditions in a growth chamber, after natural summer and autumnal exposures. Observations of strawberry plants under these conditions revealed a decrease of their growth potential which also depended upon strawberry cultivar. Results also confirmed the possible action of growth potential decrease on the vegetative growth at the end of summer. Consequently, the observation of strawberry plants under standard conditions can be used, as a test, to assess the exact moment of dormancy induction. # 1999 Elsevier Science B.V. All rights reserved. Keywords: Dormancy; Fragaria; Growth; Morphological test; Petiole length; Strawberry * Corresponding author. Tel.: ; fax: address: frobert@cicsun.univ-bpclermont.fr (Fabien Robert) /99/$ ± see front matter # 1999 Elsevier Science B.V. All rights reserved. PII: S (99)
2 218 F. Robert et al. / Scientia Horticulturae 82 (1999) 217± Introduction Effects of environmental factors on the vegetative growth of strawberry plants are well documented. At the end of summer, the decrease of vegetative growth is caused mainly by changes in photoperiod (day length) and temperature changes (Darrow and Waldo, 1934; Arney, 1956; Piringer and Scott, 1964; Heide, 1977; Durner et al., 1984). The measurement of petiole length appears to be the best parameter to evaluate vegetative growth (Chouard, 1946; Bailey and Rossi, 1964; Jonkers, 1965; Risser and Robert, 1993). The photoperiod and temperature decreases cause other effects on strawberry development, such as the decrease of runner production (Smeets, 1980), flower induction (Dennis et al., 1970; Durner and Poling, 1987) and the induction of dormancy (Darrow and Waldo, 1933; Guttridge, 1968). This last effect causes physiological changes in strawberry plants, resulting in a low level of growth potential which prevents any vegetative growth development in autumn (Arney, 1955). Later, strawberry plants recover vegetative and floral vigour under a chilling effect in autumn and winter (Chouard, 1956; Guttridge, 1958; Risser and Robert, 1993). Until now, no test was available to assess the decrease of growth potential at the end of summer (dormancy induction). Moreover, because the growth potential change occurs during the decrease of vegetative growth (directly imposed by photoperiod and temperature changes), no direct morphological observations can reveal the influence of this change on vegetative growth. In actual strawberry farming, determining the period of this dormancy is important. So, in this study, in order to control the major role of photoperiod and temperature on vegetative growth, and thus to reveal the possible influence of the growth potential decrease on vegetative growth during the induction of dormancy, the petiole lengths of strawberry plants were measured under field conditions and correlated with photoperiod and temperature values. Finally, to have a practical test to determine dormancy induction, the growth potential of some strawberry cultivars cultivated in controlled climatic conditions was evaluated by petiole length measurements and the validity of this test was discussed. 2. Materials and methods 2.1. Plant material In Avignon ( N, E), young strawberry plants (Fragaria ananassa Duch.) were planted in pots ( m 3, natural compost) and they were left outside from the 2 August in a nursery. Observations were made on the cultivars Favette, Valeta, Redgauntlet and Selva from August to November. In Clermont-Ferrand ( N, E), young strawberry plants were planted in June in pots ( m 3 ; compost of sphagnum, ph 6.5) and left outside,
3 F. Robert et al. / Scientia Horticulturae 82 (1999) 217± exposed to the natural climate in a nursery. Observations were made on the cultivars Favette, Elsanta, Redgauntlet and Selva from July to November Observations of strawberry plants in the field Vegetative growth changes were evaluated by measuring petiole lengths: the new growing petioles were marked at regular dates (seven in Avignon and nine in Clermont-Ferrand) by colour threads and their lengths were measured when the petioles were fully grown. The averages of the petiole lengths marked by the same colour thread were computed. To evaluate the influence of climatic factors on the growth changes, the petiole lengths marked at regular dates (L), were considered as the dependent variable. They were regressed against two independent variables: photoperiod (P) and temperature (T). The regression equation was as follows: L ˆ ap bt c, where c is constant. We used a two-step estimation in order to avoid the collinearity between photoperiod and temperature. The temperature variable was regressed against the photoperiod variable and the residue (rest) of this regression was saved and then used to replace the temperature variable in the above equation. The residue that is obtained represents the effect of temperature on the length of petioles which is not explained by photoperiod. We therefore obtained L ˆ ap b rest c. For these measurements, the reference date was the date the leaf emerged from the bud's sheath. For photoperiod, we used photoperiod at the emerged date (P 0 ) of the petiole or at 10, 20, 30, 40 and 50 days before emergence (P 10, P 20, P 30, P 40, P 50 ), or at 10 and 20 days after emergence (P 10, P 20 ). For temperatures (in 8C), we used day temperatures (T D ), night temperatures (T N ), average of day and night temperatures (T) or difference between day and night temperatures (T D N ) for various periods: at the emerged date of the petiole (0), average of 10, 20 or 30 days before emergence (0/ 10; 0/ 20; 0/ 30), average of 10 or 20 days after emergence (0/ 10; 0/ 20), average of 10±30 days before emergence ( 10/ 30) and average of 20±40 days before emergence ( 20/ 40) Observations under standard climatic conditions Favette, Elsanta, Redgauntlet and Selva plants of cultivars were obtained and stocked as those in field conditions in Avignon before they were transferred into a growth chamber at various dates (photoperiod): D1 ˆ 5 July (15 h 20); D2 ˆ 16 July (15 h 05); D3 ˆ 30 August (13 h 16) and D4 ˆ 4 November (10 h 10). The growth chamber conditions were 25/15 18C (day/night) with a 12 h light photoperiod (artificial metal halogen lighting mmol m 2 s 1 ), in 80% relative humidity. Vegetative growth changes of strawberry plants were evaluated,
4 220 F. Robert et al. / Scientia Horticulturae 82 (1999) 217±226 as in the field, by measuring the length of the full-grown petioles which emerged only after the transfer of plants to the growth chamber. Growth potential changes of strawberry plants were evaluated two months after the transfer of plants into the growth chamber, by comparing the petiole length measurements of different series Statistical analysis For the field observations, petiole length averages were tested for each cultivar, using a multiple range test (p < 0.05; StateGraphic software). For multiple regressions, the significance level for each term was reported. For observations under standard climatic conditions, the regressions between the averages of each cultivar were computed. 3. Results 3.1. Observations of strawberry plants in the field Petiole length measurements of strawberry plants observed under natural conditions revealed the decrease of vegetative growth. In Avignon (Table 1), a decrease in petiole lengths was noted from 16 August for cultivars Valeta, Redgauntlet and Selva plants, and from 30 August for cultivar Favette. This decrease was rapid for all cultivars, and led to short petioles for Favette, Valeta and Redgauntlet plants at the beginning of autumn. In Clermont-Ferrand (Table 2), petiole lengths of cultivars Elsanta and Selva remained long from 26 June to 16 August, whereas those of Favette and Redgauntlet decreased sooner, from 2 August to 11 July, respectively. As measured in Avignon, the petiole Table 1 Petiole lengths (in mm) of strawberry plants (average of four petioles) observed under natural climatic conditions in Avignon ( N, E) Emerged date of petioles Cultivars Favette Valeta Redgauntlet Selva 8/16 133a 149a 23a 135a 8/30 145a 109b 75b 111ab 9/13 82b 76c 54bc 78b 9/27 58b 48d 40c 70bc 10/11 30c 25e 28d 51c 10/25 24c 23e 20de 44d 11/08 23c 21e 20e 42d Note: For each cultivar, the values followed by different letters are significantly different at the 0.05 probability level.
5 Table 2 Petiole lengths (in mm) of strawberry plants (average of seven petioles) observed under natural climatic conditions in Clermont-Ferrand ( N, E) Emerged date of petioles F. Robert et al. / Scientia Horticulturae 82 (1999) 217± Cultivars Favette Elsanta Redgauntlet Selva 6/26 96a 98a 128a 147ab 7/02 102a 85a 122a 136ab 7/11 108a 110a 91b 159a 7/22 91ab 100a 96b 132ab 8/02 88b 93a 96b 133ab 8/16 71c 89a 77c 130bc 9/15 49d 48b 50d 116c 9/30 36e 38c 39e 97d 10/15 27f 28d 29f 81e Note: For each cultivar, the values followed by different letters are significantly different at the 0.05 probability level. length of cultivar Selva plants remained more important than those of the other cultivars. The small difference between petiole growth changes in Avignon and in Clermont-Ferrand was due to a temperature variation between the two cities: warmer in Avignon than in Clermont-Ferrand at the same dates, the photoperiod being approximately comparable. Regression analysis revealed that the photoperiod 30 days before the emerged date of the petiole (P 30 ) and the mean of day and night temperatures 20 days after the emerged date of the petiole (T 0/ 20 ), were the most influential factors for all the cultivars (Table 3). So, the relation between petiole length, photoperiod and temperature values, can be formulated as L ˆ ap 30 b rest 0/ 20 c, where rest 0/ 20 is the residual term obtained from the regression of T 0/ 20 (dependent variable) against P 30 (independent variable). These analyses show a clear influence of other photoperiods which should be due to the fact that photoperiod variations were closely linked in this season Observations under standard climatic conditions Petiole length measurements of strawberry plants transferred into the growth chamber at various dates were analysed. They showed different vegetative changes for the four cultivars (Fig. 1): ± For cultivar Favette, growth of petioles was reduced after D1 (5 July), D2 (16 July) and D3 (30 August) transfers, whereas it was maintained for `Selva' plants. For `Elsanta' and `Redgauntlet', petiole lengths decreased rapidly after transfer.
6 222 F. Robert et al. / Scientia Horticulturae 82 (1999) 217±226 Table 3 The best determinants of the length of petioles are estimated as L ˆ ap 30 b rest 0/ 20 c Site Cultivar c a b R 2 Cl-Fd Favette c 7.37 b 0.7 c Elsanta c 6.28 c 0.79 c Selva c c Redgauntlet c 6.93 b 0.72 c Avignon Favette c 3.55 a 0.77 c Valeta c 7.7 a 0.83 c Selva c 4.55 a 0.62 c Redgauntlet c 10.4 b 0.8 c Note: The coefficients (a and b) of the independent variables (P 30 and T 0/ 20 ) are reported in the table. Significances of the partial implication of independent variables are indicated between brackets. For Clermont-Ferrand (Cl-Fd), n ˆ 9 and for Avignon, n ˆ 7. a p < b p < c p < ± In the last series (D4; 4 November), all petiole lengths of the four cultivars remained short after transfer. The comparison of petiole lengths of the different series two months after transfers (56 days for D1, 59 for D2, 56 for D3 and 63 for D4) revealed a rapid decrease of the growth potential for cultivars Favette and Elsanta at the end of summer, whereas Redgauntlet and Selva cultivars maintained growth until autumn (Fig. 2). Regressions between petiole lengths of cultivars confirm the similarity, e.g. `Favette' against `Elsanta', r ˆ 0.98 (p < 0.05); `Redgauntlet' against `Selva', r ˆ 0.97 (p < 0.05); `Favette' against `Selva', r ˆ 0.77 (p > 0.05); `Favette' against `Redgauntlet', r ˆ 0.8 (p > 0.05); `Elsanta' against `Selva', r ˆ 0.79 (p > 0.05); `Elsanta' against `Redgauntlet', r ˆ 0.77 (p > 0.05). 4. Discussion The effect of photoperiod and temperature changes on growth decrease of strawberry plants had been shown by some authors (Darrow and Waldo, 1934; Arney, 1956; Piringer and Scott, 1964; Gosselink and Smith, 1966; Heide, 1977; Durner and Poling, 1987). Although the measurement of petiole length appears to be the best parameter to evaluate vegetative growth, no test is available to assess the autumnal decrease of growth potential during the induction of dormancy. In our study, the evaluation of vegetative growth of several strawberry cultivars observed in the field, through petiole length measurements, showed different
7 F. Robert et al. / Scientia Horticulturae 82 (1999) 217± Fig. 1. The final lengths of the petioles that emerged after plant transfers from outdoors to a growth chamber at various dates. A: D1 ˆ 5 July; B: D2 ˆ 16 July; C: D3 ˆ 30 August and D: D4 ˆ 4 November.
8 224 F. Robert et al. / Scientia Horticulturae 82 (1999) 217±226 Fig. 2. The final lengths of the petioles that emerged two months after plant transfers from outdoors to a growth chamber at various dates. D1 ˆ 5 July; D2 ˆ 16 July; D3 ˆ 30 August and D4 ˆ 4 November. morphological responses to photoperiod and temperature variations at the end of summer (Tables 1 and 2). `Redgauntlet' plants exhibited a precocious vegetative growth decrease. Length decreases of the successive growing petioles were less important for `Selva' and `Elsanta' compared to other cultivars. So, cultivars are differently sensible to environmental factors for their vegetative growth behaviour, as for flowering (Darrow and Waldo, 1934; Arney, 1956; Durner et al., 1984) or runner production (Piringer and Scott, 1964; Dennis et al., 1970; Durner and Poling, 1987). The results obtained here confirm the major role of photoperiod and temperature in the decrease of vegetative growth (Table 3). According to these results, it appears that photoperiod 30 days before the emergence of the petiole (P 30 ), and, to a lesser extent, temperature during growth of the petiole (T 0/ 20 ), had the greatest influence on petiole development (Table 3). The biometrical analyses confirm the major role of photoperiod and temperature on petiole growth decrease, but they also reveal that these factors cannot explain totally this decrease. So, the unexplained part of the influence should be due, at least partly, to internal factors, notably for `Selva' which is less influenced by external factors. The change in growth potential under photoperiod and temperature decreases (dormancy induction) should be the major internal factor contributing to the decrease of vegetative growth. To reveal this change, we evaluated the growth potential of strawberry plants during their vegetative growth decrease: the observation of strawberry plants transferred to standard climatic conditions (from 15 h 20 (D1), 15 h 05 (D2) and 13 h 16 (D3) to 12 h 00 in growth chamber) at different times showed different growth responses (Fig. 1(A)±(C)). The last transfer (D4) had no effect on the growth of petioles, even if the photoperiod conditions of the growth chamber were longer than those of field (Fig. 1(D)). In these conditions, the physiological state of the strawberry plants may be the main
9 F. Robert et al. / Scientia Horticulturae 82 (1999) 217± cause of this morphological response, petiole length depending upon the growth potential. Also, two months after transfer, petiole length comparisons between the different series of strawberry plants (Fig. 2) confirmed the growth potential decrease that was induced in late summer in `Elsanta' and `Favette'. So, these standard climatic conditions could reveal the growth potential of the strawberry plants and could be used as a test to reveal the dormancy induction of these plants. Our results confirm the possibility of a major influence of growth potential on vegetative growth. In the field, this influence occurred with the additional effect of natural factors. If natural factors are able to influence growth potential and vegetative growth, growth responses to these factors are different. For example, in Avignon, the vegetative growth decrease of `Redgauntlet' plants started on 16 August (Table 2), whereas the growth potential decrease occurred after 30 August (Fig. 3). The dormancy induction, through growth potential decrease, was later in the season than the vegetative growth decrease, which could imply drastic physiological changes. We conclude that vegetative growth decrease is an early phenomenon in the summer. Moreover, the results have shown the major role of photoperiod and temperature in the development of the petiole which was different for different cultivars, but also the effect of growth potential decrease on this vegetative growth. Petiole measurements of strawberry plant transferred from outdoors into a growth chamber have confirmed these differences between cultivars. The same measurements made two months after transfer have permitted the evolution of the growth potential of these plants to be assessed. So, these standard climatic conditions could be used to test the dormancy induction of strawberry plants. Acknowledgements The authors gratefully thank the ``Centre InterreÂgional de Recherche et d'expeârimentation de la Fraise'' for its contribution in equipment and the ``Centre Technique Interprofessionnel des Fruits et LeÂgumes'' for financial support. We also thank Mrs Lenne for her corrections and suggestions. References Arney, S.E., Studies of growth and development in the genus Fragaria. IV. Winter growth. Ann. Bot. 74, 265±276. Arney, S.E., Studies of growth and development in the genus Fragaria. VI. The effect of photoperiod and temperature on leaf size. J. Exp. Bot. 7, 65±79. Bailey, J.S., Rossi, A.W., Effect of fall chilling, forcing temperature and day length on the growth and flowering of Catskill strawberry plants. Proc. Amer. Soc. Hort. Sci. 7, pp. 245±252.
10 226 F. Robert et al. / Scientia Horticulturae 82 (1999) 217±226 Chouard, P., About effect of photoperiod on growth (in French). C.R. Acad. Sci., Paris 223, 1174±1176. Chouard, P., Forcing and temperature-photoperiod preparations. In: Tournier and Constans (Eds), Dormancy and inhibition of seeds and buds (in French). Centre de Docum. Univ., Paris, pp. 1±160. Darrow, G.M., Waldo, G.F., Photoperiodism as a cause of the rest period in strawberries. Science 77, 353±354. Darrow, G.M., Waldo, G.F., Responses of strawberry varieties and species to duration of the daily light period. USDA Tech. Bul. 453, 1±31. Dennis, F.G., Lipecki, J., Kiang, C.L., Effects of photoperiod and other factors upon flowering and runner development of three strawberry cultivars. J Amer. Soc. Hort. Sci. 95, 750± 754. Durner, E.F., Poling, E.B., Flower bud induction, initiation, differentiation and development in the `Earliglow' Strawberry. Sci. Hort. 31, 61±69. Durner, E.F., Barden, J.A., Himelrick, D.G., Poling, E.B., Photoperiod and temperature effects on flower and runner development in day-neutral, junebearing, and everbearing strawberries. J. Amer. Soc. Horti. Sci. 109, 396±400. Gosselink, J.G., Smith, C.R., Vegetative growth responses of strawberry plants to differing photoperiods. Hort. Res. 7, 24±33. Guttridge, C.G., The effect of winter chilling on the subsequent growth and development of the cultivated strawberry plant. J. Hort. Sci. 33, 119±127. Guttridge, C.G., Hormone physiology of growth regulation in strawberry. In: Plant growth Regulators, S.C.I. Monograph. 31, pp. 157±169. Heide, O.M., Photoperiod and interactions in growth and flowering of strawberry. Physiol. Plant. 40, 21±26. Jonkers, H., On the flower formation, the dormancy and the early forcing of strawberries. Med Landbwg Wageningen 65, 1±71. Piringer, A.A., Scott, D.H., Interrelation of photoperiod, chilling, and flower-cluster and runner production by strawberries. J. Amer. Soc. Hort. Sci. 84, 295±301. Risser, G., Robert, F., What cold treatments promote growth in strawberry?. Acta Hortic. 48, 381±383. Smeets, L., Effect of temperature and daylength on flower initiation and runner formation in two everbearing strawberry cultivars. Sci. Hortic 12, 19±26.
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