The temperature and photoperiod regulation of flowering and runnering in the strawberries, Fragaria chiloensis, F. virginiana, and F. x ananassa

Scientia Horticulturae 103 (2005) 167–177

The temperature and photoperiod regulation of flowering and runnering in the strawberries, Fragaria chiloensis, F. virginiana, and F. x ananassa Sedat Serçe1 , James F. Hancock∗ Department of Horticulture, Michigan State University, East Lansing, MI 48824, USA Accepted 8 April 2004

Abstract The temperature and photoperiod interactions of a number of elite genotypes of Fragaria virginiana, F. x ananassa, and F. chiloensis were studied in a series of growth chamber experiments. Several parameters were evaluated including: (1) the critical day-length (CDL) for flowering of short day (SD) genotypes under 8, 9, 10, and 11 h days at 18 ◦ C, (2) the floral and runnering response of single and multiple cropping genotypes under 8 and 16 h days at 18 ◦ C, and (3) the effect of temperature on flower bud formation in day-neutral (DN) genotypes held at 18, 22, 26, and 30 ◦ C under 12 h day-lengths. The same number of flowers were initiated under 15 and 30 day induction periods, regardless of photoperiod. Frederick 9, LH 50-4 and RH 30 (F. virginiana), ‘Aromas’ and ‘Tribute’ (F. x ananassa) and CFRA 0368 of F. chiloensis flowered under both long days (LDs) and SDs; while Eagle-14 (F. virginiana), ‘Fort Laramie’ and ‘Quinalt’ (F. x ananassa) flowered only under long days. While those genotypes that flowered under both LD and SD can be considered day-neutral, they varied in the degree of floral response to the two photoperiods. CFRA 0368 and Frederick 9 produced the same number of flowers under both LDs and SDs, while ‘Aromas’ and ‘Tribute’ had more flowers under LDs and RH 30 had more under SDs. Of the DN genotypes, LH 50-4 and RH 30 were the only ones that produced runners under SDs. Flowering in ‘Fort Laramie’ was least affected of any genotype by high temperature, although its dry weight was negatively impacted. Based on these data, several genotypes show promise as breeding parents: CFRA 0368 and Frederick 9 to equalize flower production under LD and SD conditions, LH 50-4 and RH 30 to produce more freely runnering DNs, and ‘Fort Laramie’ for floral heat tolerance. © 2004 Published by Elsevier B.V. Keywords: Germplasm; Day-neutral; Short day; Long day; Critical day-length; Heat tolerance

∗ Corresponding author. Tel.: +1-517-353-6460; fax: +1-517-353-0890. E-mail addresses: [email protected] (S. Serçe), [email protected] (J.F. Hancock). 1 Present address: Department of Horticulture, Mustafa Kemal University, Antakya, Hatay 31034,Turkey.

0304-4238/$ – see front matter © 2004 Published by Elsevier B.V. doi:10.1016/j.scienta.2004.04.017

168

S. Serçe, J.F. Hancock / Scientia Horticulturae 103 (2005) 167–177

1. Introduction Temperature and photoperiod are the most important environmental factors that regulate the transition from vegetative to floral growth in strawberries (Darrow, 1936). All three photoperiodic types, short day (SD), long day (LD), and day-neutral (DN) exist in Fragaria, although most of the commercial octoploid cultivars grown are either SD or DN (Hancock, 1999). Floral induction in SD cultivars is under facultative control, meaning that when temperatures are above about 15 ◦ C they form flower buds under SD conditions, but under cooler temperatures, they form flower buds regardless of photoperiod (Guttridge, 1985). DN cultivars generate flower buds cyclically regardless of photoperiod if temperatures are at least moderate (<28 ◦ C) (Durner et al., 1984; Galletta and Bringhurst, 1990; Guttridge, 1985). While distinct differences have been observed between SD, LD, and DN genotypes in some studies (Durner et al., 1984), several other studies have shown that the photoperiod response is actually continuous (Nicoll and Galletta, 1987; Yanagi and Oda, 1989). Darrow (1966) first suggested that strawberry genotypes actually range from obligate SD to facultative SD to complete DNs, and indicated that DN types vary in their flowering expression from weak to strong. What have been called infra short day types fall into the middle of this range (Izsak and Izhar, 1984). Nicoll and Galletta (1987) tested the temperature and photoperiod response of a number of DNs with strong, weak, and very weak flowering responses, as well as older LD and SD types and found a wide, almost continuous range in response. The use of the term “everbearing” has added complexity to the literature regarding the temperature and photoperiod interaction for flower bud formation. Everbearers have been described as plants fruiting more than one time in a year, with synonymies being “perpetual”, “rebloomer”, “cyclic flowering”, “double-cropping”, “multiple cropping” and most recently, “day-neutral” (Galletta and Bringhurst, 1990). Nicoll and Galletta (1987) stated that the term “day-neutral” and “everbearer” can be used interchangeably, only if DN is used as a physiological term to denote a relative insensitivity to day-length in flower bud initiation and everbearer is used as an agricultural term to indicate a pragmatic expectation of summer strawberry production. Runnering has been shown to be stimulated by long days and high temperatures in all flowering classes of strawberries. Darrow (1936) and Durner et al. (1984) demonstrated that if a genotype produces any runners, it will do so under long days and higher temperatures (greater than about 14 ◦ C). Smeets (1980) studied runner formation in ‘Rabunda’ and ‘Revada’ held under combinations of 14, 20, and 26 ◦ C for 8, 16, 24 h days. Although runners were observed in all treatments, 20 and 26 ◦ C treatments generated significantly more runners than 14 ◦ C, while 16 and 24 h days generated significantly more runners than the 8 h day-length treatment. Sonsteby (1997) also found higher runner numbers under high temperatures in an experiment where he studied the effect of 9, 15, and 21 ◦ C temperature regimes at 8 and 24 h days using ‘Bounty’, ‘Elsanta’, ‘Korona’ and ‘Senga Sengana’. This study was designed to compare the temperature and photoperiod requirements of a number of elite wild genotypes to DN and SD representatives of Fragaria x ananassa. These genotypes have been characterized in the field, but not under controlled conditions (Hancock et al., 2001a,b; Serçe and Hancock, 2002; Serçe et al., 2002). Several parameters

S. Serçe, J.F. Hancock / Scientia Horticulturae 103 (2005) 167–177

169

were evaluated including: (1) the critical day-length (CDL) for flowering of SD genotypes under 8, 9, 10 and 11 h days at 18 ◦ C; (2) the floral and runnering response of single and multiple cropping genotypes under 8 and 16 h days at 18 ◦ C; and (3) the effect of temperature on flower bud formation in DN genotypes held at 18, 22, 26, and 30 ◦ C under 12 h day-lengths. The primary goal was to find DN breeding parents that were free runnering, strong flowering under LD and SD conditions and had floral heat tolerance. We were also interested in determining whether there is a range in the day-length requirements of SD genotypes, in hopes of identifying genotypes that begin flowering earlier in the summer to maximize the number of floral primordia produced before fall frosts.

2. Material and methods 2.1. Experiment 1: effects of day-length on flowering and runnering This experiment was conducted to determine the CDL for floral induction in a wide range of native and cultivated SD genotypes. The representatives of F. x ananassa studied and their state of origin were: ‘Allstar’ (Maryland), ‘Chandler’ (California) and ‘Honeoye’ (New York). The elite wild genotypes examined were CFRA 0024 (central Chile) and CFRA 0368 (Alaska) of F. chiloensis, and Eagle 14 (Ontario) of F. virginiana. Runners from each genotype were gathered from a field planting at the Michigan State University (MSU) Horticultural Research Farm (East Lansing, Mich.) on 30 August 2001 and placed under mist for rooting. On 9 September 2001, 40 rooted runners were potted into 14 cm × 12 cm × 12 cm pots and set in a greenhouse. The plants were maintained under 13 h day-lengths using supplementary lights (∼800 ␮mol s−1 m−2 ) to prevent floral induction. On 31 October 2001, 40 plants of each genotype were transferred into four growth chambers at 18 ◦ C with 8, 9, 10 or 11 h day-lengths. In each chamber, photosynthetically available radiation (PAR) was varied with day-length so that the total energy received was equal (∼800, 710, 640 and 580 ␮mol s−1 m−2 for 8, 9, 10, and 11 day-length chambers, respectively). After 15 and 30 days, five plants of each genotype from each chamber were placed in a greenhouse held at 13 h day-length using supplementary lights (∼800 ␮mol s−1 m−2 ). The numbers of flowers and runners produced by each plant were recorded on 15 November, 25 November, and 6 December 2001. At the end of the experiment, dry weights were determined for each plant after washing their roots free of soil and drying them at 72 ◦ C for 3 days. The initial analysis indicated that the same number of flowers and runners were induced under both 15 and 30 h days under the various day-lengths. Thus, these two treatments could be treated as blocks in evaluating the effect of the different day-lengths. Analysis of Variance (ANOVA) was conducted for total flower and runner numbers, and dry weights using the SAS program (SAS Institute, Cary, NC). 2.2. Experiment 2: photoperiod regulation of flowering and runnering This experiment was designed to determine the photoperiod sensitivity (DN or LD) of a number of elite wild selections, old “everbearing” cultivars and more recently released DN

170

S. Serçe, J.F. Hancock / Scientia Horticulturae 103 (2005) 167–177

types. The goal was to identify new day-neutral parents. The genotypes included were the everbearing cultivars ‘Fort Laramie’ and ‘Quinalt’; the DN cultivars ‘Aromas’ and ‘Tribute’, the native F. virginiana selections Frederick 9, LH 50-4, RH 30, and the F. chiloensis selection CFRA 0368. Further information on the elite wild clones is available in Hancock et al. (2001a–c). The cultivars were purchased as frigo plants from Gurney’s Seed & Nursery (Yankton, SD), while the dormant F. virginiana clones were dug from the MSU Research Farm, East Lansing, on April 2001. Ten plants of each genotype were potted into 14 cm × 12 cm × 12 cm pots using a commercial planting mix (Michigan Peat Company, Houston, TX). The potted plants were arranged as a completely randomized design in a greenhouse at MSU on 11 April 2001 and were held for 3 months under 12 h day-length maintained with supplementary light (∼800 ␮mol s−1 m−2 ). During this period, all of the genotypes flowered. On 11 July 2001 the plants were randomly placed into two growth chambers at 18 ◦ C, 8 h day-length and 800 ␮mol s−1 m−2 PAR or 18 ◦ C, 16 h day-lengths with 400 ␮mol s−1 m−2 PAR. PAR was varied with day-length by altering the number of lights, so that the total energy received by the plants in each chamber was equal. The plants were given a 7-week induction period, and then flower and runner numbers were recorded on 4, 10, 17, 22 September 2001. No data were recorded on the flowers and runners that developed before this time, as they could have been initiated before the plants were placed into the greenhouse. At the end of the experiment, each plant was dried at ∼72 ◦ C for 3 days and weighed. Analysis of variance was calculated for all variables using the SAS program (SAS Institute, Cary, NC). 2.3. Experiment 3: temperature effects on flowering and runnering This experiment was designed to evaluate the effect of temperature on flowering in a number of old everbearing cultivars developed in North Dakota where very warm summer temperatures occur, and several elite F. virginiana genotypes collected from a wide range of environments. The goal was to identify genotypes that can form flower buds under higher temperatures (>26 ◦ C). The genotypes studied were the elite F. virginiana genotypes Brighton-3 (Utah), LH 30-4 (Montana), LH 39-15 (Montana), LH 40-4 (Montana), LH 50-4 (Montana), RH 23 (Minnesota), RH 30 (Minnesota), RH 43 (Alaska), RH 45 (Alberta); and F. x ananassa ‘Aromas’, ‘Fort Laramie’, ‘Ogallala’, and ‘Tribute’. Further information on the native elite genotypes can be found in Sakin et al. (1997) and Hancock et al. (2001a–c). The cultivars were purchased from Gurney’s Seed & Nursery (Yankton, SD) as frigo plants and the dormant F. virginiana clones were dug at the Michigan State University Horticultural Research Farm in August 1999. Twenty-eight plants of each genotype were potted on 5 August 1999 into 14 cm × 12 cm × 12 cm pots in a commercial planting mix (Michigan Peat Company, Houston, TX), and placed in different growth chambers held at either 18, 22, 26, or 30 ◦ C, 12 h day-lengths and ∼600 ␮mol s−1 m−2 PAR. Five replicates of each genotype were placed in a completely randomized design in each temperature treatment. After a 7-week induction period, the number of flowers and runners were recorded weekly for a 10-week period. At the end of this time, the plants were partitioned into root, crown, leaf and runners. The dry weights of the plant organs were determined after drying them at 72 ◦ C for three days.

S. Serçe, J.F. Hancock / Scientia Horticulturae 103 (2005) 167–177

171

The same experiment was repeated in the summer of 2002 (from 12 April to 17 August) with six instead of five replicates for each treatment; and some of the genotypes were dropped and replaced by others. The genotypes included in the second trial were: the F. x ananassa cultivars, ‘Aromas’, ‘Fort Laramie’, ‘Quinalt’, ‘Tribute’, and the elite F. virginiana genotypes, Frederick 9, LH 50-4, and RH 30. The number of flowers, and runners were recorded weekly for 4 weeks after a 7-week induction period. At the end of the experiment, the total dry weight of each plant was determined by holding them at 72 ◦ C for three days. The SAS program (SAS Institute Inc., 1990, SAS Institute, Cary, NC) was used to conduct analysis of variance. The common genotypes in each trial were considered as blocks. 3. Results 3.1. Experiment 1: effects of day-length on flowering and runnering There was not a significant difference observed between the genotypes for CDL. All genotypes produced one inflorescence, regardless of photoperiod, and the total number of flowers generated by each genotype was not significantly different under either the 15 or 30 days induction period (data not presented). Length of photoperiod had a significant effect on floral induction and runner production but not dry weights (Table 1). There were no significant differences in the number of inflorescences produced under each photoperiod, but significantly different numbers of flowers per inflorescence were observed under the different day-length treatments. The average number of flowers for 8, 9, 10, and 11 h days were 4.2, 3.5, 3.5, and 5.1, respectively. There was a broad range in response to photoperiod among the different genotypes. The flowering response of ‘Honeoye’ fit a quantitative SD model, where shorter days result in more flowers. Eagle 14 had the most flowers at the longest day-length, suggesting that it is a LD type. The other genotypes showed no consistent pattern across photoperiods (‘Allstar’, ‘Chandler’, CFRA 0024 and CFRA 368). There was a significant genotype x environment interaction between day-length and runner production (Table 1). However, only Eagle 14 and CFRA 0368 produced appreciable numbers of runners; Eagle 14 showed no consistent trend; while CFRA 0368 had the most runners under 11 h day-lengths. ‘Allstar’, ‘Honeoye’, ‘Chandler’ and CFRA 0024 produced few runners to none. 3.2. Experiment 2: photoperiod regulation of flowering and runnering Two types of flowering patterns were observed among the various genotypes tested: (1) DN types that flowered under both LD and SD conditions (‘Aromas’, ‘Tribute’, CFRA 0368, Frederick 9, LH 50-4, RH 30), and (2) LD types that flowered under LD but not SD conditions (‘Fort Laramie’ and ‘Quinalt’) (Table 2). CFRA 0368 and Frederick 9 had about the same number of flowers under 8 and 16 h photoperiods, while ‘Aromas’ and ‘Tribute’ had many more flowers under LDs, and LH 50-4 and RH 30 had more flowers under SDs. The mean inflorescence number ranged from 1.0 (CFRA 0368) to 3.0 (Frederick 9) in the DN types and 0.2 (RH 30) to 3.4 (‘Tribute’) in the LD types. Frederick 9 had the highest total number of flowers (15.4) under SDs, while ‘Tribute’ produced the most flowers under LDs (25.6).

172

S. Serçe, J.F. Hancock / Scientia Horticulturae 103 (2005) 167–177

Table 1 ANOVA and means for flower and runner numbers, and dry weights of strawberry genotypes grown at 18 ◦ C and either 8, 9, 10, or 11 h days. Means in each column not followed by the same letter are significantly different at P < 0.05 according to the Duncan‘s multple range test Source

Flower number 8h 9h 10 h

11 h

Runner number Dry Weight 8h 9h 10 h 11 h 8 h 9h

10 h

F. x ananassa ‘Allstar’ ‘Chandler’ ‘Honeoye’

3.8b 2.6a 1.9bc 1.7b 5.3c 4.2b

3.3ab 4.2b 0.0 0.7a 2.3c 0.5 3.1a 3.6ab 0.0

F. chiloensis CFRA 0024 CFRA 0368

6.5b 2.2a

5.0a 4.5c

5.8ab 7.0b 0.1 0.7 3.3b 4.0bc 0.7a 0.6a

0.2 0.1 0.4a 1.9b

F. virginiana Eagle-14

5.6b

2.8a

4.7b

2.6b 3.1c

ANOVA

d.f.

Mean square

d.f.

Mean square

d.f.

Mean square

32.2 34.5∗ 8.7 103.2∗∗ 15.2∗ 7.8

1 3 35 5 15 180

0.2 2.0∗∗ 0.4∗ 42.2∗∗ 1.3∗ 0.3

1 3 35 5 15 180

4.6 5.2 5.5 569.5∗∗ 15.4 6.8

Block 1 Day-length (D) 3 Whole-plot error 35 Genotype (G) 5 D×G 15 Error 180 ∗

9.3c

0.0 0.2 0.0

2.0a 3.0c

0.0 0.0 0.0

0.0 0.4 0.0

11 h

12.3b 9.9b 10.5b

10.8a 11.0c 9.7a

4.5b 7.4

4.5b 8.5

4.8b 8.5

3.2a 8.5

3.4b

3.8b

3.4b

2.9a

16.0c 14.3b 8.0a 8.5a 10.3b 11.1b

Mean squares significant at 0.05. Mean squares significant at 0.01.

∗∗

Table 2 Means and standard errors for flower and runner numbers, and dry weights of strawberry genotypes grown at 18 ◦ C and either 8 or 16 h days Genotypes

Inforescence number

Total flower number

Fl. Number/ inflorescence

Runner number

Dry weight (g)

8h

16 h

8h

16 h

8h

16 h

8h

16 h

8h

16 h

F. x ananassa ‘Aromas’ ‘Fort Laramie’ ‘Quinalt’ ‘Tribute’

1.4 0.0 0.0 1.8

3.2∗ 2.6∗ 3.4∗ 3.4∗

4.0 0.0 0.0 6.0

14.0∗ 13.4∗ 23.0∗ 25.6∗

3.0 0.0 0.0 3.1

4.4∗ 5.2∗ 6.9∗ 7.6∗

0.0 0.0 0.0 0.0

0.0 0.0 0.2 0.0

29.8 26.3 30.8 23.1

33.2∗ 36.0∗ 22.0∗ 30.2∗

F. chiloensis CFRA 0368

1.0

0.8

4.2

4.6

4.2

4.6

0.0

2.8

22.9

25.3∗

F. virginiana Frederick 9 LH 50-4 RH 30

3.0 2.0 1.2

2.2∗ 0.8∗ 0.2∗

15.4 8.8 5.8

16.0 4.4∗ 2.4∗

5.1 3.5 4.8

7.2∗ 2.4 2.4

0.0 1.4 0.2

0.0 4.4∗ 3.8∗

18.4 17.1 16.4

15.1 20.3 18.5

∗

Mean values in the two columns are significantly different at the 0.05 level using the t-test.

S. Serçe, J.F. Hancock / Scientia Horticulturae 103 (2005) 167–177

173

There was a significant interaction for runner production between length of photoperiod and genotype (Table 2). ‘Aromas’, ‘Tribute’, Frederick 9, and ‘Fort Laramie’ produced no runners under either LDs or SDs. CFRA 0368, and to a limited extent ‘Quinalt,’ produced runners only under LDs. LH 50-4 and RH 30 produced runners under both photoperiods, but they had many more under LDs than SDs. Differences in response to photoperiod were observed among genotypes for dry weight accumulation in the two day-length treatments. ‘Aromas’, CFRA 0368, ‘Fort Laramie’ and ‘Tribute’ had higher mean dry weight under LD than SD, whereas ‘Quinalt’ had higher mean dry weight under SD than LD (Table 2). Frederick 9, LH 50-4 and RH 30 did not vary significantly across day-length. 3.3. Experiment 3: temperature effects on flowering and runnering There was no significant difference between the two trials in numbers of crowns, inflorescences, flowers and runners (data not shown), although plants were 37% heavier in the second trial (means = 8.5 versus. 6.2 g). Temperature had a significant effect on flower number, but not crown or inflorescence numbers (Table 3). The mean number of flowers increased progressively as temperature decreased. The mean values were 1.6, 3.1, 3.9, and 6.8 at 30, 26, 22, and 18 ◦ C. F. x ananassa cultivars had higher flower numbers than the F. virginiana genotypes, 5.7 versus. 2.8 overall and 8.4 versus. 5.3, 5.5 versus. 2.5, 4.2 versus. 2.1, and 3.3 versus. 0.4 for 18, 22, 26, and 30 ◦ C, respectively. The main effect of genotype and the genotype x temperature interaction were highly significant for flower production (Table 3). The total flower number ranged from 0.7 (Frederick 9) to 10.6 (RH 43) among the F. virginiana genotypes and 2.9 (‘Fort Laramie’) to 9.1 (‘Tribute’) among the F. x ananassa cultivars. All of the genotypes but ‘Fort Laramie’ had their lowest flower numbers under high temperatures (26 and/or 30 ◦ C). Floral production in ‘Fort Laramie’ did not vary consistently across temperature, but the number of flowers was higher at 30 ◦ C than at 18 ◦ C. The main effect of genotype and the genotype x temperature interaction were highly significant for runner production under the different temperatures (Table 3). LH 40-4, RH 23, and RH 45 did not runner in any of the temperature treatments, while LH 50-4 produced almost equal runner numbers at all temperatures. All of the F. x ananassa cultivars had very low runner numbers regardless of temperature. The genotype and genotype x temperature interactions were highly significant for dry weights (Table 3). Most genotypes were negatively impacted by the higher temperatures with declines of over 50% being common at the higher temperatures, although LH 30-4, LH 40-4 and RH 30 did comparatively better than in the other genotypes, with declines being 30% or less.

4. Discussion The number of induction cycles required to form flower buds at 18 ◦ C was 15 days or less for all the genotypes studied in this experiment. CDL has been previously reported to be between 7 and 24 depending on temperature (Hartmann, 1947a,b; Went, 1957; Larson, 1984),

Source

Flower number 18 ◦ C

Runner number

Dry weight (g)

22 ◦ C

26 ◦ C

30 ◦ C

18 ◦ C

22 ◦ C

26 ◦ C

30 ◦ C

18 ◦ C

6.3b 3.5b 9.1c 7.0b 15.8c

6.1b 2.5a 8.1c 4.0a 7.1b

2.2a 1.8a 6.3b 4.3a 7.8b

1.7a 4.6c 4.3a – 2.6a

0.0 0.1 0.0 0.0 0.0

0.3 0.0 0.0 0.0 0.0

0.1 0.0 0.0 0.0 0.2

0.6 0.0 0.0 – 0.7

13.0c 13.0c 12.0d 4.7a 15.0c

F. virginiana Brighton-3 Frederick 9 LH 30-4 LH 39 LH 40-4 LH 50-4 RH 23 RH 30 RH 43 RH 45

0.4 2.2b 2.0b 2.9b 5.0b 3.9b 30.0b 5.4c 19.0c 4.0b

0.0 0.0a 0.0a 0.0a 1.0a 3.0b 2.0a 4.9bc 11.7b 2.3ab

0.0 0.0a 3.0b 0.3a 2.3a 1.0a 6.3a 3.4b 9.7b 2.7ab

0.0 – 0.0a 0.0a 0.0a 1.0a 0.0a 0.4a 2.0a 0.7a

0.0a 0.3a 0.7 0.9 0.0 2.2 0.0 0.8 0.0 0.0

0.3a 1.8b 1.0 1.0 0.0 2.7 0.0 0.6 0.0 0.0

0.3a 0.8a 0.7 0.3 0.0 2.5 0.0 1.1 0.0 0.0

2.9b – 2.0 0.6 0.0 2.4 0.0 0.1 0.0 0.0

11.4b 3.9b 2.8b 14.7b 1.0a 9.1c 4.4b 5.5b 1.3 8.8b

Block Temperature (T) Whole-plot error Genotype (G) G×T Error ∗∗

22 ◦ C 10.8b 10.4b 8.9c 8.0c 9.9b 4.8a 2.5a 2.4ab 3.3a 2.0b 5.0b 2.2a 3.4a 2.1 7.2b

d.f.

Mean square

d.f.

Mean square

d.f.

Mean square

1 3 7 14 40 340

55.1 158.1∗∗ 13.7 236.9∗∗ 56.9∗∗ 26.1

1 3 7 14 40 340

1.0 1.2 0.7 15.1 1.3 0.7

1 3 7 14 40 340

79.1 9.5 28.7∗∗ 220.5∗∗ 20.0∗∗ 8.0

Mean squares significant at 0.01.

26 ◦ C

30 ◦ C

8.9a 11.3b 5.4a 6.9b 9.5b

8.0a 6.5a 6.8b – 5.7a

3.8a 2.1a 1.7a 1.9a 3.6c 3.9a 2.6a 3.9a 1.7 3.3a

4.8a – 2.3ab 2.1a 1.7b 3.1a 2.3a 3.7a 1.8 3.9a

S. Serçe, J.F. Hancock / Scientia Horticulturae 103 (2005) 167–177

F. x ananassa ‘Aromas’ ‘Fort Laramie’ ‘Ogallala’ ‘Quinalt’ ‘Tribute’

ANOVA

174

Table 3 Means and standard errors (in parenthesis) for flower and runner numbers, and dry weights of strawberry genotypes grown in growth chambers at 12 h days and 18, 22, 26, and 30 ◦ C. Means in each column not followed by the same letter are significantly different at P < 0.05 according to the Duncan’s multiple range test

S. Serçe, J.F. Hancock / Scientia Horticulturae 103 (2005) 167–177

175

with 7–14 cycles generally being considered adequate under cool temperatures (Guttridge, 1985). There was a broad range in floral response among the different genotypes to 8, 9, 10 and 11 h day-lengths. Since the main effect of day-length was not significant for dry weights, these differences are probably a true reflection of photoperiodic response and not PAR. Honeoye‘ fit the classical SD model (Darrow, 1936; Darrow and Waldo, 1934; Durner et al., 1984), while Eagle 14 was a LD type. We have not observed Eagle 14 flowering in the late summer in the field, as would be expected for a LD genotype (Hancock et al., 2001a); however, our high summer temperatures (25–30 ◦ C) may have inhibited its flower production (Durner et al., 1984; Hartmann, 1947a,b). In our cooled greenhouse, we have observed occasional flowers on Eagle 14 during long summer days and it has proven to be an excellent parent in producing DN progeny (Hancock et al., 2002). The other genotypes did not have a consistent floral response across photoperiods (‘Allstar’, ‘Chandler’, CFRA 0024 and CFRA 0368). These genotypes are either short day types that are not influenced in a quantitative fashion or our small sample sizes may have blurred their true physiological responses. Short day genotypes that produced as many flowers under 11 h as 8 h photoperiods would be advantageous in production fields, as they might produce more flowers before fall frosts than quantitatively regulated ones. There was a significant genotype x environment interaction between day-length and runner number, although only Eagle 14 and CFRA 0368 produced more than one runner. The reason why most of our genotypes produced so few runners may have been due to our induction temperatures being so cool (18 ◦ C). Strawberries have been reported to have the most runners under LD (Darrow, 1936; Darrow and Waldo, 1934; Durner et al., 1984; Larson, 1984) and warm temperatures (Durner et al., 1984; Heide, 1977; Smeets, 1980; Sonsteby, 1997). Two types of flowering patterns were observed among the various genotypes: (1) DN which flowered under both LD and SD conditions (‘Aromas’, ‘Tribute’, CFRA 0368, Frederick 9, LH 50-4, RH 30), and (2) LD types which flowered under LD but not SD conditions (‘Fort Laramie’ and ‘Quinalt’). These patterns mirror our field observations, except for CFRA 0368, which we have not observed flowering in the fall (Hancock et al., 2002). High summer field temperatures may have inhibited floral production in CFRA 0368, as it is from Alaska where such high temperatures are probably rare. This is an interesting finding, as no DN genotype has been reported in F. chiloensis. There were differences in how the various DNs responded to LD and SD conditions. Only Frederick 9 and CFRA 0368 produced the same number of flowers under SD and LD conditions. The other DN types produced either more flowers under LDs (‘Aromas’ and ‘Tribute’) or more under short days (LH 50-4 and RH 30). Poor mid-summer floral production in eastern DN cultivars has often been attributed primarily to high temperatures, but it is also possible that they do not flower as well under the LDs of summer than the SDs of spring and fall. Based on our data, ‘Aromas’ and ‘Tribute’ could, in fact, be SD plants with an unusually long critical day-length. Frederick 9 and CFRA 0368 may prove to be useful breeding parents to increase the mid-summer flowering response of our current day-neutral cultivars. CFRA 0368, LH 50-4, RH 30 and to some extent ‘Quinalt’ produced more runners under LDs than SDs, while ‘Aromas’, ‘Tribute’, Frederick 9, and ‘Fort Laramie’ produced no

176

S. Serçe, J.F. Hancock / Scientia Horticulturae 103 (2005) 167–177

runners under either LD or SDs. It is not known why some of the genotypes did not runner under LDs, but as previously mentioned, the cool growing temperatures (<18 ◦ C) may have inhibited runner production. Perhaps runnering in ‘Aromas’, ‘Fort Laramie’, Frederick 9, and ‘Tribute’, is more sensitive to cool temperatures than the other genotypes. It is also possible that floral bud formation is a much stronger sink than stolon formation in these genotypes, and this prevents them from runnering during flowering. If this is the case, LH 50-4 and RH 30 might be used as parents to develop day-neutral varieties that are more freely runnering. Differences were observed among the dry weights of genotypes held under the SD and LD treatments, suggesting that the PAR adjustments made at the beginning of the study may not have been maintained throughout the experiment. This imbalance may have influenced relative numbers of flowers and runners in the two treatments, but the main goal of the experiment was to determine whether a genotype flowered under LD or SD conditions. The modest differences in PAR were unlikely to have greatly impeded the overall flowering response of genotypes. Of all the genotypes tested, floral induction in ‘Fort Laramie’ appeared to be the most tolerant to high temperatures. Total dry weight in ‘Fort Laramie’ was greatly reduced by high temperature like most of the other genotypes, but ‘Fort Laramie’ was the only one to produce more flowers at 30 ◦ C than at 18 ◦ C. Dry weights in LH 40-4, RH 30 and RH 43 were the least effected by high temperature, but all of them had very few flowers at high temperatures. In a previous screen for photosynthetic heat tolerance, RH 43 also appeared to be heat tolerant (Serçe et al., 2002). Crossing ‘Fort Laramie’ with RH 43 may produce a breeding parent that has both floral and photosynthetic heat tolerance. In summary, several genotypes show promise as breeding parents: CFRA 0368 and Frederick 9 to equalize flower production under LD and SD conditions, LH 50-4 and RH 30 to produce more freely runnering DNs and ‘Fort Laramie’ for floral heat tolerance. CFRA 0368 and Frederick 9 were the only genotypes with the same number of flowers under both LDs and SDs, while LH 50-4 and RH 30 were the only genotypes that produced runners under SDs. Flowering in ‘Fort Laramie’ was least affected by high temperature of any genotype, although its dry weight was negatively impacted by heat.

Acknowledgements The authors are grateful to Turkish Ministry of Education for the scholarship of the first author during his Ph.D. and Peter W. Callow for his help and support throughout this project.

References Darrow, G.M., 1936. Interaction of temperature and photoperiodism in the production of fruit buds and runners in the strawberries. Proc. Amer. Hort. Sci. 34, 360–363. Darrow, G.M., 1966. The Strawberry: History, Breeding and Physiology. Holt, Rinehart and Winston, New York. Darrow, G.M., Waldo, G.F., 1934. Responses of strawberry varieties and species to duration of the daily light period. USDA Tech. Bul., 453.

S. Serçe, J.F. Hancock / Scientia Horticulturae 103 (2005) 167–177

177

Durner, E.F., Barden, J.E., Himelrick, D.G., Poling, E.B., 1984. Photoperiod and temperature effects on flower and runner development in day-neutral, Junebearing and everbearing strawberries. J. Amer. Soc. Hort. Sci. 109, 396–400. Galletta, G.J., Bringhurst, R.S., 1990. Strawberry management. In: Galletta, G.J., Himelrick, D. (Eds.), Small Fruit Crop Management. Prentice Hall, Englewood Cliffs, New Jersey. Guttridge, C.G., 1985. Fragaria x ananassa. In: Halvey, A.H. (Ed.), CRC Handbook of Flowering. CRC Press, Boca Raton, Florida. Hancock, J.F., 1999. Strawberries. CAB International, Wallingfer, UK. Hancock, J.F., Finn, C.A., Hokanson, S.C., Luby, J.J., Goulart, B.L., Demchak, K., Callow, P.W., Serçe, S., Schilder, A.M.C., Hummer, K.E., 2001a. A multistate comparison of native octoploid strawberries from North and South America. J. Amer. Soc. Hort. Sci. 126, 579–586. Hancock, J.F., Callow, P.W., Dale, A., Luby, J.J., Finn, C.E., Hokanson, S.C., Hummer, K.E., 2001b. From the Andes to the Rockies: Native strawberry collection and utilization. HortScience 36, 221–225. Hancock, J.F., Callow, P.W., Serçe, S., Schilder, A.M.C., 2001c. Relative performance of strawberry cultivars and native hybrids on fumigated and nonfumigated soil in Michigan. HortScience 36, 136–138. Hancock, J.F., Luby, J.J., Dale, A., Callow, P.W., Serçe, S., El-Shiek, A., 2002. Utilizing wild Fragaria virginiana in strawberry cultivar development: Inheritance of photoperiod sensitivity, fruit size, gender, female fertility and disease resistance. Euphytica 126, 177–184. Hartmann, H.T., 1947a. The influence of temperature on the photoperiodic response of the several strawberry varieties grown under controlled environment conditions. Proc. Amer. Soc. Hort. Sci. 50, 243–245. Hartmann, H.T., 1947b. Some effect of temperature and photoperiod on flower formation and runner production in the strawberries. Plant Physiol. 22, 407–420. Heide, O.M., 1977. Photoperiod and temperature interactions in growth and flowering of strawberry. Physiol. Plant. 40 (40), 21–26. Izsak, E., Izhar, S., 1984. Breeding and testing of early strawberry varieties in the central and northern Negev regions. Hassadeh 64, 1774–1777. Larson, K.D., 1984. Strawberry. In: Schafer, B., Anderson, P.C. (Eds.), Handbook of Environmental Physiology of Fruit Crops, vol. I. Temperate Crops. CRC Press, Boca Raton, Florida. Nicoll, M.F., Galletta, G.G., 1987. Variation in growth and flowering habits of junebearing and everbearing strawberries. J. Amer. Soc. Hort. Sci. 112, 872–880. Sakin, M., Hancock, J.F., Luby, J.J., 1997. Identifying new sources of genes that determine cyclic flowering in Rocky Mountain populations of Fragaria virginiana ssp. glauca Staudt. J. Amer. Soc. Hort. Sci. 122, 205–210. SAS Institute Inc., 1990. SAS Users Guide SAS/STAT, version 6. SAS Inst. Inc., Cary, NC. Serçe, S., Hancock, J.F., 2002. Screening of strawberry germplasm for resistance to the two-spotted spider mite. HortScience 37, 593–594. Serçe, S., Callow, P.W., Ho, J.J., Hancock, J.F., 2002. High temperature effects on CO2 assimilation rate in genotypes of Fragaria x ananassa, F. chiloensis and F. virginiana. J. Amer. Pomol. Soc. 56, 57–62. Smeets, L., 1980. Effect of temperature and day length on flower initiation and runner formation in two everbearing strawberry cultivars. Sci. Hort. 12, 19–26. Sonsteby, A., 1997. Short-day period and temperature interactions on growth and flowering of strawberry. Acta Hort. 439, 609–616. Went, F., 1957. The Experimental Control of Plant Growth, vol. 17. Chronica Botanica, Waltham, MA. Yanagi, T., Oda, Y., 1989. Effects and interactions of pre-chilling history and day-length on successive floral formation in everbearing and non-everbearing strawberry cultivars. J. Jpn. Soc. Hort. Sci. 58, 635–640.