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Prolonged high-temperature exposure differentially reduces growth and flowering of 12 Viola × wittrockiana Gams. cvs
Scientia Horticulturae 108 (2006) 295–302 www.elsevier.com/locate/scihorti
Prolonged high-temperature exposure differentially reduces growth and flowering of 12 Viola wittrockiana Gams. cvs Ryan M. Warner 1, John E. Erwin * Department of Horticultural Science, University of Minnesota, 305 Alderman Hall, 1970 Folwell Ave., Saint Paul, MN 55108, USA Received 9 August 2004; received in revised form 16 December 2005; accepted 31 January 2006
Abstract Many cool season garden crops, including Viola wittrockiana Gams. (pansy), exhibit reduced flowering outdoors during the warm summer months. Twelve pansy cultivars varying in summer garden performance were grown under either 20 1.5 or 30 1 8C (air temperature) to determine growth and flowering responses to prolonged high-temperature exposure and to identify selection criteria to screen pansies for flowering heat tolerance. Increasing temperature from 20 to 30 8C increased leaf number below the first flower on ‘Crystal Bowl Primrose’ and ‘Skyline White’ only. Flower bud number reduction at 30 8C versus 20 8C varied from 20% for ‘Crystal Bowl Purple’ to 77% for ‘Majestic Giants Red and Yellow’. Flower diameter reduction at 30 8C versus 20 8C ranged from 14% for ‘Skyline Beaconsfield’ to 44% for ‘Super Majestic Giants Ocean’. The percentage reduction in total color (flower number estimated flower area) ranged from 60% for ‘Crystal Bowl Primrose’ to 88% for ‘Majestic Giants Rose Shades’. Based on a weighted base selection index, ‘Super Majestic Giants Canary’ and ‘Delta Yellow’ were identified as the most heat-tolerant cultivars, while ‘Super Majestic Giants Ocean’ and ‘Majestic Giants Rose Shades’ were identified as the most heat-sensitive. In a second experiment, root and shoot dry mass were determined after 10, 20, or 30 d when grown at 20 or 30 8C. Relative growth rate and root:shoot ratio were also calculated. After 30 d, ‘Crystal Bowl Primrose’, ‘Crystal Bowl Sky Blue’ and ‘Skyline White’ relative growth rates were lower at 30 8C versus 20 8C. Root:shoot ratio on day 30 was lower at 30 8C compared to 20 8C for six cultivars, but similar across temperature for five cultivars and higher for ‘Crystal Bowl Primrose’. Flower bud number at first flower was positively correlated with branch number, shoot dry mass at flowering, but not correlated with root dry mass at flowering, and negatively correlated with flower diameter and root:shoot ratio (either at flowering, or after 10, 20 or 30 d at 30 8C), suggesting that these traits may be useful when screening pansies for flowering heat tolerance. # 2006 Published by Elsevier B.V. Keywords: Pansy; Flower initiation; Flower size; Flower number; Dry mass; Stress; High-temperature tolerance
1. Introduction High temperatures can inhibit flower induction, initiation, and/or development (Schwabe, 1985; Abdul-Baki, 1991), resulting in reduced overall flowering. An economically significant floriculture crop species that exhibits reduced flowering under warm temperatures is Viola wittrockiana Gams. (pansy; Niu et al., 2000). Pansy ranked third in the United States [behind Pelargonium hortorum Bailey (geranium) and Petunia hybrida Vilm.] in total sales value in 2004 (USDA-NASS, 2005), with a wholesale value of ca. US $151 million. Pansies were traditionally a spring crop only, however, * Corresponding author. Tel.: +1 612 624 0973/9703; fax: +1 612 624 4941. E-mail addresses: [email protected] (R.M. Warner), [email protected] (J.E. Erwin). 1 Present address: Department of Horticulture, Michigan State University, A234 Plant and Soil Sciences, East Lansing, MI 48824, USA. 0304-4238/$ – see front matter # 2006 Published by Elsevier B.V. doi:10.1016/j.scienta.2006.01.034
they are now routinely marketed for outdoor color plantings in the fall and winter in the southern United States. A limiting factor in pansies sales is inhibition of flowering by warm temperatures. Pansies vary considerably in their ability to continue to produce flowering in the garden during warm periods of the year in both northern and southern climates. High temperatures can developmentally delay flowering of many common spring/summer annuals (i.e. increased number of leaves below the first flower). For example, increasing temperature from 20 to 32 8C increased leaf number below the first flower on Antirrhinum majus (snapdragon) L. ‘Rocket Rose’, Calendula officinalis (calendula) L. ‘Calypso Orange’, Impatiens wallerana Hook f. ‘Super Elfin White’ and Torenia fournieri Linden ex. E. Fourn ‘Clown Burgundy’ (Warner and Erwin, 2005). Similarly, high night temperatures (25 8C) increased leaf number below the first flower on Chrysanthemum moriflorum Ramat. (chrysanthemum; de Lint and Heij, 1987; Whealy et al., 1987) and Gomphrena globosa L. (Warner
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et al., 1997). High temperature induced developmental delay of flowering is often referred to as ‘‘heat delay’’. High temperatures can reduce flower number of many species, including Coreopsis grandiflora Hogg ex. Sweet. ‘Sunray’ and Rudbeckia fulgida Ait. ‘Goldsturm’ (Yuan et al., 1998) and Campanula carpatica Jacq. ‘Deep Blue Clips’ (Niu et al., 2001). For example, increasing temperature from 13.7 to 28.9 8C reduced Platycodon grandiflorus (Jacq.) A. DC. ‘Astra Blue’ flower number per plant from 16 to 8 flowers (Park et al., 1998). Final flower size is often affected by growth temperatures. Increasing temperature decreased flower diameter of geranium (Armitage et al., 1981), C. grandiflora ‘Sunray’ and Leucanthemum superbum Bergman ex J. Ingram ‘Snowcap’ (Yuan et al., 1998), but not P. grandiflorus ‘Astra Blue’ (Park et al., 1998). Geranium ‘Sooner Red’ flower diameter increased as temperature increased from 10 to 15 8C, but decreased as temperature further increased from 15 to 32 8C (Armitage et al., 1981). Increasing day/night temperature from 24/18 to 35/ 30 8C differentially decreased flower diameter of 19 I. wallerana cultivars (Lee et al., 1990). Variation in high-temperature tolerance for flowering across cultivars within a species has been identified for several species, including Vigna unguiculata (L.) Walp. flower development (cowpea; Patel and Hall, 1990), I. wallerana flower diameter (Lee et al., 1990) and Lycopersicon esculentum Mill. flower number per inflorescence (tomato; Abdul-Baki, 1991; Warner and Erwin, 2001). This intraspecific variation may aid in elucidating the physiological and genetic mechanisms underlying heat tolerance for flowering. Several methods have been used to evaluate variation in heat tolerance across genotypes, including electrolyte leakage (Binelli and Mascarenhas, 1990), grain yield (Ismail and Hall, 1998) and leaf gas-exchange (Ranney and Peet, 1994). For floriculture crops, plant growth, flower production and flower size may be useful measurements for evaluating heat tolerance under prolonged, sub-lethal growing temperatures (Lee et al., 1990). The objectives of work presented here were to (1) determine the impact of prolonged high-temperature exposure on growth and flowering of 12 pansy cultivars, (2) evaluate different phenotypic selection criteria to screen for heat tolerance in future studies and (3) select cultivars for variation in response to prolonged high-temperature exposure for future research aimed at elucidating the mechanisms of heat tolerance. 2. Materials and methods 2.1. General growth conditions Seeds of 12 Viola wittrockiana cultivars were sown into 25-mL cells containing a soilless medium (Germination Mix, Strong-Lite Horticultural Products, Pine Bluff, Ark.) and placed under intermittent mist (6 s every 10 min, from 07:00 to 18:00 h daily) at 23 2 8C (24-h average S.E.) air temperature. Seedlings were removed from mist and transplanted into 450-mL pots containing a soilless medium (Strong-Lite
Universal Mix) when the cotyledons were parallel to the medium surface. Seedlings were then placed in a greenhouse at constant 20 1.5 8C air temperature under ambient daylight for 5 d (January; Saint Paul, Minn; 458N). After 5 d, 60 mmol m2 s1 supplemental photosynthetically active radiation from high-pressure sodium lamps (LucoLux LU400, General Electric, Cleveland, Ohio) was supplied from 06:00 to 24:00 h daily. Experimental treatments began when two true leaves were fully expanded. Plants in each experiment described below were fertilized at each watering with 14.3 mM N, 0.72 mM P, 6.5 mM K, 1.67 mM Ca, 1.1 mM Mg, plus trace amounts of micronutrients (Miracle-Gro 15N– 2.2P–12.5K Cal–Mg, The Scott’s Co., Marysville, Ohio). 2.2. Impact of temperature on growth and morphological characteristics at flowering (Experiment I) Plants were grown under one of two constant temperatures, 20 1 or 30 1 8C. The experiment was conducted in two greenhouse sections (one per temperature) and employed a complete block statistical design, with five plants per cultivar (12 cultivars) per temperature in each of two blocks within each greenhouse section. Leaf number below the first flower, flower bud number (buds > 1 mm), lateral shoot number (>3 cm), diameter of the first flower and peduncle length on the first flower were determined on five plants per block per cultivar when the first flower opened. The media was then washed from the roots and plants were dried in an oven at 70 8C for 3 d for dry mass measurement. Dry mass gain rate was determined as whole plant dry mass at flowering divided by days to flower. 2.3. Growth analysis (Experiment II) In a separate experiment conducted simultaneously with Experiment I (identical general growth conditions as defined in Section 2.1), 10 plants of each cultivar grown at constant 20 8C air temperature were harvested for dry mass determination when two true leaves had unfolded (day 0). On day 0, 30 plants of each cultivar remained under 20 8C, while another 30 plants were moved into a greenhouse maintained at constant 30 1 8C air temperature, under ambient irradiance plus 60 mmol m2 s1 supplemental irradiance from 06:00 to 24:00 h daily. Plants in each temperature treatment were divided into two blocks (15 plants per cultivar per block). Ten, 20 and 30 d after the initiation of the experiment, five plants per block (2) per temperature treatment (2) of each cultivar were harvested for dry mass measurement. Media was washed from the roots; plants were divided into roots and shoots and placed in a 70 8C drying oven for 3 d. These data were used to calculate root:shoot ratio at each harvest, as well as root and shoot growth rates and overall relative growth rate for each 10 d interval. Relative growth rates were calculated according to the method recommended by Hoffmann and Poorter (2002): rˆ ¼
lnðW2 Þ lnðW1 Þ t2 t1
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where rˆ is the estimate of relative growth rate and lnðWt Þ is the mean of the ln-transformed whole plant dry masses at time t. This method was selected as it provides unbiased estimates of relative growth rates under all conditions, including differences in standard deviation of relative growth rate, sample size, or time between harvests (Hoffmann and Poorter, 2002). 2.4. Relative heat tolerance across cultivars and correlations Relative heat sensitivity of the cultivars was determined using a weighted base selection index based on the percentage reduction of flower number, flower diameter, total color, lateral shoot number, and dry mass gain rate as temperature increased from 20 to 30 8C (adapted from Strope, 1999). Total color is defined as flower number estimated area of the first flower (calculated using flower diameter and assuming that the flower is circular). Percentage reduction in flower number ranged from 20 to 77% across cultivars. Therefore, cultivars were given a score of 1–5 based on the following percentage reductions in flower number: 1 (20–32%), 2 (33–44%), 3 (45–56%), 4 (57– 68%), or 5 (69–80%). Scoring criteria for each variable are presented in Table 1. A weighted base selection index was used where index score = 2 (flower number score) + 2 (flower diameter score) + 2 (total color score) + branch number score + dry mass gain rate score. This index places twice as much emphasis on floral variables as on vegetative variables, as flowering performance under high temperatures is of primary importance. Selection indices were used previously to rank heat tolerance among cultivars (Strope, 1999) and are a useful method because they combine responses of numerous parameters to provide an overall indication of relative heat tolerance. To identify parameters that may be indicators of heat tolerance for flowering, a correlation matrix was developed among selected parameters from Experiments I and II using the Bivariate Correlations function from the statistical analysis software package SPSS (SPSS Inc., Chicago, IL). Growth parameters from the day 10 harvest were chosen for inclusion in the correlation analysis to determine if heat tolerance for flowering could be predicted by analyzing growth response of seedlings to high-temperature exposures. Table 1 Scoring criteria for selection index scores Variable
Flower number Flower diameter Total color Branch number Dry mass gain rate
Reduction (%) Score 1
Score 2
Score 3
Score 4
Score 5
20–32 13–17 60–65 25–31 (10)–2
33–44 18–22 66–71 32–37 3–15
45–56 23–27 72–77 38–43 16–28
57–68 28–32 78–83 44–49 29–41
69–80 33–37 84–89 50–56 42–54
Scores were based on the range of percentage reduction (Reduction) in flower number, flower diameter, total color (flower number estimated flower area), the number of lateral shoots (branch number) and dry mass gain rate exhibited by 12 Viola wittrockiana Gams. cultivars as temperature increased from 20 to 30 8C
297
3. Results 3.1. Experiment I Increasing temperature from 20 to 30 8C increased ‘Crystal Bowl Primrose’ and ‘Skyline White’ leaf number below the first flower from 6 to 7, and from 8 to 9 leaves, respectively. ‘Crystal Bowl Sky Blue’, ‘Delta Yellow’, ‘Majestic Giants Supreme Yellow’, and ‘Super Majestic Giants Canary’ flowered with seven leaves below the first flower, regardless of temperature. ‘Crystal Bowl Purple’, ‘Majestic Giants Red and Yellow’, ‘Majestic Giants Rose Shades’, ‘Skyline Beaconsfield’, ‘Super Majestic Giants Ocean’ and ‘Super Majestic Giants Snow’ flowered with eight leaves below the first flower, regardless of temperature. Temperature and cultivar interacted to affect flower bud number when the first flower opened (Table 2). Increasing temperature reduced flower bud number of all cultivars (Table 2), but the percent reduction in flower bud number varied from 20% for ‘Crystal Bowl Purple’ to 77% for ‘Majestic Giants Red and Yellow’ (Table 3). ‘Majestic Giants Red and Yellow’, ‘Majestic Giants Rose Shades’, ‘Majestic Giants Supreme Purple’, ‘Skyline Beaconsfield’, ‘Super Majestic Giants Ocean’ and ‘Super Majestic Giants Snow’ flower bud numbers were all reduced by at least 58%. Temperature and cultivar interacted to impact flower diameter and days to flower (Table 2). Increasing temperature from 20 to 30 8C reduced flower diameter of all cultivars, but the degree of reduction varied from 14% for ‘Skyline Beaconsfield’ (from 52 to 45 mm, respectively) to 44% for ‘Super Majestic Giants Ocean’ (from 81 to 45 mm, respectively; Tables 2 and 3). The percentage reduction in total color (flower number estimated flower area) ranged from 60% for ‘Crystal Bowl Primrose’ to 88% for ‘Majestic Giants Rose Shades’ (Table 3). Increasing temperature reduced days to flower for all cultivars, but the acceleration of flowering varied from 3 d for ‘Skyline White’ to 15 d for ‘Super Majestic Giants Ocean’ (Table 2). Temperature and cultivar independently affected peduncle length (Table 2). Increasing temperature from 20 to 30 8C increased peduncle length of ‘Crystal Bowl Purple’ and ‘Delta Yellow’ only (Table 2). For instance, increasing temperature from 20 to 30 8C increased ‘Delta Yellow’ peduncle length from 60 to 79 mm, respectively. Temperature and cultivar interacted to impact lateral shoot number (Table 2). Increasing temperature decreased lateral shoot number of all cultivars except ‘Delta Yellow’ (Table 2). The degree of reduction in lateral shoot number as temperature increased from 20 to 30 8C varied from 25% (‘Super Majestic Giants Canary’ from 8 to 6 lateral shoots, respectively) to 56% (‘Majestic Giants Supreme Purple’ from 9 to 4, and ‘Crystal Bowl Sky Blue’ from 16 to 7 lateral shoots, respectively; Tables 2 and 3). High temperature reduced dry mass gain rate of all but two cultivars, ‘Crystal Bowl Purple’ and ‘Skyline White’ (Table 2). ‘Super Majestic Giants Ocean’ dry mass gain rate decreased 54% (from 101 to 46 mg d1, respectively) as temperature
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Table 2 Impact of temperature (Temp) on flower bud number (>1 mm in length) at first flower (flower number), peduncle length of the first flower, number of lateral shoots (>3 cm in length; branch number), diameter of the first open flower, days to flower and dry mass gain rate of 12 Viola wittrockiana Gams. cultivars Cultivar
Temp. (8C)
Flower number
Peduncle length (mm)
Branch number
Flower diameter (mm)
Days to flower
Dry mass gain rate (mg d1)
Crystal Bowl Primrosea
20 30 20 30 20 30 20 30 20 30 20 30 20 30 20 30 20 30 20 30 20 30 20 30
20b 14a 20b 16a 25b 14a 19b 11a 22b 5a 22b 6a 19b 8a 28b 13a 18b 12a 16b 9a 22b 9a 17b 7a ***c *** ***
65a 71a 61a 78b 54a 77a 60a 79b 61a 55a 87a 86a 63a 66a 82a 85a 74a 85a 65a 70a 78a 83a 72a 66a *** * ns
12b 6a 15b 7a 16b 7a 9a 6a 9b 6a 10b 6a 9b 4a 14b 7a 11b 8a 8b 6a 9b 5a 9b 5a
62b 47a 57b 37a 57b 36a 61b 49a 69b 59a 81b 54a 62b 50a 52b 45a 64b 44a 73b 59a 81b 45a 74b 50a
53b 47a 51b 42a 48b 41a 53b 47a 63b 51a 60b 50a 49b 42a 50b 46a 50b 47a 53b 49a 60b 45a 53b 48a
81b 49a 69a 76a 96b 70a 67b 49a 82b 46a 93b 53a 67b 41a 85b 58a 59a 60a 95b 69a 101b 46a 80b 53a
Crystal Bowl Purplea Crystal Bowl Sky Bluea Delta Yellowb Majestic Giants Red and Yellowa Majestic Giants Rose Shadesa Majestic Giants Supreme Purplea Skyline Beaconsfieldb Skyline Whiteb Super Majestic Giants Canarya Super Majestic Giants Ocean a Super Majestic Giants Snowa Cultivar Temperature Cultivar Temperature
*** *** ***
*** *** ***
*** *** ***
*** *** ***
Lowercase letters represent differences in means across temperature within a cultivar, as determined by one-way analysis of variance (P 0.05). a Seed source: Sakata Seeds America, Inc. b Seed source: Syngenta Seeds, Inc. c ns, *, *** denote non-significance or significance at P 0.05 or P 0.001, respectively.
Table 3 Percentage reduction (%Red.; mean at 30 8C compared to mean at 20 8C) in flower bud number (buds > 1 mm) at first flower (flower number), diameter of the first flower, total color (flower number estimated flower area), number of lateral shoots (>3 cm; branch number) and dry mass gain rate at flowering, score of each parameter (from Table 1), total heat sensitivity index score (where index score = 2 (flower number score) + 2 (flower diameter score) + 2 (total color score) + branch number score + dry mass gain rate score) and ranking of 12 Viola wittrockiana Gams. cultivars Cultivar
Super Majestic Giants Canary Delta Yellow Skyline White Crystal Bowl Primrose Skyline Beaconsfield Crystal Bowl Purple Majestic Giants Red and Yellow Majestic Giants Supreme Purple Crystal Bowl Sky Blue Super Majestic Giants Snow Super Majestic Giants Ocean Majestic Giants Rose Shades
Flower number
Flower diameter
Total color
Branch number
Dry mass gain rate
Index
%Red.
Score
%Red.
Score
%Red.
Score
%Red.
Score
%Red.
Score
Score
44
2
19
2
63
1
25
1
28
3
14
1
42 33 30 54 20 77
2 2 1 3 1 5
20 31 24 13 35 16
2 4 3 1 5 1
63 68 60 65 66 83
1 2 1 1 2 4
33 27 50 50 53 33
2 1 5 5 5 2
27 0 40 32 10 44
3 1 4 4 1 5
15 18 19 19 22 27
2 3 4 4 6 7
58
4
19
2
73
3
56
5
39
4
27
7
44 59 59 73
2 4 4 5
37 32 32 33
5 4 4 5
78 81 87 88
4 5 5 5
56 44 44 40
5 4 4 3
27 34 54 45
3 4 5 5
30 34 35 38
9 10 11 12
A lower rank score and index score indicates higher heat tolerance.
Rank
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Table 4 Impact of temperature (Temp) on relative growth rate of 12 Viola wittrockiana Gams. cultivars from day 0–10, 10–20 or 20–30 after initiation of temperature treatments Cultivar
Crystal Bowl Primrose Crystal Bowl Purple Crystal Bowl Sky Blue Delta Yellow Majestic Giants Red and Yellow Majestic Giants Rose Shades Majestic Giants Supreme Purple Skyline Beaconsfield Skyline White Super Majestic Giants Canary Super Majestic Giants Ocean Super Majestic Giants Snow Cultivar Temperature Harvest Cultivar temperature Cultivar harvest Temperature harvest Cultivar temperature harvest
Temp. (8C)
20 30 20 30 20 30 20 30 20 30 20 30 20 30 20 30 20 30 20 30 20 30 20 30 ** a ** *** ns *** * ns
Relative growth rate (mg g1 d1) 0–10 growth interval days
10–20 growth interval days
20–30 growth interval days
144Ab 165Ab 171Ab 175Ab 218Ab 224Ac 188Ab 189Ab 169Ab 173Ab 165Ac 168Ab 144Ab 145Ab 153Ac 123Ab 134Aab 147Ab 161Ab 157Ab 165Ab 184Ab 204Ab 176Ab
146Bb 105Aa 135Aa 143Aab 110Aa 108Ab 137Bab 107Aa 101Aa 105Aa 134Ab 105Aa 132Ab 107Aa 122Ab 126Ab 147Ab 130Ab 110Aab 84Aa 124Aa 83Aa 85Aa 67Aa
96Ba 71Aa 102Aa 73Aa 101Ba 43Aa 81Aa 88Aa 85Aa 84Aa 85Aa 104Aa 90Aa 70Aa 87Aa 70Aa 76Ba 42Aa 83Aa 85Aa 116Aa 123Aa 115Aa 118Aab
Capital letters represent mean differences across temperature, within a cultivar and harvest date, determined by one-way analysis of variance (P 0.05). Lowercase letters represent multiple comparison tests (Tukey’s HSD(0.05)) across harvest date, within a cultivar and temperature. a ns, *, **, *** denote non-significance or significance at P 0.05, 0.01, and 0.001, respectively, determined by one-way analysis of variance.
increased from 20 to 30 8C, the greatest reduction of all cultivars evaluated (Tables 2 and 3). The range in percentage reduction in growth and flowering parameters across cultivars as temperature increased from 20 to 30 8C was used to develop scoring criteria for heat sensitivity index scores (Table 1).
of the 12 cultivars, similar across temperature treatments for 5 of the 12 cultivars, and greater at 30 8C than 20 8C for ‘Crystal Bowl Primrose’ (Table 5).
3.2. Experiment II
Pansy cultivars examined in this experiment varied in response to high temperature based on differences in flower number, flower size, and dry mass gain rate. Therefore, available commercial germplasm could be useful in studying the mechanisms of heat tolerance in pansy. Increasing temperature from 20 to 30 8C decreased flower number and diameter of all pansy cultivars here (Table 2). This reduction in flower number and size is consistent with previous results for other species (Armitage et al., 1981; Yuan et al., 1998). For example, increasing temperature from 15 to 32 8C decreased geranium ‘Sooner Red’ flower number per inflorescence from 49 to 21 flowers under an irradiance level of 350 mmol m2 s1 (18 h photoperiod; 22.7 mol m2 d1 daily light integral; Armitage et al., 1981). The reduction in flower diameter observed here is consistent with previous results for
Relative growth rate declined over time (Table 4). For most cultivars, temperature did not impact relative growth rate on any harvest date. However, increasing temperature from 20 to 30 8C decreased relative growth rate of ‘Crystal Bowl Primrose’, ‘Crystal Bowl Sky Blue’ and ‘Skyline White’ at one growth interval only (20–30 d after initiation of temperature treatments; Table 4). Root:shoot ratio of all cultivars at both temperatures declined over time (day 30 compared to day 10), with the exceptions of ‘Crystal Bowl Primrose’, ‘Majestic Giants Rose Shades’ and ‘Majestic Giants Red and Yellow’ at 20 8C and ‘Skyline White’ at 30 8C (Table 5). Root:shoot ratio after 30 d in temperature treatments was greater at 20 8C than 30 8C for 6
4. Discussion
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Table 5 Impact of temperature on 12 Viola wittrockiana Gams. cultivars root:shoot ratio 0, 10, 20, and 30 d after initiation of temperature treatments Cultivar
Crystal Bowl Primrose Crystal Bowl Purple Crystal Bowl Sky Blue Delta Yellow Majestic Giants Red and Yellow Majestic Giants Rose Shades Majestic Giants Supreme Purple Skyline Beaconsfield Skyline White Super Majestic Giants Canary Super Majestic Giants Ocean Super Majestic Giants Snow Cultivar Temperature Harvest Cultivar temperature Cultivar harvest Temperature harvest Cultivar temperature harvest
Temp. (8C)
20 30 20 30 20 30 20 30 20 30 20 30 20 30 20 30 20 30 20 30 20 30 20 30 ***a *** *** ns *** * ns
Root:shoot ratio 0
10
20
30
0.379a
0.254Aa 0.220Ab 0.250Aab 0.212Ab 0.229Bb 0.170Ab 0.256Bb 0.151Ab 0.293Bab 0.215Ab 0.273Aab 0.242Ab 0.328Ab 0.235Ab 0.260Ab 0.255Ab 0.351Bbc 0.239Aa 0.284Bb 0.204Ab 0.419Bb 0.311Ac 0.409Ac 0.394Ab
0.345Ba 0.191Ab 0.222Bab 0.124Aa 0.228Bb 0.140Aab 0.241Bb 0.163Ab 0.430Bb 0.250Ab 0.331Bb 0.241Ab 0.267Bb 0.190Aab 0.195Aab 0.183Aa 0.399Bc 0.240Aa 0.287Bb 0.157Aab 0.275Aab 0.227Ab 0.399Bbc 0.266Aab
0.156Aa 0.167Ba 0.145Ba 0.088Aa 0.144Ba 0.113Aa 0.148Aa 0.108Aa 0.193Ba 0.122Aa 0.183Aa 0.129Aa 0.130Aa 0.125Aa 0.147Aa 0.149Aa 0.181Aa 0.168Aa 0.186Ba 0.106Aa 0.176Ba 0.133Aa 0.255Ba 0.166Aa
0.325b 0.255b 0.205ab 0.379ab 0.361b 0.331b 0.271b 0.275b 0.174a 0.418b 0.289ab
Capital letters represent mean differences across temperature, within a cultivar and harvest date, determined by one-way analysis of variance (P 0.05). Lowercase letters represent multiple comparison tests (Tukey’s HSD(0.05)) across harvest date, within a cultivar and temperature. 0, 10, 20, 30 denote harvest date (day number). a ns, *, **, *** denote non-significance or significance at P 0.05, 0.01, and 0.001, respectively, determined by one-way analysis of variance.
pansy; ‘Universal Violet’ flower area decreased linearly as temperature increased from 9 to 31 8C (Pearson et al., 1995). The combined effects of reduced flower number and reduced flower diameter led to reductions in total color (flower number estimated flower area) of 60 (for ‘Crystal Bowl Primrose’) to 88% (for ‘Majestic Giants Rose Shades’; Table 3). Herbaceous ornamentals are purchased primarily to provide color in the landscape. This has resulted in breeders selecting plants that produce high total color, either by producing many smaller flowers or fewer but larger flowers. High temperature had little impact on leaf number below the first flower. Only ‘Crystal Bowl Primrose’ and ‘Skyline White’ leaf number below the first flower increased as temperature increased from 20 to 30 8C, and for both cultivars only one additional leaf was produced below the first flower. In contrast, calendula ‘Calypso Orange’ leaf number below the first flower increased from 16 to 42 leaves as temperature increased from 20 to 32 8C at a daily light integral (the cumulative amount of photosynthetically active radiation over a 24-h period) of 10.5 mol m2 d1 (Warner and Erwin, 2005). The impact of temperature on leaf number below the first flower has not been previously reported for pansy. Pansy
‘Universal Violet’ leaf unfolding rate increased linearly as temperature increased from 9.6 to 28.8 8C (Adams et al., 1997a), but plants were either harvested prior to flowering or flowering data were not reported. Also, pansy ‘Universal Violet’ days to flower decreased as temperature increased from 14.8 to 21.7 8C, but increased as temperature further increased from 21.7 to 26.1 8C (Adams et al., 1997b). However, leaf number below the first flower was not reported. In contrast to this result, days to flower for all cultivars reported here decreased as temperature increased from 20 to 30 8C (Table 2). Plant dry mass gain rate (determined at flowering) decreased for all pansy cultivars except ‘Skyline White’ and ‘Crystal Bowl Purple’ (Table 2). This is consistent with previous results for other species. For example, P. grandiflorus ‘Astra Blue’ dry mass at flowering decreased from 5.1 to 1.1 g as temperature increased from 13.7 to 28.9 8C (Park et al., 1998). Similarly, increasing temperature from 20 to 32 8C reduced dry mass gain rate of snapdragon ‘Rocket Rose’, calendula ‘Calypso Orange’ and Mimulus hybridus Hort. ex Sieb. and Voss ‘Mystic Yellow’, but increased dry mass gain rate of torenia ‘Clown Burgundy’ (Warner and Erwin, 2005).
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Table 6 Pearson correlation coefficient matrix of variables flower bud number (Bud), leaf number below the first flower (LN), lateral shoot number (LSN), diameter of the first flower (FD), shoot dry mass at flowering (SDM), root dry mass at flowering (RDM), root:shoot ratio at flowering [R:S(F)], and root:shoot ratio [R:S(10)], shoot dry mass gain rate [SR(10)], root dry mass gain rate [RR(10)] and total dry mass gain rate [TR(10)] after 10 d in temperature Variable
Bud
LN
LSN
FD
SDM
RDM
R:S(F)
R:S(10)
SR(10)
RR(10)
TR(10)
Bud LN LSN FD SDM RDM R:S(F) R:S(10) SR(10) RR(10) TR(10)
– 0.40 0.59 S0.29 0.35 0.00 S0.27 0.24 0.06 S0.27 0.12
0.37 – 0.20 0.07 0.11 0.04 0.02 0.08 0.06 0.04 0.08
0.49 0.31 – S0.53 0.00 0.17 0.20 0.25 0.13 S0.27 0.17
S0.39 0.10 0.09 – 0.56 0.53 0.22 0.40 0.10 0.32 0.17
0.49 0.09 0.56 0.02 – 0.57 0.11 0.07 0.10 0.09 0.11
0.12 0.24 0.32 0.09 0.50 – 0.73 0.31 0.12 0.29 0.18
S0.31 0.16 0.17 0.03 S0.34 0.62 – 0.33 0.10 0.31 0.16
S0.40 0.31 0.23 0.13 0.11 0.23 0.41 – 0.03 0.57 0.15
0.03 0.18 0.31 0.03 0.14 0.01 0.17 S0.26 – 0.77 0.98
S0.30 0.15 S0.25 0.19 0.07 0.21 0.17 S0.56 0.62 – 0.88
0.49 0.11 0.18 0.07 0.14 0.05 0.11 0.08 0.98 0.75
The upper right half of the matrix represents Pearson correlation coefficients for plants growing at 30 8C and the lower left half plants growing at 20 8C. Correlations significant at P 0.05 are shown in bold.
Root:shoot ratio decreased as temperature increased for half of the cultivars here, which is consistent with previous reports on temperature effects on root:shoot (Table 5). For example, Capsicum annuum L. ‘Resistant Giant no. 4’ root:shoot ratio decreased from 0.21 to 0.14 as temperature increased from 14 to 26 8C (Si and Heins, 1996). Similarly, high temperatures reduce root:shoot ratio of Caenothus greggii (Trel.) Jeps. (Larigauderie et al., 1991), Asimina triloba (L.) Dunal (pawpaw; Pomper et al., 2002), Trifolium repens L. (white clover; Murray et al., 2000) and Pascopyrum smithii Rydb. (Read and Morgan, 1996). Flower bud number at 30 8C was positively correlated with branch number and shoot dry mass (but not root dry mass) at flowering but negatively correlated with root:shoot ratio (Table 6). Even a 10 d exposure to 30 8C resulted in a negative correlation between flower bud number and root:shoot ratio. Therefore, when breeding for heat tolerance in pansy, selecting plants that produce high lateral shoot number and high shoot mass while growing at 30 8C may aid in accelerating selection for heat tolerance for flowering. Flower diameter was also negatively correlated with flower bud number as temperature increased from 20 and 30 8C (Table 6). Therefore, plants producing more flower buds did so at the expense of flower size, suggesting flower size may be an indicator of heat tolerance for flowering. The three cultivars that produced the largest flowers at 20 8C, ‘Super Majestic Giants Ocean’, ‘Majestic Giants Rose Shades’ and ‘Super Majestic Giants Snow’ (Table 2) were also the three lowest ranking cultivars for overall heat tolerance (Table 3). In general, cultivars from the ‘Majestic Giants’ and ‘Super Majestic Giants’ series performed poorly when grown at 30 8C, ranking in the bottom half of all cultivars evaluated with respect to selection index score (Table 3). The stark exception to this was ‘Super Majestic Giants Canary’, which ranked first among all cultivars in selection index score. ‘Super Majestic Giants Canary’ and ‘Delta Yellow’ ranked in the top five for all attributes. No cultivar ranked first in all four categories used in the selection index. ‘Crystal Bowl Purple’ was the top ranking cultivar with respect to lowest percentage reduction in flower
number (20%) and dry mass gain rate (10%), but ranked eleventh out of 12 with respect to reduction in flower diameter. ‘Skyline Beaconsfield’ flower diameter was least affected by temperature (13% reduction), and ‘Super Majestic Giants Canary’ lateral shoot number was least affected by temperature (25% reduction; Table 3). The most heat-sensitive cultivars, as determined by the weighted base selection index, were ‘Majestic Giants Rose Shades’, ‘Super Majestic Giants Ocean’ and ‘Super Majestic Giants Snow’ (Table 3). Based on our results, selecting heat-tolerant pansies for flowering may be best achieved by selecting plants with smaller flowers and high lateral shoot number, high shoot dry mass and low root:shoot ratio when grown at 30 8C. Acknowledgements The authors thank Sakata Seeds America, Inc. and Syngenta Seeds, Inc. for donating seeds. We would also like to thank the Floriculture Industry Research and Scholarship Trust (FIRST), the Fred C. Gloeckner Foundation, the Minnesota Nursery and Landscape Association, the Richard E. Widmer Teaching and Research Fund, the Minnesota Extension Service and the Minnesota Agricultural Experiment Station for financial support. References Abdul-Baki, A.A., 1991. Tolerance of tomato cultivars and selected germplasm to heat stress. J. Am. Soc. Hort. Sci. 116, 1113–1116. Adams, S.R., Pearson, S., Hadley, P., 1997a. An analysis of the effects of temperature and light integral on the vegetative growth of pansy cv. Universal Violet (Viola wittrockiana Gams.) Ann. Bot. 79, 219–225. Adams, S.R., Pearson, S., Hadley, P., 1997b. The effects of temperature, photoperiod and light integral on the time to flowering of pansy cv. Universal Violet (Viola wittrockiana Gams.) Ann. Bot. 80, 107–112. Armitage, A.M., Carlson, W.H., Flore, J.A., 1981. The effect of temperature and quantum flux density on the morphology, physiology, and flowering of hybrid geraniums. J. Am. Soc. Hort. Sci. 106, 643–647. Binelli, G., Mascarenhas, J.P., 1990. Arabidopsis: sensitivity of growth to high temperature. Dev. Genet. 11, 294–298. de Lint, P.J.A.L., Heij, G., 1987. Effects of day and night temperature on growth and flowering of chrysanthumum. Acta Hort. 197, 53–61.
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Hoffmann, W.A., Poorter, H., 2002. Avoiding bias in calculations of relative growth rate. Ann. Bot. 90, 37–42. Ismail, A.M., Hall, A.E., 1998. Positive and potential negative effects of heattolerance genes in cowpea. Crop Sci. 38, 381–390. Larigauderie, A., Ellis, B.A., Mills, J.N., Kummerow, J., 1991. The effect of root and shoot temperatures on growth of Caenothus greggii seedlings. Ann. Bot. 67, 97–101. Lee, W.-S., Barrett, J.E., Nell, T.A., 1990. High temperature effects on the growth and flowering of Impatiens wallerana cultivars. Acta Hort. 272, 121–127. Murray, P.J., Jorgensen, M., Gill, E., 2000. Effect of temperature on growth and morphology of two varieties of white clover (Trifolium repens L.) and their impact on soil microbial activity. Ann. Appl. Biol. 137, 305–309. Niu, G., Heins, R.D., Cameron, A.C., Carlson, W.H., 2000. Day and night temperatures, daily light integral, and CO2 enrichment affect growth and flower development of pansy (Viola wittrockiana). J. Am. Soc. Hort. Sci. 125, 436–441. Niu, G., Heins, R.D., Cameron, A.C., Carlson, W.H., 2001. Temperature and daily light integral influence plant quality and flower development of Campanula carpatica ‘Blue Clips’, ‘Deep Blue Clips’, and Campanula ‘Birch Hybrid’. HortScience 36, 664–668. Park, B.H., Oliveira, N., Pearson, S., 1998. Temperature affects growth and flowering of the ballon flower [Platycodon grandiflorus (Jacq.) A. DC. cv. Astra Blue] HortScience 33, 233–236. Patel, P.N., Hall, A.E., 1990. Genotypic variation and classification of cowpea for reproductive responses to high temperature under long photoperiods. Crop Sci. 30, 614–621. Pearson, S., Parker, A., Adams, S.R., Hadley, P., May, D.R., 1995. The effects of temperature on the flower size of pansy (Viola wittrockiana Gams.) J. Hort. Sci. 70, 183–190. Pomper, K.W., Layne, D.R., Jones, S.C., Kwantes, M.G., 2002. Growth enhancement of container-grown pawpaw seedlings as influenced by media type, root-zone temperature, and fertilization regime. HortScience 37, 329–333.
Ranney, T.G., Peet, M.M., 1994. Heat tolerance of five taxa of birch (Betula): physiological responses to supraoptimal leaf temperatures. J. Am. Soc. Hort. Sci. 119, 243–248. Read, J.J., Morgan, J.A., 1996. Growth and partitioning in Pascopyrum smithii (C3) and Bouteloua gracilis (C4) as influenced by carbon dioxide and temperature. Ann. Bot. 77, 487–496. Schwabe, W.W., 1985. Kalanchoe blossfeldiana. In: Halevy, A.H. (Ed.), Handbook of Flowering, vol. III. CRC Press, Boca Raton, FL, pp. 217– 235. Si, Y., Heins, R.D., 1996. Influence of day and night temperatures on sweet pepper seedling development. J. Am. Soc. Hort. Sci. 121, 699–704. Strope, K.M., 1999. The effects of heat stress on flowering and vegetative growth of New Guinea impatiens (Imatiens hawkeri Bull.). MS Thesis, Univ. Minnesota, Saint Paul. USDA-NASS, 2005. Unites States Department of Agriculture National Agricultural Statistics Service—Floriculture crops 2004. Report number Sp Cr6-1 (05). http://usda.mannlib.cornell.edu/reports/nassr/other/zfc-bb/ floran05.pdf. Warner, R., Erwin, J.E., Wagner, R., 1997. Photoperiod and temperature interact to affect Gomphrena globosa L. and Salvia farinacea Benth. development. HortScience 32, 501 (abst.). Warner, R.M., Erwin, J.E., 2001. Effect of high-temperature stress on flower number per inflorescence of 11 Lycopersicon esculentum Mill. genotypes. HortScience 36, 508 (abst.). Warner, R.M., Erwin, J.E., 2005. Prolonged high temperature exposure and daily light integral impact growth and flowering of five herbaceous ornamental species. J. Am. Soc. Hort. Sci. 130, 319–325. Whealy, C.A., Nell, T.A., Barrett, J.E., Larson, R.A., 1987. High temperature effects on growth and floral development in chrysanthemum. J. Am. Soc. Hort. Sci. 112, 464–468. Yuan, M., Carlson, W.H., Heins, R.D., Cameron, A.C., 1998. Effect of forcing temperature on time to flower of Coreopsis grandiflora, Gaillardia Leucanthemum, Leucanthemum superbum, and Rudbeckia fulgida. HortScience 33, 663–667.
Prolonged high-temperature exposure differentially reduces growth and flowering of 12 Viola wittrockiana Gams. cvs Ryan M. Warner 1, John E. Erwin * Department of Horticultural Science, University of Minnesota, 305 Alderman Hall, 1970 Folwell Ave., Saint Paul, MN 55108, USA Received 9 August 2004; received in revised form 16 December 2005; accepted 31 January 2006
Abstract Many cool season garden crops, including Viola wittrockiana Gams. (pansy), exhibit reduced flowering outdoors during the warm summer months. Twelve pansy cultivars varying in summer garden performance were grown under either 20 1.5 or 30 1 8C (air temperature) to determine growth and flowering responses to prolonged high-temperature exposure and to identify selection criteria to screen pansies for flowering heat tolerance. Increasing temperature from 20 to 30 8C increased leaf number below the first flower on ‘Crystal Bowl Primrose’ and ‘Skyline White’ only. Flower bud number reduction at 30 8C versus 20 8C varied from 20% for ‘Crystal Bowl Purple’ to 77% for ‘Majestic Giants Red and Yellow’. Flower diameter reduction at 30 8C versus 20 8C ranged from 14% for ‘Skyline Beaconsfield’ to 44% for ‘Super Majestic Giants Ocean’. The percentage reduction in total color (flower number estimated flower area) ranged from 60% for ‘Crystal Bowl Primrose’ to 88% for ‘Majestic Giants Rose Shades’. Based on a weighted base selection index, ‘Super Majestic Giants Canary’ and ‘Delta Yellow’ were identified as the most heat-tolerant cultivars, while ‘Super Majestic Giants Ocean’ and ‘Majestic Giants Rose Shades’ were identified as the most heat-sensitive. In a second experiment, root and shoot dry mass were determined after 10, 20, or 30 d when grown at 20 or 30 8C. Relative growth rate and root:shoot ratio were also calculated. After 30 d, ‘Crystal Bowl Primrose’, ‘Crystal Bowl Sky Blue’ and ‘Skyline White’ relative growth rates were lower at 30 8C versus 20 8C. Root:shoot ratio on day 30 was lower at 30 8C compared to 20 8C for six cultivars, but similar across temperature for five cultivars and higher for ‘Crystal Bowl Primrose’. Flower bud number at first flower was positively correlated with branch number, shoot dry mass at flowering, but not correlated with root dry mass at flowering, and negatively correlated with flower diameter and root:shoot ratio (either at flowering, or after 10, 20 or 30 d at 30 8C), suggesting that these traits may be useful when screening pansies for flowering heat tolerance. # 2006 Published by Elsevier B.V. Keywords: Pansy; Flower initiation; Flower size; Flower number; Dry mass; Stress; High-temperature tolerance
1. Introduction High temperatures can inhibit flower induction, initiation, and/or development (Schwabe, 1985; Abdul-Baki, 1991), resulting in reduced overall flowering. An economically significant floriculture crop species that exhibits reduced flowering under warm temperatures is Viola wittrockiana Gams. (pansy; Niu et al., 2000). Pansy ranked third in the United States [behind Pelargonium hortorum Bailey (geranium) and Petunia hybrida Vilm.] in total sales value in 2004 (USDA-NASS, 2005), with a wholesale value of ca. US $151 million. Pansies were traditionally a spring crop only, however, * Corresponding author. Tel.: +1 612 624 0973/9703; fax: +1 612 624 4941. E-mail addresses: [email protected] (R.M. Warner), [email protected] (J.E. Erwin). 1 Present address: Department of Horticulture, Michigan State University, A234 Plant and Soil Sciences, East Lansing, MI 48824, USA. 0304-4238/$ – see front matter # 2006 Published by Elsevier B.V. doi:10.1016/j.scienta.2006.01.034
they are now routinely marketed for outdoor color plantings in the fall and winter in the southern United States. A limiting factor in pansies sales is inhibition of flowering by warm temperatures. Pansies vary considerably in their ability to continue to produce flowering in the garden during warm periods of the year in both northern and southern climates. High temperatures can developmentally delay flowering of many common spring/summer annuals (i.e. increased number of leaves below the first flower). For example, increasing temperature from 20 to 32 8C increased leaf number below the first flower on Antirrhinum majus (snapdragon) L. ‘Rocket Rose’, Calendula officinalis (calendula) L. ‘Calypso Orange’, Impatiens wallerana Hook f. ‘Super Elfin White’ and Torenia fournieri Linden ex. E. Fourn ‘Clown Burgundy’ (Warner and Erwin, 2005). Similarly, high night temperatures (25 8C) increased leaf number below the first flower on Chrysanthemum moriflorum Ramat. (chrysanthemum; de Lint and Heij, 1987; Whealy et al., 1987) and Gomphrena globosa L. (Warner
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et al., 1997). High temperature induced developmental delay of flowering is often referred to as ‘‘heat delay’’. High temperatures can reduce flower number of many species, including Coreopsis grandiflora Hogg ex. Sweet. ‘Sunray’ and Rudbeckia fulgida Ait. ‘Goldsturm’ (Yuan et al., 1998) and Campanula carpatica Jacq. ‘Deep Blue Clips’ (Niu et al., 2001). For example, increasing temperature from 13.7 to 28.9 8C reduced Platycodon grandiflorus (Jacq.) A. DC. ‘Astra Blue’ flower number per plant from 16 to 8 flowers (Park et al., 1998). Final flower size is often affected by growth temperatures. Increasing temperature decreased flower diameter of geranium (Armitage et al., 1981), C. grandiflora ‘Sunray’ and Leucanthemum superbum Bergman ex J. Ingram ‘Snowcap’ (Yuan et al., 1998), but not P. grandiflorus ‘Astra Blue’ (Park et al., 1998). Geranium ‘Sooner Red’ flower diameter increased as temperature increased from 10 to 15 8C, but decreased as temperature further increased from 15 to 32 8C (Armitage et al., 1981). Increasing day/night temperature from 24/18 to 35/ 30 8C differentially decreased flower diameter of 19 I. wallerana cultivars (Lee et al., 1990). Variation in high-temperature tolerance for flowering across cultivars within a species has been identified for several species, including Vigna unguiculata (L.) Walp. flower development (cowpea; Patel and Hall, 1990), I. wallerana flower diameter (Lee et al., 1990) and Lycopersicon esculentum Mill. flower number per inflorescence (tomato; Abdul-Baki, 1991; Warner and Erwin, 2001). This intraspecific variation may aid in elucidating the physiological and genetic mechanisms underlying heat tolerance for flowering. Several methods have been used to evaluate variation in heat tolerance across genotypes, including electrolyte leakage (Binelli and Mascarenhas, 1990), grain yield (Ismail and Hall, 1998) and leaf gas-exchange (Ranney and Peet, 1994). For floriculture crops, plant growth, flower production and flower size may be useful measurements for evaluating heat tolerance under prolonged, sub-lethal growing temperatures (Lee et al., 1990). The objectives of work presented here were to (1) determine the impact of prolonged high-temperature exposure on growth and flowering of 12 pansy cultivars, (2) evaluate different phenotypic selection criteria to screen for heat tolerance in future studies and (3) select cultivars for variation in response to prolonged high-temperature exposure for future research aimed at elucidating the mechanisms of heat tolerance. 2. Materials and methods 2.1. General growth conditions Seeds of 12 Viola wittrockiana cultivars were sown into 25-mL cells containing a soilless medium (Germination Mix, Strong-Lite Horticultural Products, Pine Bluff, Ark.) and placed under intermittent mist (6 s every 10 min, from 07:00 to 18:00 h daily) at 23 2 8C (24-h average S.E.) air temperature. Seedlings were removed from mist and transplanted into 450-mL pots containing a soilless medium (Strong-Lite
Universal Mix) when the cotyledons were parallel to the medium surface. Seedlings were then placed in a greenhouse at constant 20 1.5 8C air temperature under ambient daylight for 5 d (January; Saint Paul, Minn; 458N). After 5 d, 60 mmol m2 s1 supplemental photosynthetically active radiation from high-pressure sodium lamps (LucoLux LU400, General Electric, Cleveland, Ohio) was supplied from 06:00 to 24:00 h daily. Experimental treatments began when two true leaves were fully expanded. Plants in each experiment described below were fertilized at each watering with 14.3 mM N, 0.72 mM P, 6.5 mM K, 1.67 mM Ca, 1.1 mM Mg, plus trace amounts of micronutrients (Miracle-Gro 15N– 2.2P–12.5K Cal–Mg, The Scott’s Co., Marysville, Ohio). 2.2. Impact of temperature on growth and morphological characteristics at flowering (Experiment I) Plants were grown under one of two constant temperatures, 20 1 or 30 1 8C. The experiment was conducted in two greenhouse sections (one per temperature) and employed a complete block statistical design, with five plants per cultivar (12 cultivars) per temperature in each of two blocks within each greenhouse section. Leaf number below the first flower, flower bud number (buds > 1 mm), lateral shoot number (>3 cm), diameter of the first flower and peduncle length on the first flower were determined on five plants per block per cultivar when the first flower opened. The media was then washed from the roots and plants were dried in an oven at 70 8C for 3 d for dry mass measurement. Dry mass gain rate was determined as whole plant dry mass at flowering divided by days to flower. 2.3. Growth analysis (Experiment II) In a separate experiment conducted simultaneously with Experiment I (identical general growth conditions as defined in Section 2.1), 10 plants of each cultivar grown at constant 20 8C air temperature were harvested for dry mass determination when two true leaves had unfolded (day 0). On day 0, 30 plants of each cultivar remained under 20 8C, while another 30 plants were moved into a greenhouse maintained at constant 30 1 8C air temperature, under ambient irradiance plus 60 mmol m2 s1 supplemental irradiance from 06:00 to 24:00 h daily. Plants in each temperature treatment were divided into two blocks (15 plants per cultivar per block). Ten, 20 and 30 d after the initiation of the experiment, five plants per block (2) per temperature treatment (2) of each cultivar were harvested for dry mass measurement. Media was washed from the roots; plants were divided into roots and shoots and placed in a 70 8C drying oven for 3 d. These data were used to calculate root:shoot ratio at each harvest, as well as root and shoot growth rates and overall relative growth rate for each 10 d interval. Relative growth rates were calculated according to the method recommended by Hoffmann and Poorter (2002): rˆ ¼
lnðW2 Þ lnðW1 Þ t2 t1
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where rˆ is the estimate of relative growth rate and lnðWt Þ is the mean of the ln-transformed whole plant dry masses at time t. This method was selected as it provides unbiased estimates of relative growth rates under all conditions, including differences in standard deviation of relative growth rate, sample size, or time between harvests (Hoffmann and Poorter, 2002). 2.4. Relative heat tolerance across cultivars and correlations Relative heat sensitivity of the cultivars was determined using a weighted base selection index based on the percentage reduction of flower number, flower diameter, total color, lateral shoot number, and dry mass gain rate as temperature increased from 20 to 30 8C (adapted from Strope, 1999). Total color is defined as flower number estimated area of the first flower (calculated using flower diameter and assuming that the flower is circular). Percentage reduction in flower number ranged from 20 to 77% across cultivars. Therefore, cultivars were given a score of 1–5 based on the following percentage reductions in flower number: 1 (20–32%), 2 (33–44%), 3 (45–56%), 4 (57– 68%), or 5 (69–80%). Scoring criteria for each variable are presented in Table 1. A weighted base selection index was used where index score = 2 (flower number score) + 2 (flower diameter score) + 2 (total color score) + branch number score + dry mass gain rate score. This index places twice as much emphasis on floral variables as on vegetative variables, as flowering performance under high temperatures is of primary importance. Selection indices were used previously to rank heat tolerance among cultivars (Strope, 1999) and are a useful method because they combine responses of numerous parameters to provide an overall indication of relative heat tolerance. To identify parameters that may be indicators of heat tolerance for flowering, a correlation matrix was developed among selected parameters from Experiments I and II using the Bivariate Correlations function from the statistical analysis software package SPSS (SPSS Inc., Chicago, IL). Growth parameters from the day 10 harvest were chosen for inclusion in the correlation analysis to determine if heat tolerance for flowering could be predicted by analyzing growth response of seedlings to high-temperature exposures. Table 1 Scoring criteria for selection index scores Variable
Flower number Flower diameter Total color Branch number Dry mass gain rate
Reduction (%) Score 1
Score 2
Score 3
Score 4
Score 5
20–32 13–17 60–65 25–31 (10)–2
33–44 18–22 66–71 32–37 3–15
45–56 23–27 72–77 38–43 16–28
57–68 28–32 78–83 44–49 29–41
69–80 33–37 84–89 50–56 42–54
Scores were based on the range of percentage reduction (Reduction) in flower number, flower diameter, total color (flower number estimated flower area), the number of lateral shoots (branch number) and dry mass gain rate exhibited by 12 Viola wittrockiana Gams. cultivars as temperature increased from 20 to 30 8C
297
3. Results 3.1. Experiment I Increasing temperature from 20 to 30 8C increased ‘Crystal Bowl Primrose’ and ‘Skyline White’ leaf number below the first flower from 6 to 7, and from 8 to 9 leaves, respectively. ‘Crystal Bowl Sky Blue’, ‘Delta Yellow’, ‘Majestic Giants Supreme Yellow’, and ‘Super Majestic Giants Canary’ flowered with seven leaves below the first flower, regardless of temperature. ‘Crystal Bowl Purple’, ‘Majestic Giants Red and Yellow’, ‘Majestic Giants Rose Shades’, ‘Skyline Beaconsfield’, ‘Super Majestic Giants Ocean’ and ‘Super Majestic Giants Snow’ flowered with eight leaves below the first flower, regardless of temperature. Temperature and cultivar interacted to affect flower bud number when the first flower opened (Table 2). Increasing temperature reduced flower bud number of all cultivars (Table 2), but the percent reduction in flower bud number varied from 20% for ‘Crystal Bowl Purple’ to 77% for ‘Majestic Giants Red and Yellow’ (Table 3). ‘Majestic Giants Red and Yellow’, ‘Majestic Giants Rose Shades’, ‘Majestic Giants Supreme Purple’, ‘Skyline Beaconsfield’, ‘Super Majestic Giants Ocean’ and ‘Super Majestic Giants Snow’ flower bud numbers were all reduced by at least 58%. Temperature and cultivar interacted to impact flower diameter and days to flower (Table 2). Increasing temperature from 20 to 30 8C reduced flower diameter of all cultivars, but the degree of reduction varied from 14% for ‘Skyline Beaconsfield’ (from 52 to 45 mm, respectively) to 44% for ‘Super Majestic Giants Ocean’ (from 81 to 45 mm, respectively; Tables 2 and 3). The percentage reduction in total color (flower number estimated flower area) ranged from 60% for ‘Crystal Bowl Primrose’ to 88% for ‘Majestic Giants Rose Shades’ (Table 3). Increasing temperature reduced days to flower for all cultivars, but the acceleration of flowering varied from 3 d for ‘Skyline White’ to 15 d for ‘Super Majestic Giants Ocean’ (Table 2). Temperature and cultivar independently affected peduncle length (Table 2). Increasing temperature from 20 to 30 8C increased peduncle length of ‘Crystal Bowl Purple’ and ‘Delta Yellow’ only (Table 2). For instance, increasing temperature from 20 to 30 8C increased ‘Delta Yellow’ peduncle length from 60 to 79 mm, respectively. Temperature and cultivar interacted to impact lateral shoot number (Table 2). Increasing temperature decreased lateral shoot number of all cultivars except ‘Delta Yellow’ (Table 2). The degree of reduction in lateral shoot number as temperature increased from 20 to 30 8C varied from 25% (‘Super Majestic Giants Canary’ from 8 to 6 lateral shoots, respectively) to 56% (‘Majestic Giants Supreme Purple’ from 9 to 4, and ‘Crystal Bowl Sky Blue’ from 16 to 7 lateral shoots, respectively; Tables 2 and 3). High temperature reduced dry mass gain rate of all but two cultivars, ‘Crystal Bowl Purple’ and ‘Skyline White’ (Table 2). ‘Super Majestic Giants Ocean’ dry mass gain rate decreased 54% (from 101 to 46 mg d1, respectively) as temperature
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Table 2 Impact of temperature (Temp) on flower bud number (>1 mm in length) at first flower (flower number), peduncle length of the first flower, number of lateral shoots (>3 cm in length; branch number), diameter of the first open flower, days to flower and dry mass gain rate of 12 Viola wittrockiana Gams. cultivars Cultivar
Temp. (8C)
Flower number
Peduncle length (mm)
Branch number
Flower diameter (mm)
Days to flower
Dry mass gain rate (mg d1)
Crystal Bowl Primrosea
20 30 20 30 20 30 20 30 20 30 20 30 20 30 20 30 20 30 20 30 20 30 20 30
20b 14a 20b 16a 25b 14a 19b 11a 22b 5a 22b 6a 19b 8a 28b 13a 18b 12a 16b 9a 22b 9a 17b 7a ***c *** ***
65a 71a 61a 78b 54a 77a 60a 79b 61a 55a 87a 86a 63a 66a 82a 85a 74a 85a 65a 70a 78a 83a 72a 66a *** * ns
12b 6a 15b 7a 16b 7a 9a 6a 9b 6a 10b 6a 9b 4a 14b 7a 11b 8a 8b 6a 9b 5a 9b 5a
62b 47a 57b 37a 57b 36a 61b 49a 69b 59a 81b 54a 62b 50a 52b 45a 64b 44a 73b 59a 81b 45a 74b 50a
53b 47a 51b 42a 48b 41a 53b 47a 63b 51a 60b 50a 49b 42a 50b 46a 50b 47a 53b 49a 60b 45a 53b 48a
81b 49a 69a 76a 96b 70a 67b 49a 82b 46a 93b 53a 67b 41a 85b 58a 59a 60a 95b 69a 101b 46a 80b 53a
Crystal Bowl Purplea Crystal Bowl Sky Bluea Delta Yellowb Majestic Giants Red and Yellowa Majestic Giants Rose Shadesa Majestic Giants Supreme Purplea Skyline Beaconsfieldb Skyline Whiteb Super Majestic Giants Canarya Super Majestic Giants Ocean a Super Majestic Giants Snowa Cultivar Temperature Cultivar Temperature
*** *** ***
*** *** ***
*** *** ***
*** *** ***
Lowercase letters represent differences in means across temperature within a cultivar, as determined by one-way analysis of variance (P 0.05). a Seed source: Sakata Seeds America, Inc. b Seed source: Syngenta Seeds, Inc. c ns, *, *** denote non-significance or significance at P 0.05 or P 0.001, respectively.
Table 3 Percentage reduction (%Red.; mean at 30 8C compared to mean at 20 8C) in flower bud number (buds > 1 mm) at first flower (flower number), diameter of the first flower, total color (flower number estimated flower area), number of lateral shoots (>3 cm; branch number) and dry mass gain rate at flowering, score of each parameter (from Table 1), total heat sensitivity index score (where index score = 2 (flower number score) + 2 (flower diameter score) + 2 (total color score) + branch number score + dry mass gain rate score) and ranking of 12 Viola wittrockiana Gams. cultivars Cultivar
Super Majestic Giants Canary Delta Yellow Skyline White Crystal Bowl Primrose Skyline Beaconsfield Crystal Bowl Purple Majestic Giants Red and Yellow Majestic Giants Supreme Purple Crystal Bowl Sky Blue Super Majestic Giants Snow Super Majestic Giants Ocean Majestic Giants Rose Shades
Flower number
Flower diameter
Total color
Branch number
Dry mass gain rate
Index
%Red.
Score
%Red.
Score
%Red.
Score
%Red.
Score
%Red.
Score
Score
44
2
19
2
63
1
25
1
28
3
14
1
42 33 30 54 20 77
2 2 1 3 1 5
20 31 24 13 35 16
2 4 3 1 5 1
63 68 60 65 66 83
1 2 1 1 2 4
33 27 50 50 53 33
2 1 5 5 5 2
27 0 40 32 10 44
3 1 4 4 1 5
15 18 19 19 22 27
2 3 4 4 6 7
58
4
19
2
73
3
56
5
39
4
27
7
44 59 59 73
2 4 4 5
37 32 32 33
5 4 4 5
78 81 87 88
4 5 5 5
56 44 44 40
5 4 4 3
27 34 54 45
3 4 5 5
30 34 35 38
9 10 11 12
A lower rank score and index score indicates higher heat tolerance.
Rank
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Table 4 Impact of temperature (Temp) on relative growth rate of 12 Viola wittrockiana Gams. cultivars from day 0–10, 10–20 or 20–30 after initiation of temperature treatments Cultivar
Crystal Bowl Primrose Crystal Bowl Purple Crystal Bowl Sky Blue Delta Yellow Majestic Giants Red and Yellow Majestic Giants Rose Shades Majestic Giants Supreme Purple Skyline Beaconsfield Skyline White Super Majestic Giants Canary Super Majestic Giants Ocean Super Majestic Giants Snow Cultivar Temperature Harvest Cultivar temperature Cultivar harvest Temperature harvest Cultivar temperature harvest
Temp. (8C)
20 30 20 30 20 30 20 30 20 30 20 30 20 30 20 30 20 30 20 30 20 30 20 30 ** a ** *** ns *** * ns
Relative growth rate (mg g1 d1) 0–10 growth interval days
10–20 growth interval days
20–30 growth interval days
144Ab 165Ab 171Ab 175Ab 218Ab 224Ac 188Ab 189Ab 169Ab 173Ab 165Ac 168Ab 144Ab 145Ab 153Ac 123Ab 134Aab 147Ab 161Ab 157Ab 165Ab 184Ab 204Ab 176Ab
146Bb 105Aa 135Aa 143Aab 110Aa 108Ab 137Bab 107Aa 101Aa 105Aa 134Ab 105Aa 132Ab 107Aa 122Ab 126Ab 147Ab 130Ab 110Aab 84Aa 124Aa 83Aa 85Aa 67Aa
96Ba 71Aa 102Aa 73Aa 101Ba 43Aa 81Aa 88Aa 85Aa 84Aa 85Aa 104Aa 90Aa 70Aa 87Aa 70Aa 76Ba 42Aa 83Aa 85Aa 116Aa 123Aa 115Aa 118Aab
Capital letters represent mean differences across temperature, within a cultivar and harvest date, determined by one-way analysis of variance (P 0.05). Lowercase letters represent multiple comparison tests (Tukey’s HSD(0.05)) across harvest date, within a cultivar and temperature. a ns, *, **, *** denote non-significance or significance at P 0.05, 0.01, and 0.001, respectively, determined by one-way analysis of variance.
increased from 20 to 30 8C, the greatest reduction of all cultivars evaluated (Tables 2 and 3). The range in percentage reduction in growth and flowering parameters across cultivars as temperature increased from 20 to 30 8C was used to develop scoring criteria for heat sensitivity index scores (Table 1).
of the 12 cultivars, similar across temperature treatments for 5 of the 12 cultivars, and greater at 30 8C than 20 8C for ‘Crystal Bowl Primrose’ (Table 5).
3.2. Experiment II
Pansy cultivars examined in this experiment varied in response to high temperature based on differences in flower number, flower size, and dry mass gain rate. Therefore, available commercial germplasm could be useful in studying the mechanisms of heat tolerance in pansy. Increasing temperature from 20 to 30 8C decreased flower number and diameter of all pansy cultivars here (Table 2). This reduction in flower number and size is consistent with previous results for other species (Armitage et al., 1981; Yuan et al., 1998). For example, increasing temperature from 15 to 32 8C decreased geranium ‘Sooner Red’ flower number per inflorescence from 49 to 21 flowers under an irradiance level of 350 mmol m2 s1 (18 h photoperiod; 22.7 mol m2 d1 daily light integral; Armitage et al., 1981). The reduction in flower diameter observed here is consistent with previous results for
Relative growth rate declined over time (Table 4). For most cultivars, temperature did not impact relative growth rate on any harvest date. However, increasing temperature from 20 to 30 8C decreased relative growth rate of ‘Crystal Bowl Primrose’, ‘Crystal Bowl Sky Blue’ and ‘Skyline White’ at one growth interval only (20–30 d after initiation of temperature treatments; Table 4). Root:shoot ratio of all cultivars at both temperatures declined over time (day 30 compared to day 10), with the exceptions of ‘Crystal Bowl Primrose’, ‘Majestic Giants Rose Shades’ and ‘Majestic Giants Red and Yellow’ at 20 8C and ‘Skyline White’ at 30 8C (Table 5). Root:shoot ratio after 30 d in temperature treatments was greater at 20 8C than 30 8C for 6
4. Discussion
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Table 5 Impact of temperature on 12 Viola wittrockiana Gams. cultivars root:shoot ratio 0, 10, 20, and 30 d after initiation of temperature treatments Cultivar
Crystal Bowl Primrose Crystal Bowl Purple Crystal Bowl Sky Blue Delta Yellow Majestic Giants Red and Yellow Majestic Giants Rose Shades Majestic Giants Supreme Purple Skyline Beaconsfield Skyline White Super Majestic Giants Canary Super Majestic Giants Ocean Super Majestic Giants Snow Cultivar Temperature Harvest Cultivar temperature Cultivar harvest Temperature harvest Cultivar temperature harvest
Temp. (8C)
20 30 20 30 20 30 20 30 20 30 20 30 20 30 20 30 20 30 20 30 20 30 20 30 ***a *** *** ns *** * ns
Root:shoot ratio 0
10
20
30
0.379a
0.254Aa 0.220Ab 0.250Aab 0.212Ab 0.229Bb 0.170Ab 0.256Bb 0.151Ab 0.293Bab 0.215Ab 0.273Aab 0.242Ab 0.328Ab 0.235Ab 0.260Ab 0.255Ab 0.351Bbc 0.239Aa 0.284Bb 0.204Ab 0.419Bb 0.311Ac 0.409Ac 0.394Ab
0.345Ba 0.191Ab 0.222Bab 0.124Aa 0.228Bb 0.140Aab 0.241Bb 0.163Ab 0.430Bb 0.250Ab 0.331Bb 0.241Ab 0.267Bb 0.190Aab 0.195Aab 0.183Aa 0.399Bc 0.240Aa 0.287Bb 0.157Aab 0.275Aab 0.227Ab 0.399Bbc 0.266Aab
0.156Aa 0.167Ba 0.145Ba 0.088Aa 0.144Ba 0.113Aa 0.148Aa 0.108Aa 0.193Ba 0.122Aa 0.183Aa 0.129Aa 0.130Aa 0.125Aa 0.147Aa 0.149Aa 0.181Aa 0.168Aa 0.186Ba 0.106Aa 0.176Ba 0.133Aa 0.255Ba 0.166Aa
0.325b 0.255b 0.205ab 0.379ab 0.361b 0.331b 0.271b 0.275b 0.174a 0.418b 0.289ab
Capital letters represent mean differences across temperature, within a cultivar and harvest date, determined by one-way analysis of variance (P 0.05). Lowercase letters represent multiple comparison tests (Tukey’s HSD(0.05)) across harvest date, within a cultivar and temperature. 0, 10, 20, 30 denote harvest date (day number). a ns, *, **, *** denote non-significance or significance at P 0.05, 0.01, and 0.001, respectively, determined by one-way analysis of variance.
pansy; ‘Universal Violet’ flower area decreased linearly as temperature increased from 9 to 31 8C (Pearson et al., 1995). The combined effects of reduced flower number and reduced flower diameter led to reductions in total color (flower number estimated flower area) of 60 (for ‘Crystal Bowl Primrose’) to 88% (for ‘Majestic Giants Rose Shades’; Table 3). Herbaceous ornamentals are purchased primarily to provide color in the landscape. This has resulted in breeders selecting plants that produce high total color, either by producing many smaller flowers or fewer but larger flowers. High temperature had little impact on leaf number below the first flower. Only ‘Crystal Bowl Primrose’ and ‘Skyline White’ leaf number below the first flower increased as temperature increased from 20 to 30 8C, and for both cultivars only one additional leaf was produced below the first flower. In contrast, calendula ‘Calypso Orange’ leaf number below the first flower increased from 16 to 42 leaves as temperature increased from 20 to 32 8C at a daily light integral (the cumulative amount of photosynthetically active radiation over a 24-h period) of 10.5 mol m2 d1 (Warner and Erwin, 2005). The impact of temperature on leaf number below the first flower has not been previously reported for pansy. Pansy
‘Universal Violet’ leaf unfolding rate increased linearly as temperature increased from 9.6 to 28.8 8C (Adams et al., 1997a), but plants were either harvested prior to flowering or flowering data were not reported. Also, pansy ‘Universal Violet’ days to flower decreased as temperature increased from 14.8 to 21.7 8C, but increased as temperature further increased from 21.7 to 26.1 8C (Adams et al., 1997b). However, leaf number below the first flower was not reported. In contrast to this result, days to flower for all cultivars reported here decreased as temperature increased from 20 to 30 8C (Table 2). Plant dry mass gain rate (determined at flowering) decreased for all pansy cultivars except ‘Skyline White’ and ‘Crystal Bowl Purple’ (Table 2). This is consistent with previous results for other species. For example, P. grandiflorus ‘Astra Blue’ dry mass at flowering decreased from 5.1 to 1.1 g as temperature increased from 13.7 to 28.9 8C (Park et al., 1998). Similarly, increasing temperature from 20 to 32 8C reduced dry mass gain rate of snapdragon ‘Rocket Rose’, calendula ‘Calypso Orange’ and Mimulus hybridus Hort. ex Sieb. and Voss ‘Mystic Yellow’, but increased dry mass gain rate of torenia ‘Clown Burgundy’ (Warner and Erwin, 2005).
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Table 6 Pearson correlation coefficient matrix of variables flower bud number (Bud), leaf number below the first flower (LN), lateral shoot number (LSN), diameter of the first flower (FD), shoot dry mass at flowering (SDM), root dry mass at flowering (RDM), root:shoot ratio at flowering [R:S(F)], and root:shoot ratio [R:S(10)], shoot dry mass gain rate [SR(10)], root dry mass gain rate [RR(10)] and total dry mass gain rate [TR(10)] after 10 d in temperature Variable
Bud
LN
LSN
FD
SDM
RDM
R:S(F)
R:S(10)
SR(10)
RR(10)
TR(10)
Bud LN LSN FD SDM RDM R:S(F) R:S(10) SR(10) RR(10) TR(10)
– 0.40 0.59 S0.29 0.35 0.00 S0.27 0.24 0.06 S0.27 0.12
0.37 – 0.20 0.07 0.11 0.04 0.02 0.08 0.06 0.04 0.08
0.49 0.31 – S0.53 0.00 0.17 0.20 0.25 0.13 S0.27 0.17
S0.39 0.10 0.09 – 0.56 0.53 0.22 0.40 0.10 0.32 0.17
0.49 0.09 0.56 0.02 – 0.57 0.11 0.07 0.10 0.09 0.11
0.12 0.24 0.32 0.09 0.50 – 0.73 0.31 0.12 0.29 0.18
S0.31 0.16 0.17 0.03 S0.34 0.62 – 0.33 0.10 0.31 0.16
S0.40 0.31 0.23 0.13 0.11 0.23 0.41 – 0.03 0.57 0.15
0.03 0.18 0.31 0.03 0.14 0.01 0.17 S0.26 – 0.77 0.98
S0.30 0.15 S0.25 0.19 0.07 0.21 0.17 S0.56 0.62 – 0.88
0.49 0.11 0.18 0.07 0.14 0.05 0.11 0.08 0.98 0.75
The upper right half of the matrix represents Pearson correlation coefficients for plants growing at 30 8C and the lower left half plants growing at 20 8C. Correlations significant at P 0.05 are shown in bold.
Root:shoot ratio decreased as temperature increased for half of the cultivars here, which is consistent with previous reports on temperature effects on root:shoot (Table 5). For example, Capsicum annuum L. ‘Resistant Giant no. 4’ root:shoot ratio decreased from 0.21 to 0.14 as temperature increased from 14 to 26 8C (Si and Heins, 1996). Similarly, high temperatures reduce root:shoot ratio of Caenothus greggii (Trel.) Jeps. (Larigauderie et al., 1991), Asimina triloba (L.) Dunal (pawpaw; Pomper et al., 2002), Trifolium repens L. (white clover; Murray et al., 2000) and Pascopyrum smithii Rydb. (Read and Morgan, 1996). Flower bud number at 30 8C was positively correlated with branch number and shoot dry mass (but not root dry mass) at flowering but negatively correlated with root:shoot ratio (Table 6). Even a 10 d exposure to 30 8C resulted in a negative correlation between flower bud number and root:shoot ratio. Therefore, when breeding for heat tolerance in pansy, selecting plants that produce high lateral shoot number and high shoot mass while growing at 30 8C may aid in accelerating selection for heat tolerance for flowering. Flower diameter was also negatively correlated with flower bud number as temperature increased from 20 and 30 8C (Table 6). Therefore, plants producing more flower buds did so at the expense of flower size, suggesting flower size may be an indicator of heat tolerance for flowering. The three cultivars that produced the largest flowers at 20 8C, ‘Super Majestic Giants Ocean’, ‘Majestic Giants Rose Shades’ and ‘Super Majestic Giants Snow’ (Table 2) were also the three lowest ranking cultivars for overall heat tolerance (Table 3). In general, cultivars from the ‘Majestic Giants’ and ‘Super Majestic Giants’ series performed poorly when grown at 30 8C, ranking in the bottom half of all cultivars evaluated with respect to selection index score (Table 3). The stark exception to this was ‘Super Majestic Giants Canary’, which ranked first among all cultivars in selection index score. ‘Super Majestic Giants Canary’ and ‘Delta Yellow’ ranked in the top five for all attributes. No cultivar ranked first in all four categories used in the selection index. ‘Crystal Bowl Purple’ was the top ranking cultivar with respect to lowest percentage reduction in flower
number (20%) and dry mass gain rate (10%), but ranked eleventh out of 12 with respect to reduction in flower diameter. ‘Skyline Beaconsfield’ flower diameter was least affected by temperature (13% reduction), and ‘Super Majestic Giants Canary’ lateral shoot number was least affected by temperature (25% reduction; Table 3). The most heat-sensitive cultivars, as determined by the weighted base selection index, were ‘Majestic Giants Rose Shades’, ‘Super Majestic Giants Ocean’ and ‘Super Majestic Giants Snow’ (Table 3). Based on our results, selecting heat-tolerant pansies for flowering may be best achieved by selecting plants with smaller flowers and high lateral shoot number, high shoot dry mass and low root:shoot ratio when grown at 30 8C. Acknowledgements The authors thank Sakata Seeds America, Inc. and Syngenta Seeds, Inc. for donating seeds. We would also like to thank the Floriculture Industry Research and Scholarship Trust (FIRST), the Fred C. Gloeckner Foundation, the Minnesota Nursery and Landscape Association, the Richard E. Widmer Teaching and Research Fund, the Minnesota Extension Service and the Minnesota Agricultural Experiment Station for financial support. References Abdul-Baki, A.A., 1991. Tolerance of tomato cultivars and selected germplasm to heat stress. J. Am. Soc. Hort. Sci. 116, 1113–1116. Adams, S.R., Pearson, S., Hadley, P., 1997a. An analysis of the effects of temperature and light integral on the vegetative growth of pansy cv. Universal Violet (Viola wittrockiana Gams.) Ann. Bot. 79, 219–225. Adams, S.R., Pearson, S., Hadley, P., 1997b. The effects of temperature, photoperiod and light integral on the time to flowering of pansy cv. Universal Violet (Viola wittrockiana Gams.) Ann. Bot. 80, 107–112. Armitage, A.M., Carlson, W.H., Flore, J.A., 1981. The effect of temperature and quantum flux density on the morphology, physiology, and flowering of hybrid geraniums. J. Am. Soc. Hort. Sci. 106, 643–647. Binelli, G., Mascarenhas, J.P., 1990. Arabidopsis: sensitivity of growth to high temperature. Dev. Genet. 11, 294–298. de Lint, P.J.A.L., Heij, G., 1987. Effects of day and night temperature on growth and flowering of chrysanthumum. Acta Hort. 197, 53–61.
302
R.M. Warner, J.E. Erwin / Scientia Horticulturae 108 (2006) 295–302
Hoffmann, W.A., Poorter, H., 2002. Avoiding bias in calculations of relative growth rate. Ann. Bot. 90, 37–42. Ismail, A.M., Hall, A.E., 1998. Positive and potential negative effects of heattolerance genes in cowpea. Crop Sci. 38, 381–390. Larigauderie, A., Ellis, B.A., Mills, J.N., Kummerow, J., 1991. The effect of root and shoot temperatures on growth of Caenothus greggii seedlings. Ann. Bot. 67, 97–101. Lee, W.-S., Barrett, J.E., Nell, T.A., 1990. High temperature effects on the growth and flowering of Impatiens wallerana cultivars. Acta Hort. 272, 121–127. Murray, P.J., Jorgensen, M., Gill, E., 2000. Effect of temperature on growth and morphology of two varieties of white clover (Trifolium repens L.) and their impact on soil microbial activity. Ann. Appl. Biol. 137, 305–309. Niu, G., Heins, R.D., Cameron, A.C., Carlson, W.H., 2000. Day and night temperatures, daily light integral, and CO2 enrichment affect growth and flower development of pansy (Viola wittrockiana). J. Am. Soc. Hort. Sci. 125, 436–441. Niu, G., Heins, R.D., Cameron, A.C., Carlson, W.H., 2001. Temperature and daily light integral influence plant quality and flower development of Campanula carpatica ‘Blue Clips’, ‘Deep Blue Clips’, and Campanula ‘Birch Hybrid’. HortScience 36, 664–668. Park, B.H., Oliveira, N., Pearson, S., 1998. Temperature affects growth and flowering of the ballon flower [Platycodon grandiflorus (Jacq.) A. DC. cv. Astra Blue] HortScience 33, 233–236. Patel, P.N., Hall, A.E., 1990. Genotypic variation and classification of cowpea for reproductive responses to high temperature under long photoperiods. Crop Sci. 30, 614–621. Pearson, S., Parker, A., Adams, S.R., Hadley, P., May, D.R., 1995. The effects of temperature on the flower size of pansy (Viola wittrockiana Gams.) J. Hort. Sci. 70, 183–190. Pomper, K.W., Layne, D.R., Jones, S.C., Kwantes, M.G., 2002. Growth enhancement of container-grown pawpaw seedlings as influenced by media type, root-zone temperature, and fertilization regime. HortScience 37, 329–333.
Ranney, T.G., Peet, M.M., 1994. Heat tolerance of five taxa of birch (Betula): physiological responses to supraoptimal leaf temperatures. J. Am. Soc. Hort. Sci. 119, 243–248. Read, J.J., Morgan, J.A., 1996. Growth and partitioning in Pascopyrum smithii (C3) and Bouteloua gracilis (C4) as influenced by carbon dioxide and temperature. Ann. Bot. 77, 487–496. Schwabe, W.W., 1985. Kalanchoe blossfeldiana. In: Halevy, A.H. (Ed.), Handbook of Flowering, vol. III. CRC Press, Boca Raton, FL, pp. 217– 235. Si, Y., Heins, R.D., 1996. Influence of day and night temperatures on sweet pepper seedling development. J. Am. Soc. Hort. Sci. 121, 699–704. Strope, K.M., 1999. The effects of heat stress on flowering and vegetative growth of New Guinea impatiens (Imatiens hawkeri Bull.). MS Thesis, Univ. Minnesota, Saint Paul. USDA-NASS, 2005. Unites States Department of Agriculture National Agricultural Statistics Service—Floriculture crops 2004. Report number Sp Cr6-1 (05). http://usda.mannlib.cornell.edu/reports/nassr/other/zfc-bb/ floran05.pdf. Warner, R., Erwin, J.E., Wagner, R., 1997. Photoperiod and temperature interact to affect Gomphrena globosa L. and Salvia farinacea Benth. development. HortScience 32, 501 (abst.). Warner, R.M., Erwin, J.E., 2001. Effect of high-temperature stress on flower number per inflorescence of 11 Lycopersicon esculentum Mill. genotypes. HortScience 36, 508 (abst.). Warner, R.M., Erwin, J.E., 2005. Prolonged high temperature exposure and daily light integral impact growth and flowering of five herbaceous ornamental species. J. Am. Soc. Hort. Sci. 130, 319–325. Whealy, C.A., Nell, T.A., Barrett, J.E., Larson, R.A., 1987. High temperature effects on growth and floral development in chrysanthemum. J. Am. Soc. Hort. Sci. 112, 464–468. Yuan, M., Carlson, W.H., Heins, R.D., Cameron, A.C., 1998. Effect of forcing temperature on time to flower of Coreopsis grandiflora, Gaillardia Leucanthemum, Leucanthemum superbum, and Rudbeckia fulgida. HortScience 33, 663–667.