HORTSCIENCE 54(7):1164–1167. 2019. https://doi.org/10.21273/HORTSCI13919-19 different are unclear. In this study, we aimed to characterize the different re- sponses of growth and photosynthesis The Effect of Temperature on to temperature changes among four cultivars of Gerbera hybrida. We cultivated plant Plant Growth in Four Gerbera seedlings without soil using substrate (peat:perlite = 3:1) under four different tem- hybrida Cultivars perature regimens: 15, 20, 25, and 30 C. We investigated plant growth parameters to analyze Fan Li, Shenchong Li, and Qinli Shan1 the temperature responses of plant growth, such Floriculture Research Institute, Yunnan Academy of Agricultural Sciences, as plant height, root length, aboveground National Engineering Research Center for Ornamental Horticulture, Yunnan weight, underground weight, and leaf area. The temperature response of the photosynthetic Key Laboratory for Breeding, Kunming 650200, China rate was also examined in fully expanded young Additional index words. temperature response, plant height, biomass accumulation, leaf area, leaves of each temperature regimen. The aim of photosynthesis this study was to provide scientific basis for the environmental control of soilless cultivation in Abstract. Temperature is one of the main factors that affects the growth pattern of Gerbera hybrida. Gerbera hybrida, which shows vast variation in morphology and stress adaptation among cultivars. However, little is known about temperature responses of plant growth among Materials and Methods different cultivars. In this study, four cultivars were planted in different growth temperatures to investigate the effect of temperature on plant growth of Gerbera hybrida Plant material and growth conditions. during their vegetative growth. Results showed that the optimum growth temperature of Four commercial cultivars of Gerbera the four cultivars was 20 8C, of which plant height, root length, biomass accumulation, hybrida (Autumn, Pretty Pink, Lucky, and leaf area, and photosynthetic rate were enhanced significantly. Different cultivars Yellow Storm; Fig. 1) were studied in this showed diverse temperature adaptation ranges, which were related with their genetic research. ‘Lucky’ and ‘Yellow Storm’ are the background, and the temperature adaptability of Autumn was the best among main cultivars in Yunnan Province, whereas the four cultivars. Temperature also had significant effects on photosynthetic rate, which cultivars Autumn and Pretty Pink are new was the main factor shaping plant growth. Our research provides the basic guidance for varieties that were bred according to the the growth temperature control in the cultivation of Gerbera hybrida. climatic conditions of Yunnan. The four cultivars refer different phenotypes that adapted to low-latitude and high-altitude re- Gerbera hybrida is one of the most sponse in many cases (Takeshi and Amane, gions in Yunnan Province, China. Plant important floricultural worldwide 2009). The effect of temperature on plant seedlings were obtained from Yuxi Yunxing due to the high variation of flower and growth and development differs in each Biological Technology Co., Ltd. (Yunnan inflorescence colors, which make it rank species, which has a specific temperature Province, China) and planted separately in fourth in cut flowers after , chrysanthe- range (minimum, maximum, and optimum) individual pots (diameter = 14 cm, height = mum, and according to data from the during its life cycle (Hatfield and Prueger, 12 cm) that were filled with commercial International Trade Center (Wani et al., 2015). For instance, the optimum tempera- potting substrate (peat:perlite = 3:1). All 2018). Around the world, there are hun- ture for vegetative development is 37 C and seedlings were then cultivated in environ- dreds of Gerbera hybrida cultivars with for reproductive development is 30 Cin mentally controlled growth chambers under extremely rich flower color patterns, in- cotton (Yuri et al., 2005), whereas in sor- the condition of 12 h photoperiod (photosyn- cluding white, yellow, red, pink, purple, ghum the optimum temperatures for vegeta- thetic photon flux density was 240 mmol·m–2·s–1) andbrown.Thisisbecausecommercial tive and reproductive development are 34 and and 55% relative humidity in the laboratory of varieties of Gerbera hybrida are cultivated 31 C, respectively (Prasad et al., 2006). The Yunnan Academy of Agricultural Sciences. from the hybridization of two natural species: changes of plant growth temperature induce a The growth chamber (LRH-400-GSI, 400 L; and Gerbera viridifolia range of morphological responses and alter- Zhujiang, China) was controlled by micro- (Hansen, 1999). For this highly heterozygous nations in biomass allocation, and such computer PID, with ±1 C and ±8% control species, Gerbera hybrida naturally harbors the changes lead to different temperature depen- accuracy for temperature and humidity, re- genetic diversity between different cultivars, dence of yields between species (Atkin et al., spectively. The seedlings were treated with causing distinct requirements in terms of 2006). For example, the life cycle and dura- four different temperature regimes: 15, 20, 25 growth conditions, such as temperature, light, tion of reproductive development were and 30 C, and each treatment used five moisture, and nutrients. shorter under increased temperature, result- individual seedlings as repetitions. Temperature is a primary factor that ing in decreased grain yield in maize Plant growth analysis. Plant growth anal- affects plant growth, especially cell growth (Muchow et al., 1990); however, the biomass ysis were carried out on the 60th day after and elongation, and the process of growth can of rice increased with temperature (from 8 to planting. The parameters of plant height, root be differentiated by their temperature re- 33 C), and the optimum temperature for length, aboveground weight, underground grain formation and yield was 25 C (Baker weight, leaf area, and photosynthetic rate were et al., 1995). Overall, the effect of tempera- measured in each treatment. Leaf area was Received for publication 20 Feb. 2019. Accepted ture on plant growth and the underlying determined by a leaf area meter (LI-3100C; for publication 1 Apr. 2019. growth indices are different among species, LI-COR, Lincoln, NE). Photosynthetic rate Supported by the Science and Technology Talents and the mechanisms of growth temperature was measured by a fast-photosynthetic instru- and Platform Program of Yunnan Province responses are still unclear. ment (ECA-PC0401; Shanghai Danding In- (2018HB117), China National Science and Tech- Nevertheless, growth responses to tem- ternational Trade Co., Ltd., China). nology Support Program (2015BAD10B01), the perature are not well known in Gerbera Statistical analysis. Data analysis and Key Research and Development (Agricultural hybrida, even though this species has been statistics were performed by Microsoft field) Project of Yunnan Science and Technology Program (2018BB010), and the Major Science used as an model plant for re- (Redmond, WA) Excel 2016 and Data Pro- and Technology Project of Yunnan Province search on flower development and second- cessing System (Hangzhou Ruifeng Informa- (2016ZA006). ary metabolism for decades. Indeed, the tion Technology Co., Ltd., China) (Tang and 1Corresponding author. E-mail: shqli2008@126. factors that determine the differences in Zhang, 2013). One-way analysis of variance com. temperature-related growth traits between with post hoc Tukey honestly significant

1164 HORTSCIENCE VOL. 54(7) JULY 2019 CROP PRODUCTION difference test were used for multiple samples 30 C, showing poor heat tolerance, whereas and gene regulatory network controls the mean comparison at the 5% significant level. the cultivar Lucky was unable to resist cold temperature resistance of Gerbera hybrida. because the seedlings were all dead at 15 C. Further, from the view of plant height, the Results and Discussion Only two cultivars examined in this study optimum temperature for all cultivars exam- showed a wide range of temperature adapt- ined was 20 C, which displayed a clear peak Although Gerbera hybrida is mainly ability, from 15 to 30 C, which represents at that point (Fig. 2). More specifically, the planted in modern greenhouses, and some the climate condition in low-latitude and cultivars Autumn and Yellow Storm showed of them are even equipped with a heating high-altitude regions in Yunnan Province. the highest plant height at 20 C compared system, growth temperature is still the major These differences may be caused by the with the other three temperatures, but no factor that is considered by producers be- diversity of the genetic background of the significant difference was observed between cause of low night temperature during four cultivars, because each cultivar came the two species in each four-temperature Winter. In this study, we examined the from a different progress of hybrid breeding. treatment, whereas the plant height of culti- temperature responses of plant growth am- A recent study of cold tolerance in Gerbera vars Pretty Pink and Lucky was significantly ong four Gerbera hybrida cultivars, which hybrida showed that cultivar Hongjixing lower than that of cultivars Autumn and showed large variations between temperature could tolerate the extreme cold temperature Yellow Storm. This is in line with their treatments and cultivars (Fig. 2, Supplemen- of –4 C and keep flowering even below 0 C. temperature tolerance trends. On the other tal Table 1). Generally, the optimum temper- The comparative transcriptome sequencing hand, the four cultivars displayed no differ- ature for vegetative development of Gerbera (RNA sequencing) revealed several path- ence at 15 and 20 C in terms of root length, hybrida was 20 C, of which seedling growth ways involved in the process of cold toler- but significant differences were found was the strongest and photosynthetic rate was ance of Gerbera hybrida, such as carbon at higher temperatures, indicating the the greatest. However, different cultivars metabolism, nucleotide metabolism, second- root length is less sensitive to temperature have their specific temperature limitation ary metabolism, transcription regulation, and changes. Moreover, the aboveground weight during vegetative development. For instance, stress defense-related responses (Li et al., and underground weight of all cultivars the cultivar Pretty Pink could not survive at 2018). This indicates that a complex genetic gained the most at 20 C, indicating 20 C

Fig. 1. Four commercial cultivars of Gerbera hybrida used in this study. (A) Gerbera hybrida cultivar Autumn; (B) Gerbera hybrida cultivar Pretty Pink; (C) Gerbera hybrida cultivar Lucky; (D) Gerbera hybrida cultivar Yellow Storm. The four cultivars refer to different phenotypes that adapted to low-latitude and high-altitude regions in Yunnan Province, China.

Fig. 2. Effects of temperature on plant growth in four cultivars of Gerbera hybrida (mean ± SD, n = 5). Small letters denote significant differences of growth parameters among the four cultivars at each temperature treatment. Statistical significance was analyzed based on one-way analysis of variance; P value was calculated with post hoc Tukey honestly significant difference test (a = 0.05).

HORTSCIENCE VOL. 54(7) JULY 2019 1165 is the most suitable temperature for biomass (Fig. 3). However, the photosynthetic rate of hybrida also may be related to Rubisco accumulation in Gerbera hybrida (Fig. 2). Gerbera hybrida was largely affected by capacity, which needs further research for Compared with other cultivars, the plant temperature in the four cultivars, showing the principal factor limiting photosynthetic weight of cultivar Autumn was less sensitive the lowest photosynthetic rate at 15 C and rate. to temperature changes, whereas cultivar highest at 20 C. Surprisingly, 5 C incre- Our analysis revealed the responses of Yellow Storm showed a dramatic change in ments stimulated more than 6-fold accumu- biomass accumulation, leaf area, and photo- plant weight, and cultivar Pretty Pink dis- lation of photosynthetic rate, demonstrating synthetic rate of the four cultivars to different played the lowest biomass accumulation. temperature is the main factor determining temperature treatments, which showed the Although no differences in plant height and photosynthetic rate in Gerbera hybrida. The same trend with a peak at 20 C. This pattern root length were found in cultivars Yellow study of temperature response of photosyn- suggests a regulatory relationship between Storm and Autumn, the biomass accumula- thesis in transgenic rice showed that photo- biomass accumulation and leaf area or pho- tion of cultivar Yellow Storm was less synthetic rate was predominantly limited by tosynthetic rate. To explore this possibility, efficient beyond the optimum temperature Rubisco capacity from 15 to 20 C (Makino we next assessed the correlation between range. These data demonstrated that the and Sage, 2007). Consistent with this, several biomass and leaf area, as well as the corre- temperature adaptability of cultivar Autumn studies reported that Rubisco played a main lation between biomass and photosynthetic is better than that of cultivar Yellow Storm. role in the regulation of photosynthetic rate in rate. Indeed, the regression analysis revealed Compared with photosynthetic rate, leaf many plant species, such as rice, spinach, and a significant correlation between biomass and area of the four cultivars did not show much cyanobacteria (Fukayama et al., 2012; Kasai, leaf area (P = 0.0091), as well as the biomass variation in each temperature treatment, in- 2010; Yamori et al., 2010; Zorz et al., 2015). and photosynthetic rate (P = 0.0272) (Fig. 4). dicating temperature is not a key factor Therefore, we speculate that the temperature This implies that the biomass accumulation affecting leaf area among different cultivars responses of photosynthesis in Gerbera of Gerbera hybrida is closely related to leaf

Fig. 3. Effects of temperature on leaf area and photosynthesis in four cultivars of Gerbera hybrida (mean ± SD, n = 5). Small letters denote significant differences of growth parameters among the four cultivars at each temperature treatment. Statistical significance was analyzed based on one-way analysis of variance; P value was calculated with post hoc Tukey honestly significant difference test (a = 0.05).

Fig. 4. The correlation analysis of biomass, leaf area, and photosynthetic rate in four cultivars of Gerbera hybrida (mean value, n = 5).

1166 HORTSCIENCE VOL. 54(7) JULY 2019 area and photosynthetic rate. Overall, our Hatfield, J.L. and J.H. Prueger. 2015. Temperature Takeshi, N. and M. Amane. 2009. Differences research on the temperature tolerance of extremes: Effect on plant growth and develop- between rice and wheat in temperature re- different cultivars could provide guidance ment. Weather Clim. Extremes 10:4–10. sponses of photosynthesis and plant growth. for the production of Gerbera hybrida, but Kasai, M. 2010. Regulation of leaf photosynthetic Plant Cell Physiol. 50:744–755. the molecular mechanisms underlying the rate correlating with leaf carbohydrate status Tang, Q.Y. and C.X. Zhang. 2013. Data Processing and activation state of Rubisco under a variety System (DPS) software with experimental de- tolerance still need further research to pro- of photosynthetic source/sink balances. Phys- sign, statistical analysis and data mining de- vide theoretical insights. iol. Plant. 134:216–226. veloped for use in entomological research. Li, S., Q. Shan, R. Yu, A.N. Siddique, X. Li, C. Insect Sci. 20:254–260. Literature Cited Yang, J. Ruan, and M. Li. 2018. Comparative Wani, M.A., I.T. Nazki, A. Din, S. Iqbal, S.A. Wani, Atkin, O.K., B.R. Loveys, L.J. Atkinson, and T.L. transcriptome analysis of two Gerbera hybrida and F. Khan. 2018. Floriculture sustainability Pons. 2006. Phenotypic plasticity and growth cultivars revealed cold tolerance mechanism. initiative: The dawn of new era, p. 91–127. In: temperature: Understanding interspecific vari- Plant Omics 11:10–19. E. Lichtfouse (ed.). Sustainable Agriculture Makino, A. and R.F. Sage. 2007. Temperature ability. J. Expt. Bot. 57:267–281. Reviews, vol. 27. Springer, Cham. Baker, J.T., K.J. Boote, and L.H. Allen. 1995. response of photosynthesis in transgenic rice Yamori, W., K.K. Suzuki, M. Nakai, and I. transformed with ‘sense’ or ‘antisense’ rbcS. Terashima. 2010. Effects of Rubisco kinetics Potential climate change effects on rice: Car- Plant Cell Physiol. 48:1472–1483. and Rubisco activation state on the temperature bon dioxide and temperature, p. 31–47. In: C. Muchow, R.C., T.R. Sinclair, and J.M. Bennett. dependence of the photosynthetic rate in spin- Rosenzweig (ed.). Climate change and agricul- 1990. Temperature and solar radiation effects ach leaves from contrasting growth tempera- ture: Analysis of potential international impacts. on potential maize yield across locations. tures. Plant Cell Environ. 29:1659–1670. American Society of Agronomy, Madison, WI. Agron. J. 82:338–343. Yuri, F., B. Vladimir, M. Igor, M. Valeri, and S. Fukayama, H., C. Ueguchi, K. Nishikawa, N. Katoh, Prasad, P.V.V., K.J. Boote, and L.H. Allen, Jr. Oleg. 2005. Crop responses to elevated carbon C. Ishikawa, C. Masumoto, T. Hatanaka, and S. 2006. Adverse high temperature effects on dioxide and interaction with temperature. J. Misoo. 2012. Overexpression of Rubisco acti- pollen viability, seed-set, seed yield and Crop Improv. 13:113–155. vase decreases the photosynthetic CO2 assim- harvest index of grain-sorghum [Sorghum Zorz, J., J. Allanach, C. Murphy, M. Roodvoets, ilation rate by reducing Rubisco content in rice bicolor (L.) Moench] are more severe at D. Campbell, and A. Cockshutt. 2015. The leaves. Plant Cell Physiol. 53:976–986. elevated carbon dioxide due to higher tissue Rubisco to photosystem II ratio limits the Hansen, H.V. 1999. A story of the cultivated temperatures. Agr. For. Meteorol. 139:237– maximum photosynthetic rate in picocyano- Gerbera. New Plantsman 6:85–95. 251. bacteria. Life 5:403–417.

HORTSCIENCE VOL. 54(7) JULY 2019 1167 Supplemental Table 1. Effects of temperature on plant growth in four cultivars of Gerbera hybrida (mean ± SD, n = 5). Temperature (C) Cultivars Parameters 15 20 25 30 Autumn Plant height (cm) 9.24 ± 0.69 b 11.54 ± 0.41 a 10.44 ± 1.49 ab 9.86 ± 1.17 ab Root length (cm) 8.74 ± 0.59 c 12.16 ± 0.71 a 10.44 ± 0.53 b 9.12 ± 1.00 c Aboveground wt (g) 6.72 ± 1.09 b 8.90 ± 1.28 a 7.95 ± 0.96 ab 7.10 ± 1.17 ab Underground wt (g) 3.30 ± 0.65 ab 3.90 ± 0.67 a 2.69 ± 0.46 b 2.60 ± 0.59 b Leaf area (cm2) 9.81 ± 2.18 b 17.69 ± 2.09 a 13.19 ± 1.93 b 12.90 ± 2.49 b Photosynthetic rate (mmol·m–2·s–1) 63.88 ± 15.40 c 403.52 ± 24.09 a 277.02 ± 28.65 b 265.18 ± 16.21 b Pretty Pink Plant height (cm) 5.40 ± 1.23 b 9.74 ± 1.55 a 7.06 ± 0.40 b / Root length (cm) 10.22 ± 1.21 b 11.78 ± 1.69 ab 13.54 ± 1.40 a / Aboveground wt (g) 2.08 ± 0.34 b 5.69 ± 1.53 a 3.29 ± 0.51 b / Underground wt (g) 1.92 ± 0.50 b 3.43 ± 0.86 a 1.93 ± 0.20 b / Leaf area (cm2) 9.38 ± 0.93 b 13.57 ± 2.29 a 12.60 ± 0.75 a / Photosynthetic rate (mmol·m–2·s–1) 85.22 ± 9.23 c 399.76 ± 10.23 a 243.96 ± 22.86 b / Lucky Plant height (cm) / 9.49 ± 0.75 a 8.72 ± 0.94 ab 7.82 ± 0.75 b Root length (cm) / 12.52 ± 1.08 a 9.58 ± 0.98 b 6.52 ± 0.70 c Aboveground wt (g) / 7.73 ± 0.82 a 6.79 ± 0.45 a 3.74 ± 0.65 b Underground wt (g) / 3.95 ± 0.57 a 2.89 ± 0.55 b 1.42 ± 0.26 c Leaf area (cm2) / 16.28 ± 1.81 a 12.44 ± 1.07 b 9.02 ± 1.43 c Photosynthetic rate (mmol·m–2·s–1) / 257.62 ± 22.40 a 186.26 ± 17.85 b 137.32 ± 36.55 c Yellow Storm Plant height (cm) 9.86 ± 1.03 b 12.80 ± 0.41 a 10.66 ± 0.84 b 9.90 ± 0.48 b Root length (cm) 9.94 ± 1.87 bc 13.52 ± 1.26 a 12.08 ± 0.86 ab 9.62 ± 0.62 c Aboveground wt (g) 2.55 ± 0.58 c 7.70 ± 1.73 a 4.61 ± 0.83 b 4.03 ± 0.87 bc Underground wt (g) 1.91 ± 0.57 b 3.35 ± 0.43 a 2.15 ± 0.20 b 2.03 ± 0.27 b Leaf area (cm2) 12.25 ± 2.48 b 15.49 ± 1.13 a 14.57 ± 0.62 ab 12.69 ± 1.77 ab Photosynthetic rate (mmol·m–2·s–1) 39.70 ± 9.67 c 368.98 ± 19.80 a 298.32 ± 24.31 ab 250.48 ± 80.17 b Lowercase letters denote significant differences of growth parameters among four temperature treatments of each cultivar. Statistical significance was analyzed based on one-way analysis of variance; P value was calculated with post hoc Tukey honestly significant difference test (a = 0.05).

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