Pepper Photosynthesis, Stomatal Conductance, Transpiration, and Water Use Efficiency Differ with Variety, Indigenous Habitat, and Species of Origin

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  • 1 Department of Horticultural Science, University of Minnesota, 1970 Folwell Avenue, St. Paul, MN 55108
  • | 2 Institute of Horticultural Sciences, University of Agriculture, Agriculture University Road, Faisalabad, Pakistan 38000
  • | 3 Department of Food Science and Nutrition, University of Minnesota, 1334 Eckles Avenue, St. Paul, MN 55108

The instantaneous photosynthetic rate (Pn), transpiration rate (E), and stomatal conductance (gS) were measured for 33 outdoor-grown Capsicum varieties (varying in species of origin and indigenous habitat) between 29 July and 22 Aug. 2017 using a portable gas exchange meter. Cuvette leaf temperature (Tleaf) and relative humidity (RH) were recorded at that same time. Pn differed from 3.6 to 3.7 for ‘Malawi Piquante’ and ‘Korean Long Green’ peppers to 16.3 μmol CO2/m2/s (fixed) for ‘Thai Hot’ peppers. The gS differed from 0.01 to 0.05 among 13 varieties to 0.28 mmol H2O/m2/s for ‘Thai Hot’ peppers. E differed from 0.43 to 0.59 among three varieties to 4.14 to 4.20 mmol H2O/m2/s for ‘CGN 22091’ and ‘Peruvian Purple’ peppers. Water use efficiency (WUE; Pn/E) varied from 2.92 to 3.43 among three varieties to 5.10 to 7.20 for 16 other varieties. C. annuum derived varieties had higher Pn (9.4 μmol CO2/m2/s fixed) than varieties derived from other species (4.5–8.6 μmol CO2/m2/s fixed). Varieties originating from dry climates had higher Pn (12.5 μmol CO2/m2/s fixed) than those originating from temperate or tropical climates (8.0–8.8 μmol CO2/m2/s fixed). Tleaf (27 to 33 °C) and RH (38% to 39% and 57% to 59%) differed among varieties. Pn was positively correlated with gS, E, and RH and was negatively correlated with WUE. We found that Capsicum Pn, E, and gS varied more than has been previously reported, and our data suggested that Pn, gS, and E data of outdoor-grown peppers should be used only when selecting parents for a breeding program (unless progeny is intended for greenhouse production).

Abstract

The instantaneous photosynthetic rate (Pn), transpiration rate (E), and stomatal conductance (gS) were measured for 33 outdoor-grown Capsicum varieties (varying in species of origin and indigenous habitat) between 29 July and 22 Aug. 2017 using a portable gas exchange meter. Cuvette leaf temperature (Tleaf) and relative humidity (RH) were recorded at that same time. Pn differed from 3.6 to 3.7 for ‘Malawi Piquante’ and ‘Korean Long Green’ peppers to 16.3 μmol CO2/m2/s (fixed) for ‘Thai Hot’ peppers. The gS differed from 0.01 to 0.05 among 13 varieties to 0.28 mmol H2O/m2/s for ‘Thai Hot’ peppers. E differed from 0.43 to 0.59 among three varieties to 4.14 to 4.20 mmol H2O/m2/s for ‘CGN 22091’ and ‘Peruvian Purple’ peppers. Water use efficiency (WUE; Pn/E) varied from 2.92 to 3.43 among three varieties to 5.10 to 7.20 for 16 other varieties. C. annuum derived varieties had higher Pn (9.4 μmol CO2/m2/s fixed) than varieties derived from other species (4.5–8.6 μmol CO2/m2/s fixed). Varieties originating from dry climates had higher Pn (12.5 μmol CO2/m2/s fixed) than those originating from temperate or tropical climates (8.0–8.8 μmol CO2/m2/s fixed). Tleaf (27 to 33 °C) and RH (38% to 39% and 57% to 59%) differed among varieties. Pn was positively correlated with gS, E, and RH and was negatively correlated with WUE. We found that Capsicum Pn, E, and gS varied more than has been previously reported, and our data suggested that Pn, gS, and E data of outdoor-grown peppers should be used only when selecting parents for a breeding program (unless progeny is intended for greenhouse production).

Peppers (Capsicum sp.) were one of the first crops domesticated in the Western Hemisphere using several independent, geographically distinct, and regional domestication efforts (Bosland and Votava, 2012). Cultivated peppers are derived from five species (C. annuum L., C. baccatum L., C. chinense Jacq., C. frutescens L., and C. pubescens) among the 32 documented species in the Capsicum genus (Solanaceae family) (Qin et al., 2014). These domestication efforts resulted in peppers becoming a globally important fresh vegetable (fruit) and spice crop that is now consumed by nearly one-quarter of the world’s population, with fresh and dry pepper production reaching 32.2 and 3.8 million tons annually, respectively, in 2014 (FAO, 2014). In the United States, 44,800 acres of bell peppers and 19,400 acres of chili pepper were produced in 2015, with a wholesale value of $806 million and $135 million, respectively (USDA NASS Report, 2016). Peppers are consumed as a fresh food and contain carbohydrates, fiber, and a variety of nutrients, including antioxidants such as vitamin C, vitamin E, β-carotene, and carotenoids (Carvalho et al., 2011; Howard et al., 2000; Howard and Wildman, 2007; Kantar et al., 2016; Palevitch and Craker, 1995; Russo and Howard, 2002; Topuz and Ozdemir, 2007; Wahyuni et al., 2011). Other pepper products are consumed as spices, including dried pepper flakes, processed “hot” sauces, and infused/pressed oils, among other products (Bosland, 1996; Zewdie and Bosland, 2001).

Abiotic factors such as low temperatures, high temperatures, salt stress, drought (Serrano et al., 2017), and waterlogging can limit pepper yield (Ou and Zou, 2012; Zhai et al., 2016). For instance, optimal temperatures for pepper photosynthesis range from 25 to 35 °C, and temperatures outside this range can limit the yield; for example, C. chinense flower abortion increased 2-fold and fruit set decreased 3-fold when greenhouse temperatures were increased from 30 to 40 °C (Garruna-Hernandez et al., 2014). Erickson and Markhart (2002) showed that Capcisum flower abortion after pollination was particularly sensitive to high temperatures (33 °C).

We determined whether photosynthetic and water use attributes differed among outdoor-grown pepper varieties that differed in parental species and indigenous climates. Previous studies of Capsicum focused on differences in photosynthetic and water use attributes among species only or varieties within a species. Past Capsicum research often used greenhouse-grown or controlled environment–grown plants. Our research objectives were to: 1) determine whether instantaneous Pn, gS, E, WUE meter cuvette Tleaf, and RH of 33 outdoor-grown pepper varieties differed; 2) to determine whether variety photosynthetic and water use attributes differed based on indigenous parents or habitat; and 3) to determine whether pepper photosynthetic and/or water use attributes were correlated with each other.

Materials and Methods

Thirty-three pepper varieties derived from five species (C. annuum L., C. baccatum L., C. chinense Jacq., C. frutescens L., and C. pubescens) from three indigenous habitats (dry, temperate, and tropical) were selected (Table 1). Seeds were sourced from different seed producers/suppliers, and the reported species of origin were confirmed by phenotyping of flowers, leaves, and fruits during the experiment (Table 1). Seeds were sown 0.6 cm deep in Master Garden Premium media (Premier Tech Horticulture, Ltd., Ontario, Canada) in 32-cell trays (one seed per cell; individual cell volume = 150 cm3) in January and February 2017. Trays were then covered with a clear plastic lid (10 cm above media) and were placed in a greenhouse (23 ± 2 °C air temperature). After seeds germinated and cotyledons unfolded, the lid was removed and plants were grown for 9 to 14 additional weeks under natural daylight plus 25 μmol·m−2·s−1 supplemental irradiance (0800–0200 hr; Sunblaze T5 fluorescent lights; Sunlight Supply, Inc., WA; +1.62 mol·m−2·d−1 daily light integral) in the same greenhouse. After five leaves unfolded, plants were transplanted into 18.9-L plastic pots with the same media. Potted plants were placed outdoors (St. Paul, MN) on 1 June and were watered with a drip irrigation system as needed. Nutrients were provided by incorporating granular Sustane Natural Fertilizer (4–6–4; Cannon Falls, MN) with media at a rate of 12 g/L to provide ≈100 ppm of N (3.2N–6P2O5–4K2O).

Table 1.

Variation in the instantaneous photosynthetic rate (Pn; μmol·m−2·s−1), stomatal conductance (gS; mmol H2O/m2/s), transpiration rate (E; mmol H2O/m2/s), cuvette leaf temperature (Tleaf; °C), and relative humidity after 5 min (RH; %) and water use efficiency (WUE; WUE = Pn/E) among 33 outdoor-grown pepper varieties that vary in indigenous habitat and species. Indigenous habitats used for analysis are shown as superscript numbers after the variety name (1desert; 2temperature; 3tropical; ?unknown).

Table 1.

Pn, gS, and E data were collected from the third unfolded mature leaf (expansion completed) below the shoot tip using a LI-COR LI6400XT portable gas exchange meter (LI-COR, Inc., Lincoln, NE) with an external cuvette with a built-in LED light source (cuvette dimensions = 3 × 2 cm2) on 29 July, 3 Aug., 5 Aug., 10 Aug., 17 Aug., and 22 Aug. 2017 (similar weather conditions). Because data were collected at different times, a different leaf was used each time as the plant grew. Data were recorded 5 min after placing the cuvette around a leaf (Pn had stabilized). Cuvette Tleaf and RH were also recorded at that time. Cuvette irradiance, carbon dioxide concentration, and atmospheric flow rate were set to 1000 μmol·m−2·s−1, 400 ppm (approximately outdoor ambient), and 500 μL·min−1, respectively. The outdoor air temperature, RH, and photoperiod on collection dates varied from 22.4 to 27.9 °C, 40% to 70%, and 13.25 to 15.5 h, respectively. Garruna-Hernandez et al. (2014) reported that C. chinense gS varied during the day and was highest between 1100 and 1300 hr; therefore, we only collected data between 1100 and 1300 hr. WUE was calculated by dividing Pn by E (Ou and Zou, 2012).

The experiment was organized in a completely randomized statistical design. Pn, E, gS, and WUE were dependent variables, and variety (33 levels), species of origin (5 levels), and indigenous habitat (3 levels) were independent variables (Table 1). Indigenous habitats were subjectively categorized as dry/desert, temperate, and tropical based on the climate in the country of origin (Table 1). Data were collected at six different times from a different leaf each time (198 total values each for Pn, E, gS, and WUE). Data were analyzed using an analysis of variance followed by mean separation (Tukey’s honestly significant difference and least significant difference; α < 0.05) using the SPSS statistical software package (IBM SPSS Statistics, version 24; IBM Corp., Armonk, NY). Pearson correlations among dependent variables were also determined.

Results

Pn varied from 3.6 to 3.7 for ‘Malawi Piquante’ and ‘Korean Long Green’ peppers to 16.3 μmol CO2/m2/s (fixed) for ‘Thai Hot’ peppers (Table 1). The gS varied from 0.01 to 0.59 for most varieties (Malawi, Korean Long Green, Antohi Romanian, Pakistan, Fatali, Tabasco Red, HIan Sweet Hot, Hungarian Sunshine, Red Roccoto, Moses Orange, Trinidad Moruga Scorpion, Jamaican Red Hot, and Apple Hungarian) to 0.28 mmol H2O/m2/s for Thai Hot pepper (Table 1). E varied from 0.43 to 0.59 for ‘Malawi Piquante’, ‘Korean Long Green’, and ‘Pakistan’ peppers to 4.14 and 4.21 mmol H2O/m2/s for ‘CGN 22091’ and ‘Peruvian Purple’ peppers, respectively (Table 1). WUE differed from 2.92 to 3.43 among three varieties to 5.10 to 7.20 for 16 other pepper varieties (Table 1). Tleaf varied from 27 °C for ‘Thai Hot’ and ‘Pepperoncini’ peppers to 33 °C for ‘Pakistan’, ‘Moses Orange’ and ‘Jamaican Red Hot’ peppers (Table 1). Cuvette RH differed from 38% for ‘Hawaiian Sweet’ peppers to 59% for ‘Thai Hot’ peppers (Table 1).

C. frutescens, C. baccatum, C. chinense, and C. pubescens derived varieties had lower Pn (4.5–8.6 μmol CO2/m2/s fixed) than C. annuum derived varieties (9.4 μmol CO2/m2/s fixed) (Table 1). There were no differences in gS, E, Tleaf, RH, or WUE among varieties based on parental species (Table 1). Varieties originating from temperate climates had lower Pn (8.0 μmol CO2/m2/s fixed) than those originating from dry regions (12.5 μmol CO2/m2/s fixed) (Table 1). Varieties from tropical regions had a lower cuvette RH (46% to 47%) than those from dry regions (56%) (Table 1) when tested in our experiment.

Pn was positively correlated with gS (Pearson correlation = 0.88), E (0.86), and RH (0.62), and it was negatively correlated with WUE (−0.35) (Table 2). The gS was positively correlated with E (0.95) and RH (0.56), and it was negatively correlated with Tleaf (−0.18) and WUE (−0.56) (Table 2). E was positively correlated with RH (0.44) and negatively correlated with WUE (−0.67) (Table 2). Tleaf was negatively correlated with gS (−0.18) and RH (−0.21) (Table 2). RH was negatively correlated with Tleaf (−0.21) (Table 2).

Table 2.

Pearson correlation between instantaneous photosynthetic rate (Pn), stomatal conductance (gS), transpiration rate (E), cuvette leaf temperature (Tleaf), and humidity after 5 min (RH) and water use efficiency (WUE; WUE = Pn/T).

Table 2.

Discussion

Capsicum Pn values varied more in our experiment (3.6−3.7 to 16.3 μmol CO2/m2/s fixed) than they did in other experiments reported by others; for example, Ou and Zou (2012) reported that the Pn of five Capsicum species varied from 15.8 to 21.8 μmol CO2/m2/s (fixed). Among pepper varieties within a species, Pn also varied more in our experiment than it did in others (Ghasemi et al., 2016; Rosado-Souza et al., 2015). Borisev et al. (2012) reported that the Pn of 10 C. annuum varieties differed from 14.5 to 16.6 μmol CO2/m2/s (fixed); the C. annuum variety Pn (22 varieties) in our work ranged from 3.7 to 16.3 μmol CO2/m2/s (fixed) (Table 1). Ridzuan et al. (2018) reported that the C. annuum variety/accession Pn differed from 11.5 to 19.1 μmol CO2/m2/s (fixed). In contrast, Hassan et al. (2014) reported that the C. annuum variety Pn ranged from 2.5 to 5.3 μmol CO2/m2/s (fixed; irradiance not reported). Pérez-Grajales et al. (2004) reported similar Pn rates (at a lower irradiance of 500 μmol/m2/s) for C. pubescens. Rosado-Souza et al. (2015) reported that the C. chinense accession Pn varied from 17 to 25 μmol CO2/m2/s (fixed).

Differences between our Pn values and others may have been related to the irradiance levels when Pn was measured, where plants were grown, or the number of varieties studied. For instance, irradiance in our work was at saturating photosynthetic levels (1000 μmol·m−2·s−1), whereas irradiance in other studies was undocumented or at 300 to 500 μmol·m−2·s−1. Because peppers are typically grown in the field, where they are routinely exposed to saturating irradiance levels, we believe that our data more accurately reflected actual field Pn. Furthermore, Pn can vary more for field-grown than for greenhouse-grown/controlled environment–grown Capsicum. Borisev et al. (2012) reported that the Pn of nine Capsicum varieties differed from 14.5 to 16.6 μmol CO2/m2/s (fixed), but that Pn differed from 12.8 to 18.7 μmol CO2/m2/s (fixed) when those same varieties were grown in the field. Furthermore, the greater variation in Pn in this study compared with that in some other studies may have occurred because we evaluated a greater number of varieties that were intentionally selected to represent a broad array of genetic and indigenous backgrounds.

Our data regarding the varieties derived from C. annuum included collectively higher Pn than the data regarding the varieties derived from other species. However, broad conclusions regarding which species have higher Pn should be made cautiously because abiotic factors can interact with species and affect Pn. For instance, Ou and Zou (2012) reported that the Pn of C. frutescens was higher than that of four other Capsicum species (21.8 vs. 15.8–17.7 μmol CO2/m2/s fixed) when plants were grown at 35 °C, but the Pn of C. pubescens was highest when plants were grown at 15 °C. In the same study, the Pn of C. baccatum and the Pn of C. pubescens were higher than that of three other Capsicum species when plants were drought-stressed. In contrast, Okunlola et al. (2017) reported that the C. chinense Pn was more drought-tolerant than the Pn of C. annuum or C. frutescens. The environment where a plant is grown or the water status of a plant when Pn data are collected can lead to different conclusions about which Capsicum species has higher Pn. Although varieties are reportedly derived from a species, many are interspecific hybrids (often unreported) (Petkova et al., 2014) and genetically related (Amarul J’unior et al., 2005). That hybridization alone may impact the photosynthetic or water use data. Petkova et al. (2014) showed that the Pn of four F1 pepper hybrids was more tolerant to high temperatures (33 to 35 °C) than that of parental species.

The range and gS values reported in our study (0.01–0.28 mmol H2O/m2/s) were less than those reported by others. Ridzuan et al. (2018) reported that the gS of the C. annuum variety (14) varied from 0.25 to 0.68 mmol H2O/m2/s. Hassan et al. (2014) reported that the gS of the C. annuum variety varied from 0.50 to 0.60 mmol H2O/m2/s. Differences between our gS data and that of others may have been related to the environments where plants were grown. For instance, plants grown at temperatures below 15 °C or above the optimal temperature for pepper Pn can decrease the Capsicum gS (Jaimez and Rada, 2016). Because the Tleaf data were collected on some days when the temperature was above the optimal temperature reported for Capsicum Pn (25 to 30 °C), the gS may have been impacted (Table 3).

Table 3.

Variation in instantaneous photosynthetic rate (Pn; μmol CO2/m2/s fixed), stomatal conductance (gS; mmol H2O/m2/s), transpiration rate (E; mmol H2O/m2/s), cuvette leaf temperature (Tleaf; °C), and relative humidity (RH; %) and water use efficiency (WUE; WUE = Pn/E) among 33 outdoor-grown pepper varieties.

Table 3.

Our data indicated that gS does not vary among domesticated Capsicum species (Table 1). Milla et al. (2013) also found that gS did not vary between wild-type and domesticated C. annuum or C. baccatum. Interestingly, we observed that gS differed among varieties derived from those species. Rosado-Souza et al. (2015) reported that the C. annuum variety gS differed. Furthermore, Kang et al. (2001) reported that the C. chinense variety gS differed. Yet, in both of those studies, the species gS did not differ. Similarly, Percy et al. (1996) showed that the gS of interspecific selections of cotton (Gossypium barbadense L) was higher than that of the parents or ancestral lines. Differences in the gS of varieties observed by us and others may have been due to the integration of a mutation into breeding programs over time and/or interspecific hybridization resulting in greater variations in gS than that observed for genetic parents. Furthermore, a recent study has shown a transgenerational effect on watercress (Lepidium sativum) gS; the maternal light environment effects on stomatal density and gS were expressed in seed-propagated progeny, suggesting that differences in gS in this experiment and in past experiments, to some degree, may be impacted by the environment in which seeds were produced (Vrablova et al., 2018). A similar relationship between the maternal water status and progeny WUE was also reported for Eucalyptus (Vivas et al., 2019).

The E values reported here also varied more than those reported by others, although the maximum E values were similar (3.21–4.05 mmol H2O/m2/s) (Ou and Zou, 2012). Ridzuan et al. (2018) reported that the E of the C. annuum variety differed from 4.61 to 7.11 mmol H2O/m2/s (indoor-grown). Furthermore, differences in E values in our work and that of others may have been related to where plants were grown. Borisev et al. (2012) reported that the E of Capsicum variety (nine) differed more for outdoor-grown than indoor-grown peppers (4.4–6.1 vs. 4.7–5.0 mmol H2O/m2/s, respectively).

In contrast to the Pn, E, and gS data presented here, the WUE values we observed (3.1–7.2) were similar to those reported by others for peppers grown in a controlled environment (3.9–6.8) (Ou and Zou, 2012). However, our values were generally higher than those reported by Borisev et al. (2012) who also reported that the WUE of indoor-grown C. annuum variety (nine) varied less than that of field-grown plants (3.2–3.5 and 2.3–3.9, respectively). The WUE of Capsicum is reportedly impacted by irradiance; WUE was higher when plants were grown under high irradiance (400 μmol·m−2·s−1; 2.2) compared to low irradiance (200 μmol·m−2·s−1; 1.8) (Fu et al., 2010). However, irradiance in our study was 1000 μmol·m−2·s−1; therefore, it would be considered high. Moreover, the negative correlation between Capsicum WUE and Pn that we observed agreed with the observations of Antony and Singandhupe (2004).

Ridzuan et al. (2018) reported that the C. annuum variety E and gSwere correlated with Pn, as we observed (0.55 and 0.87, respectively). However, Pn is not always correlated with gS. Yun and Ahn (2009) reported that increasing temperature and atmospheric CO2 concentrations increased the pepper Pn, but not the pepper gS. The strong correlation between pepper gS and Pn reported here (0.95) (Table 2) supports the assertion that gS limitations may reduce pepper Pn (Serrano et al., 2017). However, the observations of Yun and Ahn (2009) suggested that gS limitations on Pn may occur less if CO2 concentrations are increased, as is common for greenhouse-produced bell peppers (Dorais, 2003; Erwin and Gesick, 2017).

A negative correlation between gS and Tleaf was previously reported (r2 = 0.76) for cotton (G. barbadense L.–derived) (Radin et al., 1994), although that correlation was greater than what we observed here for pepper (Table 2). Interestingly, some have suggested that gS measurements obtained later in the afternoon (after 1300 hr) may be important when evaluating plants for higher yield based on gS; for instance, Rebetzke et al., (2003) recommended that wheat breeding projects should involve selected progeny with higher gS collected later in the day because gS collected later in the day correlated more with yield than gS collected earlier. Similarly, Radin et al. (1994) found that the cotton yield (related to Pn) was associated more with gS collected in the afternoon than in the morning, and that varieties with high yield under hot temperatures had higher gS in the afternoon, but not in the morning (Lu et al., 1997). We collected data when Pn and gS were highest during the day; whether Capsicum yield is associated more with gS collected at certain times of the day is not known.

Differences in outdoor environmental conditions for data collection dates during our experiment may have reduced the resolution of our experiment. Tleaf was higher on collection dates 3 and 4 (33.6 to 34 °C; over-reported Pn optima) than on other dates (27.7 to 29.6 °C) (Table 3). Furthermore, cuvette RH was higher on collection dates 2, 3, 4, and 5 (48% to 58%) than on collection dates 1 and 6 (40% to 43%) (Table 3). Because Tleaf and RH are correlated with Pn, gS, and E (Table 2), the environmental differences among collection dates may have impacted values.

Care should be taken when determining conclusions about plant photosynthesis or yield based on instantaneous Pn or water use data based on the leaf area per unit. Collecting data based on the leaf area per unit does not account for differences in the individual leaf area, plant leaf number, whole-plant leaf area, or whole-plant photosynthesis. Furthermore, instantaneous Pn data do not account for plant acclimation to changing environmental conditions (Hikosaka et al., 2006). Therefore, our study is of value because it compared photosynthetic and water use attributes of a larger number of pepper varieties at the same time of day and under the same environmental conditions simultaneously. Our study also demonstrated that outdoor-grown pepper variety photosynthetic and water use attributes vary more than previously reported, and that the reported parental species and indigenous habitat are associated with some photosynthetic and water use attributes.

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    • Export Citation
  • Palevitch, D. & Craker, L.E. 1995 Nutritional and medicinal importance of red pepper (Capsicum spp.) J. Herbs Spices Med. Plants 3 55 83

  • Percy, R.G., Lue, Z., Radin, J.W., Turcotte, E. & Zeiger, E. 1996 Inheritance of stomatal conductance in cotton (Gossypium barbadense) Physiol. Plant. 96 3 1662 1666

    • Search Google Scholar
    • Export Citation
  • Pérez-Grajales, M., González-Hernández, V.A., Mendoza-Castillo, M.C., Peña Valdivia, C., Peña-Lomelí, A. & Sahagún-Castellanos, J. 2004 Physiological characterization of manzano hot pepper (Capsicum pubescens R & P) landraces J. Amer. Soc. Hort. Sci. 129 88 92

    • Search Google Scholar
    • Export Citation
  • Petkova, V., Todorova, V. & Tomlekova, N. 2014 Efficiency of photosynthetic apparatus of sweet pepper (Capsicum annuum L.) F1 hybrids and their parental components in high temperature conditions. Plant Science (Bulgaria)

  • Qin, C., Changshui, Y., Shen, Y., Fang, X., Chen, L., Min, J., Cheng, J., Zhao, S., Xu, M., Luo, Y., Yang, Y., Wu, Z., Mao, L., Wu, H., Ling-Hu, C., Zhou, H., Lin, H., González-Morales, S., Trejo-Saavedra, D.L., Tian, H., Tang, X., Zhao, M., Huang, Z., Zhou, A., Yao, X., Cui, J., Li, W., Chen, Z., Feng, Y., Niu, Y., Bi, S., Yang, X., Li, W., Cai, H., Luo, X., Montes-Hernández, S., Leyva-González, M.A., Xiong, Z., He, X., Bai, L., Tan, S., Tang, X., Liu, D., Liu, J., Zhang, S., Chen, M., Zhang, L., Zhang, L., Zhang, Y., Liao, W., Zhang, Y., Wang, M., Lu, X., Wen, B., Liu, H., Luan, H., Zhang, Y., Yang, S., Wang, X., Xu, J., Li, X., Li, S., Wang, J., Palloix, A., Bosland, P.W., Li, Y., Krogh, A., Rivera-Bustamante, R.F., Herrera-Estrella, L., Yin, Y., Yu, J., Hu, K. & Zhang, Z. 2014 Whole-genome sequencing of cultivated and wild peppers provides insights into Capsicum domestication and specialization Proc. Natl. Acad. Sci. USA 111 14 1662 1666

    • Search Google Scholar
    • Export Citation
  • Radin, J.W., Lu, Z., Percy, R.G. & Zeiger, E. 1994 Genetic variability for stomatal conductance in Pima cotton and its relation to improvements of heat adaptation Proc. Natl. Acad. Sci. USA 91 7217 7221

    • Search Google Scholar
    • Export Citation
  • Rebetzke, G.J., Condon, A.G., Richards, R.A. & Farquhar, G.D. 2003 Gene action for leaf conductance in three wheat crosses Austral. J. Agr. Res. 54 4 1662 1666

    • Search Google Scholar
    • Export Citation
  • Ridzuan, R., Yusop, M.R., Yusof, M.M., Ismail, S.I., Miah, G. & Usman, M. 2018 Genetic diversity analysis of selected Capsicum annuum genotypes based on morpho-physiological, yield characteristics and their biochemical properties J. Sci. Food Agr. doi: 10.1002/jsfa.9169

    • Search Google Scholar
    • Export Citation
  • Rosado-Souza, L., Scossa, F., Chaves, I.S., Kleessen, S., Salvador, L.F., Milagre, J.C., Finger, F., Bhering, L.L., Sulpice, R., Araújo, W.L. & Nikoloski, Z. 2015 Exploring natural variation of photosynthetic, primary metabolism and growth parameters in a large panel of Capsicum chinense accessions Planta 242 3 1662 1666

    • Search Google Scholar
    • Export Citation
  • Russo, V.M. & Howard, L.R. 2002 Carotenoids in pungent and non-pungent peppers at various developmental stages grown in the field and glasshouse J. Sci. Food Agr. 82 615 624

    • Search Google Scholar
    • Export Citation
  • Serrano, L.L., Penella, C., Bautista, A.S., Galarza, S.L. & Chover, A.C. 2017 Physiological changes of pepper accessions in response to salinity and water stress Span. J. Agr. Res. 15 3 1662 1666

    • Search Google Scholar
    • Export Citation
  • Topuz, A. & Ozdemir, F. 2007 Assessment of carotenoids, capsaicinoids and ascorbic acid composition of some selected pepper cultivars (Capsicum annuum L.) grown in Turkey J. Food Compos. Anal. 20 596 602

    • Search Google Scholar
    • Export Citation
  • Vivas, M., Rolo, V., Wingfield, M.J. & Slippers, B. 2019 Maternal environment regulates morphological and physiological traits in Eucalyptus grandis For. Ecol. Mgt. 432 631 636

    • Search Google Scholar
    • Export Citation
  • Vrablova, M., Hronkova, M., Vrabl, D., Kubasek, J. & Santrucek, J. 2018 Light intensity-regulated stomatal development in three generations of Lepidium sativum Environ. Expt. Biol. 156 316 324

    • Search Google Scholar
    • Export Citation
  • Wahyuni, Y., Ballester, A.R., Sudarmonowati, E., Bino, R.J. & Bovy, A.G. 2011 Metabolite biodiversity in pepper (Capsicum) fruits of thirty-two diverse accessions: Variation in health-related compounds and implications for breeding Phytochemistry 72 1358 1370

    • Search Google Scholar
    • Export Citation
  • Yun, S. & Ahn, M. 2009 Effects on net photosynthesis in field-grown hot pepper responding to increased CO2 and temperature Korean J. Environ. Agri. 28 2 1662 1666

    • Search Google Scholar
    • Export Citation
  • Zewdie, Y. & Bosland, P.W. 2001 Capsaicinoid profiles are not good chemotaxonomic indicators for Capsicum species Biochem. Syst. Ecol. 29 161 169

  • Zhai, Y., Guo, M., Wang, H., Lu, J., Liu, J., Zhang, C., Gong, Z. & Lu, M. 2016 Autophagy, a conserved mechanism for protein degradation, responds to heat, and other abiotic stresses in Capsicum annuum L Front. Plant Sci. 7 131 doi: 10.3389/fpls.2016.00131

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Contributor Notes

The authors acknowledge and appreciate the financial support of the IRSIP Program of the Higher Education Commission of Pakistan, the Minnesota Agriculture Experiment Station, the Floriculture and Nursery Research Initiative administered by USDA-ARS, Society of Allied Florists American Floral Endowment (SAF/AFE), and the Horticulture Research Institute (HRI), and the Floriculture Research Alliance members who support University of Minnesota Research (Altman Plants, Rocket Farms, Green Circle Growers, and Smith Gardens).

J.E. is the corresponding author. E-mail: erwin001@umn.edu.

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  • Ou, L.J. & Zou, X.X. 2012 The photosynthetic stress responses of five pepper species are consistent with their genetic variability Photosynthetica 50 1 1662 1666

    • Search Google Scholar
    • Export Citation
  • Palevitch, D. & Craker, L.E. 1995 Nutritional and medicinal importance of red pepper (Capsicum spp.) J. Herbs Spices Med. Plants 3 55 83

  • Percy, R.G., Lue, Z., Radin, J.W., Turcotte, E. & Zeiger, E. 1996 Inheritance of stomatal conductance in cotton (Gossypium barbadense) Physiol. Plant. 96 3 1662 1666

    • Search Google Scholar
    • Export Citation
  • Pérez-Grajales, M., González-Hernández, V.A., Mendoza-Castillo, M.C., Peña Valdivia, C., Peña-Lomelí, A. & Sahagún-Castellanos, J. 2004 Physiological characterization of manzano hot pepper (Capsicum pubescens R & P) landraces J. Amer. Soc. Hort. Sci. 129 88 92

    • Search Google Scholar
    • Export Citation
  • Petkova, V., Todorova, V. & Tomlekova, N. 2014 Efficiency of photosynthetic apparatus of sweet pepper (Capsicum annuum L.) F1 hybrids and their parental components in high temperature conditions. Plant Science (Bulgaria)

  • Qin, C., Changshui, Y., Shen, Y., Fang, X., Chen, L., Min, J., Cheng, J., Zhao, S., Xu, M., Luo, Y., Yang, Y., Wu, Z., Mao, L., Wu, H., Ling-Hu, C., Zhou, H., Lin, H., González-Morales, S., Trejo-Saavedra, D.L., Tian, H., Tang, X., Zhao, M., Huang, Z., Zhou, A., Yao, X., Cui, J., Li, W., Chen, Z., Feng, Y., Niu, Y., Bi, S., Yang, X., Li, W., Cai, H., Luo, X., Montes-Hernández, S., Leyva-González, M.A., Xiong, Z., He, X., Bai, L., Tan, S., Tang, X., Liu, D., Liu, J., Zhang, S., Chen, M., Zhang, L., Zhang, L., Zhang, Y., Liao, W., Zhang, Y., Wang, M., Lu, X., Wen, B., Liu, H., Luan, H., Zhang, Y., Yang, S., Wang, X., Xu, J., Li, X., Li, S., Wang, J., Palloix, A., Bosland, P.W., Li, Y., Krogh, A., Rivera-Bustamante, R.F., Herrera-Estrella, L., Yin, Y., Yu, J., Hu, K. & Zhang, Z. 2014 Whole-genome sequencing of cultivated and wild peppers provides insights into Capsicum domestication and specialization Proc. Natl. Acad. Sci. USA 111 14 1662 1666

    • Search Google Scholar
    • Export Citation
  • Radin, J.W., Lu, Z., Percy, R.G. & Zeiger, E. 1994 Genetic variability for stomatal conductance in Pima cotton and its relation to improvements of heat adaptation Proc. Natl. Acad. Sci. USA 91 7217 7221

    • Search Google Scholar
    • Export Citation
  • Rebetzke, G.J., Condon, A.G., Richards, R.A. & Farquhar, G.D. 2003 Gene action for leaf conductance in three wheat crosses Austral. J. Agr. Res. 54 4 1662 1666

    • Search Google Scholar
    • Export Citation
  • Ridzuan, R., Yusop, M.R., Yusof, M.M., Ismail, S.I., Miah, G. & Usman, M. 2018 Genetic diversity analysis of selected Capsicum annuum genotypes based on morpho-physiological, yield characteristics and their biochemical properties J. Sci. Food Agr. doi: 10.1002/jsfa.9169

    • Search Google Scholar
    • Export Citation
  • Rosado-Souza, L., Scossa, F., Chaves, I.S., Kleessen, S., Salvador, L.F., Milagre, J.C., Finger, F., Bhering, L.L., Sulpice, R., Araújo, W.L. & Nikoloski, Z. 2015 Exploring natural variation of photosynthetic, primary metabolism and growth parameters in a large panel of Capsicum chinense accessions Planta 242 3 1662 1666

    • Search Google Scholar
    • Export Citation
  • Russo, V.M. & Howard, L.R. 2002 Carotenoids in pungent and non-pungent peppers at various developmental stages grown in the field and glasshouse J. Sci. Food Agr. 82 615 624

    • Search Google Scholar
    • Export Citation
  • Serrano, L.L., Penella, C., Bautista, A.S., Galarza, S.L. & Chover, A.C. 2017 Physiological changes of pepper accessions in response to salinity and water stress Span. J. Agr. Res. 15 3 1662 1666

    • Search Google Scholar
    • Export Citation
  • Topuz, A. & Ozdemir, F. 2007 Assessment of carotenoids, capsaicinoids and ascorbic acid composition of some selected pepper cultivars (Capsicum annuum L.) grown in Turkey J. Food Compos. Anal. 20 596 602

    • Search Google Scholar
    • Export Citation
  • Vivas, M., Rolo, V., Wingfield, M.J. & Slippers, B. 2019 Maternal environment regulates morphological and physiological traits in Eucalyptus grandis For. Ecol. Mgt. 432 631 636

    • Search Google Scholar
    • Export Citation
  • Vrablova, M., Hronkova, M., Vrabl, D., Kubasek, J. & Santrucek, J. 2018 Light intensity-regulated stomatal development in three generations of Lepidium sativum Environ. Expt. Biol. 156 316 324

    • Search Google Scholar
    • Export Citation
  • Wahyuni, Y., Ballester, A.R., Sudarmonowati, E., Bino, R.J. & Bovy, A.G. 2011 Metabolite biodiversity in pepper (Capsicum) fruits of thirty-two diverse accessions: Variation in health-related compounds and implications for breeding Phytochemistry 72 1358 1370

    • Search Google Scholar
    • Export Citation
  • Yun, S. & Ahn, M. 2009 Effects on net photosynthesis in field-grown hot pepper responding to increased CO2 and temperature Korean J. Environ. Agri. 28 2 1662 1666

    • Search Google Scholar
    • Export Citation
  • Zewdie, Y. & Bosland, P.W. 2001 Capsaicinoid profiles are not good chemotaxonomic indicators for Capsicum species Biochem. Syst. Ecol. 29 161 169

  • Zhai, Y., Guo, M., Wang, H., Lu, J., Liu, J., Zhang, C., Gong, Z. & Lu, M. 2016 Autophagy, a conserved mechanism for protein degradation, responds to heat, and other abiotic stresses in Capsicum annuum L Front. Plant Sci. 7 131 doi: 10.3389/fpls.2016.00131

    • Search Google Scholar
    • Export Citation
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