Impacts of Elevated Carbon Dioxide and Temperature on Physicochemical and Nutrient Properties in Strawberries
Strawberry (Fragaria x ananassa Duch.) is one of the most popular edible fruit worldwide. Strawberries are generally cultivated in open fields or under protected cropping, and are available all year round. Consumers prefer fruit with a bright red color, sweet taste, and distinct aroma. Over the past two decades, strawberry has shown one of the highest growth rates in terms of fresh fruit consumption. Such increment in consumer demand for strawberry could be attributed to its high nutrient content and perceived health benefits. Phenolic compounds and vitamins are the main antioxidants in the strawberry phytochemical profile. However, the predicted climate changes in the near future are expected to cause major challenges in modern agriculture due to its significant potential negative impacts on both quantity and quality of various crops, including strawberry. Increasing atmospheric CO2 levels and ambient temperature are the key factors in a changing climate scenario. The effects of either high CO2 or high temperature on growth, development, yield, and quality of strawberry plant has been relatively well-investigated. However, information on the effects of combined high CO2 and temperature on strawberry is lacking. This review will examine the literature available about the relationship between climate changes and strawberry production and quality, and address the information needed in the future research in this area.
Antioxidants, Biological availability, Climate change, Polyphenolic compounds, Quality
Climate change is considered to be the most serious global challenge faced by humanity today . It is predicted to cause varying degrees of negative impacts across agro-ecosystems of the world and is flagged as a major threat to global food production systems as we know them. Rapidly rising greenhouse gases such as carbon dioxide (CO2) caused by various human activities appears to be altering the global climate. In particular, rainfall distribution and frequency, due to heating of Earth's surface, oceans, and atmosphere . Based on global climate modelling atmospheric CO2 concentrations may increase over 1000 ppm, and the global surface temperature may also increase by 2.5 °C to 7.8 °C by the end of the 21st-century . These environmental factors, individually and in combination, are expected to have significant impacts on crop growth, development and production. For example, increased CO2 levels have been reported to enhance plant photosynthesis and water use efficiency, but to reduce transpiration and there by directly affecting growth and yield. On the other hand, higher temperature levels have reduced plant photosynthesis, increased transpiration, and interestingly, shortened crop cycles . However, it should be noted that the effects of climate change on crops quality and quantity may also be affected by a range of other factors, including region , crop species, harvestable yield components, and crop management .
Strawberry is one of the most nutritious fruits which can supplement high contents of micro-nutrients including phenolic compounds and vitamins into human diets. Over the past decade, significant changes have been attributed to strawberry production areas in the world due to climate change [6-10]. This paper discusses the importance of strawberry as a micronutrient rich fruit in the human diet, and reviews the independent and combined effects of high CO2 and high temperature on growth, development, production, and nutritional quality of strawberries. Further, it attempts to identify the current gaps in knowledge and future research directions in order to develop strategies for maintaining the quality and productivity of strawberries under future anticipated environmental changes. This review is an initial milestone in a current PhD research project at the University of Melbourne to define the optimum combined high CO2 and temperature for good strawberry quality and quantity.
Strawberry is one of the commonest and highly demanded edible fruits, produced worldwide. It is a member of the family Rosaceae and belongs to the genus Fragaria which refers to fragrant in Latin. There are two types of strawberries: wild and cultivated. The wild European strawberry is F. vesca L., whereas F. ananassa Duch. is the cultivated type among the 23 Fragaria species .
Strawberry is a perennial herb with a prostrate growth habit, which prefers a cool and moist climate  and requires full sun for optimum growth performance. It prefers well-drained soils with an optimal pH range from 5.3 to 6.5. Among all soft fruits, strawberry is considered as the most economically important fruit, with its very high crop production value per ha . The world leading strawberry producers in 2013 were China, the USA, Mexico, Turkey, and Spain. The total global annual strawberry production was around 7.7 million tons produced on 361,662 ha . The Food and Agriculture Organization (FAO) data show that global strawberry production has more than doubled in the last 2 decades from 3.2 million tons in 1993.
Common quality parameters of strawberry involve consumer acceptance of color, size, shape, firmness, and flavor as perceived by the combination of taste and aroma. Good-quality strawberries have high sugar and aroma levels, along with acid balance and preferred physical properties like color and firmness. It has been reported that strawberry flavor depends on the content of sucrose, glucose, and fructose, which are the organoleptic factors of sweetness . Additionally, the higher sugar concentration, acid balance, active aromatic volatile composition, and polyphenols contents contribute to aroma and flavor. Organic acids like citric acid and malic acid mainly create fruit sourness and alter fruit colour by affecting pH and anthocyanin compounds . The physicochemical characteristics of strawberry also change during fruit maturity. Total soluble solids (TSS)/titratable acidity (TA) ratio (TSS/TA), and levels of sucrose, glucose, fructose, and malic acid increase with maturity, while TA and citric acid levels decrease . Data on the composition of strawberry based on the country of origin are shown in Table 1. A considerable variation could be found in the Table 1 due to the genetic differences, environmental conditions, pre and postharvest management practices and the methods of analysis used.
Health benefits of strawberry antioxidants
Strawberries are rich in natural antioxidant compounds, including polyphenols and vitamins (vitamin C and folate). Phenolic compounds are diverse in content and include; flavonoids, phenolic acids, lignans, stilbenes, tannins, and coumarins (Table 2) and accounts for numerous health benefits . Among selected popular fruits, strawberry shows the second highest polyphenol content of 146 mg/100 g after blueberries (445 mg/100 g) and is higher than orange and apple . The level of total phenols in strawberry could vary between 43 and 273 mg/100 g fresh weight (FW) . Due to this highly nutritious features, strawberry extracts has been recently consumed as an ingredient in functional foods and dietary supplements as a human health promoting agent .
Strong research evidence on health benefits of strawberry has been well-documented through the outcomes of numerous recent epidemiological and clinical studies [19-21]. Strawberry products were used as the main dietary supplement in those studies and were tested using either in-vitro cell cultures or in-vivo in humans or animals [19,22].
The in-vitro effect of strawberry extract on the inhibition of α-amylase was studied by McDougall, et al.  and they concluded that strawberry polyphenols show an antidiabetic effect by limiting post-meal blood glucose levels, and they confirmed the antidiabetic properties recorded earlier by Bordonaba and Terry . Therefore, strawberry could be a good source to prevent and treat metabolic complications related to diabetes as further confirmed by Moazen, et al.  who investigated the impact of freeze-dried strawberry supplementation in patients with type 2 diabetes. Another study by Abdulazeez  tested the effect of freeze-dried strawberry powder in diabetic rats and observed a significant reduction in serum lipid profile up to the control condition. The effect of strawberry phytochemicals on neuronal structure and function has also been tested . Importantly, the rich polyphenol profile of strawberries caused a marked reduction in oxidatively induced neurotoxicity in general. Further, Heo H and Lee C  reported that strawberry exhibited the highest cell protective ability over banana and orange. Strawberry anthocyanins were the major contributors that performed higher protective effects. More recently, Amatori, et al.  demonstrated that a polyphenol-rich strawberry extract (PRSE) was able to decrease the cellular viability of breast cancer cells in-vitro and in-vivo in a time- and dose-dependent manner.
Strawberry response to environmental changes
Strawberry is a C3 species and plants with the C3 photosynthetic pathway respond favourably to increases in atmospheric CO2 concentrations. As a result, CO2 enrichment of horticultural crops, including strawberry, grown in protected production systems is gaining interest, mostly in temperate regions during winter through spring to increase yields . Further, strawberry is highly sensitive to the ambient temperature, importantly the day and night temperatures. Photoperiod and number of other environmental factors including management greatly influence the growth and productivity of strawberries; which however, are not addressed here. This review has focused on impacts of the two main climate change variables, i.e. CO2 and temperature on yield and quality of fresh strawberries at harvest, but it does not cover the effects of those two parameters during storage/preservation.
Effect of Elevated Carbon Dioxide on Strawberries
Effect on photosynthesis
Photosynthesis is a primary physicochemical process which drives the dry matter accumulation and synthesis of plant organic compounds. Experimental outcomes to date clearly demonstrate that net photosynthesis of strawberry plants increases under enhanced CO2 levels compared to normal atmospheric levels [29-34]. The average effect of CO2 enrichment on strawberry resulted in 73% and 55% increase in net photosynthesis and 43% and 63% increase in overall plant dry biomass, respectively, at 300 ppm and 600 ppm of atmospheric CO2 . The large variation in photosynthetic response to elevated CO2 appears to be the result of various factors, including CO2 concentration (400 to 1000 ppm), duration of exposure to a particular CO2 level, fruiting period, method of CO2 enrichment, growth medium, space availability to plant growth, cultivar, nutrient and water application, and other growth conditions including light and temperature.
Any CO2 levels above the normal ambient CO2 concentration increased net photosynthetic rate of strawberries [30,32,36]. Overwintering strawberry plants grown under 700 ppm to 1000 ppm had nearly 50% higher leaf photosynthetic rates compared to the plants grown under ambient CO2 levels of 360 ppm to 390 ppm . Increased rates of photosynthesis generally results in greater dry matter accumulation which in turn support extensive and rapid growth of strawberry plants in spring. Leaf photosynthetic rates strongly correlated with leaf age, therefore, leaf age appeared to have significant influence on photosynthetic responses to elevated CO2 levels. For example, greater improvements in photosynthetic rates at 450 ppm to 900 ppm CO2 concentrations were observed primarily in younger leaves, while the older leaves showed an increase in net photosynthesis rate only up to 600 ppm. The negative or lack of response in photosynthesis in older leaves at higher CO2 levels greater than 600 ppm was attributed to photo-inhibition at higher CO2 concentrations [32,36].
Effect on yield
Increased CO2 in the growth environment is reported to improve the fruit yield of strawberry crops . Increases in yield under elevated CO2 were due to increases in either individual fruit weights [15,33] or the number of fruits per plant  or both . The same authors reported that strawberry plants exposed to higher CO2 levels during growth and development had enhanced photo assimilation which promoted development of branch crowns, pedicels, and flower bud differentiation , with increased flowering and more fruits per plant, consequently resulting greater total fruit yield.
Enriched CO2 concentrations of 450, 600, 750, and 900 ppm, in comparison with 300 ppm, enhanced strawberry fruit productivity due to increased pedicel number per plant, fruit setting per pedicel, fruit size, dry matter content of the fruits, and an increase in average fruit yield per plant of 0.7, 2.7, 3.6, and 4.1 fold, respectively . An increase in strawberry yield of 62% at higher CO2 concentrations (700-1000 ppm) was reported due to increased number of flowers and fruits compared with plants grown at ambient concentrations of CO2 . However, the increment in strawberry fruit yields at high CO2 levels have also been attributed to increased individual fruit dry matter content [15,33] and increased fruit set .
Effect on fruit flavor
Flavor and aroma of strawberries are important factors in determining consumer acceptability. Strawberries produce complex mixtures of volatile compounds including more than 100 esters, as well as alcohols, aldehydes and also sulphur containing compounds. Many of those compounds determine the unique strawberry aroma and contribute directly to the characteristic strawberry flavor .
The major volatile aromatic compounds, such as ethyl hexanoate, ethyl butanoate, methyl hexanoate, methyl butanoate, hexyl acetate, hexyl hexanoate, methyl methanoate, butyl acetate, methyl acetate, furaneol, linalool, and methyl octanoate, have been identified and analyzed in strawberries . Fruits grown under higher CO2 levels contained significantly greater levels of flavor compounds compared to the fruits under normal CO2 levels. The concentrations of ethyl hexanoate, ethyl butanoate, and methyl hexanoate increased by 48%, 35%, and 68%, respectively, at the highest CO2 level (950 ppm). Moreover, CO2 at 950 ppm lowered organic acid (citric and malic) contents by 17% and increased total sugar to organic acids ratio by 40%, which represents a reduction in fruit sourness. Similarly, Chen, et al. [36-38] observed improved strawberry fruit quality at enriched CO2 concentrations due to higher sugar accumulation and sugar/acid ratios in fruits as a result of decreased titratable acid content. Moreover, the higher CO2 levels (600 and 900 ppm) raised non-structural carbohydrate production efficiency of strawberry plants compared to 300 ppm . Penuelas and Estiarte  has discussed the increases in carbon-based secondary or structural compounds concentrations (CBSSC) like phenols with risen atmospheric CO2 concentrations. Increments in CBSSC could be a result of highly regulated plant defensive change in biosynthesis pathways to response external abiotic changes such as elevated CO2 levels .
Finally, it appears that strawberry flavor and aroma increase with rising CO2 levels, thereby increasing the eating quality of the fruits.
Effect on antioxidant compounds
In common with many other plant constituents discussed so far the antioxidant content of strawberry increased at CO2 levels of 650 and 950 ppm compared to the ambient conditions .
Flavonoids identified in strawberry fruits include pelargonidin 3-glucoside, cyanidin 3-glucoside, p-coumaroylglucose, pelargonidin 3-glucoside-succinate, and dihydroflavonol. Their levels increased by 72%, 105%, 76%, 110%, and 269%, respectively, at 950 ppm of CO2  compared with those at ambient CO2 level. Moreover, the increased CO2 promoted ascorbic acid/dehydroascorbic acid (AA/DHA) ratio and GSH/GSSG (oxidized GSS) ratio which are associated with increased free radical scavenging capacity. The increase in antioxidant compounds may be due to enhanced metabolism and production of antioxidant compounds as a result of greater availability of carbohydrate reservoir. Fruits exposed to the 950 ppm CO2 concentration exhibited the highest antioxidant capacity compared to fruit treated with ambient CO2 concentrations.
A summary of various studies on the effect of elevated CO2 concentration on strawberry yield and quality is presented in Table 3. In general, those results support the proposition that, in the future, strawberry plants grown under higher CO2 environments will produce high yields of high-quality strawberries.
Effect of High Temperature on Strawberries
Effect on growth and yield
Temperature is a key environmental variable that affects strawberry plant growth and development and is identified as a limiting factor in crop productivity depending on the geographical location and the season of year . Strawberry is highly sensitive to day and night temperatures and their interactions with other environmental factors, especially photoperiod. Therefore, in temperate regions, strawberry production is seasonal and concentrated in the warmer months under traditional open field cultivation systems. However, production can be extended to year-round using different varieties and planting techniques and particularly if produced using protected cropping techniques . Higher temperatures alter morphological, anatomical, physiological, and ultimately, biochemical and molecular changes in strawberry plants . In addition, the temperature response can be highly dependent on the genetic make-up or cultivar of strawberry grown.
Mean temperatures between 15 °C to 23 °C have been identified as optimum for strawberry photosynthesis depending on cultivar . However, different studies have proposed different day/night temperatures as the best for strawberry growth; such as 30/25 °C ., or 25/12 °C . Another study by Palencia, et al.  indicated that temperatures higher than 20 °C decreased the yields, while growth and yield were drastically reduced at temperatures above 35 °C .
High temperatures reduced strawberry fruit size, weight, and caused irregular shaped fruit [44-46]. The reduced fruit size and weight can be attributed to lower dry matter accumulation due to higher fruit transpiration rate and decreased photosynthetic rates at higher temperatures . Generally, cooler day/night temperatures favored plant and fruit growth, while rising temperatures resulted in smaller irregular shaped fruits. In a study by Wang S and Camp , strawberries grown at various day/night temperatures (18/12 °C, 25/12 °C, 25/22 °C, and 30/22 °C) in growth cabinets showed that a day/night temperature of 30/22 °C negatively affected plant growth, fruit development and fruit quality of strawberry cultivars. The fruit weights reduced by 10%, 33% and 66% at day/night temperatures of 25/12 °C, 25/22 °C, and 30/22 °C, respectively, compared to 18/12 °C. Maintaining temperature at 40/35 °C caused complete absence of fruit formation and zero yield .
Effect on photosynthesis
Although the light dependent reactions of photosynthesis are not sensitive to temperature the light-independent reactions catalysed by enzymes are. In general, the rate of reaction increases as temperature increases and reaches an optimum after which the overall rate declines. As the temperature continues to increase enzymes are denatured until all activity stops . Depending on cultivar, temperature rises of 10 °C to 15 °C could cause reversible alteration in photosynthesis (PS), however, fluctuations below or above this level may cause irreversible damage to the photosynthetic system . In strawberries, higher day/night temperatures (40/35 °C) appeared to cause detrimental and irreversible damage to PS II as indicated by chlorophyll fluorescence and PS II efficiency measurements .
Net photosynthesis rate in strawberries decreased with increasing temperatures (20/15 °C, 30/25 °C, and 40/35 °C) and the response was cultivar-dependent. When 2 varieties, "Sweet Charlie" and "Chandler", were exposed to these increasing day/night temperatures, net photosynthetic ratedecreased by 44% and 20%, respectively, in "Sweet Charlie" and "Chandler" at the highest day/night temperatures (40/35 °C) over those exposed to 20/15 °C and 30/25 °C . Additionally, the higher day/night temperatures of 30/25 °C and 40/35 °C had a major effect on stomatal and mesophyll conductance, transpiration, water use efficiency, and it reduced chlorophyll content [43,44]. "Sweet Charlie" and "Chandler" varied in their response to elevated temperature with "Chandler" displaying higher tolerance than "Sweet Charlie". Chandler plants were less sensitive to short term exposure to high temperatures and were able to maintain a significantly higher net CO2 assimilation rate, intercellular CO2 concentration, and water use efficiency for at least 3 weeks in higher day/night temperatures .
Overall, higher temperatures appear to have negative impacts on strawberry photosynthesis and there by plant growth and development. However, strawberry response to variations in temperature is cultivar-dependent. Identification and development of heat-tolerant strawberry cultivars will be essential to enable strawberry producers to adapt to the anticipated climatic changes, particularly increased temperature and CO2 levels.
Effect on fruit development and sugar content
As high temperatures can have a significant negative impact on the vegetative growth of strawberry plants, it is anticipated that high temperatures will also have a detrimental effect on the reproductive development of strawberry. It has been reported that heat stress under high temperatures can cause sterility, lower fruit set, there by lower yields, and in extreme cases complete crop failure [9,43,49]. High temperatures can have detrimental effects on fruit size, shape, yield, color, texture, flavor, nutritional composition, and nutrient content. Consequently, increasing temperatures may reduce strawberry development significantly and lower fruit quality substantially.
Higher temperatures could also affect fruit quality by reducing sweetness . The sweetness of strawberry is directly related to the sugar content of fruit flesh including glucose, fructose, and sucrose. Fruits produced at 30/22 °C (day/night) showed lower sugar and total carbohydrate contents than fruits from plants grown at 18/12 °C, 25/12 °C and 25/22 °C . Consequently, strawberry production at higher temperatures may have a negative impact on the flavor of strawberries.
Effect on antioxidants
Ascorbic acid and total organic acids, including ellagic acid content, showed a significant decline in strawberry fruits as day/night temperatures increased from 18/12 °C to 25/12 °°C, 25/22 °C and 30/22 °C . A substantial increase in phenolic compounds in strawberries grown at the higher day/night temperature (30/22 °C) was documented by . It appears that strawberries grown at warmer day/night temperatures (30/22 °C and 22/25 °C) produce more antioxidants as a defence mechanism in response to the applied stress. In support of this view, strawberries grown at 30/22 °C had greater amounts of phenolic acids, flavonols, and anthocyanins than those grown at lower temperatures . The level of the response was cultivar-dependent, with the cultivar "Kent" showing higher antioxidant levels as well as greater antioxidant capacity compared with "Earliglow" fruit . Although sweetness of strawberry fruit is reduced when the environments become warmer, the fruits will have high nutritional value due to the increased phenolic compounds and higher antioxidant activity. However, strawberries grown under warmer conditions will have reduced yields, due in part to small and uneven-sized fruit which will make them unattractive to producers and consumers . If this is the case then there may be opportunities to utilize the fruit for high antioxidant value-added processed products.
Effect on fruit color
Strawberry fruit color is a key fruit-intrinsic visual cue that consumers use to decide fruit quality before they buy or eat. An attractive fruit appearance with dark red color and higher flesh pigment intensity were exhibited by fruits which developed at a higher growth temperature (30/22 °C) [45,50]. It was suggested that increased polyphenolic compounds, especially anthocyanin, may make the strawberries redder and cause darker fruit surfaces . However, it should be noted that results of Kadir  were in disagreement and showed reduced fruit skin color intensities at high temperature (30/25 °C). Such contradiction in these reported results may be attributed to various factors, other than temperature, including cultivars and other growth conditions. From a consumer perspective, colour alone is insufficient to determine consumer preferences for strawberry fruit without acceptable fruit size and shape. Consequently, when judging the impact of climate change on strawberry fruits, changes in all quality traits need to be considered.
Effect on proteins
Plant proteins are important macromolecules involved in every stage of plant growth and development, including biological reactions (enzymes) and cellular, structural, and membrane transport systems. Some studies reported that protein synthesis and final total protein content declined significantly in plants grown at high temperatures of 33 °C and 42 °C . Although the typical cellular protein content decreased at higher growth temperatures, new heat-shock proteins were synthesized as a result of imposed heat stress in strawberry leaves and flowers. The detected stress proteins were cultivar-and temperature-dependent with substantial differences in the level of expression between the cultivars "Nyoho" and "Toyonaka" . The newly synthesized heat-shock proteins could act as protectors (molecular chaperones) in preventing thermal aggregation of denatured proteins due to high temperatures and thermal stress [51,52].
Another response to high temperature stress is the production of reactive oxygen species (ROS) which can cause significant damage to cells. Plant peroxidases can detoxify ROS in the presence of H2O2. Peroxidase activity has been observed to increase in strawberry plant cells subjected to heat stresses there by providing some protection from oxidative damage to cells . The impact of heat on stress-protein production was analysed by Gulen and Eris  in 2 ways; with gradual growth temperature increases in 5 °C increments from 25 °C to 45 °C, and by imposing heat shocks. Both treatments showed a significant increase in peroxidase activities against ROS. The strawberry plants exposed to gradual, incremental increases in temperature had greater heat-stress tolerance due to the synthesis of more new heat stable proteins than the plants that received a sudden shock heat-stress. Therefore, strawberry plants may cope with future warmer environments by acclimatizing to rising temperatures through the production of enzymatic antioxidants. Furthermore, strawberry plants subjected to sudden heat events also have the capacity to respond and produce protective proteins, but at a reduced rate.
The reported positive and negative effects of high temperatures on strawberries are summarized in Table 4.
Interactive Effect of CO2 and Temperature on Strawberry Physicochemical Properties
Many studies have shown that strawberries respond differently to increases in temperature than to higher CO2 levels when they are applied independently. Higher yields and better-quality strawberries were recorded under higher CO2 levels, while high temperatures reduced yield and fruit quality. However, both factors caused a similar response in increasing fruit polyphenol contents. Strawberry plants produced higher-quality fruits at lower temperatures (Table 4). Despite some very good research demonstrating the independent effect of increased temperature and CO2, the combined impact of anticipated future increases in both, due to climate change, on strawberry growth and development is unclear.
The magnitude of the effects of individual CO2 or temperature factors on the strawberry can be considerably different from their combined effects. To our knowledge, only one study has reported the combined effects of both elevated CO2 and temperature on strawberry. Sun, et al.  observed decreased fruit yields of 12% to 35% at high CO2 (720 ppm) and high temperature (25/20 °C). Plants grown at high CO2 and low temperatures produced the highest fruit yields, while fruit number per plant and the yield decreased as CO2 and temperature increased. They proposed that yield reduction may be due to lower fruit set, decreased carbohydrate metabolism during flowering, inhibition of flower induction, a smaller number and size of inflorescences, and decreased pollen viability. In addition, high CO2 levels combined with high temperatures reduced anthocyanins by 27%, total flavonoids by 31% to 36%, and antioxidant capacity by 18% to 28% in strawberry fruits .
Future Research Needs
Information on the combined effects of elevated CO2 levels and temperature on strawberry growth and development, particularly berry yield, quality, and nutritional value is lacking. Therefore, it is important to investigate the effect of combined CO2 and temperature at the levels anticipated to result from climate change, particularly the physical, chemical, and nutritional properties of different strawberry cultivars. Additionally, studies on the impact of climate changes on nutritional and health value of strawberry fruits in terms of bio-accessibility or bioavailability is virtually unresearched. Such information will be helpful to develop adaptation strategies to reduce the yield losses for commercial strawberry producers under future climates. It has been well documented that the responses of strawberries to different climatic conditions are variety-dependent so existing strawberry varieties which thrive under adverse climatic conditions should be identified for their tolerance to climate change through selection and breeding.
Strawberry is widely consumed globally, is highly nutritious and is a major source of vitamin C, folate, dietary polyphenols, and antioxidants. Its total Antioxidant Capacity is greater than the most common fruits including plum, orange, red and white grape, kiwi, pink grapefruit, banana, apple, tomato, pare honey dew and melon. However, strawberry is highly sensitive to growth temperature and CO2 levels. For example, increases in CO2 concentrations enhanced photosynthesis, fruit size and numbers, overall fruit yield, flavour compounds, and antioxidant contents. On the contrary, high temperature reduced strawberry yield, photosynthesis, plant development, and fruits characteristics (size, shape, colour, flavour, and nutrients composition). Although the individual effects of high CO2 and high temperature on strawberry growth, quality, and nutritional composition are relatively well-studied, the interactive effects of temperature and atmospheric CO2 particularly at evaluated levels above the normal average conditions, on strawberry growth, productivity and quality lacking.
This is particularly important as the global warming due to elevated CO2 is said to be a reality; therefore, such information on the combined effects of high CO2 and high temperature levels during crop growth and development on strawberry quantity and quality will be of great benefit for understanding mechanisms behind the responses and in developing research strategies to overcome negative impacts while maximising the gains from any potential positive responses. The anticipated results from research currently being conducted in this area at The University of Melbourne will contribute towards achieving the above objectives, and eventually leading to generate knowledge, technology and best management practices, so strawberry industry could prepare and to adapt to the anticipated changes in climate and weather patterns.
- IPCC (2014) Climate change 2014 synthesis report, summary for policymakers.
- Cicerone RJ, Nurse P (2014) Climate change evidence and causes. An overview from the Royal Society and the US National Academy of Sciences, Washington, DC.
- Qaderi MM, Reid DM (2009) Crop responses to elevated carbon dioxide and temperature. In: SN Singh, Climate change and crops. Springer Berlin Heidelberg.
- Martin Parrya, Cynthia Rosenzweigb, Ana Iglesias, et al. (1999) Climate change and world food security: A new assessment. Glob Environ Chang 9: S51-S67.
- Jørgen E Olesena, Marco Bindib (2002) Consequences of climate change for european agricultural productivity, land use and policy. Eur J Agron 16: 239-262.
- Calleja EJ (2011) The potential impacts of climate change on diseases affecting strawberries and the UK strawberry industry. University of Warwick.
- Esitken A, Ercisli S, Yildiz H, et al. (2008) Does climate change have an effect on strawberry yield in colder growing areas? Workshop on Berry Production in Changing Climate Conditions and Cultivation Systems. COST-Action 863: Euroberry Research: from Genomics to Sustainable Production, Quality and Health.
- Davide Neri, Gianluca Baruzzi, Francesca Massetani, et al. (2012) Strawberry production in forced and protected culture in Europe as a response to climate change. Can J Plant Sci 92: 1021-1036.
- Pedro Palencia, Fátima Martínez, Juan Jesús Medina, et al. (2013) Strawberry yield efficiency and its correlation with temperature and solar radiation. Hortic Bras 31.
- Palencia P, Martinez F, Medina JJ, et al. (2009) Effects of climate change on strawberry procuction. Workshop on berry production in changing climate conditions and cultivation Systems. COST-Action 863: euroberry research: from genomics to sustainable production, quality and health, Germany.
- Nirmal K Sinha (2008) Strawberries and raspberries. In: Nirmal K Sinha, Jiwan S Sidhu, József Barta, James SB Wu, M Pilar Cano, Handbook of Fruits and Fruit Processing. Wiley-Blackwell, USA, 581-589.
- Hummer K (2008) Global conservation strategy for Fragaria (strawberry). International Society for Horticultural Science (ISHS), Leuven, Belgium.
- (2014) Food and Agriculture Organization Corporate Statistical Database (FAOSTAT).
- Shiow Y Wang (2007) Antioxidant capacity and phenolic content of berry fruits as affected by genotype, pre-harvest conditions, maturity and post-harvest handling. In: Yanyun Zhao, Berry fruit: Value-added products for health promotion. CRC Press, Boca Raton, 147-186.
- SY Wang, JA Bunce (2004) Elevated carbon dioxide affects fruit flavor in field-grown strawberries (Fragaria×ananassa Duch). J Sci Food Agric 84: 1464-1468.
- Menager I, Jost M, Aubert C (2004) Changes in physicochemical characteristics and volatile constituents of strawberry (cv. Cigaline) during maturation. J Agric Food Chem 52: 1248-1254.
- Basu A, Nguyen A, Betts N, et al. (2014) Strawberry as a functional food: An evidence-based review. Crit Rev Food Sci Nutr 54: 790-806.
- Williamson G, Holst B (2008) Dietary reference intake (DRI) value for dietary polyphenols: Are we heading in the right direction? Br J Nutr 99: S55-S58.
- Giampieri F, Forbes-Hernandez T, Gasparrini M, et al. (2015) Strawberry as a health promoter: An evidence based review. Food Funct 6: 1386-1398.
- Mazzoni L, Perez-Lopez P, Giampieri F, et al. (2016) The genetic aspects of berries: From field to health. J Sci Food Agric 96: 365-371.
- Paredes-Lopez O, Cervantes-Ceja ML, Vigna-Perez M, et al. (2010) Berries: Improving human health and healthy aging, and promoting quality life-a review. Plant Foods Hum Nutr 65: 299-308.
- Bordonaba JG, Terry LA (2011) Strawberry. In: Terry LA, Health-promoting properties of fruit and vegetables. CAB International, Oxfordshire, UK, 291-320.
- McDougall G, Shpiro F, Dobson P, et al. (2005) Different polyphenolic components of soft fruits inhibit α-amylase and α-glucosidase. J Agric Food Chem 53: 2760-2766.
- Moazen S, Amani R, Homayouni Rad A, et al. (2013) Effects of freeze-dried strawberry supplementation on metabolic biomarkers of atherosclerosis in subjects with type 2 diabetes: A randomized double-blind controlled trial. Ann Nutr Metab 63: 256-264.
- Sheriff Sheik Abdulazeez (2015) Freeze dried strawberry powder ameliorates alloxan induced hyperlipi-demia in diabetic rats. Biomed Res 26: 77-81.
- Heo HJ, Lee CY (2005) Strawberry and its anthocyanins reduce oxidative stress-induced apoptosis in PC12 cells. J Agric Food Chem 53: 1984-1989.
- Amatori S, Mazzoni L, Alvarez Suarez J, et al. (2016) Polyphenol-rich strawberry extract (PRSE) shows in vitro and in vivo biological activity against invasive breast cancer cells. Sci Rep 6: 30917.
- Y Oda (1997) Effects of light intensity, CO2 concentration and leaf temperature on gas exchange of strawberry plants-feasibility studies on CO2 enrichment in Japanese conditions. ISHS Acta Horticulturae 439: III International Strawberry Symposium.
- Bunce JA (2001) Seasonal patterns of photosynthetic response and acclimation to elevated carbon dioxide in field-grown strawberry. Photosynth Res 68: 237-245.
- Lori J Bushway, Marvin P Pritts (2002) Enhancing early spring microclimate to increase carbon resources and productivity in june-bearing strawberry. J Amer Soc Hort Sci 127: 415-422.
- X Deng, FI Woodward (1998) The growth and yield responses offragaria ananassato elevated CO2 and n supply. Ann Bot 81: 67-71.
- Norbert Keutgen, Kai Chen, Fritz Lenz (1997) Responses of strawberry leaf photosynthesis, chlorophyll fluorescence and macronutrient contents to elevated CO2. J Plant Physiol 150: 395-400.
- Lieten F (1996) Effect of CO2 enrichment on greenhouse grown strawberry. ISHS Acta Horticulturae 439: III International Strawberry Symposium.
- FJM Sung, JJ Chen (1991) Gas exchange rate and yield response of strawberry to carbon dioxide enrichment. Sci Hort 48: 241-251.
- Idso CD (2016) Plant growth database.
- Chen K, Hu GQ, Keutgen N, et al. (1997) Effects of CO2 concentration on strawberry. II. Leaf photosynthetic function. J Appl Bot-Angew Bot 71: 173-178.
- Chen K, Hu GQ, Lenz F (1997) Effects of CO2 concentration on strawberry. VI. Fruit yield and quality. J Appl Bot-Angew Bot 71: 195-200.
- Chen K, Hu GQ, Lenz F (1997) Effects of CO2 concentration on strawberry. IV. Carbohydrate production and accumulation. J Appl Bot-Angew Bot 71: 183-188.
- Josep Peñuelas, Marc Estiarte (1998) Can elevated CO2 affect secondary metabolism and ecosystem function? Trends Ecol Evol 13: 20-24.
- Daniel A Herms, William J Mattson (1992) The dilemma of plants: To grow or defend. Q Rev Biol 67: 283-335.
- Wang S, Bunce J, Maas JL (2003) Elevated carbon dioxide increases contents of antioxidant compounds in field-grown strawberries. J Agric Food Chem 51: 4315-4320.
- R Keogh, I McLeod, A Robinson (2010) Pollination aware case study: Strawberries. Rural Industries Research and Development Corporation (RIRDC).
- Hancock JF (1999) Strawberries. CABI Publishing, Wallingford, 237.
- Sorkel Kadir, Gaganpreet Sidhu (2006) Strawberry (Fragaria×ananassa Duch.) growth and productivity as affected by temperature. Hort Science 41: 1423-1430.
- Shiow Y Wang, Mary J Camp (2000) Temperatures after bloom affect plant growth and fruit quality of strawberry. Sci Hort 85: 183-199.
- Hiroyuki Miura, Mio Yoshida, Atushi Yamasaki (1994) Effect of temperature on the size of strawberry fruit. J Jpn Soc Hort Sci 62: 769-774.
- Reckitt-Benckiser RSC (2015) Rate of photosynthesis: Limiting factors.
- Berry J, Bjorkman O (1980) Photosynthetic response and adaptation to temperature in higher plants. Annu Rev Plant Physiol 31: 491-543.
- NA Ledesma, M Nakata, Sugiyama N (2008) Effect of high temperature stress on the reproductive growth of strawberry cvs. 'Nyoho' and 'Toyonoka'. Sci Hort 116: 186-193.
- Wang SY, Zheng W (2001) Effect of plant growth temperature on antioxidant capacity in strawberry. J Agric Food Chem 49: 4977-4982.
- NA Ledesma, S Kawabata, N Sugiyama (2004) Effect of high temperature on protein expression in strawberry plants. Biol Plantarum 48: 73-79.
- Hatice Gulen, Atilla Eris (2004) Effect of heat stress on peroxidase activity and total protein content in strawberry plants. Plant Sci 166: 739-744.
- Sun P, Mantri N, Lou H, et al. (2012) Effects of elevated CO2 and temperature on yield and fruit quality of strawberry (Fragaria×ananassa Duch.) at two levels of nitrogen application. PLoS One 7: e41000.
- (2015) USDA national nutrient database for standard references, release 28.
- AUSNUT 2011-13 food nutrient database.
- (2015) CoFIDS - McCance and Widdowson's The Composition of Foods Integrated Dataset.
- (2014) Association of Southeast Asian Nations (ASEANFOODS).
- (2015) Standard tables of food composition in Japan. MEXT.
- Aaby K, Skrede G, Wrolstad R (2005) Phenolic composition and antioxidant activities in flesh and achenes of strawberries (Fragaria ananassa). J Agric Food Chem 53: 4032-4040.
- Aaby K, Mazur S, Nes A, et al. (2012) Phenolic compounds in strawberry (Fragaria x ananassa Duch.) fruits: Composition in 27 cultivars and changes during ripening. Food Chem 132: 86-97.
- Buendia B, Gil MI, Tudela JA, et al. (2010) HPLC-MS analysis of proanthocyanidin oligomers and other phenolics in 15 strawberry cultivars. J Agric Food Chem 58: 3916-3926.
- Giampieri F, Tulipani S, Alvarez-Suarez JM, et al. (2012) The strawberry: Composition, nutritional quality, and impact on human health. Nutrition 28: 9-19.
- Halbwirth H, Puhl I, Haas U, et al. (2006) Two-phase flavonoid formation in developing strawberry (Fragaria ananassa) fruit. J Agric Food Chem 54: 1479-1485.
- Sandra Neli Jimenez-Garcia, Ramon Gerardo Guevara-Gonzalez, Rita Miranda-Lopez, et al. (2013) Functional properties and quality characteristics of bioactive compounds in berries: Biochemistry, biotechnology, and genomics. Food Res Int 54: 1195-1207.
- Jan Oszmianski, Aneta Wojdylo (2008) Comparative study of phenolic content and antioxidant activity of strawberry puree, clear, and cloudy juices. Eur Food Res Technol 228: 623-631.
- IF Benzie, S Wachtel-Galor (2013) Bioavailability of antioxidant compounds from fruits. In: Margot Skinner, Denise Hunter, Bioactives in fruit: Health benefits and functional foods. John Wiley & Sons, Oxford, UK, 35-54.
- Wang SY, Zheng W, Galletta G (2002) Cultural system affects fruit quality and antioxidant capacity in strawberries. J Agric Food Chem 50: 6534-6542.
- Wang SY, Chen CT, Wang C, et al. (2007) Resveratrol content in strawberry fruit is affected by preharvest conditions. J Agric Food Chem 55: 8269-8274.
Said Ajlouni, Faculty of Veterinary and Agricultural Sciences, Biosciences Section, The University of Melbourne, Parkville, Victoria 3010, Australia, Tel: +61-3-8344-8620, Fax: +61-3-8344-5037.
© 2017 Balasooriya HN, et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.