Open access peer-reviewed chapter

Improving Yield and Antioxidant Properties of Strawberries by Utilizing Microbes and Natural Products

Written By

Mahfuz Rahman, Mosaddiqur Rahman and Tofazzal Islam

Submitted: 04 July 2018 Reviewed: 29 January 2019 Published: 15 March 2019

DOI: 10.5772/intechopen.84803

From the Edited Volume

Strawberry - Pre- and Post-Harvest Management Techniques for Higher Fruit Quality

Edited by Toshiki Asao and Md Asaduzzaman

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Consumption of strawberry has gone up worldwide due to its proven health benefits. Strawberry growers are using synthetic fertilizers and pest management products to maximize yield. This situation posed a risk by affecting sustainability of strawberry production and tainting reputation of a healthy fruit by placing it in the list of dirty dozen due to pesticide residues on fruit. Alternative approaches for increasing yield and pest management of strawberry to minimize environmental and health hazards are possible. Recent studies on alternative natural products (e.g., chitosan) and beneficial microbes (e.g., Bacillus, Paraburkholderia, etc.) indicated that growth, yield, and fruit quality enhancement are supported by these products and may help in sustainable strawberry production. This chapter reviews and updates our knowledge on the health benefit of strawberry and research findings on the use of natural products and probiotic bacteria for yield and quality improvement in strawberry.


  • probiotic
  • antioxidants
  • sustainability
  • disease control
  • strawberry yield
  • microbial biostimulant

1. Introduction

Strawberries are a popular fruit in the US and worldwide. In the US, per capita consumption of strawberries has increased from 2 pounds/person/year to approximately 8 pounds/person/year in recent years [1]. This trend is also apparent in other developed and developing countries of the world. As a result, strawberry growers are using synthetic fertilizers and pest management products to maximize yield. As increased use of synthetic chemicals (fertilizers and pesticides) in crop production and protection has posed a threat to both environment and human health [2], an alternative approach for plant growth promotion, pest management, and sustainable agriculture is being explored all over the world. Strawberry and other fruits and vegetables that are mostly consumed fresh are getting special research attention to innovate production techniques excluding synthetic chemicals [3]. Strawberry growers are specifically eager to find new agro-techniques with special emphasis on the use of both plant growth promotion and nutritional quality improvement in a move toward a more sustainable and environment-friendly approach. In addition, researchers have been testing novel, sustainable approaches to improve the quality and antioxidant properties of strawberries to increase health benefits. One of the reasons for strawberry demand and consumption has been going up as this fruit is an excellent source of natural antioxidants, such as carotenoids, phenolics, vitamins, anthocyanins, and flavonoids with remarkably high capacity of scavenging free radicals [4]. Improving fruit quality and yield sustainability without synthetic inputs is a research priority for this nutritious fruit. Beneficial microorganisms that are used as bio-fertilizers or bio-stimulants possess the ability to colonize the rhizosphere, plant roots, or both when applied to seeds or plant organs that are used for vegetative propagation (strawberry tips). Some of these microbes have shown potential to promote strawberry plant growth by the release of metabolites into the rhizosphere that may inhibit various pathogens as biocontrol agents [5, 6, 7, 8]. However, Tomic et al. [9] found that the response to bacterial inoculation is cultivar-related in strawberries. These microbes were reported to improve plant nutrition and support plant development under natural or stressed conditions as well as increase yield and quality of many important crops and thus may play a crucial role in sustainable crop production in the future [10, 11, 12]. A small but significant body of literature also suggests that these microbes can increase strawberry fruit quality in terms of taste and nutritional value and thereby have a positive impact on human health with associated reduction of healthcare costs [13, 14]. The objective of this review is to update our knowledge on the research conducted on improving yield and quality of strawberry by using natural products and beneficial microbes around the globe. Major focus of the review is to relate bio-fortified strawberry fruit with human health benefit. Some novel eco-friendly approaches and potential mechanisms involved with yield and quality improvement in strawberry are also discussed.


2. Nutritional and health benefit profile of strawberry

Strawberries are an excellent source of essential and health benefitting nutrients (Table 1) and low in total calories with a 100 g serving providing only 32 kcal. Their sweet flavor makes them a delicious alternative to processed foods. Dietary fiber present in strawberries may contribute to regulating blood sugar levels by slowing digestion. Fiber content may also control calorie intake by its satiating effect. Strawberries contain fat-soluble vitamins (i.e., vitamin A and tocopherol) and carotenoids (i.e., lutein and zeaxanthin), but one of the aspects of major nutritional relevance is the extremely high content of vitamin C, even higher than citrus fruits. Together with vitamin C, folate plays a crucial role in the nutritional quality of strawberry as it is one of the richest natural sources of this essential micronutrient, and folate is an important factor in health promotion and disease prevention [15, 16]. Strawberry is a source of several other vitamins such as thiamin, vitamin B6, vitamin K, vitamin A, and vitamin E although to a lesser extent (Table 1). It is also an excellent source of manganese providing more than 20% of the daily adequate intake (AI) for this mineral per serving. The same amount of strawberries can provide about 5% of the AI for potassium and is known as a good source of iodine, magnesium, copper, iron, and phosphorus (Table 1).

2.1 Role of strawberry as a source of dietary antioxidants compared with similar sources

Strawberry consumption can help to prevent inflammation, oxidative stress, cardiovascular disease (CVD), certain types of cancers, type 2 diabetes, and obesity. The addition of berries to the diet can positively influence risk factors for CVD by inhibiting inflammation, improving plasma lipid profiles, scavenging free radicals, and increasing LDL resistance to oxidation [18]. The mechanisms by which strawberries exert these positive effects are not completely understood. Among many potential mechanisms, its role as an antioxidant is the most relevant as strawberry supplementation significantly decreases oxidative stress, protecting mononuclear blood cells against DNA damage [19, 20]. Several studies have shown that strawberry generally possesses a high level of antioxidant activity, which is linked to the levels of phenolic compounds in the fruit rather than vitamin C [1, 21, 22, 23]. Wang and Jiao [24] showed that strawberry juice extracts exhibited a high level of antioxidant capacity against free radical species. Strawberry extracts also seem to modulate cell signaling in cancer cells by inhibiting proliferation of several types of cancer cells inducing cell cycle arrest and apoptosis and suppressing tumor angiogenesis [25]. An unavoidable result of aerobic metabolism in humans and other organisms is the production of reactive oxygen species (ROS). ROS include free radicals such as the superoxide anion (O2•−) and hydroxyl radical (•OH), as well as nonradical molecules like hydrogen peroxide (H2O2), singlet oxygen (1O2), etc. All ROS can be damaging to organisms at a concentration where its level exceeds the defense mechanism. These excess ROS can put cells in oxidative stress that eventually pose a threat to cells by causing peroxidation of lipids, oxidation of proteins, damage to nucleic acids, and enzyme inhibition. The enhanced production of ROS during physiological stresses can also activate a programmed cell death (PCD) pathway that may lead to cell death [26, 27, 28, 29, 30, 31, 32, 33]. Under normal conditions, ROS molecules are unable to cause any damage as they are constantly being scavenged by a range of antioxidative mechanisms [34]. But, the delicate equilibrium between the ROS production and their scavenging by antioxidants is disturbed by multiple stress factors. An efficient antioxidative system that includes nonenzymatic as well as enzymatic antioxidants in a cell can usually scavenge or detoxify excess ROS [35]. The human antioxidant defense system includes endogenous (enzymatic and nonenzymatic) antioxidants and exogenous antioxidants such as vitamin C, vitamin E, anthocyanidins, carotenoids, flavonols, and polyphenols, with the diet being the main source [36, 37, 38, 39]. Exogenous antioxidants play a key role in this delicate equilibrium between oxidation and antioxidation in living systems [36, 37, 40, 41]. Under physiological conditions, the human antioxidative defense system allows the elimination of excess ROS. However, our endogenous antioxidant defense systems are incomplete without exogenous reducing compounds such as vitamin C, vitamin E, carotenoids, and polyphenols. Therefore, there is a continuous demand for exogenous antioxidants to prevent oxidative stress.

Strawberry polyphenolic phytochemicals perform nonessential functions in plants but have large impacts on humans. Of the polyphenolic compounds, anthocyanins in strawberries are the best-known and quantitatively the most important. Studies have determined total anthocyanin content as 150–600 mg/kg of fresh weight. [17]. Strawberries also contain small amounts of other phenolic compounds as shown in Table 2. Evidence from in vitro studies shows that strawberry phenolics may have anti-inflammatory effects and suppress mutagenesis through antioxidative and genoprotective properties. Additionally, the content and composition of flavonols have been studied [42], and these compounds are identified as derivatives of quercetin and kaempferol, with quercetin derivatives being the most abundant [43]. The contents of the flavonoid groups, flavonols, and anthocyanins in strawberry extracts have been associated indirectly and directly, respectively, with the total antioxidant capacity for low-density lipoproteins [21]. Flavonoids in strawberries exhibit antioxidant [44, 45] and anticancer properties as well [46]. Elevated levels of these secondary metabolites should provide better health benefits to the consumers of strawberry.

Type Nutrient Per 100 g
Minerals Calcium (mg) 16
Iron (mg) 0.41
Magnesium (mg) 13
Phosphorus (mg) 24
Manganese (mg) 0.386
Vitamins Vitamin C (mg) 58.8
Folate (μg) 24
Thiamin (mg) 0.024
Lutein + zeaxanthin (μg) 26
Vitamin E, a-tocopherol (mg) 0.29
Vitamin K (μg) 2.2
Vitamin B6 (mg) 0.047
Proximates Dietary fiber (g) 2.0
Fructose (g) 2.44

Table 1.

Nutrient composition of fresh strawberries.

Adapted from [17].

Class Group Compound
Flavonoids Anthocyanins Cyanidin-3-glucoside
Flavonols Quercetin-3-glucuronide
Flavanols (+)-catechin
Proanthocyanidin B1 (EC-4,8-C)
Proanthocyanidin B3 (C-4,8-C)
Phenolic acids Hydroxycinnamic acids p-coumaroyl hexose

Table 2.

Polyphenol composition reported in strawberries.

Adapted from [17].

Among numerous studies conducted on antioxidant contents in fruits and vegetables, results have shown that strawberry possessed a high level of antioxidant activity compared with others in the same group, and the activity was directly linked to the levels of phenolic compounds in the fruit [1, 21, 22]. A comparative study on the antioxidant activity of strawberry extract with other fruits based on the oxygen radical absorbance capacity assay indicated that its antioxidant capacity was higher than extracts from plum, orange, red grape, kiwifruit, pink grapefruit, white grape, banana, apple, tomato, pear, and honeydew melon [47]. However, Sun et al. [22] ranked fruit differently for antioxidant contents based on total antioxidant oxyradical scavenging assay. These results put strawberry behind cranberry, apple, and grape but before peach, lemon, banana, pear, orange, grapefruit, and pineapple in terms of antioxidant activity of fruit extracts. Total antioxidant activity of strawberry can also relate to the contents of anthocyanins, which are typically present at high levels in this fruit [47]. Great interest has developed in strawberries due to the extremely high content of vitamin C, which makes them an important source of this vitamin for human nutrition. Relatively high content of ellagic acid is also a reason of interest for strawberries to consumers. Ellagic acid is an antioxidant that has been proposed to exert antimutagenic and anticarcinogenic effects [48, 49]. Nutritional quality of strawberry is reflected in its high levels of vitamin C, folate, and phenolic constituents [17], most of which show relevant antioxidant capacities in vitro and in vivo [50]. Moreover, strawberries are economically feasible and commercially important, and are widely consumed as fresh or in processed forms such as jam, juice, and jelly. Due to the high nutritional quality, taste, and health benefits, strawberries are among the most studied berries from the aspects of horticultural, genomic, and sustainable production practices.


3. Enhancement of yield and antioxidant contents in strawberry by various natural products including chitosan

To overcome the challenge of increasing strawberry production with a significant reduction of agrochemical use and environmental pollution (especially from synthetic chemicals), a great deal of interest and research has been devoted to natural products and beneficial microbes in recent days. Many growers and researchers are actively looking for ways to create a more sustainable production system through use of natural inputs while simultaneously improving yield and antioxidant properties. A large body of literature suggested that integration of these products with conventional management tools could significantly reduce chemical use and make strawberry production more sustainable. Various natural products have been tested in strawberry production to improve yield and quality by preventing disease and stimulating growth and development. Among the natural products, chitosan is the most tested that has shown growth and yield stimulating effect together with efficacy against diseases in strawberries and other crops [51]. Chitosan is a polysaccharide derived from chitin outer skeletons of shell fish and crustaceans such as crab, crayfish, lobster, and shrimp. As chitin is deacetylated by sodium hydroxide to obtain chitosan, it is slightly basic and is soluble in dilute aqueous acidic solution (pH < 6.5). Once dissolved, it can be further diluted with water to apply on plants at all different growth stages. In general, it is nontoxic to humans and considered safe for agricultural uses due to its quick degradation in the environment. Once chitosan or its derivatives come in contact with plants, they bind with the cell plasma membrane and elicit defense responses through expression of pathogenesis-related (PR) genes, accumulation of phytoalexins, callose, oxidative burst, and formation of reactive oxygen species. Expression of these PR genes and accumulation of antimicrobial phytoalexins are believed to play a major role in controlling pre- and postharvest pathogenic diseases. A large body of published reports supports antimicrobial activities of chitosan against a wide range of phytopathogens [52]. Similar studies also found that the biostimulant chitosan promoted plant growth and development and provided enhanced disease suppression capability to plants through multiple mechanisms including induced systemic resistance [51, 53]. Chitosan has been widely used as fruit coatings to enhance storability and preserve anthocyanin and other antioxidants in strawberry [51], and various other fruit mainly for protection from postharvest losses due to microbial infections [51, 54]. In addition, many investigators reported that chitosan use as a foliar spray increased vegetative growth, yield, and biochemical contents in plants [55, 56, 57, 58]. Improvement of yield and functional properties of strawberry fruit through application of chitosan should be considered a sustainable option. A recent study by Rahman et al. [58] showed that multiple application of low concentrations (ppm level) of chitosan on the canopy of field grown strawberry plants at the prebloom stage significantly improved growth and yield. Authors also reported concurrent increase in various antioxidant contents and total antioxidant activities in treated fruit compared to nontreated control. This is an interesting and significant finding as total antioxidants and pigments such as anthocyanins are determinants of health benefits of strawberry fruit. Rahman et al. [58] also determined the effect of different doses of chitosan biopolymer on growth, fruit yield, and human health benefiting antioxidant properties of strawberry and found that both yield and contents of antioxidants are increased in a dose-dependent manner to some extent compared to untreated control. These findings indicate that the biostimulant chitosan can be an attractive agent for production of high quality and human health benefiting strawberry [58]. Results also indicated that foliar application of varying doses of chitosan on strawberry canopy stimulated all aspects of vegetative growth (plant height and root length) that may have influenced fruit yield and fruit quality compared with untreated control (Table 3). These findings were also interesting as all doses of chitosan improved growth of strawberry plants to some extent and may be experimented in similar crops being grown in soils with varying physical, chemical, and biological characteristics. This study was one of the few of its kind that determined the effects of natural products such as chitosan application on field-grown strawberry plants influencing yield and contents of multiple antioxidants in fruit. Experimental protocol for this study can be found in Rahman et al. [58].

Treatment Plant height (cm) Root length (cm) Total fruit weight/plant (g) Total anthocyanin content Total phenolic content Total antioxidant activity
Control 19.5 ± 1.0b 19.25 ± 0.4c 246.6 ± 0.4d 81.11 ± 0.9d 310.4 ± 0.7c 250.9 ± 0.9c
Ch 125 20.41 ± 0.9b 21.16 ± 0.2bc 317.5 ± 0.7c 83.1 ± 1.0cd 356.5 ± 1.0b 252.6 ± 1.0c
Ch 250 21.75 ± 0.8b 22.66 ± 0.7ab 325.7 ± 0.5c 94.6 ± 0.5c 317.8 ± 0.5c 358.6 ± 1.0b
Ch 500 25.1 ± 1.0a 24.33 ± 0.2a 351.25 ± 0.5a 184.3 ± 1.9a 363.2 ± 0.4ab 374.42 ± 1.0b
Ch 1000 24.91 ± 1.5a 24.16 ± 0.6a 337.7 ± 0.4b 163.9 ± 0.6b 370.9 ± 0.4a 415.6 ± 0.5a

Table 3.

Effect of chitosan application on yield and content of antioxidants in strawberry fruit.

Five different concentrations, 0, 125, 250, 500, and 1000 ppm, of chitosan solution were prepared by dissolving the required amount in 0.1 N HCl and diluting with distilled water with pH adjusted at 6.5 by NaOH. Freshly prepared chitosan solutions were applied onto strawberry plants in each experimental unit prior to flowering and at 10% flowering stage by spraying up to run off at five different times with 10-d intervals. Cumulative fruit harvest from each plot was recorded. The required amounts of fruit tissues from first harvest were subjected to analyses for phenolics and other antioxidants mentioned in the table. Values are means ± standard errors of three independent replications (n = 3). Different superscripted letters within the column indicate statistically significant differences among the treatments according to Fisher’s protected LSD (least significance difference) test at p ≤ 0.05, adapted from [58].

Among a few different chitosan concentrations tested in the study, 500 ppm provided the highest fruit yield (42% higher than untreated control) in “Strawberry Festival” compared with untreated control (Table 3). Similar to yield response and a few other antioxidants, chitosan spray application on the canopy of strawberry also significantly increased fruit anthocyanin contents in a dose-dependent manner that plateaued at 500 ppm with 184.3 mg cyanidin-3-O-glucoside/100 g fruit. This increase of anthocyanin contents was equivalent to 2.3-fold higher compared with untreated control. The fruit produced by the plants treated with 1000 ppm chitosan solution in the study by Rahman et al. [58] had the highest total phenolic content (370.9 μg gallic acid/g fruit) indicating that chitosan concentration should be adjusted depending on the intended quality improvement in strawberry fruit. Total antioxidant activities of strawberry fruit obtained from both varied rates of chitosan treated and untreated control plants were assayed by utilizing the DPPH method, and the results were expressed as butylated hydroxytoluene (BHT) equivalents per gram of strawberry fruit. The highest total antioxidant activity was quantified in strawberry fruit obtained from 1000 ppm chitosan (415.6 μg BHT/g fruit) treated plants. These results reveal that application of chitosan on the canopy of strawberry could increase antioxidant activity in fruit up to 1.7-fold compared to untreated control (Table 3) [58].

A few other examples of natural products that have been investigated on strawberry with varying results are derived either from seaweed or compost. Seaweed products are used as nutrient supplements, biostimulants, and biofertilizers to augment plant growth and yield in agriculture. A study by Masny [59] found no effect on disease suppression of Botrytis cinerea on strawberry by applying seaweed products. However, application of these products had a significant influence on yield with an increase in the range of 17–42%. Compost or tea extracts were also used for plant disease control and for plant nutrition and growth promotion. Welke [60] assessed the effect of compost extract application on strawberry. Aerobically prepared extracts were effective in both disease suppression (B. cinerea) and increasing yield compared to the control.


4. Strawberry growth, yield, and quality improvement by probiotic bacteria

Beneficial microorganisms especially bacteria that are associated with host plants either as rhizoplane, phylloplane, or endophyte and enhance growth of the host plants including yield are popularly known as plant probiotic bacteria (PPB). These PPB can also suppress plant diseases by various modes of action when applied proactively in adequate amounts [61]. PPB that are used as biofertilizers or biostimulants possess the ability to colonize the rhizosphere, plant roots, or both when applied to seeds or crops. Some of these microbes have shown potential to promote strawberry plant growth by the release of metabolites into the rhizosphere that may inhibit various pathogens as biocontrol agents [5, 6, 7, 8]. However, Tomic et al. [9] found that the response to bacterial inoculation is cultivar-related in strawberries, which indicates that a specific microbial strain should be tested for efficacy against a specific strawberry variety before large scale use. Microbes belonging to this group are also known as plant growth promoting rhizobacteria (PGPR) and were reported to improve availability of plant nutrient and support plant development under natural or stressed conditions as well as increase yield and quality. Although beneficial microbes have not been widely researched or used for improving yield and quality of strawberry, a large body of evidence indicates that many available beneficial microbes were found to provide growth and yield enhancement to diverse crop commodities [10, 11, 12], which can be tested for similar efficacy on strawberry and thus may play a crucial role in sustainable strawberry production in the future. A significant body of literature suggests that these microbes can increase strawberry fruit quality in terms of taste and nutritional value and thereby have a positive impact on human health with associated reduction of healthcare costs [13, 14]. A few relevant examples of positive effects of antagonistic microbes on multiple crops include protection against Verticillium dahliae [62] and protection of tomato against Alternaria solani [63]. Some of these microbes were used in vitro and should be evaluated in vivo or in field conditions. For example, in vitro-beneficially-bacterized plantlets of grapevine not only grew faster than non-bacterized controls but also were sturdier, with a better developed root system and significantly greater capacity for withstanding gray mold fungus [64]. Similarly, banana plantlets treated with endophytes Pseudomonas and Bacillus species showed improved vegetative growth, physiological attributes, and strong defense against bunchy top diseases in the field [65, 66]. Seed treatment or augmenting beneficial microbial population in soil was also found to reduce seedling mortality from soil-borne diseases [67]. Biological agents such as Trichoderma, Serratia, and Pseudomonas and different plant extracts are some of the alternative strategies that have been explored to reduce the number of microsclerotia or wilt symptoms in multiple crops [65, 68, 69, 70, 71, 72]. A few studies also showed that application of beneficial bacteria significantly improved seed germination, seedling vigor, growth, yield, and early blight disease protection in tomato through multiple mechanisms including production of growth regulators and induced biosynthesis of antioxidant peroxidase and polyphenol oxidase [63]. Although many different strains of microbes belonging to multiple genera and species have been identified and tested for their efficacy, major genera of PPBs include Bacillus, Paraburkholderia, Pseudomonas, Acinetobacter, Alcaligenes, Arthrobacter, and Serratia. Major modes of action by which PPB provide beneficial effects to host plants include production of growth promoting hormones, antibiotics, and lytic enzymes that affect harmful microbes, nitrogen fixation from the atmosphere, nutrient solubilization from soil minerals for plant availability, and systemic resistance induction in the host or treated plants. Two PPB, Bacillus amyloliquefaciens and Paraburkholderia fungorum applied on strawberry by Rahman et al. [73] not only increased yield but also significantly improved contents of several antioxidants and total antioxidant activities of fruits. Treatments of strawberry plants with bacterial strains B. amyloliquefaciens and P. fungorum consistently produced higher antioxidants, carotenoids, flavonoids, phenolics, and total anthocyanins compared to nontreated control [73]. Flores-Félix [14] reported that application of a strain of genus Phyllobacterium on strawberry showed significant increase in vitamin C contents in fruits.

A recent study [73] explored an environment-friendly option for boosting strawberry plant growth, fruit yield, and functional properties of fruits through the application of two plant growth promoting probiotic bacteria and compared the results with that of nontreated control. Results showed significant improvement in plant growth, yield, various antioxidant contents, and total antioxidant activities of strawberry fruits by the application of both B. amyloliquefaciens BChi1 and P. fungorum BRRh-4 treatment compared to nontreated control. Inoculation of strawberry plants separately with two bacterial isolates significantly increased vegetative growth (plant height and root length) of the strawberry plants (Table 4). Generally, plant growth promoting rhizobacteria facilitate plant growth directly by either assisting in resource acquisition (nitrogen, phosphorus, and essential minerals) or modulating plant hormone levels, or indirectly by inhibiting various pathogens as biocontrol agents [11]. Early colonization of root system has the potential to preclude pathogen colonization and infection in addition to induction of disease resistance or a range of beneficial secondary metabolites. Plant height and root length also were positively influenced and varied significantly due to the plant probiotic bacterial applications. The highest plant height (20.50 cm) was observed in BRRh-4 treated plants (Table 4). Similar to plant height, root length also significantly (p < 0.05) varied among the treatments and was reflected by plant vigor (Figure 1). A hypothetical pathway of strawberry growth, yield, and fruit quality improvement is shown in Figure 2. Results from this study indicated that vegetative growth enhancement by probiotic bacteria may have also enhanced fruit yield and quality, enhancing secondary metabolites such as anthocyanins, phenolics, and total antioxidant activity (Table 4). Strawberry fruit from Paraburkholderia fungorum BRRh-4 and Bacillus amyloliquefaciens BChi1 treated plants had total phenolic content 380.5 and 377.72 μg gallic acid/g fruit, respectively compared with 317.08 μg gallic acid/g fruit in untreated control plants. Detailed experimental protocol can be found in a study by Rahman et al. [73].

Treatment Plant height (cm) Root length (cm) Total fruit weight/plant (g) Total anthocyanin content Total phenolic content Total antioxidant activity
Control 18.6 ± 1.01a 19.3 ± 0.43b 316.6 ± 10.06b 81.1 ± 0.5b 317.1 ± 7.3b 250.9 ± 3.1b
BChi1* 119.3 ± 0.86a 22.7 ± 0.33a 453.0 ± 2.2a 187.5 ± 16.9a 377.8 ± 1.7a 382.0 ± 1.4a
BRRh-4 20.5 ± 0.26a 23.5 ± 1.15a 467.8 ± 2.2a 223.0 ± 3.6a 380.5 ± 5.1a 385.5 ± 3.4a

Table 4.

Effect of plant probiotic bacteria on yield and antioxidant content in strawberry fruit.

Cumulative fruit harvest from each plot was recorded. The required amounts of fruit tissues from first harvest were subjected to analyses for phenolics and other antioxidants mentioned in the table. Values are means ± standard errors of three independent replications (n = 3). Different superscripted letters within the column indicate statistically significant differences among the treatments according to Fisher’s protected LSD (least significance difference) test at p ≤ 0.05, adapted from [73].

Figure 1.

Effect of different doses of chitosan and probiotic bacteria on vegetative and reproductive growth of cv. Strawberry Festival. Adapted from [58, 73].

Figure 2.

A hypothetical pathway of stimulation of fruit yield and accumulation of antioxidants in strawberry fruit due to the root colonization by probiotic bacteria.

One of the interesting findings of this study is that both plant probiotic bacteria significantly improved growth and yield of strawberry almost at the same level with some minor differences although they belong to different bacterial genera. Probiotic bacterium, BRRh-4 provided the highest fruit yield increase (48%) in plants of “Strawberry Festival” compared to nontreated control (Table 4). Treatments of strawberry plants with bacterial strains BRRh-4 and BChi1 consistently produced higher antioxidants, carotenoids, flavonoids, phenolics, and total anthocyanins compared to nontreated control [73]. A previous study showed that the members of the genus Phyllobacterium were good plant probiotics with the capacity of increasing fruit yield as well as quality [14]. Application of plant probiotic bacteria significantly increased total anthocyanin content in strawberry fruits compared to nontreated control. The highest anthocyanin content (222.0 mg cyanidin-3-O-glucoside/100 g fruit) in strawberry fruits was recorded in plants treated with BRRh-4 followed by BChi1 (187.47 mg cyanidin-3-O-glucoside/100 g fruit). To evaluate whether plant probiotic bacteria had any effect on antioxidant activities of strawberry fruits obtained from both probiotic bacteria and nontreated control plants, we estimated total antioxidant activities of fresh strawberry fruits by DPPH assay. The results of the DPPH assay for total antioxidant activity were expressed as butylated hydroxytoluene (BHT) equivalents per gram of strawberry fruit. As expected, the total antioxidant activity of fresh strawberry fruits was the highest in BRRh-4 (385.47 μg BHT/g fruit) followed by BChi1 treatment (382.00 μg BHT/g fruit) (Table 4) [73].

4.1 Bio-rational/natural product-based approach for strawberry root disease management for boosting yield

The strawberry black root rot complex (BRRC) and crown rot are increasing problems in perennial strawberry plantings worldwide and have been identified as limiting factors of sustainable strawberry production [74, 75]. Yield loss from black root rot alone can range from 20 to 50% [76], which can dramatically increase if crown rot occurs concurrently. Because several factors are involved in BRRC of strawberry, including a range of infectious agents (nematodes and root infecting fungi) and various abiotic factors such as poor soil characteristics [77], the disease control is complicated, and no general control measure is completely effective. On the other hand, crown rot disease of strawberry caused primarily by the fungal species Colletotrichum gloeosporioides and Phytophthora cactorum [78] can sometimes also incur significant yield loss in strawberry production in the US and other strawberry growing countries [78]. Although inoculum sources for crown rot in fruiting fields may be diverse, infected planting stock is the most important source of C. gloeosporioides [79, 80, 81, 82, 83] whereas P. cactorum is mostly soil-borne and builds up in a strawberry field over time. Occurrence of crown rot caused by Fusarium oxysporum f.sp. fragariae is also on the rise. Mass [84] observed that in many cases where crop rotation was not an option, fumigation of soil was necessary to control soil-borne diseases. Methyl bromide (MeBr) was previously used as a preplant broad-spectrum soil fumigant to control soil-borne diseases, nematodes, insects, and weeds in high value crop such as strawberry [85]. However, with the disappearance of this highly effective soil fumigant MeBr, and restrictions on the allowed use of other alternative synthetic fumigants, the interest in the development of safe, sustainable, and economically viable fumigation strategies have increased to manage soil-borne fungi and nematodes [85]. More importantly, the demands from organic growers and small growers who cannot use synthetic fumigants have increased tremendously [86]. Alternative strategies are also required especially for strawberries as disease-resistant cultivars are unavailable [87]. Among multiple alternatives of soil fumigation with synthetic chemicals, glucosinolate-containing Brassica spp. is known to release volatile isothiocyanates (ITCs), which are toxic to different pathogens [88]. The chemistry involved in the biofumigation can be attributed to the action of myrosinase enzyme on the glucosinolates (GLS) to release ITCs, thiocyanates, nitriles, oxazolidine, dimethyl sulfide, and methanethiol, among other compounds [88, 89]. Several lines of evidence suggest that biofumigation with ITC-producing plants have shown promising results against soil-borne fungal pathogens, for example, Rhizoctonia, Verticillium, Fusarium, Pythium, and Phytophthora spp. [90, 91, 92]. However, the concentration of ITCs produced is influenced by mustard variety [93], soil texture, moisture, temperature, microbial community, and pH [94, 95], resulting in variable soil-borne disease control efficacy. From a NE-SARE funded project in the U.S., Balzano [93] found the highest glucosinolate content and biomass in “Caliente-199.” While these observations indicate a need for selecting the right variety, site-specific testing, optimization of the method such as selection of the best growth stage (highest content of glucosinolate), optimum tissue disruption, and quick soil incorporation may also play a significant role. This is crucial for the success of this approach as laboratory experiments indicated that the efficacy of the conversion to ITCs was only 5% of the potential when using tissue disruption methods (cutting and chopping) similar to those frequently used under field conditions [95, 96]. Matthiessen et al. [97] were able to increase soil ITC levels by 20-fold (100 nmol per g soil) using a tractor-drawn tissue pulverizing implement compared to when using a cutting and chopping implement. In addition, they showed that adding excess water to the pulverized tissue was necessary for maximum ITC release.

Another promising nonchemical soil-borne disease control alternative is anaerobic soil disinfestation (ASD), which was adapted from the previously described methods of biological soil disinfestation (BSD) and soil reductive sterilization [98, 99] to create a treatment suitable for strawberry [100]. A wide range of soil-borne plant pathogens and plant parasitic nematodes have been controlled in a variety of crops using ASD [100]. Implementation of ASD is done in three different steps. First, a labile carbon source is added to the soil followed by the generation of anaerobic conditions through application of water to fill soil pore space. In the third step, the soil is covered with plastic mulch to prevent oxygen exchange. The exact mechanisms that lead to disease suppression with ASD are not clearly understood but may involve production of organic acids and other biologically active volatiles [101] and amplification of specific microbes with biocontrol activity [102].


5. Future perspectives

Findings from many important and relevant studies indicated that natural products and plant probiotic bacteria especially the ones isolated from the native environment could be used as natural agents for sustainable production of high quality strawberry with no or little additional use of expensive synthetic inputs. However, researchers found that the effects are more pronounced in nutrient poor growing conditions. The additive effect of utilization of these products in growing environment with balanced nutrition has not been sufficiently researched. In addition, with the disappearance of soil fumigant methyl bromide that played an essential role in managing soil-borne diseases in high value crop like strawberry, more research should be directed to finding natural alternatives for sustainable management of both foliar and soil-borne diseases. Resistance development in plant pathogens against synthetic products is also a huge concern that dictates the need for developing sustainable options. Numerous natural products and microbial strains have been screened for antimicrobial properties with positive outcomes enabling plants to resist important phytopathogens and provide plant growth-promoting effects. However, only a few of these products are commercially available to growers. Large-scale use of these products did not occur due to the variability and inconsistency of results in field conditions. Lowering the variability and increasing the consistency of results from these products are among a few challenges that will have to be addressed. The scientific community must determine the factors that interfere with the reproducibility of results from one location to another or controlled condition to field condition over time. Integration of these products with other management options should help in reducing the variability of results and produce additive effects. The continuing need for natural products supporting sustainable strawberry production will make discovery and commercialization of natural and beneficial microbe-based products as an attractive and profitable pursuit in the coming days.


  1. 1. Vinson JA, Su X, Zubik L, Bose P. Phenol antioxidant quantity and quality in foods: Fruits. Journal of Agricultural and Food Chemistry. 2001;49(11):5315-5321
  2. 2. Islam MT, Hashidoko Y, Deora A, Ito T, Tahara S. Suppression of damping-off disease in host plants by the rhizoplane bacterium Lysobacter sp. strain SB-K88 is linked to plant colonization and antibiosis against soil borne Peronosporomycetes. Applied and Environmental Microbiology. 2005;71(7):3786-3796
  3. 3. Fernandes VC, Domingues VF, Mateus N, Delerue-Matos C. Pesticide residues in Portuguese strawberries grown in 2009-2010 using integrated pest management and organic farming. Environmental Science and Pollution Research. 2012;19:4184-4192
  4. 4. Huang WY, Zhang HC, Liu WX, Li CY. Survey of antioxidant capacity and phenolic composition of blueberry, blackberry, and strawberry in Nanjing. Journal of Zhejiang University. Science. B. 2012;13(2):94-102
  5. 5. Esitken A, Yildiz HE, Ercisli S, Donmez MF, Turan M, Gunes A. Effects of plant growth promoting bacteria (PGPB) on yield, growth and nutrient contents of organically grown strawberry. Scientia Horticulturae. 2010;124(1):62-66
  6. 6. Pešaković M, Karaklajić-Stajić Ž, Milenković S, Mitrović O. Biofertilizer affecting yield related characteristics of strawberry (Fragaria × ananassa Duch.) and soil micro-organisms. Scientia Horticulturae. 2013;150:238-243
  7. 7. Lingua G, Bona E, Manassero P, Marsano F, Todeschini V, Cantamessa S, et al. Arbuscular mycorrhizal fungi and plant growth-promoting pseudomonads increases anthocyanin concentration in strawberry fruits (Fragaria × ananassa var. Selva) in conditions of reduced fertilization. International Journal of Molecular Sciences. 2013;14(8):16207-16225
  8. 8. Lovaisa NC, Guerrero Molina MF, Delaporte Quintana PG, Salazar SM. Response of strawberry plants inoculated with Azospirillum and Burkholderia at field conditions. Revista Agronómica del Noroeste Argentino. 2015;35(1):33-36
  9. 9. Tomic JM, Milivojevic JM, Pesakovic MI. The response to bacterial inoculation is cultivar-related in strawberries. Turkish Journal of Agriculture and Forestry. 2015;39(2):332-341
  10. 10. Kundan R, Pant G, Jadon N, Agrawal PK. Plant growth promoting rhizobacteria: Mechanism and current prospective. Journal of Fertilizer and Pesticide. 2015;6(2):9
  11. 11. de Oliveira-Longatti SM, de Sousa PM, Marra LM, Ferreira PA, de Souza Moreira FM. Burkholderia fungorum promotes common bean growth in a dystrophic oxisol. Annals of Microbiology. 2015;65(4):1825-1832
  12. 12. Vejan P, Abdullah R, Khadiran T, Ismail S, Nasrulhaq Boyce A. Role of plant growth promoting rhizobacteria in agricultural sustainability—A review. Molecules. 2016;21(5):573
  13. 13. Bidlack WR. Interrelationships of food, nutrition, diet and health: The National Association of State Universities and Land Grant Colleges White Paper. Journal of the American College of Nutrition. 1996;15(5):422-433
  14. 14. Flores-Félix JD, Silva LR, Rivera LP, Marcos-García M, García-Fraile P, Martínez-Molina E, et al. Plants probiotics as a tool to produce highly functional fruits: The case of phyllobacterium and vitamin C in strawberries. PLoS One. 2015;10(4):e0122281
  15. 15. Tulipani S, Mezzetti B, Battino M. Impact of strawberries on human health: Insight into marginally discussed bioactive compounds for the Mediterranean diet. Public Health Nutrition. 2009;12(9A):1656-1662
  16. 16. Tulipani S, Romandini S, Suarez JM, Capocasa F, Mezzetti B, Battino M, et al. Folate content in different strawberry genotypes and folate status in healthy subjects after strawberry consumption. BioFactors. 2008;34(1):47-55
  17. 17. Giampieri F, Tulipani S, Alvarez-Suarez JM, Quiles JL, Mezzetti B, Battino M. The strawberry: Composition, nutritional quality, and impact on human health. Nutrition. 2012;28(1):9-19
  18. 18. Basu A, Rhone M, Lyons TJ. Berries: Emerging impact on cardiovascular health. Nutrition Reviews. 2010;68(3):168-177
  19. 19. Azzini E, Vitaglione P, Intorre F, Napolitano A, Durazzo A, Foddai MS, et al. Bioavailability of strawberry antioxidants in human subjects. The British Journal of Nutrition. 2010;104(8):1165-1173
  20. 20. Tulipani S, Alvarez-Suarez JM, Busco F, Bompadre S, Quiles JL, Mezzetti B, et al. Strawberry consumption improves plasma antioxidant status and erythrocyte resistance to oxidative haemolysis in humans. Food Chemistry. 2011;128(1):180-186
  21. 21. Heinonen IM, Meyer AS, Frankel EN. Antioxidant activity of berry phenolics on human low-density lipoprotein and liposome oxidation. Journal of Agricultural and Food Chemistry. 1998;46(10):4107-4112
  22. 22. Sun J, Chu YF, Wu X, Liu RH. Antioxidant and antiproliferative activities of common fruits. Journal of Agricultural and Food Chemistry. 2002;50(25):7449-7454
  23. 23. Guo C, Yang J, Wei J, Li Y, Xu J, Jiang Y. Antioxidant activities of peel, pulp and seed fractions of common fruits as determined by FRAP assay. Nutrition Research. 2003;23(12):1719-1726
  24. 24. Wang SY, Jiao H. Scavenging capacity of berry crops on superoxide radicals, hydrogen peroxide, hydroxyl radicals, and singlet oxygen. Journal of Agricultural and Food Chemistry. 2000;48(11):5677-5684
  25. 25. Giampieri F, Alvarez-Suarez JM, Mazzoni L, Romandini S, Bompadre S, Diamanti J, et al. The potential impact of strawberry on human health. Natural Product Research. 2013;27(4-5):448-455
  26. 26. Shah K, Kumar RG, Verma S, Dubey RS. Effect of cadmium on lipid peroxidation, superoxide anion generation and activities of antioxidant enzymes in growing rice seedlings. Plant Science. 2001;161(6):1135-1144
  27. 27. Mittler R. Oxidative stress, antioxidants and stress tolerance. Trends in Plant Science. 2002;7(9):405-410
  28. 28. Sharma P, Dubey RS. Drought induces oxidative stress and enhances the activities of antioxidant enzymes in growing rice seedlings. Plant Growth Regulation. 2005;46(3):209-221
  29. 29. Maheshwari R, Dubey RS. Nickel-induced oxidative stress and the role of antioxidant defence in rice seedlings. Plant Growth Regulation. 2009;59(1):37-49
  30. 30. Mishra S, Jha AB, Dubey RS. Arsenite treatment induces oxidative stress, upregulates antioxidant system, and causes phytochelatin synthesis in rice seedlings. Protoplasma. 2011;248(3):565-577
  31. 31. Srivastava S, Dubey RS. Manganese-excess induces oxidative stress, lowers the pool of antioxidants and elevates activities of key antioxidative enzymes in rice seedlings. Plant Growth Regulation. 2011;64(1):1-6
  32. 32. Verma S, Dubey RS. Lead toxicity induces lipid peroxidation and alters the activities of antioxidant enzymes in growing rice plants. Plant Science. 2003;164(4):645-655
  33. 33. Meriga B, Reddy BK, Rao KR, Reddy LA, Kishor PK. Aluminium-induced production of oxygen radicals, lipid peroxidation and DNA damage in seedlings of rice (Oryza sativa). Journal of Plant Physiology. 2004;161(1):63
  34. 34. Foyer CH, Noctor G. Redox homeostasis and antioxidant signaling: A metabolic interface between stress perception and physiological responses. The Plant Cell. 2005;17(7):1866-1875
  35. 35. Noctor G, Foyer CH. Ascorbate and glutathione: Keeping active oxygen under control. Annual Review of Plant Biology. 1998;49(1):249-279
  36. 36. Bouayed J. Polyphenols: A potential new strategy for the prevention and treatment of anxiety and depression. Current Nutrition & Food Science. 2010;6(1):13-18
  37. 37. Ratnam DV, Ankola DD, Bhardwaj V, Sahana DK, Kumar MR. Role of antioxidants in prophylaxis and therapy: A pharmaceutical perspective. Journal of Controlled Release. 2006;113(3):189-207
  38. 38. Biehler E, Bohn T. Methods for assessing aspects of carotenoid bioavailability. Current Nutrition & Food Science. 2010;6(1):44-69
  39. 39. Andre CM, Larondelle Y, Evers D. Dietary antioxidants and oxidative stress from a human and plant perspective: A review. Current Nutrition & Food Science. 2010;6(1):2-12
  40. 40. Valko M, Leibfritz D, Moncol J, Cronin MT, Mazur M, Telser J. Free radicals and antioxidants in normal physiological functions and human disease. The International Journal of Biochemistry & Cell Biology. 2007;39(1):44-84
  41. 41. Pandey KB, Rizvi SI. Plant polyphenols as dietary antioxidants in human health and disease. Oxidative Medicine and Cellular Longevity. 2009;2(5):270-278
  42. 42. Häkkinen SH, Törrönen AR. Content of flavonols and selected phenolic acids in strawberries and Vaccinium species: Influence of cultivar, cultivation site and technique. Foodservice Research International. 2000;33(6):517-524
  43. 43. Aaby K, Ekeberg D, Skrede G. Characterization of phenolic compounds in strawberry (Fragaria × ananassa) fruits by different HPLC detectors and contribution of individual compounds to total antioxidant capacity. Journal of Agricultural and Food Chemistry. 2007;55(11):4395-4406
  44. 44. Bors W, Saran M. Radical scavenging by flavonoid antioxidants. Free Radical Research Communications. 1987;2(4-6):289-294
  45. 45. Wang H, Cao G, Prior RL. Total antioxidant capacity of fruits. Journal of Agricultural and Food Chemistry. 1996;44(3):701-705
  46. 46. Das DK. Naturally occurring flavonoids: Structure, chemistry, and high-performance liquid chromatography methods for separation and characterization. Methods in Enzymology. 1994;234:410-420
  47. 47. Meyers KJ, Watkins CB, Pritts MP, Liu RH. Antioxidant and antiproliferative activities of strawberries. Journal of Agricultural and Food Chemistry. 2003;51(23):6887-6892
  48. 48. Maas JL, Galletta GJ, Stoner GD. Ellagic acid, an anticarcinogen in fruits, especially in strawberries: A review. Hortscience. 1991;26(1):10-14
  49. 49. Conney AH. Enzyme induction and dietary chemicals as approaches to cancer chemoprevention: The Seventh DeWitt S. Goodman Lecture. Cancer Research. 2003;63(21):7005-7031
  50. 50. Alvarez-Suarez JM, Tulipani S, Romandini S, Vidal A, Battino M. Methodological aspects about determination of phenolic compounds and in vitro evaluation of antioxidant capacity in the honey: A review. Current Analytical Chemistry. 2009;5(4):293-302
  51. 51. Malerba M, Cerana R. Recent advances of chitosan applications in plants. Polymers. 2018;10(2):118
  52. 52. Rahman MH, Shovan LR, Hjeljord LG, Aam BB, Eijsink VG, Sørlie M, et al. Inhibition of fungal plant pathogens by synergistic action of chito-oligosaccharides and commercially available fungicides. PLoS One. 2014;9(4):e93192
  53. 53. Pichyangkura R, Chadchawan S. Biostimulant activity of chitosan in horticulture. Scientia Horticulturae. 2015;196:49-65
  54. 54. Sakif TI, Dobriansky A, Russell K, Islam T. Does chitosan extend the shelf life of fruits? Advances in Bioscience and Biotechnology. 2016;7(08):337
  55. 55. Mukta JA, Rahman M, Sabir AA, Gupta DR, Surovy MZ, Rahman M, et al. Chitosan and plant probiotics application enhance growth and yield of strawberry. Biocatalysis and Agricultural Biotechnology. 2017;11:9-18
  56. 56. Ramakrishna R, Sarkar D, Manduri A, Iyer SG, Shetty K. Improving phenolic bioactive-linked anti-hyperglycemic functions of dark germinated barley sprouts (Hordeum vulgare L.) using seed elicitation strategy. Journal of Food Science and Technology. 2017;54(11):3666-3678
  57. 57. Pirbalouti AG, Malekpoor F, Salimi A, Golparvar A. Exogenous application of chitosan on biochemical and physiological characteristics, phenolic content and antioxidant activity of two species of basil (Ocimum ciliatum and Ocimum basilicum) under reduced irrigation. Scientia Horticulturae. 2017;217:114-122
  58. 58. Rahman M, Mukta JA, Sabir AA, Gupta DR, Mohi-Ud-Din M, Hasanuzzaman M, et al. Chitosan biopolymer promotes yield and stimulates accumulation of antioxidants in strawberry fruit. PLoS One. 2018;13(9):e0203769
  59. 59. Masny A, Basak A, Zurawicz E. Effects of foliar applications of Kelpak SL and Goemar BM 86 on yield and fruit quality in two strawberry cultivars. Journal of Fruit and Ornamental Plant Research. 2004;12:23-27
  60. 60. Welke WE. The effect of compost tea on the yield of strawberries and the severity of Botrytis cinerea. Journal of Sustainable Agriculture. 2004;25:57-68
  61. 61. Islam MT, Hossain MM. Plant probiotics in phosphorus nutrition in crops, with special reference to rice. In: Maheshwari DK, editor. Bacteria in Agrobiology: Plant Probiotics. 1st ed. Berlin: Heidelberg; 2012. pp. 325-363
  62. 62. Berg G, Zachow C, Lottmann J, Gotz M, Costa R, Smalla K. Impact of plant species and site on rhizosphere-associated fungi antagonistic to Verticillium dahliae Kleb. Applied and Environmental Microbiology. 2005;71:4203-4213
  63. 63. Babu AN, Jogaiah S, Ito S, Nagaraj AK, Tran LSP. Improvement of growth, fruit weight and early blight disease protection of tomato plants by rhizosphere bacteria is correlated with their beneficial traits and induced biosynthesis of antioxidant peroxidase and polyphenol oxidase. Plant Science. 2015;231:62-73
  64. 64. Barka EA, Belarbi A, Hachet C, Nowak J, Audran JC. Enhancement of in vitro growth and resistance to gray mould of Vitis vinifera co-cultured with plant growth-promoting rhizobacteria. FEMS Microbiology Letters. 2000;186(1):91-95
  65. 65. Kavino M, Harish S, Kumar N, Saravanakumar D, Samiyappan R. Effect of chitinolytic PGPR on growth, yield and physiological attributes of banana (Musa spp.) under field conditions. Applied Soil Ecology. 2010;45(2):71-77
  66. 66. Kavino M, Harish S, Kumar N, Saravanakumar D, Damodaran T, Soorianathasundaram K, et al. Rhizosphere and endophytic bacteria for induction of systemic resistance of banana plantlets against bunchy top virus. Soil Biology and Biochemistry. 2007;39(5):1087-1098
  67. 67. Rahman M, Punja ZK. Biological control of damping-off on American ginseng (Panax quinquefolius) by Clonostachys rosea f. catenulata (= Gliocladium catenulatum). Canadian Journal of Plant Pathology. 2007;29(2):203-207
  68. 68. Berg G, Fritze A, Roskot N, Smalla K. Evaluation of potential biocontrol rhizobacteria from different host plants of Verticillium dahliae Kleb. Journal of Applied Microbiology. 2001;91(6):963-971
  69. 69. Kurze S, Bahl H, Dahl R, Berg G. Biological control of fungal strawberry diseases by Serratia plymuthica HRO-C48. Plant Disease. 2001;85(5):529-534
  70. 70. Tahmatsidou V, O’Sullivan J, Cassells AC, Voyiatzis D, Paroussi G. Comparison of AMF and PGPR inoculants for the suppression of Verticillium wilt of strawberry (Fragaria × ananassa cv. Selva). Applied Soil Ecology. 2006;32(3):316-324
  71. 71. Meszka B, Bielenin A. Bioproducts in control of strawberry Verticillium wilt. Phytopathologia. 2009;52:21-27
  72. 72. Steffek R, Spornberger A, Altenburger J. Detection of microsclerotia of Verticillium dahliae in soil samples and prospects to reduce the inoculum potential of the fungus in the soil. Agriculturae Conspectus Scientificus. 2007;71(4):145-148
  73. 73. Rahman M, Sabir AA, Mukta JA, Khan MM, Mohi-Ud-Din M, Miah MG, et al. Plant probiotic bacteria Bacillus and Paraburkholderia improve growth, yield and content of antioxidants in strawberry fruit. Scientific Reports. 2018;8(1):2504
  74. 74. Howard CM, Albregts EE. Anthracnose of strawberry fruit caused by Glomerella cingulata in Florida. Plant Disease. 1984;68(9):824-825
  75. 75. Pritts M, Wilcox W. Black root rot disease of strawberry. Cornell Small Fruits Newsletter. 1990;5(4):1-2
  76. 76. Louws F. Black Root Rot of Strawberry [Internet]. 2014. Available from: [Accessed: January 7, 2019]
  77. 77. Wing KB. Strawberry black root rot: A review. Advances in Strawberry Research. 1994;13:13-19
  78. 78. Cannon PF, Damm U, Johnston PR, Weir BS. Colletotrichum–current status and future directions. Studies in Mycology. 2012;73:181-213
  79. 79. Eastburn DM, Gubler WD. Strawberry anthracnose: Detection and survival of Colletotrichum acutatum in soil. Plant Disease. 1990;74(2):161-163
  80. 80. Debode J, Van Hemelrijck W, Xu XM, Maes M, Creemers P, Heungens K. Latent entry and spread of Colletotrichum acutatum (species complex) in strawberry fields. Plant Pathology. 2015;64(2):385-395
  81. 81. Leandro L, Gleason M, Nutter F, Wegulo S, Dixon P. Germination and sporulation of Colletotrichum acutatum on symptomless strawberry leaves. Phytopathology. 2001;91:659-664
  82. 82. Freeman S, Shalev Z, Katan J. Survival in soil of Colletotrichum acutatum and C. gloeosporioides pathogenic on strawberry. Plant Disease. 2002;86(9):965-970
  83. 83. McInnes TB, Black LL, Gatti JM. Disease-free plants for management of strawberry anthracnose. Plant Disease. 1992;76:260-264
  84. 84. Mass JL. Compendium of Strawberry Diseases. 2nd ed. Saint Paul, Minnesota, USA: APS Press; 1998. 128 p
  85. 85. Ploeg A. Biofumigation to manage plant-parasitic nematodes. In: Ciancio A, Mukerji KG, editors. Integrated Management and Biocontrol of Vegetable and Grain Crops Nematodes. 1st ed. Dordrecht: Springer; 2008. pp. 239-248
  86. 86. Martin FN. Development of alternative strategies for management of soilborne pathogens currently controlled with methyl bromide. Annual Review of Phytopathology. 2003;41:325-350
  87. 87. Klosterman SJ, Atallah ZK, Vallad GE, Subbarao KV. Diversity, pathogenicity, and management of Verticillium species. Annual Review of Phytopathology. 2009;47:39-62
  88. 88. Matthiessen JN, Kirkegaard JA. Biofumigation and enhanced biodegradation: Opportunity and challenge in soilborne pest and disease management. Critical Reviews in Plant Sciences. 2006;25(3):235-265
  89. 89. Gimsing AL, Kirkegaard JA. Glucosinolates and biofumigation: Fate of glucosinolates and their hydrolysis products in soil. Phytochemistry Reviews. 2009;8(1):299-310
  90. 90. Mattner SW, Porter IJ, Gounder RK, Shanks AL, Wren DJ, Allen D. Factors that impact on the ability of biofumigants to suppress fungal pathogens and weeds of strawberry. Crop Protection. 2008;27(8):1165-1173
  91. 91. Friberg H, Edel-Hermann V, Faivre C, Gautheron N, Fayolle L, Faloya V, et al. Cause and duration of mustard incorporation effects on soil-borne plant pathogenic fungi. Soil Biology and Biochemistry. 2009;41(10):2075-2084
  92. 92. Hansen ZR, Keinath AP. Increased pepper yields following incorporation of biofumigation cover crops and the effects on soilborne pathogen populations and pepper diseases. Applied Soil Ecology. 2013;63:67-77
  93. 93. Balzano R. Mustard Cover Crops Offer Benefits Beyond Soil Health [Internet]. 2017. Available from: [Accessed: December 19, 2018]
  94. 94. Bending GD, Lincoln SD. Characterisation of volatile sulphurcontaining compounds produced during decomposition of Brassica juncea tissues in soil. Soil Biology and Biochemistry. 1999;31:695-703
  95. 95. Morra MJ, Kirkegaard JA. Isothiocyanate release from soilincorporated Brassica tissues. Soil Biology and Biochemistry. 2002;34:163-1690
  96. 96. Gardiner J, Morra MJ, Eberlein CV, Brown PD, Borek V. Allelochemicals released in soil following incorporation of rapeseed (Brassica napus) green manures. Journal of Agricultural and Food Chemistry. 1999;47:3837-3842
  97. 97. Matthiessen JN, Warton B, Shackleton MA. The importance of plant maceration and water addition in achieving high Brassica-derived isothiocyanate levels in soil. Agroindustria. 2004;3:277-280
  98. 98. Goud JK, Termorshuizen AJ, Blok WJ, van Bruggen AH. Long-term effect of biological soil disinfestation on Verticillium wilt. Plant Disease. 2004;88(7):688-694
  99. 99. Messiha NA, van Diepeningen AD, Wenneker M, van Beuningen AR, Janse JD, Coenen TG, et al. Biological soil disinfestation (BSD), a new control method for potato brown rot, caused by Ralstonia solanacearum race 3 biovar 2. European Journal of Plant Pathology. 2007;117(4):403-415
  100. 100. Shennan C, Muramoto J, Lamers J, Rosskopf EN, Kokalis-Burelle N, Mazzola M, et al. Anaerobic soil disinfestation for soil borne disease control in strawberry and vegetable systems: current knowledge and future directions. In: VIII International Symposium on Chemical and Non-Chemical Soil and Substrate Disinfestation; 2004; Vol. 1044. pp. 165-175
  101. 101. Hewavitharana SS, Ruddell D, Mazzola M. Carbon source-dependent antifungal and nematicidal volatiles derived during anaerobic soil disinfestation. European Journal of Plant Pathology. 2014;140(1):39-52
  102. 102. Momma N, Kobara Y, Uematsu S, Kita N, Shinmura A. Development of biological soil disinfestations in Japan. Applied Microbiology and Biotechnology. 2013;97(9):3801-3809

Written By

Mahfuz Rahman, Mosaddiqur Rahman and Tofazzal Islam

Submitted: 04 July 2018 Reviewed: 29 January 2019 Published: 15 March 2019