NE1336: Improving Quality and Reducing Losses in Specialty Fruit Crops through Storage Technologies

(Multistate Research Project)

Status: Active

NE1336: Improving Quality and Reducing Losses in Specialty Fruit Crops through Storage Technologies

Duration: 10/01/2013 to 09/30/2018

Administrative Advisor(s):


NIFA Reps:


Statement of Issues and Justification

Statement of Issues and Justification

The Need

Fruits and vegetables are essential components of a healthy diet, and their consumption is associated with decreased risk of chronic diseases and in maintaining a healthy weight. Despite the widespread availability of fresh fruit, many Americans fall short of the recommended level of five servings per day. The foremost complaint of consumers is lack of variety and quality in fruit. To increase demand, producers have adopted numerous new cultivars and expanded production of other fruits to offer a wider array of high quality fresh fruit as a means of increasing profitability. Adoption of new techniques such as postharvest application of 1-methylcyclopropene (1-MCP) has also improved quality, but application to fruits other than apples entails different protocols and may alter storage methods. Evaluation of fruit characteristics such as flavor, color, antioxidants and texture has been expanded to further understand consumer demand, ensure that growers will have better quality fruits and vegetables for high value markets, and provide information for breeders so they can better tailor breeding objectives to fit consumer desires. The key to achieving increased consumption of fresh fruit, higher grower income, a more viable U.S. fruit industry, and improved export opportunities lies in providing the consumer with a diversity of fruit that has superior quality, appealing flavor, long shelf life, and that is safe and nutritionally dense.

Throughout the United States, diversification to produce fruits for local markets, organic production practices, and new techniques for growing season extension has led to expanded cultivation of many small fruits and fruit-type vegetables, but the postharvest requirements of cultivars and genotypes suitable to these systems often differ from those used in traditional systems. Hence, postharvest technologies must be developed or modified to extend storage life and maintain quality and safety in new fruit cultivars, and in organically produced and extended-season fruits.

One of the principal desires of producers of specialty horticultural crops is to increase local consumption of agricultural products grown within the locality. Small-scale producers are often in a comparatively advantageous location that allows access to the most populated regions of the U.S. An emphasis on sustainability and health has resulted in increased popularity of locally grown and marketed horticultural products, with most small-scale producers depending upon direct markets to sell their product(s). Small-scale producers must maintain the quality of their perishable commodities and increase storage life in order to recover costs and make a profit. Pricing of perishables is difficult during a short season, being largely determined by supply and demand in the marketplace. Thus, these producers are at a disadvantage when negotiating prices during the peak, high supply harvest period. With the means to extend the storage duration of their produce, growers would have the option to sell when and where the prices are higher and still have the ability to supply top-quality products to the market.

The emergent eat locally(locavore) movement among a growing number of consumers is a concept favorable to small producers. As most consumers buy their produce at large grocery chain stores that offer only token local produce at best, small growers must rely on farm markets, schools, restaurants, home delivery and cooperative buying groups, including community-supported agriculture. Expansion of the locavore movement is creating new opportunities for small-scale entrepreneurs. Based on research conducted by the USDA Economic Research Service, the movement was estimated to have generated $4.8 billion in sales in 2008, and it is projected that locally grown foods will have generated nearly $7 billion in sales in 2012. Thus, the rising locavore trend is gradually reshaping the economics of the agriculture industry and spurring a revival of small farms, something many thought would never happen. Additionally, the organic food industry in the U.S. has been growing at a rate of 20-30% per year for the past 10 years, with a commensurate increase in land farmed under certified organic management, and an increased need for research on organic production and handling systems, and organic produce marketing practices. For example, in Washington State, organic acreage has increased 8-fold since 1993 and the organic food industry is valued at over $200 million per year.

Deterioration of quality attributes such as texture and flavor, as well as development of storage disorders and rots, continues to cause losses for producers and marketers, especially with increased environmental variability during growing seasons. As a result, the fresh fruit industries rely on prophylactic postharvest chemical applications to ensure control of losses due to ripening, softening, senescence, decay, and development of storage disorders. While advances have been made in nontoxic alternatives or sustainable systems, changes in the types and amounts of available chemicals have created a need to modify storage technologies. New approaches are also required to meet needs of organic markets, minimize losses of fruit during storage and transport, and thereby maintain regional and global market shares for domestic producers as well as allow small-scale producers to maintain local market share. A better understanding of relationships between postharvest physiology of fruits and their susceptibility to physiological disorders and decay pathogens is essential for developing improved control measures and reducing chemical use.

Therefore, the intent of this project is to increase sales of specialty crops with a primary focus on apple fruit, the major fruit crop in most participating states. However, research with other important specialty crops is also critical to the project's success. The scale of industry ranges from large, in for example, the export-oriented states of Washington and California, to the smaller industries in the northeast, where a major goal is to extend the marketing period for local markets via improved shelf life. Therefore, while addressing the needs of large-scale operations, we will also extend and adapt knowledge, and solve new problems that arise, in order to meet the needs of smaller-scale operations.


Importance of the Work

The multistate project described here is focused on fruit, reflecting the continued investment in postharvest issues related to fruit by the Agricultural Experiment Stations. The project objectives address a range of postharvest issues of fruits throughout the US as well as Canada. Previous (NE103, NE1018) and current (NE1036) versions of this project have made major contributions to the fresh fruit industry. These include industry adoption of innovative applied methods developed by the group, and basic research on postharvest problems such as superficial scald and bitter pit in pome fruits, and chilling injury (CI) in stone fruits, which has led to more effective control measures and knowledge of the genetic and biochemical causes of the disorders. Nonchemical and reduced risk chemical methods of preventing losses have been studied as a way to extend storage life of highly perishable fruits such as berries. Over the past five years, members of NE1036 have conducted extensive research on postharvest nutritional quality of many types of fruits to identify and quantify antioxidative constituents beneficial to human health, and to determine how the content and composition of these phytonutrients are influenced by cultivar and storage methods. Studies on apples have continued with an emphasis on newly emerging problems such as browning disorders and CI, which cause major losses for producers. The commercialization of 1-methylcyclopropene (1-MCP), an ethylene action and ripening inhibitor, as a means to control ripening and maintain quality in storage of apple as well as an array of other fruits has developed into a critical area of research for this project.

Consumers prefer newer apple cultivars and are willing to pay more for them compared with older cultivars (Yue and Tong, 2011). New fruit cultivars such as the Honeycrisp apple have been widely planted in the U.S., and a number of physiological disorders limit continued expansion and threaten viability of the industry. As this cultivar is widely used in breeding programs across the United States, postharvest testing of Honeycrisp and its progeny, from different orchards and regions, will provide useful information to growers and shippers, especially those forming marketing cooperatives. Information on problems with both older, established cultivars and replacement cultivars in regional growing areas has become increasingly important as fossil fuels and food safety issues have made consumers more interested in regionally produced fruit.


Technical Feasibility of the Research and Advantages for Doing the Work as a Multistate Effort

As a group, NE1036 researchers actively collaborate to find solutions to problems faced by the fruit industry. The researchers in this project have an established track record for collaboration on projects across North America. The project continues to be active in developing solutions for industries that can be implemented quickly in order to maintain profitability, but the applied research is underpinned by a strong basic program that seeks to understand fruit physiology and biochemistry, particularly in relation to responses to technologies such as 1-MCP and CA storage regimes. The genetic and biochemical mechanisms involved in the induction of storage disorders, decay susceptibility, and fruit quality are being elucidated, often in association with grants based on research that was originally carried out under the auspices of this project. Future combined efforts hold the promise of developing new scald-resistant cultivars that do not require application of chemicals currently used to control the costly disorder, and in finding the causes of browning disorders such as bitter pit and chilling injuries. Increasing consumer appeal of U.S. fruit through improvement of texture, flavor, and aroma, and preventing losses for growers can best be approached by a broad array of sensory, physiological, biochemical, and molecular genetic techniques.

Storage protocols for temperate fruits are cultivar- and often region-specific, and must be optimized to reduce postharvest losses. The broad geographical distribution of the team in this project provides a unique situation where responses of cultivars to a wide range of growing conditions can be studied. To this end, several institutions have installed equivalent facilities, such as those for CA storage, enabling parallel investigations across regions. Through combined effort, the NE1036 works as a research and extension team to solve industry problems and to provide rapid dissemination of research results that would not occur without the organization of a multistate project. No individual state has the expertise and resources required to address all aspects and issues of fruit quality, but in a multistate project their respective strengths can be synergistically applied in a coordinated effort to investigate postharvest issues and problems, and provide much needed recommendations and solutions to the fresh fruit industry, both regionally and nationally.


Impacts

The accomplishments of the NE1036 project include extensive evaluation of fruit cultivars and development or modification of methodologies to best enhance storage life, quality, and flavor; and the elucidation of mechanisms involved in flavor and storage disorder development in fruits. 1-MCP was discovered by Sylvia Blankenship in partnership with Ed Sisler. Blankenship was a former member of this project. The pioneering research carried out by members of this project provided the research basis for industry confidence in the new technology. Another excellent example of impact resulting from our collaboration is the concerted effort of at least six research units participating in NE1036 to establish the best postharvest practices for the prized and profitable Honeycrisp apple in various regions of the U.S. and Canada; this one cultivar has changed the focus of North American growers as they have realized the return of investment from new and exciting cultivars. The NE1036 program has generated key information that has at least provided short term solutions to storage of this cultivar. In addition to successful transfer of information to researchers and industries via peer-reviewed publications, grower meetings and trade publications, a website has been developed.

The proposed new project will make similar valuable contributions, continuing to develop and improve methods and technologies for evaluation, maintenance, and genetic enhancement of postharvest quality of fresh fruits. The primary goals of our new research project are to increase competitiveness for domestic fruit production and preserve 'fresh-picked' sensory and nutritional quality, which in turn will increase the availability of locally grown and highly perishable fruit. To meet these goals, we will evaluate the economic potential and storability of new cultivars, make better use of existing storage technologies, and develop new, safer technologies requiring minimal use of chemicals. Economists involved in the project will aid in defining economic benefits of these technologies. The overall impact of this project will be to improve the long-range health of the American populace via greater consumption of fresh fruits, and to increase profitability of large-scale national as well as small-scale, local and organic fruit production.

One of the most valuable aspects of this Multistate Project is connections among members conducting basic research and those involved in applied science. Fundamental information relating to fruit physiology, molecular biology, and biochemistry is developed by some members of the Technical Committee and then used by other members to guide their more applied research. Examples of such collaborations include work on ethylene action and ripening, quality loss, biosynthesis of aroma and flavor compounds, and storage disorder development. Conversely, the applied research identifies and defines problems in a way that helps refine inquiry at the fundamental level. Techniques and methods developed by NE1036 members have led to advances in maintenance of fruit quality and consistency, reduction in pesticide use, and practices that are easily tailored for regional and small-scale fruit production systems. Annual reports are available on the NIMSS project website (http://nimss.umd.edu/homepages/home.cfm?trackID=10057), and publications resulting from this project for 2008-2012 are listed in Appendix B.

Related, Current and Previous Work

The NE1036 project has made significant contributions to postharvest fruit research and producers. Applied research has centered on pre- and postharvest conditions by focusing on new cultivar evaluation, susceptibility to and identification of the causes of storage disorders, methods of decay prevention, and postharvest quality loss. Extension outreach remains an integral function of the group to assist and educate growers and packinghouse operators on issues such as disease control and modification of sanitation, storage, and handling protocols. Fundamental research on the genetic and biochemical mechanisms of storage disorder development, volatile aroma/flavor production, and ripening and fruit quality is shared with collaborators to foster multi-systems approaches that will to contribute to the development of innovations and enhance applied research.

New Cultivars with Improved Quality

Production of new cultivars continues to expand for North American fruit industries and remains key to economic success. To address new needs, the NE1036 has expanded efforts in evaluation of apples, pears, cherries, plums, peaches, muscadine grape and berry fruit. Evaluation of new cultivars is a priority for small scale and local producers as well as large producers in states such as CA, MI, NY and WA.

Most work on new cultivars has been focused on the Honeycrisp (HC) apple. Due to its popularity with consumers and high profitability for producers, HC production has substantially increased making it one of the most widely grown cultivars in North America. However, HC is highly susceptible to physiological disorders including soggy breakdown, soft scald, and bitter pit. NE1036 researchers quickly developed strategies to minimize fruit losses. Maturity at harvest and storage temperature are two primary factors inducing low temperature disorders in HC, and conditioning has become an important technique for preventing these disorders (Watkins et al., 2004; DeLong et al., 2009, Moran et al., 2010; Watkins, 2011). Preharvest 1-MCP applications also reduce soft scald (DeEll and Ehsani-Mohaddam, 2010). Research on these and other contributing factors and preventative measures has enabled the industry to produce and store HC with reduced losses, though more research is needed. The cause of soft scald and soggy breakdown remains unclear. In addition, the limits to use of CA storage for HC because of susceptibility to CO2 injury are only now being addressed (Contreras and Beaudry, 2010; Kupferman and Mattheis, 2009; Watkins and Nock, 2012). Findings of the group have also been shared via web-based resources:

http://smfarm.cfans.umn.edu/HC.htm

http://postharvest.tfrec.wsu.edu/REP2010A.pdf,
http://www.apples.msu.edu/pdf/RegionalRecHC.pdf,
http://www.apples.msu.edu/pdf/HCStorageRpt09.pdf,
http://smfarm.cfans.umn.edu/RegionalReccs.pdf.

While CA is recommended for use in NS, no formal recommendations have been made in other regions. Safe CA storage is essential as increasing fruit volumes require longer storage durations to maintain fruit quality and industry profitability. Ambrosia and Jazz are two other new apple cultivars and these and other new selections from MN, NY and WA may need tailored storage methods (Tong et al., 2013; Brown et al., 2012). While chilling injury (CI) in HC has been attenuated through new storage methods, bitter pit remains a challenge (Watkins et al., 2003; Prange et al., 2010). Attempts to describe the unique physiology of HC compared with other apples show low expression of genes encoding cell wall related enzymes may be responsible to lack of softening (Harb et al., 2012).

Superior genotypes with reduced susceptibility to decay have also been studied as a possible method for nonchemical prevention. In blueberry, four genotypes were found to be resistant to Alternaria spp. and five were resistant to Colletotrichum spp., the two most prevalent postharvest diseases. (Hancock et al., 2008). Among different apple accessions resistance occurred in four apple accessions to C. acutatum and two accessions were resistant to both P. expansum and C. acutatum , and Penicillium solitum was indicated in apple fruit decay (Jurick et al., 2009; 2010).

Postharvest strategies for emerging production systems

Small fruits and vine crops, such as blackberry, raspberry, strawberry, blueberry, grape, and kiwifruit, have become more widely planted across the U.S. These fruits have a high cash value in both direct and commercial markets, and offer a viable income for small acreage growers. Constant evaluation of new cultivars for quality and ways to extend storage life in order to grow market share is needed. Extended season systems, such as row covers and plastic tunnels and primocane fruiting add value and quality to their crops, but require concomitant research support to identify appropriate cultivars, harvest, and storage strategies (Fernandez et al., 2011). Mechanical harvesting methods are being used by large acreage producers to cope with labor shortages, but storage methodologies have to be altered to deal with reduced fruit quality and increased decay until or if mechanical harvesting can be refined to reduce harvesting damage. The highly perishable nature of small fruit necessitates special measures to ensure their availability to consumers. CA storage and modified atmosphere packaging (MAP) can be used to extend storage life of berry fruits (Almairat et al., 2011; Alsmairat et al., 2011; Hancock et al., 2008; Song et al., 2010), but present challenges in achieving economic benefits (Hancock et al., 2008 Hancock et al., 2008). Altering packaging to biobased alternatives such as polystyrene or polyactic acid has shown promise in improving shelf life of blackberries and better sensory scores in blueberry (Almenar et al., 2010). These and other emerging polymers have unique properties including enhanced water vapor transmission rates, which prevents the formation of condensation in packages, which, in turn reduces the potential for bacterial proliferation. The implication is that both human and plant pathogen activity can be suppressed, but this supposition needs to be verified.


1-Methylcycloprene (1-MCP)

1-MCP is now widely used by the industry on standard apple cultivars, with research continuing on newer cultivars such as Ambrosia, Creston, Minneiska, Silken, SnowSweet, NY1, NY2 and advanced apple selections. Research has been conducted on other fruit crops to develop further protocols for commercial use on pears (Bai et al., 2006, 2009; Acuna et al., 2011; DeEll and Ehsani-Moghaddam, 2011), kiwifruit and plums (Ioannis et al., 2013).

Improving the effectiveness of 1-MCP continues to be an important focus of research as factors are identified that can improve or limit its absorption by fruit and effectiveness in inhibiting ethylene. For instance, 1-MCP levels can be compromised by wooden and cardboard bin and bin liner materials, but not by plastic bin materials or typical wall construction materials (Vallejo and Beaudry, 2010). The physics of 1-MCP depletion has been modeled to better predict the efficacy of 1-MCP applications (Ambaw, et al., 2010). Following fresh-cut processing, 1-MCP absorption by apple tissue is markedly enhanced through non-target sorption and may involve reactive oxygen species (Lee et al., 2012). Fruit responsiveness to 1-MCP decreases with increasing levels of internal ethylene, and a greater concentration is needed to slow fruit respiration, softening and ethylene production in avocado (Zhang et al., 2011). Ongoing research is being conducted to evaluate repeat applications under various storage regimens in addition to investigating interactions of 1-MCP with the preharvest drop chemicals napthaleneacetic acid (NAA) and aminoethoxyvinylglycine (AVG) (Lu et al., 2013; Nock and Watkins, 2013). Rapid treatment of fruit with 1-MCP after harvest can afford storage operators more freedom to delay CA storage application, but attention to cultivar, fruit maturity and susceptibility of fruit to storage disorders must be considered (Watkins and Nock, 2012). Preharvest application of 1-MCP has been studied as an alternative method to postharvest application for apple (DeEll and Ehsani-Moghaddam, 2010; Watkins et al., 2010) and pear (Villalobos-Acuna et al, 2010a). 1-MCP may be used on plums for storage at warmer temperatures and thereby avoid chilling injuries (Minas et al., 2013)

Industry use of 1-MCP on pear has been complicated by the need to prevent browning disorders and yet allow for ripening. The best timing of 1-MCP treatment was 3 d after harvest to provide the best balance of reduced disorder development during storage and the ability of Bartlett pears to soften adequately thereafter (DeEll and Ehsani-Mohaddam, 2011). Extended scald control can be achieved in d'Anjou pear by combining a low dose of 1-MCP to allow for normal ripening with a delayed application of ethoxyquin (Bai et al., 2009). Lower ethylene concentrations or warmer fruit temperature during treatment increased 1-MCP inhibition of ripening, and these two factors can be used as tools to modulate 1-MCP effect on Bartlett pears (Villalobos-Acuna et al., 2010b).

1-MCP affects fruit physiology and metabolism, particularly at the level of gene expression and enzyme activity. In tomato fruit, 1-MCP was shown to maintain ethylene receptors in highly phosphorylated form, indicative of 'receptor on' status and explaining, through negative regulation, the suppression of ethylene-responsive genes (Kamiyoshihara et al., 2012). For reasons not well understood, 1-MCP mediated maintenance of high phosphorylation is less persistent with fruit at more advanced stages of ripening. Studies have also included effects on metabolism of flavor compounds and antioxidants, synthesis of esters and other aroma volatiles, and ethylene perception and biosynthesis. 1-MCP has a relatively small effect on phytochemical groups in Empire apple (Fawbush et al., 2009) but resulted in higher total antioxidant capacity in McIntosh apple (MacLean et al., 2010).


Disorder Development

The NE1036 group continues to make major contributions to the prevention of disorder development and to our understanding of their genetic and molecular control, particularly superficial scald of apple and pear, carbon dioxide injury, flesh browning and bitter pit of apple, and CI of stone fruit. Identifying key changes in apple fruit under different storage conditions that are associated with development of major disorders has been a focus with the eventual goal of developing diagnostic biomarkers for prediction and to guide storage management and marketing (Rudell and Watkins, 2011).

Superficial scald affects many cultivars of pear and apple. Accumulation of farnesene and its CTols in peel tissue was more rapid in California-grown fruit with a greater degree of scald compared to Washington-grown fruit (Whitaker et al., 2009). Metabolomic profiling of apple peel during scald development showed extensive changes associated with scald, which precede actual symptom development (Rudell et al., 2011). Transgenic apples suppressed for ethylene biosynthesis genes can produce farnesene, which can in turn oxidize to free radicals and 6-methyl-5-hepten-2-one, leading to scald development (Pesis et al., 2009). Scald was eliminated by exposure of shade-grown apple to ultraviolet-white light, and this was associated with increased levels of endogenously-produced antioxidants (Rudell and Mattheis, 2009).

1-MCP can increase susceptibility of fruit to CO2 injuries (Fawbush et al., 2007; Argenta et al., 2010) that has caused significant losses to industries across North America. Currently the disorder is controlled by DPA, but fears about continued registration exist. Alternative strategies for control include CA delay treatments (DeEll and Ehsani-Moghaddam, 2012), but acceptable management systems have yet to be established.

Production of several apple cultivars is limited by a high degree of susceptibility to bitter pit. Understanding Ca deficiency disorders at the cellular level may lead to more effective preventative measures. Ca accumulation within cellular storage organelles and within the cell wall are involved in the development of bitter pit (de Freitas et al., 2010). The growth regulator, abscisic acid, reduced water loss by increasing apoplastic Ca content in fruit, and alleviates the Ca-related disorder blossom end rot in tomato (De Freitas et al., 2011a). A constitutively active Ca2+/H+ antiporter decreased Ca distribution within the apoplast and cytosol, increased vacuolar Ca, increased membrane leakage and increased blossom end rot in tomato (de Freitas et al., 2011b).

Several browning disorders of apple occur with unknown causes. Empire apples are susceptible to flesh browning in long-term CA storage, under low temperature or with 1 MCP at warmer storage (DeEll et al., 2010; Watkins and Liu, 2010; Jung and Watkins, 2011). Other conditions that can contribute to CI include preharvest use of the herbicide glyphosate (Rosenberger et al., 2010), and advanced maturity at harvest (James et al., 2010; Watkins and Liu, 2010). In fruit susceptible to firm flesh browning, polyphenol oxidase activity was greater in fruit flesh treated with 1-MCP, but no difference occurred in total phenolics or peroxidase activity (Jung and Watkins, 2011). Ascorbate peroxidase may be involved in development, but antioxidant metabolism does not appear to have a direct role (Lee et al., 2012). Gala stem-end browning is another internal chilling-related disorder that is also associated with later harvest and is exacerbated by 1-MCP (Rudell and Mattheis, unpublished). Braeburn browning disorder develops during hypoxic cold storage in elevated CO2 and is also prevented by DPA (Mattheis and Rudell, 2008). Browning was found to start early, with metabolomic differences between DPA-treated and untreated fruit began to occur one week in storage, with flesh browning co-occurring with increased acetaldehyde, ethanol and ethyl esters (Lee et al., 2012). These findings indicate that apple flesh browning is more complex and is initiated much earlier than previously thought.

CI continues to be a barrier to storage and quality of the stone fruits, peach, nectarine, plum, pluot, cherry and apricot. CI is expressed as flesh mealiness, translucence or browning, and symptoms are more severe when fruit are stored at temperatures in the range of 2-8C (Crisosto et al., 1999); the temperatures best suited for long storage life. Application of conditioning CI in stone fruits is species dependent. In peach, conditioning or delaying cold storage for 24-48 hours improved sensory attributes compared to non-conditioned peaches during and after a cold storage period of 40 days (Infante et al., 2009). However, delayed storage of plum resulted in more extensive flesh reddening than non-delayed fruit with increased phenylalanine ammonia-lyase and greater anthocyanin accumulation (Manganaris et al., 2008a). CI is highly influenced by genetic background (Peace et al., 2006), with indications of quantitative inheritance, and for selection for resistant genotypes (Cantin et al., 2010). Endopolygalacturonase (PG) which controls the Freestone-Melting flesh locus, provides resistance to mealiness in nonmelting flesh peach (Martinez-Garcia et al., 2012). The predominant effect of chilling on the activity, protein accumulation and gene expression of PG did not correlate with pectin solubilization and depolymerization (Rugkong et al., 2010). Phenolics may be involved in metabolic changes associated with mealiness of peaches (Tsantili et al., 2010).

Nutrition and Phytochemicals

Phytochemicals encompass a host of nutritive and non-nutritive compounds found in plants that offer protective effects against chronic and degenerative diseases. Cranberry proanthocyanidins inhibit acid-induced cell proliferation in human esophageal adenocarinoma cells (Kresty et al., 2008). Incorporation of freeze-dried mango in the diet of mice improved glucose tolerance and lipid profile and reduced adiposity associated with a high fat diet (Lucas et al., 2011). Intake of dried watermelon decreased arterial blood pressure in borderline hypertensive subjects (Figueroa et al, 2011). While there is great interest in using fresh fruits and vegetables as potential alleviators of chronic diseases in medical and nutritional fields, the effects of postharvest treatments or storage on subsequent phytonutrient protection or manipulation are less studied but equally important. Jewel strawberries harvested at ¾ red and stored below 10 oC up to 12 d maintained n antioxidant and antiproliferation activities (Shin et al., 2007, 2008). However, fully red strawberries showed a loss in both antioxidant and antiproliferation activities with storage longer than 5 d.

Some of the important phytonutrient groups include phenolics, nitrogenous compounds, ascorbic acid, glutathione, tocopherols, and carotenoids. The NE1036 has researched how genotype, environment and postharvest procedures impact these compounds. Flavonoid composition of fall fruiting raspberries is affected by genotype and hours exposed to temperatures over 29 °C (Bradish et al., 2012). Vaccinium fruit had a high phenolic concentration compared to non-Vaccinium fruit, and some Vaccinium fruit were particularly rich in certain phenolic subgroups, especially anthocyanins and proanthocyanidins (Kalt et al., 2007). Muscadine grapes contain,a range of phenolics such as resveratrol, anthocyanins and ellagic acid, (Stringer et al., 2009). Mango cultivars can differ widely in in ²-carotene, ascorbic acid, and epigallocatechins (Manthey and Perkins-Veazie, 2009). Fruit of the cultivated eggplant species Solanum melongena, S. aethiopicum, and S. macrocarpon, and wild relatives have a high content of hydroxycinnamic acid conjugates and two new malonated caffeoylquinic acid isomers found in fruit of wild eggplant relatives (Ma et al., 2010; 2011). Watermelon genotype is the primary factor affecting lycopene content, while environment may affect the amino acidrulline (Perkins-Veazie, 2010). The influence of production, germplasm, storage conditions, and storage treatments on fruit phytochemicals and the synergistic effects in human health is still largely unknown.

Flavor, quality and consumer preference/liking

Methods that extend storage life such as 1-MCP, CA storage and packaging can impact flavor and consumer acceptance. Volatile production in apple is impaired by ripening inhibition and storage handling (Bangerth et al., 2012). Aroma volatile biosynthesis is reduced by CA storage, low temperature and 1-MCP. 1-MCP treatment of Gala apple reduced volatile production as well as alcohol acyl CoA transferase, which is responsible for the conversion of alcohols to esters (Singh et al., 2010). Consumers could distinguish between 1-MCP treated and untreated apples, but had no overall difference in preference (Marin et al., 2009). The volatile profile of apple fruit was characterized to develop guidelines for selecting new cultivars for desired flavor traits (Sugimoto et al., 2008, 2011).

In other fruit, 1-MCP applied to plums decreases consumer acceptance of high acid, but not low acid, cultivars (Ioannis et al., 2013). Consumers could distinguish between blueberries from different packages and preferred those packaged in the PLA containers (Almenar et al., 2009). The buildup of off-flavors was largely delayed in chitosan-coated berries, and the levels of ethyl butanoate and ethyl hexanoate, important contributors to strawberry aroma related to fruity and sweet notes, were found to be enhanced in coated fruit (Alemanar et al., 2009). Consumer sensory perceptions differ among fruits and must be defined to improve appeal for initial and repeat consumption.
In apple, aroma biosynthesis was associated with changes in gene expression during development (Park et al., 2007; Sugimoto et al., 2008). Linkages were found between ester biosynthesis and the expression of putative genes for amino acid metabolism (branched-chain aminotransferase and alpha-keto acid decarboxylase), beta-oxidation (acyl-CoA oxidase, enoyl-CoA hydratase, and acetyl-CoA acetyl transferase), ester formation (aminotransferase, alcohol dehydrogenase, and alcohol acyl transferase), and fatty acid oxidation (lipoxygenase), but not fatty acid biosynthesis (Sugimoto et al., 2008). Branched-chain amino acid accumulation was linked with the formation of branched-chain esters and data suggested the presence of an alternative pathway for their synthesis could be present in apple, similar to that demonstrated for some bacteria (Sugimoto et al., 2011)

A gene map for peach CI susceptibility was constructed and contains 133 candidate genes implicated in fruit ripening, softening, flavor, and pigmentation, and CI resistance (Ogundiwin et al., 2009). A Pop-DG map was constructed, covering 818 cM of the peach genome (Ogundiwin et al., 2009), as possible genetic markers of peach quality.

Objectives

  1. Optimize storage regimes for existing apple, pear, plum, cherry and berry cultivars, with emphasis on new cultivars arising from breeding programs in NY, BC, ON, MI, MN and WA.
  2. Investigate the effects of 1-MCP technology on fruit quality and storage disorders, and its interaction with cold storage and CA storage technology.
  3. Investigate the metabolic and physiological processes that underlie the responses of fruit to postharvest technologies.

Methods

Objective 1: Optimize storage regimes for existing apple, pear, plum, cherry and berry cultivars, with emphasis on new cultivars arising from breeding programs in NY, BC, ON, MI, MN and WA. We will characterize existing and emerging apple, plum, and cherry cultivars for their storage and shipping potential and for their susceptibility to storage defects (BC, ME, MI, MN, NC, NY-G, NY-I, ON, OR, WA-P, WA-USDA). Optimum harvest dates using existing harvest indices such as internal ethylene concentration (IEC), starch content, texture, and coloration will be determined. In appropriate instances, non-destructive instrumentation for maturity analysis will be either evaluated or developed (e.g., portable near infrared spectrometers for determining chlorophyll content). Storage conditions for these cultivars will be optimized for air and controlled atmosphere (CA) conditions by evaluating combinations of temperatures and atmospheres according to established protocols. Collaborative efforts on storage of Honeycrisp and its progeny will continue with emphasis on controlling chilling injury (e.g., soft scald and soggy breakdown) using conditioning treatments that do not cause unacceptable losses due to bitter pit and a deterioration in condition (MI, MN, NY-I, ON, WA-P, WA-USDA). Collaborative research on Honeycrisp will also include CA storage, where susceptibility to injury by low oxygen and carbon dioxide limits the usefulness of this storage technique in most growing regions. While group members have shown that the antioxidant diphenylamine (DPA) is an effective means of controlling injury due to storage atmospheres, a non-chemical means of control is needed. Optimizing preconditioning strategies to reduce CA-related injury and exploring alternative storage strategies will be priorities. In addition, the relationship between crop load (NY-I) on fruit quality, and leaf chlorosis (MN) on internal browning will be investigated. Modified atmosphere packaging (MAP) technology continues to be a investigated as a supplement to refrigerated air storage for berry crops (MI, OR) and as a replacement for CA storage of pear cultivars in OR and extended to other regions if results are promising. There are significant data gaps in respiratory physiology and optimum atmospheres in MAP for long-term storage and long-distance shipping with temperature fluctuation for Bartlett and other cultivars. MAP and retail packaging technologies, and studying the mechanism and practical solutions to postharvest splitting, pitting, and stem browning of sweet cherries, especially the newly commercialized late season cultivars will be improved and optimized (OR). Differences among cherry varieties in their fruit quality will be noted in response to pre-harvest application of gibberellic acid and post-harvest use of modified atmosphere packaging, with future use of such information to inform breeding options (WA-P). Emerging polymeric materials such as polylactic acid and nylon, which have extremely high rates of water vapor transmission are being investigated in MI as a means to achieve a modified atmosphere without attendant condensation in packed and shipped fresh produce. In addition, these and other polymeric materials are to be evaluated for their effectiveness in MAP of Chilean blueberry fruit using microperforations (MI). Where appropriate, final flavor quality of the product through descriptive and consumer sensory evaluations are included in an effort to enhance the flavor quality of produce available to U.S. consumers. Objective 2: Investigate the effects of 1-MCP technology on fruit quality and storage disorders, and its interaction with cold storage and CA storage technology The use of 1-MCP to control superficial scald and other disorders of apples and pears will continue to be refined and disorders such as CO2 injury that are sometimes enhanced by 1-MCP will be investigated (MI, NY-I, OR, WA-P). At OR and WA-USDA, a focus of 1-MCP research will be on the use of 1-MCP to extend the packing season and control superficial scald of d'Anjou, particularly with the goal of eliminating use of the antioxidant ethoxyquin. The research goal is to develop commercial protocols for extending packing season and controlling scald through postharvest application of 1-MCP at commercially manageable dosage while allowing ripening of d'Anjou to outstanding eating quality. Also, pre- and postharvest factors influencing the variable responses of Bartlett pears to 1-MCP treatments will continue (OR).

Increased susceptibility of apple cultivars to the physiological storage disorders of internal browning and carbon dioxide injury if treated with 1-MCP continues to be a major limiting factor for long-term storage and marketability. The susceptibility of new selections from breeding programs to 1-MCP-enhanced storage disorders will be assessed and investigated using laser confocal fluorescence microscopy of tissues from samples (WA-P) with and without MCP treatment. Storage of the NE cultivar, Empire, which the fresh market and the fresh cut industry would prefer to have on a 12-month basis, is severely limited because of 1-MCP induced browning. Optimization of storage conditions, including using multiple 1-MCP treatments in air, to avoid the disorder will continue (MI, NY-I).

Optimization on the use of 1-MCP for kiwifruit, persimmon, white-fleshed peaches, and plums will also be carried out (CA). In plums, 1-MCP will be used as a tool to avoid chilling injury from exposure to chilling temperatures and to save energy by storing and transporting fruit at temperature above 7.2 ºC. In kiwifruit, optimum concentration and timing of application is needed. Preliminary data indicates that 1-MCP treated kiwifruit will be storage-compatible with apples and other ethylene producing commodities. In pear, we will continue to explore the relationship between ethylene and 1-MCP in the headspace during treatment, and the role of fruit maturity in response to 1-MCP. The impact of 1-MCP on consumer acceptance will be evaluated for apple (MI, ON) and stone fruit (CA).

Objective 3: Investigate the metabolic and physiological processes that underlie the responses of fruit to postharvest technologies.

Commercial findings with 1-MCP show variations among fruit types, cultivars and ripening stage in responsiveness to treatment but information on the physiological and biochemical bases for these differences is lacking. Factors addressed will include internal ethylene concentration, accumulation and post-exposure changes in internal [1-MCP], non-target binding and oxidation of 1-MCP, and ethylene-receptor phosphorylation status. FL will investigate the physical and biological factors contributing to 1-MCP ingress and responsiveness in intact and fresh-cut tomato, avocado and apple fruits. The overall goal is to provide information that could lead to improved 1-MCP-application strategies.

Genomic, proteomic and metabolomic changes in apple fruit that are related to development of storage disorders will be investigated with the goal of characterizing the physiological basis for apple fruit necrotic disorders and identify bio markers associated with disorder development by two groups. Disorders include soft scald in Ambrosia and Honeycrisp (NS, USDA-WA), and superficial scald (USDA-WA). Quantitative proteomics including peptides dimethyl labelling and multiple reaction monitoring (SRM/MRM, LC/MS) will be used for profiling and targeted protein analysis. Untargeted metabolic profiling using GC-MS and LC-MS will be used for the metabolomics evaluations (USDA-WA).

The role of ethylene in the induction and progression of cell death processes in intact and fresh-cut cucumber fruit will be investigated (FL). Ethylene is known to be involved in the induction and progression of postharvest storage disorders, including tissue watersoaking in several fruits of the Cucurbitaceae. Using cucumber fruit as a model system, the role of programmed cell death (PCD) in the development of ethylene-induced watersoaking and other storage disorders will be explored. Our future studies will address ethylene-responsive nucleases and proteases as executioners in PCD and watersoaking. We will also explore ethylene-induced respiratory increases and hyper-production of reactive oxygen species as early signals in the induction of watersoaking and other disorders.

The molecular mechanisms governing natural and stress-induced deterioration of fresh produce quality during postharvest storage and shelf life will be studied (USDA-MD, CA). Mechanisms of cellular localization of calcium and its influence on fruit susceptibility to calcium deficiency disorders in tomato and apple will be studied by following the effects of stress and growth regulators on calcium distribution within the cells and within the plant (CA). Sap flow meters will be used to estimate sap and calcium flux from stems into fruit and leaves as affected by various external factors. Genes that regulate or otherwise determine the rate of natural or stress-induced deterioration of quality will be identified, characterized, and manipulated (USDA-MD, CA). The approach will be include two complementary directions: 1) exploration of the role of calcium in fruit ripening, senescence, and stress responses via regulation of genes, transcription factors, and enzymes; and 2) down-regulation or knockout of genes encoding enzymes thought to play key roles in degradation of cell membranes or in synthesis of stress metabolites. Additional research on apple will focus on the involvement of farnesene synthesis on the storage disorder superficial scald. Peach cultivars can sometimes develop off-flavor, mealy texture, flesh browning and pit bleeding in response to low storage temperatures. The genetic control of chilling injury of peaches will be elucidated using analyses of the transcriptome, proteome, and metabolome in populations that segregate for chilling symptoms (CA). Volatile analysis of mealy and sound fruit during ripening will complement these studies. This research, supported by the peach gene sequence and advances from previous research, should lead to an improved understanding of the mechanism of chilling injury at the molecular level. Research to improve fundamental knowledge and develop molecular tools to support development of new genetic lines of fruits and vegetables with superior with sensory quality and storage life will continue (CA, NC, USDA-WA, WA-P). In cherry and peach, systematic examination of gene expression for all members of the ethylene biosynthetic and signal transduction pathways will be undertaken to identify critical differences between the two species and key differences among sweet cherry cultivars (CA). This information will then used to examine the relationship between gene expression patterns and market life. An effort will be made to influence phytonutrient biology. The effects of storage methods on phytochemical composition of small fruits, as well as human health trials with watermelon, will be conducted (NC). Methods to bolster the content of phenylpropanoid secondary metabolites, recognized as health-beneficial compounds in fruits and vegetables will be developed at USDA-MD. The focus will be on enhancement of anthocyanin and flavonoid accumulation or bioavailability in sweet cherry and strawberry, and synthesis of novel hydroxycinnamic acid-polyamine conjugates in eggplant and related crops. Aroma is a critical aspect of the quality of all fresh fruits and fruit products. Progress has been made in identifying genes involved in the biosynthesis of precursors for straight-chain and branched-chain ester production in melon and apple (CA, MI). Characterizing the pathways of ester biosynthesis using biochemical, genomic and biotechnological approaches will continue. In MI, the involvement of de novo biosynthesis of short-chain fatty acids as ester precursors will be explored on intact fruit. Pathways for exploration include one- and two-carbon fatty acid elongation pathways. In addition, involvement of members of the lipoxygenase gene family will be explored in intact as well as masticated fruit (MI). A transient overexpression/silencing system for testing candidate gene function in vivo in melon fruit is in development (CA). This technique will also be used for screening of candidate genes involved in the regulation of aroma biosynthetic pathways. In addition, development of rapid methods for aroma analysis in fruit will continue (CA). An ultra-fast GC-SAW system for the development of robust screening tools for aroma quality analysis in fruit will be employed, and other promising rapid methods (electronic noses), will be compared with "gold standard" GC-MS measurements, as well as sensory perception by trained sensory and consumer panels.

Measurement of Progress and Results

Outputs

  • Optimum harvest and storage parameters will be defined for four new apple selections from breeding programs in BC, NY, MN and WA to ensure high quality fruit for the consumer and to provide the industry with the information needed to ensure that quality in the marketplace.
  • Safe and effective air and CA storage regimes will be identified for Honeycrisp apples grown in all regions of North America to ensure that increasing volumes of fruit can be stored for up to 10 months.
  • The optimum pre-harvest factors (harvest maturity, crop load, and PGRs) and postharvest practices for improving shipping quality will be studied for the new sweet cherry, pear and plum cultivars.
  • Optimum MAP conditions for long-term storage (replacing CA) and long-distance sea transportation (with temperature fluctuations) of pear varieties will be determined to ensure arrival quality at exporting markets. The MAP conditions for long-distance sea shipping and perforation of retail packaging will be optimized to ensure arrival quality and consumer acceptance for the PNW sweet cherry cultivars. New polymers having high water vapor transport will be characterized and their potential for consumer-sized and bulk packaging of blueberry and other perishables will be determined.
  • Develop methods that allow application of 1-MCP to pears, kiwifruit, persimmon, peaches and plums with appropriate ripening characteristics for the consumer.
  • Develop strategies to avoid carbon dioxide injuries and flesh browning that are enhanced by postharvest applications of 1-MCP.
  • Basic understanding of the action of 1-MCP, its binding and metabolism to target and non-target materials will lead to improved application strategies.
  • The genomic and metabolomic changes underlying development of four physiological disorders of apple and peach will be investigated.
  • A basic understanding of the development of calcium deficiency disorders will be gained and genes associated with fruit susceptibility to calcium deficiency disorders will be identified for use by fruit breeders. Improved field treatments will be developed for use by the industry to control calcium deficiencies in fruit.
  • Increase knowledge of the biochemistry of aroma volatile production by apple and other fruit crops. Focus will be on the formation of precursors for the formation of esters and on the synthesis of aldehydes and alcohols. Pathways of interest include fatty acid biosynthesis and lipid oxidation.
  • Identify and clone genes encoding calcium/calmodulin-regulated, lipid catabolic, and stress-induced proteins with potential roles in ripening, senescence, and stress metabolism in fresh fruits; those that can be manipulated to enhance production and retention of anthocyanins and other flavonoids in rosaceous fruits including sweet cherry and strawberry; and those involved in biosynthesis of health-beneficial hydroxycinnamic acid conjugates in eggplant and related wild Solanum species.

Outcomes or Projected Impacts

  • Knowledge gained from research on harvest and postharvest performance of new apple, pear, plum, cherry and berry cultivars will help fruit breeders in making future selections, and aid industry partners to ensure high quality fruit for the consumer.
  • The identification of safe CA storage regimes for the Honeycrisp apple cultivar will allow marketing over at least a 10 month period, thereby extending the season of availability and maintaining profitability for grower and storage operators.
  • The optimum MAP conditions, high CO2/O2 injury thresholds, and respiration dynamics affected by cultivars, temperature, and O2 and CO2 concentrations are essential knowledge for the industry to adopt MAP technologies successfully to extend packing season and ensure arrival quality of pear, blueberry and sweet cherry varieties at export markets.
  • Identification of storage protocols to avoid the 1-MCP enhanced physiological disorders of carbon dioxide injury and flesh browning will improve storage operator confidence in affected cultivars and increase their storage potential.
  • Develop a better understanding of genetic and metabolic mechanisms that determine the postharvest quality and storage life of fruits, which can be applied to devise new strategies to maintain quality and reduce losses due to ripening, senescence, and physiological disorders.
  • Improved understanding of metabolic processes that precede or coincide with chilling-related cell death disorder of apple and peach fruit during cold storage. These disorders result in serious yearly losses to U.S. producers and research is expected to contribute to more accurate approaches to monitoring fruit storage for risk of disorder development as well as a better understanding of the genes that are related to their provocation during storage. Such information may be used to develop means to reduce breeder selections that are susceptible to chilling-related disorders.
  • Information on the reasons for variable responses of fruit to 1-MCP will lead to improved strategies for 1-MCP application and thereby better economic returns for growers and storage operators.
  • Furthering our understanding of how calcium deficiency develops will allow for development of more effective control strategies for practitioners to reduce the high losses that frequently occur. In addition, identifying genes associated with fruit susceptibility will allow fruit breeders to avoid releasing susceptible cultivars.
  • Identification of the pathways and genes involved in the formation of aroma will improve the capacity of breeders to identify lines with potential for elevated aroma compound production and will help identify biological mechanisms involved in the decline in capacity for aroma production as a result of postharvest handling practices. The development of better tasting produce could also have a positive impact on consumers dietary choices by increasing acceptance of fruits and vegetables.
  • Development of nutritionally enhanced lines of sweet cherry and strawberry bearing fruit, and food lines of eggplant and possibly other solanaceous fruits will lead to higher concentrations of health-beneficial phytonutrients in fruits and vegetables.

Milestones

(2014):
  • Responses of at least four new apple, pear, plum, cherry and berry selections/cultivars to air and CA storage will be published;
  • Studies contrasting metabolism among stress related physiological disorders of apple fruit will be published;
  • The role of cytokinins and auxins in calcium deficiency development in fruit will be studied;
  • At least two papers on the metabolism of 1-MCP in fruit will be published, and a predictive model for pear fruit response to 1-MCP tested;
  • The involvement of lipoxygenase in the formation of aroma volatiles in apple and associations with sensory changes will be defined;
  • A study on the diversity of esters produced by members of the Geneva Malus Core collection will be published;
  • Transgenic SlSR gene tomato lines for extended storage and shelf life, and increased resistance to biotic and abiotic stress will be tested;
  • Tomato and eggplant tissues will be silenced or over-expressed with constructs of previously identified members of the tomato SlSR gene family encoding calcium/calmodulin-binding transcription factors, specific SHT genes and select transgenic lines exhibiting the highest levels of SHT expression;
  • A silencing construct of Law Rome apple AFS1 cDNA in suitable binary vector will be used to transform Granny Smith apple shoot tissue. Granny Smith transformants exhibiting the greatest degree of suppression of AFS1 and graft shoots onto suitable rootstock to induce rapid flowering and fruit development will be selected.


(2015):
  • Deliver protocols to small-scale producers in the NE for harvest and storage of novel plum and apple cultivars;
  • Publish recommendations for minimizing chilling and CA injury of Honeycrisp and other sensitive apple cultivars;
  • Publish at least one paper on preharvest factors that affect Honeycrisp apple storage;
  • Publish one study on harvest and storage of new plum cultivars;
  • Present findings to stakeholders and publish at least two papers on the links between metabolic processes with different apple and peach postharvest disorders;
  • Provide the pear and blueberry industries with the optimum MAP conditions, high CO2/O2 injury thresholds as influenced by temperature fluctuations, and identify films with the right gas permeability for long-term cold storage and long-distance sea shipment;
  • Publish two studies on pear MAP;
  • Characterize lipoxygenase enzymes in apple and determine changes in their expression with shifts in fatty acid substrates. Evaluate the potential for the involvement of the 2-carbon fatty acid synthetic pathway in the formation of short-chain precursors to esters;
  • Publish one study on the involvement of lipoxygenase in aroma development in apple;
  • Transform strawberry tissue with over-expression construct of UDP glycosyltransferase gene FvUGT1 previously shown to be required for anthocyanin accumulation in strawberry fruit.


(2016):
  • Investigate and publish the impact of preconditioning protocols on the sensory quality of Honeycrisp apple fruit;
  • Responses of at least two new apple and berry selections/cultivars to air and CA storage will be published and presented to respective industries;
  • A review on the effects of 1-MCP on physiological disorders of fruits and vegetables will be written;
  • Evaluate the performance of high water vapor transport polymers on package atmosphere for fresh produce and determine their potential for quality maintenance;
  • Evaluate the expression of aroma biosynthetic genes and transcription factors involved in volatile biosynthesis regulation in model fruits;
  • Determine the genes involved in calcium deficiency development in fruit and the homogeneity of response across different types of fruit;
  • Evaluate transgenic strawberry lines over-expressing FvUGT1 for enhanced concentrations of anthocyanins and other flavonoid phytonutrients, and fruit from SHT transgenic eggplant an

    Projected Participation

    View Appendix E: Participation

    Outreach Plan

    Results of this research will be made available through refereed publications, (members of this project having excellent performance in publishing research results), conference papers and proceedings, project reports, on-line sources (web), and industry reports. Several participants have partial extension appointments and therefore will develop outreach materials through fact sheets and other extension publications. Extension publications include the Maine Apple Pest Report, NY Fruit Quarterly. In addition, states such as CA, ME, MI, NY and WA have extensive formal industry venues for presentation of results to growers. These include Storage workshops in MI and NY, which are held every two years, the New England Vegetable and Fruit Growers Conference and Trade Show, The NY Fruit and Vegetable Expo, Carolinas Fruit and Vegetable Expos, the NC Winter vegetable meeting, the SE Fruit and Vegetable Expo, Annual Hood River Winter Horticultural Meeting, Pear Packers Pre-harvest meeting, MN Apple Growers Association, and Great Lakes Horticulture meeting. UC Davis runs a number of specific outreach courses, e.g. Fruit Ripening and Retail Handling Workshop, each year.

    Several project participants attend and present regularly results at grower meetings in other states and Canadian provinces.

    Organization/Governance

    One person at each participating agency is designated, with approval of the agency director, as a voting member of the Technical Committee. Other persons at agencies are encouraged to participate as non-voting members. The Chair, Chair-Elect, Secretary, and Administrative Advisor will conduct the activities of the multistate project between annual meetings. Officers can be any member, including the official voting representatives. The officers are elected every second year by voting members and serve a two year term. A succession of officers from Secretary to Chair-Elect to Chair is normal, but is adjusted depending on circumstances.

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    Hertog, M.L.A.T.M., Rudell, D.R., Pedreschi, R., Schaffer, R.J., Geeraerd, A.H., Nicolai, B.M., Ferguson, I. 2011. Where systems biology meets postharvest. Postharv Biol Technol. 62:223-237.

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    Peck, G.M., Merwin, I.A., Watkins, C.B., Chapman, K.W., Padilla-Zakour, O.I. 2009. Maturity and quality of Liberty apple fruit under integrated and organic fruit production systems are similar. HortScience 44:1382-1389.

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