Abstract
Potatoes are at the heart of the world’s diet, being cultivated in more than 100 countries. Being the fourth largest crop after maize, wheat and rice, the potato production is of utmost interest for food industry, supporting a wide range of research projects. This is particularly the case of storage, an essential step for the potato industry, which is regularly studied. Indeed, sprouting of potatoes during storage is very problematic, resulting in a net loss for industries and increased food waste. Therefore, there has been a lot of research on sprout suppressive molecules since the beginning of the twentieth century. However, to date, there is no publication gathering all the studied molecules. This review presents an overview of the current knowledge on sprout suppressive molecules, natural and synthetic, along with a comparison of their effectiveness.
Resumen
Las papas están en el corazón de la dieta del mundo, cultivándose en más de 100 países. Siendo el cuarto mayor cultivo después del maíz, trigo y arroz, la producción de papa es de máximo interés para la industria alimentaria, respaldando una gran amplitud de proyectos de investigación. Esto es particularmente el caso de almacenamiento, un paso esencial en la industria de la papa que se estudia regularmente. De hecho, la brotación de las papas durante el almacenamiento es muy problemático, lo que resulta en pérdidas netas para la industria y en un aumento de desperdicio de comida. De aquí que ha habido mucha investigación en moléculas inhibidoras de la brotación desde principios del siglo 20. No obstante, a la fecha no hay una publicación que reúna a todas las moléculas estudiadas. Esta revisión presenta una vista general del conocimiento actual de moléculas supresoras de la brotación, naturales y sintéticas, junto con una comparación de su efectividad.
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Introduction
Although the history of potato began 8000 years ago in the Andean region of South America, it was only in the seventeenth century that this vegetable was adopted throughout Europe, and from there, imported to Asia before North America (International Year of the Potato 2008). Without being exhaustive, the average world’s production of potato represented 368.17 millions tons in 2018, with an average consumption of about 33.47 kg per capita in 2017 (FAOstat 2019). In North America, this number almost doubled to reach 53.79 kg per capita per year which places this vegetable as one of the most present in the North American diet (International Year of the Potato 2008; FAOstat 2019). Since markets must be supplied year-round, potatoes are stored from periods of up to several months. Long-term storage of potatoes can be problematic due to two main phenomena: spread of diseases and sprouting. In order to prevent these phenomena, a wide range of chemical products can be applied to avoid significant economic losses. Although, some of these products, such as chlorpropham (also known as CIPC), have demonstrated toxic properties for both, environment and consumer health, there are still widely used (Paul et al. 2015, 2018). In response, several governments are increasingly regulating and even considering banning the use of chlorpropham such as the European Union in June 2019 (Juncker 2019). Therefore, it becomes urgent to develop and market new sprout suppressive products, which are more environmental-friendly.
In order to develop alternative products, several research projects have investigated sprout suppressive properties of various molecules. To our knowledge, there is currently no review reporting on all the molecules (synthetic and natural) studied and their effectiveness as sprout suppressant. Therefore, the aim of this literature review is to gain an understanding of the existing research on sprout suppressive agents, and to present that knowledge into two categories: commercially available sprout suppressive products and molecules, which have shown promising results.
Storage
In order to manage different depository conditions, a reliable potato storage facility must be able to control temperature as well as humidity, and be equipped with a good ventilation system. Since potatoes may have been damaged during harvest, a pre-storage of potatoes under high relative humidity (95%) at 10–15 °C for about two weeks is usually done (Pinhero et al. 2009). The pre-storage conditions allow the potatoes to dry and heal the peel (Pinhero et al. 2009). After pre-storage, potatoes are generally stored in crates at lower temperatures for a period ranging from a few weeks to several months.
As previously mentioned, one of the main challenges during storage is early sprouting. After potato harvest, tubers are naturally dormant thus, no sprouting occurs. Unfortunately, this period of innate dormancy does not last as long as the storage period required by the market. Therefore, premature sprouting needs to be controlled, otherwise potatoes will lose weight and nutritional value. Moreover, the processing qualities of the tubers may be affected leading to major economic losses (Mani et al. 2014). Thus, inhibit sprouting by managing environmental conditions (e.g. cold temperature of storage, humidity regulation and regulated gas composition conditions) and by the application of chemical sprout suppressants (Fig. 1), help prevent these losses (Pinhero et al. 2009; Alamar et al. 2017). Regulating sprouting with chemical products comes with many challenges including the restriction of chlorpropham residues and the control of sweetening processes, ensuring tuber marketability (Alamar et al. 2017). Also, it is important to consider the storage conditions, which are different according to markets targeted. For example, cold storage is not an option for the processing sector because low temperatures increase the concentration of reducing sugars, which cause undesirable colours during frying (Wiltshire and Cobb 1996). Nevertheless, higher temperature storage of tubers is not a better option, because it increases tuber’s respiration and considerable weight loss occurs (Wiltshire and Cobb 1996). Taking that into account, potatoes to be sold for processing will be stored between 8 and 13 °C whereas the storage of fresh market potatoes is below 7 °C (Alamar et al. 2017). Processing potatoes thus need application of sprout suppressant to prevent tubers sprouting promoted by a higher storage temperature.
Sprout Suppressants Commercially Available and Currently Used
Used since the mid-twentieth century, chlorpropham (CIPC), a well-known cost effective potato sprout suppressant, is used as a postharvest product during storage. However, more and more studies shown that this product is dangerous for environment and consumer health because of the metabolites produced during its degradation and the long-lasting residues. Indeed, breakdown products of CIPC are more harmful than CIPC itself (Paul et al. 2015). For example, 3-chloroaniline (3-CA) is produced by thermal degradation of CIPC, a phenomenon which takes place during fogging and microbial or digestive activity (Paul et al. 2018). Although no studies show direct evidences of the carcinogenic effect of 3-chloroaniline (3-CA), 3-CA is highly toxic specifically on the haematopoietic and renal systems (m-Chloroaniline 1992; Arena et al. 2017). Furthermore, 3-CA has been suggested to be toxic because of its structural similarity to 4-CA known to be carcinogenic and genotoxic (Paul et al. 2018; Boehncke et al. 2003). Moreover, prolong and continuous use of CIPC lead to a gradual accumulation and its residues can be found everywhere. Actually, breakdown products of CIPC are not only found in fresh potatoes, they are also found in the processed potato products such as French fries and potatoes chips (Paul et al. 2018). CIPC residues have also been found in the oil used for frying and the water used for washing supporting the long-last presence of such residues (Paul et al. 2015, 2018). Furthermore, even in presence of low concentration of CIPC, cases of cross-contamination occurred and resulted in yield losses because of the presence of CIPC-residues exceeding the maximum level permitted (Douglas et al. 2019; Frazier and Olsen 2015).
Faced with this issue, many studies reported on alternatives less toxic and currently commercially available (Table 1). Astonishingly, CIPC is still used in over 90% of all current post-harvest sprout suppressant applications (AHDB 2020). However, it will be reduced since the ban on CIPC has begun in some countries notably the European Union (Juncker 2019).
In Canada, despite CIPC, active ingredients registered as sprout suppressant are 1,4-DMN, 2,6-DIPN, eugenol, maleic hydrazide and 3-decen-2-one (Agriculture et Agroalimentaire Canada 2017). In United States, we can add to the previous list R-carvone, hydrogen peroxide plus (Olsen 2016). In Europe, Talent is use as a sprout suppressant in the Netherlands since 1995 (Baker 1997) and orange oil is currently undergoing registration. Worldwide, organic potato production can rely clove oil, spearmint oil and caraway oil but they are also hydrogen peroxide plus and ethylene gas (Restrain) (Olsen 2016; Frazier et al. 2004).
Sprout suppressants can basically be classified according to their modes of action either preventive or curative. Preventive treatments act as a retardant to the sprouting process by prolonging dormancy through different physiological processes. For example, we can cite plant growth regulator analogs such as 2,6-DIPN or cell division inhibitor such as CIPC (Table 1). In opposition, curative treatments act by damaging sprouts, which is the case for most essential oils but also of 3-decen-2-one, HPP and CIPC. Since several of these products require several applications to maintain their effectiveness, many are currently used in combination with CIPC to ensure enhanced efficiency rate. This combination method allows to reduce both the cost of alternative product application since CIPC is cheaper and the maximum residues level of CIPC.
Beside CIPC breakdown products, residues from others sprout suppressants can also be an issue like hydrazine, a derivative of MH produce by plants, is reputed to be mutagen and carcinogen (Swietlinksa and Zuk 1978). Breakdown products of eugenol (by bacteria: ferulic acid, vanillin, vanillic acid (Tadasas and Kayahara 1983)), S-carvone (dihydrocarvone, dihydrocarveol (Patočka and Kuča 2013; Bhatia et al. 2008; Arena et al. 2018)) and HPP (oxygen, water) are considered to be safe while in other cases like 1,4-DMN (4-methyl-1-naphtanoic acid, 1-hydroxymethyl-4-naphtalene (European Food Safety Authority 2013)), 2,6-DIPN (2-[6(1-hydroxy-1-methyl)ethylnaphthalen-2-yl]-2-hydroxypionic acid (U.S. Environmental Protection Agency 2003; Höke and Zellerhoff 1998)) and 3-decen-2-one (2-decanone, 2-decanol (European Food Safety Authority 2015)), information about their toxicity is still missing.
Screening of Sprout Suppressant Molecules According to their Effectiveness
The search for molecules with sprout suppressive properties has been going on for several decades. Many studies have determined the efficiency of such molecules and they have been listed in Tables 2 and 3. Sprout suppressant molecules can be divided by their composition either single molecule or extracts. Single molecules are chemically synthesized in the lab or purified from a biological source (Table 2) whereas natural plant extracts (Table 3) which are composed of multiple molecules, biosynthesized by living organisms, all present in a mixture. Although the molecules tested in Table 2 are often of synthetic origin, it is important to note that most are also synthesized, in small amount, in plants. For example, various naphthalene molecules that have shown promising results (Table 2) have also been isolated from potatoes (Baker 1997). Yet, it was mostly chemically synthesized naphthalene molecules that were tested. It must be noted that the ranking of efficiency of the tables has been determined according to authors’ results and conclusions. It is also an approximation since the methodologies between each study differed.
The first report of use of plant extracts for their sprout suppressive properties can be traced back to the time of the Incas at the very beginning of potato cultivation. Indeed, the precursor to essential oils currently used were Muña plants, which are rich in essential oil and contain more than 98% monoterpenes (Song et al. 2008). Table 3 presents a list of plant extracts, mostly essential oils that have been tested for their sprout suppressant activities.
Many essential oils display sprout suppressant properties such as dill, coriander, spearmint and muña. However, many applications are required during storage period to maintain sprouting inhibition and since the production of essential oil is costly, it makes it difficult to implement these kinds of sprout suppressant on the market (Daniels-Lake et al. 2013; Raut and Karuppayil 2014; Martin 2013).
Could the Forest Resource Be an Avenue for Sprout Suppressive Molecules?
Canada’s forest resource is abundant, particularly in the province of Quebec where it represents 2.3% of the world’s forest (Delisle 2019). In 2018, Quebec forest industry generates alone about 2 million tons of anhydrous bark residues (Delisle 2019). Like essential oils, it has been demonstrate that barks molecules can possess a multitude of biological properties such as antioxidant, antimicrobial or anticancer (Royer et al. 2012). Then perhaps some bark extractions will have sprout suppressant properties especially since terpenoid and phenolic compounds can be enriched in bark extracts, and which are the same family compounds as found in essential oils gathered herein. In addition, because bark is a residue produced by sawmills, production cost could be lower than essential oils depending on the extraction process. This novel avenue is presently under investigation by UQTR and Innofibre.
Non-chemical Alternatives to Control Potato Sprouting
Beside the utilization of single or mixture of molecules for regulating sprouting during the storage of potatoes, other ways such as physical treatment (e.g. cold temperature, gamma radiation (Daniels-Lake et al. 2013; Rezaee et al. 2013), UV-C (Pristijono et al. 2018) or pressure treatments (Saraiva and Rodrigues 2011)) as well as biological treatment (e.g. micro-organisms (Slininger et al. 2000) or genetic engineering (Munger et al. 2015)) have been studied.
Future Perspectives
Overall, it is hard to recommend best possible options of sprout suppressant since there is a lot of variables to consider including if the production is organic or conventional, who is the end-user market, and what is the genetic variety of the potatoes (which influences dormancy period and susceptibility to diseases). The secret of managing potato sprouting probably lies in planification by coordinating applications of different treatment to retrieve maximum benefits from diversified mechanisms of action. This was the case with CIPC, before its was banned. For instance, prolonging dormancy with 2,6-DIPN (easier to apply then MH, because the window of application is easily missed with MH (Daniels-Lake et al. 2013)) combined with applications of essential oils like Talent which can also prevent the propagation of disease during storage (Baker 1997). By doing so, it would be possible to profit from the antimicrobial activity and the low toxicity of essential oil while reducing, at the same time, costs. Essential oils pose no problem regarding the storage of potato seeds in the same facility as the treated potatoes, compared to CIPC, since their effect is reversible and that their volatility makes it easy to clear the air of the storage facility from any chemical residues. Hopefully, bark extracts will prove themselves as sprout suppressant and eventually be more price competitive than essential oils.
Conclusion
Although CIPC is a sprout suppressant highly efficient and available at low cost, its consequences on environment and consumer health cannot be ignored which prompt for the development of alternatives. This review provided an overview of sprout suppressive molecules that have been tested and reported so far. A list of currently commercialized sprout suppressants along with promising molecules have been described to offer an overall guide for the research in this area. In addition, the efficiency of single molecules and mixtures of molecules from different essential oils was reported. Several alternatives showed promising results and can possess additional interesting activities such as antimicrobial, which is very valuable for industry. Indeed, the application of such agent will not only help to control sprouting and diseases of potatoes during storage but would also be cost-effective for the potato industry.
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Acknowledgements
The authors wish to thank Olivier Rezazgui for his helpful comments and for the revision of the manuscript. The authors gratefully acknowledge Mitacs and the Fonds de recherche du Québec Nature et technologies (FRQNT) for scholarship to M.B. Also, the Consortium de Recherche et Innovations en Bioprocédés Industriels au Québec (CRIBIQ), project number 2017-042-C30, is acknowledged for its financial support to N.B, S.B. and I.D-P. This review was also funded by the Canada Research Chair on plant specialized metabolism Award No 950-232164 to I.D-P. Thanks are extended to the Canadian taxpayers and to the Canadian government for supporting the Canada Research Chairs Program.
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Boivin, M., Bourdeau, N., Barnabé, S. et al. Sprout Suppressive Molecules Effective on Potato (Solanum tuberosum) Tubers during Storage: a Review. Am. J. Potato Res. 97, 451–463 (2020). https://doi.org/10.1007/s12230-020-09794-0
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DOI: https://doi.org/10.1007/s12230-020-09794-0