Improving apple quality by hot water treatment

Improving apple quality by hot water treatment PhD Thesis by Peter Maxin

Foreword This Ph.D. dissertation has been submitted to Aarhus University in partial fulfillment of the requirements of the degree Doctor of Philosophy. Dr. Hanne Lindhard Pederson (Associate Professor) was my primary supervisor until she left the University on 31 August 2011, at which time Dr. Michelle Williams (Head of Department) took on this responsibility. Dr. Roland Weber (Esteburg, Fruit Research and Advisory Centre, Jork; Germany) and Prof. Susan Lurie (Department of Food Science, Volcani Center, Israel) were co-supervisors. This study was conducted from 3 September 2008 to 9 December 2011 at the Department of Food Science, Aarhus University, located at Aarslev, Denmark. The study had a short-term interruption due to paternity leave for a total of 14 weeks. In February to March 2011, I stayed at the Esteburg Fruit Research and Advisory Center to carry out an ad hoc Ph.D. course. The primary focus of this Ph.D. project was apple fruit quality in relation to pre-storage hot-water treatments. The first year results showed neither an improvement nor any difference in physiological fruit quality following cold storage. Therefore, the main emphasis of the second and third project years was on fungal decay, the impact of hot water treatments, influences of pre-harvest factors on storage rot development and the introduction of a short term hot water treatment. Work on the latter aspect was initiated in October 2009 during a seven-day visit to the Volcani Center, Israel, where I worked with Professor Elazar Fallik. I am indebted to Roland Weber for his input and for the time we spend identifying the different fungi associated with storage rots. I also thank him for his contribution to PCR identification of the fungi which provided the opportunity to produce highimpact results. This thesis is presented in eight chapters. Chapter 1 is a general introduction on the Danish fruit growing sector and the connections to this study; Chapter 2 is a literature review on different fungi causing storage rots as well as commonly used chemical treatments and hot water treatments to reduce postharvest losses in apples. General methods that were used and developed in this Thesis are presented in Chapter 3. Chapter 4 contains a series of short trials that describe unpublished and preliminary results. It is the intention to repeat some of these findings for subsequent publication. i

Chapters 5 to 7 contain the results of key experimental work. In Chapter 8 key general results from this thesis are discussed, brief conclusions and a perspective for this technology are provided. References are contained in Chapter 9. I am very grateful for fruit donations generously made by Heinrich zum Felde (Jork), Alexander and Berbel Maxin (Jork), Peter Rolker (Jork), the Esteburg Centre and Michael Clever (Jork). This research needed a copious supply of plastic boxes, as used by many fruit farmers but not necessarily universities. I therefore extend my special thanks to Peter Rolker and to Bastian Benduhn (Esteburg Centre) for lending me the fruit storage boxes, and to Ørskov Frugt (Oure, Denmark) for shipping these boxes to Denmark and back to Germany. I also thank Berg GmbH and Jürgen Schacht (Jork) for their input of time and equipment in the first year trials on hot water rinsing. Carsten Sørensesn, Innotheque APS, Middelfart, Denmark generous provided time and initiative in developing and creating the prototype of a hot-water rinsing machine that could, after modifications, run the second year hot water rinsing experiments. Dr. Dirk Köpcke (Esteburg Centre) collaborated on both DCA and CA experiments, and stored hot water treated apples in his research facilities, therefore helping to clarify the behavior of pretreated fruit in these storage environments. I am very grateful to the technical staff at the Department of Food Science, Aarhus University, Aarslev, and especially to Annette and Stig Sørensen. A special “thank you” also goes to the secretarial staff for their smooth and efficient help with administrative matters. I am grateful for the support given to me by the Weber, Williams and Maxin families, and especially by my own family; Meike and Paul. This is in acknowledgement of the time my supervisors spent with me rather than their families, and of the time that I spent on the road instead of being at home. Thank you, Hanne, Michelle and Roland, for your critical advice in sharpening and polishing this Thesis and the various publications that form part of it. I thank my sister Uta Maxin for her input into improving the process figures in Chapter 4.

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Thanks are also given to all the colleagues at the Department of Food Science, Aarhus University for providing a collaborative, welcoming and positive study environment.

Thank you! Peter Maxin Aarslev; Denmark 25 March, 2012

This research was partially funded by the EU found ‘Isafruit’ (Project No. 016279), by the Danish Ministry of Food, Agriculture and Fisheries funded project ‘Bæredygtig fremtid for dansk konsumfrugt’ (J.nr: 3412-09-02385) and Plan Danmark funding.

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Table of contents Foreword ...................................................................................................................................................................... i Table of contents .................................................................................................................................................. iv Summary .................................................................................................................................................................. vii Resumé ...................................................................................................................................................................... ix Chapter 1: Introduction ...................................................................................................................................... 1 Chapter 2: Literature review .......................................................................................................................... 5 2.1 Scale of postharvest losses.................................................................................................................. 5 2.2 Incidence of storage-rot fungi........................................................................................................... 6 2.3 Postharvest fruit rots of apples ........................................................................................................ 10 2.4 Invasions of new fungi (neomycota) .......................................................................................... 22 2.5 Chemical control of storage rots................................................................................................... 24 2.6 Fungicides under pressure ............................................................................................................... 26 2.7 Control with heat, GRAS yeasts and hygiene ....................................................................... 28 2.8 Heat treatments...................................................................................................................................... 29 2.9 Apple Quality........................................................................................................................................... 32 Chapter 3: General methodology ............................................................................................................ 35 3.1 Introduction ............................................................................................................................................... 35 3.2 Example of the sequence of procedures of an entire experiment ............................ 35 3.3 Hot water dipping method............................................................................................................... 40 3.4 Hot water rinsing methods ............................................................................................................... 41 3.5 Identification of fungi .......................................................................................................................... 45 Chapter 4: Preliminary results ...................................................................................................................... 47 4.1 Pre-harvest effects on the development of storage rots ................................................. 47 4.2 Effects of HWT on fruit quality and physiology ..................................................................... 55 4.3 Effects of HWT on pathology .......................................................................................................... 73 Chapter 5: Paper 1 Hot-Water Dipping of Apples to Control Penicillium expansum, Neonectria galligena and Botrytis cinereaI: Effects of Temperature on Spore Germination and Fruit Rots ........................................................................................................................... 82 Summary ............................................................................................................................................................ 82 Introduction....................................................................................................................................................... 83 Materials and Methods ............................................................................................................................... 84 iv

Results .................................................................................................................................................................. 86 Discussion .......................................................................................................................................................... 91 Acknowledgements .................................................................................................................................... 95 References ........................................................................................................................................................ 96 Chapter 6: Paper 2 Control of Phacidiopycnis washingtonensis storage rot of apples by hot-water treatments but not by 1-MCP ...................................................................................... 100 Abstract ............................................................................................................................................................ 100 1

Introduction ........................................................................................................................................... 101

2

Materials and methods ................................................................................................................... 101

3

Results and discussion..................................................................................................................... 103

Acknowledgements ................................................................................................................................. 106 References ..................................................................................................................................................... 106 Chapter 7: Paper 3 Control of a wide range of storage rots in naturally infected apples by hot-water dipping and rinsing .......................................................................................... 108 Abstract ............................................................................................................................................................ 108 Keywords ........................................................................................................................................................ 109 1. Introduction............................................................................................................................................... 109 2. Materials and methods ...................................................................................................................... 110 3. Results .......................................................................................................................................................... 113 4. Discussion .................................................................................................................................................. 120 5. Conclusions .............................................................................................................................................. 122 Acknowledgements ................................................................................................................................. 123 References ..................................................................................................................................................... 123 Chapter 8: General Discussion................................................................................................................. 127 8.1 Hypotheses underlying this Thesis ............................................................................................ 127 8.2 Effects of delayed ripening on the incidence of storage rots .................................... 128 8.3 The influence of heat on spores and fruit ............................................................................. 131 8.4 Perspectives .......................................................................................................................................... 134 Chapter 9: Literature ...................................................................................................................................... 137

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Summary The Danish fruit industry has a focus on sustainable production systems. However, there is a need for new tools and technologies to enable orchardists to deliver quality fruit at competitive prices into the market. Research activities at Aarhus University aim to improve the availability and consumption of quality and healthy fruit. The use of postharvest hot-water treatments (HWT) can reduce storage losses of organically grown apples, as has been shown in several trials for different fungi. Preliminary results are presented as a follow up on different research activities in this Thesis. Seven short studies are aligned to three themes; pre harvest effect on the developing storage rots, effect of hot water treatments on fruit quality and physiology and effect of hot water treatments on pathology. The distribution of storage rot fungi in apples over two years was investigated in one orchard. The single-tree infection rate influenced by local inoculum and changing between years is reported. The influence of root pruning of different rootstocks on inoculum and decay rate in apples was investigated. The effect of crop load and nutrition level on fruit quality parameters (firmness, colour, sugar content, heat scald index) was also examined. Neither an improvement nor a quality decrease could be found following moderate hot water treatments. Hot water dipping (HWD) temperatures exceeding 54°C for 3 min resulted in severe heat scald. The influence of hot water rinsing (HWR), hot water dipping and 1-methycyclopropene (1-MCP) on the incidence of ‘Elstar’ skin spots under different atmosphere storage was evaluated. Evaporation of water through the fruit skin of HWR, HWD and cold water dipped control fruit was evaluated during a 36 h stress treatment. After 36 h, HWR treated fruit showed a trend towards a reduced loss of water through the cuticle relative to control fruit. The efficacy of HWD in limiting the further development of Sooty-blotch disease during storage was examined. Following HWD, Sooty-blotch fungi neither showed any further development in storage, nor was there any reduction in the existing mycelium. Hot water dipping (HWD) of spore suspensions of different storage rots was carried out to determine the effective temperature causing a 50% inhibition of spore viability (ET50) and the mortality curve in response to dipping temperature. Spore suspensions of Penicillium expansum, Neonectria galligena and Botrytis cinerea were used to inoculate apple fruit and to evaluate HWD efficacies in a wide range of vii

temperatures. Spores of P. expansum were inoculated both pre- and post-HWD. Similar developments of P. expansum rot in fruit inoculated pre- and post-HWD in the temperature range of 44-53°C led to a new perspective on the mode of action of HWD. An indirect effect of HWD as a heat-shock which induces the immune response of the fruit is contrasted with its direct inhibitory effect on fungal inoculum. A new storage rot, rubbery rot caused by the fungus Phacidiopycnis washingtonensis, was reported for the first time from Denmark. A description of the new rot, the orchard where it was detected and the incidence of decay were documented. The response of P. washingtonensis spores to HWD and the response of artificially inoculated fruit towards HWD were investigated. Naturally infected fruit with P. washingtonensis were subjected to HWD and HWR, and compared with fruit subjected to 1-MCP in both controlled atmosphere (CA) and dynamically controlled atmosphere (DCA) storage. The efficacies of HWD and HWR towards P. washingtonensis were comparable to Neofabraea spp. The influence of ripening inhibition caused by 1-MCP, CA or DCA did not influence the incidence of P. washingtonensis.. Combinations in time and temperature for rinsing and dipping of naturally infected apples in hot water were tested against natural infections of Neofabraea perenanns,

N. alba, N. galligena, B. cinerea, P. expansum, Monilinia fructigena, Colletrotricum acutatum, P. washingtonensis, Phoma exigua, Gibberella avenacea, Mucor spp. and Cladosporium spp. The influence of heat scald on the incidence of storage infections by P. expansum and a higher disease incidence by several pathogens following elevated temperatures were discussed. HWR showed comparable efficacies to HWD. Several advantages of HWR were discussed. The findings of this study are compared to previously reported and recent research results within the area of hot water dipping, fruit quality and fungal storage rots in apples. An overview on storage rots and postharvest control means is given in the context of organic farming. The general mode of action of HWT is evaluated for different fungi and apple varieties. Possible implementation strategies and perspectives of HWR for the apple industry are discussed.

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Resumé Den danske frugtbranche og Aarhus Universitet har i fællesskab sat fokus på bæredygtige produktionssystemer, som har til formål at forbedre adgangen til og forbruget af sund kvalitetsfrugt. I den forbindelse er der behov for at udvikle nye værktøjer og teknologier for at frugtavlerne kan producere kvalitetsfrugt til konkurrencedygtige priser. Brugen af varmtvands-behandlinger (HWT) efter høst er en sådan ny teknologi, som allerede har vist sig effektiv til bekæmpelse af flere forskellige rådsvampe i økologisk æbleproduktion. Der blev gennemført forsøg med neddypning af sporesuspensioner i varmtvand (HWD) og efterfølgende blev LD50 og mortalitetskurver for forskellige rådsvampe fastlagt i relation til vandets temperatur. Æbler blev podet med sporesuspensioner af Penicillium expansum, Neonectria galligena og Botrytis cinerea og effekten af HWD blev evalueret ved forskellige temperaturer. Sporer af P. expansum blev inokuleret både før og efter HWD (44-53° C) og efterfølgende sås en ensartet udvikling af P. expansum råd uafhængig af podningstidspunkt. Det førte til nye erkendelser omkring virkningsmekanismen bag HWD. Tidligere antog man HDW havde en direkte hæmmende effekt på svampesporerne, mens det nu forekommer sandsynligt, at der er tale om en indirekte virkning af HWD, hvor varmechokket inducerer en immunrespons i frugten. En ny lagersygdom forårsaget af svampen Phacidiopycnis washingtonensis, er fundet for første gang i Danmark. Symptomerne på sygdommen er en gummiagtig forrådnelse af hele frugten. Sygdommen er beskrevet og angrebsgraden og forekomsten i den plantage, hvor den blev fundet er dokumenteret. Virkningen af HDW på P. washingtonensis sporer og kunstig inokuleret frugt blev undersøgt. Naturligt inficeret frugt med P. washingtonensis blev udsat for HWD og varmtvandsoverbrusning (HWR), og sammenlignet med frugt der blev behandlet med SmartFresh (1-methylcyclopropen). Frugterne blev efterfølgende opbevaret under hhv. kontrolleret atmosfære (CA) og dynamisk kontrolleret atmosfære (DCA). Effekten af HWD og HWR mod P. washingtonensis var positiv og sammenlignelig med hvad der blev opnået overfor Neofabraea spp. Derimod havde SmartFresh, som

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hæmmer modningsprocesserne i frugten, ingen indflydelse på forekomsten af P. washingtonensis. Frugter der var naturligt inficeret med Neofabraea perenanns, N. alba, N. galligena, B. cinerea, P. expansum, Monilinia fructigena, Colletrotricum acutatum, P. washingtonensis , Phoma exigua, Gibberella avenacea, Mucor spp. og Cladosporium spp. blev dyppet eller overbruset med varmtvand i forskellige kombinationer af tid og temperatur. Ved både HWD og HWR kan for høje temperaturer forårsage skoldningsskader på frugten, som giver anledning til øgede angreb af P. expansum og andre patogener. HWR og HWD viste sammenlignelige virkningsgrader, og flere fordele ved HWR diskuteres. Yderligere resultater præsenteres mere kortfattet. Det blev undersøgt om HWD kunne begrænse den videre udvikling af sodplet under lagring, og der kunne ikke konstateres nyvækst af svampen på lageret, og eksisterende infektioner ikke kunne dræbes ved HWD. Forekomsten af lagersygdomme blev fulgt over 2 år i den samme plantage, og forskelle i infektionsgrader mellem træer og år blev beskrevet. Effekten af rodbeskæring på forekomsten af rådsvampe og tab under lagring blev undersøgt. Betydning af udbytteniveau og ernæringstilstand for forekomsten af skader efter HWD blev undersøgt. Det kunne konkluderes at moderat (og effektiv) HWD hverken forbedrede eller forringede frugtkvaliteten (fasthed, farve, sukkerindhold). HWD, hvor temperaturen overstiger 54° C i 3 minutter, resulterede i alvorlige skoldningsskader. Det blev undersøgt om frugterne mistede spændstighed (fordampning gennem frugtskrællen) efter behandling med HWD og HWR. Efter 36 timers varmestress tenderede de HWR behandlede frugter til at have mistet mindre vand end frugter som var behandlet med HWD eller kontrol frugter, som var dyppet i koldt vand. Resultaterne i denne afhandling er sammenlignet med tidligere publicerede forskningsresultater inden for området af varmtvandsbehandling, frugtkvalitet og lagersygdomme i æbler. Der gives en oversigt over lagersygdomme og mulige kontrolforanstaltninger indenfor en kontekst af økologisk frugtavl. Den overordnede virkningsmekanisme af HWT vurderes på forskellige svampe og æblesorter. Mulighederne for implementering og fremtidige strategier for HWR til brug i æbleindustrien diskuteres. x

Chapter 1: Introduction The fruit industry in Denmark is challenged by global competitors. Denmark’s economy is one of the strongest in the world in terms of per capita income (Einhorn and Logue 2010) and, therefore, it is an attractive market for all types of highly priced food products. Despite this competition in the market place, Danish apples are sold at high prices in the supermarkets. However, relatively little revenue is returned to Danish orchardists; in the years 2009 (reflecting the season 2008/9), 2010 and 2011 the average payment to growers was 2.75 DKK (=0.21€) per kg apples (pers. communication Ejvin Straaup, Langeland, DK). This return to the growers did not cover the production costs in established orchards, which were equivalent to 3 DKK (=0.23€) per kg apples (Pedersen 2006). Danish regulations currently disadvantage Danish orchardists in the market place. Danish growers must meet tight Danish regulations and yet they compete on their own market with imported fruit produced under different environmental and social requirements. For example, in 2009 the only registered active compounds for organically managed Danish orchards were wettable sulphur and Bacillus thuringiensis, whereas a comparable orchardist in Germany would have had access to more than 20 registered compounds (based on Annex II of the organic EU directive 2092/91 from 1991, subsequently replaced by EU directive 834/2007). In addition, production costs in Denmark are comparatively high as a result of high salary costs and taxation on pesticides and fertilizers. Previously, a reasonable income for orchardists in the years 2002 to 2005 (ca. 4-5 DKK/kg) led to enhanced planting activities in 2005 as well as 2006, thereby increasing the apple growing area. In Denmark 1,267 ha apples were cultivated in 2005, increasing to 1,609 ha in 2010. These numbers include organic apple orchards which increased from 158 ha in 2005 to 300 ha in 2010. To limit overhead in growers’ organizations (GO) and to reduce sales competition, restructuring and merging of some GO started in 2008 and has not yet been completed in 2012. The annual Danish apple season starts with the summer apple ‘Transparente’ which is harvested at the end of July in average years. Due to climate limitations, ‘Golden Delicious’ marks the latest possible variety with an approximate harvest time from 1

Chapter 1: Introduction

mid-October until early November. The average Danish apple consumption is 15 kg fresh apple per person per annum. The local production has a market share of 30%, the remaining demands being met by imports (Danmarks Statistik 2007). Danish fruits are marketed until March (Dansk Kernefrugt, 2011).

Figure 1.1: Variety spectrum of Danish apple production (1,486 ha in total) for the year 2007. Varieties grown on less than 20 ha (30% of the days having rainfall and an average temperature of 11-16°C for more than 8 h per day (Beresford and Kim 2011). Sporulation, spore dispersal and infections of N.

galligena are directly linked with rainfall (McCracken et al. 2003). Fruit infections by N. galligena can be categorized into two groups, i.e. eye rot (blossom-end rot) and lenticel rot (Table 2.1). The former develops from infections during blossom time, and the infection becomes clearly visible at the blossom end of the fruit by harvest time (Xu and Robinson 2010). Lenticel rot (Figure 2.3E) occurs during storage after a latency interval of several weeks as a result of infections originating from the field (Xu and Robinson 2010). During further storage, pale brown sporodochia of N. galligena are formed; these produce the highly diagnostic, elongated, 1- to 5-septate macroconidia of the Cylindrocarpon anamorph (Figure 2.3F). Lenticel rot caused by N. galligena has not so far been reported to be controlled by HWD. In fact, Maxin et al. (2005) found that its incidence increased after 1 min HWD at 49, 51 and 53°C compared to an untreated control, whereas there was no positive or negative influence on decay by 2 and 3 min HWD treatments. 2.3.3 Rubbery rot caused by Phacidiopycnis washingtonensis

Phacidiopycnis washingtonensis has only recently been identified as the cause of a fruit rot in American (Kim and Xiao 2006) and European (Weber 2011) apple production. From 2003–2006, in approximately 25% of the surveyed orchards of Washington State (USA), 1-4% of the apples were infected with P. washingtonensis (Kim and Xiao 2006). Following 9 months’ storage up to 24% losses caused by P.

washingtonensis were observed in ‘Red Delicious’ apples. Depending on the apple variety, invasion of P. washingtonensis occurred through stem end, calyx end, 12

Chapter 2: Literature review

lenticels or wounds (Kim and Xiao 2006; Weber 2012). The first report of P.

washingtonensis on apples in Europe was from the Lower Elbe region in Northern Germany, where fruit losses were below 1% in most orchards (Weber 2011). Mummified fruits of ‘Golden Hornet’ crabapples commonly planted as pollinators were identified as a major source of inoculum; fruit mummies of dessert apple varieties such as ‘Elstar’ were also infected, albeit to a lesser degree (Weber 2011). In Europe, cankers caused by P. washingtonensis have not yet been found. Mycelium of

P. washingtonensis may spread from an infected fruit to an adjacent intact fruit, causing clusters of rubbery rot (Weber 2012). Rubbery rot is a highly variable disease, appearing as a very pale but firm rot when fruit are removed from long-term storage under an atmosphere of reduced oxygen content, but rapidly undergoing a browning if sufficient oxygen becomes available during subsequent cold storage or at room temperature (Weber 2012). Conidiomata (pycnidia) are produced only on blackened fruit (Figure 2.3G). These extrude pale grey or yellow tendrils or drops of conidia which are hyaline, ellipsoid with pointed ends in outline, and contain two large or several smaller lipid droplets (Figure 2.3H). To date there are no reports on the efficacy of HWD on rubbery rot. 2.3.4 Bitter rot (anthracnose) caused by Colletotrichum acutatum

Colletotrichum acutatum has a wide range of hosts; both trees and fruit are infected by this pathogen. In Northern Europe, high pre- and postharvest fruit losses in strawberries, blueberries and cherries were attributed to C. acutatum (Sundelin et al. 2005; Børve and Stensvand 2006; Stensvand et al. 2006). C. acutatum has been reported as the most prevalent storage pathogen in Norway (Weber 2009b; Børve et al. 2010). In the rest of NW Europe, the relative importance of this fungus in stored apples is low, although losses may be on the increase (Weber 2009a). In subtropical and tropical areas, C. acutatum as well as C. gloeosporioides are well known pathogens (Peres et al. 2005). In apple orchards, conidia are splash-dispersed from buds formed during the previous growing season, and these may infect young leaves and fruit (Børve and Stensvand 2007). Fruit mummies and twig cankers cause infections on the maturing apples (Stensvand and Ren 2010). During storage, the development of C. acutatum decay is similar to Neofabraea spp. in that mycelium appears to grow from fungal spores deposited in the lenticels, colonizing the apple 13

Chapter 2: Literature review

within some weeks. The resulting lesion appears sunken and is often covered by dark grey mycelium extruding yellowish-pink spore drops (Figure 2.3I). Conidia are readily distinguished from N. perennans and N. alba in being straight, symmetrical and somewhat pointed at one or both ends (Figure 2.3J). However, a reliable distinction between C. acutatum and C. gloeosporioides is only possible by PCR analysis. Therefore it is important to determine by PCR if reports of infections of Swedish apples with G. cingulata (Tahir et al. 2009), teleomorph of C. gloeosporioides, can be confirmed. 2.3.5 Brown rot caused by Monilinia fructigena Brown rot caused by Monilinia fructigena is an important disease in apple orchards in Europe (Jijakli and Lepoivre 2004). High fruit losses due to M. fructigena have been reported in Hungary (Holb 2008), where up to 40% of apples were infected during the production phase in organically managed orchards. In comparison, orchards under IP management suffered losses up to 10% (Holb 2008). In the humid climate of NW Europe, the importance of M. fructigena is lower, 5% fruit loss from this fungus being regarded as high (Palm and Kruse 2005).

M. fructigena is a wound pathogen on apple fruit (Xu and Robinson 2000). Preharvest infections commonly occur in fruit that have been attacked by biting insects such as larvae of codling moth (Cydia pomonella) and leaf rollers (e.g. Adoxophyes orana). Mechanical damage caused by wind, birds, hailstorms or passing machinery in the alley ways may also result in M. fructigena infections (Holb 2008). The ability of M.

fructigena to infect a wound depends on the developmental stage of the fruit, wound age and the presence of free water or relative humidity above 97%. The highest rates of infection from M. fructigena have been observed in freshly (52°C). Hypothesis 8: The reduction of Penicillium rot in artificially inoculated apples is due to an effect of HWD on the fruit, not on the fungus. This hypothesis was accepted in Chapter 5, thereby also addressing hypotheses 5 and 6. In Section 8.3 general aspects on the acceptance of this hypothesis are discussed.

8.2 Effects of delayed ripening on the incidence of storage rots Apple storage methods have been revolutionized by the concepts of controlled atmosphere (CA) and dynamically controlled atmosphere (DCA) which enable fruit to be kept for much longer time periods than in cold storage under ambient atmosphere (Veltman et al. 2003). The main mode of action of CA and DCA is to delay fruit ripening. Treatment with 1-methyl-cyclopropene (1-MCP) achieves the same result through the different means of inhibiting ethylene production and 128

Chapter 8: General discussion

activity. However, none of these methods directly eliminates fungal inoculum. This explains why there are few, if any, synergies between 1-MCP and CA or DCA (Chapter 5). In terms of efficacy against the development of fungal postharvest diseases, CA or DCA after 8 months may be comparable to cold storage with 1-MCP after 6 months, or simple cold storage after 3 months (Spotts et al. 2007; Lafer 2010; see Chapter 6). In order to reduce the incidence of fruit rots after the end of a CA or DCA storage period, i.e. the time of fruit distribution, sale and consumption, fungal inoculum must be eliminated. This may be achieved by preharvest fungicide applications which are under public scrutiny, hygiene measures (e.g. removal of fruit mummies) which are labour-intensive and therefore costly, and HWD or HWR which have not (yet) gained full acceptance by fruit producers. The research presented in this Thesis indicates that these HWT hold significant unrealized potential. 8.2.1 Interactions between HWT and ripening inhibition A summary of existing literature knowledge of the efficacies of the above-mentioned methods to control postharvest diseases (pre-harvest fungicides, removal of mummies, low-temperature storage with or without CA or DCA, application of 1MCP) is presented in Table 8.1. The incidence of the major storage rots, caused by

Neofabraea spp., has been reported to be decreased by a delay in fruit ripening associated with CA, DCA, reduced storage temperatures, and 1-MCP (Spotts et al. 2007; Lafer 2010). The effect of CA on controlling blue mould caused by Penicillium

expansum may be due in part to a retarded fruit ripening, and partly to direct effects of the modified atmosphere on the fungus (Yackel et al. 1971). In contrast, other fungal storage rots such as Botrytis cinerea or Neonectria galligena were not affected by CA or DCA (Berrie et al. 2011). Similarly, the recently discovered Phacidiopycnis

washingtonensis failed to show any obvious response to CA, DCA and 1-MCP (Chapter 6). This provides a plausible explanation for the frequent discoveries of rubbery rot after prolonged DCA and CA storage (Weber 2011), in contrast to a lowered incidence of Neofabraea spp. under these conditions. Although, the efficacy of HWD against Neofabraea spp., P. expansum and M.

fructigena has been well documented (Burchill 1964; Maxin et al. 2005; Amiri and Bompeix 2010), recent reports have so far indicated a similar potential for HWR only 129


against P. expansum (Fallik et al. 2001). Prior to the publications originating from this Thesis, no literature existed on the efficacy of HWR on any other storage-rot fungus on apples. This Thesis has provided a new insight in to the potential of HWR and HWD in controlling major storage rot fungi (Table 8.1). In the present study high efficacies of both HWD and HWR were characterized for a wide range of storage-rot fungi including C. acutatum, Cladosporium spp., N galligena, P. washingtonensis, N. alba and N. perennans (Chapter 7). Further, P. expansum and B. cinerea were controlled in artificially infected fruit subjected to HWD (Chapter 5). These findings greatly expand our understanding of the potential offered by the physical HWT of apples. It is apparent from Table 8.1 that the range of fungi susceptible to HWD or HWR is wider than that of species controlled by 1-MCP, CA or DCA. Further, HWD and HWR can be expected to show synergies with ripening delay caused by CA, DCA or 1-MCP treatments because they are based on different modes of action. 8.2.2 Preharvest chemical treatments vs. postharvest HWT Efficacies of HWT in reducing storage rots and their possible positive interactions with any ripening delay procedures are an important basis for evaluating risks and benefits of HWR and HWD in the context of registration of new chemical substances in the EU for the use in plant protection (Section 2.6). The EU 2009/128/EC directive, which is currently being transformed into national legislation by all EU member states, requires that the new pesticide registration system “also establishes a mechanism for the substitution of more toxic pesticides by safer (including non-chemical) alternatives” (GD Health and Consumer, 2010). In providing such an alternative to chemical treatments, HWR and HWD may be expected to gain importance and acceptance as methods to control postharvest fungi in future. A similar focus may also be anticipated for preharvest hygiene measures aimed at reducing inoculum during the growing season or at harvest. These may consist of the removal of fruit mummies or sporulating cankers. However, although such measures may significantly reduce post-harvest decay caused by specific fungi (Holb and Scherm 2007), the efficacy of such measures against a wider range of species under NW European conditions remains to be proven. On biological grounds, synergistic effects between (1) hygiene measures, (2) HWT and (3) ripening delay caused by CA, DCA or 1-MCP may be expected.

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8.3 The influence of heat on spores and fruit ‘Elstar’ apples artificially inoculated with Penicillium expansum and subjected to 3 min HWD at 55°C or above showed a higher incidence of blue mold than fruit subjected to HWD at 52°C. The choice of a relatively high temperature was based on the assumption that HWD Table 8.1: Efficacies of various methods for the reduction of post-harvest storage rots of apples, indicated as +++ (>75%), ++ (50-75%), + (50% and therefore provide a valuable tool that broadens options available to fruit growers and pack-house managers. Hot water treatments may be incorporated either pre- or post-storage into CA and DCA strategies and have the potential to reduce fruit wastage during the distribution and consumer phases and to enhance consumer satisfaction. The technology evaluated in this study showed that HWR gave rise to only slightly reduced disease control efficacies as compared to HWD, but that HWR holds several other advantages over HWD. The cost of HWR per unit of treated apples is expected to be much lower than for HWD because no additional labour is required and the amount of energy required to heat the water for a 30 s rinse should be about 20% of the energy used in a 3 min HWD process. A further advantage of HWR is that it can be incorporated into existing fruit grading lines, thus avoiding the need for additional equipment or parallel structures. Traditionally, harvested fruit in storage boxes are emptied by submersion in cold water, followed by floating the fruit to a conveyor belt, where they are dried and passed to the grading unit. Apples are then separated by size and pigmentation. Several exits on the grading unit are opened or closed, depending on the desired parameters. A HWR unit could easily be placed on such an exit, permitting a fraction of the total crop to be treated with hot water. Alternatively, all fruit could be treated by HWR prior to entering the drying unit. A closed HWR unit needs to be developed to minimize the emission of water vapor in the packing hall. Additional positive effects of HWR on fruit quality can be expected. In particular, it has been observed that fruit were less waxy and more homogenous following HWR and storage than after HWD or without hot-water treatments (see Section 4.2.3). Further, HWR may be associated with enhanced fruit firmness (Fallik et al. 2001). These attributes, which may be due to a partial melting of epicuticular waxes above 55°C (Aggarwal 2001), should be explored in future studies and may further address

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Hypothesis 1 which war rejected based on the grounds of the preliminary work reported in this Thesis. Further research should also be aimed at identifying the proteins and/or lowmolecular weight substances induced by heat shock in apples. An understanding of their identity should enable us to optimise parameters and time-points of HWT in apples. An additional area of interest is a detailed characterisation of the responsiveness of fruit to HWR directly after harvest in comparison with fruit subjected to HWR after short- or long-term storage. Finally, the question remains whether apples treated by HWR before storage are capable of mounting an additional heatshock response if they are exposed to a second HWT during the packing phase, following a pre-storage HWR and, if so, how this might further improve fruit quality during the distribution phase.

.

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