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Current trends and issues in Japanese domestic production of Auricularia polytricha
Yasuhito Okuda
The Tottori Mycological Institute, 211 Kokoge, Tottori 689-1125
Originally published in Volume 29(4) pg 134-140, 2021, Mushroom Science and Biotechnology, by the Japanese Society of Mushroom Science and Biotechnology. (日本きのこ学会誌、Vol 29(4) 134-140, 2021.一社団法人日本きのこ学会)
Abstract
The edible species of the genus Auricularia mainly include A. polytricha and A. auricula-judae (aragekikurage and kikurage in Japanese, respectively). Together these edible mushrooms are ranked 6th in terms of consumption in Japan. Since most official statistical surveys in Japan do not distinguish between either of these mushrooms species and group them together loosely in the “kikurage group”, detailed statistical data for each species do not exist. However, it is clear that A. polytricha accounts for the majority of domestic production in Japan. The supply of A. polytricha has been strongly dependent on imports. Since the risks associated with imported products have increased in recent years, domestic demand has increased and rapid growth in domestic production has occurred. On the other hand, various problems with breeding, cultivation techniques, pest control, taxonomy, and food science have arisen. In addition, possible future threats include erosion of the domestic market by imported culture bags and disguised production areas. In this review, the author will clarify the production trends, current challenges, and future threats with the aim of strengthening and developing domestic production bases in the future.
Key words: Auricularia polytricha, Cloud ear mushroom, Japanese domestic production, Present and future issues, Production trends
1. Introduction

Demand is high globally for the kikurage (wood ear) genus, which includes Auricularia polytricha, with expanded production in Asia placing it after shiitake and oyster mushrooms in terms of volume produced. Because Japanese official statistical surveys and basic special forestry data conventionally group Auricularia polytricha and Auricularia auricula-judae together as “kikurage mushrooms”, there are no accurate consumption and import figures on A. polytricha alone. However, A. polytricha makes up the majority of wood ear mushrooms produced in Japan. Therefore, in this paper it is appropriate to use the domestic production volume of wood ear mushrooms in basic special forestry data as the figures for A. polytricha.

According to 2020 basic special forestry data, the combined domestic consumption of fresh and dried kikurage mushrooms ranked 6th (fresh equivalent: 26,308 tonnes) after enoki mushrooms, bunashimeji, shiitake, maitake and king oyster mushrooms (Table 1). Although there is such great demand for kikurage mushrooms, only 3,132 tonnes are produced domestically, a mere 11.9% of the amount consumed, with the majority imported in dried form (Table 1). In recent years, it has come to light that the risks associated with imported products have not been to limited to vegetables, but also mushrooms, so the growing preference for domestic products has resulted in a rapid increase in the domestic production of A. polytricha. With the risks of imported agricultural products not limited to only vegetables, but also apparent in mushrooms, there has been an increase in preference for locally produced goods and domestic A. polytricha production has been rising sharply.

However, with the increase in production and consumption, various issues have become apparent, including the limited number of cultivated varieties, a lack of knowledge about substrate composition and other cultivation technology as well as pest and diseases control, the need for taxonomic review, and the non-standardisation and inaccuracy of food labeling. Since the author started working at The Tottori Mycological Institute (hereinafter “The Institute”) in 2013, he has been in charge of A. polytricha cultivation guidance and variety development, and involved in launching production facilities, including in Tottori and Yamaguchi prefectures. Therefore, in order to strengthen the A. polytricha domestic production base and its sustainable development moving forward, in this paper he will explain the current production trends, the issues to be addressed now and the issues that may pose a threat in the future.

2. A. polytricha domestic production trends

As of 2020, imports of kikurage mushrooms reached 23,190 tonnes, 7.4 times that of domestic production (Table 1), which is a high import dependency rate among the main cultivated mushrooms in Japan, even higher than that of dried shiitake(2). Recently, problems such as residual pesticides and origin misrepresentation have arisen primarily in imported mushrooms 3), leading to a decline in consumer confidence in imported mushrooms. Imported kikurage mushrooms are no exception. In 2006, the Ministry of Health, Labour and Welfare implemented the “Positive List System for Agricultural Chemical Residues in Food,” a system that, in principle, bans the distribution of foods containing pesticide residues above a certain level. As a result of the stricter pesticide residue standards, insecticidal ingredients such as fenpropathrin(4), methamidophos, chlorpyrifos and imidacloprid(6) have been detected exceeding the standard values. Under these circumstances, although the volume of imports is still high, in the 15 years from 2006 to 2020, domestic production of A. polytricha increased 34-fold from 92 tonnes to 3,132 tonnes (wet weight) with demand steadily increasing.

According to 2020 basic special forestry data, the domestic production of dried A. polytricha by prefecture was greatest in Yamaguchi at 29.2 tonnes followed by Tottori at 21.1 tonnes then Miyagi, Ibaraki and Kagoshima. Additionally, the domestic production volume of fresh was highest in Gifu at 306.2 tonnes followed by Miyagi at 169.5 tonnes then Kumamoto, Ibaraki and Tottori. In Tottori in particular, a project by the Japan Kinoko Research Center Foundation to promote the prefecture as an A. polytricha production area has led to a sharp increase in production.

However, with the price of domestically-grown produce 2-5 times that of overseas-grown produce (according to the author), it is necessary to solve the following issues facing A. polytricha production and strengthen its competitiveness in order to continue expanding its domestic production.
3. Issues in A. polytricha domestic production

3-1. Development of cultivated varieties

The number of registered major mushroom varieties, excluding those removed or rejected, has been 238 shiitake, 62 enoki mushrooms, 69 bunashimeji, 47 maitake, 39 king oyster mushrooms, 26 nameko and 17 oyster mushrooms (including Pleurotus pulmonarius or Phoenix oyster mushrooms). In contrast, there have only been nine patent-pending or registered varieties of A. polytricha (Table 2. Accessed December 2021). Cultivated varieties that bring stable yields are crucial for the promotion of A. polytricha domestic production, but despite increasing domestic production volumes, the number of patent-pending and registered varieties remains small. In an attempt to expand the domestic consumption base of A. polytricha, the Japan Kinoko Research Center Foundation has applied for and registered three white varieties (albino), Kinko 90 (registration number 2268, application filed in 1987), Kinko 91 (registration number 5304, application filed 1993) and Kinko 92 (Figure 1: registration number 28145, application filed 2014).
3-5. Future threats and challenges associated with the expansion of A. polytricha domestic production

It is anticipated that the country of origin misrepresentation will be a problem that can greatly hinder the domestic production of A. polytricha in the future.
As a prior example, it is estimated that 2,000-3,000 tonnes of overseas-produced dried shiitake were falsely labelled as Japan-produced in the 2000s, greatly affecting domestic dried shiitake production with the unfair drop in prices. Since then, however, techniques have been developed to determine the country of origin, such as physical property investigation using texturometers, observation using stereo microscopy, inorganic element analysis using inductively coupled plasma emission spectrometer (ICP-AES) and mass spectrometer (ICP-MS), and carbon and nitrogen stable isotope ratio analysis using stable isotope specific mass spectrometer, which have produced a certain level of deterrence against origin misrepresentation in dried shiitake, allowing prices to recover.

Like shiitake, there is a high import volume of A. polytricha with a marked price difference between overseas and Japan-produced products so there is a high possibility of imported A. polytricha products being fraudulent labelled and sold as being produced in Japan. Thus, technical development was required to determine the country of origin and it was revealed that the content of elements such as iron, manganese, aluminum, zinc and lead varied significantly depending on the country of origin (China or Japan) of the A. polytricha in the ICP-MS inorganic element analysis of dried A. polytricha and A. auricula-judae. Moving forward, it is expected that the development of country-of-origin identification technology that use this knowledge will be an effective way to deal with the possible problem of origin misrepresentation in A. polytricha.

Variety identification technology is critical for preventing the outflow and misuse of varieties overseas, protecting cultivator rights, and maintaining and improving the mushroom brand.

A. polytricha is mainly distributed as a processed food so it bears no resemblance to its original shape, making it difficult to identify the variety from its appearance. Therefore, what is important is breed identification technology using DNA. As domestic production has been low and varieties have not been actively developed, little is known about identifying A. polytricha varieties. For this reason, variety identification markers CI-1 and CI-2 were developed based on the Intergenic Spacer 1 (IGS1) sequence to identify Kinko AP-1 (Figure 1).CI-1 was amplified using the primer set CI-F1 (5’-AGGGCTCTGGCTGTGTTATTT-3’) and CI-R1 (5’-ATCCCCTCGCCGTTTAA-3’). The process involved an initial heat denaturation at 94°C for 2 minutes, followed by 30 cycles of 94°C for 10 seconds (denaturation), 66°C for 10 seconds (annealing), and 72°C for 30 seconds (extension reaction), with a final extension reaction at 72°C for 10 minutes. Additionally, CI-2 was amplified using the primer sets CI-F25’-GTGTACAGTTTGTTATTCTCCGT-3’) and CI-R2 (5’-GCCTTCTTCCTAGGCCCC-3’). The process was carried out under the same conditions as above, with modifications to the annealing temperature at 67°C and the extension reaction time at 40 seconds.Figure 3 shows an example of electrophoresis of this amplified product with a 2.0% agarose gel at 100V for 30 minutes.In Kinko AP1, CI-1 amplifies a fragment of 418bp and CI-2 a fragment of 570bp.By using a combination of these variety identification markers CI-1 and CI-2, it was possible to identify Kinko AP1 for three cultivated varieties distributed in Japan, 13 domestic products distributed as dried products and 26 imported products. Such variety identification markers are not only important for the protection of cultivator rights, but also as a means to ensure the reliability of quality in the domestic production expansion and branding of A. polytricha.
With shiitake, the import volume of substrate blocks incubated and matured overseas reached an all-time high in 2018 and it was estimated that 10% of domestically produced shiitake were grown on these blocks, highlighting the fact that the large influx of inexpensive imported substrate blocks is putting pressure on cultivation using domestically produced substrate blocks. In response, the Consumer Affairs Agency stated in the Food Labeling Standards Q&A in 2020 that if the place where the shiitake spawn are inoculated differs to where the fruiting bodies are harvested, then it is recommended that the harvest site be displayed separately to the inoculation site, along with the cultivation method. The actual situation for A. polytricha is not clear, but like shiitake, imported substrate blocks are cheaper than those produced in Japan with the fruiting bodies sold as domestically-produced products, which is a big blow to Japanese companies supplying substrate blocks and spawn. Country-of-origin and variety identification techniques can be effective in dealing with these problems.

The above issues, while not yet apparent, not only dampen the enthusiasm of variety developers and cultivators, but also significantly undermine consumer and end-user trust in domestically-produced A. polytricha, thereby greatly impeding the development of domestic production. Therefore, early development of origin and variety identification techniques are crucial preventive measures.
Further, in 2019 the Foundation overcame the phenomenon of the fruiting body pigmentation becoming paler, which is considered a cause of quality degradation, and applied for and registered Kinko AP1 as a high-yield variety that displays a stable dark brown pigment (Figure 1: Registration number 28531). Recently, the University of the Ryukyus (application number 33738, application filed 2019) and the Aomori Industrial Technology Center (registration number 28713, application filed 2020) and other public testing and research institutions have applied for and registered new varieties (Table 2). Although the development of new varieties has gradually been gaining momentum, the domestic production base of A. polytricha admittedly remains tenuous, with the acceleration of new variety development a critical challenge. Now, while there is increasing consumer awareness towards food safety and rising domestic A. polytricha production, the development of new cultivated varieties will contribute to the promotion of area-based production and strengthening of domestic production systems.

3-2. Review of cultivation techniques

Because A. polytricha supply has relied on imports, substrate composition and other cultivation conditions are not as well understood compared to other cultivated mushrooms. However, in recent years, with the gradual increase in domestic production, the composition conditions for substrate using highly local base material and nutrition supplement such as bagasse and shochu lees from the common nutrition supplements of wheat bran and rice bran is in the process of being examined. Further, the addition of calcium carbonate material is essential in A. polytricha cultivation and many reports, including cultivation manuals and cultivation trials, have mentioned its addition. However, the author was unable to find any reports that investigated the effects of added calcium carbonate.

Therefore, the author verified the addition of fossilised shell, which is widely distributed throughout Japan and is primarily composed of calcium carbonate, using Kinko AP1 No. 8 as the test strain. The substrate composition was a mix of a base (beech sawdust) and nutrition supplement (6:4 of wheat bran to rice bran) at a ratio of 8:2 (hereinafter, all in dry weight ratios). The moisture content was prepared to 63 ± 2% then fossilised shell was added in increments of 0.5% from 0% to 3.5% based on the weight of the substrate after the addition of water. In the mycelial growth test, the test group with 3.0% added fossilised shell was found to be the most effective. Based on this result, cultivation tests were conducted which showed a marked increase in yield in the groups with added fossilised shell (3.0 ± 0.5%) compared to the control group with no added shell. Further, the incubation period for A. polytricha is generally over 60 days, but no significant difference in yield was observed among all the test groups with 40, 50 and 60-day incubation periods, with the exception of the group with no added shell (Table 3). From this, it became evident that the appropriate addition of fossilised shell is effective in shortening the incubation period and contributes to enhancing the competitiveness of domestically-produced A. polytricha. However, this study used Kinko AP1 as the test strain so further investigation will be needed in other cultivation varieties in future.

A. polytricha cultivation methods have been studied and publicly released by public research institutes with the aim of introducing it to each prefecture, and its cultivation is expanding throughout Japan. It has been found that A. polytricha can be cultivated not only in air-conditioned facilities that ensure the warm growing conditions favoured by the species, but also in simple facilities without air-conditioning during the warm season with other mushrooms (log-cultivated shiitake in particular) grown during the cool season, thus enabling year-round production. The fact that A. polytricha production can be started with minimal investment is believed to be a factor in its increasing production in Japan.

On the other hand, there has been an increase in the number of large-scale air-conditioned facilities to more efficiently achieve large-scale production. Although research into cultivation techniques aimed at efficient and stable production is thus steadily progressing, further efforts are needed to strengthen domestic production of A. polytricha.
With shiitake, the import volume of substrate blocks incubated and matured overseas reached an all-time high in 2018 and it was estimated that 10% of domestically produced shiitake were grown on these blocks, highlighting the fact that the large influx of inexpensive imported substrate blocks is putting pressure on cultivation using domestically produced substrate blocks. In response, the Consumer Affairs Agency stated in the Food Labeling Standards Q&A in 2020 that if the place where the shiitake spawn are inoculated differs to where the fruiting bodies are harvested, then it is recommended that the harvest site be displayed separately to the inoculation site, along with the cultivation method. The actual situation for A. polytricha is not clear, but like shiitake, imported substrate blocks are cheaper than those produced in Japan with the fruiting bodies sold as domestically-produced products, which is a big blow to Japanese companies supplying substrate blocks and spawn. Country-of-origin and variety identification techniques can be effective in dealing with these problems.

The above issues, while not yet apparent, not only dampen the enthusiasm of variety developers and cultivators, but also significantly undermine consumer and end-user trust in domestically-produced A. polytricha, thereby greatly impeding the development of domestic production. Therefore, early development of origin and variety identification techniques are crucial preventive measures.
3-3. Pest control

There have been many reports cited of diseases in artificially cultivated mushrooms with mycosis such as shiitake bacterial disease caused by Pseudomonas fluorescens (Migula), bacterial diseases such as brown blotch disease in oyster mushrooms caused by Pseudomonas tolaasii (Paine), various trichoderma diseases in shiitake caused by the Trichoderma genus of fungi and dry bubble disease in button mushrooms caused by Lecanicillium fungicola (Preuss Zare & W Gams). There is also pest damage with various insects such as long-horned beetles causing feeding damage on shiitake cultivation logs. With the recent increase in A. polytricha cultivation, there have been reports of new pests and diseases emerging. One pest and disease issue affecting A. polytricha identified in Japan is feeding damage caused by slugs, which is also occasionally seen in other mushroom species. There are also reports of rot disease caused by Pseudomonas sp., which dissolves fruiting bodies and emits an unpleasant odor, as well as feeding damage by the larvae of moths such as Diomea cremata and Anatatha lignea and feeding damage by Neoempheria carinata and Neoempheria bifurcata larvae 25). For these such pest and disease issues, particularly rot disease, it is possible to prevent and control them by reducing the humidity by improving ventilation to reduce moisture as an excess is often the cause. Further, for feeding damage caused by slugs and moth larvae, occasionally seen in simple cultivation facilities, those using vinyl houses in particular, the installation of insect nets and various pest control devices to manage temperature and humidity should be considered when using facilities prone to pests entering along with outdoor air.

Based on the author’s experience, it is unlikely that damage will spread greatly as long as it is dealt with. Early detection of feeding damage signs and prompt eradication can minimise the extent of the damage. However, because Neoempheria carinata and Neoempheria bifurcata have high reproductive capacities, damage will spread easily with the above-mentioned measures alone and, depending on the extent of the damage, disposal of all the substrate blocks and cleaning of the entire facility may be required.

Recently there have also been many cases of cottony soft rot exhibiting fluffy signs on A. polytricha fruiting bodies(26). This disease is caused by Hypomyces pseudocorticiicola (Tokiwa and Okuda). In the early stage of infection, a fluffy mycelium that forms a large number of asexual spores covers the entire fruiting body, and in the later stage, yellowing and ascocarp formation occur, and ultimately the diseased fruiting bodies either shrink or decompose (Figure 2). Because this pathogen forms a large number of asexual spores, these spores are dispersed through irrigation, spreading the infection throughout the substrate blocks lining the shelves. Further, like A. polytricha, it prefers a hot and humid environment. Based on the above points, in air-conditioned facilities where damage tends to spread, avoiding cultivation management in which the indoor area is always moist and establishing a dry-wet differential is considered effective for prevention and control. The author has so far confirmed damage caused by this fungus in the prefectures of Tottori, Hiroshima, Ehime and Miyazaki, but it can be difficult to distinguish from spore-induced contamination so it is likely that it is often overlooked.
Slippery Scar disease, caused by the imperfect fungus Scytalidium lignicola (Pesante), which dramatically reduces yield when it infects the substrate of A. polytricha, has been noted as an unreported disease in Japan. With the expansion of domestic production, it is expected that new pests and diseases will continue to be reported. As the pests and diseases described here can become a major obstacle to domestic production, it is necessary to cultivate disease-resistant varieties and establish control techniques early.

3-4. Taxonomic review and food labeling standardisation

The Japanese name for Auricularia polytricha (Mont. Sacc.), “arage kikurage”, was coined by Kawamura. In recent years, Shirozu et al. conducted molecular phylogenetic analysis of Japanese species of Auricularia genus fungi and many specimens and strains called “arage kikurage” (A. polytricha) were identified as A. cornea (Ehrenb). (“nankai kikurage” in Japanese). This result suggests the need to change the Japanese name and scientific name of this fungus. However, further investigation is required to compare the specimens identified as A. polytricha by Kawamura with those identified as A. cornea by Shirozu et al., so there is room for continued investigation.

Food labeling, which is the only source of information that consumers can verify from food, illuminates the responsibility of companies and producers and ensures food safety.

Based on the Food Labeling Act, it is also compulsory to display ingredients and names on processed foods, including dried, and names on fresh products, with ingredients and names to be listed using their common names. The author obtained 49 dried A. polytricha products distributed in Japan and investigated the ingredients listed. He found that there was no set common name with “white-backed wood ear mushroom”, “wood ear mushroom” and “wood ear” displayed in addition to “A. polytricha”, revealing that it is also difficult to distinguish A. polytricha from A. auricula-judae (Table 4). Further, many of the names of fresh A. polytricha products that are often seen on the market recently tend to be listed as A. auricula-judae, so there is a need to decide on a common name.

The current situation with Japanese names, scientific names, and food labels as described above causes confusion for producers, consumers and end users, as in the past when oyster mushrooms were sold as “shimeji” and beech shimeji as “honshimeji”, and undermines the reliability of A. polytricha as a food ingredient. Further, because there is a difference in price between A. auricula-judae and A. polytricha, there is a risk of fraudulent labeling, including misrepresentation of origin as described in the next section. Therefore, prompt action from all relevant parties is expected.
4. Conclusion

Although currently produced in various places in Japan with production on an upward trend, domestically-produced A. polytricha is still less competitive in terms of price compared to imported products of this mushroom. As domestic production volumes increase, enhancing the competitiveness of domestic production and achieving continuous expansion requires the production of wood ear mushrooms that leverage the advantages of being domestically produced, ensuring safety, reliability, and appeal. With growing interest in reducing environmental impact and concerns about food safety in the past few years, the Ministry of Agriculture, Forestry and Fisheries has established the Japanese Agricultural Standards (JAS) for organic agricultural products, commonly known as the Organic JAS Standards. Prompted by the risks associated with imported mushrooms in recent years, there has been a growing trend among some retailers and the food service industry to actively use domestically-produced organic mushrooms. As a result, the grading results for organic mushrooms in Japan for the fiscal year 2018 amounted to 542 tonnes for A. polytricha and several producers, including the Japan Kinoko Research Center Foundation (Tottori Prefecture Certification No. A19-0038), have obtained organic certification.

As described, there are many problems to be solved in domestic A. polytricha production and it can be said that we are now at the crossroads that will determine the rise or fall of the mushroom variety in the Japanese domestic market. Since A. polytricha is primarily used in the food and restaurant industry as a processed food, it is difficult to say that the current situation, where nearly 90% of consumption is of foreign origin, is widely recognised by consumers. Against this backdrop, actively disseminating information about domestically produced A. polytricha is effective not only in stimulating the purchasing interest of consumers but also in breaking free from reliance on imports. This will contribute to both the expansion of domestic production and the strengthening of its competitiveness.
This English translation was done for the Japanese Exotic Mushroom Journal, and any errors in terminology, transcription, or in the presentation of the data are the responsibility of the Japanese Exotic Mushroom Journal. Please contact journal editors at jemj@salai.jp for a full list of citations and references (not translated).

About the Translator: Naomi Roulston has over a decade of experience as a Japanese to English translator and specialises in food, mushrooms, nutrition and lifestyle medicine, and travel and tourism. She has a postgraduate degree in translation, is NAATI-certified, and holds a Kinoko Meister certificate from the Japan Kinoko (mushroom) Meister Association.

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Current trends and issues in Japanese domestic production of Auricularia polytricha