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Journal of Resources and Ecology >

2021 , Vol. 12 >Issue 6: 869 - 875

DOI: https://doi.org/10.5814/j.issn.1674-764x.2021.06.014

Typical Ecological Restoration Modes and Their Ecological Effects

Suppressive Effects of Traditional Mulching Using Japanese Knotweed (Fallopia japonica) on Solanaceae Crop Diseases

  • INAGAKI Hidehiro , * ,
  • KUBOTA Sakiko ,
  • HASEGAWA Kana ,
  • UNNO Nahoko ,
  • USUI Yukiko ,
  • TAKIKAWA Yuichi
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  • Shizuoka University, Shizuoka 422-8529, Japan
*INAGAKI Hidehiro, E-mail:

Received date: 2020-08-17

  Accepted date: 2021-01-30

  Online published: 2021-11-26

Supported by

Japan Society for the Promotion of Science (JSPS) KAKENHI(JP15K06930)

Japan Society for the Promotion of Science (JSPS) KAKENHI(JP18H02286)

Japan Society for the Promotion of Science (JSPS) KAKENHI(JP19K06108)

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Abstract

Poaceae plant species, such as silver grass, are commonly used in mulching activities Japan. In contrast, local farmers have traditionally used Japanese knotweed (Fallopia japonica) mulch in the cultivation of solanaceous crops in the Nishi-Awa area of Japan, which is a Globally Important Agricultural Heritage Systems site. We have previously evaluated the positive effects of Japanese knotweed mulching on solanaceous crops, such as eggplants, tomato, and potato. In the present study, we observed that the naturally occurring diseases in the solanaceous crops tended to decrease when the knotweed mulching system was adopted, in comparison to when Poaceae mulch was adopted. In eggplants, leaf mold and powdery mildew decreased under Japanese knotweed mulching. We further evaluated the effects of Japanese knotweed mulching by inoculating test plants with Pseudomonas cichorii. We observed suppression of bacterial disease and tomato mosaic virus under Japanese knotweed mulching and following spraying with Japanese knotweed extracts. In addition, disease-resistance genes were expressed at high levels in Arabidopsis thaliana, a model plant, following treatment with Japanese knotweed extracts. The results suggest that Japanese knotweed has potential applications in future sustainable agriculture activities.

Key words： Traditional Ecological Knowledges (TEK); Globally Important Agricultural Heritage Systems (GIAHS); Japanese knotweed; Solanaceae; mulching; systemic acquired resistance (SAR)

Cite this article

INAGAKI Hidehiro , KUBOTA Sakiko , HASEGAWA Kana , UNNO Nahoko , USUI Yukiko , TAKIKAWA Yuichi . Suppressive Effects of Traditional Mulching Using Japanese Knotweed (Fallopia japonica) on Solanaceae Crop Diseases[J]. Journal of Resources and Ecology, 2021 , 12(6) : 869 -875 . DOI: 10.5814/j.issn.1674-764x.2021.06.014

1 Introduction

Traditional farming communities in rural areas have developed various traditional ecological knowledge (TEK) systems as products of long years of interaction and co-evo- lution between natural environments and human society (Altieri et al., 2015). Such TEK systems are being reevaluated for potential application in future sustainable agriculture activities (Altieri et al., 2015). The Food and Agriculture Organization of the United Nations initiated a program named Globally Important Agricultural Heritage Systems (GIAHS) in 2002 with the aim of transmitting the value and knowledge of traditional agriculture to subsequent generations (FAO, 2020a). The data on traditional agricultural systems collated in the GIAHS site (UNU, 2011) offer insights on how to achieve sustainable agricultural production in the future. Numerous TEK systems have been reported from such GIAHS sites.
The mountainous area of Nishi-Awa in Tokushima, Japan, was recognized as a GIAHS site in 2018 (TTGAHPC, 2019; FAO, 2020b). The most important TEK on this site is grass mulching (FAO, 2020b). In the area, farmers have traditionally carried out mulching using cut wild grass (Hayashi, 2015; TTGAHPC, 2019), which has been recognized to effectively prevent soil erosion, supply organic matter, and control weeds (Hayashi, 2015). Poaceae species, such as silver grass (Miscanthus sinensis), are generally used in mulching activities in Japan (Hadama et al., 1996; Inagaki and Kusumoto, 2015). In the Nishi-Awa area, silver grass has been the main species used for mulching (Hayashi, 2015). Local farmers mow the grass around the farmland in autumn, dry the grass in winter, and then use it to completely cover the ground surface before planting vegetable seedlings in spring (Hayashi, 2015). From ancient times it has been known that “Japanese knotweed mulching is suitable for cultivating Solanaceous crops” and farmers have used it as mulch instead of silver grass when cultivating solanaceous crops such as eggplant (Hayashi, 2015). Japanese knotweed is a perennial weed species, growing around crop fields and along forest edges. The Japanese knotweed is mowed around the farmland in spring, the mowed plants are allowed to dry for about one day, and then spread over the soil in a laver that completely covers the ground surface before planting Solanaceae seedlings. At a present, it remains unclear why its use is restricted to only in solanaceous crop systems.
To date, we have verified the positive effects of Japanese knotweed mulching on solanaceous crops such as eggplant, tomato, and potato, with the following observations. 1) It does not adversely affect eggplant growth and yield; conversely, it increases the sugar content and softens the skin in eggplant fruits (Hasegawa et al., 2018; Inagaki et al., 2019). 2) It does not affect the tomato growth and yield adversely; on the contrary, it increases sugar content in tomato fruits (Unno and Inagaki, 2019; Unno et al., 2020). 3) Although the minimization of the continuous cropping challenge is not observed in eggplant (Hasegawa et al., 2019), it is observed in tomato and potato (Inagaki et al., 2020b; Unno and Inagaki, 2020). 4) Japanese knotweed mulching does not influence organic matter supply in a single cropping year (Hasegawa et al., 2019). While the above-mentioned studies were conducted, a decrease in naturally occurring diseases in solanaceous crops was observed when Japanese knotweed mulching was applied. Therefore, we hypothesized that the traditional Japanese knotweed mulching has been used to control the disease incidence in solanaceous vegetables.
Pest control was an essential aspect in traditional agricultural activities, considering there were no chemical pesticides in the era in question. For example, traditional mixed planting and use of cover crops could protect cultivated plants from indigenous natural enemies and controlling disease (Stephen, 2015). In addition, some of the practices have been adopted in current integrated pest management approaches (Stephen, 2015). Moreover, paddy fish farming, which is practiced extensively from South China to Southeast Asia, and has been recognized as a GIAHS, is not only effective for raising fish in paddy fields to obtain a protein source, but also for controlling pests and weeds (GIAHS Book Editorial and Production Committee, 2015; Qin et al., 2015; FAO, 2020a). In Japan, the “Aigamo paddy farming”, which applies traditional paddy fish farming, is applied as a novel method of organic rice farming (Asano et al., 1999; Tojo et al., 2007). Elucidating whether traditional Japanese knotweed mulching is effective in controlling solanaceous diseases will offer useful information for future agricultural technology.
In this paper, we studied the effects of Japanese knotweed mulching on Solanaceae crop disease, and explore the mechanism of action of disease control by Japanese knotweed based on a disease-resistance gene in Arabidopsis thaliana, a model plant, since the resistance gene has not been revealed in eggplant.

2 Materials and methods

2.1 Disease in Solanaceae crops

2.1.1 Diseases of eggplants (Field experiment 1)

The tests were conducted in 2016 and 2017. Eggplant (cultivar ‘Senryo nigou’) seedlings were planted in 30-cm-diameter plastic pots containing culture soils (Hanachan baiyodo ®) on 27 April 2016 and 28 April 2017. The pots were placed in a greenhouse in the Fujieda field at Shizuoka University (63 Kariyado, Fujieda, Japan). Three mulching treatments were prepared: 1) Japanese knotweed (20 g fresh weight) mulch; 2) Silver grass (Miscanthus sinensis) (fresh weight 20 g) mulch; 3) No mulching (control). A randomized block design with five replicates was adopted.
The degrees of naturally occurring disease were evaluated as 0, 0-5%, 5%-25%, 25%-50%, 50%-75%, and 75%-100%, based on the ratio of the area with lesions to the total leaf area, on 29 September 2016 and on 16 June 2017. The suppression rates for symptoms following the application treatment of distilled water were calculated by substituting the median value of each class.

2.1.2 Eggplants: Brown spot bacterial disease bioassay (Field experiment 2)

Eggplant (cultivar ‘‘Senryo nigou”) seedlings were planted at 12-cm-diameter plastic pots on 27 April 2016 and cultivated for one month. The pots were placed in a greenhouse at the Fujieda field at Shizuoka University (63 Kariyado, Fujieda, Japan). Two experimental pots were set up: 1) Japanese knotweed (3 g fresh weight) mulching; 2) No mulching (control), with a randomized block design and five replicates.
Ten-fold dilutions of a Pseudomonas cichorii (strain SUPP178) cell suspension (ca. 107 cfu mL-1) was inoculated onto the surfaces of the first leaves on the first flowers of each plant using a hand sprayer (1.6 mL plant-1), and a bacterial suspension without dilution (ca. 108 cfu mL-1 was inoculated onto the surfaces of the second leaves on the first flowers of each plant using a hand sprayer (0.8 mL plant-1), on 25 May, 2016. After five days, the degrees of naturally occurring disease were evaluated in a manner similar to that in experiment 1.

2.1.3 Disease in tomato plants (Field experiment 3)

Tomato (cultivar ‘Aiko’) seedlings were planted in 30-cm diameter plastic pots containing culture soils (Product name: DCM-Tomatonobaiyodo, DCM Holdings Co., Ltd., N: P: K = 8:8:8) on 17 May 2019. Three experimental pots were set up: 1) Japanese knotweed (90 g fresh weight), 2) Japanese knotweed extract spraying; 3) No mulching (control). The pot experiments were conducted based on a randomized block design, with five replicates. The degrees of naturally occurring disease were evaluated using the method adopted in Experiment 1, on 14 June 2019 and 28 June 2019.

2.2 Effects of extracts of Japanese knotweed on disease-resistance gene expression

2.2.1 Preparation of extracts of Japanese knotweed and treatment of Arabidopsis

Japanese knotweed extracts were prepared using 1 g leaf fresh weight in 10 mL of distilled water. A. thaliana (Col-0) seeds were sown in Petri dishes and stored under cool dark conditions for 1 day. Thereafter, the Petri dishes were placed in an incubator at 24 ℃ under 3000 lux light conditions for 16 h until germination and the emergence of 5-mm long roots. Young A. thaliana plants were transplanted into cell trays containing autoclaved vermiculite and grown in an incubator until rosette leaves formed. One milliliter of Japanese knotweed extract containing Tween 20 was applied on the surfaces of several A. thaliana leaves using cotton buds. One milliliter of 50 ppm salicylic acid was applied as the positive control. Salicylic acid potentially induces systemic acquired resistance (SAR) in A. thaliana (Hunt et al., 1996; Cameron et al., 1999).
Twenty-four hours after treatment, untreated leaves above the treated leaves were sampled. Total RNA was isolated from A. thaliana using DNase I (New England Biolabs Japan Inc., Tokyo, Japan).

2.2.2 Expression of PR gene in A. thaliana

Complementary DNA was synthesized from 500 ng of total RNA primed with random hexamers using the Perfect Real Time™ RT-PCR kit (Takara Bio, Tokyo, Japan) according to the manufacturer’s protocol. To quantify PR1 and PR5 expression, putative SAR markers in A. thaliana (Il-Pyung et al., 2005), a 40-fold dilution of cDNA mixture was used as the template with SYBR® Premix Ex Taq™ reagent (Takara Bio) for the quantitative real-time PCR assay, which was performed on a Thermal Cycler Dice™ Real Time System (Takara Bio). Reverse-transcribed mRNAs of PR1 and PR5 were amplified with a specific primer pairs (AtPR1-F: 5-CTCGGAGCTACGCACAACAA-3 and AtPR1-R: 5-TTC TCGCTAACCCACATGTTCA-3, and AtPR5-F: 5-GTGTT CATCACAAGCGGCATT-3 and AtPR5-R: 5-CGACCTTG GGTCCTTCAC-3, respectively) (Il-Pyung et al., 2005). The levels of expression of the PRs were normalized against the levels of expression of the actin gene (AtAct-F: 5-TC CTCCGTCTTCACCTTGCT-3 and AtAct-R: 5-ATTTCCC GCTCTGCTGTTGT-3; 226-bp amplicon). We confirmed that actin expression was stable in all treatments. The cycling conditions were as follows: 10 s of polymerase activation at 95 ℃, followed by 40 cycles at 95 ℃ for 5 s and 64 ℃ for 30 s. Each assay included a standard curve with eight serial dilution points of the water-treated sample for the internal control gene, or of the salicylic acid-treated sample for the target gene (ranging from 50 to 640 ng). The assays included a no-template control for each primer set, and cDNA sequences were used. All assays were performed in triplicate.

2.2.3 Data analysis

Data from this study were analyzed using BellCurve for Excel 5.0 (Social Survey Research Information Co., Ltd.) software. After conducting an analysis of variance, the Tukey’s multiple rrange test was used to detect significant differences among the treatments with a probability of 95% (α = 0.05).

3 Results

3.1 Disease in Solanaceae crops

3.1.1 Effect of Japanese knotweed mulching on disease in eggplants (Field experiment 1)

We observed leaf mold (Mycovellosiella nattrassii) and powdery mildew in 2016, and leaf mold (M. nattrassii) in 2017. In 2016, there were no significant differences in the number of diseased plants and proportion of area with leaf mold lesions among the experimental plots (Table 1). The number of diseased plants and proportion of area with lesions were lower in silver grass mulching and Japanese knotweed mulching compared with in the no mulching treatment (control). In 2017, there were no significant differences in the number of leaf mold diseased plants and leaf mold lesion area between silver grass mulching and no mulching. The proportions of leaf area with leaf mold lesions in the Japanese knotweed mulching treatment were significantly lower than in the no mulching treatment.
Table 1 Effects of plant-mulching on plant disease in eggplant
Mulching treatments 2016 2017
Leaf mold (Mycovellosiella nattrassii) Powdery mildew Leaf mold (Mycovellosiella nattrassii)
No. of
diseased plants		 Lesion area percentage (%) Preventive value No. of
diseased plants		 Lesion area
percentage (%)		 Preventive value No. of
diseased plants		 Lesion area percentage (%) Preventive value
Japanese knotweed mulching 4/5 53.5 5.3 1/5 3.0 a 75.0 4/5 11.0 a 66.2
Silver grass mulching 4/5 49.5 10.5 1/5 3.0 a 75.0 4/5 25.0 ab 23.1
Non-treatment 4/5 59.5 - 4/5 12.0 b - 5/5 32.5 b -
ANOVA ns ** *

Note: **, * indicate significant difference at 1% level and 5% level respectively in ANOVA after aricsin transform and ns indicates no siginificant difference. Different letters indicate significant differences among treatments based on Tukey’s multiple range test at 5% level.

3.1.2 Effect of Japanese knotweed mulching on brown spot bacterial disease in eggplants (Field experiment 2)

Under the 10-fold dilution P. cichorii cell suspensions, there were no significant differences in percentage of lesion area with brown spot bacterial disease between the no-mulching plot (51.5%) and the silver glass mulching plot (45.8%) (Table 2). In addition, the proportions of area with brown spot bacterial disease lesions under Japanese knotweed mulching (24.2%) were significantly lower than in the other treatments. The preventive value of the Japanese knotweed mulching on brown spot bacterial disease was 53.0%. Without dilution, there were no significant differences in proportions of areas with brown spot bacterial disease lesions between the no-mulching plot (37.5%) and the silver glass mulching plot (28.7%). The proportion of area with brown spot bacterial disease lesions under Japanese knot weed mulching (13.9%) were significantly lower than in the treatments. The preventive value in the Japanese knotweed mulching plot was 62.9%.
Table 2 Effects of plant-mulching on brown spot bacterial disease (Pseudomonas cichorii (Swingle) Stapp) in eggplant by inoculation test
Mulching treatments Bacterial concentration (×10) Bacterial concentration (×1)
Lesion area percentage (%) Preventive value Lesion area percentage (%) Preventive value
Japanese knotweed mulching 24.2 a 53.0 13.9 a 62.9
Silver grass mulching 45.8 b 11.1 28.7 ab 23.5
Non-treatment 51.5 b - 37.5 b -
ANOVA ** *

Note: **, * indicate significant difference at 1% level and 5% level respectively in ANOVA after aricsin transform. Different letters indicate significant differences among treatments based on Tukey’s multiple range test at 5% level.

3.1.3 Effect of Japanese knotweed treatment on disease in tomato plants (Field experiment 3)

We examined the effects of mulching with Japanese knotweed on tomato spotted bacterial disease (P. syringae) and tomato mosaic virus (ToMV). The number of leaves with tomato spotted bacterial disease in the Japanese knotweed extract plot was lower than that in the control (Table 3). The proportions of areas with lesions of tomato spotted bacterial disease in the Japanese knotweed extract treatments and Japanese knotweed mulching treatments were slightly lower than those in the control treatment. The preventive value against tomato spotted bacterial disease was 15.7% in the Japanese knotweed mulching treatments and 28.2% in the Japanese knotweed extract treatments. ToMV was observed in the control and Japanese knotweed mulching treatments. In contrast, ToMW was not observed in the Japanese knotweed extract treatments. The number of ToMV-diseased leaves was lower in the Japanese knotweed mulching treatment than in the control treatment. The preventive value against ToMV was 43.9% in the Japanese knotweed mulching treatment.
Table 3 Effects of plant-mulching on plant disease in tomato
Mulching treatments Tomato spotted bacterial disease (Pseudomonas syringae) Tomato mosaic virus (ToMV)
No. of
diseased plants		 No. of
diseased leaves		 Lesion area percentage (%) Preventive value No. of
diseased plants		 No. of
diseased leaves		 Preventive value
Japanese knotweed mulching 5/5 4.8 ab 13.5 15.7 2/5 0.8 ab 43.9
Japanese knotweed extract 5/5 3.6 a 11.5 28.2 0/5 0 a 100.0
Non-treatment 5/5 5.0 b 16.0 0 3/5 1.4 b 0
ANOVA * ns *

Note: * indicate significant difference at 5% level in ANOVA after aricsin transform, ns indicates no significant difference. Different letters indicate significant differences among treatments based on Tukey’ multiple range test at 5% level.

3.2 PR expression in Arabidopsis thaliana

Generally, disease-resistance genes in plants are considered sufficiently expressed when their levels of expression are
three-fold or higher relative to those of the negative control (Gilliland et al. 1990). PR1 and PR5 expression levels were 3.6-fold and 24.3-fold higher following treatment with salicylic acid, relative to the levels of expression under the dis-
tilled water control (Fig. 1). In addition, PR1 and PR5 levels of expression under the Japanese knotweed extract treatment were 6.3-fold and 17.6-fold higher than the levels of expression under the distilled water control (Fig. 1).
Fig. 1 Relative levels of expression of PR genes in Arabidopsis thaliana leaf under treatment with salicylic acid and Japanese knotweed extract

4 Discussion

We observed that Japanese knotweed mulching suppressed eggplant and tomato diseases. Furthermore, the inhibitory effects were enhanced by the application of Japanese knotweed extract, when compared to Japanese knotweed mulching in tomato plants. This suggests that some chemicals exuded from Japanese knotweed may have a positive effect on disease control in Solanaceae plants. Thus, local farmers may have used Japanese knotweed mulch empirically to control the disease of solanaceous vegetables, even if that was not the main purpose of its use. In addition, our data show that the Japanese knotweed extract induces the expression of PR genes in Arabidopsis. This suggests that the Japanese knotweed extract may induce the systemic acquired resistance (SAR), in addition to having antibacterial activity. Recently, SAR has gained considerable attention in crop production as a novel next-generation pesticide (Hunt et al., 1996; Ryals et al., 1996; Sticher et al., 1997; Vallad and Goodman, 2004). SAR is the plant’s own defense mechanism induced to achieve broad-spectrum and long-lasting immunity in non-infected tissues (Gaffney et al., 1993; Mauch-Mani and Metraux, 1998; Nakashita et al., 2003). Plant activators are novel substances that protect plants by enhancing their inherent disease-resistance mechanisms (Kessmann et al., 1994; Tally et al., 1999; Iwata, 2001). Plant activators do not act directly on the pathogen, but rather activate the defense mechanisms of the plant, ultimately activating disease pathogen control. Therefore, it is expected that plant activators do not favor the growth of resistant pathogens. In contrast, they may contribute to the reduction in negative environmental impacts (Glynn, 2001). The extracts of Japanese knotweed could harbor novel plant activators. However, although its extract is shown to upregulate the PR gene in Arabidopsis, a genus from the Brassicaceae family, it remains unclear why the Japanese knotweed has been used only in solanaceous crops. The effects of Japanese knotweed extract on crops other than Solanaceae is an issue for future research.
At present, the active ingredient of the Japanese knotweed extract is unknown. One of the possible candidates is oxalic acid. Namely, Japanese knotweed is rich in oxalic acid (Spoerke and Smolinke, 1990; Siener et al., 2006), and it has been reported that extracts of plants with copious amounts of oxalic acid, such as rhubarb and spinach, induce SAR in other plants (Doubrava et al., 1988). Japanese knotweed is generally considered a weed. However, it has been exploited as a medicinal plant in Asia for a long time, and various effective substances have been identified in the species (Patocka et al., 2017). In recent years, resveratrol and anthraquinone have been reported as active ingredients of Japanese knotweed (Kato et al., 2009; Békési et al., 2016). These substances might induce disease resistance in plants, but further research is needed to verify whether these or some other unknown components contribute to the resistance. On the other hands, positive effects of its extracts on crop disease resistance have been confirmed in the giant knotweed (Reynoutria sachalinensis), which is closely related to Japanese knotweed (Daayf et al., 1997; Stavroula and Annegret, 1998; Ishii 2002; Umemura, 2019). The extracts from giant knotweed, such as SAKALIA® (Syngenta, 2020), MILSANA® (Wurms et al., 1999; Fofanab et al., 2002; Konstantinidou-Doltsinis, 2006), and REGALIA® (Pamela, 2002), have been applied as foliar sprays in Europe to control plant diseases without identification of the active ingredient. The extract of Japanese knotweed may thus be used as a novel pesticide. We demonstrated that plants rich in allelechemicals can be used as pellets in agriculture (Inagaki et al., 2020a). We expect that Japanese knotweed can be similarly pelletized for use in agriculture.
In conclusion, our results suggest that the traditional application of Japanese knotweed in the West Awa area has potential applications in future sustainable agriculture initiatives, as a “Traditional Ecological Knowledge” system.

5 Conclusions

The Food and Agriculture Organization of the United Nations initiated a program named Globally Important Agricultural Heritage Systems (GIAHS) in 2002 with the aim of transmitting the value and knowledge of traditional agriculture to subsequent generations. The traditional agricultural systems in GIAHS should offer insights on how to achieve sustainable agricultural production in the future. Recently, traditional ecological knowledge systems are being reevaluated for potential application in future sustainable agriculture activities. In Japanese traditional mulch farming, poaceae species such as silver grass or reed are commonly used. In contrast, local farmers have learned from long- standing experience that Japanese knotweed (Fallopia japonica, polygonaceae) is better for cultivation of solanaceous crops in the Nishi-Awa area, where is a GIAHS site. To date, we have revealed the positive effects of Japanese knotweed mulching on solanaceous crops are: 1) Increased the sugar content and softens the skin in eggplant fruits; 2) Increases sugar content in tomato fruits; 3) Suppression of continuous cropping disorder in tomato and potato. In these studies, we have observed naturally occurring diseases in solanaceous crops tended to decrease when knotweed mulching was applied. Therefore, we study the effects of Japanese knotweed mulching on solanaceous crop disease. As a result, leaf mold and powdery mildew decreased in eggplants under Japanese knotweed mulching. We further evaluated the effects of Japanese knotweed mulching by inoculating test plants with Pseudomonas cichorii. In tomato plants, we observed suppression of bacterial disease and tomato mosaic virus under Japanese knotweed mulching and following spraying with Japanese knotweed extracts. Although Japanese knotweed has not been traditionally used to be applied with the aim of controlling disease, in the present study, we concluded that Japanese knotweed had a potential disease suppressing effect.

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