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Tolerance to Fusarium Root Rot and Changes in Antioxidative Ability in Mycorrhizal Asparagus Plants

Authors:
Abu Shamim Mohammad NahiyanThe United Graduate School of Agricultural Science, Gifu University, 1-1 Yanagido, Gifu 501-1193, Japan

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Yoh-ichi MatsubaraFaculty of Applied Biological Sciences, Gifu University, 1-1 Yanagido, Gifu 501-1193, Japan

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Article Category:
Research Article
Online Publication Date:
Mar 2012
Page(s):
356–360
Volume/Issue:
Volume 47: Issue 3
Copyright:
© American Society for Horticultural Science 2012
DOI:
https://doi.org/10.21273/HORTSCI.47.3.356
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Abstract

Tolerance to fusarium root rot caused by Fusarium oxysporum f. sp. asparagi (Foa, MAFF305556 and N9-31) and the changes in antioxidative abilities in mycorrhizal asparagus (Asparagus officinalis L., cv. Welcome) plants were investigated. Asparagus plants were inoculated with arbuscular mycorrhizal fungus (AMF, Glomus sp. R10) and Foa was inoculated 10 weeks after AMF inoculation. AMF plants accumulated higher dry weight of ferns and roots than non-AMF plants before and after Foa inoculation. AMF colonization level reached more than 70% and no difference noted among the treatments. As for disease tolerance, non-AMF plants showed 100% in incidence of root rot and highest severity in both Foa isolates; the severity of symptom was relatively higher in MAFF305556 compared with N9-31. However, AMF plants showed lower severity than non-AMF plants in both Foa isolates. Before and after Foa inoculation, antioxidative abilities increased in most of the AMF plants than non-AMF in the following items: activity of superoxide dismutase (SOD) and ascorbate peroxidase (APX), 1,1-diphenyl-2-picrylhydrazyl (DPPH) radical scavenging activity, and total contents of polyphenol and ascorbic acids. These results suggest that plant growth enhancement and tolerance to fusarium root rot appeared in mycorrhizal asparagus plants. In this case, the disease tolerance might be associated with the increase in antioxidative ability.

Keywords: arbuscular mycorrhizal fungi; asparagus decline; Fusarium oxysporum f. sp. asparagi; growth promotion; symbiosis

Asparagus (Asparagus officinalis L.) is a low-input, high-market value and long-term perennial vegetable crop with a production cycle of up to 15 years or more (Hamel et al., 2005; Yergeau et al., 2006). It is a rich source of phytochemicals such as flavonoids (e.g., rutin and anthocyanins), other phenolic and polyphenolic compounds, saponins, etc., which have biological and medicinal impact on human health (Hartung et al., 1990). However, asparagus decline is a serious and increasing threat in asparagus-producing regions over the world (Hamel et al., 2005; Knaflewski et al., 2008; Reid et al., 2002; Wong and Jeffries, 2006). Asparagus decline is typified by a decrease in yields with a reduction in spear size and number and then eventual death of plants within a few years of planting (Wong and Jeffries, 2006). As a result, asparagus is eventually abandoned and alternative crops are planted. The problem is exacerbated by a replant phenomenon such that additional loss is incurred if fields are replanted with asparagus (Blok and Bollen, 1995). A number of facts worldwide contribute to asparagus decline, but the most significant is crown and root rot caused by Foa and Fusarium proliferatum (Elmer et al., 1996; Knaflewski et al., 2008; Nahiyan et al., 2011; Reid et al., 2002; Wong and Jeffries, 2006). In addition, abiotic factors such as allelopathic residues can increase plant stress and accelerate the decline phenomenon (Lake et al., 1993; Miller et al., 1991; Yong, 1984). The biotic factors (diseases) and the abiotic factors (allelopathy, etc.) are difficult to control because no resistant cultivar or disinfesting method has been developed. Actually, breeding of disease-resistant cultivars has been attempted (Pontaroli and Camadro, 2001); however, it takes a long time to develop. On the other hand, biological control of fusarium disease was tried by inoculation with non-pathogenic isolates of the fusarium species (Blok et al., 1997; Reid et al., 2002). However, the method is not enough to control and has no growth-promoting effect.

Arbuscular mycorrhizal fungi are well known as wide-spectrum biocontrol agents (Yergeau et al., 2006) that has the effect of promoting host plant growth mainly by enhancing phosphorus uptake through symbiosis (Marschner and Dell, 1994). Previously, we found tolerance to fusarium root rot in mycorrhizal asparagus (cv. Mary Washington 500W) plants (Matsubara et al., 2003); however, many points remain unclear about the mechanisms of disease tolerance in mycorrhizal plants. In pathogen stress conditions, production of a higher concentration of reactive oxygen species (ROS) such as H2O2, superoxide anion (O2–), and hydroxyl radical has been shown to create cytotoxic conditions (Sahoo et al., 2007). To overcome this negative consequence of ROS, plants have evolved various protective mechanisms either to reduce or completely eliminate antioxidative abilities of producing antioxidative enzymes and substances under environmental stresses such as plant disease, drought, and temperature (Moghaddam et al., 2006; Sahoo et al., 2007). As for mycorrhizal plants, Garmendia et al. (2006) reported that disease tolerance and an increase in SOD activity occurred in pepper, and drought tolerance and antixodative enzymes (activity of SOD and APX) increased in mycorrhizal citrus plants (Wu et al., 2006). In addition, Zhu et al. (2010) demonstrated that tolerance to high-temperature stress and an increase in antioxidative enzymes occurred in mycorrhizal maize plants. However, it has been unclear how antioxidative factors change through symbiosis with AMF in asparagus plants and how the changes are associated with disease tolerance.

In this study, the influence of AMF colonization on tolerance to fusarium root rot and the changes in antioxidative ability in mycorrhizal asparagus plants were investigated to clarify the mechanisms of disease tolerance.

Materials and Methods

Inoculation of arbuscular mycorrhizal fungus.

Seeds of asparagus (Asparagus officinalis L., cv. Welcome) were sown in commercial soil (autoclaved at 1.2 kg·cm−2 and 121 °C for 1 h) in a plastic container (43 × 27 × 17 cm). During the time of seed sowing, plant holes were made; each hole contained 3 g/plant commercial AMF (Glomus sp. R10) inocula supplied by Idemitsukosan Co. Ltd. (Tokyo, Japan). Then, seeds were sown onto the inocula, finally covered with soil, and administered with mixed fertilizer (13N:11P:13K, 0.5 g per plant). Forty plants per plot with three replications were irrigated as regularly and grown in a greenhouse.

Inoculation of Fusarium oxysporum f. sp. asparagi.

Two strains of Foa (MAFF305556 and N9-31) were grown on potato dextrose agar media. The conidia were harvested in potato sucrose liquid media and incubated at 25 °C in the dark for 7 d. The conidial suspension was sieved and the concentrations adjusted to 106 conidia/mL. Ten weeks after AMF inoculation, each plant was inoculated by pouring 50 mL of the conidial suspension onto the soil.

Evaluation of arbuscular mycorrhizal fungus colonization level.

Ten weeks after AMF inoculation and 8 weeks after Foa inoculation, roots of asparagus were preserved with 70% ethanol and stained according to Phillips and Hayman (1970). The rate of AMF colonization in 1-cm segments of lateral roots (abbreviated RFCSL) was calculated. Hence, RFCSL expresses the percentage of 1-cm AMF-colonized segments to the total 1-cm segments of all lateral roots; the number of total segments was ≈30 per plant. Average colonization was calculated from the values of five plants in each time.

Estimation of symptoms of fusarium root rot.

Eight weeks after Foa inoculation, the symptoms (reddish brown root lesion and transparent rotted part of roots) of fusarium root rot were rated to 6 degrees as follows: 0, no symptom; frequency of diseased storage roots in a root system: 1, less than 20%; 2, 20% to 40%; 3, 40% to 60%; 4, 60% to 80%; and 5, 80% to 100%. In addition, the disease index was calculated by the following formula:
DE1

Analysis of antioxidative abilities.

Ten weeks after AMF inoculation and 8 weeks after Foa inoculation, 10 plants were sampled and partitioned into ferns and roots and frozen in liquid nitrogen. Analysis of antioxidative enzyme activities and antioxidative substances were carried out according to the methods of Beauchamp and Fridovich (1971) (SOD), Wu et al. (2006) (APX), Burits and Bucar (2000) (DPPH radical scavenging activity), Folin and Denis (1915) (polyphenol), and Roe et al. (1948) (ascorbic acid), respectively.

Statistical analysis.

Mean values were separated by t test for dry weight (10 weeks after AMF inoculation), RFCSL, and antioxidative abilities at P ≤ 0.05. Dry weight (8 weeks after Foa inoculation) was analyzed by Tukey's multiple range test at P ≤ 0.05. All analyses were performed using XLSTAT pro statistical analysis software (Addinsoft, New York, NY).

Results

Ten weeks after AMF inoculation, AMF plants significantly enhanced the dry weight of ferns and roots compared with the non-AMF plants (Fig. 1). AMF colonization occurred successfully and reached up to 63%, 10 weeks after AMF inoculation (data not shown). As for antioxidative ability, 10 weeks after AMF inoculation, SOD and APX activity were higher in AMF plots than non-AMF in both ferns and roots (Fig. 2). On the other hand, DPPH radical scavenging activity and polyphenol contents increased in most of the plant parts of AMF plots than non-AMF, except ferns in polyphenol contents. Ascorbic acid contents showed no difference in both ferns and roots between AMF and non-AMF plots.

Fig. 1.
Fig. 1.

Dry weight of ferns and roots in mycorrhizal asparagus plants 10 weeks after arbuscular mycorrhizal fungus (AMF) inoculation. N = non-AMF-inoculated plants; AMF = Glomus sp. R10. Bars represent ses (n = 10). *Significant difference between non-AMF and AMF plants (t test, P ≤ 0.05).

Citation: HortScience horts 47, 3; 10.21273/HORTSCI.47.3.356

Fig. 2.
Fig. 2.

Superoxide dismutase (SOD), ascorbate peroxidase (APX), 1,1-diphenyl-2-picrylhydrazyl (DPPH) radical scavenging activity, polyphenol, and ascorbic acid contents in ferns and roots 10 weeks after arbuscular mycorrhizal fungus (AMF) inoculation. N = non-AMF-inoculated plants; AMF = Glomus sp. R10. Bars represent se (n = 10). *Significant difference between non-AMF and AMF plants (t test, P ≤ 0.05); ns = nonsignificant.

Citation: HortScience horts 47, 3; 10.21273/HORTSCI.47.3.356

Eight weeks after Foa inoculation, non-AMF plants showed 100% in incidence of root rot and highest severity in both Foa isolates; the severity of symptom was relatively higher in MAFF305556 compared with N9-31(Fig. 3); no disease symptom appeared in the plants without Foa inoculation (data not shown). However, AMF plants showed lower severity than non-AMF plants, and the severity of symptoms varied depending on Foa isolates; MAFF305556 plants showed relatively lower incidence and severity than N9-31 in AMF plants. The disease indices of fusarium root rot reached more than 80 in non-AMF plants of the Foa isolates, whereas it was low as 37 in MAFF 305556 and 57 in N9-31 of AMF plants (Fig. 4). Hence, the disease indices and incidence of fusarium root rot for the AMF and non-AMF plants followed a similar pattern. As for growth condition of asparagus plants 8 weeks after Foa inoculation, dry weight of ferns and roots was greater in AMF plants than non-AMF in both Foa (Fig. 5). AMF colonization level (RFCSL) reached more than 70% and no differences were noted between the treatments (Fig. 6).

Fig. 3.
Fig. 3.

Incidence of fusarium root rot in asparagus plants 8 weeks after Fusarium oxysporum f. sp. asparagi (Foa) inoculation. Ratio of diseased roots in a root system: , –20; , 20–40; ,40–60; , 60–80; , 80% to 100%. N = non-AMF-inoculated; AMF = Glomus sp. R10; MAFF305556 and N9-31, Foa.

Citation: HortScience horts 47, 3; 10.21273/HORTSCI.47.3.356

Fig. 4.
Fig. 4.

Disease indices of fusarium root rot in asparagus plants 8 weeks after Fusarium oxysporum f. sp. asparagi (Foa) inoculation. N = non-AMF-inoculated; AMF = Glomus sp. R10; MAFF305556 and N9-31, Foa.

Citation: HortScience horts 47, 3; 10.21273/HORTSCI.47.3.356

Fig. 5.
Fig. 5.

Dry weight of ferns and roots in mycorrhizal asparagus plants 8 weeks after Fusarium oxysporum f. sp. asparagi (Foa) inoculation. N = non-AMF-inoculated plants; AMF = Glomus sp. R10; MAFF305556 and N9-31, Foa. Bars represent ses (n = 10). Columns denoted by different letters indicate significant difference by Tukey's test (P = 0.05).

Citation: HortScience horts 47, 3; 10.21273/HORTSCI.47.3.356

Fig. 6.
Fig. 6.

Arbuscular mycorrhizal fungus (AMF) colonization level (RFCSL) in asparagus plants 8 weeks after Fusarium oxysporum f. sp. asparagi (Foa) inoculation. AMF = Glomus sp. R10; MAFF305556 and N9-31, Foa. Bars represent ses (n = 5). ns = indicates no significant difference between the treatments (t test, P ≤ 0.05).

Citation: HortScience horts 47, 3; 10.21273/HORTSCI.47.3.356

In the analysis of antioxidative ability 8 weeks after Foa inoculation, AMF plants showed higher SOD activity in both ferns and roots than non-AMF plants (Fig. 7). APX activity was higher in ferns of AMF plants, but no difference appeared in roots of AMF and non-AMF. On the other hand, DPPH radical scavenging activity increased in roots of AMF plants, whereas polyphenol and ascorbic acid contents were higher in both ferns and roots of AMF plants compared with non-AMF.

Fig. 7.
Fig. 7.

Superoxide dismutase (SOD), ascorbate peroxidase (APX), 1,1-diphenyl-2-picrylhydrazyl (DPPH) radical scavenging activity, polyphenol, and ascorbic acid contents in ferns and roots of mycorrhizal asparagus plants 8 weeks after Fusarium oxysporum f. sp. asparagi (Foa) (MAFF 305556) inoculation. N = non-AMF-inoculated plants; AMF = Glomus sp. R10. Bars represent ses (n = 10). *Significant difference between non-AMF and AMF plants (t test, P ≤ 0.05); ns = nonsignificant.

Citation: HortScience horts 47, 3; 10.21273/HORTSCI.47.3.356

Discussion

In this study, dry weight of ferns and roots increased in all the AMF plants compared with non-AMF before and after Foa inoculation, which indicates the growth enhancement through symbiosis appeared in mycorrhizal asparagus plants. Previous reports revealed similar results indicating that AMF had a growth-promoting effect in host plants (Ozgonen and Erkilic, 2007; Wu et al., 2006). As for tolerance to fusarium root rot in this experiment, both incidence and severity of symptoms were reduced by AMF, suggesting that tolerance to fusarium root rot appeared in mycorrhizal asparagus plants. Matsubara et al. (2003) reported that AMF increased root rot tolerance in asparagus (cv. Mary Washington 500W) plants; our results in ‘Welcome’ agreed with those findings. Norman et al. (1996) reported that the incidence of the symptom caused by Phytophthora fragariae in strawberry plants was reduced by the inoculation of AMF, although the effect differed with AMF species. Ozgonen and Erkilic (2007) reported that growth promotion and tolerance to Phytophthora capsici had no correlation with the mycorrhizal colonization levels in peppers. In the present experiment, we could not clarify AMF fungal difference in disease tolerance, and no characteristic relationship between colonization levels and disease tolerance appeared. On the other hand, Sutton (1973) demonstrated that AMF colonization consisted of three phases: 1) a leg phase during which spore germination, germ tube growth, and initial penetration occur; 2) a rapid growth phase, coinciding with the development of external mycelium, and spread of the fungus within the roots; and 3) a stable phase during which the proportion of infected roots to non-infected ones remains nearly constant. In this study, colonization level was checked only twice so that it is difficult to estimate when AMF reached the maximum colonization level during the experimental period and how the colonization level affects the disease tolerance.

Some reports described that AMF colonization itself induced a temporary increase in antioxidative abilities such as SOD, guaiacol peroxidase, catalase, APX, and flavonoid content, suggesting that colonization might be temporary stress for host plants. (Blilou et al., 2000; Salzer et al., 1999; Volpin et al., 1995; Wu et al., 2006; Zhu et al., 2010). In this study, SOD, APX, and DPPH radical scavenging activity in both ferns and roots and polyphenol contents in roots increased in all the AMF plants before Foa inoculation. In the aspects of such antioxidative factors, our results support their findings. However, ascorbic acid contents did not increase before Foa inoculation, so it is difficult to estimate completely whether AMF colonization is a stress factor for asparagus plants.

SOD acts as a defensive reaction and detoxifies O2– among the antioxidative enzymes; thus, SOD activity is considered the most important key enzyme in antioxidative abilities in plants (Fridovich, 1986). Sahoo et al. (2007) mentioned that SOD activity increased in Phytopthora blight in taro under induced blight condition compared with controls. In mycorrhizal pepper plants, increase in SOD activity and disease tolerance appeared in pathogen (Verticillium dahliae) stress conditions (Garmendia et al., 2006). Moghaddam et al. (2006) mentioned that SOD activity was higher in a resistant strawberry cultivar than susceptible cultivars with Mycosphaerella fragariae infection. In the present study, tolerance to fusarium root rot appeared in mycorrhizal asparagus plants, and SOD and APX activity increased in most of the parts of AMF plants after Foa inoculation. Our results showed similar patterns to those findings because the increase in SOD activity related to disease tolerance. From these findings, antioxidative enzyme activity might be closely related with disease tolerance in mycorrhizal plants. However, in this study, analysis of antioxidative abilities was carried out only twice; on the contrary, it is difficult to clarify the detailed relationship between disease tolerance and antioxidative enzyme abilities. Further studies would be needed in this context to increase the frequency of analysis of antioxidative abilities both before and after Foa inoculation with a short interval.

Antioxidative substances such as polyphenol contents have lower electron reduction potential than the electron reduction potential of oxygen radicals; as a result, polyphenol contents directly scavenge reactive oxygen intermediates without promoting further oxidative reactions (Ainsworth and Gillespie, 2007). Vanitha et al. (2009) mentioned that total phenol content increased in bacterial wilt in tomato on pathogen inoculation. Hichem et al. (2009) reported that salt stress induced DPPH free radical scavenging activity and polyphenolic compounds in maize. In mycorrhizal St. John's wort plants, increased ascorbic acid content and disease tolerance appeared in pathogen (Colletotrichum gloeosporioides) stress conditions (Richter et al., 2011). From these facts, antioxidative substances have some relation with stress factors. Our results showed similar patterns to those findings as the increase in DPPH radical scavenging activity, polyphenol, and ascorbic acid contents in most of the Foa-inoculated AMF plots. Hence, antioxidative substances also have an association with disease tolerance in mycorrhizal asparagus plants, the same as antioxidative enzymes.

On the other hand, Pozo et al. (2002) reported that in tomato plants with a split root system, tolerance to Phytophthora parasitica appeared in both non-AMF-inoculated roots and inoculated roots in AMF plants, so that induced systemic disease tolerance was recognized. In this study, some of the antioxdative abilities increased in ferns, where no colonization occurred. From these facts, we estimate the induced systemic disease tolerance in mycorrhizal asparagus plants with a split root system for fusarium disease in addition to fern disease such as stem blight and the relationship between antioxidative ability and induced disease tolerance.

In conclusion, these results suggest that tolerance to fusarium root rot was induced in asparagus plants by AMF, and disease tolerance has an association with the changes in antioxidative abilities. This proposal seeks to develop a sustainable practice to manage the disease and improve plant health, thus contributing to an improvement in asparagus decline.

Literature Cited

  • Ainsworth, E.A. & Gillespie, K.M. 2007 Estimation of total phenolic content and other oxidation substrates in plant tissues using Folin-Ciocalteu reagent Nat. Protoc. 2 875 877

    • Search Google Scholar
    • Export Citation

  • Beauchamp, C. & Fridovich, I. 1971 Superoxide dismutase: Improved assays and an assay applicable to acrylamide gels Anal. Biochem. 44 276 287

  • Blilou, I., Bueno, P., Ocampo, J.A. & Garrido, J.M. 2000 Induction of catalase and ascorbate peroxidase activities tobacco roots inoculated with the arbuscular mycorrhizal Glomus mosseae Mycol. Res. 104 722 725

    • Search Google Scholar
    • Export Citation

  • Blok, W.J. & Bollen, G.J. 1995 Fungi on roots and stem bases of asparagus in the Netherlands: Species and pathogenicity Eur. J. Plant Pathol. 101 15 24

    • Search Google Scholar
    • Export Citation

  • Blok, W.J., Zwankhuizen, M.J. & Bollen, G.J. 1997 Biological control of Fusarium oxysporum f. sp. asparagi by applying non-pathogenic isolates of F. oxysporum Biocont. Sci. Tech. 7 527 541

    • Search Google Scholar
    • Export Citation

  • Burits, M. & Bucar, F. 2000 Antioxidant activity of Nigella sativa essential oil Phytother. Res. 14 323 328

  • Elmer, W.H., Johnson, D.A. & Mink, G.I. 1996 Epidemiology and management of the diseases causal to asparagus decline Plant Dis. 80 117 125

  • Folin, O. & Denis, W. 1915 A colorimetric method for the determination of phenols (and phenol derivatives) in urine Biol. Chem. 22 305 308

  • Fridovich, I. 1986 Biological effects of the superoxide radicals Arch. Biochem. Biophys. 247 1 11

  • Garmendia, I., Aguirreolea, J. & Goicoechea, N. 2006 Defence-related enzymes in pepper roots during interactions with arbuscular mycorrhizal fungi and/or Verticillium dahliae Biocont. 51 293 310

    • Search Google Scholar
    • Export Citation

  • Hamel, H., Vujanovic, V., Nakano-Hylander, A., Jeannotte, R. & St-Arnaud, M. 2005 Factors associated with fusarium crown and root rot of asparagus outbreaks in Quebec Phytopathology 95 867 873

    • Search Google Scholar
    • Export Citation

  • Hartung, A.C., Nair, M.G. & Putnam, A.R. 1990 Isolation and characterization of phytotoxic compounds from asparagus (Asparagus officinalis L.) roots J. Chem. Ecol. 16 1707 1718

    • Search Google Scholar
    • Export Citation

  • Hichem, H., Mounir, D. & Naceur, E.A. 2009 Defferential responses of two maize (Zea mays L.) varieties to salt stress: Changes on polyphenols composition of foliage and oxidative damages Ind. Crops Prod. 30 144 151

    • Search Google Scholar
    • Export Citation

  • Knaflewski, M., Golinski, P., Kostecki, M., Waskiewicz, A. & Weber, Z. 2008 Mycotoxins and mycotoxin-producing fungi occurring in asparagus spears Acta Hort. 776 183 189

    • Search Google Scholar
    • Export Citation

  • Lake, R.J., Falloon, P.G. & Cook, D.W.M. 1993 Replant problem and chemical components of asparagus roots N. Z. J. Crop Hort. Sci. 21 53 58

  • Marschner, H. & Dell, B. 1994 Nutrient uptake in mycorrhizal symbiosis Plant Soil 159 89 102

  • Matsubara, Y., Hasegawa, N. & Ohba, N. 2003 Relation between fiber and pactic substance in root tissue and tolerance to fusarium root rot in asparagus plants infected with arbuscular mycorrhizal fungus J. Jpn. Soc. Hort. Sci. 72 275 280

    • Search Google Scholar
    • Export Citation

  • Miller, H.G., Ikawa, M. & Peirce, L.C. 1991 Caffeic acid identified as an inhibitory compound in asparagus root filtrate HortScience 26 1525 1527

  • Moghaddam, B., Charles, M.T., Carisse, O. & Khanizadeh, S. 2006 Superoxide dismutase responses of strawberry cultivars to infection by Mycosphaerrella fragariae J. Plant Physiol. 163 147 153

    • Search Google Scholar
    • Export Citation

  • Nahiyan, A.S.M., Boyer, L.R., Jeffries, P. & Matsubara, Y. 2011 PCR-SSCP analysis of fusarium diversity in asparagus decline in Japan Eur. J. Plant Pathol. 130 197 203

    • Search Google Scholar
    • Export Citation

  • Norman, J.R., Atkinson, D. & Hooker, J.E. 1996 Arbuscular mycorrhizal fungal-induced alteration to root architecture in strawberry and induced resistance to the root pathogen Phytophthora fragariae Plant Soil 185 191 198

    • Search Google Scholar
    • Export Citation

  • Ozgonen, H. & Erkilic, A. 2007 Growth enhancement and Phytophthora blight (Phytophthora capsici Leonian) control by arbuscular mycorrhizal fungal inoculation in pepper Crop Prot. 26 1682 1688

    • Search Google Scholar
    • Export Citation

  • Phillips, J.M. & Hayman, D.S. 1970 Improved procedures for clearing roots and staining parasitic and vesicular–arbuscular mycorrhizal fungi for rapid assessment of infection Trans. Br. Mycol. Soc. 55 158 163

    • Search Google Scholar
    • Export Citation

  • Pontaroli, A.C. & Camadro, E.L. 2001 Increasing resistance to fusarium crown and root rot in asparagus by gametophyte selection Euphytica 122 343 350

    • Search Google Scholar
    • Export Citation

  • Pozo, M.J., Cordier, C., Gaudot, E.D., Barea, J.M. & Aguilar, C.A. 2002 Localized versus systemic effect of arbuscular mycorrhizal fungi on defence responses to Phytophthora infection in tomato plants J. Expt. Bot. 53 525 534

    • Search Google Scholar
    • Export Citation

  • Reid, T.C., Hausbeck, M.K. & Kizilkaya, K. 2002 Use of fungicides and biological controls in the suppression of fusarium crown and root rot of asparagus under green house and growth chamber conditions Plant Dis. 86 493 498

    • Search Google Scholar
    • Export Citation

  • Richter, J., Baltruschat, H., Kabrodt, K. & Schellenberg, I. 2011 Impact of arbuscular mycorrhiza on the St. John's wort (Hypericum perforatum) wilt disease induced Colletotricuhum cf. gloeosporioides J. Plant Dis. Prot. 118 109 118

    • Search Google Scholar
    • Export Citation

  • Roe, J.H., Mary, B.M., Oesterking, M.J. & Charlotle, M.D. 1948 The determination of diketo-L-gluconic acid, dehydro-L-ascorbic acid, and L-ascorbic acid in the same tissues by 2,4-dinitrophenyl hydrazine method Biol. Chem. 174 201 208

    • Search Google Scholar
    • Export Citation

  • Sahoo, M.R., Dasgupta, A.M., Paresh, A., Kole, C., Jayant, A., Bhat, S. & Mukherjee, A. 2007 Antioxidative enzymes and isozymes analysis of taro genotypes and their implications in Phytophthora blight disease resistance Mycopathologia 163 241 248

    • Search Google Scholar
    • Export Citation

  • Salzer, P., Corbiere, H. & Boller, T. 1999 Hydrogen peroxidase accumulation in Medicago truncatula roots colonized by the arbuscular mycorrhiza-forming fungus Glomus intraradices Planta 208 319 325

    • Search Google Scholar
    • Export Citation

  • Sutton, J.C. 1973 Development of vesicular–arbuscular mycorrhizae in crop plants Can. J. Bot. 51 2487 2493

  • Vanitha, S.C., Niranjana, S.R. & Umesha, S. 2009 Role of phenylalanine ammonia lyase and polyphenol oxidase in host resistance to bacterial wilt of tomato J. Phytopathol. 157 552 557

    • Search Google Scholar
    • Export Citation

  • Volpin, H., Phillips, D.A., Okon, Y. & Kapulnik, Y. 1995 Suppression of an isoflavonoid phytoalexin defense response on mycorrhizal alfalfa roots Plant Physiol. 108 1449 1454

    • Search Google Scholar
    • Export Citation

  • Wong, J.Y. & Jeffries, P. 2006 Diversity of pathogenic fusarium populations associated with asparagus roots in decline soils in Spain and the UK Plant Pathol. 55 331 342

    • Search Google Scholar
    • Export Citation

  • Wu, Q., Zou, Y. & Xia, R. 2006 Effect of water stress and arbuscular mycorrhizal fungi on reactive oxygen metabolism and antioxidant production by citrus (Citrus tangerine) roots Eur. J. Soil Biol. 42 166 172

    • Search Google Scholar
    • Export Citation

  • Yergeau, E., Vujanovic, V. & St-Arnaud, M. 2006 Changes in communities of fusarium and arbuscular mycorrhizal as related to different asparagus cultural factors Microb. Ecol. 52 104 113

    • Search Google Scholar
    • Export Citation

  • Yong, C.C. 1984 Autointoxication in root exudates of Asparagus officinalis L Plant Soil 82 247 253

  • Zhu, X., Song, F. & Xu, H. 2010 Influence of arbuscular mycorrhiza on lipid peroxidation and antioxidative enzyme activity of maize plants under temperature stress Mycorrhiza 20 325 332

    • Search Google Scholar
    • Export Citation
Received:
27 Dec 2011
|
Accepted:
06 Feb 2012
|
Published-print:
01 Mar 2012
Received:
27 Dec 2011
|
Accepted:
06 Feb 2012
|
Published-print:
01 Mar 2012
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    Dry weight of ferns and roots in mycorrhizal asparagus plants 10 weeks after arbuscular mycorrhizal fungus (AMF) inoculation. N = non-AMF-inoculated plants; AMF = Glomus sp. R10. Bars represent ses (n = 10). *Significant difference between non-AMF and AMF plants (t test, P ≤ 0.05).

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    Superoxide dismutase (SOD), ascorbate peroxidase (APX), 1,1-diphenyl-2-picrylhydrazyl (DPPH) radical scavenging activity, polyphenol, and ascorbic acid contents in ferns and roots 10 weeks after arbuscular mycorrhizal fungus (AMF) inoculation. N = non-AMF-inoculated plants; AMF = Glomus sp. R10. Bars represent se (n = 10). *Significant difference between non-AMF and AMF plants (t test, P ≤ 0.05); ns = nonsignificant.

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    Incidence of fusarium root rot in asparagus plants 8 weeks after Fusarium oxysporum f. sp. asparagi (Foa) inoculation. Ratio of diseased roots in a root system: , –20; , 20–40; ,40–60; , 60–80; , 80% to 100%. N = non-AMF-inoculated; AMF = Glomus sp. R10; MAFF305556 and N9-31, Foa.

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    Disease indices of fusarium root rot in asparagus plants 8 weeks after Fusarium oxysporum f. sp. asparagi (Foa) inoculation. N = non-AMF-inoculated; AMF = Glomus sp. R10; MAFF305556 and N9-31, Foa.

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    Dry weight of ferns and roots in mycorrhizal asparagus plants 8 weeks after Fusarium oxysporum f. sp. asparagi (Foa) inoculation. N = non-AMF-inoculated plants; AMF = Glomus sp. R10; MAFF305556 and N9-31, Foa. Bars represent ses (n = 10). Columns denoted by different letters indicate significant difference by Tukey's test (P = 0.05).

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    Arbuscular mycorrhizal fungus (AMF) colonization level (RFCSL) in asparagus plants 8 weeks after Fusarium oxysporum f. sp. asparagi (Foa) inoculation. AMF = Glomus sp. R10; MAFF305556 and N9-31, Foa. Bars represent ses (n = 5). ns = indicates no significant difference between the treatments (t test, P ≤ 0.05).

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    Superoxide dismutase (SOD), ascorbate peroxidase (APX), 1,1-diphenyl-2-picrylhydrazyl (DPPH) radical scavenging activity, polyphenol, and ascorbic acid contents in ferns and roots of mycorrhizal asparagus plants 8 weeks after Fusarium oxysporum f. sp. asparagi (Foa) (MAFF 305556) inoculation. N = non-AMF-inoculated plants; AMF = Glomus sp. R10. Bars represent ses (n = 10). *Significant difference between non-AMF and AMF plants (t test, P ≤ 0.05); ns = nonsignificant.

Dry weight of ferns and roots in mycorrhizal asparagus plants 10 weeks after arbuscular mycorrhizal fungus (AMF) inoculation. N = non-AMF-inoculated plants; AMF = Glomus sp. R10. Bars represent ses (n = 10). *Significant difference between non-AMF and AMF plants (t test, P ≤ 0.05).

Superoxide dismutase (SOD), ascorbate peroxidase (APX), 1,1-diphenyl-2-picrylhydrazyl (DPPH) radical scavenging activity, polyphenol, and ascorbic acid contents in ferns and roots 10 weeks after arbuscular mycorrhizal fungus (AMF) inoculation. N = non-AMF-inoculated plants; AMF = Glomus sp. R10. Bars represent se (n = 10). *Significant difference between non-AMF and AMF plants (t test, P ≤ 0.05); ns = nonsignificant.

Incidence of fusarium root rot in asparagus plants 8 weeks after Fusarium oxysporum f. sp. asparagi (Foa) inoculation. Ratio of diseased roots in a root system: , –20; , 20–40; ,40–60; , 60–80; , 80% to 100%. N = non-AMF-inoculated; AMF = Glomus sp. R10; MAFF305556 and N9-31, Foa.

Disease indices of fusarium root rot in asparagus plants 8 weeks after Fusarium oxysporum f. sp. asparagi (Foa) inoculation. N = non-AMF-inoculated; AMF = Glomus sp. R10; MAFF305556 and N9-31, Foa.

Dry weight of ferns and roots in mycorrhizal asparagus plants 8 weeks after Fusarium oxysporum f. sp. asparagi (Foa) inoculation. N = non-AMF-inoculated plants; AMF = Glomus sp. R10; MAFF305556 and N9-31, Foa. Bars represent ses (n = 10). Columns denoted by different letters indicate significant difference by Tukey's test (P = 0.05).

Arbuscular mycorrhizal fungus (AMF) colonization level (RFCSL) in asparagus plants 8 weeks after Fusarium oxysporum f. sp. asparagi (Foa) inoculation. AMF = Glomus sp. R10; MAFF305556 and N9-31, Foa. Bars represent ses (n = 5). ns = indicates no significant difference between the treatments (t test, P ≤ 0.05).

Superoxide dismutase (SOD), ascorbate peroxidase (APX), 1,1-diphenyl-2-picrylhydrazyl (DPPH) radical scavenging activity, polyphenol, and ascorbic acid contents in ferns and roots of mycorrhizal asparagus plants 8 weeks after Fusarium oxysporum f. sp. asparagi (Foa) (MAFF 305556) inoculation. N = non-AMF-inoculated plants; AMF = Glomus sp. R10. Bars represent ses (n = 10). *Significant difference between non-AMF and AMF plants (t test, P ≤ 0.05); ns = nonsignificant.

  • Ainsworth, E.A. & Gillespie, K.M. 2007 Estimation of total phenolic content and other oxidation substrates in plant tissues using Folin-Ciocalteu reagent Nat. Protoc. 2 875 877

    • Search Google Scholar
    • Export Citation

  • Beauchamp, C. & Fridovich, I. 1971 Superoxide dismutase: Improved assays and an assay applicable to acrylamide gels Anal. Biochem. 44 276 287

  • Blilou, I., Bueno, P., Ocampo, J.A. & Garrido, J.M. 2000 Induction of catalase and ascorbate peroxidase activities tobacco roots inoculated with the arbuscular mycorrhizal Glomus mosseae Mycol. Res. 104 722 725

    • Search Google Scholar
    • Export Citation

  • Blok, W.J. & Bollen, G.J. 1995 Fungi on roots and stem bases of asparagus in the Netherlands: Species and pathogenicity Eur. J. Plant Pathol. 101 15 24

    • Search Google Scholar
    • Export Citation

  • Blok, W.J., Zwankhuizen, M.J. & Bollen, G.J. 1997 Biological control of Fusarium oxysporum f. sp. asparagi by applying non-pathogenic isolates of F. oxysporum Biocont. Sci. Tech. 7 527 541

    • Search Google Scholar
    • Export Citation

  • Burits, M. & Bucar, F. 2000 Antioxidant activity of Nigella sativa essential oil Phytother. Res. 14 323 328

  • Elmer, W.H., Johnson, D.A. & Mink, G.I. 1996 Epidemiology and management of the diseases causal to asparagus decline Plant Dis. 80 117 125

  • Folin, O. & Denis, W. 1915 A colorimetric method for the determination of phenols (and phenol derivatives) in urine Biol. Chem. 22 305 308

  • Fridovich, I. 1986 Biological effects of the superoxide radicals Arch. Biochem. Biophys. 247 1 11

  • Garmendia, I., Aguirreolea, J. & Goicoechea, N. 2006 Defence-related enzymes in pepper roots during interactions with arbuscular mycorrhizal fungi and/or Verticillium dahliae Biocont. 51 293 310

    • Search Google Scholar
    • Export Citation

  • Hamel, H., Vujanovic, V., Nakano-Hylander, A., Jeannotte, R. & St-Arnaud, M. 2005 Factors associated with fusarium crown and root rot of asparagus outbreaks in Quebec Phytopathology 95 867 873

    • Search Google Scholar
    • Export Citation

  • Hartung, A.C., Nair, M.G. & Putnam, A.R. 1990 Isolation and characterization of phytotoxic compounds from asparagus (Asparagus officinalis L.) roots J. Chem. Ecol. 16 1707 1718

    • Search Google Scholar
    • Export Citation

  • Hichem, H., Mounir, D. & Naceur, E.A. 2009 Defferential responses of two maize (Zea mays L.) varieties to salt stress: Changes on polyphenols composition of foliage and oxidative damages Ind. Crops Prod. 30 144 151

    • Search Google Scholar
    • Export Citation

  • Knaflewski, M., Golinski, P., Kostecki, M., Waskiewicz, A. & Weber, Z. 2008 Mycotoxins and mycotoxin-producing fungi occurring in asparagus spears Acta Hort. 776 183 189

    • Search Google Scholar
    • Export Citation

  • Lake, R.J., Falloon, P.G. & Cook, D.W.M. 1993 Replant problem and chemical components of asparagus roots N. Z. J. Crop Hort. Sci. 21 53 58

  • Marschner, H. & Dell, B. 1994 Nutrient uptake in mycorrhizal symbiosis Plant Soil 159 89 102

  • Matsubara, Y., Hasegawa, N. & Ohba, N. 2003 Relation between fiber and pactic substance in root tissue and tolerance to fusarium root rot in asparagus plants infected with arbuscular mycorrhizal fungus J. Jpn. Soc. Hort. Sci. 72 275 280

    • Search Google Scholar
    • Export Citation

  • Miller, H.G., Ikawa, M. & Peirce, L.C. 1991 Caffeic acid identified as an inhibitory compound in asparagus root filtrate HortScience 26 1525 1527

  • Moghaddam, B., Charles, M.T., Carisse, O. & Khanizadeh, S. 2006 Superoxide dismutase responses of strawberry cultivars to infection by Mycosphaerrella fragariae J. Plant Physiol. 163 147 153

    • Search Google Scholar
    • Export Citation

  • Nahiyan, A.S.M., Boyer, L.R., Jeffries, P. & Matsubara, Y. 2011 PCR-SSCP analysis of fusarium diversity in asparagus decline in Japan Eur. J. Plant Pathol. 130 197 203

    • Search Google Scholar
    • Export Citation

  • Norman, J.R., Atkinson, D. & Hooker, J.E. 1996 Arbuscular mycorrhizal fungal-induced alteration to root architecture in strawberry and induced resistance to the root pathogen Phytophthora fragariae Plant Soil 185 191 198

    • Search Google Scholar
    • Export Citation

  • Ozgonen, H. & Erkilic, A. 2007 Growth enhancement and Phytophthora blight (Phytophthora capsici Leonian) control by arbuscular mycorrhizal fungal inoculation in pepper Crop Prot. 26 1682 1688

    • Search Google Scholar
    • Export Citation

  • Phillips, J.M. & Hayman, D.S. 1970 Improved procedures for clearing roots and staining parasitic and vesicular–arbuscular mycorrhizal fungi for rapid assessment of infection Trans. Br. Mycol. Soc. 55 158 163

    • Search Google Scholar
    • Export Citation

  • Pontaroli, A.C. & Camadro, E.L. 2001 Increasing resistance to fusarium crown and root rot in asparagus by gametophyte selection Euphytica 122 343 350

    • Search Google Scholar
    • Export Citation

  • Pozo, M.J., Cordier, C., Gaudot, E.D., Barea, J.M. & Aguilar, C.A. 2002 Localized versus systemic effect of arbuscular mycorrhizal fungi on defence responses to Phytophthora infection in tomato plants J. Expt. Bot. 53 525 534

    • Search Google Scholar
    • Export Citation

  • Reid, T.C., Hausbeck, M.K. & Kizilkaya, K. 2002 Use of fungicides and biological controls in the suppression of fusarium crown and root rot of asparagus under green house and growth chamber conditions Plant Dis. 86 493 498

    • Search Google Scholar
    • Export Citation

  • Richter, J., Baltruschat, H., Kabrodt, K. & Schellenberg, I. 2011 Impact of arbuscular mycorrhiza on the St. John's wort (Hypericum perforatum) wilt disease induced Colletotricuhum cf. gloeosporioides J. Plant Dis. Prot. 118 109 118

    • Search Google Scholar
    • Export Citation

  • Roe, J.H., Mary, B.M., Oesterking, M.J. & Charlotle, M.D. 1948 The determination of diketo-L-gluconic acid, dehydro-L-ascorbic acid, and L-ascorbic acid in the same tissues by 2,4-dinitrophenyl hydrazine method Biol. Chem. 174 201 208

    • Search Google Scholar
    • Export Citation

  • Sahoo, M.R., Dasgupta, A.M., Paresh, A., Kole, C., Jayant, A., Bhat, S. & Mukherjee, A. 2007 Antioxidative enzymes and isozymes analysis of taro genotypes and their implications in Phytophthora blight disease resistance Mycopathologia 163 241 248

    • Search Google Scholar
    • Export Citation

  • Salzer, P., Corbiere, H. & Boller, T. 1999 Hydrogen peroxidase accumulation in Medicago truncatula roots colonized by the arbuscular mycorrhiza-forming fungus Glomus intraradices Planta 208 319 325

    • Search Google Scholar
    • Export Citation

  • Sutton, J.C. 1973 Development of vesicular–arbuscular mycorrhizae in crop plants Can. J. Bot. 51 2487 2493

  • Vanitha, S.C., Niranjana, S.R. & Umesha, S. 2009 Role of phenylalanine ammonia lyase and polyphenol oxidase in host resistance to bacterial wilt of tomato J. Phytopathol. 157 552 557

    • Search Google Scholar
    • Export Citation

  • Volpin, H., Phillips, D.A., Okon, Y. & Kapulnik, Y. 1995 Suppression of an isoflavonoid phytoalexin defense response on mycorrhizal alfalfa roots Plant Physiol. 108 1449 1454

    • Search Google Scholar
    • Export Citation

  • Wong, J.Y. & Jeffries, P. 2006 Diversity of pathogenic fusarium populations associated with asparagus roots in decline soils in Spain and the UK Plant Pathol. 55 331 342

    • Search Google Scholar
    • Export Citation

  • Wu, Q., Zou, Y. & Xia, R. 2006 Effect of water stress and arbuscular mycorrhizal fungi on reactive oxygen metabolism and antioxidant production by citrus (Citrus tangerine) roots Eur. J. Soil Biol. 42 166 172

    • Search Google Scholar
    • Export Citation

  • Yergeau, E., Vujanovic, V. & St-Arnaud, M. 2006 Changes in communities of fusarium and arbuscular mycorrhizal as related to different asparagus cultural factors Microb. Ecol. 52 104 113

    • Search Google Scholar
    • Export Citation

  • Yong, C.C. 1984 Autointoxication in root exudates of Asparagus officinalis L Plant Soil 82 247 253

  • Zhu, X., Song, F. & Xu, H. 2010 Influence of arbuscular mycorrhiza on lipid peroxidation and antioxidative enzyme activity of maize plants under temperature stress Mycorrhiza 20 325 332

    • Search Google Scholar
    • Export Citation
Abu Shamim Mohammad NahiyanThe United Graduate School of Agricultural Science, Gifu University, 1-1 Yanagido, Gifu 501-1193, Japan

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Yoh-ichi MatsubaraFaculty of Applied Biological Sciences, Gifu University, 1-1 Yanagido, Gifu 501-1193, Japan

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Contributor Notes

This study was supported by Grants-in-Aid for Scientific Research (No. 21580029), Japan Society for the Promotion of Science (JSPS).

To whom reprint requests should be addressed; e-mail ymatsu@gifu-u.ac.jp.

Received:
27 Dec 2011
|
Accepted:
06 Feb 2012
|
Published-print:
01 Mar 2012
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