Abstract
Allelochemical compounds released by plants to signal their presence and needs interact in soils with very important macromolecules, such as humic acids (HAs), which are able to modulate the ultimate effects on target organisms. Most of the available studies on plants and microorganisms report the effects of allelochemicals or those of humic fractions, separately. In this study, we investigated the combined activity of these two types of compounds on the soil-resident fungus Sclerotinia sclerotiorum. Thus, ferulic acid (FA), caffeic acid (CA), benzoic acid (BA), salicylic acid (SA), gallic acid (GA) and phthalic acid (PA), exogenously applied to the fungal growth medium, were tested both alone and in combination with a soil HA (SHA) and a compost HA (CHA). The two HAs were also tested alone on the fungus. When the allelochemicals were applied alone, only FA, BA and SA evidenced a significant inhibition of mycelial growth, whereas FA, BA and CA increased the number of sclerotia formed. The two HAs alone reduced the early growth of the fungus and markedly stimulated sclerotia formation. A significant attenuation or, in some cases, suppression of the allelochemical effect on mycelial growth was caused by the coexistence in the medium of the allelochemical and each HA, especially CHA. Moreover, in general, the combinations of HA-allelochemical significantly stimulated sclerotia formation, with respect to the sole allelochemical, but decreased it with respect to HA alone. Thus, investigations on the response of fungi to plant-released allelochemicals should not exclude interactive aspects of these compounds with ubiquitous coexisting humic macromolecules.
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References
Chen Y, Aviad T (1990) Effects of humic substances on plant growth. In: MacCarthy P, Clapp CE, Malcolm RL, Bloom PR (eds) Humic substances in soil and crop sciences: selected readings. American Society of Agronomy, Madison, pp 161–186
Christias C, Lockwood JL (1973) Conversion of mycelial constituents in four sclerotium-forming fungi in nutrient deprived conditions. Phytopathology 63:602–605
Chung IM, Ahn JK, Jun SJ (2001) Identification of allelopathic compounds from rice (Oryza sativa L.) straw and their biological activity. Can J Plant Sci 81:815–819
Forchetti G, Masciarelli O, Izaguirre MJ, Alemano S, Alvarez D, Abdala G (2010) Endophytic bacteria improve seedling growth of sunflower under water stress, produce salicylic acid, and inhibit growth of pathogenic fungi. Curr Microbiol 61:485–493
Hao WY, Ren LX, Ran W, Shen QR (2010) Allelopathic effects of root exudates from watermelon and rice plants on Fusarium oxysporum f.sp. niveum. Plant Soil 336:485–497
Harborne JB (1980) Plant Phenolics. In: Bell EA, Charlwood BW (eds) Secondary plant products. Enciclopedia of Plant Physiology, New Series, Vol. 8. Springer-Verlag, Berlin, pp 329–402
Litterick AM, Harrier L, Wallace P, Watson CA, Wood M (2004) The role of uncomposted materials, composts, manures, and compost extracts in reducing pest and disease incidence and severity in sustainable temperate agricultural and horticultural crop production—a review. Crit Rev Plant Sci 23:453–479
Loffredo E, Senesi N (2009) In vitro and in vivo assessment of the potential of compost and its humic acid fraction to protect ornamental plants from soil-borne pathogenic fungi. Sci Hortic 122:432–439
Loffredo E, Monaci L, Senesi N (2005) Humic substances can modulate the allelopathic potential of caffeic, ferulic, and salicylic acids for seedlings of lettuce (Lactuca sativa L.) and tomato (Lycopersicon esculentum Mill.). J Agric Food Chem 53:9424–9430
Loffredo E, Berloco M, Casulli F, Senesi N (2007) In vitro assessment of the inhibition of humic substances on the growth of two strains of Fusarium oxysporum. Biol Fert Soils 43:759–769
Loffredo E, Berloco M, Senesi N (2008) The role of humic fractions from soil and compost in controlling the growth in vitro of phytopathogenic and antagonistic soil-borne fungi. Ecotoxicol Environ Saf 69:350–357
Loffredo E, Traversa A, Gattullo CE (2012) Benefits from compost use in the preparation of growing substrates for plants in container: inhibition of Sclerotinia sclerotiorum and protection of Philodendron. Fresenius Environ Bull 21:2208–2214
Makoi JHJR, Ndakidemi PA (2012) Allelopathy as protectant, defence and growth stimulants in legume cereal mixed culture systems. N Z J Crop Hortic 40:161–186
Margherita E, Brunetti G, Garcia C, Cavalcante F, Fiore S, Senesi N (2006) Humic substances and clay minerals in organically-amended semiarid soils. Soil Sci 171:322–333
Moliszewska E, Pisarek I (1996) Influence of humic substances on the growth of two phytopathogenic soil fungi. Environ Int 22:579–584
Mouhamadou B, Puissant J, Personeni E, Desclos-Theveniau M, Kastl EM, Schloter M, Zinger L, Roy J, Geremia RA, Lavorel S (2013) Effects of two grass species on the composition of soil fungal communities. Biol Fertil Soils 49:1131–1139
Pascual JA, Garcia C, Hernandez T (1999) Comparison of fresh and composted organic waste in their efficacy for the improvement of arid soil quality. Biores Technol 68:255–264
Pascual JA, Garcia C, Hernandez T, Lerma S, Lynch JM (2002) Effectiveness of municipal waste compost and its humic fraction in suppressing Pythium ultimum. Microb Ecol 44:59–68
Ponts N, Pinson-Gadais L, Boutigny AL, Barreau C, Richard-Forget F (2011) Cinnamic-derived acids significantly affect Fusarium graminearum growth and in vitro synthesis of type B Trichothecenes. Phytopathology 101:929–934
Pramanik MHR, Nagai M, Asao T, Matsui Y (2000) Effects of temperature and photoperiod on phytotoxic root exudates of cucumber (Cucumis sativus) in hydroponic culture. J Chem Ecol 26:1953–1967
Provenzano MR, Ouatmane A, Hafidi M, Senesi N (2000) Differential scanning calorimetric analysis of composted materials from different sources. J Therm Anal Calorim 61:607–614
Purdy LH (1979) Sclerotinia sclerotiorum: history, diseases and symptomology, host range, geographic distribution and impact. Phytopathology 69:875–880
Qi PF, Johnston A, Balcerzak M, Rocheleau H, Harris LJ, Long XY, Wei YM, Zheng YL, Ouellet T (2012) Effect of salicylic acid on Fusarium graminearum, the major causal agent of fusarium head blight in wheat. Fungal Biol 116:413–426
Ravn H, Andary C, Kovács G, Mǿlgaard P (1989) Caffeic acid esters as in vitro inhibitors of plant pathogenic bacteria and fungi. Biochem Syst Ecol 17:175–184
Rice EL (1984) Allelopathy, 2nd edn. Academic Press, Orlando
Schnitzer M (1982) Organic matter characterization. In: Page BL, Miller RH, Keeney DR (eds) Methods of soil analysis, Part 2, Chemical and microbiological properties, 2nd edn Agronomy Monograph No. 9. Soil Science Society of America, Madison, pp 581–594
Senesi N, Loffredo E (1994) Influence of soil humic substances and herbicides on the growth of pea (Pisum sativum L.) in nutrient solution. J Plant Nutr 17:493–500
Senesi N, Loffredo E (2001) Soil humic substances. In: Hofrichter M, Steinbüchel A (eds) Lignin, humic substances and coal. Wiley-VCH, Weinheim, pp 247–299
Smidt E, Lechner P (2005) Study on the degradation and stabilization of organic matter in waste by means of thermal analyses. Thermochim Acta 438:22–28
Souto C, Pellisier F, Chiapusio G (2000) Allelopathic effects of humus phenolics on growth and respiration of mycorrhizal fungi. J Chem Ecol 26:2015–2023
Srivastava P, Andersen PC, Marois JJ, Wright DL, Srivastava M, Harmon PF (2013) Effect of phenolic compounds on growth and ligninolytic enzyme production in Botryosphaeria isolates. Crop Prot 43:146–156
Traversa A, Molinari S, Loffredo E (2012) Quantitative aspects of the interaction between chemical activators of systemic acquired resistance in plants and humic acids. Agrochimica LVI:112–119
Vaughan D, Malcolm RE (1985) Influence of humic substances on growth and physiological processes. In: Vaughan D, Malcolm RE (eds) Soil Organic Matter and Biological Activity. Nijhoff-Junk Publisher, Dordrecht, pp 37–75
Vaughan D, Malcolm RE, Ord B (1985) Influence of humic substances on biochemical processes in plants. In: Vaughan D, Malcolm RE (eds) Soil Organic Matter and Biological Activity. Nijhoff-Junk Publisher, Dordrecht, pp 77–108
Vinken R, Schäffer A, Ji R (2005) Abiotic association of soil-borne monomeric phenols with humic acids. Org Geochem 36:583–593
Vyvyan JR (2002) Allelochemicals as leads for new herbicides and agrochemicals. Tetrahedron 58:1631–1646
Wang Z, Tan X, Zhang Z, Gu S, Li G, Shi H (2012) Defense to Sclerotinia sclerotiorum in oilseed rape is associated with the sequential activations of salicylic acid signaling and jasmonic acid signaling. Plant Sci 184:75–82
Wu HS, Raza W, Fan JQ, Sun YG, Bao W, Liu D-Y, Huang Q-W, Mao Z-S, Shen Q-R, Miao W-G (2008) Antibiotic effect of exogenously applied salicylic acid on in vitro soilborne pathogen. Fusarium oxysporum f. sp. Niveum. Chemosphere 74:45–50
Wu HS, Liu DY, Ling N, Bao W, Ying RR, Shen QR (2009) Influence of Root Exudates of Watermelon on Fusarium oxysporum f. sp niveum. Soil Sci Soc Am J 73:1150–1156
Yu JQ, Matsui Y (1993) Extraction and identification of phytotoxic substances accumulated in nutrient solution for the hydroponic culture of tomato. Soil Sci Plant Nutr 39:691–700
Yu JQ, Ye SF, Zhang MF, Hu WH (2003) Effects of root exudates and aqueous root extracts of cucumber (Cucumis sativus) and allelochemicals, on photosynthesis and antioxidant enzymes in cucumber. Biochem Syst Ecol 31:129–139
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This work was funded by the University of Bari, Italy.
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Loffredo, E., Traversa, A. Soil and compost humic fractions regulate the response of Sclerotinia sclerotiorum to exogenously added allelochemical compounds. Biol Fertil Soils 50, 1281–1290 (2014). https://doi.org/10.1007/s00374-014-0944-5
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DOI: https://doi.org/10.1007/s00374-014-0944-5