Abstract
Nowadays, crop production is at risk due to global warming, especially in Mediterranean areas where the increase of air temperature and/or reduction of precipitation is relevant. Climate changes that are occurring can severely prejudice plant defensive mechanisms during host-pathogen interactions by modifying growth and physiology of the host plant. In particular, viral diseases cause serious economic losses destroying crops and reducing agronomic productivity, and, in some cases such as tomato crops, they become the limiting factor production of both open field and under greenhouse cultivation systems. This is because plant viruses are obligate parasites and require living tissue for their multiplication and spread. Therefore, they are able to interfere with plant metabolism and compete for host plant resources, so determining a decrease of plant growth and productivity. Severe outbreaks of Cucumber mosaic virus (CMV) and other viruses caused disruption of tomato plants in the Mediterranean region and in Southern Italy since the 1970s. In such a scenario, it is necessary to introduce new strategies for controlling plant pathogens and parasites in order to help maintain ecosystems and to boost sustainable agriculture. The aim of this work is to give an up-to-date overview on the recent breakthroughs in the use of microorganisms on plants for improving crop yields, quality and plant tolerance against pathogens. In particular, here we report a case study regarding an innovative strategy to control a viral disease (CMV) in tomato, based on the use of rhizosphere microorganism (Trichoderma harzianum, strain T-22) as an antagonist biocontrol agent (BCA).
You have full access to this open access chapter, Download chapter PDF
Similar content being viewed by others
Keywords
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.
1 Introduction
In the Mediterranean basin, horticultural crops have a great economic relevance. If we think of the Mediterranean diet, which is considered as one of the healthiest amongst world cuisines, above all since November 2010, when it was inscribed on the representative list of the intangible cultural heritage of humanity of UNESCO, tomato (Solanum lycopersicum) is certainly the vegetable most widely consumed. In Italy, in particular in the South, tomato is not only the first vegetable employed for fresh consumption, but it also represents the principal ingredient of many dishes, and it is above all used cooked to prepare sauces. The importance of tomato consists in its nutraceutical properties, due to the presence of an antioxidant substances mixture, such as lycopene, ascorbic acid, phenolic compounds, flavonoids and vitamin E. For this reason, nowadays tomato is cultivated both in open field and under greenhouse conditions in order to be always available for both fresh consumption and industrial processing.
Unfortunately, crop production is at risk due to global warming, especially in areas where the increase of air temperature and/or reduction of precipitation is relevant. In addition, climate changes can prejudice plant defensive mechanisms and increase the risk of illness, through growth and physiology alteration of the host plant and also by modifying host-pathogen interactions. In particular, viral diseases cause serious economic losses destroying crops and reducing agronomic productivity. In many Mediterranean coastal areas, several viral infections have become the limiting factor in the tomato production of both open field and under greenhouse cultivation systems. For example, in Italy, Spain, Portugal and Greece, the cultivations are at risk due to Tomato spotted wilt virus (TSWV) infections (Pappu et al. 2009). Another important example is Tomato yellow leaf curl virus (TYLCV), which caused serious economic problems in the eastern Mediterranean basin in the 1970s, and it is still now a threat (Lapidot et al. 2014). In late summer 2000, more than 30 ha of Greek tomato greenhouses (Avgelis et al. 2001) were affected and the disease incidence by TYLCV, in 2001, in most cases, was 80–90 %, or even 100 % (Dovas et al. 2002). In the same the 1970s, Cucumber mosaic virus (CMV) severe outbreaks caused disruption and death of tomato plants in the Mediterranean region (Gallitelli et al. 1991). Tomato necrosis epidemic occurred in the eastern coastal area of Spain in the late 1980s and early 1990s (GarcÃa-Arenal et al. 2000). During this period, in Southern Italy (Puglia, Basilicata and Campania regions), some high-quality varieties of tomato, i.e. San Marzano, were severely affected by the strong CMV epidemic (Valanzuolo et al. 1999).
Indeed, plant viruses are obligate parasites because they require living tissue for their multiplication and spread, interfering with plant metabolism and/or competing for host plant resources, and all this is translated as decreasing of plant growth and productivity. The ability of viruses to significantly interfere with physiological processes of plants is closely related to a range of symptoms caused by an abnormal growth, as stunting, galls, enations and tissue distortions. In particular, CMV is the plant virus with the largest host range of all RNA viruses; therefore, its spreading on crop plants may cause serious economic damages. It infects more than 1,200 plant species in 100 families (Edwardson and Christie 1991) and has been widely studied because it represents an interesting model from a physico-chemical point of view, as it causes a wide range of symptoms, especially yellow mottling, distortion and plant stunting (Nuzzaci et al. 2009; Whitham et al. 2006).
In such a scenario, the present work contributed to elucidate the importance in the use of sustainable agricultural practices in disease defence. In addition, here we report a case study regarding an innovative strategy to control a viral disease (CMV) in tomato cherry, based on the use of rhizosphere microorganism (Trichoderma harzianum, strain T-22) as an antagonist biocontrol agent (BCA).
2 Sustainable Agricultural Practices in Disease Defence
During the last decade, the studies on alternative environmental friendly technologies have received a strong impulse and have proposed a wide range of options, including agronomical, physical and biological control means. Recently, it was growing the idea that the plants have enormous self-defence potentiality, and this would allow a natural disease control with positive effects on environmental and human health safeguard (Sofo et al. 2014).
Many factors, both biotic (pathogens, insects, nematodes) and abiotic (e.g. wounds, pollutants, thermal, water and nutritional imbalances, environmental contaminants) are causes of plant stress. Plants can react to these stressors through a series of constitutive and/or inductive mechanisms which result in the elimination or the limitation of the negative effects induced by the adverse factors. The studies on these biochemical mechanisms allow to individuate control strategies against plant pathogens and parasites, based on the exploitation of the natural mechanisms of plant defence. One of this type of mechanism, already documented by Ross (1961), is known as systemic acquired resistance (SAR). It is effective against a wide range of pathogens and its action differs in relation to the inducer agent. Actually, the SAR represents a valid opportunity in plant natural protection, and, therefore, the research activities are oriented to the use of biocontrol agents as inducers of SAR in agronomically important species against some of their most severe pathogens (Sofo et al. 2014). In fact, research data accumulated in the past few years have produced a completely novel understanding of the way by which bacteria and fungi interact not only with other microbes but especially with plants and soil components. This has opened an avenue of new applications, both in agriculture and biotechnology, that exploit the ability of some microorganisms to change plant metabolism and resistance to biotic and abiotic stresses (Woo et al. 2006). Generally, as a response to diseases, plants may compensate with a broad range of cellular processes by up- or down-regulating certain genes; changing the levels of substances implicated in plant defence pathway; increasing the levels of reactive oxygen species (ROS); activating specific transcription factors, defence-regulated genes and heat shock proteins; and enhancing the transport of macromolecules, enzymes and phytohormones involved in defence signalling pathways [e.g. salicylic acid (SA); jasmonic acid (JA); ethylene (ET); auxins, such as indole-3-acetic acid (IAA); cytokinins (CKs); abscisic acid (ABA); gibberellic acid (GA)] (Bari and Jones 2009; Vitti et al. 2013). On the other hand, all physiological process changes of plants as response to pathogens negatively affect the crops’ yield with a loss of billions of euros each year not only for direct productivity decrease but also for the consequent managing of the pests. In addition, the use of traditional methods such as chemical pesticides, herbicides or fertilizer is not an eco-friendly approach, and their continued employment resulted on contamination of water, atmosphere pollution and the release of harmful residues in soils (Naher et al. 2014).
A safe method to reduce plant disease incidence without collateral damages to the environment and to human health induced by synthetic chemicals is the biological control (Tucci et al. 2011). In such a way, it is possible to manage pests by means of a sustainable approach where biocontrol agents can be used either alone or with other chemicals in an integrated practice of disease defence, according to European legislation Directives establish. The use of microorganisms for controlling plant pathogens has been shown to be very efficacious for some fungi of the genus Glomus, Streptomyces, Trichoderma and some species of bacteria (e.g., Agrobacterium radiobacter and Bacillus subtilis). In particular, some of these fungi interact with other fungi in a mechanism called mycoparasitism, wherein one fungus directly kills and obtains nutrients from other fungi. Mycoparasitism is one of the most important biocontrol mechanisms of Trichoderma spp. (Mukherjee 2011), which is considered the most versatile amongst all biocontrol agents and, for this reason, has long been used for managing plant pathogenic fungi (Vinale et al. 2009; Weindling 1934; Wells 1988). It was demonstrated that some fungal diseases can be also prevented when plants are treated with the conidial suspensions of Trichoderma spp. (Harman et al. 2004a). Fungi belonging to the genus Trichoderma are used as biocontrol agents to antagonize plant pathogens through a series of mechanisms including, in addition to mycoparasitism, competition for nutrients and space, fungistasis, antibiosis and/or modification of the rhizosphere (BenÃtez et al. 2004). Trichoderma spp. are some of the most abundant fungi found in many soil types and are able to colonise plant roots and plant debris (Harman et al. 2004a). They are agriculturally important also for their beneficial effects on plant growth and development and for their capability to induce plant defence responses against pathogens, damage provoked by insects and abiotic stress (Yedidia et al. 1999; Harman et al. 2004a; Woo and Lorito 2006). For this reason, more than 60Â % of all registered products used for plant disease control are Trichoderma-based and they are a major source of many biofungicides and biofertilizers (Verma et al. 2007; Kaewchai et al. 2009).
In particular, the strain T-22 of T. harzianum (here called T22) represents the active ingredient of registered products widely employed in plant disease control. It is known that T22, by working as a deterrent, protects the roots from the assault of pathogens fungi (e.g. Fusarium, Pythium, Rhizoctonia and Sclerotinia). Establishing itself in the rhizosphere, T22 can grow on the root system, along which it establishes a barrier against pathogens. The action of T22 is not to produce something toxic to the pathogen but to induce the plant to change its physiology and metabolism to ameliorate its resistance to that disease (Harman et al. 2008). It was demonstrated that T22 improves growth in maize plants, increasing root formation (size and area of main and secondary roots) and, at the same time, rising crop yields, drought tolerance and resistance to compacted soils (Harman 2000; Harman et al. 2004b). This improvement in growth was probably due to direct effects on plants because of a better solubilization of soil nutrients or by a direct enhancing plant uptake of nutrients linked to the presence of T22 in the agroecosystems (Yedidia et al. 2001). The beneficial effects of T22 application depend on the treated plant genotype, as recently demonstrated by Tucci et al. (2011) on tomato plants.
3 The Case Study of Tomato Cherry Protected by Trichoderma harzianumT-22 Against CMV
In the context of plant defence by biotic stresses, understanding biochemical and molecular mechanisms deriving from the host-pathogen-Trichoderma interaction is without doubt essential for investigating the dynamics of infectious processes. This knowledge can be very useful for the development of new approaches for controlling phytopathogens, particularly viruses, against which chemical treatments have no effect (Vitti et al. 2015b). Thanks to recent studies, new strategies have been based on the use of peptaibols, a class of linear peptides biosynthesized by many species of Trichoderma (Daniel and Filho 2007). For example, it was demonstrated that trichokonins, antimicrobial peptaibols isolated from Trichoderma pseudokoningii SMF2, can induce tobacco systemic resistance against Tobacco mosaic virus (TMV) via the activation of multiple plant defence pathways based on an elicitor-like cellular response: production enhanced in tobacco plants of superoxide anion radical and peroxide; production enhanced of enzymes involved tobacco resistance, as peroxidase (POD); up-regulation of antioxidative enzyme genes, known to be associated with the ROS intermediate-mediated signalling pathway; and of SA-, ET- and JA-mediated defence pathway marker genes (Luo et al. 2010). This finding implies the antiviral potential of peptaibols, supporting the hypothesis to using them as biocontrol antiviral agents. Therefore, Trichoderma spp., already used as BCAs against bacterial (Segarra et al. 2009) and fungal phytopathogens (Vinale et al. 2009; Akrami et al. 2011), it was hypothesized could be advantageously used also in the control of virus diseases. Trichoderma spp. and/or their secondary metabolites were able to induce resistance mechanisms, similar to the hypersensitive response (HR), SAR and induced systemic resistance (ISR) in plants (BenÃtez et al. 2004; Harman et al. 2004a), regulated through a complex network of signal transduction pathways involving not only the above-mentioned molecules, such as ROS, SA, JA and ET but also the crosstalk between them (Kunkel and Brooks 2002) and the so-called pathogenesis-related (PR) genes, a series of marker genes for the activation of SA, JA and ET signalling, involved in these defence transduction pathways (Bouchez et al. 2007). At this regard, Hermosa et al. (2012) assert that the expression of defence-related genes of the JA/ET and/or SA pathways may overlap just because of the dynamics in the Trichoderma-plant crosstalk.
To date, the effects of Trichoderma spp. in the induction of plant defence against CMV were poorly known. Only studies conducted by Elsharkawy et al. (2013) demonstrated that Arabidopsis plants were exploited against CMV by using Trichoderma asperellumSKT-1. In particular, when the researchers used barley grain inoculum, the fungus induced SAR, while ISR was elicited when T. asperellum was utilized as culture filtrate. On the other hand, the biochemical and molecular mechanism involved in this kind of three-way crosstalk between the plant, virus and antagonist agent has still to be well elucidated.
In such a scenario, our work represents the starting point to improve the knowledge on the possible underlying mechanisms involved in plant-pathogen-antagonist interactions and, at the same time, to develop an innovative strategy against CMV infection in tomato plants, based on the activity of a biocontrol agent (Vitti et al. 2015a).
Trichoderma harzianum strain T-22 (T22) was the antagonist microorganism used in this study. It was utilized as a granule formulation (Trianum G, Koppert, Berkel en Rodenrijs, the Netherlands). Cucumber mosaic virus strain Fny (CMV-Fny) was propagated in tobacco plants, purified as described by Lot et al. (1972), so that the purified CMV-Fny was used to mechanically inoculate tomato plants (Solanum lycopersicum var. cerasiforme).
As shown schematically in Fig. 1, tomato plants were treated with T22 and/or inoculated with CMV, according to the following six conditions: control plants untreated and healthy (PA); plants only treated with T22 (PB); plants only inoculated with CMV (PC); plants first treated with T22 and after 7 days inoculated with CMV (PD); plants simultaneously treated and inoculated with T22 and CMV (PE); and plants first inoculated with CMV and after 1 week treated with T22 (PF).
During the entire cycle of plant’s life, symptom observations were monitored. Fourteen days after CMV inoculation (that is when the plants were at 1 month of age) and when the plants were 5 months old, leaves were collected and used for the following analyses: histochemical staining of O2 − and H2O2 in leaf discs, in order to study the involvement of ROS and total RNA extraction from leaf tissues followed by reverse transcription polymerase chain reaction (RT-PCR) analysis, for the verification of the presence of CMV in tomato seedlings, or by real-time reverse transcription PCR (qRT-PCR), in order to analyse the transcript levels of the genes implicated in plant defence, such as genes encoding for antioxidant enzymes and for pathogenesis-related protein (Vitti et al. 2015a). In addition, here we report the yield evaluation for each experimental condition, determined since plants started to produce flowers and fruits (3 months of age) and until plants were 5 months old.
T22 showed the ability to control CMV infection on tomato cherry plants by modulating the viral symptoms during the entire life cycle of the plants and also by inhibiting the presence of CMV in 5-month-old plants. Furthermore, an involvement of ROS in plant defence against a viral disease when Trichoderma is applied was demonstrated. In fact, it can be hypothesized that the interaction between CMV and tomato plants results in an oxidative burst and hence elevated ROS production, which becomes toxic for the plants. Conversely, during the CMV-tomato-T22 interaction, ROS are implicated as secondary messengers of the host’s defence responses against the viral pathogen, mediated by the fungal biocontrol agent. In addition, an indication on the fact that a particular combination whereby plants first inoculated with CMV and then treated with T22 could guarantee the best control against CMV has been speculated. Finally, results obtained could also indicate an SAR-related response by the tomato plants against CMV attack, but further investigation is required to confirm these findings (Vitti et al. 2015a).
Tomato fruits were harvested from bottom branch of 3-month-old plants. As reported in Fig. 2, plants treated only with T22 (PB) showed the best size fruit and also the best root development, as expected. On the contrary, the control plants inoculated with CMV alone (PC) showed the smallest fruits, with delayed ripening, accompanied by the worst root development. Plants treated with T22 and inoculated with CMV (PD, PE and PF) were similar to the controls (PA), considering both size fruit and root development.
As clearly showed in Fig. 3, in terms of yield, considered as production of flowers and fruits in 3–5-month-old plants, those treated only with T22 (PB) showed the highest values, as expected. Conversely, plants inoculated with CMV alone (PC) not showed the lowest yield, as we expected. This is because the number of fruits was not low, but they resulted in an important reduction in size, as Fig. 2 shows, accompanied by chlorotic/necrotic spots when they were ripe, confirming the observations previously made by Vitti et al. (2015a). Instead, as it is possible to see in Fig. 3, plants treated with T22 and also inoculated with CMV, in particular in the case of co-inoculation/treatment (PE), showed an increase in yield respect to that inoculated with only CMV (PC), except for plants first treated with T22 and then inoculated with CMV (PD).
4 Conclusion
In conclusion, data produced in the case study here reported demonstrate that Trichoderma harzianumT-22 stimulates the induction of defence responses against CMV-Fny in Solanum lycopersicum var. cerasiforme, by the clear involvement of ROS, as well as an enhancement in yields and root development. Furthermore, the knowledge on the molecular and biochemical aspects of the plant-virus-biocontrol agent interactions, in combination with the dynamics of application, has been improved. In this way, a new system based on the use of T22 as a microbial antagonist could be made available for the protection of tomato against CMV disease, which can be also extended to other plant species. Furthermore, a routine utilization of T22 in the agricultural practices in disease defence could surely bring to a reduction of the use of fertilizers and fungicides in agricultural production, with consequent benefits for the environment. Today, more than ever, this is necessary to help maintain ecosystems and to develop sustainable agriculture.
References
Akrami M, Golzary H, Ahmadzadeh M (2011) Evaluation of different combinations of Trichoderma species for controlling Fusarium rot of lentil. Afr J Biotechnol 10:2653–2658
Avgelis AD, Roditakis N, Dovas CI et al (2001) First report of tomato yellow leaf curl virus on tomato crops in Greece. Plant Dis 85:678
Bari R, Jones JDG (2009) Role of plant hormones in plant defence responses. Plant Mol Biol 69:473–488
BenÃtez T, Rincon AM, Limon MC, Codon AC (2004) Biocontrol mechanisms of Trichoderma strains. Int Microbiol 7:249–260
Bouchez O, Huard C, Lorrain S et al (2007) Ethylene is one of the key elements for cell death and defense response control in the Arabidopsis lesion mimic mutant vad1. Plant Physiol 145:465–477
Daniel JFS, Filho ER (2007) Peptaibols of Trichoderma. Nat Prod Rep 24:1128–1141
Dovas CI, Katis NI, Avgelis AD (2002) Multiplex detection of Criniviruses associated with epidemics of a yellowing disease of tomato in Greece. Plant Dis 86:1345–1349
Edwardson JR, Christie RG (1991) Cucumoviruses. In: Edwardson JR, Christie RG (eds) CRC handbook of viruses infecting legumes. CRC, Boca Raton, FL, pp 293–319
Elsharkawy MM, Shimizu M, Takahashi H et al (2013) Induction of systemic resistance against cucumber mosaic virus in Arabidopsis thaliana by Trichoderma asperellum SKT-1. Plant Pathol J 29:193–200
Gallitelli D, Vovlas C, Martelli GP et al (1991) Satellite-mediated protection of tomato against cucumber mosaic virus: II. Field test under natural epidemic conditions in southern Italy. Plant Dis 75:93–95
GarcÃa-Arenal F, Escriu F, Areanda MA et al (2000) Molecular epidemiology of cucumber mosaic virus and its satellite RNA. Virus Res 71:1–8
Harman GE (2000) Myths and dogmas of biocontrol. Changes in perceptions derived from research on Trichoderma harzianum T22. Plant Dis 84:377–393
Harman GE, Howell CR, Viterbo A et al (2004a) Trichoderma species—opportunistic, avirulent plant symbionts. Nat Rev Microbiol 2:43–56
Harman GE, Petzoldt R, Comis A, Chen J (2004b) Interactions between Trichoderma harzianum strain T22 and maize inbred line Mo17 and effects of this interaction on diseases caused by Pythium ultimum and Colletotrichum graminicola. Phytopathology 94:147–153
Harman GE, Björkman T, Ondik K, Shoresh M (2008) Changing paradigms on the mode of action and uses of Trichoderma spp. for biocontrol. Outlooks Pest Manag 19:24–29
Hermosa R, Viterbo A, Chet I, Monte E (2012) Plant-beneficial effects of Trichoderma and of its genes. Microbiology 158:17–25
Kaewchai S, Soytong K, Hyde KD (2009) Mycofungicides and fungal biofertilizers. Fungal Diver 38:25–50
Kunkel BN, Brooks DM (2002) Cross talk between signaling pathways in pathogen defense. Curr Opin Plant Biol 5:325–331
Lapidot M, Legg JP, Wintermantel WM, Polston JE (2014) Management of whitefly-transmitted viruses in open-field production systems. In: Loebenstein G, Katis N (eds) Control of plant virus diseases: seed-propagated crops, vol 90, 1st edn. Elsevier/Academic Press, New York, pp 147–206
Lot H, Marrou J, Quiot JB, Esvan C (1972) Contribution à l’étude du virus de la mosaique du cocombre (CMV). I. Mèthode de purification rapide du virus. Ann Phytopathol 14:25–38
Luo Y, Zhang DD, Dong XW et al (2010) Antimicrobial peptaibols induce defense responses and systemic resistance in tobacco against tobacco mosaic virus. FEMS Microbiol Lett 313:120–126
Mukherjee PK (2011) Genomics of biological control—whole genome sequencing of two mycoparasitic Trichoderma spp. Curr Sci 101:268
Naher L, Yusuf UK, Ismail A, Hossain K (2014) Trichoderma spp.: a biocontrol agent for sustainable management of plant diseases. Pak J Bot 46:1489–1493
Nuzzaci M, Bochicchio I, De Stradis A et al (2009) Structural and biological properties of cucumber mosaic virus particles carrying hepatitis C virus-derived epitopes. J Virol Methods 155:118–121
Pappu HR, Jones RAC, Jain RK (2009) Global status of tospovirus epidemics in diverse cropping systems: successes achieved and challenges ahead. Virus Res 141:219–236
Ross AF (1961) Systemic acquired resistance induced by localized virus infections in plants. Virology 14:340–358
Segarra G, Van der Ent S, Trillas I, Pieterse CMJ (2009) MYB72, a node of convergence in induced systemic resistance triggered by a fungal and a bacterial beneficial microbe. Plant Biol 11:90–96
Sofo A, Nuzzaci M, Vitti A et al (2014) Control of biotic and abiotic stresses in cultivated plants by the use of biostimulant microorganisms. In: Ahmad P, Wani MR et al (eds) Improvement of crops in the era of climatic changes. Springer, New York, pp 107–117
Tucci M, Ruocco M, De Masi L et al (2011) The beneficial effect of Trichoderma spp. on tomato is modulated by the plant genotype. Mol Plant Pathol 12:341–354
Valanzuolo S, Monti SS, Colombo M, Cassani C (1999) Field release of transgenic virus tolerance tomatoes. In: Cresti M, Cai G, Moscatelli A (eds) Fertilization in higher plants—molecular and cytological aspects. Springer, Berlin, pp 405–412
Verma M, Brar SK, Tyagi RD et al (2007) Antagonistic fungi, Trichoderma spp.: panoply of biological control. Biochem Eng J 37:1–20
Vinale F, Flematti G, Sivasithamparam K et al (2009) Harzianic acid, an antifungal and plant growth promoting metabolite from Trichoderma harzianum. J Nat Prod 72:2032–2035
Vitti A, Nuzzaci M, Scopa A et al (2013) Auxin and cytokinin metabolism and root morphological modifications in Arabidopsis thaliana seedlings infected with cucumber mosaic virus (CMV) or exposed to cadmium. Int J Mol Sci 14:6889–6902
Vitti A, La Monaca E, Sofo A, Scopa A, Cuypers A, Nuzzaci M (2015a) Beneficial effects of Trichoderma harzianum T-22 in tomato seedlings infected by cucumber mosaic virus (CMV). BioControl 60(1):135–147
Vitti A, Nuzzaci M, Scopa A, Sofo A (2015b) Indirect and direct benefits of the use of Trichoderma harzianum strain T-22 in agronomic plants subjected to abiotic and biotic stresses. In: Chakraborty U, Chakraborty B (eds) Abiotic stresses in crop plants. CABI, Wallingford. ISBN 9781780643731
Weindling R (1934) Studies on lethal principle effective in the parasitic action of Trichoderma lignorum on Rhizoctonia solani and other soil fungi. Phytopathology 24:1153–1179
Wells DH (1988) Trichoderma as a biocontrol agent. In: Mukerji KG, Garg KL (eds) Biocontrol and plant diseases. CRC, Boca Raton, FL, pp 71–82
Whitham SA, Yang C, Goodin MM (2006) Global impact: elucidating plant responses to viral infection. Mol Plant Microbe Interact 19:1207–1215
Woo SL, Lorito M (2006) Exploiting the interactions between fungal antagonists, pathogens and the plant for biocontrol. In: Vurro M, Gressel J (eds) Novel biotechnologies for biocontrol agent enhancement and management. Springer, Amsterdam, pp 107–130
Woo SL, Scala F, Ruocco M, Lorito M (2006) The molecular biology of the interactions between Trichoderma spp., phytopathogenic fungi, and plants. Phytopathology 96:181–185
Yedidia I, Benhamou N, Chet I (1999) Induction of defense responses in cucumber plants (Cucumis sativus L.) by the biocontrol agent Trichoderma harzianum. Appl Environ Microbiol 65:1061–1070
Yedidia I, Srivastva AK, Kapulnik Y, Chet I (2001) Effect of Trichoderma harzianum on microelement concentrations and increased growth of cucumber plants. Plant Soil 235:235–242
Acknowledgments
This work was supported by a grant from University of Basilicata, Potenza, Italy.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Open Access This chapter is distributed under the terms of the Creative Commons Attribution Noncommercial License, which permits any noncommercial use, distribution, and reproduction in any medium, provided the original author(s) and source are credited.
Copyright information
© 2015 The Author(s)
About this chapter
Cite this chapter
Vitti, A., Sofo, A., Scopa, A., Nuzzaci, M. (2015). Sustainable Agricultural Practices in Disease Defence of Traditional Crops in Southern Italy: The Case Study of Tomato Cherry Protected by Trichoderma harzianum T-22 Against Cucumber Mosaic Virus (CMV). In: Vastola, A. (eds) The Sustainability of Agro-Food and Natural Resource Systems in the Mediterranean Basin. Springer, Cham. https://doi.org/10.1007/978-3-319-16357-4_9
Download citation
DOI: https://doi.org/10.1007/978-3-319-16357-4_9
Publisher Name: Springer, Cham
Print ISBN: 978-3-319-16356-7
Online ISBN: 978-3-319-16357-4
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)