INDUCED GENETIC RESISTANCE IN CULTIVATED PLANTS
Nathália Leal Carvalho
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SUMMARY
Resistance induction involves the activation of latent defense mechanisms in plants in response to treatment with biotic or abiotic agents. The plants have an inducible defense system, in order to save energy. Thus, resistance induced under natural conditions will represent a cost only in the presence of the pathogen. However, plants that invest their resources to defend themselves in the absence of pathogens will bear costs that will reflect on productivity, since the metabolic changes that lead to resistance have an associated adaptive cost, which can weigh more than the benefit. The negative effect on productivity occurs mainly where chemical inducers are used repeatedly or at higher doses. Thus, in some cases we may be walking on a narrow line between cost and benefit, where the cure can be bad as much as the disease itself.
Keywords: tolerance, pathogen selectivity, disease.
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ABSTRACT
Induction of resistance involves the activation of latent existing defense mechanisms in plants in response to treatment with biotic or abiotic agents. The plants have inducible defense system, in order to save energy. Thus, induced resistance under natural conditions would cost only in the presence of the pathogen. However, plants that invest their resources to defend themselves in the absence of pathogens to bear costs that reflect the productivity, since the metabolic changes that lead to adaptive resistance present cost associated, which can weigh more than the benefit. The negative effect on productivity is mainly chemical inducers which are used repeatedly or in higher doses. Thus, in some cases can be walking on a narrow line between cost and benefit, where the cure can be as bad as the disease itself.
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INTRODUCTION
Any plant population in which constituent individuals have a variation genetically inherited from tolerance to a certain measure of control, applied repeatedly and regularly, will undergo changes in its population structure over time, so that this population can go from susceptible to resistant. Such a change is a consequence of natural selection, as proposed by Darwin in 1859. Infectious diseases in plants have accompanied man since the beginning of agriculture, having increased their importance from cultivation in monoculture. Currently, due to the population increase and the growing need for food, despite disease control methodologies, new cultivation technologies and the increase in the cultivated area with plants of food and industrial interest should reflect on phytopathological problems (Carvalho & Barcellos, 2012), possibly aggravating existing ones and causing the appearance of new ones (Vanderplank, 1968). In addition to the traditional chemical control of diseases, it is faced with the emergence of isolates of pathogens resistant to the chemical substances used, forcing man to a continuous search for new chemical agents. Finally, due to the increasing awareness of the population regarding the conservation of the environment, the unbridled use of agrochemicals is beginning to be rethought and the search for new measures to protect plants against diseases begins to gain more and more space (Camargo & Bergamin Filho, 1995).
In this context of plant protection, we can insert the induction of resistance that can be visualized as naturally occurring during host-pathogen interactions, requiring only the interference of man for the possible use on a commercial scale of it (Stadnik, 2000). Induced resistance would involve the activation of latent resistance mechanisms in plants in response to previous treatment with biotic agents (e.g. viable or inactivated microorganisms) or abiotic agents (e.g. acetylsalicylic acid). This response, which may include, for example, the accumulation of phytoalexins (compounds toxic to fungi and bacteria), protects the plant against subsequent infections with pathogens. These resistance mechanisms are genetically determined and their effectiveness is shown to be dependent on their expression at the right time, adequate magnitude and in a logical sequence, after contact of the pathogen with the host (Stadnik, 2000, Camargo & Bergamin Filho, 1995, Vanderplank, 1968).
The protection of plants through the induction of resistance can occur in greenhouse and field conditions, in addition to exhibiting advantages such as: effectiveness against viruses, bacteria, fungi and nematodes; stability due to the action of different resistance mechanisms; systemic, persistent and natural character of protection; transmission by grafting; metabolic energy saving - the plant remains in a "warning state" and the resistance mechanisms are activated in the presence of the pathogen; presence of the genetic potential for resistance in all susceptible plants (Vanderplank, 1968). Among the different advantages mentioned, thinking about the potential use of the phenomenon in disease control, we must highlight the systemic character of protection, where the treatment of the plant with microorganisms or chemical compounds, asystemically activate the defense mechanisms of the plant (Stadnik, 2000). The occurrence of induced systemic resistance, both in monocotyledons and dicotyledons, is illustrated in table 1 proposed by Rompf, 1999.
Since the phenomenon of induced systemic resistance was conclusively demonstrated in the 1960s and suggested a potential role for it in plant protection, the release of BHT represents a significant advance for new strategies to control plant diseases. It is quite likely that resistance induced against diseases through chemical activators, such as BHT or other means, will become an important component of disease management programs, particularly in cases where current control methods are ineffective, as well as in the control of post-harvest diseases involving fruit and vegetables (Rezende et al., 2005). Obviously, one of the results of this new technology should be the decrease in the use of traditional pesticides, which meets the global concern regarding the preservation of the environment and reduction of pollution (Agrios, 2007).
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INDUCED GENETIC RESISTANCE IN CULTIVATED PLANTS
Disease control becomes more effective, economical and ecological, when various tactics are used in an integrated way. Among these, the use of genetic resistance represents one of the most efficient control methods, easily accessible to producers and economical, significantly reducing the losses with the disease and production costs (Rezende et al., 2005). In addition, plant genetic resistance is the main form of control of vascular wilts, rust, coal, powdery mildew and viruses, allowing production at acceptable levels, without the application of other control methods (Agrios, 2007; Camargo & Bergamin Filho, 1995).
Currently, world agricultural production is aimed at greater specialization in crops, monoculture and globalization of production and market. These factors promote, respectively, greater susceptibility to diseases, variation in pathogen populations and consequent loss of resistance, and also dissemination of causal agents, which are not restricted by quarantine services (Rezende et al., 2005). In this production system, massive amounts of fungicides are used to control diseases, interfering with the environment and causing significant damage to the health of consumer populations. Thus, the use of alternative methods of controlling plant diseases is a great challenge for modern agriculture, highlighting among others the use of genetic resistance of plants to pathogens (Tuzun & Kuc, 1991).
To overcome disease problems, we mainly adopted the application of fungicides (Rezende et al., 2005). However, the intensive use of these fungicides can cause resistance of the pathogen to them, as well as affect the human health of both the consumer and that of the professionals involved in production processes and cause negative effects on the environment (Tuzun & Kuc, 1991). One of the alternatives to chemical control, the use of genetic resistance has been one of the most efficient practices within integrated management (Rezende et al., 2005). However, a breeding program is costly and time-consuming, not always responding quickly to the need for agriculture (Cavalcanti et al., 2005). However, an easy-to-manage and low-cost alternative is induced resistance, which consists of increasing the level of plant resistance through the use of external agents (inducers), without any change in the plant genome (Stadnik, 2000). The use of cultivars with any type of resistance should be encouraged, given the advantages it offers in relation to the environment, limitation of the use of fungicides and reduction of the population of pathogens at the local and regional level. Currently, there are still few studies on genetic resistance to diseases (Rezende et al., 2005).
In addition to the use of biotic agents for the induction of systemic resistance, several chemical compounds (e.g. salicylic acid and dichloroisonicotinic acid [INA]), have been used for the same purpose in several plants. In this context, recently a new compound, an S-methyl ester of benzo acid (1,2,3) thiadiazole-7 carbyoic acid (known as Bion, BTH or CGA 245704) was produced and commercially released in Germany, as the first plant defense activator (Rezende et al., 2005). BTH was shown to be particularly effective in monocotyledonous plants, and a single application in wheat (usually 60 g/hectare) resulted in significant protection of plants for several weeks against Erysiphe graminis (cause of powdery mildew), in addition to suppressing the leaf spot and rust caused by Septoria sp. and Pucinia sp., respectively. Similarly, a single application of BHT in rice provided a very long protection against Pyricularia oryzae, the agent of blast (Cavalcanti et al., 2005).
The plant activator also induced resistance in dicotyledonous plants such as tobacco, cucumber, tomatoes and beans, but several applications were necessary for significant reductions in symptoms. Like other chemical compounds, such as INA, BTH is easily translocated inside the plant and does not exhibit a direct antimicrobial effect. Apparently, BTH stimulates the same defense responses observed after the treatment of plants with INA, and is probably another functional analogue of salicylic acid (Van Loon et al., 1998, Agrios, 2007).
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TYPES OF GENETIC RESISTANCE
Resistance is a genetic characteristic of the host plant that can prevent or reduce the incidence and/or severity of the disease (Carvalho & Barcellos, 2012). It is obtained from breeding programs aimed at the incorporation of resistance genes or by applying biological or chemical inducers that activate defense systems in the plant (Camargo & Benjamin Filho, 1995). Plant resistance was classified by Vanderplank (1968) as vertical (RV) and horizontal (RH) due to the significant differential interaction between pathogen breeds and host cultivars. Conceptually, VR occurs when there is a significant differential interaction between breeds and cultivars, and the resistance is effective against some breeds and not to others. This type of resistance is known as race-specific, oligogenic, complete or qualitative resistance (Cavalcanti et al., 2005).
It usually has a characterized expression when there are no symptoms of the disease, such as in the cultivar Diamante 22 de D. alata, resistant to anthracnose in Colombia. Because genetic changes to pathogenicity constantly occur in pathogen populations, genes that confer VR may not be effective in all regions and, therefore, completely resistant cultivars in one place may be susceptible in another (Vanderplank, 1968; Rezende et al., 2005). On the other hand, HR is characterized by not exhibiting differential interaction between breeds and cultivars, being effective against all breeds of the pathogen. It is called non-specific, partial, polygenic breed, field resistance or adult and qualitative plant. HR is characterized by incomplete protection, where infection occurs, however it progresses slowly, resulting in sometimes significant damage to production (Camargo & Benjamin Filho, 1995; Agrios, 2007). During the evolutionary process, plants acquired a sophisticated defensive strategy to 'perceive' the attacks of pathogens and insects, translating this perception into an appropriate response and in an adaptive way. The innate immunity of the plant is surprisingly based on the complex response that is highly flexible in its ability to recognize and respond to the most diverse invaders (Camargo & Benjamin Filho, 1995).
In the evolutionary process, plants have developed defense mechanisms that are only activated in response to infection by pathogens or treatment with certain chemical compounds, natural or synthetic, called elicitors (Cavalcanti et al., 2005). Resistance, in this case, is classified as induced. This type of resistance can occur in tissues close to the necrosis reaction, caused by pathogen infection or chemical treatment, being called acquired local resistance (Vanderplank, 1968; Rezende et al., 2005). Following this process, through the transmission of biochemical signals, other parts of the plant are induced to produce defense substances, characterizing the acquired systemic resistance (Agrios, 2007). Acquired systemic resistance (RSR) can be distinguished from other types of resistance by expression against a wide spectrum of pathogens. In smoking, the activation of ARS resulted in a significant reduction in symptoms caused by the fungi Phytophthora parasitic, Cercospora nicotinae and Peronospora tabacina, the smoke mosaic viruses (TMV) and tobacco necrosis (TNV) and the bacteria Pseudomonas syringae pv tabaci and Erwinia carotovora (Tuzun & Kuc, 1991). The main defense mechanisms involved in ARS are cell wall lignification and production of pathogenesis-related proteins, such as chitinases and β-1-3-glucanases (Sticher et al., 1997).
The induction of ARS is an important alternative method of controlling plant diseases and, given the practicality of use in the field, several chemicals have been researched for the inducing effect in leaf sprays. In yams, Rompf (1999) verified the production of several chitinases using biotic (Autoclaved Fusarium oxysporum) and abiotic (ethylene, chitin and chitosan) elicitors applied to calluses of D. alata. In cell cultures of D. bulbifera (airyam), it demonstrated the expression of a PR-protein defense by elicitation with the fungus Colletotrichum gloeosporioides (Rompf, 1999). The study of the genetics of factors involved in the regulation of ARS has made it possible, in some pathosystems, to obtain transgenic plants with marked expression of ARS, making the use of this type of resistance in the control of plant diseases very promising (Cao et al., 1998).
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RHIZOBACTERIC-INDUCED SYSTEMIC RESISTANCE
Non-pathogenic strains, rhizosphere colonizing bacteria are designated as plant growth promoting rhizobacteria (PGPR), because they can stimulate plant growth (Kloepper et al., 1980). Growth results mainly from the repression of soil pathogens and other harmful microorganisms (Schippers et al., 1987), but there are also reports of the direct effect on growth (Van Peer & Schippers, 1989). Fluorescent bacteria, Pseudomonas spp., are among the most effective PGPR's and have been shown to be responsible for reducing diseases in naturally uninfested soils (Raaijmaker & Weller, 1988). The biological control activity of selected strains of Pseudomonas spp. is effective under certain field conditions (Tuzun & Kuc, 1991; Cao et al., 1998) and in commercial greenhouses (Leeman et al., 1995), and may result from competition for nutrients, competition for iron with siderophores and antibiosis (Bakker et al., 1991).
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DIFFERENCE IN THE EFFECTIVENESS OF ISR AND SAR
One of the parallels between rhizobacteria-induced RSI and pathogen-induced SAR is that both types of induced resistance are effective against a wide spectrum of plant pathogens (Tuzun & Kuc, 1991; Van Loon et al., 1998). To compare the spectrum of effectiveness of RSI and SAR, a large number of pathogens (viruses, bacteria, fungi and oomycetes) of Arabidopsis were tested. RSI and SAR in WCS417r were induced by an avirulent strain of the pathogen Pst DC3000, being effective against bacterial stain and black rot, caused, respectively, by the bacteria Pst DC3000 and X. campetris pv. armoraciae (Pieterse et al., 1998; Ton et al., Fusarium wilting caused by the fungus F. oxysporum f.sp. raphani was also affected by activated defensive responses during RSI and SAR (Pieterse et al., 1998; Van Wees et al, 1999). In addition, the disease caused by P. parasitica, mildew, was inhibited in both cases, although SAR was significantly more effective than RSI (Ton et al., 2002). In addition to these similar effects, there are some clear differences. For example, plants expressing ISR demonstrate an increase in resistance against infection by the fungus A. brassicicola, while SAR is not effective against this pathogen (Tuzun & Kuc, 1991). In contrast, SAR expression inhibits the multiplication of the turnip crestamento virus and strongly reduces the symptoms caused by this virus, while RSI has no effect at all (Ton el. al., 2002). Thus, the spectrum of effectiveness of RSI and SAR partially overlaps, but also diverges, suggesting that the defensive responses activated during the two types of induced resistance are at least different (Pieterse et al., 1998).
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ROLE OF JASMONIC ACID (JA) AND ETHYLENE (ET) IN ISR
In Arabidopsis, both LA and ET activate a group of defense-related genes and when applied exogenously, confer resistance against Pst DC3000 (Pieterse et al., 1998; Van Wees et al., 1999). In order to investigate whether RSI is associated with changes in gene expression of JA and ET, Van Wees et al. (1999) monitor the expression of a group of well-characterized genes related to JA and/or ET (for example, LOX1, LOX2, VSP, PDF1.2, HEL, CHIR-B and PAL1) in the Arabidopsis model plant expressing RSI by WCS417r. None of these genes tested had their expressions altered in the inducing plant, neither locally in the roots nor systematically in the leaves. This suggests that the resistance achieved was not associated with further changes in LA and ET levels (Van Wess et al., 1999). In fact, local and systemic analyses of JA and ET levels have shown that CRSI by WCS417r is not associated with the production of these signal molecules. This result suggests that the dependence of LA and ET to RSI is based on increased sensitivity to these hormones, rather than on an increase in their production (Pieterse et al., 1998).
If the dependence on ISR to LA and ET is based on an increase in sensitivity to these molecules, plants expressing ISR would be able to react more quickly and more potently to the production of LA and ET when infected by pathogens. This hypothesis is anchored in the result that the expression of some Arabidopsis genes induced by AJ and ET (VSP, PDF1.2, HEL) is significantly increased in leaves expressing ISR, then being inoculated with Pst DC3000 or after the exogenous application of MeJA or the ET percussor, the ACC, when compared to control plants (Van Wees et al., 1999). These results suggest that RSI in Arabidopsis is associated with an initial expression of a group of genes that respond to LA. The expression of defense genes, which leads to a rapid or higher level of expression after inoculation, appears as a common action in the different types of induced resistance (Conrath & Pieterse, 2002). This may explain, on the one hand, the apparent lack of changes in gene expression in induced tissues in the absence of the challenging pathogen, while on the other hand, aplanta is able to react more efficiently against an invading pathogen (Conrath & Pieterse, 2002).
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EXPRESSED INDUCED RESISTANCE WITH INCREASED BASAL RESISTANCE
Unlike their roles in induced systemic resistance, the defense signal molecules, AS, AJ, and ET are described to be involved in the primary regulation of defense response. Evidence for the role of AS, AJ and ET in basal resistance comes from genetic analysis of mutant Arabidopsis and transgenic plants that are affected in the biosynthesis or perception of these compounds (Van Wees et al., 1999). In many cases, the genotypes affected in AS, AJ or ET signaling have shown an increase in susceptibility to pathogen or insect attack (Camargo & Bergamin Filho, 1995). AS, AJ and ET are involved in different magnitudes in basal resistance against specific pathogens. For example, basal resistance in Arabidopsis
against the oomycete P. parasitica and the turnip blight virus, it seems to be controlled predominantly by an AS-dependent route (Conrath & Pieterse, 2002). Only NahG plants that do not accumulate AS have shown an increase in susceptibility to these pathogens (Rabbit, 2003). In contrast, basal resistance against pathogenic fungi A. brassicicola and B. cinerea is reduced only in mutants insensitive to LA and ET, and not in NahG plants (Ton et al., 2002). Interestingly, basal resistance against Pst DC3000 and X. campestris pv. armoraciae bacteria is affected in NahG plants and in mutants responsive to AJ and ET (Pieterse et al., 1998; Ton et al., 2002), suggesting that basal resistance against these pathogens is controlled by a combination of actions of AS, AJ and ET (Conrath & Pieterse, 2002). Comparisons of the effectiveness of AS-dependent SAR and AJ/ET-dependent RSI against these different Arabidopsis pathogens revealed that SAR is predominantly effective against pathogens that in non-induced plants are resistant through the AS-dependent basal resistance mechanism, while RSI is predominantly effective against pathogens that in non-induced plants are resistant through the AJ and ET-dependent basal resistance responses (Ton et al., 2002). Thus, SAR seems to constitute an increase in AS-dependent defenses, while ISR seems to be based on an increase in AJ and ET-dependent defenses (Coelho, 2003).
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GENETIC RESISTANCE TO THE MAIN YAM DISEASES
Through hybridization, IITA has developed new genotypes of the most cultivated yam species and made these materials available to the various producing regions in the world (Conrath & Pieterse, 2002). In multiplication fields in Nigeria, clones are evaluated for reaction to some shoot diseases, such as: anthracnose; leaf spots and viruses. Despite the availability of genetic material, there are few studies worldwide aimed at the use of genetic resistance in the control of yam diseases. Most of the works have been developed in relation to anthracnose, mosaic and meloidoginosis (Coelho, 2003).
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USE OF SILICON AS A RESISTANCE INDUCER
Silicon has been reported as one of the elements associated with the induction of resistance in plants and its absorption can bring an increase in this resistance, especially for crops that accumulate it (Mauad et al., 2003). Research conducted with various cultures has confirmed the potential of silicon in reducing the intensity and severity of diseases (Menzies et al., 1991; Datnoff et al., 1997). Rice plants (Oryza sativa L.), for example, grown with increasing doses of this element had the severity of sheath burning (Rhizoctonia solani Kühn) reduced (Rodrigues et al., 2002). However, for papaya, the effects of silicon on diseases have not yet been tested. The mechanism by which silicon affects the development of diseases in plants is possibly the result of the action of this element on the host tissue, providing physical impediment and a greater accumulation of phenolic compounds and lignin at the site of injury (Chérif et al., 1992). This structural function provides anatomical changes in tissues, such as epidermal cells with a thicker cell wall due to silica deposition in them (Blaich & Grundh Fer, 1998), favoring better plant architecture, in addition to increasing photosynthetic capacity and disease resistance (Menzies et al., 1991). Among the sources of silicon, calcium silicate (CaSiO3) is the most widely used form in most commercial products (Rodrigues et al., 2002). Among the products marketed are silicate clay, whose trade name is Rocksil®. Another example of a commercial product is organomineral fertilizer, whose trade name is Micromix®, which acts by providing a rapid assimilation of available nutrients, increasing the production of plant mass, a fact that can make the plant resistant to pathogens (Rodrigues et al., 2002).
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COMBINING ISR AND SAR TO IMPROVE PLANT DISEASE CONTROL
Plant diseases are responsible for high losses in agriculture. Conventional control methods are based on the application of chemical agents and genetic improvement aimed at resistance (Pieterse et al., 1998; Van Wees et al, 1999). The use of chemical agents and their presence in the soil are highly dangerous to the environment, especially when these chemicals are repeatedly applied in an exaggerated way to the soil for the control of pathogens. Classic breeding methods depend on the availability of resistance genes, which often have short durability (Rabbit, 2003). In addition, these two disease control strategies are directed against one or a small group of pathogens. Induced resistance is an attractive alternative form for plant protection, being based on the activation of existing resistance mechanisms in the plant and the effect against a wide spectrum of plant pathogens (Van Loon et al., 1998). Thus, detailed knowledge of the molecular mechanisms of induced resistance will be important in the development of biological, durable and non-harmful actions to the environment to protect crops (Camargo & Bergamin Filho, 1995).
Simultaneous activation of RSI and SAR results in a higher level of induced protection against P. syringae pv. tomato (Van Wees et al., 2000). This indicates that the route of JA- and ET-dependent RSI and AS-dependent SAR act independently and additively at the level of protection against this particular pathogen. In addition, evidence that RSI and SAR provide differentiated protection against the most different types of pathogens (Ton et al., 2002). Then the combination of these two types of induced resistance can protect the plant against a complementary spectrum of pathogens, and can even result in an additive level of induced protection against pathogens, whose resistance of the respective host is processed through the dependent routes of AJ/ET and AS (Rabbit, 2003). Biological plant control is still in its infancy, due to the level of protection and its consistency being general and not sufficient to compete with conventional methods of disease control (Carvalho & Barcellos, 2012). An important action to improve the efficacy and consistency of biological control against soil pathogens would be to apply combinations of antagonistic microorganisms with different means of action (De Boer et al., 1999). In addition, the combination of RSI and SAR provides protection against a large number of pathogens and an increase in the levels of protection against specific bacterial pathogens (Van Wees et al., 1999), offers us great potential to integrate both forms of induced resistance protection into future agronomic practices (Camargo & Bergamin Filho, 1995).
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CONCLUSIONS
Plants have developed defense mechanisms that are only activated in response to infection by pathogens or treatment with certain chemical compounds (natural or synthetic); Induced resistance can occur in tissues near the necrosis reaction, caused by pathogen infection or chemical treatment, being called acquired local resistance; Acquired systemic resistance is characterized by the transmission of biochemical signals, and other parts of the plant are induced to produce defense substances; Both RSI and SAR are important tools in the control of plant diseases and are effective against a wide spectrum of plant pathogens; SAR constitutes an increase of SS-dependent defenses, while RSI is based on an increase in AJ and ET-dependent defenses; Simultaneous activation of RSI and SAR results in a higher level of protection; Induced resistance is an attractive alternative form for plant protection; Research with induced resistance should be stimulated and work on pathogen variability and resistance inheritance should be encouraged so that control through genetic resistance is more
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