Alternative Management of Fungal Diseases in Plants: Comparison
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Fungal pathogens pose a major threat to food production worldwide. Traditionally, chemical fungicides have been the primary means of controlling these pathogens, but many of these fungicides have recently come under increased scrutiny due to their negative effects on the health of humans, animals, and the environment. Furthermore, the use of chemical fungicides can result in the development of resistance in populations of phytopathogenic fungi. Therefore, new environmentally friendly alternatives that provide adequate levels of disease control are needed to replace chemical fungicides—if not completely, then at least partially. A number of alternatives to conventional chemical fungicides have been developed, including plant defence elicitors (PDEs); biological control agents (fungi, bacteria, and mycoviruses), either alone or as consortia; biochemical fungicides; natural products; RNA interference (RNAi) methods; and resistance breeding. 

  • plant defence elicitors
  • fungal disease management
  • plants

1. Introduction

Plant pathogens pose a significant threat to the agricultural industry and are one of the most important factors in agricultural yield losses and food insecurity across the globe. Fungal pathogens alone may account for up to 20% of worldwide yield losses [1]. Conventional breeding techniques alone cannot provide adequate protection against fungal pathogens for many crops because fungal pathogens are able to overcome introduced genetic resistance [2]. These pathogens pose a particularly serious problem in perennial crops such as apples and other tree fruits. Orchards are expected to last 20–30 years, making it unrealistic to replace vulnerable cultivars with resistant ones, especially since resistance can be overcome long before the end of an orchard’s productive life. Considering that genetic resistance is generally not sustainable and the development of resistant cultivars takes many years, disease control has relied for decades on the application of chemical fungicides [2]. Although very effective, these fungicides are notorious for their hazardous effects on human and animal health as well as for their environmental toxicity [3,4][3][4]. Concerns over the potential environmental consequences of the uncontrolled use of these active substances has led to regulations on their use based on environmental risks assessments, and these restrictions can range from reductions in the number of applications per crop season to the outright removal of specific active substances from the market [3]. In addition, plant pathogenic fungi can develop resistance to chemical fungicides, particularly single-site fungicides, which are more likely to lead to the development of resistance in fungal pathogen populations. In the past few decades, numerous disease management strategies have been developed as an alternative to traditional chemical fungicides and breeding methods, including the use of plant defence elicitors (PDEs), biological control or biochemical fungicides, and RNA interference (RNAi). We have reached a crossroads in which these alternatives to chemical fungicides will be called on to play an increasingly important role in disease management. 

1.1. Chemical Fungicides

Fungicides can be broadly defined as chemical substances used to control fungal diseases by inhibiting the growth of pathogenic fungi or by eradicating them completely. Fungicides can be classified as inorganic or organic based on their chemical composition. Inorganic fungicides do not contain carbon in their structure and are typically based on sulphur or metal ions. This group of fungicides has been in use since the discovery of Bordeaux mixture (copper sulphate pentahydrate and lime) by Pierre-Marie Alexis Millardet in the in the late 19th century [5]. Centuries after this discovery, copper- and sulphur-based fungicides are still used extensively in conventional and organic agriculture [6,7,8,9][6][7][8][9]. Examples of modern inorganic fungicides include copper sulphate, copper oxychloride, and copper hydroxide [10,11][10][11]. In contrast, organic fungicides contain carbon atoms in their structure [6]. These organic synthetic compounds have become more popular, although inorganic fungicides continue to be used in modern agriculture. All synthetic inorganic or organic fungicides, regardless of their composition, can be divided into two distinct classes based on their mobility in the plant: contact (protective) fungicides, which remain on the surface of the plant, and systemic (mobile/curative) fungicides, which are absorbed into the plant.
Contact fungicides typically have a wide range of action against different fungal pathogens and are effective in preventing the infection of plant tissues. They usually achieve this by killing fungal spores or by inhibiting their germination before they penetrate and colonize the host tissues [6,12][6][12]. Contact fungicides are not effective in a curative strategy and to be effective, must be applied before the pathogen infects the plant [13]. Most contact fungicides are not absorbed by the plant and remain on the plant tissue surface. However, the frequency of application must be carefully monitored, since contact fungicides can become phytotoxic in the rare cases when they are absorbed [14]. Because contact fungicides usually remain on the plant surface, protection is temporary and can be quickly lost due to rainfall or other weather conditions [15,16][15][16]. Contact fungicides can also be eliminated from the plant surface by wind or degraded by UV radiation, and therefore, their protective action does not exceed 10–12 days [6]. It is also important to bear in mind that contact fungicides are only effective on the leaf surface present at the time of application and thus are less efficacious during heavy leaf growth. Therefore, the effectiveness of contact fungicides is particularly reliant on the proper timing of application, which generally must be performed prior to the known or predicted infection periods of the targeted pathogens. Furthermore, since these fungicides are gradually removed from the plant surface, repeated applications during the growing season are necessary for sustained protection. In some circumstances, this characteristic is beneficial to growers, since contact fungicides, unlike systemic fungicides, have the advantage of being easily removed from treated produce before it reaches the consumer [6].
Systemic fungicides are a more recent development in disease control and are considered to be more promising than contact fungicides [17]. While providing a protective effect by suppressing spore germination, these fungicides can also be absorbed into plant tissues, either locally or more broadly, and are therefore able to kill fungal pathogens after they have penetrated and infected host tissues [18]. The degree of systemic activity—which ranges from simple translaminar activity in leaf tissues to local spread from the absorption site and mobility within the xylem of the plant—is generally determined by the chemistry of the compound and can play an important role in determining the efficacy of a fungicide against specific fungal pathogens [18,19,20][18][19][20]. Because of the ability of systemic fungicides to be absorbed in plant tissues, using them to treat plant materials has become routine practice, and the seeds of most agricultural crops are treated with systemic fungicides to protect against both seed- and soil-borne pathogens [21]. Although systemic fungicides are highly effective, most of the compounds involved operate through a single mode of action (i.e., they generally target a single essential fungal enzyme or metabolic pathway) and, therefore, are extremely vulnerable to the development of resistance by target fungal pathogens [22].

1.2. The Disadvantages of Chemical Fungicides: Environmental Toxicity and Resistance Development

Despite their high efficacy, both contact and systemic fungicides have numerous drawbacks associated with their use. One substantial shortcoming is that, due to their lack of specificity, chemical fungicides can disrupt both beneficial and pathogenic microorganisms. For instance, the application of fungicides to mango leaves has been demonstrated to eliminate many endophytes, creating a window of opportunity for pathogens to colonize the tissues formerly that the endophytes formerly inhabited [23]. While this phenomenon has been most readily observed in foliar spray treatments, fungicidal seed treatments have also been associated with similar reductions in beneficial endophytes, and the negative consequences of fungicides on soil microbial communities are well documented [24,25,26,27,28][24][25][26][27][28]. Indeed, mounting evidence suggests that seeds protected with systemic fungicides may negatively impact plant health and vigour by targeting beneficial endophytes in the absence of pathogen pressure, the practice may be counterproductive [21]. Therefore, the application of chemical fungicides can have negative consequences for plant health and yield by eliminating beneficial microbes that promote growth, development, and resistance to biotic and abiotic stresses.
Fungicides can severely impact the aquatic environment, as they are able to enter aquatic ecosystems through different ways, including wastewater, runoff, and subsurface drainage [29[29][30],30], and can be toxic to a wide range of aquatic organisms, including algae, fish, and invertebrates [31,32][31][32]. Furthermore, fungicides could harm important pollinators like bees through mechanisms such as the impairment of larval and physiological development, the promotion of increased sensitivity to other pesticides, and increased mortality [33]. Exposure to fungicides can lead to acute and chronic neurotoxicity in humans, and thus significantly impact human health [34].
In addition to fungicides’ environmental toxicity, concerns have been raised over the durability of fungicide efficacy. Fungi have tremendous evolutionary potential to rapidly develop resistance against fungicides due to the intense selective pressure exerted by repeated fungicide applications [22]. Mutations in DNA sequences can arise from errors in DNA replication, damage from UV radiation, or exposure to mutagens or viral infections. Environmental stress may play a significant role in determining the rate of mutation. For example, stress from increasing temperatures accelerated the rate observed in the fungal pathogen Zymoseptoria tritici [35]. Although mutations are inherently random, those that result in enhanced resistance to fungicides will be positively selected for by the eradication of strains without resistance. Over time, this inevitably results in fungicide-resistant strains of the targeted pathogen [22].
Fungicide resistance is a stable and heritable change in an individual fungus that results in a reduction in its susceptibility to fungicides. Fungicide resistance is well documented to develop more often against single-site fungicides than those with a multi-site mode of action, making modern synthetic fungicides especially vulnerable to resistance development [22]. The threat of fungicide resistance is a major concern to growers worldwide, and numerous strategies are employed in order to prevent its emergence. The Fungicide Resistance Action Committee broadly divides fungicides by their mode of action in order to identify those with potential resistance concerns. Its recommendations include applying multiple fungicides with varying modes of action over the course of the growing season, restricting the use of the fungicides most likely to induce resistance with repeated use, and prioritizing multi-site fungicides, to which fungi are less likely to develop resistance [36]. To date, over 43 different modes of action have been identified, although the mechanisms for some of these are not yet known [36].
In conclusion, while chemical fungicides are an extremely effective tool—at least in the short term—for reducing disease incidence in the crops, they have harmful effects on beneficial plant microbiota, the health of humans and other animals, and on the environment. These factors, in addition to the rising threat of fungicide resistance, have led to increasing restrictions on the use of chemical fungicides. Given these challenges, conventional chemical fungicides must be complemented with cost-effective, eco-friendly alternatives to maintain appropriate levels of disease control with the absence or reduced usage of these vital compounds. An overview of the benefits and drawbacks of chemical fungicides and alternative disease control methods can be found in Figure 1.
Figure 1. Methods for controlling fungal plant pathogens. The potential advantages (green) and disadvantages (red) inherent in conventional and alternative methods of disease control are also shown.

2. Alternative Management of Fungal Diseases

2.1. Agronomic Practices and Cultivation Methods

Agronomic practices and cultivation methods can greatly influence the vulnerability of crops to fungal pathogens through a variety of mechanisms, including disruption of the pathogen lifecycle, improving the vegetative performance and thus the natural health status of the plant host, or the removal of sources of inoculum from the field. The main drawback of these agronomic practices is that they tend to be laborious, expensive, and less effective than conventional fungicides, and thus, they are more suited as complementary tools to more effective methods. These practices include but are not limited to: sanitation, tillage, crop rotation, pruning and thinning, the intermixing of different crops or different varieties of the same crop, and the manipulation of canopy architecture. The impacts of cultivation methods on pathogen pressures have been the subject of many thorough reviews [37,38,39][37][38][39].
Foremost among cultivation methods which can enhance the control of fungal pathogens is proper sanitation, that is, the removal of sources of inoculum from the field. For instance, the removal of crop residues, which often serve as the source of primary inoculum for Colletotrichum species, is an effective means for reducing anthracnose and black spot in guava fruit [40]. Leaf shredding is a common means of removing inoculum sources of foliar pathogens and has long been promoted as a means to control apple scab (Venturia inaequalis) [41]. However, as with many cultivation practices, sanitation practices on their own do not provide disease control comparable to chemical fungicides. In a direct comparison, the removal of senescent and necrotic leaves and the removal of unmarketable fruit from the alleys between beds of strawberries significantly reduced Botrytis fruit rot caused by Botrytis cinerea in annual strawberry compared to controls, but losses remained significantly higher than in the fungicide control [42]. Nevertheless, sanitation practices are an effective means of complementing chemical fungicides. Recently, it has been demonstrated that leaf shredding in combination with the application of demethylation inhibitor fungicides significantly influenced the fungicide sensitivity of V. inaequalis populations. V. inaequalis isolates from orchards treated with demethylation inhibitor fungicides which also underwent leaf shredding retained fungicide sensitivities close to that of unexposed populations, potentially as a result of a smaller initial effective population size [43]. Thus, the inclusion of proper sanitation practices with chemical fungicides in an integrated treatment regime may both improve disease control and delay the development of fungal resistance, though further research will be required to determine the extent of this effect.
There is conflicting evidence on the impacts of tillage on disease control, and whether specific tillage practices promote or reduce fungal diseases is reliant on the specific pathogen and macro-environmental conditions [44,45,46][44][45][46]. The removal of organic matter in conventional tillage practices, while consequential for soil health, also removes potential sources of primary inoculum, while conservation (or reduced) tillage can promote pathogen survival by providing residues for the pathogen between crop plantings [47]. Furthermore, conservation tillage can alter soil characteristics in ways which may either be beneficial or detrimental to individual pathogens, such as increasing soil moisture, altering soil temperatures, and failing to disrupt the soil [48]. However, compared to conventional tillage, conservation or no-tillage has been shown to improve the general disease suppressiveness of the soil by reducing tillage-induced losses in microbial biomass, and disease suppression in spring barley was improved by long-term conventional tillage and no-tillage [46]. Given the significance of the soil microbiome in the determination of the prevalence of disease, particularly in the case of soil-borne pathogens, the impact of these practices on soil and rhizosphere microbiomes is an area of intense interest [49,50][49][50].
The continuous cultivation of a particular crop results in the accumulation of pathogens and increased disease pressure [51]. As such, the rotation of crops from host to non-host species serves as an effective break to reduce pathogen inoculum [52]. Crop rotation is especially important for the control of soil-borne pathogens, and longer duration periods have been demonstrated to be more effective in preventing disease [53]. Furthermore, crop rotation may have beneficial effects on the general disease suppressiveness of the soil. Numerous studies have investigated crop rotation either alone or in combination with tillage for its potential in modulating general disease suppressiveness in the soil in crop systems such as potato, banana, and peanut [53,54,55][53][54][55]. Thus, ideal rotation strategies will not only serve as a break in pathogen pressure but as a means of enriching the soil’s capacity to ward off pathogens. Similar to crop rotations, the inter-cropping of different species can serve to reduce pathogen pressures [56]. In this respect, the examination of soil microbiomes as a result of multi-cropping in five organic vegetable farming systems revealed that inter-cropping was associated with a decrease in the abundance of soil-borne pathogens [57]. Thus, determining the ideal combinations for inter-cropping for each species may serve as an effective form of disease control.
Plant canopy architecture is another important factor in determining disease pressure, as the density of the canopy can significantly influence the micro-climate of the canopy as well as spore dispersal. Thus, for fungal pathogens that are dispersed over short distances by splashing rain, canopy architecture is a major factor in determining the dispersal of the pathogen [58,59,60][58][59][60]. On the other hand, dense canopies are also associated with a microclimate of increased humidity which favours pathogen infection, and thinning systems which promote aeration within the canopy have been shown to reduce the incidence of apple scab infection [61,62][61][62]. Thus, the determination of the optimal density for a given crop represents a significant challenge in the pursuit of enhanced disease control. Intriguingly, the uniformity of crop height in current cropping systems may be advantageous to splash dispersed fungal pathogens, as it has recently been demonstrated that growing wheat cultivars of contrasting height together enhanced the control of Septoria triciti blotch (Zymoseptoria triciti) [63]. While more research is necessary to determine whether this approach is applicable to other crop systems or pathogens, it is clear that further research into the interplay between canopy architecture and disease will be beneficial for disease management.
Whether it be through the direct removal of primary inoculum sources, the rotation of non-host crops, or the establishment of physical barriers to pathogen dispersal, cultivation methods have significant influence on the vulnerability of crops to fungal pathogens. Understanding how common cultivation practices interact with disease management will allow for the optimization of growth conditions in order to reduce disease pressure, especially as these cultivation practices can readily be combined with chemical fungicides or their alternatives for improved disease control.

2.2. Improving Plants’ Genetic Resistance through the Use of R and S Genes

Plants have evolved numerous genetic defence mechanisms to protect themselves from pathogens. Growers have long relied on the manipulation of these mechanisms, traditionally by breeding for resistance as a way to reduce crops’ susceptibility to fungal pathogens. Host plants can recognize non-specialized fungal pathogens by toll-like receptors that detect pathogen-associated molecular patterns, in turn activating the host’s downstream defense mechanisms. Specialized pathogens are able to overcome these basal defence mechanisms by secreting effector molecules into host plants [64]. However, the co-evolution of plants and fungal pathogens over millennia has provided plants with a means of defence against effector molecules: resistance (R) genes. The R-gene family is incredibly diverse and well conserved in plant species. R-genes encode for nucleotide-binding leucine-rich receptors (NLRs), which collectively recognize a broad spectrum of plant pathogens and pests, inducing an array of resistance mechanisms in response to infection or predation [65,66][65][66]. NLRs are activated by the binding and recognition of pathogen effectors but, in some cases, may detect a pathogen indirectly, generally by recognizing pathogen modified host proteins. An example of this form of recognition occurs in Arabidopsis in response to Pseudomonas syringae infection, where the effector (in this case, a protease) cleaves the Arabidopsis PBS1 kinase, triggering its recognition by the NLR RPS5 [67]. The successful recognition of effector molecules or effector-modified host proteins in plants by the associated NLR typically results in effector-triggered immunity, a localized response characterized by a hypersensitive reaction (HR) in which the plant cells near the infection undergo apoptosis [68,69][68][69]. In addition, the recognition of a pathogen by plant pattern-recognition receptors (PAMPs) or an effector protein by R proteins triggers the production of salicylic acid (SA) and the downstream induction of broad, systemic defence mechanisms against subsequent infections, triggered independently of the HR response [70,71][70][71].
The direct or indirect recognition of effector proteins by R-gene-encoded receptors involves a gene-for-gene relationship in which the R-gene receptor identifies a single effector protein (encoded by a matching avirulence [Avr] gene); therefore, a host with a given R-gene will be resistant to a pathogen with the matching Avr gene [72]. In most plant–pathogen systems, the host and pathogen species may collectively have numerous R- or Avr genes. For example, twenty R-genes have been identified in apples (Malus × domestica) that match the corresponding Avr genes identified in the pathogen Venturia inaequalis, which causes apple scab. However, it should be noted that no single cultivar or individual line will contain all these resistance genes; for example, Honeycrisp apples have Rvi19 and Rvi20 in their genomes, while Golden Delicious cultivars contain Rvi1. Therefore, while many apple cultivars have some resistance to Venturia inaequalis, these cultivars are still vulnerable to some Venturia inaequalis strains that do not have corresponding Avr genes [73].
A typical mechanism in pathogens for overcoming host resistance is Avr gene mutations to prevent the product (or activity, in the case of indirect mechanisms) from being recognized by R-gene-encoded receptors. If the effector is recognized, pathogens can also overcome resistance by interfering with the host response [74]. The presence of an R-gene in a host plant population will naturally select for pathogens in which the corresponding Avr gene has been lost or modified so that it is no longer recognized by the R-gene-encoded receptor. In turn, successful mutations in the Avr gene will induce selection pressure on host plants for R-genes which impart resistance to the mutated effector. Thus, host plants and their pathogens are continuously engaged in an evolutionary arms race and, in wild populations, the frequencies of Avr and R-genes will cycle over time [75,76][75][76]. In modern agricultural settings, the uniformity of resistance genes in a population may accelerate the selection process, leading to rapid loss of resistance in these settings [77].
The identification of R-genes and their incorporation in economically important crops is a vital pillar in the development of resistant plants. Along with the use of conventional fungicides, resistance breeding techniques have served as the most effective method of disease control for decades, particularly in annual crops [78]. Although resistance breeding is also practiced in perennial crops, its effectiveness is often limited by the lifetime of the crop. Modern tree fruit crops, for instance, are expected to have lifespans of 20–30 years, giving ample time for selective pressure from resistant cultivars to result in pathogens overcoming the associated R-genes [77]. This is particularly problematic since introducing cultivars with new resistance genes is difficult due to orchards’ long lifespans. Furthermore, plant breeding is very time-consuming and, in recent years, plant breeders have relied on transgenic tools or gene transformation to expedite resistance-breeding efforts, since they allow the faster introduction of R-genes from otherwise incompatible species as well as from compatible species [79].
Numerous strategies have been developed to reduce the ability of fungal pathogens to overcome R-genes, such as rotating R-genes in a field (most suitable for annual crops), mixing cultivars with distinct R-genes in a field or between fields, and pyramiding multiple R-genes in a single cultivar to confer more durable resistance [77]. Somewhat like multi-site fungicides, pyramiding R-genes in a single cultivar makes it more difficult for pathogens to overcome resistance despite their evolutionary potential [80]. However, pathogens are still capable of overcoming multiple R-genes in the same host plant. For example, the oomycete pathogen Phytophthora infestans can escape multiple resistance genes in potato [81]. The breakdown of resistance to rust fungi in cereal crops under different strategies was recently modelled, and it was demonstrated that, although pyramiding could provide the most effective pathogen resistance, this resistance is less durable when mutation rates in the pathogen population are high [77]. Under such conditions, mixing or rotating crops was more successful at delaying the breakdown of resistance to different R-genes. For example, in mixed populations, the breakdown of resistance to one major R-gene was correlated with increased durability of the other R-genes in the population. Rotations were particularly successful since they were modelled so that pathogens were consistently challenged with new R-genes. Consequently, the authors concluded that rotating different pyramids of R-genes was the most promising method of ensuring durable R-gene resistance [77]. However, many resistant varieties may incur yield and/or crop quality penalties when compared to their susceptible counterparts, and these costs must be carefully considered with the associated benefits [82]. Therefore, the rotation of resistant varieties may not be a feasible strategy in many cases due to economic implications. Furthermore, this strategy is unlikely to be useable or effective in perennial crops, such as apples, pears, and cherries, which have longer lifespans and a juvenile period.
Beyond the introduction of R-genes in susceptible genotypes, advances in genome editing have allowed researchers to identify other mechanisms for reducing disease severity or improving resistance, such as targeting susceptibility (S) genes [83]. S-genes are genes in the host plant required for pathogen infection. Interaction of a pathogen’s effector/toxin molecules with S-genes can assist the pathogen in a variety of ways, such as the recognition and penetration of the host, sustained compatibility between the pathogen and host, and the inhibition of immune signalling [84]. Therefore, the genetic silencing or knocking out of S-genes can improve the host plant’s resistance to the pathogen and is one of the newest frontiers in conferring durable pathogen resistance [83]. Recently, CRISPR/Cas9-mediated knockouts of three S-genes in potato, StDND1, StCHL1 and StDMR6, increased resistance to potato late blight caused by Phytophthora infestans [85]. Likewise, in apple, the expression of the MdCNGC2 gene, which encodes a cyclic nucleotide-gated ion channel, was observed to be strongly induced by Botryosphaeria dothidea infection in susceptible cultivars [86]. Improved resistance to the pathogen was observed with both virus-induced gene silencing and CRISPR/Cas9-mediated mutagenesis of MdCNGC2 [86]. To date, targeting S-genes has proven to be a successful strategy for inducing disease resistance in a number of crop systems, including cucumbers, rice and tomato [87].
Directly introducing resistance in crops is an effective disease management strategy. However, while both R-genes and S-genes can be modified or integrated in the host genome to improve disease resistance, the process is costly, laborious, and time-consuming. In addition, the rapid breakdown of resistance in the field makes resistant cultivars less effective in long-lived crops. Therefore, complementary tools are needed to help delay the breakdown of resistance in crops that cannot be rotated annually.

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