Abstract
India is amongst the top countries consuming, producing and exporting chillies. Chilli (Capsicum annuum), known as chilli peppers, belongs to the family Solanaceae. Heavy losses have been observed in the yield due to diseases caused by bacterial, fungal and viral pathogens. Over utilization of synthetic agents to control these diseases causing pathogens have raised serious biological and ecological issues. Along these lines, late endeavours have been centred on utilizing natural ways for controlling plant pathogens. Interest in biological control using microbial agents has increased over the past years as an alternative to chemicals which are toxic to the environment and lead to the development of resistant pathogenic populations. Biological control using microorganisms is a more environmentally friendly alternative and is utilized either on its own or as a part of integrated management strategy to reduce the use of synthetic agents. This research approach reviews various pathogen causing diseases in the Capsicum annuum, toxicity of the chemical agents used for controlling the pathogens and the biocontrol agents against chilli phytopathogens along with their suggested mode of action. This article will deepen our knowledge about the consistent beneficial effects of microbial biocontrol agents.
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Introduction
Chillies (Capsicum annuum) also known as ‘mirchi’, are an indispensable ingredient in Indian cuisine. They were brought in Asia by Portuguese navigators in the 16th Century. Chilli plant belongs to Solanaceae family, are herbaceous annuals, have glabrous or pubescent lanceolate leaves, white flowers and fruit that vary in length, colour and pungency depending on the cultivar (Stommel et al. 2018). They are rich in Vitamin C (ascorbic acid), E (tocopherols and tocotrienols), P (citrin), B1 (thiamine), B2 (riboflavin), B3 (niacin) and provitamin A (β-carotene) (Gopalakrishnan 2007; Bosland et al. 2012). They are also known to be a good source of flavonoids, carotenoids and xanthophylls (Lee et al. 1995). India has been amongst the major countries producing, consuming and exporting chillies. A rising demand for chillies combined with higher value acknowledgment in the domestic market has spurred farmers to expand areas under chilli cultivation for export (Surepeddi and Giridhar 2015). However heavy yield loss of Chilli crop is observed across the country due to diseases caused by both abiotic and biotic factors.
Abiotic factors affecting chilli plant
Non-living factors responsible for crop damage include extreme levels of temperature, moisture and light, change in nutrients and pH, air pollutants and overdose of pesticides (Peter and Hazra 2012). The major abiotic factor which cause stress conditions in the chilli plant is deficiency or toxicity of the macro and micronutrients. Deficiency of the nutrients may lead to conditions like stunted growth of the plant, chlorosis of leaves, limited foliage and reduced size of fruits. Excessive nutrients are also harmful for the plant and may lead to burning of foliage and root system (Balakrishnan 1999). Due to factors like inconsistent watering, calcium deficiency, increased soil salinity or excessive applications of nitrogen fertilizers; Blossom-End rot is observed in chilli fruit which results in early fruit drop (Taylor and Locascio 2004). This condition manifests in the water soaked lesions on immature fruits, resulting as a prime location for microbial infections by opportunistic disease causing pathogens. Exposure to intense sunlight results in ‘Sun scalding’ where wrinkling of foliage is observed making the plant light-coloured and papery textured. Occasionally fruit skin is affected and cracked open (Rabinowitch et al. 1983). Presence of air pollutants such as peroxyacetyl nitrate (PAN) is reported to cause stunting, chlorosis and even senescence in the chilli plant leaves (Goyal et al. 2020).
Diseases caused by microbial pathogens in chilli plant
Losses incurred in agriculture due to microbial pathogens sums up to around 16% globally (Oerke 2006). The growth and yield of a chilli plant is most affected by bacterial, fungal and viral pathogens (Gachomo et al. 2003). Disease symptoms have been noticed in seedlings, mature plant, fruit or leaves depending on the phytopathogen that attacks the plant. Table 1 enlists the diseases caused by microbial phytopathogens in chilli plants along with the symptoms associated with the disease. Wilting and rotting are manifested in the mature plants by soil borne fungal pathogens belonging to genera Macrophomina, Phytophthora, Rhizoctonia, Sclerotinia, Fusarium, Sclerotium and Verticillium. Bacterial wilt is particularly caused by a bacterium Ralstonia solanacearum leading to the death of the plant (Sanogo 2003). Fungus belonging to genera Pythium or Phomopsis show damping off symptoms in seeds or young seedlings. Infected seeds fail to germinate and the damaged seedlings generally rot, causing the seedling to wilt and eventually die, or collapse from the ground line (Mishra et al. 2013). Leaves of the plant affected by bacterial pathogens (Xanthomonas sp.) and fungal pathogens (Leveillula sp., Alternaria sp. or Cercospora sp.) show powdery mildew and spot symptoms. Formation of mosaic pattern on leaves, curling of leaves, vein bending, mottling of leaves is mostly caused by the viral pathogens affecting the plant (Damiri 2014). Chilli fruits are primarily affected by abiotic factors which can eventually lead to secondary infection by fungal pathogens belonging to the genera Colletotrichum or Phytophthora. These pathogens can attack fruit directly or can attack tissue weakened by environmental factors (Reddy 2009; Naik and Savitha 2014).
Use of synthetic pesticides for controlling chilli crop pathogens and the associated problems
The term pesticide in agriculture refers to a component or mixture of components to prevent, control, reduce or inhibit a pest (bacteria, fungi, virus, nematodes, vectors and even unwanted species of plants or animals) interfering with the production, processing, storage or marketing of any agricultural commodity. Synthetic pesticides are those which are formulated or manufactured using chemical processes using chemically synthesized components or by chemically changing any component derived from natural sources (Stoytcheva 2011). For any pest problem, chemical agents are usually preferred over organic ones as they are cheaper, readily available and have longer shelf life than the later. They are mostly broad-spectrum agents thus can be applied against various pests. They are even known to be more persistent in nature thus reducing the frequency of application in the field, which in turn saves time and economics (McCoy and Frank 2020). However due to such properties of persistency and broad spectrum activity, the indiscriminate use of synthetic pesticides has resulted in serious biological and ecological problems (Whipps 2001; Muthukumar et al. 2008). Table 2 summaries the chemical agents used against chilli plant pathogens and the reported toxicity of each agent. As reported by Pimentel (1995), only < 0.3% of chemical pesticides showed interaction and inhibition only of target pathogens. Most of the chemical pesticides affect the beneficial organisms in the soil which assist natural processes of mycorrhizal colonization, transformation or fixation of nitrogen, improvement of soil porosity and fertility (Aktar et al. 2009). Overuse of pesticides has also resulted in acquirement of resistance by the target pathogens. Some of the chemical agents are seen to be converted to toxic byproducts in the soil thus hampering other plants, animals and even humans (Smith and Perfetti 2020). Studies have revealed many associated adverse effects of the pesticides on human health viz. irritation of eyes and skin, mutations and carcinogenicity, disruption of endocrine functions, impaired reproductive capacity, atherogenicity and interference with neural transmission in the central and peripheral nervous system (Pruett et al. 2001; Atreya and Sitaula 2011; Budzinski and Couderchet 2018). Synthetic pesticides have been detected into aquatic systems due to field runoff or leaching, thus affecting the multiple developmental stages of aquatic life and even wild life (Nabi et al. 2019). Aragaki et al. (1994) has reported the phytotoxicty in a higher plant due to decomposition of a fungicide in water. Disruption of endocrine function, ovarian toxicity, oxidative stress and neuropathological effects has been identified in animals due to toxic chemical agents (Moser et al. 2001; Lu et al. 2004; Tahir and Nour 2009). Considering the risks associated with synthetic pesticides, there is need to shift to biological ways of controlling phytopathogens.
Biocontrol agents against phytopathogens infecting chilli plants
Recent efforts have been focused on developing natural or biological control for the management of plant diseases for increasing the yield. Biocontrol is a safer option as it avoids environmental pollution and is specific to target pathogens. Being from a natural source they don’t tend to pose any harm to plants, animals or humans. According to Eilenberg (2006), “biological control or biocontrol is the use of living organisms to suppress the population density or impact a specific pest organism, making it less abundant or less damaging than it would otherwise be”. In other words, biological control is a phenomenon related to the antagonism between microorganisms (Cook 1985). Numerous microorganisms have been shown to be capable in suppressing plant pathogens and are therefore considered as biological control agents (BCAs). Table 3 summarizes BCAs against plant pathogens affecting chilli crops along with the suggested mode of action. Single BCA may show different modes of action against a phytopathogen which may be expressed sequentially, concurrently or synergistically. There are three main modes of antagonism exhibited by a candidate BCA against a phytopathogen: direct antagonism, indirect antagonism and mixed path antagonism (Pal and Gardener 2006).
Direct antagonism
Direct antagonism, involves the principle of parasitism or predation. In predation, the predator (in this case a BCA) kills the prey (a phytopathogen) for its survival. Some predatory bacteria use the cytoplasmic constituents of other bacteria as a source of nutrition, thereby killing the later (Köhl et al. 2019). Parasitism is a biological interaction wherein the parasite (in this case a BCA) lives on or inside a host (a phytopathogen), thus harming the later. This type of antagonism is termed as hyperparasitism or mycoparasitism/mycophagy (when target pathogen is a fungus). In mycoparasitism, a BCA secretes lytic enzymes that lyse the fungal cell wall leading to the leakage or disorganisation of cell contents. Hyphal deformation (abnormal swelling, curling and branching of mycelia), vacuolization and disintegration have also been reported. This results in a decrease of pathogen population or even complete inhibition (Heydari and Pessarakli 2010). A study carried out by Sid Ahmed et al. (1999) evaluated Trichoderma harzianum as a biocontrol agent for root rot caused by Phytophthora capsici in pepper plants. The study revealed how the hypha of Trichoderma harzianum coils around those of Phytophthora capsici resulting in vacuolization and disintegration of the hyphae of later. Another study exhibited coiling, vacuolation and swelling of the hyphae of Colletotrichum truncatum by Burkholderia rinojensi, resulting in inhibition of the pathogen, thus suppressing the anthracnose in chillies (Sandani et al. 2019).
Indirect antagonism
Indirect modes of antagonism exhibited by BCAs can be either competition for space and nutrition with the pathogen or induction of resistance in the host against the pathogen. Competing for nutrients is generally observed among the species sharing the same ecological niche and having the same physiological prerequisites when resources are constrained. Such competition may lead to reduced proliferation or inhibition of the pathogen (Pal and Gardener 2006). A BCA may limit the growth of the pathogen by competing for host supplied nutrients (exudates, leachates, or senesced tissue), essential soluble nutrients (iron sequestering by producing siderophore) or for colonising root and plant tissues, thus depriving access of the pathogen at the infection site (Vurukonda et al. 2018). When starved of Iron, a Bacillus sp. exhibited inhibition of Fusarium oxysporum Schl. f. sp. capsici, the causal agent of wilt of Capsicum annuum by producing siderophores. This bacterium also did show antagonism against several other plant fungal pathogens, belonging to genus Fusarium, Colletotrichum, Pythium, Magnaporthe and Phytophthora (Yu et al. 2011). Another study revealed rapid root colonization of chilli plant by Arbuscular mycorrhizal (AM) fungi Funneliformis caledonium thus increasing the nutrient acquisition by plant and suppression of Phytophthora blight (Hu et al. 2020). Induced systemic resistance is an indirect type of antagonism wherein inoculation with BCAs triggers the induction or enhancement of defence mechanism of plants. This is achieved via production of defence related metabolites (phenolics, reactive oxygen species, phytoalexins, pathogenesis-related proteins) or via activation of pathways (jasmonic acid, salicylic acid) or via formation of physical barriers (modifications of cell walls and cuticles) (Jayapala et al. 2019; Köhl et al. 2019). Suppression of Colletotrichum truncatum Anthracnose in Chilli Pepper was observed due to resistance induced by Trichoderma harzianum, Trichoderma asperellum and Paenibacillus dendritiformis in host. The chilli plant exhibited enhancement of the activity of defence-related and antioxidative enzymes, accumulation of phenolic compounds and reactive oxygen species (Yadav et al. 2021). Another study revealed the suppression of disease symptoms caused by Pectobacterium carotovorum, Phytophthora capsici and Colletotrichum acutatum by a Bacillus sp. via induction of systemic resistance via a salicylic acid-dependent mechanism (Park et al. 2013). Jisha et al. (2019) reported the induction of defense enzymes peroxidase, polyphenol oxidase and phenylalanine ammonia lyase by Pseudomonas aeruginosa in chilli plant. Such induction of host systemic resistance also increased the total phenolic contents in the plant. Thus the strain of Pseudomonas proved to be capable of reducing antharcnose disease in chilli.
Mixed path antagonism
In this type of antagonism BCAs produce secondary metabolites toxic to the target pathogens. This not only include antibiotics, but also lytic enzymes, unregulated waste products and volatile compounds. Such metabolites interfere in the pathogenesis of the target pathogen (Nega 2014). A BCA can also impart the host plant with growth promoting activities which boost the plant growth and help in disease suppression (Beneduzi et al. 2012). Plant growth promoting BCA can confer the host with various attributes like atmospheric nitrogen fixation, solubilisation of unavailable nutrients such as phosphate, potassium, zinc and silicon thus making it readily available to the plant. They also accelerate production of hormones viz. auxins (Indole Acetic Acid), cytokinin and gibberellins (Bhattacharyya and Jha 2012) or of enzymes such as 1-aminocyclopropane-1-carboxylic acid (ACC) deaminase, thus helping the plant tolerate various stress conditions (Pourbabaee et al. 2016). A BCA can alternatively secret lytic enzymes like proteases, amylases, lipases, chitinases, glucanases and cellulases which target and degrade the cell wall of pathogens (Subrahmanyam et al. 2020). A Bacillus sp. isolated from chilli rhizosphere produced appreciable levels of three mycolytic enzymes chitinase, glucanase and cellulase and showed antagonism against Colletotrichum gloeosporioides for management of anthracnose disease of chilli (Ashwini and Srividya 2014). Similar studies were undertaken by Nguyen et al. (2012), who reported increased activity of chitinase and β-1,3-glucanase in roots and surrounding rhizosphere soil of pepper plants treated with Streptomyces griseus. This resulted in suppression of Root Rot Disease cause Phytophthora capsici in the host plant. Microbial unregulated waste products such as Hydrogen cyanide (HCN) may also contribute to pathogen suppression by effectively blocking the cytochrome oxidase pathway. Volatile metabolite such as ammonia at a particular concentration has also been reported to be toxic to various fungal pathogens (Howell et al. 1988). Whereas other volatiles mainly alkenes, alcohols and ketones, are known stimulate plant growth by enhancing mineral uptake, modifying root structure and modulating hormone signalling. Bacterial volatiles also play important role in functions like bacterial motility, biofilm formation and induction of systemic resistance in the host plant (O’Brien 2017). Most of the times a BCA exhibit several of the above mentioned traits to help the host plant in growth and disease suppression. Treatment of chilli plant with a Streptomyces sp. positive for production of protease, chitinase, Indole Acetic Acid (IAA), siderophore, ammonia and HCN and phosphate solubilization activity reduced the percentages of damping-off and root rot severity caused by Rhizoctonia solani and Macrophomina phaseolina (Alaa Fathalla and El-Sharkawy 2020). Shrestha et al. (2014) reported potential of Lactic acid bacteria (LABs) to colonise roots, produce indole-3-acetic acid (IAA) and siderophores and solubilise phosphate. These LABs showed the inhibition of bacterial pathogens Xanthomonas campestris pv. vesicatoria and Ralstonia solanacearum which are the causative agents of leaf spot disease and wilt in Capsicum annuum. Apart from all these secondary metabolites, the major reason for antagonism is the production of antibiotics by BCAs. These are chemically heterogeneous group of organic, low-molecular weight antimicrobial compounds that hamper the growth or metabolism of the target microorganism at a particular concentration (Thomashow et al. 1997). Table 4 enlists some of the antimicrobial compounds produced by BCAs against pathogens affecting chilli plant. Each of these compounds have a different mode of action, thus some organisms are susceptible to certain antibiotics but others are not, depending on the specific moiety of cellular constituent the antibiotic attacks (Ulloa-Ogaz et al. 2015). Vegetative Catalase protein (KatA) produced by a Bacillus sp. induced abnormal conidial swelling and elongation and rupture of hyphae of Colletotrichum capsici thus suppressing the anthracnose disease of chili pepper (Srikhong et al. 2018). Wu et al. (2019) suggested that the lipopeptides produced by a Bacillus sp. inhibited mycelial growth of Rizoctonia solani, thus assisting in the suppression of disease symptoms in chilli plant. Another antimicrobial compound Gliotoxin exhibited anti oomycete activity against Phytophthora capsici thus suppressing blight in chilli (Tomah et al. 2020). Whereas the study by Ko et al. (2009) suggested that the inhibition of Phytophthora capsici by 4-hydroxyphenylacetic acid produced by Lysobacter antibioticus could be due to the deformation, lysis, and bending of hyphae of the fungus. Some antibiotics such as fusaricidin have been also known to induce systematic reistance in host (chilli) to suppress Phytophthora blight (Lee et al. 2013). Similar results were reported by Sundaramoorthy et al. (2012) wherein the synthesis of phytolaexins by Bacillus subtilis induced systemic resistance against wilt disease caused by Fusarium solani in chilli. Cell free supernatant of Paenibacillus polymyxa containing 3-hydroxy-2-butanone and 2,3-butanediol showed wrinkles on mycelia of Colletotrichum scovillei which causes anthracnose in chilli (Suprapta et al. 2020). Antimicrobial compound Phenazine-1-carboxamide produced by Pseudomonas aeruginosa showed deformation of mycelia and inhibition of sporulation thus inhibiting the growth of fungal pathogen Colletotrichum capsici causative agent of fruit rot in chilli (Kumar et al. 2005).
Conclusion
Biological control agents (BCAs) have generated great enthusiasm as safe and sustainable plant protection tool but still make up only a small percentage of the chilli crop protection market due to lack of availability of formulated products. There is a need for more extended biocontrol research and better understanding of the mechanisms involved in the antagonistic abilities of microbial BCAs so as to improve its efficacy, stability and consistency in fields. The present review identifies potential microbial BCAs with inhibitory activity against various fungal, bacterial and viral pathogens infecting the chilli crop. This review also gives us insight of how BCAs (single or consortium) employ several mechanisms (direct, indirect and mixed path antagonism) to act as an effective biocontrol agent against target pathogens and trigger different promotional effects on chilli plant growth parameters. Being from a natural source these BCAs are also safe to the environment and thus are a great alternative to replace chemical counterparts which are harmful to environment and ecology. Moreover, the field trials of chilli plants inoculated with these microbial BCAs have also proven its effect in-vivo. In conclusion, through thorough understanding of biocontrol activities of such microbes, multiple facets of disease suppression and plant growth promotion is revealed. This will thus aid in the achievement of the objective of commercialization of potential strains against the target pathogens and their implementation in the agriculture industry for protection of chilli plants.
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Pawaskar, M., Kerkar, S. Microbial biocontrol agents against chilli plant pathogens over synthetic pesticides: a review. Proc.Indian Natl. Sci. Acad. 87, 578–594 (2021). https://doi.org/10.1007/s43538-021-00053-2
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DOI: https://doi.org/10.1007/s43538-021-00053-2