Also, the interactions between plant-associated microbial communities and pathogens are not well understood, and our knowledge of the intimacy and decisiveness of such associations with respect to the behavior and survival of participating organisms is still in its infancy Trivedi et al. In general, pathogen triggers a cascade of reactions in plants, leading to the synthesis of defensive compounds which in turn enable it to withstand pathogen attack either directly e.
The altered conditions after the pathogen attack could have variable effects on the survival and proliferation of different groups of plant-associated microbes. For example, infection by Las Sagaram et al. Pathogen infection caused a decrease in the overall bacterial diversity in the infected host Trivedi et al. Interestingly, the abundance of bacteria belonging to Sphingobacterium was increased in the plants infected from Las and Phytoplasama Trivedi et al. Interestingly obligate endophytic pathogens have been reported to restructure the native microbial community even when a direct competition effect is lacking.
For example, significant changes in the microbial community structure of rhizosphere soil samples were observed in Las infected citrus Trivedi et al. In this case, alteration in plant physiology leading to quantitative and qualitative changes in partitioning the photo-assimilates was the primary cause of the shift in microbial diversity of the diseased host.
Typical rhizosphere inhibiting bacteria such as those belonging to Proteobacteria were significantly reduced in the infected plants suggesting that rhizosphere bacteria react more strongly to changes in plant physiology and exudation induced by pathogen infection.
Using Las and citrus huanglongbing as a model for pathogen—disease interactions that involve the blockage of vascular tissues, Trivedi et al. As the diversity and stability of the plant-associated microbial communities heavily influence soil and plant quality and ecosystem processes Nannipieri et al.
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In addition shrinking genetic and functional diversity in response to pathogen infection, will compromise the capacity of adaptive responses to further perturbation. These results pointed toward the beyond yield effect of plant diseases on ecosystem processes and suggested that in the long term, these fluctuations might have important implications for the productivity and sustainability of agro-ecosystems. Currently, the management of diseases caused by phytoplasma and Ca. Liberibacter species is commonly based on the control of the insects, i. It is well recognized that the use of chemical insecticides as the main control strategy is not sustainable, and is known to have negative side-effects, including both environmental and biological effects Qureshi and Stansly, ; Tiwari et al.
Based on information on the insect associated microbial community Crotti et al. Some first steps of MRM applications have been already carried out on insect vectors, with the aim of defining the microbial community composition and functionality within the insects Marzorati et al. Researchers have reported various potential biological control bacteria associated with insect vectors that can provide opportunities for controlling these economically important vectors, either through potential paratransgenesis or cytoplasmic incompatibility Powell and Tabachnick, The final aim is to propose a biocontrol approach based on the management of the microbial symbiont associated with the vector in order to counteract directly the pathogen or to reduce the vector competence.
This species has been reported to be associated with ACP and has been described as a pathogen of Lepidoptera, Coleoptera Samson, ; Shimazu and Takatsuka, and the greenhouse whitefly of the order Hemiptera Scorsetti et al.
Application of conidial based formulations of endophytic fungi Metarhizium anisopliae , Isaria fumosorosea and Hirstuella citriformis resulted in high mortality of vectors of Ca. Although the speed of kill caused by an entomopathogenic fungus is not comparable with that of a chemical insecticide, entomopathogenic fungi are known to reduce the feeding activity of infected hosts Avery et al. Further research is required before the true potential of controlling insect vectors by biocontrol agents can be realized.
Given the efficacy of biocontrol agents is reported to influenced by a range of parameters such as type of formulations, time and mode of applications and environmental and climate conditions, developing whole microbiome approach can potentially provide better disease control. However, this would require the development of effective tools to manipulate microbiome of the vector. Plant-associated microbes which improve the fertility status of soil and contribute in augmenting overall plant growth and health known as Plant Growth Promoting Microbes PGPM are receiving increased attention for use as microbial inoculants in agriculture Estrada-De Los Santos et al.
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This favors efficient establishment and survival of the introduced bacteria leading to increased performance and also does not affect the preexisting balance among indigenous populations. Mechanisms used by plant growth promoting microbes PGPM. Details of the assays shown to demonstrate beneficial activities are provided in the supplementary section. It has been noticed that certain trees called escape plants may survive in heavily infected areas under heavy load of pathogen and vector Sagaram et al.
Because these escape plants have the same genotype as susceptible plants and have developed under similar edaphic and climatic conditions, a possible explanation for the lack of disease symptoms may lie in the nature of the microbial community associated with these plants. In previous studies, it has been documented that specific endophytic bacterial communities are associated with these escape plants Sagaram et al.
Some of the bacteria isolated from these escape plants showed typical traits of potential biocontrol agents Bulgari et al. These isolates belonged to Pseudomonas , Bacillus , and Lysinibacillus species and have been previously developed as a carrier based bio-inoculant to increase plant productivity and health of various plant species Trivedi and Pandey, ; Trivedi et al. The research on screening effective biocontrol agents against obligate endophytic pathogens such as phytoplasma and Ca.
The widely used dual culture technique could not be applied to screen bacteria antagonistic to these obligate endophytes due to our inability to culture these bacteria. Trivedi et al. The selected novel isolates are further being tested in planta and in field conditions to determine whether they could be used in management of HLB. Beneficial soil-borne microbes can induce an enhanced defensive capacity in above-ground plant parts to protect plants against insect herbivores Figure 3.
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This induced systemic resistance ISR triggered by soil-borne microbes is often not associated with enhanced biosynthesis of plant hormones that are important for defense against insect herbivores, nor with massive changes in defense-related gene expression. Very recently, the concept of inducing enhanced resistance to phytoplasma with beneficial bacteria has been evaluated using Chrysanthemum as a model organism Gamalero et al.
Results showed that pretreatment with Pseudomonas putida S1Pf1Rif decreases the negative effects on plant growth infected with chrysanthemum yellows phytoplasma CYP , but had no effect on CYP viability and proliferation Gamalero et al. Co-inoculation of P. Musetti et al. The inconsistency in performance Bashan, ; Pandey et al.
Appropriate screening and the application of molecular tools to understand and manage the plant and insect associated microbiome can lead to new products or novel disease management strategies Box 1.
This fundamental knowledge can then pave the way to develop new products or tools for sustainable disease management. Box 1. Recent breakthroughs in sequencing technologies have provided concrete evidence that the number of microbial cells and the sum of their genetic information are numerically dominant than that of their host. Taken together, these interactions characterize the holobiont as a single and unique biological identity. Since that microbiome can adjust more rapidly and by more processes than the host genome to environmental dynamics including disease progression , it plays fundamental role in the adaptation and fitness of the holobiont Rosenberg and Zilber-Rosenberg, Mueller and Sachs have proposed a novel approach to improve animal and plant fitness by artificially selecting upon microbiomes, thus engineering evolved microbiomes with specific effects on host fitness.
The host-mediated microbiome engineering approach selects upon microbial communities indirectly through the host and leverages host traits that evolved to influence microbiomes Mueller and Sachs, Evidence that microbiome can be optimized for disease resistance by the application of phytohormones that activate defense responses is also available Lebeis et al. Generating host-mediated artificial selection of microbiomes may be a cheaper way to help curb plant and animal diseases rather than pesticides and antibiotics, or creating genetically modified organisms.
Sheth et al. Plant ecological engineering e.
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The research progress to better understand the interactions between obligate endophytic pathogens belonging to Ca. Liberibacter species and their hosts and vector has moved slowly because of the inability to isolate these fastidious bacteria on culture media.
Studies of plant—pathogen and insect—pathogen interactions are taking advantage from high-throughput techniques and also from the constant improvement of genome sequencing and annotations of both microbes and their hosts Mitter et al. However, there is lack of application of these techniques in the area of interaction between host, pathogens and biocontrol agents. Even the most intimate association between the pathogen and its host in the natural environment, whether occurring at the epiphytic or endophytic phase are influenced by a myriad of microbes that are intimately associated with plants or insects.
Although it is well documented that various groups of microbes can increase plant productivity in several important crops or defend against pathogen attacks, there are significant challenges that need to overcome in order to harness host associate microbes for sustainable disease management Box 2. Emerging technologies e. Furthermore, research on the host-associated microbial community, and its variability, would provide insights into the ecological behavior of pathogenic bacteria in the context of surrounding microorganisms present in the same niches.
Such knowledge on multi-trophic microbiome interactions has potential to be harnessed for development of more effective and sustainable management of vector-borne plant diseases. Microbiome approach to manage vector mediated plant disease has enormous potential but to achieve this goal, there are some key challenges that need to be solved by integrated fundamental and applied research. These priority challenges include:. All authors listed, have made substantial, direct, and intellectual contribution to the work, and approved it for publication.
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. Al-Sadi, A. Euphytica , — Antoun, H. Siddiqui Netherlands: Springer , 1— Google Scholar. Diversity of endophytic bacterial populations and their interaction with Xylella fastidiosa in citrus plants. Avery, P. Diaphorina citri Hemiptera: Psyllidae infection and dissemination of the entomopathogenic fungus Isaria fumosorosea Hypocreales: Cordycipitaceae under laboratory conditions.
Florida Entomol. Characterisation of entomopathogenic fungi used in the biological control programme of Diaphorina citri in Mexico. Biocontrol Sci. Bai, X. Living with genome instability: the adaptation of phytoplasmas to diverse environments of their insect and plant hosts. Bashan, Y. Inoculants of plant growth-promoting bacteria for use in agriculture.
Berg, G. Unraveling the plant microbiome: looking back and future perspectives. Bertaccini, A. Phytoplasmas and phytoplasma diseases: a severe threat to agriculture. Plant Sci. Bourtzis, K.go to link
Insect Symbiosis. Phloem-and xylem-restricted plant pathogenic bacteria. Buchner, P. Endosymbiosis of Animals with Plant Microorganisms. Bulgarelli, D. Structure and functions of the bacterial microbiota of plants.