Phyllospheric Microbiomes: Diversity, Ecological Significance, and Biotechnological Applications
- 182 Downloads
The phyllosphere referred to the total aerial plant surfaces (above-ground portions), as habitat for microorganisms. Microorganisms establish compositionally complex communities on the leaf surface. The microbiome of phyllosphere is rich in diversity of bacteria, fungi, actinomycetes, cyanobacteria, and viruses. The diversity, dispersal, and community development on the leaf surface are based on the physiochemistry, environment, and also the immunity of the host plant. A colonization process is an important event where both the microbe and the host plant have been benefited. Microbes commonly established either epiphytic or endophytic mode of life cycle on phyllosphere environment, which helps the host plant and functional communication with the surrounding environment. To the scientific advancement, several molecular techniques like metagenomics and metaproteomics have been used to study and understand the physiology and functional relationship of microbes to the host and its environment. Based on the available information, this chapter describes the basic understanding of microbiome in leaf structure and physiology, microbial interactions, especially bacteria, fungi, and actinomycetes, and their adaptation in the phyllosphere environment. Further, the detailed information related to the importance of the microbiome in phyllosphere to the host plant and their environment has been analyzed. Besides, biopotentials of the phyllosphere microbiome have been reviewed.
KeywordsBiotechnological applications Diversity Ecological significance Phyllospheric microbiomes Plant growth promotion
The term phyllosphere is referred to as “the aerial part of the plant or the parts of a plant above the ground usually surface of leaves, considered as a habitat for microorganisms.” This is a place where normally a variety of microorganism (bacteria, yeasts, and fungi) colonizes. The global leaf area corresponds to both upper and lower surfaces, has approximately twice as great as the land surface area (Vorholt 2012). The phyllosphere is the ambient region for microbes to colonize and establish its association with plants usually epiphytes. Microbial communities in the phyllosphere are highly complex and consist of many cultured and uncultured microorganisms (Müller and Ruppel 2014). It has a heterogeneous group of the microbial association at the micrometer scale area due to its diverse microenvironments (habitats). The phyllospheric microbes are adapted to the insensitive environmental conditions, specifically microbial epiphytes are highly exposed to atmospheric temperature, light, UV radiation, less water, and nutrient availability. These external factors affect the composition and diversity of phyllospheric microbial communities (Vorholt 2012). However, the type of plant and invading microbial populations (pathogens) are also influencing the commensals and/or mutualistic relationship with their host plant (Lindow and Brandl 2003). Less number of studies are available for the microbiology of phyllosphere rather than plant root. Moreover, with increasing anthropogenic stresses, the diversity and community structure of phyllosphere microflora have been continually modified. In this chapter, we focused on the phyllospheric microbiome, structure and diversity, epiphytic mechanism, molecular interactions, ecological significance, and the microbial importance in biotechnology.
5.2 Basic Understanding of Leaf Structure
Glandular trichome of the epidermis releases a wide spectrum of leaf exudates, such as polysaccharide salts, lipids, volatile compounds, and proteins, and its function is associated with plant–microbe and plant–insect interactions (Hirano and Upper 1983). But, non-glandular trichome involves regulation of water tension, light absorption, and protect the leaf from UV radiation and heat as well as drought tolerance (Hirano and Upper 1983).
5.3 Phyllosphere Habitat
The phyllosphere is a unique and dynamic habitat which constitutes irregular, and sometimes relatively large microbial community inhabitant in the ecosystem (Whipps et al. 2008). The total terrestrial phyllosphere area estimated is around 6.4 × 108 km2 (Morris and Kinkel 2002), and it exhibits numerous microhabitat which represents a major source of microorganism. Variety of bacteria, filamentous fungi, and yeasts are naturally colonized on the phyllosphere region and less frequently, protozoa and nematodes. These microorganisms exhibit commensalism and/or mutualism (symbionts) or antagonism type of relationship on their host plants. The microbial association in phyllosphere has several advantages and importance to global processes including biogeochemical cycles (carbon and nitrogen) and environmental impact.
5.3.1 Microbial Assembly on Leaf
5.4 Microbial Diversity in the Phyllosphere
The cultivable yeasts genera such as Cryptococcus, Sporobolomyces, and Rhodotorula and its species have been largely inhabitant in the plant leaf (Thompson et al. 1993; Glushakova and Chernov 2004). Moreover, the culture-dependent methods have been used to study the abundance of filamentous fungi, ranging from 102 to 108 CFU g−1. Genera such as Cladosporium, Alternaria, Penicillium, Acremonium, Mucor, and Aspergillus are the frequent filamentous fungi colonizing as epiphytes and endophytes (Arnold et al. 2000; Inacio et al. 2002; Rana et al. 2019a, b, c).
However, the culture-independent strategy is the best to investigate the diversity and distribution of specific bacterial groups of interest (Miyamoto et al. 2004; Sessitsch et al. 2006). Other than the 16S/18S rDNA sequences, multiplex terminal restriction fragment length polymorphism (TRFLP) has been used to analyze several phylogenetic groups or functional genes in the microenvironment (Singh et al. 2006). Soils, water, air, tree buds, and plant debris from the previous crops are the sources for microbes in phyllosphere (Manceau and Kasempour 2002). Those microorganisms may be habited in phyllosphere either transient or residual epiphytes (Suslow 2002; Zak 2002). The atmospheric microflora, rainfall, humidity, wind, etc. can directly influence the transients of microorganisms to the phyllosphere (Lighthart 1997). During the plant growth period, the epiphytic bacterial population will increase in quantity (Inacio et al. 2002). The microorganisms on the seed or roots may be established as epiphytes or endophytes (Wulff et al. 2003). Some epiphytes may be injected into the internal space of the leaf and colonize as endophytes. The distribution pattern of the phyllosphere microorganisms is not even, mostly bacteria colonize at the epidermal wall junctions, specifically in the grooves and the veins or stomata or at the base of trichomes (Melotto et al. 2008), also found in the cuticle layer, near hydathodes and stomatal pits (Aung et al. 2018). The microbial load is higher at the lower leaf surface perhaps the lower leaf surface contains thin cuticle, stomata, and/or trichomes (Beattie and Lindow 1999). Mostly, all microorganisms that appear in the phyllosphere are capable to colonize and grow (Whipps et al. 2008), and it disperses throughout the surface by rain splash, bounce-off, wash-off, water movement, or removal by insects or pest (Kinkel 1997; Yang et al. 2001; Lambais et al. 2006).
5.4.1 Bacterial Diversity in the Phyllosphere
Phyllosphere is a heterogeneous environment (Koskella 2013), bacteria are considered the most abundant inhabitants of the leaves, and its average number is being around 106–108 cells cm−2 (Andrews and Harris 2000; Hirano and Upper 2000). But the population of epiphytic bacteria differs depending on the plant species and its surrounding environment. The variation is mainly due to the physical and nutritional conditions of the phyllosphere. Commonly, the broad-leaf plants have the highest number of bacteria than the grasses or waxy broad-leaf plants (Kinkel et al. 2000).
Generally, the phyllosphere contains four major phyla of bacteria such as the Proteobacteria, Firmicutes, Bacteroides, and Actinobacteria (Kembel et al. 2014; Durand et al. 2018). Methylotrophic bacteria are predominant in phyllosphere which includes genera such as Methylobacterium, Methylophilus, Methylibium, Hyphomicrobium, Methylocella, Methylocapsa, and Methylocystis (Mizuno et al. 2013; Iguchi et al. 2013; Kwak et al. 2014; Krishnamoorthy et al. 2018). Methylobacterium and Sphingomonas are the predominant genera belonging to the class alphaproteobacteria reported in several plant phyllospheres (Delmotte et al. 2009; Kumar et al. 2019a). The bacterial community organization on phyllosphere is controlled by specific assemblage regulations (Buee et al. 2009; Reinhold-Hurek et al. 2015). Normally, soil type, plant genotype and species, immune system of the plant, age, climatic condition, and the geographic region are the factors forcing the bacterial community assembly (Leff et al. 2015; Zarraonaindia et al. 2015; Copeland et al. 2015). Extensive studies are available for the soil and rhizosphere bacterial community on phyllosphere bacterial colonization in Arabidopsis thaliana (Bodenhausen et al. 2013; Maignien et al. 2014; Bai et al. 2015; Muller et al. 2015) and maize (Peiffer et al. 2013). Proteobacteria, Actinobacteria, and Bacteroidetes are the most abundant phyla colonizing the leaf and root of A. thaliana (Delmotte et al. 2009; Redford et al. 2010; Bodenhausen et al. 2013). Massilia, Flavobacterium, Pseudomonas, and Rathayibacter are a prevalent bacterial genus in A. thaliana (Bodenhausen et al. 2013), Deinococcus thermus on tree phyllosphere (Redford et al. 2010), and Bacillus and Pantoea dominate the lettuce (Rastogi et al. 2012).
Kembel et al. (2014) studied the bacterial communities on tropical tree leaves, around 400 bacterial taxa the phyllosphere has been dominated with Actinobacteria, Alpha-, Beta-, and Gammaproteobacteria, and Sphingobacteria. However, Archaea is the profuse members of the plant-associated microbe, commonly Thaumarchaeota, Crenarchaeota, and Euryarchaeota make the endophytic mode of life in plants (Müller et al. 2015). Durand et al. (2018) characterized the bacterial genera such as Methylobacterium, Kineococcus, Sphingomonas, and Hymenobacter of the phylum Firmicutes from the leaf surface. The phyllosphere of the grapevine contains Acinetobacter, Bacillus, Citrobacter, Curtobacterium, Enterobacter, Erwinia, Frigoribacterium, Methylobacterium, Pantoea, Pseudomonas, and Sphingomonas as dominant genera (Kecskeméti et al. 2016). Steven et al. (2018) characterized Pseudomonas and Enterobacteriaceae as predominant taxa from apple. Several studies revealed Pseudomonas as the most abundant genus of phyllosphere region (Aleklett et al. 2014; Kecskeméti et al. 2016; Steven et al. 2018). Seed coat associated bacteria that have been reported in phyllosphere are mainly Actinobacteria, Bacteroidetes, Firmicutes, and Proteobacteria (Johnston-Monje and Raizada 2011; Rodríguez-Escobar et al. 2018).
The most notable bacterial pathogen is Pseudomonas syringae, it causes diseases in a wide range of economically important plant species (Mansfield et al. 2012; Morris et al. 2013; Burch et al. 2014). Hamd Elmagzob et al. (2019) identified taxa such as Rhizobiales, Clostridiales, Pseudomonadales, Burkholderiales, Bacteroidales, Enterobacteriales, Rhodocyclales, Sphingomonadales, Lactobacillales, and Bacillales from the leaves of Cinnamomum camphora (L.) Presl. Several studies reported diazotrophic bacteria on phyllosphere (Fürnkranz et al. 2008; Rico et al. 2014). Diazotrophic bacteria can use atmospheric dinitrogen (N2) as nitrogen source for its metabolic activities. Bacterial diazotrophic include Beijerinckia, Azotobacter, Klebsiella, and Cyanobacteria (e.g., Nostoc, Scytonema, and Stigonema). Diazotrophic nitrogen fixation has been reported in many species which contains an enzyme nitrogenase (encoded by nif genes) (Rico et al. 2014). Recently, 16 s rRNA gene-based high-throughput sequencing technology has been used for the diversity analysis of phyllosphere, for example, the distribution of endophytic bacteria of C. camphora (L.) Presl leaves has been analyzed by 16S rRNA gene metagenomics, revealing Proteobacteria, Firmicutes, Bacteroidetes, Actinobacteria, Gemmatimonadetes, Acidobacteria, Planctomycetes, Chloroflexi, and Fusobacteria are the major phyla of the polymicrobial community (Hamd Elmagzob et al. 2019).
5.4.2 Fungal Microbiota of Phyllosphere
Fungi are saprophytic and they may be associated with plants either epiphytic or endophytic, and mostly they are known for their pathogenesis on plant system (Voříšková and Baldrian 2013; Yadav et al. 2019b, c, d). There are several reports revealed that phyllosphere fungi have a profound role in the residing host. Both epiphytic and endophytic fungi inhabiting the leaf are of high species diversity with diverse metabolic functions (Yao et al. 2019), such as leaf litter decomposition and recycling the carbon and nitrogen (Kannadan and Rudgers 2008; Guerreiro et al. 2018). In general, endophytic fungi can help plant growth and also provide resistance to biotic (pathogens) and abiotic (drought and salinity) stresses, (Arnold et al. 2007; Purahong and Hyde 2011; Guerreiro et al. 2018; Yadav et al. 2018c). In culture-dependent approaches, several fungal species have been isolated from small herbs to larger woody plants. Inácio et al. (2010) reported that the density of yeast-like fungi may vary from plant to plant and approximately 5 × 104 cells cm−2. Aureobasidium pullulans are yeast-like fungi abundant in phyllosphere (Cordier et al. 2012; Setati et al. 2012). Apart from yeast-like fungi, many filamentous fungi have been reported from health as well as infected plant leaves. Through the culture-dependent method, Ripa et al. (2019) isolated Aspergillus niger, Fusarium oxysporum, Penicillium aurantiogriseum, Fusarium incarnatum, Alternaria alternata, Alternaria tenuissima, Cladosporium cladosporioides, Talaromyces funiculosus, Aspergillus flavus, Trichoderma aureoviride, Trichoderma harzianum, Penicillium janthinellum, Fusarium proliferatum, Fusarium equiseti, and Aspergillus stellatus from wheat plant.
Phyllosphere fungal endophytes
Aspergillus, Phomopsis, Wardomyces, Penicillium
Euterpe oleracea (palm)
Vitis riparia (grapevine)
Kernaghan et al. (2007)
Absidia sp., Aspergillus sp., Cladosporium sp., Cunninghamella sp., Fusarium sp., Nigrospora sp., Paecilomyces sp., Penicillium sp., Rhizopus sp.,
Meyna spinosa Roxb.
Bhattacharyya et al. (2017)
Penicillium chrysogenum, and Penicillium crustosum
El-Din Hassan (2017)
Alternaria alternata, Setosphaeria sp., Cochliobolus sp., Alternaria sp. Phoma herbarum, Davidiella tassiana, Botryosphaeria dothidea, Ulocladium alternariae, Phoma macrostoma var. incolorata, Phoma exigua var. exigua, Cladosporium cladosporioides strain, Botryosphaeria sp., Guignardia mangiferae, Pyrenophora tritici-repentis, Guignardia alliacea, Rhizopus oryzae
Sreekanth et al. (2017)
Ascomycetes: Trichoderma, Penicillium, Fusarium, and Aspergillus. Non-ascomycetes: Mucor (Mucoromycota) and Schizophyllum (Basidiomycota)
Salazar-Cerezo et al. (2018)
Trichothecium sp., Epicoccum nigrum, Alternaria alternaria, Alternaria arborescens, Nigrospora sphaerica, Epicoccum sp., Alternaria sp. Nigrospora sp., Colletotrichum gloeosporioides, Fusarium oxysporum, Trichothecium roseum
Vitis vinifera (Grape fruit cells)
Huang et al. (2018)
Euphorbia indica L.
Ismail et al. (2018)
Alternaria spp., Trichophyton spp., Geotrichum spp., Candida spp., Aspergillus spp., Aureobasidium spp., Fusarium spp., Exserohilum spp., Curvularia spp., Coccidioides spp., Bipolaris spp.
Epipremnum aureum, Azadirachta indica, Piper betle, Catharanthus roseus, Ficus religiosa, Musa acuminate, Ficus Benghalensis, Ficus racemosa, Calotropis procera, Ocimum tenuiflorum
Jariwala and Desai (2018)
Nigrospora sphaerica, Acremonium falciforme, Allomyces arbuscula, Penicillium chrysogenum, Acrophialophora sp, Mycelia sterilia
Deka and Jha (2018)
Colletotrichum gloeosporioides f. sp. camelliae and Pleosporales sp.
Win et al. (2019)
Tremellales, Davidiellaceae, Basidiomycota, Rhodotorula, Tremellales, Meria, Cryptococcus, Cladosporium, Acaromycetes, Erythrobasidium, etc.
Aegiceras corniculatum (Myrsinaceae), Avicennia marina (Verbenaceae), Bruguiera gymnorrhiza, Kandelia candel and Rhizophora stylosa (Rhizophoraceae), and Excoecaria agallocha (Euphorbiaceae)
Yao et al. (2019)
Osono (2008) reported that endophytic Colletotrichum gloeosporioides and C. acutatum, and epiphytes Pestalotiopsis sp., Aureobasidium pullulans, Phoma sp., and Ramichloridium sp. are the phyllosphere fungi in the plant Camellia japonica. However, the abundance and diversity of the fungi differ in plant species as well as in different eco-climatic conditions. Moreover, seasonal and leaf age-dependent variations also occur in the epiphytic and endophytic phyllosphere fungal assembly, for example, Geniculosporium sp. is varied in leaf age, and Cladosporium cladosporioides has been varied in both season and leaf age of the plant Camellia japonica (Osona 2008). Phyllosphere fungi play an important function in mineral absorption and mineral recycling process, specifically carbon, nitrogen, and phosphorus recycling in the forest ecosystem. Therefore, the study about the phyllosphere fungi and its physiology with host plant is important.
5.4.3 Actinomycetes Diversity in Phyllosphere
Diversity of endophytic actinobacteria
Microbispora sp., Micromonospora sp., Nocardioides sp., Streptomyces sp.,
Coombs and Franco (2003)
Chen et al. (2009)
Actinoallomurus acaciae, Streptomyces sp., Actinoallomurus coprocola, Amycolatopsis tolypomycina, Kribbella sp., Microbispora mesophila
Thamchaipenet et al. (2010)
Actinomadura glauciflava, Pseudonocardia halophobica, Nocardia alba, Nonomuraea rubra, Streptomyces javensis
Nimnoi et al. (2010)
Indananda et al. (2011)
Xie et al. (2011)
Micromonospora sp. Nonomuraea sp., Pseudonocardia sp., Planotetraspora sp.
Chen et al. (2011)
Bian et al. (2012)
Wang et al. (2013b)
Actinoplanes hulinensis, Streptomyces harbinensi, Wangella harbinensis
Li et al. (2013)
Qin et al. (2013)
Kaewkla and Franco (2013)
Blastococcus endophyticus, Plantactinospora endophytica
Zhu et al. (2013)
Actinoplanes brasiliensis, Couchioplanes caeruleus, Gordonia otitidis, Micrococcus aloeverae, Streptomyces zhaozhouensis
He et al. (2014)
Micromonospora schwarzwaldensis Streptomyces sp., Wenchangensis
Ernawati et al. (2016)
Glutamicibacter halophytocola, Kineococcus endophytica, Streptomyces sp.,
Feng et al. (2017)
Jiang et al. (2017)
Huang et al. (2017)
Kaewkla et al. (2017)
Nocardiopsis sp., Pseudonocardia sp. Streptomyces sp.,
Salam et al. (2017)
Liu et al. (2017)
Actinoplanes sp., Agrococcus sp., Amnibacterium sp., Brachybacterium sp., Brevibacterium sp., Citricoccus sp., Curtobacterium sp., Dermacoccus sp., Glutamicibacter sp., Gordonia sp., Isoptericola sp., Janibacter sp., Kocuria sp., Leucobacter sp., Mycobacterium sp., Micrococcus sp., Nocardioides sp., Kineococcus sp., Kytococcus sp., Marmoricola sp., Microbacterium sp. Micromonospora, sp., Nocardia sp., Nocardiopsis sp., Pseudokineococcus, sp., Sanguibacter sp., Streptomyces sp., Verrucosispora sp.,
Avicennia marina, Aegiceras corniculatum, Kandelia obovota, Bruguiera gymnorrhiza, and Thespesia populnea
Jiang et al. (2018)
Zhang et al. (2018)
5.5 Mechanism of Microbial Interaction with the Phyllosphere
The leaf physiology determines the microbial diversity and abundance on the phyllosphere. It establishes the microhabitat where the microorganisms adapt to their physiology to survive in this habitat (Staley et al. 2014; Shiraishi et al. 2015). The epiphytic microbes formed as colonial form, which gives protection to the microorganisms from this harsh microhabitat (Lindow and Brandl 2003; Remus-Emsermann et al. 2012). Commonly, bacteria develop larger sized colonial association on the leaf surface, especially at veins as well as the groves of epidermal cells (Morris et al. 1997; Hirano and Upper 2000). The epidermal grooves are rich in nutrients specifically sugar and water. This region is less waxy cuticle, usually the leaf surface is fully coved with waxy cuticle which prevents the permeability and wettability of the leaf surface and regulates the colonization of the microbes on phyllosphere (Lindow and Brandl 2003; Burch et al. 2014).
The leaf surface water droplets diffuse the waxy cuticle and improve the permeability by which the compounds are diffused from the apoplast to phyllosphere surface (Schreiber 2005). These leached compounds and water on the phyllosphere are making the availability of nutrients to the microorganisms. Most commonly, the flow of water from the stomata (transpiration) is increasing the permeability and wettability of guard cells and its surface cuticles (Schönherr 2006). Hence, higher permeation of the cuticle layer permits the microbes to colonize densely (Krimm et al. 2005). Moreover, the surface bacteria are able to produce certain compounds like biosurfactants (syringafactin produced by Pseudomonas syringae) (Krimm et al. 2005; Burch et al. 2014) which can modify the cuticle surfaces of the leaf and establish its association. This can facilitate water availability and alter sugar availability that can improve living conditions for epiphytic bacterial growth (Lindow and Brandl 2003; Van der Wal and Leveau 2011). Epiphytes such as Pseudomonas sp., Stenotrophomonas sp., and Achromobacter increase the water permeability of the lipophilic cuticle present in Hedera and Prunus, which increases the availability of the compounds at the phyllosphere which will improve the epiphytic fitness on the leaf surface (Schreiber et al. 2005).
It has been experimentally proved in the bean phyllosphere containing fructose facilitates the growth of Erwinia herbicola and Pantoea agglomerans (Remus-Emsermann et al. 2013; Tecon and Leveau 2016). However, irregular distribution of fructose differentially promotes the P. eucalypti population on bean leaves (Mercier and Lindow 2000; Leveau and Lindow 2001; Remus-Emsermann et al. 2011). These studies suggested that the permeated carbon sources on the leaf surface are merrily exploited by the epiphytic microorganisms for their growth and multiplication. At the same time, the phyllosphere microbial population can influence the modulation of the physicochemical properties of the leaf with the help of both biotic and abiotic surroundings (Bringel and Couée 2015; Ohshiro et al. 2016; Quan and Liang 2017). Soil microbial community may also influence the determination of phyllosphere microbial diversity. However, the microbes can construct the niches in the phyllosphere microhabitat wherein it can sustain and establish its population steadily (Agler et al. 2016; San Roman and Wagner 2018). Recent studies revealed the special relationships between the bacterial species in the phyllosphere community. Presence of sugars and nutrients in this environment significantly change the individual bacterial cells within the microbial aggregates (Fig. 5.2) would spatially be established with cell-to-cell interactions along with direct physical interactions (Levy et al. 2018; Tecon et al. 2018). The community structure is organized based on the driven factors such as dispersal, selection of microbes, diversification, and ecological drift. The fitness of the community is due to internal (strain types) and external determinants (environment) of the phyllosphere (Schlechter et al. 2019).
In general, the internal factors of the community are based on the microbial relationship within the aggregates. The microbes usually have either commensal or antagonistic or mutualistic or cooperative association by which the community structure can be established. Both cooperative and mutualistic microbial interactions shape the community structure as well as to develop larger colonial association containing the maximum microbial population. While commensals have weak interactive partners in the community, they are randomly distributed in the habitat. The commensals should not influence the interactive association within the structured community (Stubbendieck et al. 2016). Besides, antagonistic microbes have a negative interaction within the community, one can outcompete the other and the sensitive microbes have been eliminated from the environment. The effect of cooperative microbial interactions on the phyllosphere community structure establishment is not demonstrated (Schlechter et al. 2019).
Bacteria can ascertain the cell-to-cell communication system and establish a larger community structure with heterogeneous populations, usually with mutualistic and cooperative partners. However, some kind of mutualistic relationship may occur between rapid growing bacteria and pathogenic fungi, which leads to cause superficial infection on the host plant which increases the nutrient accessibility of the bacteria to rich its population (Suda et al. 2009; Zeilinger et al. 2016; Amine Hassani et al. 2018). Inversely, fungal–fungal interactions seem to decrease the bacterial population, for example, oomycete species Dioszegia sp. and Albugo sp. outcompete the bacterial microbiota on A. thaliana leaf (Chou et al. 2000; Agler et al. 2016). Moreover, competitive interactions of microbes involve negative effects on at least one species of the habitat. Some competitive microbes produce certain toxic chemical substances (antibiotics and siderophores) as secondary metabolites which pose a negative effect on its competitor microbes. The best example of such interaction is a gram-negative Pantoea agglomerans bacteria which inhibit the growth of Erwinia amylovora, a phytopathogen of apple by antibiotic activity (Wright et al. 2001; Pusey et al. 2011).
Generally, the competition of microbes is mainly for their nutrition and space. The phyllosphere is a nutrient-limited environment, wherein the competitive partner has compromised their growth by either coexisting or excluded from the site (Saleem et al. 2017). Besides, the phyllosphere is greatly colonized by both oligotrophic and competitive microbes which play an important role in community structure formation (Schlechter et al. 2019). However, the key factors of the phyllosphere community assemblage are currently vague. Hence, more studies required to find the key factors determining the phyllosphere community structure assemblage.
5.6 Factors Controlling Phyllosphere Microbiomes
Once microbes arrived at the phyllosphere, a variety of factors resolve whether microbial cells are competent to colonize the leaf and become confined. Colony establishment depends on the leaf–atmosphere environmental interaction with the residing microorganisms in the phyllosphere. At the beginning, the microbe reaches the cuticle layer, a waxy surface that protects the leaf from the pathogens. In general, cuticle restricts the microbial association due to the functions such as barrier, reducing water and solute lass, aqueous pollution, reflectance to minimize the temperature, conferring water repellent, etc. (Beattie 2002; Whipps et al. 2008). The whole-cell biosensor-based study revealed the available nutrients on the leaf surface facilitate the growth of residing microbes at a limited level (Miller et al. 2001). This was confirmed by the microscopic observation of leaf surfaces, at the low nutrient region contains less dense microbial colonization than the nutrient-rich surface (Monier and Lindow 2005). Naturally, nutrient enrichment may happen by pollen deposits and honeydew at the phyllosphere surface (Lindow and Brandl 2003), besides plant leaves release a large array of volatile organic substances into the margin layer around leaves (Jackson et al. 2006). Nutrients that include CO2, acetone, terpenoids, aldehydes, alcohols, long-chain hydrocarbons, sesquiterpenoids, and nitrogen-containing compounds (Whipps et al. 2008) are available nutrients for microbial growth. Some of the compounds may act as growth inhibitor or toxic to microbial growth (Dingman 2000; Shepherd et al. 2005). Hence, microbes establish several adaptive mechanisms for maintaining their growth in adverse conditions.
5.6.1 Microbial Adaptations in Phyllosphere Environment
Microbes like bacteria establishing colonies at the phyllosphere are limited by various factors including both biotic and abiotic. Abiotic factors such as the available nutrient (Delmotte et al. 2009), seasonal variation, rainfall, temperature, plant immunity, and competitor microbes (Rastogi et al. 2013) are influencing surveillance of microbes in the phyllosphere. Metaproteomic studies on the leaf surface communities have been identified as microbes producing vitamins and siderophores which give adaptation to the microbes at the environment. For example, phyllosphere of soybean, clover, and Arabidopsis plants largely colonized by Sphingomonas and Methylobacterium provides vitamins and siderophores to the plant (Green 2006; Delmotte et al. 2009) and it competes for other microbes. Methylobacterium spp. are involved in the assimilation of methanol at the phyllosphere, a by-product of demethylated pectin during the cell wall metabolism of the plant (Galbally and Kirstine 2002; Delmotte et al. 2009), and it gives epiphytic fitness to the microbes. Proteome studies revealed that some unique properties of rhizosphere bacteria have been found in the phyllosphere microbiota. For example, genes of methanol dehydrogenase and formaldehyde-activating enzyme (of Rhizosphere Methylobacterium spp.) and nitrogen fixation (Rhizobium sp.) are also reported in both phyllosphere and rhizosphere samples of rice (Knief et al. 2012). Gourion et al. (2006) observed upregulation of methylotrophic proteins such as MxaF and Fae and stress-related protein PhaA during epiphytic growth of Methylobacterium extorquens.
Phyllosphere colonization may occur in two different habitats, (1) the surface (epiphytic) and (2) the apoplast or leaf interior (endophytic). During the epiphytic life, many of the environmental factors regulate the growth such as solar radiation, temperature, water availability, nutrient, humidity, etc., whereas the endophytes are challenged with a plant defense mechanism. A bacteria colonizing at both habitats may differentially express their genes, for example, P. syringae pv. syringae B728a at epiphytic growth express the genes involved in motility, chemosensing, phosphate mobilization, and utilization of tryptophan which is higher than in endophytic growth (Yu et al. 2013). However, the secondary metabolite (syringomycin, syringopeptin) production was higher in the endophytic stage. One such adaptation is the production of pigments, bacteria such as Pseudomonas, Sphingomonas, and Methylobacterium produce pigmentation by which they give protection against UV light (Lindow and Brandl 2003). Presence of extracellular polysaccharide is another protective measure of plant-bacteria against desiccation and osmotic stress (Monier and Lindow 2004). Delmotte et al. (2009) found several stress-resistant proteins (PhyR and EcfG) from the phyllosphere of soybean, clover, and Arabidopsis through metaproteogenomic survey. Flagellin-like protein is high in pseudomonas at the epiphytic growth which enables the bacteria to access the nutrition by the chemostatic model (Yu et al. 2013).
5.6.2 Plant Immunity/Responses to Control Microbial Colonization
Mode of life cycle of pathogen established against plant immunity
Ding et al. (2011)
Biotrophic and necrotrophic
Vargas et al. (2012)
Yang et al. (2013)
Jupe et al. (2013)
Gan et al (2013)
Hemibiotrophic and necrotrophic
Meinhardt et al. (2014)
Lanubile et al. (2014)
Van Kan et al. (2014)
Biotrophic, hemibiotrophic, and necrotrophic
Kabbage et al. (2015)
Rudd et al. (2015)
Zuluaga et al. (2016)
Foley et al. (2016)
Signaling pathway inhibits pathogenic microbes in phyllosphere
Miranda et al. (2007)
Jasmonic acid, ethylene, and the flavonoid
Uppalapati et al. (2009)
Methyl jasmonate and ethylene
Gaige et al. (2010)
Jasmonic acid and ethylene
Sun et al. (2010)
Jasmonate and ethylene
Gottwald et al. (2012)
Ethylene and jasmonate
Shin et al. (2014)
Methyl jasmonate, 12-oxo-phytodienoic acid, salicylic acid, and flavonol
Fusarium oxysporum f.sp. lycopersici
Krol et al. (2015)
Phyllosphere region is usually colonized by a variety of microorganisms. Naturally, leaf epidermises are always contacted to external and internal environments and are enriched with a diverse group of bacteria, yeast, fungi, and viruses. The cuticle layer of the leaf surface plays a significant role during the contact with leaf microbiota (Vacher et al. 2016). Though some group of microorganism may not multiply after it reaches on the surface, many continue to survive and multiply, until they can attain maximum number (Schönherr 2006; Innerebner et al. 2011; Pusey et al. 2011). To multiply, microorganisms require carbon, nitrogen, inorganic, and organic energy sources. However, in the absence of such nutrients, phyllosphere is still usually colonized by a large number of bacteria (105–107 CFU/g of the leaf) in the presence of high relative humidity and free water at suitable environmental conditions (Schönherr 2006; Baldwin et al. 2017). This is due to the release of nutrients or leaf exudates which adequately supported the microbial growth. There are varieties of molecules leached from the plant leaves such as sugar, amino acids, organic acids, minerals, etc. (Beattie 2011; Remus-Emsermann et al. 2011; Meiners et al. 2017). These leaching materials may differ with plant species and the environmental condition (Beattie 2011; Remus-Emsermann et al. 2011; Mendes et al. 2013).
Nutrients such as sugar photosynthates from the leaf interior may be diffused through the cuticle reached the outer surface (Schreiber 2005), and are chiefly used by phyllosphere bacteria. Moreover, water droplets on a leaf surface facilitate the outward diffusion of these sugars (Van der Wal et al. 2013). Both non-pathogenic and pathogenic microorganisms establish colonization on the leaf surface. To survive and thrive, epiphytic microbes have several adaptive properties such as the production of antibiotics, extracellular polymeric substances (EPS), biosurfactant for increasing cuticle permeability, and availability of nutrients volatile organic compounds (VOCs) to the leaf surface. However, in order to avoid the entry of pathogens, plants develop defense reactions. The preliminary defense is activated by recognition of the chemical compounds released during the contact with microbes (Boller and Felix 2009). Pathogen-induced molecular patterns (PAMPs)-triggered immunity (PTI) is a broad spectrum of defenses against the pathogen invades. However, effectors produced by the pathogens often interfere with PTI activation and are recognized by specific proteins, which stimulate effector-triggered immunity (ETI) that induces a hypersensitive response (Craig et al. 2009).
5.7 How to Study Phyllosphere Microbiome?
Advancements in molecular techniques, next-generation DNA sequencing is the potent method that significantly reduces the costs and allows to perform hundreds of samples in a single attempt. These techniques open up new windows of omics, specifically “environmental omics.” The 454 pyrosequencing is the first to be widely executed to study in microbial community analysis. This method comprises rRNA or ITS amplicon sequencing, whole-genome sequencing, shotgun metagenomics, and transcriptional profiling (Delmotte et al. 2009; Rastogi et al. 2012). Recently, Illumina platform has been performed better and allows ultra-high-throughput sequencing of microbial communities with high-quality reads (Degnan and Ochman 2012). Proteogenomic is another method used for the microbial community structure analysis (Delmotte et al. 2009), a combination of genomics and proteomics to a great extent makes easy the structural and functional differences of microbiota in the phyllosphere environments. Through those methods, microbial diversity of several host plants such as Arabidopsis, Apple tree, Beech, grapevine, oak, poplar, Prunus, rice, soybean, spinach, tomato wheat, etc. was documented. The metadata of the metagenomic studies helps to understand the growth behavior, colonization ability, genus-level community structure formation (or) association, low and high index of diversity, and the host genotype effects on the self-defense as well as the cell wall integrity have been reported.
Studies on high-throughput molecular approaches to phyllosphere communities
16S rRNA gene pyrosequencing
Soybean, clover, Arabidopsis
Epiphytic fitness of Sphingomonas and Methylobacterium
Delmotte et al. (2009)
Pine and other trees
Phyllosphere bacteria community composition
Redford et al. (2010)
Genus-level communities of Proteobacteria and Firmicutes-associated spinach leaves
Lopez-Velasco et al. (2011)
Bacterial communities on the surface of leaves and berries from grapevine
Leveau and Tech (2011)
A “core” community composed of Pseudomonas, Bacillus, Massilia, Arthrobacter, and Pantoea found in lettuce foliage
Rastogi et al. (2012)
Variation in phyllosphere microbiota composition. Effect of E. coli O157:H7 inoculation on microbiota composition
Williams et al. (2013)
Metagenomic analysis of rice phyllospheric bacterial communities in relation to blast disease
Prasad Sahu and Kumar (2015)
Common bean, soybean, and canola
Seasonal community succession of the phyllosphere microbiome
Copeland et al. (2015)
Microbial and functional diversity within the phyllosphere.
Ruiz-Pérez et al. (2016)
16/18S rRNA gene pyrosequencing
Fungal communities in the oak phyllosphere
Jumpponen and Jones (2009)
Geographical location is a major determinant of phyllosphere bacterial communities
Finkel et al. (2011)
Plant genotype-based fungal communities on leaf surfaces
Cordier et al. (2012)
Plant species-based fungal
Balint et al. (2013)
Rapid microbial community changes during initial stages of pine litter decomposition
Gołębiewski et al. (2019)
Soybean, clover, Arabidopsis
Metabolic adaptations contribute to the epiphytic fitness of Sphingomonas and Methylobacterium
Delmotte et al. (2009)
Several methylotrophic enzymes and their role in the carbon cycle by Methylobacterium
Knief et al. (2012)
Functional genes that distinguish maize phyllosphere metagenomes in drought and well-watered conditions
Methé et al. (2017)
Moreover, the high-throughput studies revealed the special functions/metabolism of the microbes associated with leaf surfaces, specifically carbohydrate transport, leaf litter decomposition, light-driven ATP pumps, methanol metabolism, C1 metabolism (Ottesen et al. 2013; Shade et al. 2013), and the effect of ecological factors such as climate change, temperature, seasonal variation, sporadic contact to soil, and/or anthropogenic activities such as the use of agricultural chemicals and pesticides (Ikeda et al. 2011; Shade et al. 2013; Karlsson et al. 2014; Copeland et al. 2015; Glenn et al. 2015). To attain better perceptive of the phyllosphere ecosystem and understand the functional relationship among plants, microbiota, and environment, metaproteome and metagenomics have been used (Rastogi et al. 2012; Bálint et al. 2013; Dees et al. 2015).
5.8 Impact of Phyllosphere Microbiome on Ecosystem
Phyllosphere microflora significantly influences the ecological relationship of the plants. The phyllosphere usually has bacteria, fungi, lichens, algae, and viruses that have actively participated in the adaptation, growth, resistance, and infection of the plant host (Walker et al. 2017; Verma et al. 2017; Yadav et al. 2018a). The phyllosphere microbiota has not been completely studied with their ecological significance, specifically plant and ecosystem level (Remus-Emsermann and Schlechter 2018). From seed germination to plant reproduction, studies have revealed how the phyllosphere microbiome affects the leaf functions and longevity, seed mass, apical growth, flowering, and fruit development (Jones and Dangl 2006; Sawinski et al. 2013; Kembel et al. 2014); however, the net interplay of the phyllosphere ecosystem in and around the plant is scanty. Recent scientific advancements that simplify the phyllosphere microbial life become understandable. The high-throughput genomics, such as environmental genomics and metagenomics, have greatly expanded our perceptive and understanding on the functional life of phyllosphere microbial communities in plant–environment and the impact on the ecosystem.
Environmental factors are drastically influencing the microbiome changes on phyllosphere. This is common to epiphytic microorganisms, exposed with heavy stress during the season cycle, the day/night cycle, and the growth, age, and anatomical dynamics of the plant. For instance, at drought condition, the epiphytic microbial community was notably increased on Holm oak (Rico et al. 2014). Similarly, at hot condition, bacterial endophytic communities are altered in lower leaves of paddy, but not in the epiphytes (Ren et al. 2014). However, the epiphytic fungal community responded well in worming seasons (Coince et al. 2014; Bálint et al. 2015). Besides, an increase of CO2 at the phyllosphere region never affects the bacterial abundance (Ren et al. 2014; Vacher et al. 2016), except a few fungal genera.
Microbes have flexible metabolic adaptations, which helps them to survive in the phyllosphere microenvironment. During the metabolic functions, the plant releases carbohydrates, polyols, amino acids, amines, isoprenoids, halogenated compounds, or alcohols, as well as water and salts, which are the available nutrients for epiphytic microorganisms (Trouvelot et al. 2014). However, leaf surface commonly exhibits desolate properties such as saline or alkaline pH which generates stress in phyllosphere microbes (Finkel et al. 2012). Several alphaproteobacteria express PhyR-based stress regulation and colonization on leaf surface (Iguchi et al. 2013). Additionally, they develop multiple mode adaptation to survive in phyllosphere such as tolerance, antimicrobial, and immunity compounds against a microbial competitor (Trouvelot et al. 2014), synthesis of extracellular polysaccharides, and also synthesize phytohormonal compounds.
Besides, biotic and abiotic factors induce molecular level regulations in plants to synthesize a diverse range of phytohormones. Generally, the gaseous ethylene, jasmonate, methyl jasmonate, salicylate, and methylsalicylate are induced by bacterial pathogens (Bodenhausen et al. 2014; Horton et al. 2014). For example, many plant defense mechanisms are induced by the interaction of the biotic component of the ecosystem through signals like volatile and nonvolatile chemicals, and microbes can degrade such chemicals resulting in reduced activity (Mason et al. 2014).
Studies on Phyllospheric methylotrophic metabolism
Methanotrophs and Methylobacteria
Linden, pine and blue spruce lilac, maple, and apple
Diversity of Methanotrophs in woody plant tissues within the winter period
Doronina et al. (2004)
Methylotrophic metabolism is advantageous for colonization under competitive conditions
Sy et al. (2005)
A proteomic study of Methylobacterium extorquens reveals a response regulator essential for epiphytic growth
Gourion et al. (2006)
Methylobacterium extorquens AM1
PhyR is involved in the general stress response
Gourion et al. (2008)
Methylocystis heyeri H2(T) and M. echinoides IMET10491(T)
Acetate utilization metabolism as a survival strategy
Belova et al. (2011)
Methylobacterium extorquens DSM 21961
Monitoring the plant epiphyte Methylobacterium extorquens DSM 21961
Verginer et al. (2010)
Arabidopsis thaliana or Medicago truncatula
The influence of the factor site, host plant species, time and the presence of other phyllosphere bacteria on Methylobacterium community composition and population size
Knief et al. (2010)
Yeast methylotrophy and autophagy in a methanol-oscillating environment on growing leaves
Kawaguchi et al. (2011)
Methylobacterium sp. (NC4), (NC28)
Sugarcane, pigeon pea, mustard, potato, and radish
Epiphytic pink-pigmented methylotrophic bacteria enhance germination and seedling growth of wheat (Triticum aestivum) by producing phytohormone
Meena et al. (2012)
Methylobacterium sp. strain OR01
Dominant colonization and inheritance of Methylobacterium sp.
Mizuno et al. (2013)
Methylosinus sp. B4S
Stress resistance and C1 metabolism involved in plant colonization of a methanotroph Arch
Iguchi et al. (2013)
plant-probiotic methylotroph in the phyllosphere
Kwak et al. (2014)
Methylobacterium radiotolerans VRI8-A4
Diversity of culturable methylotrophic bacteria in different genotypes of groundnut and their potential for plant growth promotion
Krishnamoorthy et al. (2018)
Chloromethane (CH3Cl) is one of the abundant chlorinated organic compounds in the atmosphere (currently ∼550 ppt) and is to be responsible for the depletion of stratospheric ozone over 16% (World Meteorological Organization 2014). The fluorescence-based bacterial bioreporter study reported that phyllosphere microbes, M. extorquens CM4 (Roselli et al. 2013) and Hyphomicrobium sp. (Nadalig et al. 2011), having the genes for chloromethane utilization (cmu), and also volatile dimethylsulphide (DMS) and dimethylsulfoniopropionate (DMSP), considered as global climate regulator (Schäfer et al. 2010; Nevitt 2011). In the biosphere, a small number of plants like salt marsh grasses Spartina and sugarcanes (Saccharum sp.) are reported as producers of DMSP. Microbes that are associated with these plants have adaptive metabolism by which it transforms or metabolizes the DMS and DMSP (Ansede et al. 2001). Hence, the phyllosphere microbes are the major source of carbon and sulfur biogeochemical cycles, in the ecosystem and climate regulation through their active filtration or utilization of plant-related volatile compounds (DeLeon-Rodriguez et al. 2013; Šantl-Temkiv et al. 2013).
Microbial populations reside at phyllosphere as epiphytes or as endophytes, and have close contact with the rhizosphere. A microbe can be established as an epiphytic and endophytic association has the metabolic plasticity required for them to thrive. Many experimental evidences suggested that microorganisms commonly associated with plants maybe vital for nutrient accessibility and decomposition of biomass (Bernal et al. 2006; Ramírez Gómez 2011; Lizarazo-Medina and Gómez-Vásquez 2015). The functional ecology of the plant influences the composition and interaction of the phyllosphere microbes (Bodenhausen et al. 2013; Ruiz-Pérez et al. 2016). Many of the phyllosphere microbial communities share the common metabolic properties of the soil microbes. For example, the major phyllosphere bacterial communities such as Bacillus, Burkholderia, Methylobacterium, Pseudomonas, Sphingomonas, and Xanthomonas are the soil inhabitant, which have carbohydrate metabolizing genes involved in utilization of starch, hemicellulose, pectin, and cellulose, rich in humus materials (Rawat et al. 2012; Bodenhausen et al. 2013; Bulgarelli et al. 2013). The nitrogen metabolism such as ammonification, denitrification, and anammox, and the degradation of aromatic compounds are also reported in foliar microbes (Usubillaga et al. 2001; Rawat et al. 2012; Ruiz-Pérez et al. 2016).
Tropospheric microbes (aerosols) play a vital function in global carbon cycles and also metabolize the organic compounds. Some airborne Gammaproteobacteria have ice nucleation-active (INA) property and contains specific gene (ina) via deposition of cloud droplets (Hill et al. 2014) on the leaf surface and mineralize the carbon compounds (Vaïtilingom et al. 2013). Reports confirmed the relationship of INA bacteria and phyllosphere microbiota, combined activities of both phyllosphere microbiota and cloud microbiota actively participating carbon cycle, and strong support for climate regulation (Bringel and Couée 2015). The above information suggested that the phyllosphere microbiome not only supports the health of its host but is also beneficial to the environment, specifically it regulates plant-derived greenhouse and other gaseous pollutants.
5.9 Biotechnological Potential of Phyllosphere Microbiota
The plant beneficial microbes are agriculturally important bioresources, and it can stimulate the plant growth and enhance plant nutrient uptake through solubilization and mobilization (of P, K, and Zn), nitrogen fixation, and siderophore production (microbes-mediated bio-fortification of Fe in different crops). Beneficial microbes can play an important role in increasing yields of the crop, remove contaminants, inhibit pathogens, and produce novel substances. The growth stimulation by beneficial microbes can be a consequence of biological nitrogen fixation, production of plant growth regulators such as IAA, gibberellic acids, and cytokines, and biocontrol of phytopathogens through the production of antibiotic, antifungal, or antibacterial, Fe-chelating compounds, induction of acquired host resistance, enhancing the bioavailability of minerals (Kour et al. 2019; Kumar et al. 2019b; Yadav et al. 2019a).
In this contest, the phyllosphere microbes may positively influence the growth of host plant and produce some antagonistic compound against pathogens. Phyllosphere endophytes with properties such as nitrogen fixation (Jones 1970; Freiberg 1998; Furnkranz et al. 2008), bioremediation of harmful chemicals/pollutants, and biocontrol agents against important foliar plant pathogens (Beattie and Lindow 1995; Balint-Kurti et al. 2010; De Marco et al. 2004) have been documented. Further, the microbiome of phyllosphere is a reflection of environmental conditions; they can contribute significantly to global food webs and nutrient linkages. Many beneficial microbes such as Achromobacter, Bacillus, Beijerinckia, Burkholderia, Flexibacterium, Methylobacterium, Micrococcus, Micromonospora, Nocardioides, Pantoea, Penicillium, Planomonospora, Pseudomonas, Streptomyces, and Xanthomonas have been reported from the phyllosphere environment of different crop plants (Verma et al. 2013a, b; Mukhtar et al. 2010; Meena et al. 2012; Dobrovol’skaya et al. 2017). However, compared with most other microbial habitats, the investigation of phyllosphere microbes is quite limited. Some of its important biotechnological potentials are listed below.
5.9.1 Biocontrol Agents
Biocontrol is the measure to control pathogens and disease-causing pest including nematodes weeds, insects, and mites by other beneficial microbes or harmless living materials. In nature, plant diseases are caused by bacterial pathogens which provide a substantial decline in the development of agricultural products. For sustainable agriculture, scientific approaches use the antagonistic properties of beneficial microbes against the harmful pathogens instead of using toxic harmful chemicals as biological control (Erwin and Ribeiro 1996; Sharma et al. 2012). Biological treatment is a desirable strategy for controlling plant diseases (You et al. 2015) and there are an increasing number of biocontrol agents (BCAs), such as Bacillus spp., Pseudomonas spp., Trichoderma spp., etc. being commercialized for various crops (Trabelsi and Mhamdi 2013; Cha et al. 2016). Most of them habitat either on phyllosphere or soil and can play a significant role in killing the number of plant pathogens on the surface of the leaves by competitive principle.
Plant-associated microbial compounds and bioactivity
Streptomyces griseochromogenes I
Control the rice blast caused by Pyricularia oryzae
Rice blast caused by Pyricularia oryzae, leaf spot in sugar beet and celery by Cercospora spp., and scab in pears and apples caused by Venturia spp.
Umezawa et al. (1965)
Ito et al. (1974)
Park et al. (1977)
S. hygroscopicus subsp. aureolacrimosus
Insecticidal and acaricidal
Mishima et al. (1983)
Bacillus subtilis and Bacillus cereus
Stierle et al. (1990)
Spinosad (X): spinosyn A and spinosyn D
Controls the caterpillar (Helicoverpa zea Boddie, Pieris rapae (L.), Keiferia lycopersicella (Walsingham), thrips (Ceratitis capitata (L.), Thrips palmi (Karny)) and beetles (Leptinotarsa decemlineata (Say))
Mertz and Yao (1990)
Maculosin is a cyclic dipeptide—phytotoxin
Stierle et al. (1990)
Pesticide and insecticide
Insecticide and acaricide
Jansson and Dybas (1996)
Ondeyka, et al. (1997)
Gerwick et al. (1997)
Pseudomonas syringae ESC 10/11
Fungicide-citrus green mold Penicillium digitatum
Bull et al. (1998)
Destruxin A and B
Strasser et al. (2000)
Strasser et al. (2000)
Beauvericin A and B
Beauveria bassiana and Paecilomyces spp
Lane et al. (2000)
Streptomyces species- neau-D50
Antifungal activity against Phytophthora sojae
Worapong et al. (2001)
Streptomyces hygroscopicus and Streptomyces viridochromogenes
Streptomyces sp. CP1130
Lewer et al. (2003)
Block et al. (2005)
Bacillus sp. sunhua
Fungicide—Fusarium oxysporum and Streptomyces scabies
Han et al. (2005)
Collier et al. (2005)
Pseudomonas syringae var. tabaci
Hoagland et al. (2007)
Zonno et al. (2008)
Nectria sp. DA60047
Irvine et al. (2008)
Beauvericin A and B
Beauveria bassiana and Paecilomyces spp.
Miller et al. (2008)
Streptomyces hygroscopicus AM3672
Benzaquinoid ansamycin antibiotic with potential herbicidal a
Hahn et al. (2009)
Streptomyces albus subsp. chlorinus NRRL B-24108
Hahn et al. (2009)
Phytotoxic to Cirsium arvense L.
Berestetskii et al. (2010)
Duke et al. (2011)
Antibiotic 1233A (XXIV)
Cephalosporium sp., Fusarium sp.,
Duke and Dayan (2011)
Phytotoxic to Cynodon dactylon
Radhakrishnan et al. (2017)
Aguilera et al. (2017)
Microbes with the production of compounds like indole acetic acid and N-acyl homoserine lactone (AHL) assist the bacteria to colonize on plant surface (Lindow and Brandl 2003). Sartori et al. (2015) studied the biocontrol potential of phyllosphere microorganisms from maize against Exserohi lumturcicum, the causal agent of leaf blight. Shrestha et al. (2016) investigated the prospects of biological control of rice-associated Bacillus against sheath blight and panicle blight of rice caused by Rhizoctonia solani and Burkholderia glumae, respectively. A variety of Bacillus isolates were observed to inhibit the sclerotial germination of the fungus, which could be attributed to the various antimicrobial secondary metabolites produced by the bacteria. Various gram-negative bacteria also show plant protection activity. For example, Pseudomonas graminis isolated from the apple phyllosphere showed control against fire blight caused by Erwinia amylovora (Mikiciński et al. 2016), Pseudomonas protegens CS1 from the lemon phyllosphere are used as a biocontrol against citrus canker (Michavila et al. 2017).
Phyllosphere endophytic fungi as biocontrol agent
Falk et al. (1996)
Aspergillus flavus and Fusarium verticillioides
Wicklow et al (2005)
Tobacco, bean, iris
Radish, strawberry, cucumber, potato, and tomato
Nectria galligena, Botrytis cinerea
Reino et al. (2008)
Colletotrichum gloeosporioides, Clonostachys rosea, and Botryosphaeria ribis
Moniliophthora roreri (frosty pod rot), Phytophthora palmivora (black pod rot), and Moniliophthora perniciosa (witches broom)
Mejía et al. (2008)
Cacao (Theobroma cacao)
Hanada et al. (2009)
Hue et al. (2009)
Cladosporium, Colletotrichum, Gibberella, Hypocrea, and Trichoderma
Smallanthus sonchifolius (Poepp.) H. Rob.
Lecythophora sp. and Fusarium oxysporum
Rosa et al. (2012)
Vitis vinifera L.
Núñez-Trujillo et al. (2012)
Colletotrichum gloeosporioides, Flavodon flavus, Diaporthe helianthi, Diaporthe phaseolorum, Aporospora terricola
Vitis labrusca L.
Brum et al. (2012)
Colletotrichum acutatum, Colletotrichum fragariae, Colletotrichum gloeosporioides, and P. viticola
Wang et al. (2013a)
Bionectria ochroleuca, Aureobasidium pullulans, Chaetomium spirochaete
Cosoveanu et al. (2014)
Videira et al. (2015)
5.9.2 Plant Growth-Promoting Compounds
Plant growth is regulated by the growth hormones, available nutrient, good environmental condition, and beneficial microbial interaction. Many of the microbes are the prime producers of plant growth hormones, specifically plant-associated or phyllosphere microbial communities produce IAA, gibberellic acids, and cytokines and could fix nitrogen and mobilize nutrients (Dourado et al. 2015). There are many bacteria and fungi which produce IAA, similar to those of plants (Sun et al. 2014; Venkatachalam et al. 2016; Thapa et al. 2018. Microbes use plant tryptophan to produce IAA, which can effectively improve plant growth and enhance overall health (Hayat et al. 2010; Yadav et al. 2015a, b). The genus Methylobacterium is among the most commonly observed leaf epiphytes and represents an abundant and stable member of the phyllosphere microbial community of a wide range of crop plants such as sugarcane (S. officinarum L.), pigeon pea (Cajanus cajan L.), mustard (Brassica campestris L.), potato (Solanum tuberosum L.), and radish (Raphanus sativus L.) (Meena et al. 2012), and has produced variety of growth-promoting phytohormones. The association of plant growth-promoting bacteria (PGPB), especially Methylobacterium sp., with plant hosts greatly benefits plant growth by production of phytohormones like auxins and cytokinins, and increased activity of enzymes such as urease and 1-aminocyclopropane-1-carboxylate deaminase (ACCD), which promotes growth and enhances the production of siderophores, thereby enhancing the uptake of essential nutrients.
The benefits associated with plant–microbe interactions are also dependent on the variety of inoculation methods such as soil, foliar, and combination of both soil and foliar inoculations (Lee et al. 2011). A study has been conducted to investigate the inoculation of Erwinia herbicola on plant growth by IAA production. The test results showed that about 65% of the E. herbicola strain recovered from the leaves showed higher expression of the ipdC gene than in culture. The study indicated that physical or chemical microclimates directly influence the differential expression of ipdC (Brandl et al. 2001). Similarly, endophytic bacteria such as Bacillus pumilus E2S2 (Luo et al. 2012), B. amyloliquefaciens NBRI-SN13 (Nautiyal et al. 2013), B. atrophaeus EY6 and B. sphaericus B EY30, B. subtilis EY2, S. kloosii EY37, and K. erythromyxa EY43 (Karlidag et al. 2011) also produce PGPs.
Endophytic Bacillus produces phytohormones such as abscisic acid, auxins, brassinosteroids, cytokinins, ethylene, gibberellins, jasmonates, and strigolactones, and increases nutrient (nitrogen and phosphorous) accessibility to the host (Reinhold-Hurek and Hurek 2011; Brader et al. 2014; Santoyo et al. 2016; Shahzad et al. 2016; Ek-Ramos et al. 2019). Zeiller et al. (2015) reported that C. botulinum 2301 significantly produce PGPs in a field experiment of clover. A cold-tolerant bacterial strain Exiguobacterium acetylicum 1P promotes wheat seedlings growth (Selvakumar et al. 2010), Brevibacillus brevis improve the growth of cotton crop (Nehra et al. 2016) and Bacillus spp. induce phosphate solubilization more efficiently when present as endophytes in citrus (Giassi et al. 2016). The diazotrophic bacteria associated with phyllosphere gives benefits to the plant by fixing atmospheric nitrogen, solubilization of phosphorus (P), and utilization of available nutrients through its organic end product-mediated solubilization of rock phosphates (Mohammadi 2012; Kembel et al. 2014; Mwajita et al. 2013; Batool et al. 2016; Lambais et al. 2017).
5.9.3 Biopharmaceutical Importance
Pharmaceutical valuable products from phyllosphere microbes
Hypericum perforatum, Diaporthe helianthi
Hypericin, emodin, tyrosol
Rapamycin, cyclododecane, petalostemumol
Streptomyces sp., Kennedia nigricans
Kumar et al. (2014)
Dutta et al. (2014)
Kakadumycin A, hypericin
Alvin et al. (2014)
Golinska et al. (2015)
Boesenbergia rotunda Streptomyces coelicolor
5.9.4 Other Applications
Besides the use of phyllosphere microbes for enhanced growth as well as biocontrol agent, some plant-associated bacteria helps the plant to improve phytoremediation of toxins. For example, hydroxamate siderophores producing bacteria compact heavy metal toxicity and improve the phytoremediation property in A. thaliana (Grobelak and Hiller 2017). Some endophytes provide additional functions to the host plant like drought tolerance, for example, endophytic B. subtilis strain B26 induces drought resistance to Brachypodium distachyon grass. The drought resistance mechanism is due to a specific carbohydrate metabolism, the endophytic bacteria increases stress-responsive raffinose-related family carbohydrates in the host (Gagné-Bourque et al. 2015). In another example, the endophytic association increases osmotic responses of the host plant. Endophytic strains such as Arthrobacter sp. and Bacillus spp. in pepper plant increase the proline accumulation, which gives osmotic tolerance (Sziderics et al. 2007).
Further, endophytic bacterial inoculants provide abiotic stress tolerance mechanism to the host by its extracellular enzymes. For example, the endophytic association of various Bacillus spp. increases the superoxide dismutase, phenylalanine lyase, catalase, and peroxidase enzymes activity in gladiolus plants under sodium high concentration conditions (Damodaran et al. 2014). Little studies reported that isolation of endophytic bacteria and their enzyme production potential vary when it colonizes in the plant tissues. Moreover, Jalgaonwala et al. (2011) observed maximum proteolytic activity in Lactobacillus fermentum isolated from leaves of Vinca rosea, which is considered greater to nonendophytic isolates. Similarly, endophytic fungi isolated from Ocimum sanctum and Aloe vera has better enzymatic activity (Yadav et al. 2015a, b). Besides these mechanisms, plant-associated microorganisms improve nutrient acquisition by supplying minerals and other micro/macronutrients from the soil (Singh et al. 2017; Singh and Singh 2017). Above all merits provide new insights in the field of phyllosphere microbiome and its essentiality of interactions to host plant growth and protection and also its significant role in the ecosystem.
5.9.5 Conclusion and Future Prospects
The phyllosphere is a unique environment colonized by a wide variety of microorganisms including epiphytes and endophytes, beneficial and pathogenic, bacteria, fungus, viruses, etc. Understanding the phyllosphere community structure, networking, and physiology is a great challenge. However, extensive research on phyllosphere microbiota gives great potential for the applications in economic plant productivity, specifically agriculture and forestry, ecosystem cleaning, and health. Hitherto, both in vitro and in vivo experiments are required to improve the understanding of microbial aggregations in the phyllosphere and dynamic play in the ecosystem. Based on the literature understanding, further and future studies should aim to (1) study the community interplay within the closely related and distanced microbial interactions and its stimulatory response on host plant and ecosystem, (2) to know the potentials of beneficial microbes and their commercial value, (3) impact on climate change on phyllosphere microbiome, and their contribution to climate change, (4) moreover, documentation of host-specific, geographic-specific, and seasonal-specific microbial interactions—guiding host–parasite and beneficial–pathogen interactions. Besides, phyllosphere microbiome research assures to understand the current challenges highlighting the terrestrial ecosystem change and the impact of global warming, especially the dominance of pathogenesis.
Authors thank DST-PURSE, Madurai Kamaraj University for providing Internet and computer facility and Department of Biotechnology, India for providing the infrastructure facilities.
- Aguilera S, Alvarez-Morales A, Murillo J, Hernández-Flores JL, Bravo J, De la Torre-Zavala S (2017) Temperature-mediated biosynthesis of the phytotoxin phaseolotoxin by Pseudomonas syringae pv. phaseolicola depends on the autoregulated expression of the phtABC genes. PLoS ONE 12(6): e0178441. https://doi.org/10.1371/journal.pone.0178441PubMedPubMedCentralCrossRefGoogle Scholar
- Beattie GA (2002) Leaf surface waxes and the process of leaf colonization by microorganisms. In: Lindow SE, Hecht-Poinar EI, Elliott VJ (eds) Phyllosphere microbiology. APS Press, St. Paul, USA, pp 3–26Google Scholar
- Berestetskii AO, Yuzikhin OS, Katkova AS, Dobrodumov AV, Sivogrivov DE, Kolombet LV (2010) Isolation, identification, and characteristics of the phytotoxin produced by the fungus Alternaria cirsinoxia. Appl Microbiol Biot 46:75–79Google Scholar
- Bernal E, Celis S, Galíndez X, Moratto C, Sánchez J, García D (2006) Microflora cultivable endomicorrizas obtenidas en hojarasca de bosque (Páramo Guerrero finca Puente de Tierra) Zipaquirá, Colombia. Acta Biol Colomb 11:125–130Google Scholar
- Bhattacharyya LH, Borah G, Parkash V, Bhattacharyya PN (2017) Fungal endophytes associated with the ethnomedicinal plant Meyna spinosa Roxb. Current Life Sci 3(1):1–5Google Scholar
- Carlos A, Ruiz-Pérez SR, Zambranoa MM (2016) Microbial and functional diversity within the phyllosphere of Espeletia Species in an Andean high-mountain ecosystem. Appl Environ Microbiol 82:6Google Scholar
- Cha JY, Han S, Hong HJ, Cho H, Kim D, Kwon Y, Kwon SK, Crüsemann M, Yong BL, Kim JF (2016) Microbial and biochemical basis of a Fusarium wilt-suppressive soilGoogle Scholar
- Chen MH, Zhang L, Zhang X (2011) Isolation and inoculation of endophytic actinomycetes in root nodules of Elaeagnus angustifolia. Mod Appl Sci 5:264–267Google Scholar
- Cosoveanu A, Gimenez-Mariño C, Cabrera Y, Hernandez G, Cabrera R (2014) Endophytic fungi from grapevine cultivars in Canary Islands and their activity against phytopatogenic fungi. Int J Agric Crop Sci 7(15):1497–1503Google Scholar
- Deka D, Jha DK (2018) Antimicrobial activity of Endophytic Fungi from leaves and barks of Litsea cubeba Pers., A Traditionally important medicinal plant of north east India. Jordan J Biol Sci 11(1):73–79Google Scholar
- DeLeon-Rodriguez N, Lathem TL, Rodriguez-R LM, Barazesh JM, Anderson BE, Beyersdorf AJ et al (2013) Microbiome of the upper troposphere: species composition and prevalence, effects of tropical storms, and atmospheric implications. Proc Natl Acad Sci USA 110:2575–2580PubMedCrossRefPubMedCentralGoogle Scholar
- Dhayanithy G, Subban K, Chelliah J (2019) Diversity and biological activities of endophytic fungi associated with Catharanthus roseus. BMC Microbiol 19(1):22Google Scholar
- Ding L et al (2011) Resistance to hemi-biotrophic Fusarium graminearum infection is associated with coordinGoogle Scholar
- Durand A, Maillard F, Alvarez-Lopez V, Guinchard S, Bertheau C, Valot B et al (2018) Bacterial diversity associated with poplar trees grown on a Hg-contaminated site: community characterization and isolation of Hg-resistant plant growth promoting bacteria. Sci Total Environ 622:1165–1177PubMedCrossRefPubMedCentralGoogle Scholar
- El-Din Hassan S (2017) Plant growth-promoting activities for bacterial and fungal endophytes isolated from medicinal plant of Teucrium polium L J Adv Res 8(6):687–695Google Scholar
- Erwin DC, Ribeiro OK (1996) Phytophthora diseases worldwide. APS press, New YorkGoogle Scholar
- Gerwick BC, Fields SS, Chapin EL, Cleveland JA, Heim DR (1997) Pyrizadocidin, a new microbial phytotoxin with activities in a Mehler’s reaction. Weed Sci 45:654–657Google Scholar
- Godstime OC, Enwa FO, Augustina JO, Christopher EO (2014) Mechanisms of antimicrobial actions of phytochemicals against enteric pathogens—a review. J Pharm Chem Biol Sci 2:77–85Google Scholar
- Green PN (2006) Methylobacterium. The Prokaryotes, vol 5 (Falkow S, Rosenberg E, Schleifer K-H, Stackebrandt E, Dworkin M, eds). Springer, New York, NY, pp 257–265Google Scholar
- Huang MJ, Rao MP, Salam N, Xiao M, Huang HQ, Li WJ (2017) Allostreptomyces psammosilenae gen. nov., sp. nov., an endophytic actinobacterium isolated from the roots of Psammosilene tunicoides and emended description of the family Streptomycetaceae. Int J Syst Evol Microbiol 67:288–293PubMedCrossRefPubMedCentralGoogle Scholar
- Ismail K, Abdullah S, Chong K (2014) Screening for potential antimicrobial compounds from Ganoderma boninense against selected food borne and skin disease pathogens. Int J Pharm Pharm Sci 6:771–774Google Scholar
- Jalgaonwala RE, Mohite BV, Mahajan RT (2011) Natural products from plant associated endophytic fungi. J Microbiol Biotechnol Res 1:21–32Google Scholar
- Jansson RK, Dybas RA (1996) Avermectins: biochemical mode of action, biological activity, and agricultural importance. In: Ishaaya I (ed) Insecticides with novel modes of action: mechanisms and applications. Springer Verlag, BerlinGoogle Scholar
- Jariwala B, Desai B (2018) Isolation and identification of endophytic fungi from various medicinal plants. BMR Microbiology 4(1):1–7Google Scholar
- Kaewkla O, Thamchaipenet A, Franco CM (2017) Micromonospora terminaliae sp. nov., an endophytic actinobacterium isolated from the surface sterilized stem of the medicinal plant Terminalia mucronata. Int J Syst Evol Microbiol 225–230Google Scholar
- Knief C, Frances L, Vorholt JA (2010) Competitiveness of diverse Methylobacterium strains in the phyllosphere of Arabidopsis thaliana and identification of representative models, including M. extorquens PA1. Microb Ecol 60(2):440–52. https://doi.org/10.1007/s00248-010-9725-3PubMedCrossRefPubMedCentralGoogle Scholar
- Kotasthane AS, Agrawal T, Waris Zaidi N, Singh US (2017) Identification of siderophore producing and cynogenic fluorescent Pseudomonas and a simple confrontation assay to identify potential bio-control agent for collar rot of chickpea. 3 Biotech 7(2):137Google Scholar
- Kour D, Rana KL, Yadav N, Yadav AN, Singh J, Rastegari AA, Saxena AK (2019) Agriculturally and industrially important fungi: current developments and potential biotechnological applications. In: Yadav AN, Singh S, Mishra S, Gupta A (eds) Recent advancement in white biotechnology through fungi, Volume 2: Perspective for value-added products and environments. Springer International Publishing, Cham, pp 1–64. https://doi.org/10.1007/978-3-030-14846-1_1Google Scholar
- Krishnamoorthy R, Kwon SW, Kumutha K, Senthilkumar M, Ahmed S, Sa T, Anandham R (2018) Diversity of culturable methylotrophic bacteria in diffrent genotypes of groundnut and their potential for plant growth promotion. 3 Biotech 8:275Google Scholar
- Krol P, Iqielski R, Pollmann S, Kepczynska E (2015) Priming of seeds with methyl jasmonate induced resistance to hemi-biotroph Fusarium oxysporum f.sp. lycopersici in tomato via 12-oxo-phytodienoic acid, salicylic acid and flavonol accumulation. J Plant Physiol 179:122–132PubMedCrossRefPubMedCentralGoogle Scholar
- Kumar S, Aharwal RP, Shukla H, Rajak RC, Sandhu SS (2014) Endophytic fungi: as a source of antimicrobials bioactive compounds. World J Pharm Pharm Sci 3:1179–1197Google Scholar
- Kumar M, Saxena R, Rai PK, Tomar RS, Yadav N, Rana KL, Kour D, Yadav AN (2019b) Genetic diversity of methylotrophic yeast and their impact on environments. In: Yadav AN, Singh S, Mishra S, Gupta A (eds) Recent advancement in white biotechnology through fungi, Volume 3: Perspective for sustainable environments. Springer International Publishing, Cham, pp 53–71. https://doi.org/10.1007/978-3-030-25506-0_3CrossRefGoogle Scholar
- Lane GA, Christensen MJ, Miles CO (2000) Coevolution of fungal endophytes with grasses: the significance of secondary metabolites. In: Bacon CW, White JFJ (eds) Microbial endophytes. Marcel Dekker, New York, pp 341–388Google Scholar
- Legard DE, McQuilken MP, Whipps JM, Fenlon JS, Fermor TR, Thompson IP, Bailey MJ, Lynch JM (1994) Studies of seasonal changes in the microbial populations on the phyllosphere of spring wheat as a prelude to the release of a genetically modified microorganism. Agricult Ecosyst Environ 50:87–101CrossRefGoogle Scholar
- Lopez-Velasco G, Welbaum GE, Boyer RR, Mane SP, Ponder MA (2011) Changes in spinach phylloepiphytic bacteria communities following minimal processing and refrigerated storage described using pyrosequencing of 16S rRNA amplicons. J Appl Microbiol 110:1203–1214PubMedCrossRefPubMedCentralGoogle Scholar
- Lurdes Inácio M, Henriques J, Sousa E (2010) Mycobiota associated with Platypus cylindrus Fab. (Coleoptera: Platypodidae) on cork oak in Portugal. Integrated Protection in Oak Forests. IOBC/wprs Bull 57:87–95Google Scholar
- Manceau CR, Kasempour MN (2002) In Endophytic versus epiphytic colonization of plants: what comes first? In: Lindow SE, Hecht-Poinar EI, Elliott VJ (eds) Phyllosphere microbiology. APS Press, St Paul, USA, pp 115–123Google Scholar
- Mase S (1984) Meiji Herbiace (MW-801, SF-1293) (common name: bialaphos) A new herbicide. Jpn Pestic Inf 45:27–30Google Scholar
- Meena KK, Kumar M, Kalyuzhnaya MG, Yandigeri MS, Singh DP, Saxena AK et al (2012) Epiphytic pink-pigmented methylotrophic bacteria enhance germination and seedling growth of wheat (Triticum aestivum) by producing phytohormone. Antonie Van Leeuwenhoek 101:777–786PubMedCrossRefPubMedCentralGoogle Scholar
- Methé BA, Li K, Talley SP, Gupta N, Frank B, Xu W, Gordon SG, Goodner B, Stapleton AE (2017) Functional genes that distinguish Maize phyllosphere metagenomes in drought and well-watered conditions. BioRxiv preprint online http://dx.doi.org/10.1101/104331
- Miranda M, Ralph SG, Mellway R, White R, Heath MC, Bohlmann J, Constabel CP (2007) The transcriptional response of hybrid poplar (Populas trichocarpa × P. deltoides) to infection by Melamspora medusa leaf rust involves induction of flavonoid pathway genes leading to accumulation of Proanthocyanidins. Mol Plant Microbe Interact 20:816–831PubMedCrossRefPubMedCentralGoogle Scholar
- Mohammadi K (2012) Phosphorus solubilizing bacteria: occurrence, mechanisms mechanisms and their role in crop production. Resour Environ 2:80–85Google Scholar
- Morris CE, Kinkel LL (2002) Fifty years of phylosphere microbiology: significant contributions to research in related fields. In: Lindow SE, Hecht-Poinar EI, Elliott V (eds) Phyllosphere microbiology. APS Press, St. Paul, Minn, pp 365–375Google Scholar
- Mukhtar I, Khokhar I, Sobia M, Ali A (2010) Diversity of epiphytic and endophytic microorganisms in some dominant weeds. Pak J Weed Sci Res 16:287–297Google Scholar
- Nadalig T, Ul F, Haque M, Roselli S, Schaller H, Bringel F, Vuilleumier S (2011) Detection and isolation of chloromethane-degrading bacteria from the Arabidopsis thaliana phyllosphere, and characterization of chloromethane utilization genes. FEMS Microbiol Ecol 77:438–448PubMedCrossRefPubMedCentralGoogle Scholar
- Núñez-Trujillo G, Cabrera R, Burgos-Reyes RL, Silva ED, Giménez C, Cosoveanu A et al. (2012) Endophytic fungi from Vitis vinifera L. isolated in Canary Islands and Azores as potential biocontrol agents of Botrytis cinerea Pers.: Fr J Hortic For Biotechnol 16:1–6Google Scholar
- Ondeyka JG, Helms GL, Hensens OD, Goetz MA, Zink DL, Tsipouras A, Shoop WL, Slayton L, Dombrowskii AW, Polishook JD, Ostlind DA, Tsou NN (1997) Nodulisporic acid A, a novel and potent insecticide from Nodulisporium sp. Isolation, structure determination and chemical transformation. J Am Chem Soc 119:8809–8816CrossRefGoogle Scholar
- Parthasarathi S, Sathya S, Bupesh G, Samy DR, Mohan MR, Selva GK et al (2012) Isolation and characterization of antimicrobial compound from marine Streptomyces hygroscopicus BDUS 49. World J Fish Mar Sci 4:268–277Google Scholar
- Prasad Sahu K, Kumar A (2015) Metagenomic analysis of rice phyllospheric bacterial communities in relation to blast disease. M.Sc., Thesis, Krishikosh Indian Agricultural Research Institute, New DelhiGoogle Scholar
- Qin S, Bian GK, Zhang YJ, Xing K, Cao CL, Liu CH et al (2013) Modestobacter roseus sp. nov., an endophytic actinomycete isolated from the coastal halophyte Salicornia europaea Linn, and emended description of the genus Modestobacter. Int J Syst Evol Microbiol 63:2197–2202PubMedCrossRefPubMedCentralGoogle Scholar
- Quan M, Liang J (2017) The influences of four types of soil on the growth, physiological and biochemical characteristics of Lycoris aurea (L’ Her.) Herb Sci Rep 7. ( https://doi.org/10.1038/srep43284)
- Radhakrishnan R, Hashem A, Abd_Allah EF (2017) Bacillus: a biological tool for crop improvement through bio-molecular changes in adverse environments. Front Physiol 8:667. https://doi.org/10.3389/fphys.2017.00667
- Ramírez Gómez M (2011) Importancia de los microorganismos y la edafofauna en los páramos. Colombia tiene Páramos 2011(1):42–57Google Scholar
- Rana KL, Kour D, Sheikh I, Dhiman A, Yadav N, Yadav AN, Rastegari AA, Singh K, Saxena AK (2019a) Endophytic fungi: biodiversity, ecological significance and potential industrial applications. In: Yadav AN, Mishra S, Singh S, Gupta A (eds) Recent advancement in white biotechnology through fungi, vol 1. Diversity and Enzymes Perspectives. Springer, Switzerland, pp 1–62Google Scholar
- Rana KL, Kour D, Sheikh I, Yadav N, Yadav AN, Kumar V, Singh BP, Dhaliwal HS, Saxena AK (2019b) Biodiversity of endophytic fungi from diverse niches and their biotechnological applications. In: Singh BP (ed) Advances in endophytic fungal research: present status and future challenges. Springer International Publishing, Cham, pp 105–144. https://doi.org/10.1007/978-3-030-03589-1_6CrossRefGoogle Scholar
- Rana KL, Kour D, Yadav AN (2019c) Endophytic microbiomes: biodiversity, ecological significance and biotechnological applications. Res J Biotechnol 14:142–162Google Scholar
- Rodriguez RJ, White JF, Arnold AE, Redman RS (2009) Fungal endophytes: diversity diversity and functional roles. New Phytol 182:314–330Google Scholar
- Rosa LH, Tabanca N, Techen N, Pan Z, Wedge DE, Moraes RM (2012) Antifungal activity of extracts from endophytic fungi associated with Smallanthus maintained in vitro as autotrophic cultures and as pot plants in the greenhouse. Can J Microbiol 58(10):1202–1221PubMedCrossRefPubMedCentralGoogle Scholar
- Roselli S, Nadalig T, Vuilleumier S, Bringel F (2013) The 380 kb pCMU01 plasmid encodes chloromethane utilization genes and redundant genes for vitamin B12- and tetrahydrofolate-dependent chloromethane metabolism in Methylobacterium extorquens CM4: a proteomic and bioinformatics study. PLoS ONE 8:e56598PubMedPubMedCentralCrossRefGoogle Scholar
- Rudd JJ et al (2015) Transcriptome and metabolite profiling the infection cycle of Zymoseptoria tritici on wheat (Triticum aestivum) reveals a biphasic interaction with plant immunity involving differential pathogen chromosomal contributions, and a variation on the hemibiotrophic lifestyle definition. Plant Physiol 167:1158–1185PubMedPubMedCentralCrossRefGoogle Scholar
- Santhanam R, Groten K, Meldau DG, Baldwin IT (2014) Analysis of plant-bacteria interactions in their native habitat: bacterial communities associated with wild tobacco are independent of endogenous jasmonic acid levels and developmental stages. PLoS ONE 9:e94710PubMedPubMedCentralCrossRefGoogle Scholar
- Saxena S (2014) Microbial metabolites for development of ecofriendly agrochemicals. Allelopath J 33(1):1–24Google Scholar
- Scavino AF, Pedraza RO (2013) The role of siderophores in plant growth-promoting bacteria. In: Maheshwari DK, Saraf M, Aeron A (eds) Bacteria in agrobiology: crop productivity. Springer, Berlin, pp 265–285. https://doi.org/10.1007/978-3-642-37241-4-11
- Shukla ST, Habbu PV, Kulkarni VH, Jagadish KS, Pandey AR, Sutariya VN (2014) Endophytic microbes: a novel source for biologically/pharmacologically active secondary metabolites. Asian J Pharmacol Toxicol 2:1–16Google Scholar
- Singh R, Dubey AK (2015) Endophytic actinomycetes as emerging source for therapeutic compounds. Indo Global J Pharm Sci 5:106–116Google Scholar
- Singh R, Ashok K, Dubey (2018) Diversity and applications of endophytic actinobacteria of plants in special and other ecological niches 9:1767Google Scholar
- Sreekanth D, Kristin IM, Brett AN (2017) Endophytic fungi from Cathranthus roseus: a potential resource for the discovery of antimicrobial polyketides. Nat Prod Chem Res 5:256Google Scholar
- Stierle A, Cardellina H, Strobel G (1990) Maculosin, a host-specific phytotoxin from Alternaria alternata on spotted knapweed. Am Chem Soc Symp Ser 439:53–62Google Scholar
- Suslow TV (2002) Production practices affecting the potential for persistent contamination of plants by microbial foodborne pathogens. In: Lindow SE, Hecht-Poinar EI, Elliott VJ (eds) Phyllosphere microbiology. APS Press, St Paul, USA, pp 241–256Google Scholar
- Tachibana K (2003) Bialaphos, a natural herbicide. Meiji Seika Kenkyo Nenpo 42:44–57Google Scholar
- Trabelsi D, Mhamdi R (2013) Microbial inoculants and their impact on soil microbial communities: a review. Biomed Res IntGoogle Scholar
- Umezawa H, Okami Y, Hashimoto T, Suhara Y, Otake N (1965) A new antibiotic kasugamycin. J Antibiot Ser A 18:101–103Google Scholar
- Verma P, Yadav AN, Kazy SK, Saxena AK, Suman A (2013) Elucidating the diversity and plant growth promoting attributes of wheat (Triticum aestivum) associated acidotolerant bacteria from southern hills zone of India. Natl J Life Sci 10:219–227Google Scholar
- Verma P, Yadav AN, Khannam KS, Panjiar N, Kumar S, Saxena AK, Suman A (2015) Assessment of genetic diversity and plant growth promoting attributes of psychrotolerant bacteria allied with wheat (Triticum aestivum) from the northern hills zone of India. Ann Microbiol 65:1885–1899CrossRefGoogle Scholar
- Verma P, Yadav AN, Khannam KS, Kumar S, Saxena AK, Suman A (2016a) Molecular diversity and multifarious plant growth promoting attributes of Bacilli associated with wheat (Triticum aestivum L.) rhizosphere from six diverse agro-ecological zones of India. J Basic Microbiol 56:44–58PubMedPubMedCentralCrossRefGoogle Scholar
- Verma P, Yadav AN, Khannam KS, Mishra S, Kumar S, Saxena AK, Suman A (2016b) Appraisal of diversity and functional attributes of thermotolerant wheat associated bacteria from the peninsular zone of India. Saudi J Biol Sci. https://doi.org/10.1016/j.sjbs.2016.01.042CrossRefPubMedPubMedCentralGoogle Scholar
- Verma P, Yadav AN, Kumar V, Singh DP, Saxena AK (2017) Beneficial plant-microbes interactions: biodiversity of microbes from diverse extreme environments and its impact for crop improvement. In: Singh DP, Singh HB, Prabha R (eds) Plant-microbe interactions in agro-ecological perspectives, vol 2. Microbial Interactions and Agro-Ecological Impacts. Springer, Singapore, pp 543–580. https://doi.org/10.1007/978-981-10-6593-4_22Google Scholar
- Vorholt JA (2012) Microbial life in the phyllosphere. Nat Rev 10:828–840Google Scholar
- Wang M, Ma Q (2011) Antagonistic Actinomycete XN-1 from phyllosphere microorganisms of cucumber to control corynespora cassiicola. Cucurbit Genet Coop Rep 33–34:17–21Google Scholar
- Wensing A, Braun SD, Buttner P, Expert D, Volksch B, Ullrich MS et al (2010) Impact of siderophore production by Pseudomonas syringae pv. syringae 22d/93 on epiphytic fitness and biocontrol activity against Pseudomonas syringae pv. glycinea 1a/96. Appl Environ Microbiol 76:2704–2711PubMedPubMedCentralCrossRefGoogle Scholar
- Worapong J, Strobel GA, Ford EJ, Li JY, Baird G, Hess WM (2001) Muscodor albus anam. nov., an endophyte from Cinnamomum zeylanicum. Mycotaxon 79:67–79Google Scholar
- Yadav AN (2017) Agriculturally important microbiomes: biodiversity and multifarious PGP attributes for amelioration of diverse abiotic stresses in crops for sustainable agriculture. Biomed J Sci Tech Res 1:1–4Google Scholar
- Yadav AN, Yadav N (2018) Stress-Adaptive Microbes for Plant Growth Promotion and Alleviation of Drought Stress in Plants. Acta Sci Agric 2:85–88Google Scholar
- Yadav N, Yadav AN (2019) Actinobacteria for sustainable agriculture. Journal of Applied Biotechnology and Bioengineering 6:38–41Google Scholar
- Yadav AN, Verma P, Kumar S, Kumar V, Kumar M, Singh BP, Saxena AK, Dhaliwal HS (2018b) Actinobacteria from Rhizosphere: Molecular Diversity, Distributions and Potential Biotechnological Applications. In: Singh B, Gupta V, Passari A (eds) New and Future Developments in Microbial Biotechnology and Bioengineering. USA, pp 13–41. https://doi.org/10.1016/b978-0-444-63994-3.00002-3CrossRefGoogle Scholar
- Yadav AN, Verma P, Kumar V, Sangwan P, Mishra S, Panjiar N, Gupta VK, Saxena AK (2018c) Biodiversity of the Genus Penicillium in Different Habitats. In: Gupta VK, Rodriguez-Couto S (eds) New and Future Developments in Microbial Biotechnology and Bioengineering, Penicillium System Properties and Applications. Elsevier, Amsterdam, pp 3–18. https://doi.org/10.1016/b978-0-444-63501-3.00001-6CrossRefGoogle Scholar
- Yadav AN, Kour D, Sharma S, Sachan SG, Singh B, Chauhan VS, Sayyed RZ, Kaushik R, Saxena AK (2019a) Psychrotrophic Microbes: Biodiversity, Mechanisms of Adaptation, and Biotechnological Implications in Alleviation of Cold Stress in Plants. In: Sayyed RZ, Arora NK, Reddy MS (eds) Plant Growth Promoting Rhizobacteria for Sustainable Stress Management: Volume 1: Rhizobacteria in Abiotic Stress Management. Springer Singapore, Singapore, pp 219–253. https://doi.org/10.1007/978-981-13-6536-2_12CrossRefGoogle Scholar
- Yadav AN, Mishra S, Singh S, Gupta A (2019b) Recent Advancement in White Biotechnology Through Fungi Volume 1: Diversity and Enzymes Perspectives. Springer International Publishing, ChamGoogle Scholar
- Yadav AN, Singh S, Mishra S, Gupta A (2019c) Recent advancement in white biotechnology through fungi. Volume 2: Perspective for Value-Added Products and Environments. Springer International Publishing, ChamGoogle Scholar
- Yadav AN, Singh S, Mishra S, Gupta A (2019d) Recent Advancement in White Biotechnology Through Fungi. Volume 3: Perspective for Sustainable Environments. Springer International Publishing, ChamGoogle Scholar
- Zak JC (2002) Implications of a leaf surface habitat for fungal community structure and function. In: Lindow SE, Hecht-Poinar EI, Elliott VJ (eds) Phyllosphere Microbiology. APS Press, St Paul, USA, pp 299–315Google Scholar