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Rhizosphere microbiome: revisiting the synergy of plant-microbe interactions

Rhizosphere microbiome: revisiting the synergy of plant-microbe interactions Sustainable enhancement in food production from less available arable land must encompass a balanced use of inorganic, organic, and biofertilizer sources of plant nutrients to augment and maintain soil fertility and productivity. The varied responses of microbial inoculants across fields and crops, however, have formed a major bottleneck that hinders its widespread adoption. This necessitates an intricate analysis of the inter-relationships between soil microbial communities and their impact on host plant productivity. The concept of Bbiased rhizosphere,^ which evolved from the interactions among different components of the rhizosphere including plant roots and soil microflora, strives to garner a better understanding of the complex rhizospheric intercommunications. Moreover, knowledge on rhizosphere microbiome is essential for developing strategies for shaping the rhizosphere to benefit the plants. With the advent of molecular and Bomics^ tools, a better understanding of the plant-microbe association could be acquired which could play a crucial role in drafting the future Bbiofertilizers.^ The present review, therefore aims to (a) to introduce the concepts of rhizosphere hotspots and microbiomes and (b) to detail out the methodologies for creating biased rhizospheres for plant-mediated selection of beneficial microorganisms and their roles in improving plant performance. . . . . Keywords Biased rhizosphere Microbial inoculants Microbiome Rhizosphere engineering Root border cells Introduction these plant growth-promoting organisms, which are capable of exerting beneficial effects on plants. Generally, 60–90% of Biofertilizers are preparations containing specialized living the total applied fertilizer is lost and in this regard, microbial organisms that can fix, mobilize, solubilize, or decompose inoculants have prominence in sustainable integrated nutrient nutrient sources which, when applied through seed or soil, management systems (Bhardwaj et al. 2014). Moreover, the enhance nutrient uptake by plants. Biofertilizer research utility of poor-quality native nutrients in soil necessitates mi- started with BNitragin,^ the first commercially produced and crobial interventions. For example, approximately 90% of to- patented culture of Rhizobium, by Nobbe and Hiltner in 1895 tal soil K is found in crystalline, insoluble mineral forms like (Nobbe and Hiltner 1896). The introduction of yellow seeded feldspars and mica, which plants cannot utilize (Meena et al. soybean in India in the 1960s led to a spurt in demand for 2014). To make them available for plant nutrition, microor- soybean inoculants in the region. This intensified research in ganisms which can solubilize and release K should be development of microbial formulations for pulses, groundnut, deployed. and even forage legumes. The discovery of Azotobacter, While positive responses have been recorded in a range of Azospirillum, blue-green algae and a host of other beneficial field trials, the beneficial effects from the application of mi- microorganisms soon followed. Interestingly, Bbiofertilizer^ is crobial inoculants are found to differ greatly under different amisnomer andtheterm Bmicrobial inoculants^ better suit agro-environmental conditions and this has resulted in incon- sistency in responses across crops and regions (Table 1). There are also reports on the efficacy of microbial inoculants on particular varieties of crops, but not others. For example, the * Saritha Mohanram sarithamohanram@gmail.com Rhizobium strain G , which increased the yield of four chick- pea varieties—T ,Gwalior ,G-130, andPusa-53—was inef- 3 2 fective on the varieties R.S.II and N-59 (Sundara Rao 1974). Division of Integrated Farming System, ICAR-Central Arid Zone Research Institute, Jodhpur, Rajasthan 342003, India This suggests the host plant-specificity and strain-specificity 308 Ann Microbiol (2019) 69:307–320 Table 1 Varied responses of crops to microbial inoculation Microbial inoculant Crop Remarks Reference Bacillus megaterium Vegetable crops, grains, Yield increases of 0%–70% Smith et al. (1961) and potatoes Rhizobium Chickpea Yield ranging from 30 to 610 kg/ha Subba Rao (1976) Arbuscular mycorrhizal fungi Various crops Negative interactions to 14-fold yield Black and Tinker (1979), McGonigle (1988), increase Owusu-Bennoah and Mosse (1979) Associative nitrogen-fixing bacteria Rice Yield increases of 10%–30% Chongbiao (1990) Azotobacter Wheat Yield ranging from 34 to 247 kg/ha Hegde and Dwivedi (1994) Azospirillum brasilense and Flax and cereals Yield increases of 8%–30% Mikhailouskaya and Bogdevitch (2009) Bacillus circulans Azospirillum Wheat 12.9%–22.5% increase in dry weight Veresoglou and Menexes (2010) Pseudomonas, Azospirillum, Maize, wheat, sunflower, Yield increases of 19%–40% Rubin et al. (2017) Azotobacter, Bacillus lettuce associated with microbial inoculants. Several physical, chem- plant root exudates; (b) detritusphere, the soil region associat- ical, and biological factors affect the survival and functioning ed with decomposition of plant litter and turnover of soil or- of microorganisms in the soil. Soil water deficit and high ganic matter; (c) biopores, formed by deep growing roots and temperature are the major abiotic factors that affect their per- burrowing fauna; and (d) the soil aggregate surfaces (Kautz formance in dryland agriculture. Inadequacy of soil organic 2015;Krameretal. 2016; Kuzyakov and Blagodatskaya matter further aggravates the problem as the non-symbiotic 2015). These regions provide inputs of labile and recalcitrant microorganisms depend on organic matter for energy and organics for bioprocesses and are also relevant with respect to growth. Microbial inoculation in soil also influences the ac- the factors like soil moisture, oxygen availability, and nitrogen tivity of indigenous microflora, ultimately having a bearing on nutrition, which limit microbial activity (Kuzyakov and their own survival (Ramos et al. 2003). This is because the Blagodatskaya 2015). introduced microorganism must adhere to the plant roots, The localized availability of labile carbon and other compete for space and nutrients released through root exuda- readily utilizable nutrients leads to a concentration of tion, and must be able to occupy the new niche in sufficient events like respiration, gas exchange, nutrient and moisture numbers so as to exert its effect on the host plant (Barriuso utilization, and other bioprocesses in the rhizosphere et al. 2008b). Often, the native inhabitants of soil, which are (Richter et al. 2011). The major phenomenon underlying better adapted to the environmental conditions, outcompete the establishment of such distinct rhizosphere characteris- the inoculated population. Development of an effective micro- tic is rhizodeposition, wherein plant roots secrete a wide bial inoculant thus requires the presence of multiple fitness range of low- and high-molecular weight compounds in- traits that can facilitate its colonization and survival under cluding sugars, organic acids, amino acids, polysaccha- harsh environmental conditions (Rana et al. 2011). To facili- rides, vitamins, and other secondary metabolites into the tate this, bioprospecting for more tolerant strains and novel surrounding soil (Badri and Vivanco 2009). These methodologies for understanding the plant-microbe interac- rhizodeposits account for ∼ 11% of net photosynthetically tions are necessitated. fixed carbon and 10–16% of total plant nitrogen (Jones et al. 2009). These exudates play an important role in shap- ing the rhizosphere by altering soil chemistry in the imme- The rhizospheric hotspot of plant microbiome diate vicinity of plant roots and by serving as substrates for the growth of selected soil microorganisms (Yang and In spite of the vast microbial diversity in soil, microorganisms Crowley 2000). Components of plant root exudates get are congregated in small pockets which constitute only 1% of varied, both qualitatively and quantitatively, depending the total soil volume (Young et al. 2008). These microhabitats on the nutritional status of the plant, growth stage, and wherein microorganisms are aggregated to form colonies or even in time and space relative to the position of the root biofilms are characterized by faster rates of different biogeo- (Hartmann et al. 2009;Malusàet al. 2016). This creates a chemical processes than bulk soil (Kuzyakov 2009). strong selective pressure in the rhizosphere leading to a Kuzyakov and Blagodatskaya (2015) defined these soil vol- plant-driven selection of specific rhizosphere microbial umes as Bmicrobial hotspots^ and identified four such communities. Interestingly, only 2–5% of the rhizosphere hotspots in soil. These include (a) rhizosphere, the region of microorganisms promote plant growth (Antoun and Kloepper 2001) and plants naturally select for these soil surrounding living roots which is under the influence of Ann Microbiol (2019) 69:307–320 309 beneficial microorganisms which help in their growth and for photosynthates and for some of the genes involved in survival, especially under constrained conditions (Lareen nitrogen fixation (Hunter 2016). Mycorrhizal fungi enhance et al. 2016). The rhizosphere microorganisms may also the nutrient absorptive capacity of roots by increasing the enter the roots and migrate to the plant’s aerial surfaces effective surface area and the release of hydrolytic enzymes. (phyllosphere) (Thapa and Prasanna 2018) and internal tis- Besides nutrient translocation, mycorrhizae also improve soil sues (endosphere). Hence, plants are often associated with structure by creating stable soil aggregates (Rillig 2004). The communities of microorganisms, living on or within them, similarity in signaling crosstalk and the similar cellular re- exhibiting mutually beneficial symbioses. This entire ge- sponses of the rhizobial and mycorrhizal symbionts led to nome of microbial community, referred to as the the establishment that the rhizobium-legume symbiosis re- microbiome, plays vital roles in host’s nutrient uptake, cruited mechanisms established to support the more ancient metabolic capabilities and tolerance to biotic and abiotic endosymbiotic relationship with arbuscular mycorrhizal fungi stresses (Bulgarelli et al. 2013; Sessitsch and Mitter 2015). (Rogers and Oldroyd 2014; Streng et al. 2011). However, Therefore, defining a host plant’s core distinct microbiome understanding the fundamental differences between the two that supports its growth is the preliminary step in improv- responses is crucial in realizing the age-old dream of develop- ing the plant’s characteristic traits. ing in planta systems to transform cereals into autonomous N- fixing plants, by engineering into them the legume symbiosis pathway (Geurts et al. 2012). Significance of plant microbiome on crop Several other nitrogen-fixing endophytic and free-living growth rhizobacteria of the genera Bradyrhizobium, Azotobacter, Pseudomonas, Azospirillum, Bacillus, Burkholderia,and In an ecological perspective, plants are more than individual Achromobacter have been found to have positive impacts on entities as they co-habit with the plant microbiota that impact crops by enhancing both above and belowground biomass plant growth and productivity. The microbial diversity of soil (Guimarães et al. 2012; Gyaneshwar et al. 2011; Igiehon and and rhizosphere microbiomes is highly underestimated as only Babalola 2018). Several phosphate-solubilizing bacteria 5% of microorganisms have been cultured by current method- (Pseudomonas, Bacillus, Alcaligenes, Aerobactor) and fungi ologies (Mendes et al. 2013). The plant-associated (Aspergillus, Penicillium, Fusarium, Chaetomium, microbiomes consist of beneficial organisms like nitrogen- Cephalosporium) are also important members of the plant fixing bacteria, mycorrhizal fungi, other plant growth- microbiome (Chen et al. 2006; Sharma et al. 2013; Uribe promoting rhizobacteria (PGPR), and biocontrol agents, as et al. 2010). They increase the solubility of inorganic phos- well as organisms that are deleterious to plant growth like phorus (P) by releasing protons, OH ,or CO , and organic pathogenic microorganisms. Next-generation sequencing acid anions such as citrate, malate, and oxalate and can also technologies based on 16S rRNA gene have illustrated the mineralize organic P by release of various phosphatase en- vast diversity of microorganisms, particularly bacteria, present zymes (Marschner et al. 2010). Rhizosphere microorganisms in the core microbiome of plants (Table 2). Hawkes et al. also facilitate the uptake of trace elements such as iron (Fe) (2007) conducted a meta-analysis of clone libraries obtained and zinc (Zn). Microorganisms release organic acid anions or 3+ from the rhizosphere of 14 different plant species and found siderophores that chelate ferric ion (Fe ) and transfer it to the that the plants were associated with more than 1200 bacterial cell surface where it gets reduced to the soluble ferrous ion 2+ taxa and the phylum Proteobacteria was the most dominant. (Fe ) (Mendes et al. 2013). These siderophores include These assemblages of plants and microorganisms deal with enterobactin, pyoverdine, and ferrioxamines produced by bac- perturbations in the surroundings by detecting and responding teria and ferrichromes produced by fungi (Marschner et al. to environmental stimuli, resulting in specific adjustments in 2010). Fluorescent pseudomonads have been found to pro- their growth and development. As opined by Gopal and Gupta mote iron nutrition via siderophores for Graminaceous as well (2016), the overall fitness of the plant depends greatly on the as dicotyledonous plant species (Shirley et al. 2011). ecological services of plant-associated microorganisms that Rhizosphere microorganisms (Curtobacterium, Plantibacter, include biofertilization, protection from diseases and tolerance Pseudomonas, Stenotrophomonas, Streptomyces) are also to abiotic stresses. known to mobilize zinc (Zn) by acidification of medium via gluconic acid production (Costerousse et al. 2018; Whiting Role of plant microbiome in nutrient acquisition et al. 2001). The rhizosphere microbiome also plays an important part Research on plant microbiome actually started with the earli- in organic matter decomposition which enhances soil fertility est observations of legume-Rhizobium and mycorrhizal sym- and ultimately improves plant productivity. Lignocellulolytic biotic relationships. Rhizobia fix atmospheric nitrogen in a fungi like Trichoderma harzianum, Pleurotus ostreatus, form that is utilized by legumes and in turn depend on host Polyporus ostriformis,and Phanerochaete chrysosporium 310 Ann Microbiol (2019) 69:307–320 Table 2 Vast diversity of Host plant Dominant members of the rhizosphere microbiome Reference microorganisms identified in the rhizosphere microbiome of plants Oak (Characterized by 16S rRNA gene sequencing) identified Uroz et al. (2010) 5619 bacterial OTUs (operational taxonomic unit) with 38% Proteobacteria,24% Acidobacteria,11% Actinobacteria, and 20% unclassified bacteria Sugarbeet (Characterized by 16S rRNA gene microarray) Mendes et al. (2011) Detected 33,346 bacterial and archaeal OTUs, of which 39% were Proteobacteria (Gamma-and Betaproteobacteria), 20% were Firmicutes,9% were Actinobacteria Rice (Characterized by 16S rRNA gene sequencing) Edwards et al. (2015) Bacteroidetes, Firmicutes, Chloroflexi,and Betaproteobacteria (Rhodocyclaceae, Comamonadaceae), Alphaproteobacteria, Deltaproteobacteria Sugarcane (Characterized by 16S rRNA gene sequencing) Yeoh et al. (2016) Betaproteobacteria (Undibacterium, Burkholderia), Alphaproteobacteria (Bradyrhizobium, Rhizobium), Bacteroidetes (Niastella, Chitinophaga), Gammaproteobacteria (Dyella, Frateuria), Actinobacteria (Streptomyces, Cryocola), Chloroflexi and Firmicutes (Bacillus) Sugarcane (Characterized by sequencing of 16S and ITS ribosomal de Souza et al. (2016) RNA genes) Identified 23,811 bacterial OTUs and 11,727 fungal OTUs. Major families were Chitinophagaceae, Rhodospirillaceae, Hyphomicrobiaceae, Burkholderiaceae, Rhizobiaceae, Sphingobacteriaceae, Sphingomonadaceae, Sistotremataceae, Meruliaceae, Ceratocystidaceae, Chaetosphaeriaceae, Glomeraceae Oilseed rape (Characterized by RNA stable isotope probing and Gkarmiri et al. (2017) high-throughput sequencing) Verrucomicrobia, Proteobacteria, Planctomycetes, Acidobacteria, Gemmatimonadetes, Actinobacteria, Flavobacterium, Rhodoplanes, Sphingomonas, Streptomyces, Chloroflexi, Rhizobium Arabidopsis thaliana (Characterized by sequencing of the ITS2 region) Urbina et al. (2018) Ascomycetes (542 OTUs) and Basidiomycetes (145 OTUs) were the abundant phyla, and Archaeorhizomycetes, Leotiomycetes, Dothideomycetes, Eurotiomycetes and Sordariomycetes were the abundant classes Canola (Characterized by sequencing of 16S and ITS ribosomal Lay et al. (2018) RNA genes) Identified 6376 bacterial OTUs, 679 fungal OTUs and 49 archaeal OTUs, including Amycolatopsis sp., Serratia proteamaculans, Pedobacter sp., Arthrobacter sp., Stenotrophomonas sp., Fusarium merismoides, Fusicolla sp. Blueberry (Characterized by 16S rRNA and 18S rRNA gene Yurgel et al. (2018) sequencing) Abundant bacterial classes were Proteobacteria (Alphaproteobacteria and Gammaproteobacteria), Acidobacteria, Actinobacteria, Bacteroidetes, Saprospirae, Chloroflexi, Ktedonobacteria,and Verrucomicrobia Spartobacteria. Fungal taxa identified were Ascomycota, Basidiomycota, Mucoromycota, Glomeromycota,and Chytridiomycota and bacteria like Pseudomonas sp., Cellulomonas sp., nutrition, but also for plant nutrition (Ahmed et al. 2018; Cytophaga sp., Sporocytophaga sp., Chryseobacterium Mendes et al. 2013; Singh and Nain 2014; Woo et al. 2014). gleum,and Streptomyces sp. are known to degrade plant bio- The plant microbiome, therefore, facilitates the growth of mass, thereby releasing nutrients not only for their own plants even in nutrient-poor soils. Ann Microbiol (2019) 69:307–320 311 Role of plant microbiome in protection polyphenol oxidase, and phenylalanine ammonia lyase, en- from pathogens and host immunity hanced phytoalexin production, and enhanced expression of stress-related genes (Heil and Bostock 2002;Whipps 2001;Yi The rhizosphere antagonistic microorganisms ward off patho- et al. 2013). Therefore, multiple microbial interactions in the gens by producing antibiotics or hydrolytic enzymes and also rhizosphere provide enhanced biocontrol against pathogens, by competing for nutrients and space (Caravaca et al. 2015; besides modulating the plant immune system. Raaijmakers and Mazzola 2012). Antimicrobial metabolites produced by microorganisms include ammonia, butyrolactones, oligomycin A, phenazine-1-carboxylic acid Role of plant microbiome in tolerance to abiotic (PCA), pyoluterin, pyrrolnitrin, and other moieties (Wackett stresses 2013; Whipps 2001). Pseudomonas fluorescens suppresses soilborne pathogens like Meloidogyne incognita and Rhizosphere microorganisms, with their intrinsic metabolic Fusarium oxysporum by production of the antibiotic 2,4- and genetic capabilities, contribute to alleviate abiotic stresses diacetylphloroglucinol (DAPG) (Meyer et al. 2016). Bacteria in plants (Gopalakrishnan et al. 2015). Several microflora of are also known to parasitize and degrade spores of fungal plant the genera Pseudomonas, Bacillus, Achromobacter, pathogens through the production of extracellular cell wall- Burkholderia, Enterobacter, Azotobacter, Methylobacterium, degrading enzymes such as chitinase and β-1,3 glucanase and Trichoderma have been widely studied in plant growth (Whipps 2001). Most microbial biocontrol strains produce promotion by mitigation of multiple kinds of abiotic stresses more than one antibiotic compound with varying degrees of (Atieno et al. 2012; Meena et al. 2017; Sorty et al. 2016). antimicrobial activity. Agrobacterium radiobacter produces Wheat inoculated with Burkholderia phytofirmans PsJN re- agrocin 84, which is antibiotic to closely related strains, and ported an increased photosynthesis, high chlorophyll content, polyketide antibiotics which are broad-spectrum in nature and grain yield than the control under water deficit in field (Raaijmakers et al. 2010). Bacterial iron chelators also effec- conditions (Naveed et al. 2014). Treatment of Indian mustard tively play a role in the biocontrol of pathogens by sequester- (Brassica juncea) with the fungus, Trichoderma harzianum, ing the available iron and making it unavailable to pathogenic improved the uptake of essential nutrients and enhanced ac- microorganisms, thereby restricting their growth. cumulation of antioxidants and osmolytes and decreased Na Siderophores produced by Bacillus subtilis significantly man- uptake under saline conditions (Ahmad et al. 2015). Better aged the Fusarium wilt of pepper caused by Fusarium root colonizing capability of Pseudomonas sp. along with its oxysporum (Yu et al. 2011). Siderophores produced by ability to produce exopolysaccharides led to enhanced toler- Aspergillus niger, Penicillium citrinum,and Trichoderma ance towards salinity (Sen and Chandrasekhar 2014). Volatile harzianum were found to be effective biocontrol agents and organic carbons emitted from Bacillus subtilis GB03 were enhanced the growth of chickpeas (Cicer arietinum)(Yadav found to downregulate the HKT1 (high-affinity K transport- et al. 2011). er 1) expression in roots of Arabidopsis and upregulate it in Rhizobacteria, particularly Pseudomonas and Bacillus, shoots, resulting in lower Na accumulation throughout the could also act as elicitors for inducing systemic resistance plant thereby inducing tolerance to salt stress (Zhang et al. against pathogens in some plants. The siderophores produced 2008). Srivastava et al. (2008) isolated a thermotolerant by Pseudomonas aeruginosa, pyoverdine, pyochelin, and its Pseudomonas putida strain NBR10987 from drought- precursor salicylic acid (SA), can induce resistance to diseases stressed rhizosphere of chickpea and the strain was able to caused by Botrytis cinerea on bean and tomato, combat stress by producing exopolysaccharides with unique Colletotrichum lindemuthianum on bean, and tobacco mosaic water holding characteristics. Rhizosphere microorganisms virus on tobacco (Bigirimana and Höfte 2002; Höfte and also increase tolerance to low nonfreezing temperatures Bakker 2007). Similarly, the catechol-type siderophore pro- resulting in higher and faster accumulation of stress-related duced by Serratia marcescens 90-166 induces resistance to proteins and metabolites (Theocharis et al. 2012). Novel fungal, viral, and bacterial pathogens such as Colletotrichum stress tolerant bacteria such as Brachybacterium orbiculare, Fusarium oxysporum, cucumber mosaic virus, saurashtrense, Zhihengliuella sp., and Brevibacterium casei Pseudomonas syringae,and Erwinia tracheiphila in cucum- have also been reported from plant rhizospheres (Jha et al. ber (Press et al. 2001). The rhizobacterial association trigger 2012). Moreover, the bacteria such as Pseudomonas, either the salicylic acid dependent signal transduction pathway Microbacterium, Verrucomicrobia, and Actinobacteria and or the jasmonic acid and ethylene signaling pathway for pro- fungi such as Lewia sp. and mycorrhizal fungi are potential tection against pathogens (Ton et al. 2002). Plants with such candidates for rhizoremediation as they alter the mobility and induced resistance show strengthening of epidermal and cor- bioavailability of metals, thereby increasing their uptake by tical cell walls by deposition of callose, lignin, and phenolics, plants (Cruz-Hernández et al. 2012;Kawasakietal. 2012; increased levels of enzymes such as chitinase, peroxidase, Yang et al. 2016). 312 Ann Microbiol (2019) 69:307–320 Role of plant microbiome in phytohormone Bacteria and fungi are two major groups of the plant production microbiome, and their interactions via antibiosis, modulation of the physiochemical environment, cooperative metabolism, Plant growth-promoting rhizobacteria and fungi are known to protein secretion, or even gene transfer can lead to either an- improve plant growth by the production of phytohormones. tagonism or cooperation (Chen et al. 2018; Frey-Klett et al. These plant hormones are mostly synthesized as secondary 2007). This implies that an alteration of the rhizosphere char- metabolites as they are not essential for the growth and repro- acteristics can influence plant growth and in this context, duction of microorganisms (Shi et al. 2017). Gibberellins were shaping the rhizosphere microbiome provides a sound alter- firstly discovered when it was noticed that a chemical synthe- native for the conventional microbial inoculation. sized in Gibberella fujikuroi can contribute to the disease of rice plants (Kurosawa 2003). Gibberellins can stimulate plant growth and regulate various developmental processes like Engineering a biased rhizosphere to promote seed germination, stem elongation, sex expression, and fruit plant-microbe interactions formation (Bömke and Tudzynski 2009). Production of gibberellin-like substances have been reported in numerous Taking into account the role of plant root exudates in attracting bacterial genera including Azospirillum sp., Rhizobium sp., rhizosphere microorganisms, altering the root exudate compo- Acetobacter diazotrophicus, Herbaspirillum seropedicae, sition, both qualitatively and quantitatively, is a major ap- Bacillus sp., and Fusarium moniliforme (Bottini et al. 2004; proach to reshape the rhizosphere microbiome. The creation Meleigy and Khalaf 2009). Auxin and cytokinin production of a Bbiased rhizosphere^ is a novel procedure which involves are thought to be involved in root growth stimulation by ben- the expression of specific genes in transgenic plants that eficial bacteria and in associative symbiosis. Auxin biosynthe- would enable roots to produce the specific nutritional com- sis by Pseudomonas, Agrobacterium, Rhizobium, pound, which can be used or recognized by specific beneficial Bradyrhizobium, Azospirillum, Botrytis, Aspergillus,and microorganisms (Reddy et al. 2002; Savka et al. 2013). The Rhizopus are well studied (Costacurta and Vanderleyden goal of rhizosphere engineering is to direct the plant-microbe 1995; Hui et al. 2007). Apart from synthesis, plant- interaction towards enhanced beneficial outcomes including associated microorganisms also alter the hormonal signaling nutrient cycling, mineralization and organic matter decompo- in plants, in response to environmental stimuli. As stated in a sition, tolerance to drought, salinity and other abiotic stresses, previous section, the systemic resistance response induced in and resistance to diseases (Marasco et al. 2012; Quiza et al. plants by beneficial rhizobacteria is in many cases regulated 2015). The methods of application of microbial inoculants in by the phytohormones jasmonic acid and ethylene (Zamioudis soil, employment of tillage, plant breeding approaches, and and Pieterse 2012). Therefore, microorganism-mediated phy- the use of fungicides and antibiotics for plant protection are, tohormone production is a potent mechanism to alter plant to a certain extent, conventional rhizosphere modification physiology, leading to diverse outcomes from pathogenesis strategies. The application of plant growth-promoting to promotion of plant growth (Spaepen 2014). rhizobacteria (PGPR), nitrogen fixers, phosphate solubilizers, and arbuscular mycorrhizal fungi (AMF) improve plant per- Role of microbiome in impairing plant health formance by enhancing nutrient availability, phytohormone and productivity production, and pathogen control. But, maintenance of high population densities of these microorganisms after inoculation Besides plant growth-promoting microorganisms, the root is a major constraint owing to their decline over time and microbiome also consists of rhizosphere microorganisms distance from the inoculum source (O’Callaghan et al. 2001; which are detrimental to plants, competing for nutrients and Quiza et al. 2015). Similarly, tillage, plant protection mea- space. Plant pathogenic fungi, bacteria, and nematodes cause sures, and cultivar selection may induce soil vulnerability, various plant diseases resulting in substantial economic dam- even though they may influence microbial populations by age to crops. Agrobacterium tumefaciens, Ralstonia inhibiting or enhancing the growth of soil microorganisms solanacearum, Dickeya sp., Pectobacterium carotovorum, (Bakker et al. 2012; Brussaard et al. 2007). Consequently, Pythium sp., Phytopthora sp., Fusarium oxysporum, the avenue of rhizosphere microbiome engineering has Rhizoctonia sp., Gaeumannomyces graminis, Colletotrichum emerged which aims to alter the rhizosphere to express a bias sp., and Magnaporthe oryzae are a few of the major plant towards beneficial microorganisms enabling plants to evolve pathogenic microorganisms prevalent in soils (Dean et al. into better hosts. It harnesses the variations in plant root exu- 2012; Doehlemann et al. 2017; Mansfield et al. 2012). The dation patterns in order to enhance the favorable rhizosphere phenolic compounds present in plant root exudates, in low microbiome (Philippot et al. 2013; Quiza et al. 2015). Genetic concentrations, facilitate conidial germination, while in higher alteration of root exudation patterns could influence microbial communities by enhancing or inhibiting the growth of concentrations; inhibit mycelia growth (Mendes et al. 2013). Ann Microbiol (2019) 69:307–320 313 selected microorganisms. The important strategies for rhizo- to remain active for a long time in the detached border cells sphere modification being researched widely include the ma- and the transgenic potato plants expressed 94.9% resistance to nipulation of root border cells, engineering of inhibitors and the potato cyst nematode Globodera pallid (Lilley et al. 2011). enhancers, and induction of microbial gene expression in host Similarly, the expression of Cry proteins in roots and border plant cells. cells of transgenic cotton, which are involved in controlling lepidopteran pests, was investigated by Knox et al. (2007). Tailoring root border cells for creation of biased ELISA was used to quantify the in vitro expression of rhizoshere Cry1Ac and Cry2Ab proteins in root border cells of transgenic cultivars of cotton and it was found to be constitutive and at In the process of exudation, roots are found to release a group detectable levels (Knox et al. 2007). of metabolically active cells known as border cells into the Root border cells are also found to impart resistance to surrounding soil (O'Connell et al. 1996). These are actually aluminum (Al) toxicity (Yu et al. 2009). The responses of root the sloughed-off root cap cells, which are attached to the root apices of pea (Pisum sativum) to Al exposure in mist culture surface by a water-soluble polysaccharide matrix (Hawes et al. revealed that border cells enhanced the Al resistance of root 2000). In the presence of water, the middle lamellae of these apices by immobilizing Al in their cell-wall pectin (Yu et al. cells become solubilized by the action of pectinolytic enzymes 2009). Inhibition of root elongation, induction of callose syn- in the cell wall and get dispersed from root tips (Wen et al. thesis, and accumulation of Al were more pronounced in root 1999). These border cells serve in mucilage secretion, sensing apices stripped from border cells. Such border cell trapping of gravity, and other environmental signals, synthesis, and has also been found to be associated with cadmium, arsenic, export of extracellular chemicals, enzymes, antibiotics, and copper, lead, mercury, and nickel (Hawes et al. 2016;Huang sugars, which can rapidly attract and stimulate growth in some et al. 2009;Kopittkeetal. 2011;Zelko andLux 2003). Root microorganisms or repel and inhibit the growth of others, border cells are also reported to actively take up glucose, and thereby mediating rhizosphere processes (Hawes et al. 1998, also release it, thereby playing a significant role in the net 2000;Jian-Wei etal. 2002). More importantly, border cells glucose exchange in rhizosphere (Stubbs et al. 2004). These remain viable even after their detachment from the root cap aspects could be effectively utilized to drive the rhizospheric and are characterized by distinct mRNA and protein profiles characteristics towards better plant-microbe associations and with respect to that of the root cap cells (Brigham et al. 1995; plant growth. The ability of root border cells to produce mu- Zhu et al. 2004). The ability of border cells to engineer the cilage can be employed for better penetration of root tips chemical and physical properties of the external environment through hard soils and mineral surfaces for better uptake of has been demonstrated by their ability to attract fungal spores, water and nutrients. The negatively charged groups on side to repel pathogenic bacteria, to synthesize defensive structures chains of mucilagenous polysaccharides of root border cells 2+ against pathogen invasion, and to influence gene expression in can also facilitate attraction of cations like Ca , providing symbiotic bacteria (Gunawardena and Hawes 2002; Hawes exchange sites from which roots might absorb nutrients et al. 2000; Somasundaram et al. 2008). These cells, therefore, (Brundrett et al. 2016). In this way, the thousands of border are attractive targets to be engineered for developing a biased cells released by plant roots can be tailored to engineer the rhizosphere to facilitate association with beneficial rhizosphere to suit plant health and nutrition. microorganisms. Chemotactic attraction facilitating the association of plant Engineering inhibitors and enhancers in plants roots and border cells with soil microflora has been reported. to induce rhizosphere bias Hawes et al. (2000) studied the interaction of root knot nem- atode with root border cells of pea and found that the nema- Plants can be genetically modified to alter soil organic anion todes get attracted and immobilized by the border cells. efflux and transportation from roots by engineering plants Experiments also revealed that border cells synthesize and with a greater capacity to synthesize organic anions and to export into the surrounding mucilage, histone-linked extracel- transport them out of the cell (Quiza et al. 2015). Plants lular DNA (exDNA), which attracts, traps, and immobilizes engineered with higher ability to excrete citrate from the roots pathogens in a host-microbe-specific manner (Hawes et al. grew better on P-limited soil than the wild type, indicating 2012). Recently, molecular techniques are being used to their ability to grow in acid soils (Koyama et al. 1999). identify and manipulate the expression of plant genes that Root-secreted organic acids, such as malate and citrate, opti- control the production and specialized properties of border mize the carbon economy of soil microorganisms as they are cells in transgenic plants. Lilley et al. (2011) reported the easily consumed by the microflora (Wu et al. 2018). Also, the targeting of inhibitory peptides specifically to root border cells organic acid-chemotaxis regulates the recruitment of benefi- of potato using a root-cap-specific MDK4–20 promoter of cial rhizobacteria to the root surface (Rudrappa et al. 2008). In Arabidopsis thaliana. The AtMDK4-20 promoter was found tobacco and alfalfa plants genetically engineered to 314 Ann Microbiol (2019) 69:307–320 overproduce citric or malic acid, an increased colonization by class I β-1,3-glucanase gene in tomato resulted in increased mycorrhizal fungi and rhizobacteria has been reported resistance to Fusarium oxysporum f. sp. lycopersici with 36% (López-Bucio et al. 2000; Tesfaye et al. 2003). In other stud- to 58% reduction in disease severity (Jongedijk et al. 1995). ies, rhizosphere pH has been altered by over-expressing the Strittmatter et al. (1995) reported the inhibition of fungal path- genes controlling proton efflux from plant cells (Ryan et al. ogens by engineering controlled cell death in plants. The ex- 2009). Tobacco plants transformed with a modified plasma pression of bacterial ribonuclease barnase, driven simulta- membrane proton pump ATPase (H -ATPase) exhibited in- neously by a chimeric pathogen-inducible promoter (prp1-1) creased H -efflux from roots and a more acidic rhizosphere from potato and the CaMV 35S promoter, in order to avoid (Gévaudant et al. 2007). The edaphic variables, especially pH, detrimental effects of the RNAse, was studied and the induc- shape the structure and function of microbial communities in tion of barnase activity at the infection site was found to lead the rhizosphere (Fierer and Jackson 2006). However, Yuan to a significant reduction of Phytophthora infestans sporula- et al. (2008), by transcriptome profiling and functional analy- tion on leaves (Strittmatter et al. 1995). sis, have revealed that an acidic soil pH induces the virulence of Agrobacterium tumefaciens. Plants may also be engineered Engineering microbial signaling molecules in plants to promote the growth of desired microorganisms by releasing to bias the rhizosphere nutritional compounds which only the specific microorganism can catabolize (O'Connell et al. 1996). The phenomenon of Plants recognize and actively respond to different rhizosphere Agrobacterium tumefaciens mediated transfer of a region of microorganisms by producing signals that modulate microbial its plasmid DNA that encodes opine biosynthesis to plant cells colonization (Haichar et al. 2014). Hence, plant rhizosphere forms the basis of this strategy. Guyon et al. (1993)have may be modified by engineering plants to release microbial demonstrated that opines produced by roots of transgenic signal molecules like isoflavonoids or lipooligosaccharides plants increase the population of opine-catabolizing which induce microbial gene expression in the rhizosphere. Agrobacterium. Similar results have also been obtained by This method can be effectively utilized in ensuring nodule Mansouri et al. (2002) who reported that transgenic Lotus occupancy by the appropriate rhizobial species in leguminous plants producing opines specifically favor the growth of crop plants by utilizing nodule-specific compounds as growth opine-degrading rhizobacteria, irrespective of soil type and enhancers (Savka et al. 2002). The regulatory mechanism of plant species. quorum sensing, which involves the synthesis and accumula- Plants may also be engineered for the production of recom- tion of low-molecular weight signal molecules as a function of binant proteins in order to overcome the difficulties involved the population density of microbes producing these molecules in introducing complex antibiotic synthesis machinery in in a given environment, finds applications in this area (Savka plants for inhibiting the growth of antagonists. Transfer of et al. 2002). Several microbial functions like biofilm forma- genes encoding inhibitory proteins and peptides to plants en- tion, pathogenicity, and iron uptake are regulated via quorum ables their diffusion into the rhizosphere resulting in the sensing (Abisado et al. 2018; Rutherford and Bassler 2012). growth of only selected soil microorganisms. This approach The ability to generate bacterial quorum-sensing signaling is being studied for possible applications in the control of soil- molecules in the plant opens new avenues for manipulating borne pathogens. Pathogens infect plant tissues by producing the plant-microbe interactions. Some of the microbial signals a wide array of plant cell wall degrading enzymes. To prevent like the N-acyl-L-homoserine lactones (AHLs) and volatile this, polygalacturonase-inhibiting proteins (PGIPs) that inhibit organic compounds, which belong to a class of bacterial quo- the pectin-depolymerizing activity of polygalacturonases rum sensing signals from Gram-negative bacteria such as (PGs) secreted by microbial pathogens are made use of Pseudomonas, play a role in plant morphogenetic processes (Kalunke et al. 2015). Transgenic tomato plants, expressing (Ortíz-Castro et al. 2009). Transgenic tobacco and tomato a pear (Pyrus communis L.) PGIP (PcPGIP), capable of plants expressing the LasI gene from Pseudomonas inhibiting the PGs secreted by Bacillus cinerea showed 15% aeruginosa, responsible for the synthesis of AHLs have been and 25% reduction of disease lesions caused by the fungus on synthesized (Barriuso et al. 2008a). These AHLs produce get ripening fruit and leaves, respectively (Powell et al. 2000). In diffused across the plasma membranes into the rhizosphere, another study, Jach et al. (1995) detected high-level expres- where they have the potential to affect bacterial processes sion of genes transferred to tobacco for the production of regulated by such molecules (Ortíz-Castro et al. 2009). chitinase, β-1,3-glucanase, and ribosome-inactivating protein, Providing transgenic plants with the ability to block or de- under the control of the CaMV 35S-promoter. Fungal infec- grade AHL signals, otherwise termed as quorum quenching, tion assays revealed that the expression of individual genes may provide an alternative approach for engineering plant resulted in increased protection against the soil-borne fungal resistance to microbial pathogens. Transgenic tobacco and pathogen Rhizoctonia solani (Jach et al. 1995). Similarly, si- potato plants expressing the aiiA gene responsible for AHL multaneous expression of a tobacco class I chitinase and a degradation have shown resistance to Erwinia carotovora pv. Ann Microbiol (2019) 69:307–320 315 Pooling rhizosphere samples of crop species with specific phenotype carotovora infections even at very high bacterial inocula growing under different environmental and soil conditions (Dong et al. 2000). Future prospects of plant-microbiome associations Using this soil mixture as inoculum to inoculate crop plants grown under defined aseptic conditions The rhizosphere microbiome facilitates communication be- tween the plant and the surrounding soil environment and they together contribute to creating a productive metagenome which leads to improved crop productivity (Zorner et al. Using the inoculated soil from aseptically grown plants to inoculate fresh sets of crop plants under defined conditions 2018). Studies connecting comparative genomics and meta- bolomics have shown that specific rhizosphere bacteria are naturally selected depending on the root exudates contents (Zhalnina et al. 2018). For instance, comparison of wild and domesticated common bean (Phaseolus vulgaris) grown in Repeating the process for several generations using soil from agricultural soil revealed that as the genotype transitioned previous set as inoculum for the next generation from wild to domesticated, the relative abundance of Fig. 1 Process of identification of trait-specific microbiome associated Bacteroidetes (Chitinophagaceae and Cytophagaceae)de- with crop plants. The synergy of plant-microbiome associations forms the basis of this selection which can be utilized to enhance plant fitness and creased while Actinobacteria and Proteobacteria productivity (Nocardioidaceae and Rhizobiaceae) increased (Pérez- Jaramillo et al. 2017). The synergistic and complementary mechanisms among microorganisms and of plant-microbe in- plant traits including growth, flowering, and abiotic stress tol- teractions can be unveiled with the use of model plants grown erance have been reported (Bainard et al. 2013; Sugiyama under gnotobiotic conditions as such studies throw light into et al. 2013). Panke-Buisse et al. (2015) used a multi- the phenomenon of microbiome-mediated host plant immuni- generation experimental system using Arabidopsis thaliana ty (Sessitsch and Mitter 2015). Researchers have investigated Col to select for soil microbiomes inducing earlier or later immune responses elicited by plant microbiomes using the flowering times of their hosts. They found that the flowering FlowPot system (Kremer et al. 2016). Microbe-free seeds of phenotype was reproducible across plant hosts which showed Arabidopsis were grown in sterile, bottom-irrigated pots shifts in flowering time corresponding with the inoculation of alongside Arabidopsis colonized with diverse microbial com- early or late flowering microbiomes. Moreover, this resulted munities from various soils. Transcriptome profiling revealed in a mutual selection of plant host and the surrounding that colonized plants had significantly more defense- microbiome (Hunter 2016). As the host plants get co- associated transcripts involved in innate immunity, when ex- evolved with their microbiome, this strategy of microbiome posed to speck disease of tomatoes, caused by Pseudomonas selection could be adopted in future crop breeding strategies syringae pv tomato. The study also revealed a microbiome- for low-input sustainable agriculture. Also, the hologenome of influenced host and pathogen gene expression and suggested a host-microbiome association functions as an intermediate be- Bplant-pathogen-microbiome disease triangle^ concept for ad- tween the genotype-environment interaction in shaping the vanced studies of microbial pathogenesis and plant disease host plant phenotype (Hassani et al. 2018). Considering the resistance. The phenomenon of transfer of microbiome, from functional significance of plant-microbe interactions, an in- disease-suppressive soils to pathogen prevalent soils, for man- depth study into the microbiome function, particularly, the agement of crop diseases has also been reported (Gopal et al. microbiome constituents that are active during the different 2013; Turner et al. 2013). developmental stages of plant growth and their functions is Due to the direct influence of microbial interactions on needed (Mendes et al. 2013). plants and the ability of host plants to mediate microbiome Genetic improvement of plants focused on an efficient in- assembly, selection on a host-microbial association is an teraction with beneficial microorganisms and selection of ag- emerging approach to enhance plant fitness and productivity ricultural practices with less adverse effects on microbiome (Mueller and Sachs 2015). Protocols may be designed therefore need to be evolved (Gopal and Gupta 2016; targeting the selection of a characteristic host phenotype af- Sessitsch and Mitter 2015). Application of such works in the fected by the microbiome function which then gradually fa- field, as opined by Hunter (2016) would permit crops to ex- cilitates the transfer of specific trait-associated microbiomes ploit the beneficial microorganisms in soil, as several com- into new plant hosts (Fig. 1). Such studies describing the abil- mercial crop varieties have lost this capability due to injudi- ity of plant-associated microbiomes to influence different cious use of chemical amendments. 316 Ann Microbiol (2019) 69:307–320 development of vesicular-arbuscular mycorrhizal infection in barley Compliance with ethical standards and on the enophyte spore density. New Phytol 83:401–413 Bömke C, Tudzynski B (2009) Diversity, regulation, and evolution of the Conflicts of interest The authors declare that they have no conflict of gibberellin biosynthetic pathway in fungi compared to plants and interest. bacteria. Phytochem 70(15–16):1876–1893 Bottini R, Cassán F, Piccoli P (2004) Gibberellin production by bacteria Ethical approval No studies with humans/animals have been performed and its involvement in plant growth promotion and yield increase. by any of the authors for the purpose of this review article. Appl Microbiol Biotechnol 65:497 Brigham LA, Woo H-H, Nicoll SM, Hawes MC (1995) Differential ex- Informed consent Informed consent was obtained from all the authors pression of proteins and mRNAs from border cells and root tips of and the authors agreed to the manuscript being submitted to the journal. pea. 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Rhizosphere microbiome: revisiting the synergy of plant-microbe interactions

Annals of Microbiology , Volume 69 (4) – Feb 23, 2019

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References (166)

Publisher
Springer Journals
Copyright
Copyright © 2019 by Università degli studi di Milano
Subject
Life Sciences; Microbiology; Microbial Genetics and Genomics; Microbial Ecology; Mycology; Medical Microbiology; Applied Microbiology
ISSN
1590-4261
eISSN
1869-2044
DOI
10.1007/s13213-019-01448-9
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Abstract

Sustainable enhancement in food production from less available arable land must encompass a balanced use of inorganic, organic, and biofertilizer sources of plant nutrients to augment and maintain soil fertility and productivity. The varied responses of microbial inoculants across fields and crops, however, have formed a major bottleneck that hinders its widespread adoption. This necessitates an intricate analysis of the inter-relationships between soil microbial communities and their impact on host plant productivity. The concept of Bbiased rhizosphere,^ which evolved from the interactions among different components of the rhizosphere including plant roots and soil microflora, strives to garner a better understanding of the complex rhizospheric intercommunications. Moreover, knowledge on rhizosphere microbiome is essential for developing strategies for shaping the rhizosphere to benefit the plants. With the advent of molecular and Bomics^ tools, a better understanding of the plant-microbe association could be acquired which could play a crucial role in drafting the future Bbiofertilizers.^ The present review, therefore aims to (a) to introduce the concepts of rhizosphere hotspots and microbiomes and (b) to detail out the methodologies for creating biased rhizospheres for plant-mediated selection of beneficial microorganisms and their roles in improving plant performance. . . . . Keywords Biased rhizosphere Microbial inoculants Microbiome Rhizosphere engineering Root border cells Introduction these plant growth-promoting organisms, which are capable of exerting beneficial effects on plants. Generally, 60–90% of Biofertilizers are preparations containing specialized living the total applied fertilizer is lost and in this regard, microbial organisms that can fix, mobilize, solubilize, or decompose inoculants have prominence in sustainable integrated nutrient nutrient sources which, when applied through seed or soil, management systems (Bhardwaj et al. 2014). Moreover, the enhance nutrient uptake by plants. Biofertilizer research utility of poor-quality native nutrients in soil necessitates mi- started with BNitragin,^ the first commercially produced and crobial interventions. For example, approximately 90% of to- patented culture of Rhizobium, by Nobbe and Hiltner in 1895 tal soil K is found in crystalline, insoluble mineral forms like (Nobbe and Hiltner 1896). The introduction of yellow seeded feldspars and mica, which plants cannot utilize (Meena et al. soybean in India in the 1960s led to a spurt in demand for 2014). To make them available for plant nutrition, microor- soybean inoculants in the region. This intensified research in ganisms which can solubilize and release K should be development of microbial formulations for pulses, groundnut, deployed. and even forage legumes. The discovery of Azotobacter, While positive responses have been recorded in a range of Azospirillum, blue-green algae and a host of other beneficial field trials, the beneficial effects from the application of mi- microorganisms soon followed. Interestingly, Bbiofertilizer^ is crobial inoculants are found to differ greatly under different amisnomer andtheterm Bmicrobial inoculants^ better suit agro-environmental conditions and this has resulted in incon- sistency in responses across crops and regions (Table 1). There are also reports on the efficacy of microbial inoculants on particular varieties of crops, but not others. For example, the * Saritha Mohanram sarithamohanram@gmail.com Rhizobium strain G , which increased the yield of four chick- pea varieties—T ,Gwalior ,G-130, andPusa-53—was inef- 3 2 fective on the varieties R.S.II and N-59 (Sundara Rao 1974). Division of Integrated Farming System, ICAR-Central Arid Zone Research Institute, Jodhpur, Rajasthan 342003, India This suggests the host plant-specificity and strain-specificity 308 Ann Microbiol (2019) 69:307–320 Table 1 Varied responses of crops to microbial inoculation Microbial inoculant Crop Remarks Reference Bacillus megaterium Vegetable crops, grains, Yield increases of 0%–70% Smith et al. (1961) and potatoes Rhizobium Chickpea Yield ranging from 30 to 610 kg/ha Subba Rao (1976) Arbuscular mycorrhizal fungi Various crops Negative interactions to 14-fold yield Black and Tinker (1979), McGonigle (1988), increase Owusu-Bennoah and Mosse (1979) Associative nitrogen-fixing bacteria Rice Yield increases of 10%–30% Chongbiao (1990) Azotobacter Wheat Yield ranging from 34 to 247 kg/ha Hegde and Dwivedi (1994) Azospirillum brasilense and Flax and cereals Yield increases of 8%–30% Mikhailouskaya and Bogdevitch (2009) Bacillus circulans Azospirillum Wheat 12.9%–22.5% increase in dry weight Veresoglou and Menexes (2010) Pseudomonas, Azospirillum, Maize, wheat, sunflower, Yield increases of 19%–40% Rubin et al. (2017) Azotobacter, Bacillus lettuce associated with microbial inoculants. Several physical, chem- plant root exudates; (b) detritusphere, the soil region associat- ical, and biological factors affect the survival and functioning ed with decomposition of plant litter and turnover of soil or- of microorganisms in the soil. Soil water deficit and high ganic matter; (c) biopores, formed by deep growing roots and temperature are the major abiotic factors that affect their per- burrowing fauna; and (d) the soil aggregate surfaces (Kautz formance in dryland agriculture. Inadequacy of soil organic 2015;Krameretal. 2016; Kuzyakov and Blagodatskaya matter further aggravates the problem as the non-symbiotic 2015). These regions provide inputs of labile and recalcitrant microorganisms depend on organic matter for energy and organics for bioprocesses and are also relevant with respect to growth. Microbial inoculation in soil also influences the ac- the factors like soil moisture, oxygen availability, and nitrogen tivity of indigenous microflora, ultimately having a bearing on nutrition, which limit microbial activity (Kuzyakov and their own survival (Ramos et al. 2003). This is because the Blagodatskaya 2015). introduced microorganism must adhere to the plant roots, The localized availability of labile carbon and other compete for space and nutrients released through root exuda- readily utilizable nutrients leads to a concentration of tion, and must be able to occupy the new niche in sufficient events like respiration, gas exchange, nutrient and moisture numbers so as to exert its effect on the host plant (Barriuso utilization, and other bioprocesses in the rhizosphere et al. 2008b). Often, the native inhabitants of soil, which are (Richter et al. 2011). The major phenomenon underlying better adapted to the environmental conditions, outcompete the establishment of such distinct rhizosphere characteris- the inoculated population. Development of an effective micro- tic is rhizodeposition, wherein plant roots secrete a wide bial inoculant thus requires the presence of multiple fitness range of low- and high-molecular weight compounds in- traits that can facilitate its colonization and survival under cluding sugars, organic acids, amino acids, polysaccha- harsh environmental conditions (Rana et al. 2011). To facili- rides, vitamins, and other secondary metabolites into the tate this, bioprospecting for more tolerant strains and novel surrounding soil (Badri and Vivanco 2009). These methodologies for understanding the plant-microbe interac- rhizodeposits account for ∼ 11% of net photosynthetically tions are necessitated. fixed carbon and 10–16% of total plant nitrogen (Jones et al. 2009). These exudates play an important role in shap- ing the rhizosphere by altering soil chemistry in the imme- The rhizospheric hotspot of plant microbiome diate vicinity of plant roots and by serving as substrates for the growth of selected soil microorganisms (Yang and In spite of the vast microbial diversity in soil, microorganisms Crowley 2000). Components of plant root exudates get are congregated in small pockets which constitute only 1% of varied, both qualitatively and quantitatively, depending the total soil volume (Young et al. 2008). These microhabitats on the nutritional status of the plant, growth stage, and wherein microorganisms are aggregated to form colonies or even in time and space relative to the position of the root biofilms are characterized by faster rates of different biogeo- (Hartmann et al. 2009;Malusàet al. 2016). This creates a chemical processes than bulk soil (Kuzyakov 2009). strong selective pressure in the rhizosphere leading to a Kuzyakov and Blagodatskaya (2015) defined these soil vol- plant-driven selection of specific rhizosphere microbial umes as Bmicrobial hotspots^ and identified four such communities. Interestingly, only 2–5% of the rhizosphere hotspots in soil. These include (a) rhizosphere, the region of microorganisms promote plant growth (Antoun and Kloepper 2001) and plants naturally select for these soil surrounding living roots which is under the influence of Ann Microbiol (2019) 69:307–320 309 beneficial microorganisms which help in their growth and for photosynthates and for some of the genes involved in survival, especially under constrained conditions (Lareen nitrogen fixation (Hunter 2016). Mycorrhizal fungi enhance et al. 2016). The rhizosphere microorganisms may also the nutrient absorptive capacity of roots by increasing the enter the roots and migrate to the plant’s aerial surfaces effective surface area and the release of hydrolytic enzymes. (phyllosphere) (Thapa and Prasanna 2018) and internal tis- Besides nutrient translocation, mycorrhizae also improve soil sues (endosphere). Hence, plants are often associated with structure by creating stable soil aggregates (Rillig 2004). The communities of microorganisms, living on or within them, similarity in signaling crosstalk and the similar cellular re- exhibiting mutually beneficial symbioses. This entire ge- sponses of the rhizobial and mycorrhizal symbionts led to nome of microbial community, referred to as the the establishment that the rhizobium-legume symbiosis re- microbiome, plays vital roles in host’s nutrient uptake, cruited mechanisms established to support the more ancient metabolic capabilities and tolerance to biotic and abiotic endosymbiotic relationship with arbuscular mycorrhizal fungi stresses (Bulgarelli et al. 2013; Sessitsch and Mitter 2015). (Rogers and Oldroyd 2014; Streng et al. 2011). However, Therefore, defining a host plant’s core distinct microbiome understanding the fundamental differences between the two that supports its growth is the preliminary step in improv- responses is crucial in realizing the age-old dream of develop- ing the plant’s characteristic traits. ing in planta systems to transform cereals into autonomous N- fixing plants, by engineering into them the legume symbiosis pathway (Geurts et al. 2012). Significance of plant microbiome on crop Several other nitrogen-fixing endophytic and free-living growth rhizobacteria of the genera Bradyrhizobium, Azotobacter, Pseudomonas, Azospirillum, Bacillus, Burkholderia,and In an ecological perspective, plants are more than individual Achromobacter have been found to have positive impacts on entities as they co-habit with the plant microbiota that impact crops by enhancing both above and belowground biomass plant growth and productivity. The microbial diversity of soil (Guimarães et al. 2012; Gyaneshwar et al. 2011; Igiehon and and rhizosphere microbiomes is highly underestimated as only Babalola 2018). Several phosphate-solubilizing bacteria 5% of microorganisms have been cultured by current method- (Pseudomonas, Bacillus, Alcaligenes, Aerobactor) and fungi ologies (Mendes et al. 2013). The plant-associated (Aspergillus, Penicillium, Fusarium, Chaetomium, microbiomes consist of beneficial organisms like nitrogen- Cephalosporium) are also important members of the plant fixing bacteria, mycorrhizal fungi, other plant growth- microbiome (Chen et al. 2006; Sharma et al. 2013; Uribe promoting rhizobacteria (PGPR), and biocontrol agents, as et al. 2010). They increase the solubility of inorganic phos- well as organisms that are deleterious to plant growth like phorus (P) by releasing protons, OH ,or CO , and organic pathogenic microorganisms. Next-generation sequencing acid anions such as citrate, malate, and oxalate and can also technologies based on 16S rRNA gene have illustrated the mineralize organic P by release of various phosphatase en- vast diversity of microorganisms, particularly bacteria, present zymes (Marschner et al. 2010). Rhizosphere microorganisms in the core microbiome of plants (Table 2). Hawkes et al. also facilitate the uptake of trace elements such as iron (Fe) (2007) conducted a meta-analysis of clone libraries obtained and zinc (Zn). Microorganisms release organic acid anions or 3+ from the rhizosphere of 14 different plant species and found siderophores that chelate ferric ion (Fe ) and transfer it to the that the plants were associated with more than 1200 bacterial cell surface where it gets reduced to the soluble ferrous ion 2+ taxa and the phylum Proteobacteria was the most dominant. (Fe ) (Mendes et al. 2013). These siderophores include These assemblages of plants and microorganisms deal with enterobactin, pyoverdine, and ferrioxamines produced by bac- perturbations in the surroundings by detecting and responding teria and ferrichromes produced by fungi (Marschner et al. to environmental stimuli, resulting in specific adjustments in 2010). Fluorescent pseudomonads have been found to pro- their growth and development. As opined by Gopal and Gupta mote iron nutrition via siderophores for Graminaceous as well (2016), the overall fitness of the plant depends greatly on the as dicotyledonous plant species (Shirley et al. 2011). ecological services of plant-associated microorganisms that Rhizosphere microorganisms (Curtobacterium, Plantibacter, include biofertilization, protection from diseases and tolerance Pseudomonas, Stenotrophomonas, Streptomyces) are also to abiotic stresses. known to mobilize zinc (Zn) by acidification of medium via gluconic acid production (Costerousse et al. 2018; Whiting Role of plant microbiome in nutrient acquisition et al. 2001). The rhizosphere microbiome also plays an important part Research on plant microbiome actually started with the earli- in organic matter decomposition which enhances soil fertility est observations of legume-Rhizobium and mycorrhizal sym- and ultimately improves plant productivity. Lignocellulolytic biotic relationships. Rhizobia fix atmospheric nitrogen in a fungi like Trichoderma harzianum, Pleurotus ostreatus, form that is utilized by legumes and in turn depend on host Polyporus ostriformis,and Phanerochaete chrysosporium 310 Ann Microbiol (2019) 69:307–320 Table 2 Vast diversity of Host plant Dominant members of the rhizosphere microbiome Reference microorganisms identified in the rhizosphere microbiome of plants Oak (Characterized by 16S rRNA gene sequencing) identified Uroz et al. (2010) 5619 bacterial OTUs (operational taxonomic unit) with 38% Proteobacteria,24% Acidobacteria,11% Actinobacteria, and 20% unclassified bacteria Sugarbeet (Characterized by 16S rRNA gene microarray) Mendes et al. (2011) Detected 33,346 bacterial and archaeal OTUs, of which 39% were Proteobacteria (Gamma-and Betaproteobacteria), 20% were Firmicutes,9% were Actinobacteria Rice (Characterized by 16S rRNA gene sequencing) Edwards et al. (2015) Bacteroidetes, Firmicutes, Chloroflexi,and Betaproteobacteria (Rhodocyclaceae, Comamonadaceae), Alphaproteobacteria, Deltaproteobacteria Sugarcane (Characterized by 16S rRNA gene sequencing) Yeoh et al. (2016) Betaproteobacteria (Undibacterium, Burkholderia), Alphaproteobacteria (Bradyrhizobium, Rhizobium), Bacteroidetes (Niastella, Chitinophaga), Gammaproteobacteria (Dyella, Frateuria), Actinobacteria (Streptomyces, Cryocola), Chloroflexi and Firmicutes (Bacillus) Sugarcane (Characterized by sequencing of 16S and ITS ribosomal de Souza et al. (2016) RNA genes) Identified 23,811 bacterial OTUs and 11,727 fungal OTUs. Major families were Chitinophagaceae, Rhodospirillaceae, Hyphomicrobiaceae, Burkholderiaceae, Rhizobiaceae, Sphingobacteriaceae, Sphingomonadaceae, Sistotremataceae, Meruliaceae, Ceratocystidaceae, Chaetosphaeriaceae, Glomeraceae Oilseed rape (Characterized by RNA stable isotope probing and Gkarmiri et al. (2017) high-throughput sequencing) Verrucomicrobia, Proteobacteria, Planctomycetes, Acidobacteria, Gemmatimonadetes, Actinobacteria, Flavobacterium, Rhodoplanes, Sphingomonas, Streptomyces, Chloroflexi, Rhizobium Arabidopsis thaliana (Characterized by sequencing of the ITS2 region) Urbina et al. (2018) Ascomycetes (542 OTUs) and Basidiomycetes (145 OTUs) were the abundant phyla, and Archaeorhizomycetes, Leotiomycetes, Dothideomycetes, Eurotiomycetes and Sordariomycetes were the abundant classes Canola (Characterized by sequencing of 16S and ITS ribosomal Lay et al. (2018) RNA genes) Identified 6376 bacterial OTUs, 679 fungal OTUs and 49 archaeal OTUs, including Amycolatopsis sp., Serratia proteamaculans, Pedobacter sp., Arthrobacter sp., Stenotrophomonas sp., Fusarium merismoides, Fusicolla sp. Blueberry (Characterized by 16S rRNA and 18S rRNA gene Yurgel et al. (2018) sequencing) Abundant bacterial classes were Proteobacteria (Alphaproteobacteria and Gammaproteobacteria), Acidobacteria, Actinobacteria, Bacteroidetes, Saprospirae, Chloroflexi, Ktedonobacteria,and Verrucomicrobia Spartobacteria. Fungal taxa identified were Ascomycota, Basidiomycota, Mucoromycota, Glomeromycota,and Chytridiomycota and bacteria like Pseudomonas sp., Cellulomonas sp., nutrition, but also for plant nutrition (Ahmed et al. 2018; Cytophaga sp., Sporocytophaga sp., Chryseobacterium Mendes et al. 2013; Singh and Nain 2014; Woo et al. 2014). gleum,and Streptomyces sp. are known to degrade plant bio- The plant microbiome, therefore, facilitates the growth of mass, thereby releasing nutrients not only for their own plants even in nutrient-poor soils. Ann Microbiol (2019) 69:307–320 311 Role of plant microbiome in protection polyphenol oxidase, and phenylalanine ammonia lyase, en- from pathogens and host immunity hanced phytoalexin production, and enhanced expression of stress-related genes (Heil and Bostock 2002;Whipps 2001;Yi The rhizosphere antagonistic microorganisms ward off patho- et al. 2013). Therefore, multiple microbial interactions in the gens by producing antibiotics or hydrolytic enzymes and also rhizosphere provide enhanced biocontrol against pathogens, by competing for nutrients and space (Caravaca et al. 2015; besides modulating the plant immune system. Raaijmakers and Mazzola 2012). Antimicrobial metabolites produced by microorganisms include ammonia, butyrolactones, oligomycin A, phenazine-1-carboxylic acid Role of plant microbiome in tolerance to abiotic (PCA), pyoluterin, pyrrolnitrin, and other moieties (Wackett stresses 2013; Whipps 2001). Pseudomonas fluorescens suppresses soilborne pathogens like Meloidogyne incognita and Rhizosphere microorganisms, with their intrinsic metabolic Fusarium oxysporum by production of the antibiotic 2,4- and genetic capabilities, contribute to alleviate abiotic stresses diacetylphloroglucinol (DAPG) (Meyer et al. 2016). Bacteria in plants (Gopalakrishnan et al. 2015). Several microflora of are also known to parasitize and degrade spores of fungal plant the genera Pseudomonas, Bacillus, Achromobacter, pathogens through the production of extracellular cell wall- Burkholderia, Enterobacter, Azotobacter, Methylobacterium, degrading enzymes such as chitinase and β-1,3 glucanase and Trichoderma have been widely studied in plant growth (Whipps 2001). Most microbial biocontrol strains produce promotion by mitigation of multiple kinds of abiotic stresses more than one antibiotic compound with varying degrees of (Atieno et al. 2012; Meena et al. 2017; Sorty et al. 2016). antimicrobial activity. Agrobacterium radiobacter produces Wheat inoculated with Burkholderia phytofirmans PsJN re- agrocin 84, which is antibiotic to closely related strains, and ported an increased photosynthesis, high chlorophyll content, polyketide antibiotics which are broad-spectrum in nature and grain yield than the control under water deficit in field (Raaijmakers et al. 2010). Bacterial iron chelators also effec- conditions (Naveed et al. 2014). Treatment of Indian mustard tively play a role in the biocontrol of pathogens by sequester- (Brassica juncea) with the fungus, Trichoderma harzianum, ing the available iron and making it unavailable to pathogenic improved the uptake of essential nutrients and enhanced ac- microorganisms, thereby restricting their growth. cumulation of antioxidants and osmolytes and decreased Na Siderophores produced by Bacillus subtilis significantly man- uptake under saline conditions (Ahmad et al. 2015). Better aged the Fusarium wilt of pepper caused by Fusarium root colonizing capability of Pseudomonas sp. along with its oxysporum (Yu et al. 2011). Siderophores produced by ability to produce exopolysaccharides led to enhanced toler- Aspergillus niger, Penicillium citrinum,and Trichoderma ance towards salinity (Sen and Chandrasekhar 2014). Volatile harzianum were found to be effective biocontrol agents and organic carbons emitted from Bacillus subtilis GB03 were enhanced the growth of chickpeas (Cicer arietinum)(Yadav found to downregulate the HKT1 (high-affinity K transport- et al. 2011). er 1) expression in roots of Arabidopsis and upregulate it in Rhizobacteria, particularly Pseudomonas and Bacillus, shoots, resulting in lower Na accumulation throughout the could also act as elicitors for inducing systemic resistance plant thereby inducing tolerance to salt stress (Zhang et al. against pathogens in some plants. The siderophores produced 2008). Srivastava et al. (2008) isolated a thermotolerant by Pseudomonas aeruginosa, pyoverdine, pyochelin, and its Pseudomonas putida strain NBR10987 from drought- precursor salicylic acid (SA), can induce resistance to diseases stressed rhizosphere of chickpea and the strain was able to caused by Botrytis cinerea on bean and tomato, combat stress by producing exopolysaccharides with unique Colletotrichum lindemuthianum on bean, and tobacco mosaic water holding characteristics. Rhizosphere microorganisms virus on tobacco (Bigirimana and Höfte 2002; Höfte and also increase tolerance to low nonfreezing temperatures Bakker 2007). Similarly, the catechol-type siderophore pro- resulting in higher and faster accumulation of stress-related duced by Serratia marcescens 90-166 induces resistance to proteins and metabolites (Theocharis et al. 2012). Novel fungal, viral, and bacterial pathogens such as Colletotrichum stress tolerant bacteria such as Brachybacterium orbiculare, Fusarium oxysporum, cucumber mosaic virus, saurashtrense, Zhihengliuella sp., and Brevibacterium casei Pseudomonas syringae,and Erwinia tracheiphila in cucum- have also been reported from plant rhizospheres (Jha et al. ber (Press et al. 2001). The rhizobacterial association trigger 2012). Moreover, the bacteria such as Pseudomonas, either the salicylic acid dependent signal transduction pathway Microbacterium, Verrucomicrobia, and Actinobacteria and or the jasmonic acid and ethylene signaling pathway for pro- fungi such as Lewia sp. and mycorrhizal fungi are potential tection against pathogens (Ton et al. 2002). Plants with such candidates for rhizoremediation as they alter the mobility and induced resistance show strengthening of epidermal and cor- bioavailability of metals, thereby increasing their uptake by tical cell walls by deposition of callose, lignin, and phenolics, plants (Cruz-Hernández et al. 2012;Kawasakietal. 2012; increased levels of enzymes such as chitinase, peroxidase, Yang et al. 2016). 312 Ann Microbiol (2019) 69:307–320 Role of plant microbiome in phytohormone Bacteria and fungi are two major groups of the plant production microbiome, and their interactions via antibiosis, modulation of the physiochemical environment, cooperative metabolism, Plant growth-promoting rhizobacteria and fungi are known to protein secretion, or even gene transfer can lead to either an- improve plant growth by the production of phytohormones. tagonism or cooperation (Chen et al. 2018; Frey-Klett et al. These plant hormones are mostly synthesized as secondary 2007). This implies that an alteration of the rhizosphere char- metabolites as they are not essential for the growth and repro- acteristics can influence plant growth and in this context, duction of microorganisms (Shi et al. 2017). Gibberellins were shaping the rhizosphere microbiome provides a sound alter- firstly discovered when it was noticed that a chemical synthe- native for the conventional microbial inoculation. sized in Gibberella fujikuroi can contribute to the disease of rice plants (Kurosawa 2003). Gibberellins can stimulate plant growth and regulate various developmental processes like Engineering a biased rhizosphere to promote seed germination, stem elongation, sex expression, and fruit plant-microbe interactions formation (Bömke and Tudzynski 2009). Production of gibberellin-like substances have been reported in numerous Taking into account the role of plant root exudates in attracting bacterial genera including Azospirillum sp., Rhizobium sp., rhizosphere microorganisms, altering the root exudate compo- Acetobacter diazotrophicus, Herbaspirillum seropedicae, sition, both qualitatively and quantitatively, is a major ap- Bacillus sp., and Fusarium moniliforme (Bottini et al. 2004; proach to reshape the rhizosphere microbiome. The creation Meleigy and Khalaf 2009). Auxin and cytokinin production of a Bbiased rhizosphere^ is a novel procedure which involves are thought to be involved in root growth stimulation by ben- the expression of specific genes in transgenic plants that eficial bacteria and in associative symbiosis. Auxin biosynthe- would enable roots to produce the specific nutritional com- sis by Pseudomonas, Agrobacterium, Rhizobium, pound, which can be used or recognized by specific beneficial Bradyrhizobium, Azospirillum, Botrytis, Aspergillus,and microorganisms (Reddy et al. 2002; Savka et al. 2013). The Rhizopus are well studied (Costacurta and Vanderleyden goal of rhizosphere engineering is to direct the plant-microbe 1995; Hui et al. 2007). Apart from synthesis, plant- interaction towards enhanced beneficial outcomes including associated microorganisms also alter the hormonal signaling nutrient cycling, mineralization and organic matter decompo- in plants, in response to environmental stimuli. As stated in a sition, tolerance to drought, salinity and other abiotic stresses, previous section, the systemic resistance response induced in and resistance to diseases (Marasco et al. 2012; Quiza et al. plants by beneficial rhizobacteria is in many cases regulated 2015). The methods of application of microbial inoculants in by the phytohormones jasmonic acid and ethylene (Zamioudis soil, employment of tillage, plant breeding approaches, and and Pieterse 2012). Therefore, microorganism-mediated phy- the use of fungicides and antibiotics for plant protection are, tohormone production is a potent mechanism to alter plant to a certain extent, conventional rhizosphere modification physiology, leading to diverse outcomes from pathogenesis strategies. The application of plant growth-promoting to promotion of plant growth (Spaepen 2014). rhizobacteria (PGPR), nitrogen fixers, phosphate solubilizers, and arbuscular mycorrhizal fungi (AMF) improve plant per- Role of microbiome in impairing plant health formance by enhancing nutrient availability, phytohormone and productivity production, and pathogen control. But, maintenance of high population densities of these microorganisms after inoculation Besides plant growth-promoting microorganisms, the root is a major constraint owing to their decline over time and microbiome also consists of rhizosphere microorganisms distance from the inoculum source (O’Callaghan et al. 2001; which are detrimental to plants, competing for nutrients and Quiza et al. 2015). Similarly, tillage, plant protection mea- space. Plant pathogenic fungi, bacteria, and nematodes cause sures, and cultivar selection may induce soil vulnerability, various plant diseases resulting in substantial economic dam- even though they may influence microbial populations by age to crops. Agrobacterium tumefaciens, Ralstonia inhibiting or enhancing the growth of soil microorganisms solanacearum, Dickeya sp., Pectobacterium carotovorum, (Bakker et al. 2012; Brussaard et al. 2007). Consequently, Pythium sp., Phytopthora sp., Fusarium oxysporum, the avenue of rhizosphere microbiome engineering has Rhizoctonia sp., Gaeumannomyces graminis, Colletotrichum emerged which aims to alter the rhizosphere to express a bias sp., and Magnaporthe oryzae are a few of the major plant towards beneficial microorganisms enabling plants to evolve pathogenic microorganisms prevalent in soils (Dean et al. into better hosts. It harnesses the variations in plant root exu- 2012; Doehlemann et al. 2017; Mansfield et al. 2012). The dation patterns in order to enhance the favorable rhizosphere phenolic compounds present in plant root exudates, in low microbiome (Philippot et al. 2013; Quiza et al. 2015). Genetic concentrations, facilitate conidial germination, while in higher alteration of root exudation patterns could influence microbial communities by enhancing or inhibiting the growth of concentrations; inhibit mycelia growth (Mendes et al. 2013). Ann Microbiol (2019) 69:307–320 313 selected microorganisms. The important strategies for rhizo- to remain active for a long time in the detached border cells sphere modification being researched widely include the ma- and the transgenic potato plants expressed 94.9% resistance to nipulation of root border cells, engineering of inhibitors and the potato cyst nematode Globodera pallid (Lilley et al. 2011). enhancers, and induction of microbial gene expression in host Similarly, the expression of Cry proteins in roots and border plant cells. cells of transgenic cotton, which are involved in controlling lepidopteran pests, was investigated by Knox et al. (2007). Tailoring root border cells for creation of biased ELISA was used to quantify the in vitro expression of rhizoshere Cry1Ac and Cry2Ab proteins in root border cells of transgenic cultivars of cotton and it was found to be constitutive and at In the process of exudation, roots are found to release a group detectable levels (Knox et al. 2007). of metabolically active cells known as border cells into the Root border cells are also found to impart resistance to surrounding soil (O'Connell et al. 1996). These are actually aluminum (Al) toxicity (Yu et al. 2009). The responses of root the sloughed-off root cap cells, which are attached to the root apices of pea (Pisum sativum) to Al exposure in mist culture surface by a water-soluble polysaccharide matrix (Hawes et al. revealed that border cells enhanced the Al resistance of root 2000). In the presence of water, the middle lamellae of these apices by immobilizing Al in their cell-wall pectin (Yu et al. cells become solubilized by the action of pectinolytic enzymes 2009). Inhibition of root elongation, induction of callose syn- in the cell wall and get dispersed from root tips (Wen et al. thesis, and accumulation of Al were more pronounced in root 1999). These border cells serve in mucilage secretion, sensing apices stripped from border cells. Such border cell trapping of gravity, and other environmental signals, synthesis, and has also been found to be associated with cadmium, arsenic, export of extracellular chemicals, enzymes, antibiotics, and copper, lead, mercury, and nickel (Hawes et al. 2016;Huang sugars, which can rapidly attract and stimulate growth in some et al. 2009;Kopittkeetal. 2011;Zelko andLux 2003). Root microorganisms or repel and inhibit the growth of others, border cells are also reported to actively take up glucose, and thereby mediating rhizosphere processes (Hawes et al. 1998, also release it, thereby playing a significant role in the net 2000;Jian-Wei etal. 2002). More importantly, border cells glucose exchange in rhizosphere (Stubbs et al. 2004). These remain viable even after their detachment from the root cap aspects could be effectively utilized to drive the rhizospheric and are characterized by distinct mRNA and protein profiles characteristics towards better plant-microbe associations and with respect to that of the root cap cells (Brigham et al. 1995; plant growth. The ability of root border cells to produce mu- Zhu et al. 2004). The ability of border cells to engineer the cilage can be employed for better penetration of root tips chemical and physical properties of the external environment through hard soils and mineral surfaces for better uptake of has been demonstrated by their ability to attract fungal spores, water and nutrients. The negatively charged groups on side to repel pathogenic bacteria, to synthesize defensive structures chains of mucilagenous polysaccharides of root border cells 2+ against pathogen invasion, and to influence gene expression in can also facilitate attraction of cations like Ca , providing symbiotic bacteria (Gunawardena and Hawes 2002; Hawes exchange sites from which roots might absorb nutrients et al. 2000; Somasundaram et al. 2008). These cells, therefore, (Brundrett et al. 2016). In this way, the thousands of border are attractive targets to be engineered for developing a biased cells released by plant roots can be tailored to engineer the rhizosphere to facilitate association with beneficial rhizosphere to suit plant health and nutrition. microorganisms. Chemotactic attraction facilitating the association of plant Engineering inhibitors and enhancers in plants roots and border cells with soil microflora has been reported. to induce rhizosphere bias Hawes et al. (2000) studied the interaction of root knot nem- atode with root border cells of pea and found that the nema- Plants can be genetically modified to alter soil organic anion todes get attracted and immobilized by the border cells. efflux and transportation from roots by engineering plants Experiments also revealed that border cells synthesize and with a greater capacity to synthesize organic anions and to export into the surrounding mucilage, histone-linked extracel- transport them out of the cell (Quiza et al. 2015). Plants lular DNA (exDNA), which attracts, traps, and immobilizes engineered with higher ability to excrete citrate from the roots pathogens in a host-microbe-specific manner (Hawes et al. grew better on P-limited soil than the wild type, indicating 2012). Recently, molecular techniques are being used to their ability to grow in acid soils (Koyama et al. 1999). identify and manipulate the expression of plant genes that Root-secreted organic acids, such as malate and citrate, opti- control the production and specialized properties of border mize the carbon economy of soil microorganisms as they are cells in transgenic plants. Lilley et al. (2011) reported the easily consumed by the microflora (Wu et al. 2018). Also, the targeting of inhibitory peptides specifically to root border cells organic acid-chemotaxis regulates the recruitment of benefi- of potato using a root-cap-specific MDK4–20 promoter of cial rhizobacteria to the root surface (Rudrappa et al. 2008). In Arabidopsis thaliana. The AtMDK4-20 promoter was found tobacco and alfalfa plants genetically engineered to 314 Ann Microbiol (2019) 69:307–320 overproduce citric or malic acid, an increased colonization by class I β-1,3-glucanase gene in tomato resulted in increased mycorrhizal fungi and rhizobacteria has been reported resistance to Fusarium oxysporum f. sp. lycopersici with 36% (López-Bucio et al. 2000; Tesfaye et al. 2003). In other stud- to 58% reduction in disease severity (Jongedijk et al. 1995). ies, rhizosphere pH has been altered by over-expressing the Strittmatter et al. (1995) reported the inhibition of fungal path- genes controlling proton efflux from plant cells (Ryan et al. ogens by engineering controlled cell death in plants. The ex- 2009). Tobacco plants transformed with a modified plasma pression of bacterial ribonuclease barnase, driven simulta- membrane proton pump ATPase (H -ATPase) exhibited in- neously by a chimeric pathogen-inducible promoter (prp1-1) creased H -efflux from roots and a more acidic rhizosphere from potato and the CaMV 35S promoter, in order to avoid (Gévaudant et al. 2007). The edaphic variables, especially pH, detrimental effects of the RNAse, was studied and the induc- shape the structure and function of microbial communities in tion of barnase activity at the infection site was found to lead the rhizosphere (Fierer and Jackson 2006). However, Yuan to a significant reduction of Phytophthora infestans sporula- et al. (2008), by transcriptome profiling and functional analy- tion on leaves (Strittmatter et al. 1995). sis, have revealed that an acidic soil pH induces the virulence of Agrobacterium tumefaciens. Plants may also be engineered Engineering microbial signaling molecules in plants to promote the growth of desired microorganisms by releasing to bias the rhizosphere nutritional compounds which only the specific microorganism can catabolize (O'Connell et al. 1996). The phenomenon of Plants recognize and actively respond to different rhizosphere Agrobacterium tumefaciens mediated transfer of a region of microorganisms by producing signals that modulate microbial its plasmid DNA that encodes opine biosynthesis to plant cells colonization (Haichar et al. 2014). Hence, plant rhizosphere forms the basis of this strategy. Guyon et al. (1993)have may be modified by engineering plants to release microbial demonstrated that opines produced by roots of transgenic signal molecules like isoflavonoids or lipooligosaccharides plants increase the population of opine-catabolizing which induce microbial gene expression in the rhizosphere. Agrobacterium. Similar results have also been obtained by This method can be effectively utilized in ensuring nodule Mansouri et al. (2002) who reported that transgenic Lotus occupancy by the appropriate rhizobial species in leguminous plants producing opines specifically favor the growth of crop plants by utilizing nodule-specific compounds as growth opine-degrading rhizobacteria, irrespective of soil type and enhancers (Savka et al. 2002). The regulatory mechanism of plant species. quorum sensing, which involves the synthesis and accumula- Plants may also be engineered for the production of recom- tion of low-molecular weight signal molecules as a function of binant proteins in order to overcome the difficulties involved the population density of microbes producing these molecules in introducing complex antibiotic synthesis machinery in in a given environment, finds applications in this area (Savka plants for inhibiting the growth of antagonists. Transfer of et al. 2002). Several microbial functions like biofilm forma- genes encoding inhibitory proteins and peptides to plants en- tion, pathogenicity, and iron uptake are regulated via quorum ables their diffusion into the rhizosphere resulting in the sensing (Abisado et al. 2018; Rutherford and Bassler 2012). growth of only selected soil microorganisms. This approach The ability to generate bacterial quorum-sensing signaling is being studied for possible applications in the control of soil- molecules in the plant opens new avenues for manipulating borne pathogens. Pathogens infect plant tissues by producing the plant-microbe interactions. Some of the microbial signals a wide array of plant cell wall degrading enzymes. To prevent like the N-acyl-L-homoserine lactones (AHLs) and volatile this, polygalacturonase-inhibiting proteins (PGIPs) that inhibit organic compounds, which belong to a class of bacterial quo- the pectin-depolymerizing activity of polygalacturonases rum sensing signals from Gram-negative bacteria such as (PGs) secreted by microbial pathogens are made use of Pseudomonas, play a role in plant morphogenetic processes (Kalunke et al. 2015). Transgenic tomato plants, expressing (Ortíz-Castro et al. 2009). Transgenic tobacco and tomato a pear (Pyrus communis L.) PGIP (PcPGIP), capable of plants expressing the LasI gene from Pseudomonas inhibiting the PGs secreted by Bacillus cinerea showed 15% aeruginosa, responsible for the synthesis of AHLs have been and 25% reduction of disease lesions caused by the fungus on synthesized (Barriuso et al. 2008a). These AHLs produce get ripening fruit and leaves, respectively (Powell et al. 2000). In diffused across the plasma membranes into the rhizosphere, another study, Jach et al. (1995) detected high-level expres- where they have the potential to affect bacterial processes sion of genes transferred to tobacco for the production of regulated by such molecules (Ortíz-Castro et al. 2009). chitinase, β-1,3-glucanase, and ribosome-inactivating protein, Providing transgenic plants with the ability to block or de- under the control of the CaMV 35S-promoter. Fungal infec- grade AHL signals, otherwise termed as quorum quenching, tion assays revealed that the expression of individual genes may provide an alternative approach for engineering plant resulted in increased protection against the soil-borne fungal resistance to microbial pathogens. Transgenic tobacco and pathogen Rhizoctonia solani (Jach et al. 1995). Similarly, si- potato plants expressing the aiiA gene responsible for AHL multaneous expression of a tobacco class I chitinase and a degradation have shown resistance to Erwinia carotovora pv. Ann Microbiol (2019) 69:307–320 315 Pooling rhizosphere samples of crop species with specific phenotype carotovora infections even at very high bacterial inocula growing under different environmental and soil conditions (Dong et al. 2000). Future prospects of plant-microbiome associations Using this soil mixture as inoculum to inoculate crop plants grown under defined aseptic conditions The rhizosphere microbiome facilitates communication be- tween the plant and the surrounding soil environment and they together contribute to creating a productive metagenome which leads to improved crop productivity (Zorner et al. Using the inoculated soil from aseptically grown plants to inoculate fresh sets of crop plants under defined conditions 2018). Studies connecting comparative genomics and meta- bolomics have shown that specific rhizosphere bacteria are naturally selected depending on the root exudates contents (Zhalnina et al. 2018). For instance, comparison of wild and domesticated common bean (Phaseolus vulgaris) grown in Repeating the process for several generations using soil from agricultural soil revealed that as the genotype transitioned previous set as inoculum for the next generation from wild to domesticated, the relative abundance of Fig. 1 Process of identification of trait-specific microbiome associated Bacteroidetes (Chitinophagaceae and Cytophagaceae)de- with crop plants. The synergy of plant-microbiome associations forms the basis of this selection which can be utilized to enhance plant fitness and creased while Actinobacteria and Proteobacteria productivity (Nocardioidaceae and Rhizobiaceae) increased (Pérez- Jaramillo et al. 2017). The synergistic and complementary mechanisms among microorganisms and of plant-microbe in- plant traits including growth, flowering, and abiotic stress tol- teractions can be unveiled with the use of model plants grown erance have been reported (Bainard et al. 2013; Sugiyama under gnotobiotic conditions as such studies throw light into et al. 2013). Panke-Buisse et al. (2015) used a multi- the phenomenon of microbiome-mediated host plant immuni- generation experimental system using Arabidopsis thaliana ty (Sessitsch and Mitter 2015). Researchers have investigated Col to select for soil microbiomes inducing earlier or later immune responses elicited by plant microbiomes using the flowering times of their hosts. They found that the flowering FlowPot system (Kremer et al. 2016). Microbe-free seeds of phenotype was reproducible across plant hosts which showed Arabidopsis were grown in sterile, bottom-irrigated pots shifts in flowering time corresponding with the inoculation of alongside Arabidopsis colonized with diverse microbial com- early or late flowering microbiomes. Moreover, this resulted munities from various soils. Transcriptome profiling revealed in a mutual selection of plant host and the surrounding that colonized plants had significantly more defense- microbiome (Hunter 2016). As the host plants get co- associated transcripts involved in innate immunity, when ex- evolved with their microbiome, this strategy of microbiome posed to speck disease of tomatoes, caused by Pseudomonas selection could be adopted in future crop breeding strategies syringae pv tomato. The study also revealed a microbiome- for low-input sustainable agriculture. Also, the hologenome of influenced host and pathogen gene expression and suggested a host-microbiome association functions as an intermediate be- Bplant-pathogen-microbiome disease triangle^ concept for ad- tween the genotype-environment interaction in shaping the vanced studies of microbial pathogenesis and plant disease host plant phenotype (Hassani et al. 2018). Considering the resistance. The phenomenon of transfer of microbiome, from functional significance of plant-microbe interactions, an in- disease-suppressive soils to pathogen prevalent soils, for man- depth study into the microbiome function, particularly, the agement of crop diseases has also been reported (Gopal et al. microbiome constituents that are active during the different 2013; Turner et al. 2013). developmental stages of plant growth and their functions is Due to the direct influence of microbial interactions on needed (Mendes et al. 2013). plants and the ability of host plants to mediate microbiome Genetic improvement of plants focused on an efficient in- assembly, selection on a host-microbial association is an teraction with beneficial microorganisms and selection of ag- emerging approach to enhance plant fitness and productivity ricultural practices with less adverse effects on microbiome (Mueller and Sachs 2015). Protocols may be designed therefore need to be evolved (Gopal and Gupta 2016; targeting the selection of a characteristic host phenotype af- Sessitsch and Mitter 2015). Application of such works in the fected by the microbiome function which then gradually fa- field, as opined by Hunter (2016) would permit crops to ex- cilitates the transfer of specific trait-associated microbiomes ploit the beneficial microorganisms in soil, as several com- into new plant hosts (Fig. 1). Such studies describing the abil- mercial crop varieties have lost this capability due to injudi- ity of plant-associated microbiomes to influence different cious use of chemical amendments. 316 Ann Microbiol (2019) 69:307–320 development of vesicular-arbuscular mycorrhizal infection in barley Compliance with ethical standards and on the enophyte spore density. New Phytol 83:401–413 Bömke C, Tudzynski B (2009) Diversity, regulation, and evolution of the Conflicts of interest The authors declare that they have no conflict of gibberellin biosynthetic pathway in fungi compared to plants and interest. bacteria. Phytochem 70(15–16):1876–1893 Bottini R, Cassán F, Piccoli P (2004) Gibberellin production by bacteria Ethical approval No studies with humans/animals have been performed and its involvement in plant growth promotion and yield increase. by any of the authors for the purpose of this review article. Appl Microbiol Biotechnol 65:497 Brigham LA, Woo H-H, Nicoll SM, Hawes MC (1995) Differential ex- Informed consent Informed consent was obtained from all the authors pression of proteins and mRNAs from border cells and root tips of and the authors agreed to the manuscript being submitted to the journal. pea. 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Published: Feb 23, 2019

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