Plant Cell Tiss Organ Cult DOI 10.1007/s11240-016-1144-9
REVIEW
Bacteria in the plant tissue culture environment Teresa Orlikowska1 · Katarzyna Nowak1 · Barbara Reed2
Received: 28 June 2016 / Accepted: 26 November 2016 © Springer Science+Business Media Dordrecht (outside the USA) 2016
Abstract Bacteria and plants are joined in various symbiotic relationships that have developed over millennia and have inluenced the evolution of both groups. Bacteria inhabit the surfaces of most plants and are also present inside many plant organs. These bacteria may have positive, neutral or negative impacts on their plant hosts. Probiotic efects may improve plant nutrition or increase resistance to biotic and abiotic stresses. Conversely pathogenic bacteria may kill or reduce the vigor of plant hosts. In addition some bacteria inhabit plants and proit from excess metabolites or shelter while not injuring the plant. Micropropagation of plants is based on the stimulation of organogenesis or embryogenesis from explants that are supericially decontaminated and placed into a sterile environment. If successful, this process removes bacteria from surfaces, but those inhabiting inner tissues and organs are usually not afected by these steriliants. In vitro conditions are designed for optimal plant growth and development, however these conditions are also often ideal for bacterial multiplication. The presence of bacteria in the in vitro environment was almost universally considered negative for plant culture, but more recently this view has been questioned. Certain bacteria appear to have a beneicial efect on the explants in culture; increasing multiplication and * Barbara Reed
[email protected] Teresa Orlikowska
[email protected] Katarzyna Nowak
[email protected] 1
Research Institute of Horticulture, Skierniewice, Poland
2
Department of Horticulture, Oregon State University and U S Department of Agriculture, Corvallis, OR, USA
rooting, increasing explant quality, and organo- and embryogenesis of recalcitrant genotypes. The most important role of beneicial bacteria for micropropagated plants is likely to be during acclimatization, when growth is resumed under natural conditions. This review includes the role of bacterial interactions in plants, especially those grown in vitro. Keywords Beneicial bacteria · Biotization · Burkholderia · Contamination · Stress · Symbiosis
The role of bacteria in plants Plant-associated bacteria form both epiphytic and endophytic populations throughout plants (Compant et al. 2011; Friesen et al. 2011; Turner et al. 2013), including meristematic cells (detected using in-situ hybridization) (Pirttilä et al. 2000) or pollen (Madmony et al. 2005). Such colonizing populations of bacteria and other microorganisms are recognized as the host’s microbiome (Turner et al. 2013) also referred to as its “second genome” (Berg et al. 2014). Thus plants in their natural environment, like any other eukaryote or prokaryote, are holobionts (Hardoim et al. 2008; Rosenberg et al. 2010), also known as superorganisms (Podolich et al. 2009), meta-organisms (Berg et al. 2014) or pan-genomes (Turner et al. 2013), and may be considered as expanded phenotypes (Meldau et al. 2012). This co-habitation may extend the life potential of the partners (Rout et al. 2013). Bacteria have accompanied higher organisms from their beginning, thus participating in their creation and evolution (Rosenberg et al. 2010). Bacteria-host plant interactions are classiied as commensalistic, mutualistic or antagonistic (Senthilkumar et al. 2008, 2011; Vacheron et al. 2013). The most plant contact with bacteria
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takes place in the root zone, where a wide range of bacteria live, where bacterial and plant metabolites mediate the establishment of contacts, and where penetration into the roots occurs. Bacteria can also enter plants through leaves, lowers, stems and cotyledons. A frequent outcome is the colonization of the whole plant (Compant et al. 2008a). Bacteria can be transmitted across plant generations, either vertically through generative organs, or horizontally via vegetative propagules (Partida-Martinez and Heil 2011). Plant endophytes are those organisms that live throughout the whole, or a part of the life cycle within living plant tissue, without causing symptoms of disease (Wilson 1995). Endophytes can afect physiological processes of the plant, to an extent not unlike the plant genotype (Sessitsch et al. 2012), as a source of metabolites similar to, or different from, those produced by plants (Brader et al. 2014; Ludwig-Müller 2015a). Therefore, in any examination of individual functional characteristics of plants it is obligatory to take into account not only the traits resulting from the plant genotype, but also from the genotypes of endophytic microorganisms that inhabit it (Friesen et al. 2011). Some endophytes are known to be highly speciic to the host genotype, but others have a broader range of potential hosts (Hardoim et al. 2011). In nature, a microbiome is usually speciic to plants of the same species (Berg and Smalla 2009) growing in the same conditions. Nevertheless, it is shaped by internal and external factors, being much richer in the roots than in the above ground parts. Badri et al. (2013) argued that plants’ phenolic components and their derivatives secreted by the roots modify the composition of the rhizosphere microbiome, conirming the active role of plants in recruitment of bacteria (Turner et al. 2013). However, according to Santhanam et al. (2015), a study carried out on Nicotiana attenuata revealed that the major driver of the variability in root bacterial communities is a local soil niche from which bacteria move into plant roots. When bacteria useful to plants are discovered, it would be important to determine whether they are speciically associated with a host genotype or whether they will also be able to colonize other genotypes and enter into similar interactions. Both of these variants are possible (Ma et al. 2011), due to strong bacterial versatility and speciicity in relation to plants, and because the plant response, that to some extent can control the level of bacterial colonization in qualitative and quantitative terms (Hardoim et al. 2008). Plants react defensively to pathogenic microorganisms but also encourage those beneicial to their own survival (Oldroyd 2013). Several mechanisms of recognition were discovered but the inal result depends on both, signals released by bacteria and plant receptors (Carvalho et al. 2016).
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Beneits of plant-bacteria association Beneits can vary depending on bacteria-speciic characters and interactions between plants and bacteria. Some bacteria can produce not only all the hormones produced by plants (Friesen et al. 2011), but also other growth regulators, unusual for plants, which can afect plant morphogenesis and development. Vereecke et al. (2000) reported that the supernatant of the culture medium of Rhodococcus fascians, which causes both in vivo and in vitro distortions within plants (galls, stem fasciation, brooms) contained 11 distinct cytokinins, which interfered with the metabolism of plants, including inluencing morphogenesis of in vitro cultures. Rodestrine, a phytohormone with the properties of auxin, but not produced by plants, was obtained from the bacterium Rhodobacter sphaeroides (Sunayana et al. 2005). Auxins that are produced by many bacteria afect the development of the root system, thereby enhancing the absorption of nutrients and water from the soil (Patten and Glick 2002). Bacteria both produce plant growth regulators, and stimulate the production and distribution of these compounds in plants (Vacheron et al. 2013). Cytokinins extend the period of leaf ability to assimilate, thereby increasing the amount of products of photosynthesis and replace plant cytokinins lost during drought conditions (Arkhipova et al. 2007). Giron et al. (2013) emphasized the role of bacterial cytokinins as key regulators of growth and defense processes. Bacterial gibberellins support elongation growth independently and in interaction with other hormones (Bottini et al. 2004), and the ethylene level can be decreased by bacterial 1-aminocyclopropane-1-carboxylate (ACC) deaminase, thus reducing the susceptibility of plants to stress (Saleem et al. 2007; Saravanakumar 2012). Bacterial indole acetic acid (IAA) is known as an intermediary factor in shaping plant-microorganism interactions (Spaepen et al. 2007; Ludwig-Müller 2015b). Bacteria associated with disease resistance responses may also act as bio-control factors. Reduced susceptibility to pathogens may be related to the role of competitive colonization of tissues, or with antibiosis, consisting of disrupting the metabolism or degrading pathogens or pathogen toxins or virulence factors or by activating (priming) plant resistance (Compant et al. 2013). Bacteria have also been shown to protect plants before predators attack. Aballay et al. (2011) found that seven bacteria isolated from vineyards restricted the nematode population and the resulting damage to the in vitro produced grapevine plants in a greenhouse experiment. Protection against abiotic stresses can result from exposure to substances that modify stress responses or stimulate the plant to activate metabolic responses associated with stress tolerance such as the production of osmoprotectants like glycine betaine or proline (Dimkpa et al. 2009; Grover et al. 2011). For example, Burkholderia phytoirmans
Plant Cell Tiss Organ Cult
PsJN can adapt grapevine to cold by modiication of carbohydrate metabolism resembling natural cold acclimation (Fernandez et al. 2012) or/and by modiication of scavenging system (Theocharis et al. 2012). Bacteria that provide protection against drought include Azospirillum brasilense (improved water status of wheat), Achromobacter piechaudii (ACC deaminase induced systemic tolerance of pepper and tomato), Bacillus megaterium (increased IAA and proline in Trifolium), Pseudomonas mendocina (increased lettuce resistance to drought by improving antioxidant status), Pseudomonas polymyxa (altered hormonal balance and stomatal conductance of Phaseolus vulgaris) (Grover et al. 2011). Rolli et al. (2015) reported that three bacteria— Pseudomonas plecoglossicida, Acinetobacter calcoaceticus and Sphingobacterium canadense protected grapevine plants in the ield against drought. Pseudomonas luorescens YsS6 and P. migulae 8R6, produced ACC deaminase and signiicantly reduced the harmful efects of salinity in the cultivation of tomatoes (Ali et al. 2014b) Among the common features of these bacteria is the production of IAA, the ability to dissolve phosphates, resistance to 20% PEG and the acceptance of a temperature in the range of 4 to 42 °C (Saravanakumar 2012). Bacteria can also afect plant metabolism by producing extracellular volatiles (Kanchiswamy et al. 2015). For example Bacillus subtilis (GB03) produces volatile metabolites that in the long-term stimulate growth, the eiciency of photosynthesis, the accumulation of iron, and result in a greater seed yield in Arabidopsis thaliana (Xie et al. 2009). Volatiles of Bacillus badius M12 stimulated shoot regeneration from callus of Sesamum indicum, and increased the chlorophyll and carotenoid content, phenols and callus browning and induced organogenesis in tobacco callus (Gopinath et al. 2015). Zamioudis et al. (2013) showed that three strains of Pseudomonas spp. isolated from the rhizosphere had, in addition to providing protection against abiotic stressors and inducing a defense system against a number of pathogens, the ability to reprogram the mode of primary root growth in Arabidopsis thaliana. Endophytic bacteria can also participate in protection of plant photosystems against extreme environmental conditions through activation of a hormone dependent plant defense system and improving PSII electron transport (Burlak et al. 2013). Multi-efect microbial inluence on plants is sometimes called “priming”. In the primed state plants can respond more rapidly or/and efectively to a future stress (Goellner and Conrath 2008). Many endophytes exist in plants in a dormant state by maintaining a low metabolism, but they can resume the active state when environmental conditions change. Andreote et al. (2010) found that the endogenous bacterial population can be activated by the addition of beneicial bacteria to the growth environment. Ardanov et al. (2012)
reported that inoculation of potato plants with a strain of Methylobacterium induced the plant’s protection system against bacterial and fungal pathogens, with a force dependent on the cultivar and density of the pathogen inoculum. The Methylobacterium itself had no antagonistic activity against pathogens, but inoculation signiicantly changed the composition of the entire endophyte population in plant tissue, and thus increased the degree of resistance. This shows that the efect of bacteria introduced into plant tissue might also activate other pre-existing endophytes. However, it is not always clear whether accelerated growth or increased resistance is solely a result of bacterial metabolites, or also due to induction of the plant’s genetic apparatus by endophyte metabolites. According to Ludwig-Müller (2015a) plants and endophytes are equal partners in the production of secondary metabolites and can interact in the production of compounds and produce metabolites that are new to both organisms. For instance, Scherling et al. (2009) found that in tissue cultures of poplar inoculated with Paenibacillus sp. strain 22, 11 metabolites were changed in the plant, especially those related to the assimilation of nitrogen. Bacteria in plant tissue cultures For many years, the presence of bacteria in tissue culture was usually not disclosed in published manuscripts and was considered derogatory to a laboratory, as in vitro cultures should be maintained in sterile conditions. However, over time it has become clear that despite surface sterilization of initial explants, cultures are not necessarily free from bacteria. The presence of some bacteria can be apparent in the initial stage, but at other times the contaminants may not be detected until the multiplication stage, and often even later when suboptimal conditions or acclimation may spur the growth of the bacteria. Contamination of plant explants, detection and elimination of contaminant bacteria were the focus of several reviews (Reed and Tanprasert 1995; Cassells 1997; Stead et al. 2000; Dunaeva and Osledkin 2015), including those in textbooks (Cassells 2011) but according to our knowledge there are no recent reviews concerning beneicial bacteria in plant tissue culture (Nowak 1998). Microorganisms in culture, even those that are nonpathogenic or not apparent, can have detrimental efects on the cultures and cause lack of multiplication or variation in experimental results (Tsao et al. 2000). Undetected bacteria can begin multiplying after a long period in culture. Pathogenic Xanthomonas axonapodis persisted as asymptomatic in anthurium shoot cultures for 1 year (Norman and Alvarez 1994) and pathogenic Agrobacterium vitis was able to persist in the latent stage within Vitis vinifera in vitro shoot cultures for 14 weeks (Poppenberger et al. 2002). There is much evidence that the interior of explants used for in vitro culture are colonized with a quantity of bacteria
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(Buckley et al. 1995; Reed et al. 1995; Reed and Tanprasert 1995). These are a combination of free-living bacteria, plant-inhabiting, animal-associated, but also those associated with processed food and sewage and even human pathogens (Cassells and Tahmatsidou 1996; Fletcher et al. 2013). Thomas et al. (2007) found 14 isolates of bacteria belonging to nine genera, including those from human or animal related bacteria in 1 cm long shoot apices of papaya, prepared by surface sterilization. Some multiplied on the medium only in the presence of papaya shoots or extracts. De Almeida et al. (2009) using an electron microscope, found bacterial endosymbionts inside cells of in vitro peach palm shoots considered axenic. Further analyses of DNA from these endosymbionts using PCR and denaturing gradient gel electrophoresis (DGGE) revealed the presence of three non-cultivable bacteria that showed similarity of rRNA sequences to Moraxella sp., Brevibacillus sp., and to a cyanobacterium. A similar molecular analysis by AbreuTerazi et al. (2010) found bacterial endophytes belonging to Actinobacteria, Alphaproteobacteria and Betaproteobacteria in 5-year old axenic cultures of pineapple, sterilized supericially before DNA extraction. The authors observed diferences in the bacterial community within diferent plant organs. Lucero et al. (2011) using microbiological, microscopic and nucleotide sequencing methods of identiication, found a rich microbiome consortium in regenerated leaves and roots of two Atriplex species that consisted of known and unknown bacteria and fungi. Fang and Hsu (2012) isolated bacteria of 13 genera from meristematic explants of six cultivars of Aglaonema; 30% of the colonies isolated were Pseudomonas aeruginosa. In a study of bacteria found in contaminated plant cultures obtained from several laboratories in Poland, 108 isolates in several genera were detected; with the most common being bacteria of the genera Bacillus, Methylobacterium and Pseudomonas (Kaluzna et al. 2013). All isolates in this study, with the exception of Staphylococcus, were obtained from living explants, without disease symptoms. Although the bacteria are not always detectable, they may still have a negative impact on in vitro cultures (Thomas 2004b, 2011; Pirttilä et al. 2008). For example, crypto bacteria Bacillus circulans, Sphingomonas paucimobilis Staphylococcus huminie and Micrococcus kristinae signiicantly decreased shoot proliferation in the shoot cultures of apricot (Marino et al. 1996). The above bacteria changed the medium composition, as well as the composition of the atmosphere in the vessels, which negatively inluenced culture growth. The habituation of plant tissue cultures has been known for decades and may be the result of bacterial contamination. Habituated cultures at a certain point in their growth can continue to grow without addition of exogenous plant growth regulators. Comparison of transcripts of habituated and non-habituated Arabidopsis thaliana cells showed
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various expressions of 800 genes, including up-regulation of genes coding for cytokinin receptors (Pischke et al. 2006). In the light of more current knowledge of diicult to detect endophytic microorganisms, at least some cases of habituation can be considered the result of changing in auxin or cytokinin balance, possibly caused by endophyte metabolic activity. This is possible as indicated by indings that endophytes produce auxins, cytokinins, gibberellins and other plant hormones (Arshad and Frankenberger 1991; Lata et al. 2006; Weilharter et al. 2011). For bacteria non-pathogenic for ex-vitro grown plants but harmful for in-vitro explants Herman (1987) proposed the term “vitropaths”. Sterilization methods If pathogen-free donor plants are not available, sanitation protocols should be implemented. Removal or reduction of pathogens in donor plants may involve using fungicides, bactericides, antibiotics, and thermo- or chemotherapy followed by the isolation and culture of true meristems or the smallest possible shoot tips (Cassells and Doyle 2006; Cassells 2011). Shoot multiplication then should be carried out with culture lines derived from single initial explants. A broad spectrum and varying amounts of endophytic bacteria inhabit plants in situ and eradicating all of them is practically impossible. Several methods of minimizing the contamination in plant tissue cultures were proposed (Reed and Tanprasert 1995; Bunn and Tan 2002). One of the most important is improving the phytosanitary condition of donor plants. Signiicantly fewer contaminations in the initial material are in donor plants growing in the greenhouse, watered to the substrate and preventively protected against bacteria and fungi (Leifert et al. 1994). Very important is a supericial surface sterilization that includes efective steriliants, their concentration and time, as well as the sequence of use. The most popular traditional biocides used are ethanol, calcium or sodium hypochlorite, mercuric chloride, hydrogen peroxide, and dichloroizocyanurates (Rowntree 2006; Cassells 2011), chlorine dioxide (Bhawana et al. 2015) or nano silver (Abdi et al. 2008). The eiciency of sterilization can increase if preparations are administered to explants through vacuum iniltration (Miyazaki et al. 2010). For parts of donor plants that are dormant or for storage organs, a hot water treatment is recommended before explanting (Langens-Gerrits et al. 1997). Sometimes an inner sterilization, by means of forcing of shoots in 8-hydroxyqinoline-citrate (Szendrák et al. 1997) or soaking in antibiotics (Falkiner 1997) or sulphonamide (Zenkteler et al. 1997) can reduce the number of bacteria. At this stage, when the nature of the bacteria is unknown, broad-spectrum antibiotics could be applied. Initial obviously contaminated explants should be discarded. All
Plant Cell Tiss Organ Cult
remaining viable explants should be repeatedly indexed, at least for the irst few subcultures to determine the presence of bacteria by incubation of basal fragments of explants on the microbiological liquid and semi-solid media and discarding those contaminated ones (Reed et al. 1995; Reed and Tanprasert 1995; Thomas 2004a). Another possibility is a treatment of explants with biocides added to the culture medium, as sodium hypochlorite (Kohmura et al. 1999), antibiotics (Reed et al. 1995, 1997; Falkiner 1997; Thomas et al. 2006), and other biocides such as PPM (Orlikowska et al. 2012), Vitrofural (González-Olmedo et al. 2005) or plant extracts (Marino et al. 2015). The antibiotic type and its concentration should be chosen on the basis of results of anti-biograms and having in mind that for plant cultures use, concentration should be further optimized. All types of biocides included in the growth medium should be irst tested for phytotoxicity to make sure that they are efective against the bacteria, and not detrimental to the explants (Buckley et al. 1995; Orlikowska et al. 2012). Even if the above measures are not successful for all bacteria, routine screenings followed by discarding contaminated cultures or applying biocides to a medium, cyclically repeated may allow a signiicant reduction of contaminations and enable the continuation of shoot propagation (Cassells 1991; Buckley et al. 1995).
Detection of bacteria The variety and amount of bacteria that occur naturally in plant tissues indicates why it is not practically possible to get completely clean plant explants. In the beginning of culture it is necessary and possible to remove bacteria that can easily multiply massively on plant media. They can be dangerous due to the ability to dominate over plant explants, isolating them from oxygen and competing for nutrition. A more diicult problem concerns bacteria that do not multiply on plant media. Some of them can be disclosed on bacteriological media if they are cultivable. Latent infections with pathogenic bacteria and covert contaminations with non-pathogenic types are the most troublesome. Unfortunately, only a few laboratories test explants for cultivable microorganisms. In addition, a testing procedure should be repeated to ensure that pathogenic microorganisms are not present at culture initiation and stabilization, during micropropagation and at acclimatization in the greenhouse. For optimal certainty, detection of pathogens in the initial explants and their ofspring should be carried out using extremely sensitive tests based on immunological or DNA markers, capable of detecting very small amounts of microbial DNA/RNA (Stead et al. 2000; James et al. 2014) with the best solution likely to be integrated tests (Alvarez 2004). These kinds of tests are especially needed for
disclosure of potentially pathogenic bacteria and several sensitive tests are currently in use. Some bacteria can remain in a hidden state (covert, cryptic) in plant tissues for many subcultures, appearing only when subjected to stress factors, resulting from changing the medium, prolonged passage, elevated temperature, or long-term storage at low temperatures (Leifert et al. 1994; Thomas et al. 2007). Some bacteria can multiply only in the presence of the plant tissue in which they dwell, i.e. Curtobacterium citreum in shoot culture of chrysanthemum (Panicker et al. 2007). These kinds of bacteria are diicult to ind and deine, because even molecular methods are sometimes not sensitive enough to detect such low amounts of bacterial DNA, especially when amplifying them together with prevalent amounts of plant DNA and with plant polymerase inhibitors, using PCR techniques. Pohjanen et al. (2014) detected endophytes associated with tree meristems using in situ hybridization of bacterial DNA. Müller and Döring (2009) isolated particles visible in electron microscopy as bacteriosomes from plant cells, with the help of a 3-D micromanipulator and then studied their genomes independently of the plant DNA background. Bacteria can be also revealed with speciic staining and video imaging, recording their movements in the cytoplasm and periplasm. Some bacteria can be disclosed after biocide application, when is possible to diferentiate between them and other micro-particles in the cytoplasm (Thomas and Sekhar 2014). A disclosure of the uncultivable Methylobacterium sp. in potato explants grown in vitro was possible using molecular markers, but isolation was possible when its cultivability was increased in the efect of co-cultivation of cultures with Pseudomonas luorescens IMGB163 (Podolich et al. 2009). Efremova et al. (2012) suggested that more knowledge concerning the presence of endophytic bacteria in plant tissues in vitro might be available through protoplast or cell cultures. In this condition, microorganisms multiply, rapidly overgrowing the culture, often producing toxic metabolites resulting in the death of the cultures. A possible explanation is that the bacteria do not proliferate, or multiply to a very limited extent, if they are secured in their life niches in intact cells, but after removing the cell wall to obtain protoplast culture, or after breaking the connections between cells to obtain cell cultures, they reproduce and quickly become visible. Also Klocke et al. (2012) reported that endophytes hidden in the cells were able to multiply as a result of protoplast isolation. These and other examples of rapid disclosure of endophytes can be attributed to two factors—the appearance of a bacteria stressor (removal of the cell walls, the presence of cell wall degrading enzymes, elevated temperature or presence of other microorganisms), and/or host explants stressors that decrease host explants resistance (change of medium, including
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growth regulators, the use of mutagenic agents, elevated or decreased temperature). In vitro applications of bacteria The symbiosis of bacteria with plants has prompted imitative use in plant production, including in vitro propagation. A spectacular example of the practical use of bacteria is the exploitation of Agrobacterium tumefaciens and A. rhizogenes. These soil bacteria, which cause pathogenesis in many plants, possess genetic equipment enabling colonization of plant cells. Since 1980, disarmed forms (deprived of tumorogenes) were used as vectors for transferring desirable genetic information (Păcurar et al. 2011). Disarmed bacteria can introduce a speciic genetic construction to the nucleus or plastid of a plant. If this construction joins stably to the plant DNA, it can be transferred to daughter cells. Regeneration of whole plants from such “genetically enriched” cells lies at the base of transgenesis, and ofers an excellent source of new genetic variability that can be used in plant breeding (Ziemienowicz 2014). Numerous taxa of bacteria have been isolated from plant tissue cultures, and at least some of them displayed a possibility to increase plant growth rates or inluence morphogenesis in vitro. In comparison to ex-vitro plant production, it is sometimes easier to adjust optimum conditions favoring the growth and organogenesis of explants during in vitro culture, for both research and industry. Genotypes that are recalcitrant or diicult in culture do not respond with efective regeneration, a high multiplication coeicient, or efective rooting. In this case, the inoculation of cultures with beneicial bacteria might help in overcoming the recalcitrance, by supporting cultures with growth regulators or other metabolites. For example, Rhodobacter sphaeroides produces the phytohormone rodestrine enhancing the rooting of mulberry microshoots (Sunayana et al. 2005) and Bacillus spp. producing IAA promoted rooting of strawberry (Dias et al. 2009). Quambusch et al. (2014) found a link between endogenous bacteria and the eicacy of micropropagation of Prunus avium genotypes. Sometimes unexpected morphology or better quality of cultures may suggest the activity of endophytic bacteria. For example, elderberry cultures naturally contaminated with pink bacteria (Methylobacterium) formed fewer but longer axillary shoots when compared to non-contaminated ones. Raspberry shoots contaminated with a creamcolored bacterium were spiky and longer in comparison with those not contaminated. These and other bacteria were isolated and screened against rose, chrysanthemum, gerbera and hosta in vitro cultures. None of these bacteria were detrimental to the explants, and some combinations of bacteria/plant species signiicantly improved multiplication and rooting (Zawadzka et al. 2014). In this study
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Curtobacterium increased shoot proliferation of all four plant species, as well as the rooting of rose; Methylobacterium increased productivity of gerbera and hosta while Bacillus lengthened shoots of chrysanthemums. The above and other examples of the beneicial impact of bacteria on in vitro cultures are listed in Table 1. The most important role of beneicial bacteria in the micropropagation industry is connected with acclimation of microplants, which is often a bottleneck of the process. The nonfunctional (open) stomata, not fully-functional roots and photosynthetic apparatus make the adaptation diicult for microplants in rapidly changing conditions. Inoculation of microplants at the last stage of propagation or at the weaning with beneicial bacteria could help overcome this challenge (Nowak 1998; Vestberg and Cassells 2009; Panigrahi et al. 2015). Bacteria belonging to 13 genera (Azorhizobium, Azospirillum, Azotobacter, Bacillus, Burkholderia, Curtobacterium, Enterobacter, Halomonas, Methylobacterium, Microbacterium, Methilophylus, Paenibacillus, Pseudomonas, Ralstonia, Rhodococcus, Rhodopseudomonas, and Sphingopyxis) caused positive impacts on micropropagation processes and in some instances possible mechanisms responsible for increased productivity were proposed. Bacteria stimulated shoot elongation, increased shoot weight, leaf number, axillary shoot growth, accelerated rooting, increased rate of rooted shoots, increased number and length of roots, induced somatic embryogenesis and helped in microplants’ acclimation to ex vitro conditions (Table 2). The special role of Burkholderia phytofirmans PsJN in micropropagation A group of Pseudomonas species (Bergey et al. 1984) were reclassiied as Brevundimonas based on phenotypic characterization, DNA-rRNA hybridization, protein patterns, and fatty acid composition (Segers et al. 1994). The genus Burkholderia includes more than 60 extremely variable species, inhabiting many life niches, and also acting as pathogens of humans, animals and plants (Suarez-Moreno et al. 2012). Recently, all bacteria in this group, which are primarily environmental, were proposed to constitute a new genus Paraburkholderia gen. nov. (Sawana et al. 2014). Over 30 non-pathogenic Burkholderia species live in association with plants and can be considered potentially useful due to characteristics that can be beneicial for the host. These include the ability to convert atmospheric nitrogen into ammonia, provision of phosphorus and iron, production of growth regulators, protection against pathogens, and others (Compant et al. 2008b). Members of this genus are capable of supporting the growth of plants due to ACC deaminase and quinolinate phosphoribosyl transferase activity. Moreover, they can secrete into the environment siderophores,
From microbial collection
Azospirillum brasilense/Cd and Az39
Bacillus licheniformis/ R14M10 Pseudomonas luorescens R16M10
From roots and rhizosphere of On emerged roots Vitis vinifera
From spent alcohol used in subculturing of grapevine, residing as covert in explants From pelargonium seedlings On hypocotyl segments
Bacillus pumilus
Bacillus circulans
From rhizosphere
Azotobacter chroococcum/42
Azospirillum brasilense/Sp245 Surface of wheat roots
1. From microbial collection 2., 3. Locally isolated
1. Azospirillum brasilense/Cd 2. A. brasilense/Sp7 3. A. brasilense Az 39
Induced somatic embryogenesis in genotypes resistant for TDZ Increased shoot and root length, and leaf area, increased ABA and IAA level in leaves and roots, prevented water loss, induced mono- and sesquiterpene production
Larraburu and Llorente (2015)
Russo et al. (2008)
Andressen et al. (2009)
Thomas (2004b)
Murthy et al. (1999)
Salomon et al. (2014)
More eicient nutrient uptake
Assimilation of aerial nitrogen, IAA and PAA production, antimicrobial activity
NA
NA
NA
Production of ABA, IAA, GA1 and GA3
Carletti et al. (1998) Larraburu et al. (2007) Gonzalez et al. (2015)
On shoot base of Simmondsia Increased root number chinensis before rooting On microshoots of Photinia × Accelerated rooting, increased fraseri before rooting shoot and root fresh and dry weight and root surface area; increased salt tolerance On shoots bases of Handroan- Increased % of rooted shoots, length of shoots and roots thus impetiginosus after root number, decreased auxin induction requirement Accelerated rooting, increased Before or after rooting on number, length and weight shoot base of Prunus cerasof roots, number of nodes, ifera Mr.S 2/5 length and weight of shoots; during rooting and acclimatization, protection of microshoots for Rhizoctonia spp Increased number of axillary On bases of shoots of Simshoots mondsia chinensis before rooting On microshoots of grape Increased number and weight before rooting of roots; accelerated rooting
From microbial collection
Parray et al. (2015)
Authors
Excretion of plant growth regulators Replacement of exogenous auxin; resistance for salt
1., -3.-6. IAA production On 30–70 day-old-cormlets of 1., 2., 4. 100% cormlet ger2.-6. Siderophore production Crocus sativus mination 3.-5. Increased cormlet weight 1.-6. Phosphate solubilization 3. + 4. + 5. Increased cormlet proliferation
From safron rhizosphere
The impact mechanism
1. Acintobacter lwoi 2. A.haemolyticus 3. Bacillus subtilis 4. Klebsiella sp 5. Pantoea sp 6. Pseudomonas sp Azospirillum brasilense/Cd
Type of action
Subject of inoculation
Source
Taxon/strain
Table 1 Taxon, source, action and impact of bacteria used in bacterization on in vitro plant cultures
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13 On nodal explants of potato
From roots of onion
As above
As above
As above
As above
From vineyard soil
From in vitro cultures of chry- Persistent contamination santhemum covert-type in chrysanthemum culture On shoot bases before rooting 1. and 2. From contaminated of chrysanthemum, gerbera, raspberry cultures hosta and rose (shoot tips 3. From contaminated hosta were used for multiplication cultures studies)
From shoots of sugar canes
Rhizosphere of Equisetum debile
Burkholderia phytoirmans /PsJN™ (earlier Pseudomonas sp. /PsJN)
As above
As above
As above
As above
Burkholderia spp. IF25
Curtobacterium citreum (3 morphotypes)
1. Curtobacterium pusillum 2. Methylobacterium extorquens 3. Paenibacillus glucanolyticus
Enterobacter sp. /SC20
Halomonas desiderata /RE1
On rooted shoots of Saccharum oicinarum Inoculation of germinated seeds, internodal explants and callus of Brassica oleracea
On bases of microcuttings
On rooted shoots of potato
On weaned seedling roots of Panicum virgatum On the base of microshoots in rooting medium of Helleborus sp
On nodal segments of Vitis vinifera
Subject of inoculation
Source
Taxon/strain
Table 1 (continued)
1. Increased number of axillary shoots, number and length of rose roots 2. Increased number and length of shoots and roots gerbera and hosta, number of shots of chrysanthemum 3. Increased number and length of chrysanthemum shoots and length of chrysanthemum roots Increased dry weight of shoots and roots Increase in shoot length, adventitious shoots and callus proliferation depending on supernatant concentration and explants type
Stimulated microshoots growth; increased roots number, dry weight of shoots and roots, stimulated cuticular hairs on leaves, secondary roots and ligniication Increased shoot length, number of nodes, dry weight of shoots and rots and overall biomass microplants, protected of shoot explants against Botritis cinerea Increased shoot and root growth, of Alamo cv Increased number of rooted shoots, number and length of roots and acclimatization at non-optimal temperature Increased fresh weight of microplants Fastened rooting, increased roots number Increased number of axillary shoots
Type of action
Assimilation of aerial nitrogen, production of IAA Salt tolerance, IAA production
1.-3.Assimilation of aerial nitrogen 2., 3. IAA production
Change in amount of IAA, trans-zeatin and GA3 Modulation of auxin biosynthesis Replacement of BAP and kinetin
Ali and Hasnain (2007)
Mirza et al. (2001)
Zawadzka et al. (2014)
Panicker et al. (2007)
Muganu et al. (2015)
Kurepin et al. (2015)
Orlikowska et al. (2017)
NA
Barka et al. (2000)
Inhibition of Botritis cinerea on PDA medium
Kim et al. (2012)
Frommel et al. (1991)
Production of plant hormones
NA
Authors
The impact mechanism
Plant Cell Tiss Organ Cult
Source
NA not available
On oregano microshoots
From soybean
Pseudomonas mucidolens, P. sp./ATCC 31461 Not identiied
From in vitro cultures of Pinus On hypocotyl bases of Pinus elliotti elliotti after cut of roots
On base of raspberry shoots
As above
As above
On base of oregano shoots
From contaminated oregano cultures
On bases of shoots diicult to propagate Prunus avium genotypes On the bases of populus microshoots bases Co-cultivation of soybean calli for 45 days Added to rooting medium to MILCAP substrate On nodal segments of Mentha piperita Increased number and length of roots Induced nodular calli followed by somatic embryos Promoted growth of Primula roots 2.-4. increased shoot fresh and dry weight 1.-4. Increased ramiication 4. increased leaf number 1., 2., 4. Increased essential oils yield Prevented hyperhydricity of oregano explants, increased content of phenolics and chlorophyll Prevented hyperhydricity of raspberry cultures Prevented hyperhydricity of oregano cultures Enabled rooting and acclimatization of seedlings
Quambush et al. (2014)
Kalyaeva et al. (2003)
Authors
Santoro et al. (2015)
Shetty et al. (1995)
1.-3. production of IAA 1., 4.siderophore production, 1.-4. phosphate solubilisation
Production of extracellular polysaccharides
NA
Burns and Schwarz (1996)
Ueno and Shetty (1997)
Ueno et al. (1998)
Digat et al. (1987)
NA
Production of extracellular polysaccharides As above
Yang et al. (1991)
NA
Assimilation of aerial nitrogen Ulrich et al. (2008)
1., 3. Stimulated formation of Production of IAA and cytokinins morphogenic calli 2., 4. Stimulated development of primary shoots 3. Stimulated formation of morphogenic calli and shoot regeneration Increased % of rooting and NA number of roots
On immature embryos
The impact mechanism
Type of action
Subject of inoculation
Pseudomonas sp./F
1. Methylobacterium sp. /D10 In order: from soil, from maize rhizosphere, from rice 2. Methylovorus mays /VKM rhizosphere, or sewage V-2221 3. Methyloilus glucoseoxidans /B VKM V-1607 4. Methilophylus methylotrophus /VKM V-1623 From contaminated explants Microbacterium testaceum of easy for micropropagation /D-1-1 Prunus genotype Rhodopseudomonas sp./N-1-2 Paenibacillus humicus/P22 From contamination of Populus cultures Pseudomonas maltophilia/ From contaminated soybean PmSoy1 cultures Unknown Pseudomonas putida/G-92 and P. luorescens/L 26-1 From rhizospere of ield Pseudomonas putida grown Mentha plants 1. /SJ04 2. /SJ25 3. /SJ48 4. P. luorescens WC5417r
Taxon/strain
Table 1 (continued)
Plant Cell Tiss Organ Cult
13
Source
13
Paenibacillus macerans
Enterobacter sp./SC20
1. Bacillus sp./CaB5 2. Pseudomonas luorescens/ R68 3. Pseudomonas putida/ R79
Bacillus subtilis Bacillus sp Pseudomonas corrugata Bacillus, consortium of 3 strains/INR7/T4/IN 937b
Type of action
Protected microshoots for On shoot base of Prunus cerasifera Mr. S 2/5 before or Rhizoctonia spp. during rooting and acclimatization after rooting Facilitated acclimatization, On bases of microshoots of increased shoots length and rootstocks Mr.S2/5 (Prunus nodes number cerasifera x P. spinosa), GF 677 (P. persica x P. amygdalus) after rooting Mixed with substrate for accli- Increased survival rate, shoot matization of tee microplants length, root number, fresh weight, protected before pathogenic wilting On rooted plantlets Increased number and weight of roots and shoots in ex vitro tests
Subject of inoculation
To the substrate at planting of microshooots of Picrorhiza kurrooa
Increased % of survival, length of shoots and roots, plant biomass and P content in shoots and roots From rhizosphere of tea plants To growth substrate at planting Enhanced survival of microof tea microplants plants, increased shoot length and leaves number 20 days after transplanting Increased fresh and dry From microbial collection banana plantlets to trays weight, pseudostem diam(presumably from rhizoseter, foliar surface and conphere) tents of N, P, K in leaves 4× to the substrate for microIncreased leaf number and From rhizosphere propagated banana size, height of plants, num1. Capsicum annuum 2.Sizygber and length of roots, fresh ium jambos weight of shoots and roots; 3. Phyllanthus amarus reduced hardening period From shoots of sugar canes On rooted shoots of SacchaIncreased dry weight of shoots rum oicinarum and roots Increased number, length From meristems of Cymbidium On the microshoot bases of and dry weight of roots and eburneum Cattleya loddigestii at the number of leaves acclimatization stage in the greenhouse
From spent alcohol used for subculturing of grapevine shoots, existing as cover in shoots From bacterial collection
Bacillus pumilus
Bacillus megaterium Bacillus subtilis Pseudomonas corrugata
From soil of tea plantation
Azospirillum spp
Azospirillum brasilense/Sp245 As above
Azospirillum brasilense/Sp245 From surface of wheat roots
Taxon/strain
Table 2 Taxon, source, action and impact of bacteria used in bacterization on acclimatization of microplants to ex vitro conditions
Russo et al. (2008)
Assimilation of aerial nitrogen, IAA and PAA production, antimicrobial activity As above
Trivedi and Pandey (2007)
Jaizme-Vega et al. (2004)
Suada et al. (2015)
Antifungal activity against fungi isolated from plants during acclimatization in in vitro tests Antifungal activity against pathogens of tea in in vitro tests NA
NA
Assimilation of aerial nitrogen, production of IAA Production of indole compounds
Thomas (2004b)
NA
Faria et al. (2013)
Mirza et al. (2001)
Pandey et al. (2000)
Thomas et al. (2010)
Higher activity of defense enzymes, nitrogen ixation
Vettori et al. (2010)
Authors
The impact mechanism
Plant Cell Tiss Organ Cult
NA not available
Not identiied (RB)
Rhizobium 7 strains
Pseudomonas mucidolens/ ATCC 4685 P. sp./ATCC 31461
Pseudomonas sp./F
Pseudomonas luorescens/ CHA0 and IP10
From rhizosphere (microbial collections)
On microcuttings of potato and Increased stem length, rooting eiciency and survival in the strawberry as a spray with greenhouse and increased Pseudomonas irst then with resistance against Erwinia Mehylovorus carotovora, Sclerotinia sclerotiorum and Phytophthora infestans From potato tubers On potato microplants before Increased plant survival at acclimatization acclimatization, fresh weight of shoots and number and weight of tubers (IP10) and shoot growth (CHA0); protected against Rhizoctonia solani From contaminated oregano On base of raspberry shoots Increased % of acclimatized tissue cultures microplants, decreased water content and phenolic compounds From bacterial collection On oregano microshoots Increased % of acclimatized (presumably from soil) microplants, increased content of chlorophyll, phenolic compounds and dry weight, decreased fresh weight Increased survival rate and From root nodules of Robinia On the top of soil before pseudocaccia plantlets of R. pseudoacaccia growth rate, depending on strain transplantation From in vitro cultures of Pinus On hypocotyls base of Pinus Enabled acclimatization of elliotti elliotti after cut of roots seedlings
Type of action
1. Pseudomonas aureofaciens BS 1393 2.Methylovorus mays/VKM B-2221
Subject of inoculation
Source
Taxon/strain
Table 2 (continued)
Dufy et al. (1999)
Ueno et al. (1998)
Ueno and Shetty (1997)
Balla et al. (1998)
NA
Production of extracellular polysaccharides
Production of extracellular polysaccharides
NA
Burns and Schwarz (1996)
Zakharchenko et al. (2011)
Solubilization of phosphates and secretion of active substances with fungistatic action
NA
Authors
The impact mechanism
Plant Cell Tiss Organ Cult
13
Plant Cell Tiss Organ Cult
antibiotics, protective elicitors, such as polysaccharides, and activate induced systemic resistance in plants (SuarezMoreno et al. 2012). Burkholderia spp. colonize the outer and inner plant tissues and are endosymbionts of many plant species. Some strains are predators of pathogenic microorganisms, which make them potential candidates for bio-protection (Cain et al. 2000). Due to these unique characteristics, the search for Burkholderia isolates is ongoing (Young et al. 2013). B. phytoirmans strain PsJN, isolated from onion roots inhabited by mycorrhizal fungi (Frommel et al. 1991) is the most widely described bacterium having a beneicial efect on plants for both ex vitro and in vivo propagation and growth. It was initially classiied based on biochemical and physiological traits as a non-luorescent pseudomonad and named Pseudomonas sp strain PsJN (after its discoverer Dr. Jerzy Nowak). According to sequence analysis of the 16S rRNA it was renamed as B. phytoirmans (Mitter et al. 2013). It became a model for studying bacterization in plant tissue culture (Bordiec et al. 2011; Poupin et al. 2013; Lara-Chavez et al. 2015). B. phytoirmans strain PsJN can colonize several plants species, positively afecting their growth and wellness, initially colonizing the roots before moving onto the aerial parts (Compant et al. 2008b). Several species responded positively to colonization with this bacterium, for example Arabidopsis thaliana (Poupin et al. 2013), maize (Naveed et al. 2014b), switchgrass (Kim et al. 2012) and Helleborus (Orlikowska et al. 2017). The growth promotion in potato (Conn et al. 1997; Kurepin et al. 2015) and in switchgrass was cultivar speciic (Kim et al. 2012). Interestingly, Kurepin et al. (2015) found that after inoculation of potato with PsJN, a slower growing cultivar matched the growth rate of the rapidly growing cultivar, and that growth was accompanied by an increase GA3 and reduction of transzeatin in the slow growing cultivar. This indicates that the interaction of bacteria and plant is associated with the biosynthesis of plant growth regulators. PsJN inhibited colonization of in vitro grapevine cultures by Botrytis cinerea (Barka et al. 2002) and tomato by Verticillium dahliae (Sharma and Nowak 1998). Colonization with B. phytoirmans increased resistance of plants to non-optimal growth temperatures—low in grapevine (Theocharis et al. 2012) and high in potato (Bensalim et al. 1998). Arabidopsis thaliana colonized by PsJN was less susceptible to plasmalemma disruption under freezing stress (Su et al. 2015). Colonization of Helleborus microshoots with this bacterium showed better growth under non-optimal temperatures (23 vs. 15 °C) (Orlikowska et al. 2017). Wheat (Naveed et al. 2014a) and maize (Naveed et al. 2014c) plants from seeds inoculated with PsJN were less sensitive to drought stress under ield conditions than those not inoculated. Poupin et al. (2013) determined that B. phytoirmans PsJN when inoculated into germinated seeds of Arabidopsis
13
thaliana, inluenced the plant throughout the complete growth cycle. It initially stimulated vegetative growth, then accelerated the development of generative organs, and thus shortened the life cycle. Transcriptome analysis of inoculated plants showed that 364 genes were over expressed and 282 genes were under expressed, when compared to noninoculated plants. Zhao et al. (2016) revealed in PsJN inoculated Arabidopsis seedlings expression of genes related to iron storage, siderophore biosynthesis and transport, as well as higher absorption minerals Fe, Zn and Cr, which can contribute to plant growth promotion and alteration of metabolites (Su et al. 2016). PsJN has a large genome, unlike other endophytic bacteria. This may have resulted in the presence of a large number of genes encoding a number of physiological functions that enable its endophytic behavior (Mitter et al. 2013). Ali et al. (2014a) demonstrated by means of comparative genomic analysis of several endophytes, that B. phytoirmans has all the genes of nine other bacteria studied, related to transportation, secretion, degradation of polymers, regulation of transcription, detoxiication, stabilizing redox potential that help in the efective colonization, as well as the establishment of positive interactions with host plants. According to Mitter et al. (2013) the ability of PsJN to colonize plants and to establish an endophytic relationship resulting in a beneicial inluence on unrelated plants, is the efect of the bacterial genes coding for such metabolites as siderophores that improves iron assimilation, poly-3-hydroxybutyrate than overcomes carbon starvation, heavy metal and drug resistance, unfavorable compound degradation and other characteristics that enable bacteria to adapt to diferent conditions. Park and Lazarovits (2014) obtained results suggesting that plant growth enhancement after inoculation with PsJN can be the result of more eicient sugar uptake through direct or indirect stimulation of hexokinase1 activity. B. phytoirmans PsJN has a genetic equipment to produce IAA and that allows it to be involved in plant growth and root proliferation. It also has the operon involved in a degradation of IAA what was suggested as a factor enabling root colonization (Zúñiga et al. 2013). Despite the sequencing of the entire genome of B. phytoirmans PsJN, most of its functions, especially those related to the interaction with plant genes are not yet explained (Sessitsch et al. 2005). Despite the ability to colonize many plant species and repeatedly proven beneicial impact on several plants, level of growth promotion by PsJN is cultivar speciic (Conn et al. 1997). In vitro and ex vitro bacterization/biotization of micropropagated plants It is reasonable to use some bacteria for supporting plant growth and resistance in biofertilization or bioprotection, in
Plant Cell Tiss Organ Cult
order to reduce the use of mineral fertilizers and pesticides in agriculture. Bacterization can be particularly meaningful in organic plant production. Many microorganisms were found to be beneicial for plants, but their efectiveness in the ield was not conirmed in the ield trials or ield trials were not conducted (Owen et al. 2015). The efectiveness of preparations based on living organisms and provided for living organisms is very dependent on environmental conditions. Especially diicult is maintaining a high bacterial population in the soil during the time of plant colonization. Research should include the highest concern for searching for more efective bacteria, including genetically engineered, better formulated, resistant to sub-optimal environmental conditions, and consortia of microorganisms, which will mimic at least partly, the natural plant microbiome that is numerous, multispecies and multifunctional, as well as for positively reacting cultivars (Owen et al. 2015). A history of bacterial inoculation on the background of contemporary knowledge was reviewed earlier (Bashan 1998; Bashan et al. 2014). The idea of an application of bacteria to improve the efectiveness of micropropagation emerged more than three decades ago. The possibility of improving the eiciency of plant tissue cultures with the aid of some bacterial “contaminators” was originally suggested by Herman (Herman 1987, 1990). The result of bacterization of plant cultures in vitro was at irst reported by Digat et al. (1987), who discovered the positive inluence of Pseudomonas luorescens and P. putida strains on the rooting and acclimatization of primula microshoots. Subsequent reports showed the beneicial efect of Pseudomonas sp. and P. mucidolens in avoiding hyperhydricity in oregano and raspberry cultures (Shetty et al. 1995; Ueno et al. 1998). Nowak (1998) reviewed the idea of bacterization of in vitro explants quoting a number of beneicial efects caused by some bacteria on in vitro cultures, emphasizing beneits on post in-vitro growth. The microplants are exposed to high stress after being transferred to ex vitro conditions, when they must become autotrophic organisms. At this time, poor development of vascular and covering tissues and a lack of functional roots, dryness of leaves, photo-inhibition caused by excessive exposure to the sun in the absence of a matured photosynthetic apparatus, and infections by pathogenic microorganisms are all real threats. Beneicial bacteria may help in the ight against stress, not only by providing growth regulators, facilitating nutrient uptake and direct or indirect protection against stresses, but also through initiating microplant defense responses in the process of biohardening or priming (Nowak and Shulaev 2003; Chandra et al. 2010; Panigrahi et al. 2015). This process was described broadly in potato cultures (Nowak et al. 1999). Compant et al. (2005) noted that the beneicial bacteria used when inoculating explants at the in vitro stage, could
stimulate the induction of defense processes, which may be crucial in overcoming transplanting stress. Although technically, biotization of explants during in vitro culture is relatively easy, some condition parameters such as inoculation density and temperature should be met (Pillay and Nowak 1997; Ardanov et al. 2011). As was mentioned above, bacterization is not always rational at the in vitro stage of propagation, but may be more appropriate for the acclimatization, and added at weaning, after delasking, to the naked roots or the growth substrate. Several examples illustrating the role of bacterization in acclimatization are given in Table 2. They include Rhizobium for Robinia (Balla et al. 1998) or Bacillus for banana (JaizmeVega et al. 2004; Suada et al. 2015), Efect of bacterization before or during acclimatization can be maintained also during the ield cultivation, positively inluencing growth and yielding of plants by the constant presence of bacteria in plants or by the activation of defensive processes initiated in the previous growth stage (priming) (Table 3). Although it is easier to perform bacterization on explants at the stage of in vitro cultures, it may be not preferable in all cases. Thomas et al. (2010) found that inoculation at the in vitro rooting stage of tea microshoots with Pseudomonas luorescens and Azospirillum brasilense isolated from tea plants was not efective, as the irst one did not colonize and the second one overgrew the cultures and inhibited the growth of shoots. However, when these bacteria were added to the substrate during acclimatization in the greenhouse they increased survival by 30% for Pseudomonas luorescens and 60% for Azospirillum brasilense and stimulated growth of roots and shoots. The advantage of using bacteria for growth promotion and priming for resistance against stresses still depends on the genotypes of bacteria and the host plants and the growing conditions, for both in vitro as well as in vivo conditions. In vitro cultures as a useful model for studying efects of bacteria on plants The ease of bacterial application and deining the plant response in vitro are factors to consider in the pre-selection of suitable microorganisms as bioprotectors or biofertilizers to apply in the ield. The impact of Burkholderia phytoirmans PsJN on the ability of in vitro grapevine cultures to resist low temperatures (4 °C) was studied using as a markers the weight of roots (Barka et al. 2006), activity of scavenging system (Theocharis et al. 2012), and carbohydrate metabolism (Fernandez et al. 2012). Sensitivity of potato to high temperatures (33/25 °C), was decreased by PsJN and expressed by increased stem length, shoot and root biomass and stronger tuberization post in vitro (Bensalim et al. 1998). Gonzalez et al. (2015) stated that jojoba microshoots inoculated in vitro with Azospirillum brasilense
13
13
As above
From shoots of sugar canes
1. From microbial collection 2. From rhizosphere of papaya
As above
Enterobacter sp./SC20
1. Gluconoacetobacter diazotrophicus PAL 5 2. Diazotroph Pachaz 008
NA not available
As above
From meristems of 3 strawberry cultivars propagated in vitro From onion roots
Bacillus subtilis—7 strains Sphingopyxis sp.
As above
From diseased wheat seeds
Bacillus subtilis DAR26659
As above
1. From microbial collection 2., 3. Locally isolated
1. Azospirillum brasilense/Cd 2. A. brasilense/Sp7 3. A. brasilense/Az 39
Burkholderia phytoirmans/ PsJN™ (earlier Pseudomonas sp./PsJN) As above
Inoculated on embryogenic callus of rice
From stem nodules of Aeschynomene aspera
Azorhizobium caulinodans/ ORS 571
Type of action
Increased length of shoots, weight of biomass and number of grains Before rooting of Photinia × Better adaptation to in vivo fraseri conditions; accelerated leaves development, stimulated the thickening of the cuticle and elongation of the hair root zone Reduced disease incidence, On fully acclimatized microincreased fresh and dry plants of ginseng planted weight of shoots and rhiin the soil infected with F. zomes oxysporum f. sp. zingiberi On base of strawberry microIncreased number and length of shoots roots, dry matter of roots and shoots and number of leaves On tomato plantlets sensitive Protected plants in greenhouse for Verticillium dahliae during early growth stage (5 months) against V. dahliae On nodal explants of 18 potato Promoted growth of 10 potato clones breeding clones, increased shoot length and biomass weight of shoots and roots, tuber number and weight On weaned seedling roots of Increased shoot and root Panicum virgatum biomasses, accelerated tillering. The growth stimulation difered with genotypes On germinating Arabidopsis Increased fresh weight of seeds 14-day old seedlings, number of hair roots, content of chlorophyll and leaves surface, accelerated tillering On rooted shoots of Saccharum Increased dry weight of shoots oicinarum and roots On roots of pre-hardened 1. Increased plants height Agave tequilana plants 2. Increased stem diameter
Subject of inoculation
Source
Taxon/strain
Table 3 Taxon, source, action and impact of bacteria used in bacterization of microplants on the plant ield performance
Senthilkumar et al. (2008)
Larraburu et al. (2010)
Rames et al. (2009)
Dias et al. (2009)
Sharma and Nowak (1998)
Bensalim et al. (1998)
Kim et al. (2012)
Nitrogenase activity
Development of microaggregates around roots (7-yearold trees)
Ability to lyse fungal hyphae
Solubility of phosphates and IAA production NA
NA
NA
Assimilation of aerial nitrogen, Mirza et al. (2001) production of IAA Nutritional and hormonal Ruiz et al. (2011) support
Activates 408 genes, including Poupin et al. (2013) those connected with auxin and gibberellin metabolism and with stress response
Authors
The impact mechanism
Plant Cell Tiss Organ Cult
Plant Cell Tiss Organ Cult
were less sensitive to NaCl in the medium as expressed by rooting ability. B. phytoirmans PsJN inoculated on vitro microshoots of grapevine protected cultures against grey mold indicating its usability in the ield. Rakotoniriana et al. (2013) tested in vitro a possibility to protect Centella asiatica against Colletotrichum higginsianum with the aid of Bacillus subtilis BCA31. (See also Table 3). In vitro cultures were used to study the potency of bacteria as biofertilizers in several instances. Wang et al. (2015) tested in vitro inluence of PsJN on switchgrass and revealed that inoculated seedlings had higher biomass, which constitutes very good indication for the use of this bacterium in ield production. Guglielmetti et al. (2013) tested the in vitro efect of Luteibacter rhizovicinus MIMR1, producing IAA and molecules chelating iron ions, and dissolving calcium phosphate on root growth of barley seedlings and found that it was a good candidate to apply as a bio-fertilizer component. Montañez et al. (2012) and Naveed et al. (2014b), conirmed that the method using in vitro culture in testing usefulness of bacteria for maize growth promotion can be used for preselecting bacteria for their use as bio-inoculants under ield conditions.
Conclusions One of the reasons for the propagation of plants under in vitro conditions is that the planting material produced is free from diseases and pests. The use of sterile technique during in vitro propagation ensures that uninfected explants introduced into culture, are likely to remain so. For this reason, an important and obligatory element of the initial step is to verify that pathogenic microorganisms (fungi, bacteria, phytoplasma, viruses and viroids) are not present in the donor plants (Reed and Tanprasert 1995). There is a common belief that the total (hypothetical) elimination of bacteria from plant tissues would cause signiicant changes in the phenotype of plants in terms of morphological and functional features (Rosenblueth and Martinez-Romero 2006; de Almeida et al. 2009). Due to the undetected bacteria present in plant tissues, the term “axenic” (explants free of all biological contaminations) can not be used. Instead, the term “aseptic” (free of detectable contamination) is best used for properly maintained plants in vitro cultures (Cassells 2011) that are free of pathogens and visible contaminants and are periodically tested for cultivable microbiota. Pathogenic bacteria and those that easily multiply on plant media should be strictly prohibited from in vitro cultures. The others should be detected through routine bacteriological indexing and removed (Reed et al. 1995). In addition to the removal of pathogenic and contaminating bacteria, positive attention
should be paid to those bacteria that can be helpful in micropropagation. Partida-Martinez and Heil (2011) propose that plants and their inhabiting bacteria form “super-organisms” that should be treated as an ecosystem. The interaction between plant and endophytic bacteria can range from commensalism to mutualism or switch to antagonism under certain conditions. Bacteria can inluence plants through molecular signaling, modulation of host hormonal balance, modiication of plant nutrition, and priming for tolerance of stresses, thus increasing plant productivity (Hardoim et al. 2015). Plants also inluence the number, diversity and activity of microorganisms in the rhizosphere as well as those that inhabit the tissues endophytically (Vacheron et al. 2013). Given the myriad of microorganisms living in the environment that may afect the plant and each other, many unknowns can be expected regarding their interactions. To better understand this world, it is necessary use more eicient methods, such as next-generation (high-throughput) sequencing technologies (NGS) (Mendes et al. 2011; Knief 2014) for the identiication of microbiomes and genes involved in these interactions. These technologies are now more available and afordable than earlier sequencing methodologies. The multiplicity and diversity of bacteria provoke scientists to study interactions of plant microbes for practical use in agriculture. This has been realized for years in the form of commercial preparations containing beneicial bacteria. It would be naive to hope that single microorganisms or a limited number of microorganisms organized in consortia will improve wellness of a diverse range of plants grown in varied environmental conditions. Therefore their success mostly depends on plant type, place of growth and vegetation season. Nevertheless, the most beneits should be expected from situations where plants grow in suboptimal or poor conditions. There are several examples indicating that intentional inoculation of cultures with growth promoting bacteria can signiicantly improve in vitro propagation, adventitious organogenesis or embryogenesis, but many more reports show the beneicial role of inoculation with those bacteria for acclimatization of microplants to ex vitro conditions (Chandra et al. 2010). A supplementation of microplants with selected bacteria can help to re-establish at least partly the ex vitro microbiome and thus protect young plants before the stresses that accompany acclimatization. Although interaction of some beneicial endophytic bacteria with some plant hosts are partially deined and some are practically exploited, the relationship of these bacteria with other microorganisms living on and in the plant and in the rhizosphere remains largely unknown in most cases (Compant et al. 2013) and therefore their inluence is not always repeatable and even can be unpredictable.
13
Plant Cell Tiss Organ Cult
Bacterization of microcuttings or microplants during in vitro culture is relatively easy and allows better control of the colonization process during the rooting on solid or in liquid medium or upon transfer to a greenhouse in a sterile substrate. On the other hand, the efect of bacterization is of less importance for in vitro stages, since the conditions for growth are generally suitable. Keeping in mind that endophytic bacteria reveal their full beneicial impact on plants growing in adverse conditions (Lowman et al. 2015), their use for in vitro cultures is not always necessary due to the ease of optimizing the in vitro conditions by other means but it can be beneicial in the acclimated plant. Author contributions TO conceived the project and did most of the writing with emphasis on beneicial bacteria, KN collected and analyzed the literature, BR assisted with literature analysis, writing with emphasis on contamination, reference management and editing. Compliance with ethical standards Conlict of interest of interest.
The authors declare that they have no conlict
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