Abstract
Shoot endophytic bacteria have mainly been isolated during plant tissue culture started from shoot tips (buds) or embryos. With methods such as in situ hybridization and transmission electron microscopy, endophytic bacteria have been localized in buds, seeds, and flowers of forest trees. By GFP tagging of endophytic bacteria, colonization of tree seedlings has been observed. It is still unknown whether shoot-associated bacteria are transmitted to new trees via seeds, although many results point to this direction. Interactions between the plant and endophytic bacteria in the shoots likely differ to some extent from those in the roots. Shoot endophytic bacteria share some mechanisms of plant growth promotion with the root endophytes, such as the ability of producing plant growth hormones. In addition, some shoot endophytes may affect plant growth through production of adenine derivatives or bacterial photosynthesis. An interesting new mechanism of enhancing host growth is suggested for intracellular bacteria that can act directly through production of nucleomodulins, eukaryotic transcription factors, encoded in the bacterial genome. This mechanism was identified through genome sequencing of a shoot endosymbiont. Therefore, we can expect further interesting discoveries in the future on shoot endophytes of forest trees.
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1 Introduction
Whereas the majority of endophyte studies of forest trees have concentrated on the diversity of fungi, very little is known about endophytic bacteria and especially their function in tree tissues. Endophytic bacteria mainly in the genera Pseudomonas, Bacillus, Paenibacillus, Erwinia and Burkholderia are found almost in every tissue of a tree (for details, see chapter by Frank in this volume). Most studies have been performed on root-associated endophytic bacteria, which differ from the shoot-associated endophytes by their diversity and function (Moore et al. 2006; Yrjälä et al. 2010; Beckers et al. 2017). Plant shoot tissues are exposed to UV radiation, rapidly fluctuating temperatures, alternation in relative humidity and limited nutrient resources compared to roots. Due to exposure to different spectra of light, the shoot tissues are dominated by pigmented bacteria with the capacity for photosynthesis. Shoot tissues produce methanol, which is emitted to the atmosphere (Nemecek-Marshall et al. 1995), and the ability to utilize methanol as an energy source is typical for shoot-associated bacteria (Fall 1996; Pirttilä et al. 2008; Yrjälä et al. 2010; Compant et al. 2011).
In this chapter tree shoot tissues, especially shoot tips (buds), flowers, seeds, and seedlings, are discussed with respect to endophytic bacteria and their role in tree development and growth. Lately some significant new developments have been made within this area.
2 Tissue Cultures and Shoot Tips
Typically endophytic bacteria of tree shoot tips or buds are found during tissue culture, because the shoot tip meristems or embryos are often used as the starting material. For example, endophytic bacteria have been detected in the tissue cultures of hazelnut (Corylus avellana L., C. contorta C.) (Reed et al. 1998), cherry (Prunus cerasus L., P. avium L.) (Kamoun et al. 1998; Quambusch et al. 2014), various species of poplar, larch, black locust (Robinia pseudoacacia L.), Norway spruce (Picea abies Karst.) (Ulrich et al. 2008; Van Aken et al. 2004), and Scots pine (Pinus sylvestris L.) (Laukkanen et al. 2000; Pirttilä et al. 2000). In the study by Ulrich et al. (2008), the majority of endophytes were identified as members of Paenibacillus in 5-year old cultures initiated from shoot tips or immature or mature zygotic embryos of poplar, larch, black locust and spruce. Other genera such as Methylobacterium, Stenotrophomonas and Bacillus were occasionally detected in these cultures (Ulrich et al. 2008). The Paenibacillus spp. had no visible negative effect on the plant development, and one strain isolated from poplar cultures had a growth-promoting effect on seedlings (Ulrich et al. 2008).
Plant tissue culture as a propagation tool is selective on endophytes, as some species can thrive in the cultured tissues, being enriched through generations, and others can vanish or die during the procedures (Koskimäki et al. 2010). The quality of the enriched endophyte species, whether beneficial for the host or not, can affect the result of tissue culture. Growth-promoting bacteria will promote growth and differentiation of the plant tissue, but tissue cultures with enriched endophytic bacteria that are commensalistic or have other roles with the host will not grow well. This has been shown in wild cherry (Prunus avium L.), where presence of Rhodopseudomonas sp. and Microbacterium sp. strains improved the success of tissue culture (Quambusch et al. 2014, 2016), and in walnut, where Moraxella spp. was associated with well-growing cultures (Pham et al. 2017). Diversity of endophytes might similarly affect the success of tissue culture of Scots pine. The endophytic bacteria Methylobacterium extorquens, Pseudomonas synxantha, Mycobacterium sp. and the yeast Rhodotorula minuta were isolated from callus cultures originating from shoot tips (Laukkanen et al. 2000; Pirttilä et al. 2000, 2003). These endophytes were detected by in situ hybridization to form biofilms in the cells of the growing callus of Scots pine, whereas no endophytes were detected in embryogenic tissue of European black pine (Pinus nigra Arn.) (Pirttilä et al. 2002). The biofilm might be a common form of endophytic bacteria living inside plant tissue (Bandara et al. 2006; Podolich et al. 2009).
Even though the isolated strains are useful for studying phenotype, genotype, and other characteristics, the majority of endophytes, especially those having the most intimate relationships with the host, are probably unculturable. Therefore culture-independent techniques should be applied and developed for the research on endophytes. By in situ hybridization, the endophytes isolated from Scots pine tissue cultures were further observed in the cells of scale primordia, the meristems, and around the resin ducts of intact buds (Pirttilä et al. 2000, 2003). Using transmission electron microscopy (TEM) and the tag of green fluorescent protein (GFP), the intracellular location was recently confirmed for these endophytes in bud tissues of Scots pine (Koskimäki et al. 2015).
The endophytes of Scots pine were most abundant or metabolically active in the bud tissues prior to growth or differentiation of the buds (Pirttilä et al. 2005), suggesting a role in regeneration of the shoot tips. Our recent study on bud endophytes of mountain birch supports this view. By next-generation sequencing (NGS), we studied the microbiome of buds of mountain birch trees, which have a recovery mechanism of producing sprouts after moth herbivory. We discovered that members of Xanthomonadaceae and Pseudomonales comprise the majority of mountain birch bud microbiome. Most importantly, we found that the shoot tips of mountain birch sprouts have the highest diversity of endophytes and contain significantly more Pseudomonas species than the shoot tips of mature trees (Riikola et al., unpublished).
3 Flowers, Seeds and Seedlings
Seed endophytes are potentially highly important for the host, providing the first members of the endophytic microbiome in the growing seedling. They can have a significant effect on the health of the seedling, depending on the quality of interaction with the host. Recently, the microbiome in seeds of a bee-pollinated leguminous tree Anadenanthera colubrina was characterized by culturing and NGS (Alibrandi et al. 2017). Several strains of Methylobacterium and Staphylococcus were identified as endophytes, along with members in the genera Friedmaniella, Bifidobacterium, Delftia, Anaerococcus and Actinomyces. These seed-associated endophytic bacteria were localized by fluorescent in situ hybridization (FISH) in intercellular spaces or vascular tissue of the seed (Alibrandi et al. 2017).
Study on seed endophytes is somewhat motivated by the question of whether endophytes are transmitted vertically between generations. In Eucalyptus, the endophyte transmission was studied between seeds and seedlings by Ferreira et al. (2008). They discovered that the same strains of Bacillus, Paenibacillus, and Enterococcus were present both in seeds and seedlings grown from the seeds. When a GFP-tagged endophyte of E. grandis, Pantoea agglomerans, was inoculated into Eucalyptus seeds, the colonization was confirmed for E. grandis and the hybrid E. grandis × E. globulus, but not for E. urophylla. The strain was detected colonizing intercellular spaces of seedling roots and xylem vessels of the stem. No leaves of any seedling were colonized by the GFP-tagged strain (Ferreira et al. 2008), which, on the other hand, indicates a horizontal transmission.
However, for a true vertical transmission to occur, an endophyte should be present in the flowers of the mother plant and transfer through the seed to a new seedling. The presence of endophytes in the flowers has been studied in several conifer species. For example, the bacterium Enterobacter cloacae has been isolated from pollen of Aleppo pine (Pinus halepensis M.) and stone pine (P. pinea L.), and from fertilized ovules of Turkish pine (P. brutia Tenore) (Madmony et al. 2005). If found in seeds, this bacterium could represent an example of vertically transmitted endophyte. In Scots pine, endophytes were not detected in pollen grains but the sporogenous cells of the male flowers contained endophytes as biofilm-like structures based on in situ hybridization studies (Pirttilä 2011). Endophytes were found in lower numbers in the female inflorescences of Scots pine, but seed embryos were heavily colonized (Pirttilä 2011). In the seeds of Norway spruce, bacterial endophytes belonging to the genus Rahnella have been isolated from the embryo and endosperm (Cankar et al. 2005). Therefore, a lot of evidence exists on the potentially vertical transmission of endophytic bacteria in conifers. However, proving a true vertical transmission is difficult in forest trees due to their longevity.
4 Effect of Shoot-Associated Bacteria on Plant Host
Methanol plays a significant role in the plant-endophyte interaction in the shoots, because it is produced by the shoots. Methanol represents an excellent carbon source for methylotrophic bacteria, which can utilize methanol and methane as the energy source (Fall 1996; Fall and Benson 1996). Methylotrophs have the unique ability to utilize methanol and methane as the energy source and are ecologically important organisms as they minimize the emission of methanol and methane from plants to the atmosphere (Fall 1996; Fall and Benson 1996; Keppler et al. 2009). The methylotropic endophytes are beneficial for the plant simply by consuming methanol, because methanol is toxic for the plant (Gout et al. 2000). The facts that methanol applied exogenously on the shoots increases growth, but on the roots leads to toxic effects (Nonomura and Benson 1991; Ramírez et al. 2006), suggests that methylotrophs not only consume methanol but also transform it to compounds useful for the host.
In general, many studies have outlined the positive effects of shoot endophytic bacteria, specifically in the genus Methylobacterium, on tissue organogenesis and embryogenesis (Holland and Polacco 1994; Visser et al. 1994; Murthy et al. 1999; Kalyaeva et al. 2001). Methylotrophic bacteria stimulate seed germination of soybean (Holland and Polacco 1994; Freyermuth et al. 1996; Holland 1997; Koenig et al. 2002), induce formation of morphogenic calli and shoots and promote the development of the regenerated plants of Triticum aestivum L., Nicotiana tabacum L., Solanum tuberosum L., and Linum usitatissimum L. (Kalyaeva et al. 2001). Some Methylobacterium strains are reported to produce plant growth hormones (Ivanova et al. 2000, 2001; Koenig et al. 2002). Additional mechanisms for plant growth promotion have been suggested to exist (Koenig et al. 2002). It is likely that endophytic bacteria of the shoots have several ways of affecting the development and the growth of tree host. Below, some generally known growth-promoting effects are described and considered with regard to shoot endophytes.
4.1 Phytohormone Production
Plant-associated bacteria typically produce plant growth hormones such as cytokinins, auxins and gibberellins. Whereas gibberellin production is most typical for the root-associated bacteria, cytokinins have been identified in some leaf isolates, and auxin production is common to all plant-associated microbes (Bottini et al. 2004; Ivanova et al. 2008). Although many plant-associated bacteria produce plant growth hormones, there may be great variations in the quantities between the strains within a species (Ivanova et al. 2008). Furthermore, it should be noted that a study on endophytic bacteria of Solanum nigrum suggests that the growth promotion effects cannot be generalized to all host plants, even if the underlying mechanisms were general, such as phytohormone production (Long et al. 2008).
Auxins are a group of indole derivatives that have various growth-promoting functions in plants, such as promotion of root formation, regulation of fruit ripening, and stimulation of cell division, extension, and differentiation. Indole-acetic acid (IAA) is the most-well known auxin. In poplar, the endophytes Enterobacter str. 638, Stenotrophomonas maltophilia str. R551-3, Serratia proteamaculans and Pseudomonas putida str. W619 have been identified as IAA-producing bacteria (Taghavi et al. 2009). Another interesting finding is that the endophytic bacterium Enterobacter cloacae, isolated from pollen grains of Pinus spp., produces IAA and promotes growth of mung bean cuttings (Madmony et al. 2005).
Cytokinins are a group of compounds with the backbone of adenine having a substitution at the N-6 atom of the purine ring. These compounds are important in many steps of plant development, as they stimulate plant cell division, induce germination of seeds, activate dormant buds and play a role in apical dominance. Because cytokinins induce the biosynthesis of chlorophyll, nucleic acids, and chloroplast proteins at the early stages of leaf development (Skoog and Armstrong 1970), one would expect a role for them in shoots by endophytic bacteria. However, no reports are found on cytokinin-producing endophytic bacteria isolated from shoot tissues. Perhaps an endophyte producing cytokinin in the photosynthetic tissues would create imbalance and have drastic effects on the host health.
4.2 Other Plant Growth Promoting Compounds
The bud endophytes of Scots pine, Methylobacterium extorquens DSM13060 and Pseudomonas synxantha DSM13080, produce compounds that extend the viability and affect morphology of callus tissues in vitro (Pirttilä et al. 2004). However, these compounds are not the most common phytohormones, such as cytokinins, gibberellins, or auxins. Instead, M. extorquens DSM13060 excretes adenine and adenine ribosides in the culture medium (Pirttilä et al. 2004). Adenine can be used in plant meristem cultures to induce growth. Whereas the mode of action of adenine on plant growth promotion is unknown, it is most effective when applied together with ammonium nitrate and cytokinins (George and Sherrington 1984). Furthermore, in feeding experiments with Coffea arabica, adenine riboside has been detected as the metabolite of adenine (Baumann et al. 1994). Adenine riboside is also abundant in the vascular cambial region of Pinus sylvestris, which is uncommon for other plants (Moritz and Sundberg 1996; Pirttilä et al. 2004).
4.3 Aminocyclopropane-1-Carboxylate (ACC) Deaminase
A plant growth-promoting trait of endophytes often discussed is the production of aminocyclopropane-1-carboxylate (ACC) deaminase. This bacterial enzyme transforms the ethylene precursor ACC to 2-oxobutanoate and ammonia to be used in bacterial nitrogen metabolism. Ethylene, a plant stress hormone, is stored and transported mainly as ACC within the plant tissues, and transformation of ACC to other compounds prevents ethylene signaling. The ACC deaminase enzyme produced by endophytes could therefore enhance plant growth in stressful conditions and overcome defense responses during bacterial infection (Glick 2005). In fact, inactivation of ACC deaminase in the root endophyte Burkholderia phytofirmans PsJN removes the effect of root elongation in canola seedlings, indicating a growth-promoting role for this enzyme (Sun et al. 2009). Although the endophytes with ACC deaminase enzyme are primarily associated with roots, a study on cut flowers showed that endophytic bacteria can activate the ACC deaminase in the shoots to prolong flowering (Ali et al. 2012). Furthermore, ACC deaminase might have an important role in the seeds, as the ethylene phytohormone is associated with germination. In fact, an ACC deaminase-carrying endophytic actinomycete Kibdelosporangium phytohabitans has been identified in the seeds of the oil plant Jatropha curcas L. (Xing et al. 2012).
However, the analysis on bacterial endophyte genomes made in the first volume of this book (Frank 2011) indicated that ACC deaminase might not be as important trait in endophytes as previously thought. Furthermore, several annotated ACC deaminase genes might represent another enzyme highly similar by amino acid sequence, D-cysteine desulfhydrase. The bud endophyte Methylobacterium extorquens DSM13060 carries this gene, which is rarely activated during colonization of pine seedlings (Koskimäki et al. 2015).
4.4 Vitamin B12 Production
Vitamin B12 production has been considered a plant growth-promoting trait in epiphytes (Toraya et al. 1975; Ivanova et al. 2006) and endophytes (Ivanova et al. 2008), and most methylotrophs are able to synthesize vitamin B12 (Nishio et al. 1977; Ivanova et al. 2006, 2008). Vitamin B12 is a group of compounds with trivalent cobalt as a cofactor. These compounds function as the coenzyme in isomerization and transmethylation reactions in the biosynthesis of compounds containing methyl groups. The enzymes with the coenzyme form of vitamin B12 are found in many flowering plants that cannot synthesize vitamin B12 themselves (Holland and Polacco 1994). Therefore, vitamin B12 produced by endophytic bacteria is suggested to benefit plants, and studies have shown the importance in algae and bryophytes (Basile et al. 1985; Croft et al. 2005). When applied exogenously, vitamin B12 increases the biomass, amount, length, and the degree of branching of moss gametophytes (Basile et al. 1985), the same effects, which are induced by methylotrophs (Koopman and Kutschera 2005; Croft et al. 2005).
However, when the shoot endophyte M. extorquens DSM13060 carrying a fluorescent reporter controlled by the cobalamin synthase (cobS) promoter was inoculated into pine seedlings, no activity was observed (Koskimäki et al. 2015). This suggests a smaller role for vitamin B12 as an endophytic product in the higher plants than anticipated. Because vitamin B12-independent methionine synthase has been identified from higher plants, they might not depend on the bacterial source (Eichel et al. 2008).
4.5 Photosynthesis
Bacterial photosynthesis is a little discussed subject considering endophytic shoot bacteria and their benefits for the host, but well studied in stem nodulation of legumes. In stem-nodulating Bradyrhizobium strains, photosynthesis is associated with higher infection rates and more efficient nitrogen fixation (Giraud et al. 2000). The photosynthesis is activated in response to far-red light by the bacteriophytochrome (BphP) in Bradyrhizobium spp. (Giraud et al. 2002). However, the capacity for photosynthesis is restricted to the stem-nodulating strains of Bradyrhizobium spp., but photosynthetic capacity is universally found within the genus Methylobacterium (Koskimäki et al. 2015). This suggests that photosynthesis has a conserved and important role, potentially in plant-endophyte interactions, of members of the genus Methylobacterium. When the bud endophyte M. extorquens DSM13060 carrying a fluorescent reporter controlled by the BphP promoter was inoculated to pine seedlings, the promoter was activated in bacteria infecting root cells. However, no activation of BphP was observed in bacteria colonizing shoot tissues. This would indicate that the bacteriophytochrome of M. extorquens DSM13060 is synthesized in the dark, and that activation of photosynthesis is important at the beginning of infection (Koskimäki et al. 2015). Similar observations have been made in the stem-nodulating Bradyrhizobia (Giraud et al. 2000, 2002). Bacteriophytochromes can have additional signaling functions, as shown for nonphotosynthetic bacteria. In Pseudomonas syringae, the BphP1 together with blue light receptor LOV-HK positively regulate swarming motility in response to red and far-red light (Wu et al. 2013), affecting infection capacity (Río-Álvarez et al. 2014).
4.6 Nitrogen Fixation
Nitrogen fixation is a well-studied trait in the rhizobial and actinorhizal symbioses, and almost all root endophytes fix nitrogen (Baldani et al. 1997). However, the agricultural significance of endophytic nitrogen fixation has been considered low (Dalla Santa et al. 2004). Diazotrophic (nitrogen-fixing) strains have also been isolated as endophytes from tree tissues. For example, Burkholderia, Rahnella, Sphingomonas and Acinetobacter have been isolated from stems of poplar and willow (Doty et al. 2009). When poplar seedlings were grown in vitro with the diazotrophic endophyte Paenibacillus str. P22, the metabolite profile of the inoculated plants suggested that nitrogen was fixed by the bacterium and assimilated by the plant (Ulrich et al. 2008; Scherling et al. 2009). Nitrogen fixation and assimilation by host plant have recently been shown in seedlings of lodgepole pine (Pinus contorta D.) (Anand et al. 2013) and, most interestingly, in needles of limber pine (Pinus flexilis E. James) (Carrell and Frank 2014; Moyes et al. 2016). The diversity of diazotrophic strains was found the highest in the foliage under shade in Eucalyptus, which might suggest participation of light in the process (Miguel et al. 2016). Due to significant recent progress within this area, nitrogen fixation by endophytic bacteria in forest trees is discussed in detail by Oses et al. in this volume of the book.
4.7 Other Mechanism of Interaction
The bud endophyte of Scots pine, M. extorquens DSM13060, is a methylotroph and has the capacity to consume methanol as the carbon and energy source (Koskimäki et al. 2015). Upon infection of the host, the bacterium can biosynthesize the carbon reserve compound polyhydroxybutyrate (PHB) from plant-produced methanol. During colonization process, PHB becomes degraded by phaZ depolymerases, not only for an energy source, but also for producing antioxidants. The PHB degradation yields methyl-esterified 3-hydroxybutyrate oligomers, which have antioxidant activity towards host-induced oxidative stress. Production of these oligomers will help the bacterium to bypass host defenses for colonization of further tissues (Koskimäki et al. 2016).
Once intracellular, M. extorquens DSM13060 aggregates around the nuclei of living host cells (Koskimäki et al. 2015). This suggests modification of the host nuclear processes. The genome of M. extorquens DSM13060 encodes eukaryotic effector-like proteins, so-called nucleomodulins, which can target host nuclear functions. The nucleomodulins could be responsible for several effects observed on the host (Koskimäki et al. 2015).
Besides producing antioxidants and manipulating host cells, shoot endophytic bacteria have been discovered to co-synthesize compounds with the host. In strawberry, Methylobacterium spp. have been reported to produce lactaldehyde, the precursor of the strawberry flavor compound 2,5-dimethyl-4-hydroxy-2H-furan-3-one (DMHF) from 1,2-propanediol (Zabetakis 1997; Koutsompogeras et al. 2007). Using in situ hybridization, endophytic bacteria have been observed in the receptacle vascular tissue and in the cells of achenes of raw strawberry. Furthermore, the bacterial methanol dehydrogenase, responsible of 1,2-propanediol oxidation, and plant DMHF biosynthesis genes were simultaneously activated in the same receptacle tissues or cells where endophytes were present. This indicates that the methanol dehydrogenase of the endophytic bacteria helps the host to synthesize well-known plant compounds (Nasopoulou et al. 2014).
5 Conclusions
Although many endophytes probably enter the plant from the soil through the roots and are able to colonize the entire plant through vascular tissues, tree shoot tissues and reproductive organs provide different ecological niches for endophytic bacteria compared to roots (Moore et al. 2006; Yrjälä et al. 2010). Furthermore, some shoot endophytic bacteria are likely vertically transmitted through the seeds. Because the growth-promoting effects of endophytes can be strain- and host-specific (Long et al. 2008), the term “endophyte” cannot be generalized with respect to function and significance, and each case should be studied separately. Shoot endophytes can increase growth of the host to the same extent as mycorrhizal fungi (Pohjanen et al. 2014). Many interesting new mechanisms specific for shoot endophytic bacteria have been uncovered, demonstrating that there is more to the plant-endophyte interaction than previously thought. As mycorrhizal fungi are today acknowledged significant organisms for health and growth of forest trees, endophytic bacteria can provide a number of benefits for forestry in the future. Advancing methodologies such as genomics and metabolomics will be valuable tools for describing the significance of endophytic bacteria for forest trees.
Abbreviations
- TEM:
-
Transmission electron microscopy
- PHB:
-
Polyhydroxybutyrate
- GFP:
-
Green fluorescent protein
- IAA:
-
Indole-acetic acid
- NGS:
-
Next-generation sequencing
- DMHF:
-
2,5-dimethyl-4-hydroxy-2H-furan-3-one
- BphP:
-
Bacteriophytochrome
- ACC:
-
Aminocyclopropane-1-carboxylate
- FISH:
-
Fluorescent in situ hybridization
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Pirttilä, A.M. (2018). Endophytic Bacteria in Tree Shoot Tissues and Their Effects on Host. In: Pirttilä, A., Frank, A. (eds) Endophytes of Forest Trees. Forestry Sciences, vol 86. Springer, Cham. https://doi.org/10.1007/978-3-319-89833-9_8
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