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Isolation, Characterization and Plant Growth Promotion Effects of Putative Bacterial Endophytes Associated with Sweet Sorghum (Sorghum Bicolor (L) Moench)

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Isolation, Characterization and Plant Growth Promotion Effects of Putative Bacterial Endophytes Associated with Sweet Sorghum (Sorghum Bicolor (L) Moench) Ann Microbiol (2015) 65:1057–1067 DOI 10.1007/s13213-014-0951-7 ORIGINAL ARTICLE Isolation, characterization and plant growth promotion effects of putative bacterial endophytes associated with sweet sorghum (Sorghum bicolor (L) Moench) Cintia Mareque & Cecilia Taulé & Martín Beracochea & Federico Battistoni Received: 21 April 2014 /Accepted: 28 July 2014 /Published online: 13 August 2014 # Springer-Verlag Berlin Heidelberg and the University of Milan 2014 Abstract Sweet sorghum (Sorghum bicolor)iscultivatedin Chryseobacterium, Kocuria, Brevibacillus, Uruguay in complementation with sugarcane (Saccharum Paenibacillus, Bacillus and Staphylococcus.PGPand officinarum) as a feedstock for bioethanol production. It re- infection features were investigated in vitro, and re- quires the application of high levels of chemical fertilizer for vealed some promising biotechnological candidates. In optimal growth, which causes environmental degradation. addition, isolates UYSB13 and UYSB45 showed PGP Plant growth-promoting (PGP) bacteria are of biotechnologi- effects in greenhouse assays. This work provides the cal interest since they can improve the growth of several basis for further studies under field conditions, with important agronomical crops. Of particular interest are endo- the final aim of developing an effective inoculant for phytes, which are those bacteria that can be detected at a sorghum. particular moment within the internal tissues of healthy plants from where they can promote their growth. The Keywords Endophytes . Sweet sorghum . Plant growth aims of this work were to isolate and characterize, as promotion well as identify putatively endophytic bacteria associat- ed with sweet sorghum (cv-M81E), and also to study the inoculation effects of selected isolates on sorghum Introduction growth. A collection of 188 putative endophytes from surface-sterilized stems and roots was constructed and Fossil energy resources are depleting dramatically in characterized. Bacterial isolates were shown to belong order to meet the increasing world energy demands. to different genera including Pantoea, Enterobacter, Moreover, climate change caused by carbon emissions Pseudomonas, Acinetobacter, Stenotrophomonas, from fossil fuels reinforces the need to search for alter- Ralstonia, Herbaspirillum, Achromobacter, Rhizobium, natively energy sources. Crop plants are one of the best sources of renewable energy, as they can be used as Electronic supplementary material The online version of this article feedstock for biofuel production. With this aim, several (doi:10.1007/s13213-014-0951-7) contains supplementary material, complementary crops are cultivated in Uruguay, such as which is available to authorized users. : : : sugarcane (Saccharum officinarum) and sweet sorghum C. Mareque C. Taulé M. Beracochea F. Battistoni (*) (Sorghum bicolor (L.) Moench) (Kim and Day 2011; Microbial Biochemistry and Genomics Department. Instituto de Ratnavathi et al. 2011). Globally, sweet sorghum is the Investigaciones Biológicas Clemente Estable (IIBCE), Avenida Italia 3,318, Montevideo 11600, Uruguay fourth most important cereal, and is known as a multi- e-mail: [email protected] purpose crop since it is used for grain, forage, syrup, C. Mareque fodder and bioethanol production (Almodares and Hadi e-mail: [email protected] 2009; Shoemaker and Bransby 2010). Nevertheless, this C. Taulé crop has a high demand for chemical fertilizer for e-mail: [email protected] optimal productivity, resulting in leaching and run-off M. Beracochea of nutrients, especially nitrogen (N) and phosphorus (P), e-mail: [email protected] leading to environmental degradation (Adesemoye and 1058 Ann Microbiol (2015) 65:1057–1067 Kloepper 2009). These problems emphasize the need for Materials and methods new technologies in agriculture with the aim of attaining more sustainable production systems. A prom- Isolation of putatively endophytic bacteria associated ising alternative to chemical fertilization is the use of with sweet sorghum plant growth-promoting bacteria (PGPB) (Lugtenberg and Kamilova 2009). Amongst these, bacterial endo- With the aim of isolating putative endophytes associated with phytes are referred to as those bacteria that can be the commercial sweet sorghum cv. M81E, two approaches detected at a particular moment within the internal tis- were employed. In the first one, bacteria were isolated from sues of an apparently healthy host plant (Hallmann the roots and stems of trap plants. For this, sterilized seeds et al. 1997;Schulzetal.2006). In contrast to phyto- were sowed into pots containing sterile sand and soil from the pathogenic bacteria, they do not cause any disease sweet sorghum cropping region, Bella Union, Artigas, Uru- symptoms; indeed, they can promote plant growth guay (30°37′56′S, 57°21′18′W, 120 m asl). In the second (James 2000;Berg2009). Mechanisms involved in en- approach, bacteria were isolated from seeds, roots and stems dophytic plant growth promotion (PGP) could be direct of plants collected directly from the field in the same cropping or indirect. Direct PGP mechanisms include biological region. The same surface-sterilization protocol was used for nitrogen fixation (BNF) and mineral solubilisation (P, seed and plant material in both cases. Briefly, 10 g of material Fe), as well as the production of plant phytohormones were incubated for 5 min in 70 % EtOH, then 20 min in 4 % (auxins, cytokinins and gibberellins), while indirect sodium hypochlorite, and finally rinsed 4 times with sterile mechanisms include biocontrol against phytopathogens deionized water. Sterilized seeds for trap plants were germi- mediated by antibiotics, competition for nutrients and nated on 0.8 % water agar plates before sowing. On the other niches, or the induction of an induced systemic resis- hand, for bacterial isolation from roots, stem and seeds, they tance (ISR) response (Rosenblueth and Martínez- were aseptically macerated in a solution of 0.9 % NaCl sup- Romero 2006; Mei and Flinn 2010; Compant et al. plemented with cyclohexamide (100 μg μl−1). Serial dilutions 2010). A number of reports have demonstrated the from the suspensions obtained, were inoculated onto agar association of sweet sorghum with several bacterial en- plates containing DYGs and LGI media in the case of trap dophytes belonging to the genera Herbaspirillum, plants, or TSA (Tryptic Soy Agar; Difco) medium in the case Azospirillum, Klebsiella, Enterobacter, Burkholderia, of field plants. Those culture media were selected with the aim Paenibacillus and others (Olivares et al. 1996; Budi to have a high diversity of heterotrophic bacteria isolates. All et al. 1999; Zinniel et al. 2002; Grönemeyer et al. isolates obtained were purified and stored at −80 °C in 50 % 2011). Moreover, a PGP effect was demonstrated for glycerol. several diazotrophic endophytes, such as Azospirillum lipoferum, A. amazonense, Herbaspirillum seropedicae Screening for biofertilization activities and Gluconacetobacter diazotrophicus, when they were inoculated onto sweet sorghum under greenhouse and With the aim of detecting putatively diazotrophic isolates, the field conditions (Pereira et al. 1988; Sarig et al. 1990; whole collection was subjected to nifH PCR amplification by Chiarini et al. 1998). In consideration of this, the man- using the primers PolF (5′-TGCGAYCCSAARGCBGACTC- agement of the interaction between endophytes and their 3′) and PolR (5′-ATSGCCATCATYTCRCCGGA-3′) (Poly hosts (such as sweet sorghum) might play a significant et al. 2001). In all cases, cell lysates were used as templates role in the development of more sustainable agricultural (Rivas et al. 2001) and a single colony resuspended in water as production systems. In Uruguay, the major sweet sor- a starting material. The PCR mixture was 2.5 μl 10× ghum cultivar used by the producers is cv. M81E, Fermentas Taq reaction buffer, 3.0 mM MgCl2, 0.16 mM which is of national interest. However, until now, no dNTP’s, 0.8 μM of both set of primers, 0.5 U Fermentas studies have been conducted in Uruguay on the native Taq polymerase, 4 % BSA and 4.0 μl of a cell lysate template, microorganisms naturally associated with sweet sorghum or in a final reaction volume of 25 μl. The PCR conditions were have evaluated their potential PGP capability. The aims of this as follows: 1 cycle at 95 °C for 5 min; 30 cycles at 95 °C for work were: (1) to obtain a collection of culturable putatively 45 s; 58 °C for 45 s, and 72 °C for 30 s; and a final cycle at endophytic bacteria associated with sweet sorghum cv. M81E, 72 °C for 5 min. The amplification products were analyzed by (2) to characterize the collection based on PGP and infection 1 % (w/v) agarose gel electrophoresis in TAE buffer and features and thus to identify isolates of interest, and (3) to stained with GoodView (Beijing SBS; Genetech). study the inoculation effects of selected isolates on sweet In addition, the ability to fix N2 was tested in those isolates, sorghum growth. The data obtained will contribute to future which harbored the nifH gene, in vials containing LGI, LGI-P research aimed at developing sweet sorghum inoculants based and JNFb N-free semisolid media (Reis et al. 1994; Perin et al. on native PGPB specifically for cv. M81E. 2006). The vials were incubated at 30 °C for up to 7 days and Ann Microbiol (2015) 65:1057–1067 1059 those which showed a growth pellicle were replicated into a containing 200 μl of TSB (Tryptic Soy Broth; Difco) medium, new fresh vial containing the same media with
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