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We assessed the structure of the microbiome associated to the drought-sensitive pepper plant (Capsicum annuum L.) cultivated in a traditional Egyptian farm, focusing on microbe contribution to a crucial ecosystem service, i.e. plant growth under water deficit. The root system was dissected by sampling root/soil with a different degree of association to the plant: the endosphere, the rhizosphere and the root surrounding soil that were compared to the uncultivated soil. Bacterial community structure and diversity, determined by using Denaturing Gradient Gel Electrophoresis, differed according to the microhabitat, indicating a selective pressure determined by the plant activity. Similarly, culturable bacteria genera showed different distribution in the three root system fractions. Bacillus spp. (68% of the isolates) were mainly recovered from the endosphere, while rhizosphere and the root surrounding soil fractions were dominated by Klebsiella spp. (61% and 44% respectively). Most of the isolates (95%) presented in vitro multiple plant growth promoting (PGP) activities and stress resistance capabilities, but their distribution was different among the root system fractions analyzed, with enhanced abilities for Bacillus and the rhizobacteria strains. We show that the C. annuum rhizosphere under desert farming enriched populations of PGP bacteria capable of enhancing plant photosynthetic activity and biomass synthesis (up to 40%) under drought stress.

Copyright: 2012 Marasco et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

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Therefore, this study is aimed to assess the impact of desert farming on plant-microbe association in pepper cultivated in arid conditions. We aimed to assess the diversity and topological repartition of bacteria in the pepper root system grown under desert farming and investigate whether under such a crop management practice the root system enriches bacteria capable of supporting the plant resistance to drought and water stress.

With this aim we adopted both culture-independent and -dependent approaches. Cluster analysis was applied to DGGE (Denaturing Gradient Gel Electrophoresis) to dissect the structure and the composition of the microbiome associated to pepper endosphere, rhizosphere and root surrounding soil in comparison to unvegetated soil (bulk). A large collection of isolates from different fractions of the plant root system was established and screened in vitro for PGP activities. The rhizo-competence of the bacterial strains was evaluated through an adhesion assay on both Arabidopsis thaliana and pepper rhizoplane. Finally we assessed the capacity of selected strains to support plant growth under water deficiency.

We demonstrated that the application of desert greening techniques in arid lands generate hotspots of microbial diversity in the rhizosphere of plants. These techniques include a virtuous use of water for irrigation, field fertilization with organic fertilizers originating from residues of crops and animal manure and other similar traditional agricultural management practises. Furthermore we documented that plant rhizosphere and endosphere are repository for selected and specialized microbial populations, able to promote plant growth under drought. Thus, desert farming hampers desertification by establishing fertility islands and allows to achieve crop yields despite the adverse environmental conditions.

The potential functionality of pepper associated isolates to sustain plant growth under drought was assessed by a large screening for PGP abilities in relation to drought tolerance, and the resistance to abiotic stresses occurring in arid soils (Table 5). We assessed whether PGP abilities are differentially distributed in the different microhabitats of the pepper root system. All the fractions demonstrated to be colonised with a similar frequency by potential beneficial strains, even though in the non-cultivated arid soil PGP traits were less abundant (Table 5). While none of the isolates showed all the assayed PGP activities, 31,7% and 22,5% of strains presented respectively four and five PGP activities (Fig. S1). All the isolates presented the potential to adapt to unfavourable environmental conditions of arid soils, showing a certain halotolerance, resistance to low water availability and to variable temperature range (Table 5). Similarly, bacteria isolated from the E, R and S plant-associated fractions exhibited a large number of PGP traits compared to isolates from arid non-cultivated root-free soil (B fraction) (Table 5). Nevertheless, some abilities like nutrient supply (phosphate solubilisation, siderophore release), are more frequent in soil bacteria, while auxin synthesis, directly affecting plant hormone homeostasis, was primarily presented by endophytes (Table 5). PGP traits distribution among the different bacterial genera revealed that the Bacillus and Klebsiella showed a predominant role, even though other genera less frequently isolated, like Pseudomonas, Raoultella and Paenibacillus, exhibited a higher number of PGP potential activities (Table 6 and Table S2).

Rhizobacteria were evaluated for the capability of promoting plant growth under water stress. A cluster analysis performed by combining the rhizobacteria PGP phenotypic traits (Fig.4) grouped the strains in three major clusters. Cluster I is the largest and summed Bacillus spp., Klebsiella spp. and Pseudomonas spp. The great majority of bacteria exhibiting ACCd activity were in this cluster that, moreover, included the strains with the highest number of potential PGP abilities. Clusters II and III displayed only one strain, respectively an ACCd-producing Achromobacter xylosoxidans and an Acinetobacter calcoaceticus. Both isolates exhibited just one PGP trait (Fig. 4). Consistent with ACCd activity in lowering plant ethylene under abiotic stress conditions, ACCd-producing rhizobacteria from the three clusters were selected to be further assayed in their ability to sustain plant growth in vivo under drought. These isolates were affiliated to genera Citrobacter (R16ACCd), Klebsiella (R01ACCd, R05ACCd, R08ACCd and R15ACCd), Achromobacter (R10ACCd) and Acinetobacter (R04ACCd), with Klebsiella spp. as the most frequent, as showed in the phylogenetic tree (Fig. 4 and S3).

The distribution of the bacterial genera reflects adaptation to the different microhabitats. The Bacillus genus was isolated in all the pepper fractions, with higher prevalence in the endosphere. Garbeva et al. [30] showed that the majority of Gram-positive bacteria in soils under different types of management regimes (permanent grassland, grassland turned into arable land and arable land), were putative Bacillus species. Bacillus spp. are also commonly found in arid land as a consequence of their ability to form endospores that allow bacterial survival for extended time periods under adverse environmental conditions [31]. Bacillus and related genera have been already reported to be associated to and promote the growth of a wide range of plants [32].

In all the soil fractions strains belonging to Gammaproteobacteria were predominant with many of the isolates assigned to the Enterobacteriaceae family. It comprises many species with enteric habitat, which origin could be attributable to the low hygienic quality of the irrigation water. The decline in the availability of pristine freshwater for irrigation due to allocation to urban and/or industrial supply, often results, especially in arid and semi-arid regions, in the intensive use of low-quality water to satisfy the increasing demand for irrigation. Representative species of Enterobacteriaceae genera, especially Klebsiella, Enterobacter, Citrobacter, have been isolated from different plant species grown in arid lands [44], [45], [46], [47]. In non-cultivated soil not subjected to irrigation and soil amendment, Enterobacteriaceae decreased in favour of Actinobacteria, with the prevailing genera Cellulosomicrobium and Rhodococcus. Together with Bacillus spp., Actinobacteria can survive as spores under adverse environmental conditions, hence making them typical desert taxa [4], [48].

The plasmid pHM2-gfp [78] was used to label R1-ACCd strain, affiliated to Klebsiella spp. Overnight culture of R1-ACCd was re-inoculated in fresh KB medium and the growth was monitored spectrofotometrically. When the culture reached 0.3 OD, 1 ml aliquot of cells were centrifuged (4000 rpm, 4C) and washed twice with MilliQ water prior to be resuspended in 50 l of MilliQ water and 10% glycerol. 30 l of cells were used to be transformed by electroporation (Eppendorf 2510) with 50 ng of pHM2-gfp plasmid. Successful transformation was checked by growth on a selective medium (KB+50 g/ml of kanamicin). To evaluate R1-gfp colonization ability, three-days Arabidopsis thaliana seedlings or seven-days Capsicum annuum L. seedlings were exposed to 108 cells/mL. Seedlings dipped in sterilized water were used as negative control. After 15h, plants were rapidly washed to remove weakly bound bacteria and observed under a confocal laser scanning microscope (Leica TCSNT). Images were acquired using Leica Confocal Software, using BP530/30 GFP filter (exitation at 488 nm) and LP590 TRITC filter (excitation length at 568 nm). For pepper rhizocompetence analysis, images were acquired also using the TRICT filter to observe root architecture by exploiting root autofluorescence in this channel. The acquired images were analyzed by using the MBF ImageJ software.

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