Genetic diversity, symbiotic efficiency, stress tolerance, and plant growth promotion traits of rhizobia nodulating Vachellia tortilis subsp. raddiana growing in dryland soils in southern Morocco

Plants living in deserts or hot arid environments are subjected to several abiotic constraints, such as water scarcity, extreme temperatures, and high levels of irradiance stresses (Lambers et al., 2008). Under these conditions, low soil–water uptake is the principal adaptation trait that enables plants to develop effectively under restricted soil–water availability Aref et al., 2003. Acacia is one of the well-adapted tree species to arid environments and a keystone species across arid environments in Africa. It is recognized as the most widespread, drought-resistant, and heat-tolerant species in the arid and semi-arid regions of Africa and the Middle East Fagg and Stewart, 1994, Noumi and Chaieb, 2012.

The genus Vachellia (formerly Acacia) contains several species described as multipurpose trees and shrubs (Ross, 1981). They have long been used for gum, wood, fodder production, and as a source of fuelwood and other materials Grouzis, 2003. They are known for their capacity to improve soil nutrient availability Hagos and Smit, 2005, soil fertility restoration, and agroforestry production (Bohra, 2012). Vachellia appears also as a suitable pioneer plant to be used in rehabilitation, restoration, and revegetation programs of eroded or degraded areas Grouzis, 2003. This is due to its wide geographical distribution and nitrogen fixation abilities Abdedaiem et al., 2020 as well as its capacity to improve soil fertility. Moreover, its potential to decrease evapo-transpiration affects the establishment, growth, and survival of other plants Noumi and Chaieb, 2012, Abdallah et al., 2008, Labidi et al., 2007.

The genus Vachellia has a large pantropical distribution covering a variety of geographic areas, with 73 species in Africa, 60 species in the Americas, 36 species in South Asia, and 9 species in the tropical North of Australia Labidi et al., 2007, Orchard and Maslin, 2003. However, V. tortilis remains a specific species in the arid and Saharan regions Grouzis, 2003. In Morocco, three species of Vachellia grow spontaneously: Vachellia tortilis subsp. raddiana (V. t. subsp. raddiana), V. gummifera, and V. ehrenbergiana (Mhirit and Blerot, 1999). V. tortilis, which was renamed by Kyalangalilwa et al. (Mhirit and Blerot, 1999), is the symbol of the desert in North Africa and the most widespread tree in the Moroccan Sahara (Kyalangalilwa et al., 2013).

Vachellia trees nodulate and fix atmospheric nitrogen through a symbiotic association with different genera of bacteria of both Alpha- and Beta-rhizobia (Beukes et al., 2019). The species V. t. subsp. raddiana can be nodulated by species of Ensifer (Ba et al., 2002, Degefu et al., 2012, Khbaya et al., 1998, Lortet et al., 1996, Romdhane et al., 2006, Sakrouhi et al., 2016); Mesorhizobium (Ba et al., 2002, Degefu et al., 2012, Odee et al., 2002); Rhizobium (Ba et al., 2002). The other species of Vachellia growing in Africa are also nodulated by strains belonging to Ensifer (Degefu et al., 2012, Khbaya et al., 1998, Boukhatem et al., 2012, De Lajudie et al., 1998, Diouf et al., 2015, Haukka et al., 1998, Leary et al., 2006, Nick et al., 1999), in addition to some strains of Mesorhizobium (Odee et al., 2002, De Lajudie et al., 1998); Rhizobium (Nick et al., 1999, McInroy et al., 1999), and Bradyrhizobium (Odee et al., 2002, McInroy et al., 1999, Dupuy et al., 1994). Most of these studies have used 16S rRNA gene sequencing for strains identification. However, this housekeeping genetic marker presents some limitations to distinguish among closely related species due to a high level of sequence conservation (Rajendran et al., 2012). Hence, core genes sequencing, including recA, gyrB, dnaK, and rpoB are used to complement 16S rRNA sequence-based genetic identification (Martens et al., 2008, Martens et al., 2007) and Multilocus Sequence Analysis (MLSA) is performed to infer highly resolved rhizobial species phylogenies. It should be noted that recently Kuzmanovic et al. (2022) while using whole genome-based phylogenetic analyses proposed a framework for genus delimitation based on monophyletic groups in a core-genome gene phylogeny separated by pairwise core-proteome average amino acid identity (cpAAI) thresholds. The whole genome-based phylogenetic analysis proposes to restrict the genus Ensifer to E. adhaerens, E. sesbaniae, and E. morelensis, while all other species are regarded as Sinorhizobium. This highlights the importance of incorporating core-genome-based phylogenetic analyses in bacterial taxonomy to better understand the relationships between closely related species and to accurately define genus and species boundaries (Martens et al., 2008).

Rhizobial identification can also be done at the symbiovar level by analyzing core and symbiotic genes. Symbiovars are defined based on nodA symbiotic gene (Nandasena et al., 2007), the nitrogen fixing gene nifH (Rincón-Rosales et al., 2013), and mainly nodC phylogenies (Velázquez et al., 2016). Authors have also defined the symbiovar as a group of strains within a rhizobial species that can set up a symbiotic relationship with a particular leguminous plant by taking into account the nodulation specificity in legume species (Rincón-Rosales et al., 2013).

Several reports on the genetic diversity of Vachellia symbiontes in its areas of distribution in Africa have been published. They concern mostly Morocco (Ba et al., 2002, Khbaya et al., 1998); Algeria (Noureddine et al., 2010), Tunisia (Romdhane et al., 2006, Ben Romdhane et al., 2005), Mauritania and Senegal (Ba et al., 2002), and Kenya (Odee et al., 2002). Moreover, a recent study based on symbiotic nod genes phylogenetic analysis and plant inoculation tests showed that Ensifer strains nodulating V. gummifera in some semi-arid areas of Morocco clustered in a particular symbiovar named “vachelliae” (Bouhnik et al., 2019). However, to the best of our knowledge there is no earlier studies that have explored the Plant Growth Promoting (PGP) characteristics of the Vachellia rhizobia in Africa. Hence, the aim of the present study was to perform genetic and symbiotic characterization of the rhizobia nodulating local V. t. subsp. raddiana trees grown in an arid area of Morocco. The genetic diversity of the isolates was assessed using DNA fingerprinting (Rep-PCR) analysis and phylogenies of core genes (16S rRNA, recA, gyrB, dnaK, and rpoB), symbiotic genes (nodC, nodA), and the nitrogen fixing gene nifH. In addition, Multilocus Sequence Analyses (MLSA) was used to precise the taxonomic position of the isolated rhizobia. The PGP potential and stress tolerance of representative strains were studied in vitro, and their nodulation capacity and their symbiotic efficiency with V. t. subsp. raddiana were evaluated under greenhouse conditions.

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