Among the arid zones of the globe, which occupy a third of the Earth’s surface (Neilson et al., 2017), the Gulf Cooperation Council (GCC) region, known for its large sandy deserts (Alsharif et al., 2020), has experienced the most intense climate changes over the last two decades, inducing profound disruptions that seriously threaten the sustainability of existing agrosystems (Fernández-López et al., 2022).

Within this area, the cultivation of date palm (Phoenix dactylifera L.), or phœniciculture, is the flagship activity, the symbol of life, and the cornerstone of oasis agrosystems. It is considered as a “holy tree” due to its vital nutritional (fruits and by-products) and socio-economic importance (Almadini et al., 2021; Naqvi et al., 2021). In addition to its agronomic and economic importance, date palm is known to tolerate harsh environmental conditions such as extreme temperature, drought, and high salinity of soil (Abumaali et al., 2023b). Since the Middle East has sandy soils and a dry climate, this tree contributes efficiently to mitigating desertification and erosion and preserving the oasis microclimate (Jain et al., 2011). Nevertheless, and despite this robustness, date palm encounters diverse constraints that, if no intelligent strategies are urgently implemented, would progressively compromise its sustainability and, in the long term, its extinction from this geographical area (El-juhany, 2014; Almadini et al., 2021). Among these structural and climatic constraints are: low organic soil matter content (Darwish and Fadel, 2017), limited and reduced groundwater levels (Sherif et al., 2023), growing salinity (Al Kharusi et al., 2019), resurgence and spread of pests and diseases (Alotaibi et al., 2023), and a very limited survival rate of newly planted plantlets due to their low potential to adapt to the harsh conditions of the environment (Saadaoui et al., 2019). Indeed, date palms are adapted to arid and semi-arid regions. They withstand moderately alkaline soils, with a pH ranging from 7 to 8.5, but extremely high alkalinity can be detrimental to their growth (Alotaibi et al., 2023; Sanka Loganathachetti and Mundra, 2023). They are adapted to soils with low organic matter levels, ranging from 0.1 to 1 (Mlih et al., 2016, 2019), while proper fertilization is essential to ensure their optimal growth. Furthermore, date palms exhibit a notable tolerance to salinity levels, commonly ranging from 4 to 8 dS/m or even higher under specific conditions (Muller et al., 2017; Alotaibi et al., 2023). Nevertheless, the irrigation of date palm with saline groundwater, due to water scarcity, is a common practice in the MENA regions, which threatens the sustainability of date palm cultivation (Shamim et al., 2022; Sanka Loganathachetti and Mundra, 2023).

To overcome these constraints, several useful solutions have been developed (Cai and Liu, 2015), among them, biotechnological approaches involve innovative breeding programs (Hazzouri et al., 2020). However, the efficiency of these conventional approaches in combating various stresses in plants was limited on one hand, and the non-conventional approaches, such as tissue in vitro technology, require more labor and may produce less resilient plants, particularly in woody trees (Al-Khateeb et al., 2020). Moreover, the excess of chemical fertilizer amendments and agricultural practices (e.g., tillage) has dramatically affected the diversity of the beneficial soil microbiota. This situation is worsened by intense climate changes, which impart severe impacts on plant–soil–microorganism interactions by altering the structure, abundance, composition, and functional activity of the rhizosphere microbiome (Sabir et al., 2021). Indeed, plants’ endosphere, rhizosphere, leaves, and other tissues are home to a multitude of microorganisms, known as the microbiome (Bonatelli et al., 2021). The rhizosphere microbiome interacts with and affects, often positively, the adaptation of its host plants to their environment (Bais et al., 2006; Kumar and Dubey, 2020). Indeed, the influence of plant roots on microbes is governed by the root exudates (Williams and de Vries, 2020), which include low-molecular-weight primary metabolites, like organic acids, amino acids, and sugars, and secondary metabolites, such as phenols, flavonoids, and terpenoids (De Vries et al., 2019). A plant’s exudate may be affected by climate change as a result of alterations in the plant’s photosynthetic apparatus, which will indirectly affect the root microbes by changing the carbon sources available to them and leading to their cell lysis (Chen et al., 2022). In their study, Naylor et al. (2017) compared the root rhizosphere of 18 species of monocot plants under drought stress and found that Actinobacteria are more abundant during a water deficit. Rice root-associated microbiota were also found to be enriched in Actinobacteria and Chloroflexi under drought stress, while several Acidobacteria and Deltaproteobacteria were depleted (Andreo-Jimenez et al., 2019).

Several ecosystem processes are directly or indirectly influenced by soil microorganisms, which play a vital role in enhancing ecosystem resilience and complexity (Robinson et al., 2023). These microorganisms are known to have beneficial attributes promoting nutrient cycling (e.g., solubilizing or decomposing soil’s below-ground complexed phosphorus, Ben Zineb et al., 2019b), plant health (e.g., systemic tolerance can be induced by plant growth-promoting microorganisms through biochemical mechanisms) (De Zelicourt et al., 2013), and climate regulation (e.g., CO₂, CH₄, and N₂O producing or consuming). Therefore, their use in the restoration, conservation, and maintenance of the date palm ecology and production is becoming more challenging. There is an urgent need for more integrated research to improve simultaneously the productivity of the low-cost date palm system and its sustainability and to develop technologies favoring/restoring its microbial diversity.

Microbes play crucial roles in the rhizosphere of date palm, contributing to its overall health and nutrient availability. Indeed, several investigations have uncovered a wide spectrum of interactions between plant growth-promoting (PGP) microbes and date palm, including the promotion of shoot and root growth (Cherif et al., 2015), inducing systemic tolerance against abiotic stresses (Harkousse et al., 2021), as well as the inhibition of some pathogenic fungi (Siala et al., 2016). In light of this, date palm sustainability can be met through the intelligent use of native plant microbiomes, which boost plant potential to adapt and survive under intense abiotic stresses (Koziol et al., 2018; Qiu et al., 2019; Alsharif et al., 2020). Among these, desert indigenous microorganisms are increasingly recognized as a long-term environmental and ecological potential solution to sustain agriculture in the oasis ecosystem (Almutawa, 2022). Their application benefits have been documented to: (i) promote date palm growth and survival rate of seedlings in the nursery (Shabbir et al., 2011); (ii) improve nutrient uptake by maintaining metabolic processes (Van Oosten et al., 2017; Alsharif et al., 2020); (iii) improve resistance to harmful pathogens (Mefteh et al., 2018); and (iv) induce better tolerance to complex abiotic stresses, drought, and salinity at a priority level (Benhiba et al., 2015; Akensous et al., 2022b). Consequently, focusing on beneficial microorganisms from arid and desertic lands would represent potential and innovating biotechnological tools to restore and promote agricultural activity in desertic areas in general and of date palm in oases in particular (Symanczik et al., 2014; Ferjani et al., 2015).

Alotaibi et al. (2023) reported on date palm biotechnology, including overviews of soil and environmental conditions of date palm cultivation, and Jain et al. (2011) reported on research progress and applications in this domain. Nevertheless, no holistic and comprehensive review has yet been conducted on the arid land’s microbiome, including prokaryotic and fungal communities, and its contribution to phœniciculture sustainability. Therefore, a deep study of the diversity and role of the date palm microbiome, including bacteria, fungi, archaea, viruses, and other microbes, is particularly relevant. Decades of research have demonstrated the importance of gathering information from the genetic repertoires of microbial communities from various hosts (Lucaciu et al., 2019). The recent advent of high-throughput sequencing technologies coupled with a variety of “omics” techniques has marked the beginning of a new green era in agriculture (Pantigoso et al., 2023). Modern sequencing techniques, such as next-generation sequencing, 16S rRNA gene sequencing, internal transcribed spacer sequencing, or the combination of these methods, provide in-depth information about plant microbial partners. They were able to better characterize the structure and function of these communities (Mitter et al., 2019; Satam et al., 2023). Still, the cultivation of those microbial partners is needed. Indeed, engineering date palm cultivable microbes might involve two approaches, either by re-introducing in situ enriched indigenous beneficial microorganisms or by inoculating them with exogenous beneficial microorganisms. In situ direct inoculation of microbes with PGP activities is the most commonly used strategy to enhance date palm growth (Yaish et al., 2015; Hazzouri et al., 2020). Although inoculating date palm with exogenous microorganisms may not directly promote their growth, they could still benefit by recruiting other microbial species able to enhance their resilience against abiotic stress (Alsharif et al., 2020).

Along with the incessant search for sustainable processes to produce dates in hyper-arid ecosystems, like the GCC area, there is a need to collect updated information, encouraging researchers to engage in new eco-friendly, insightful studies. Therefore, this review critically reports knowledge and pertinent scientific achievements on desert plant-associated microorganisms and their applications on date palms. We also targeted the knowledge available, the gaps, and what would be recommended for the desert plant microbes’ inoculation approaches to sustain the GCC phœniciculture, with a particular emphasis on Qatar.

Decades of empirical and theoretical research have revealed that plants are not standalone entities. They are influenced by their association with microbiota, named “holobiont” (Vandenkoornhuyse et al., 2015; Wagg et al., 2022). The holobiont of desert plants is the center of interest regarding its performance under severe environmental constraints (Araya et al., 2020). Nowadays, several projects have reported promising results for the improvement of agricultural production systems sustainability, owing to inoculation with microbial rhizospheres deriving from plants surviving in arid and desertic areas (Köberl et al., 2011, 2013; Eida et al., 2018; Ha et al., 2021; Procter et al., 2022).

This high-performance potential was reported for the holobiont of the desert plant cassava (Manihot esculenta Crantz) (Ha et al., 2021). The African desert grass Stipagrostis pungens, grown under severe drought conditions, revealed harboring beneficial bacteria that produce extracellular polymeric substances (e.g., exopolysaccharide), which form a hydrophilic biofilm around plant roots (Rolli et al., 2015). Thus, protecting the roots from desiccation as well as amending the soil structure and its aggregation properties result in increased soil water holding capacity and improve the overall resilience of the holobiont (Huang et al., 2022; Marasco et al., 2022). For the Atacama’s desert plants, Cistanthe longiscapa and Citrullus colocynthis, it has been reported that their survival strategy was forged through intimate interactions with associated soil bacteria and fungi (Araya et al., 2020; Procter et al., 2022). Citrullus colocynthis was reported to develop symbiotic interactions with plant growth-promoting bacteria such as Acidobacteria, Bacterioidetes, and Actinobacteria for nitrogen, sulfur, and carbon cycles, as well as for the solubilization of phosphate and the synthesis of indole-2-acetic acid and siderophores (Procter et al., 2022). The four native Saudi Arabian desert plants, Zygophyllum simplex, Panicum turgidum, Euphorbia granulate, and Tribulus terrestris, harbor bacterial strains that exhibit distinct biochemical pathways regarding nutrient uptake and survival under stress conditions (Eida et al., 2018). Recently, Abumaali et al. (2023a,b) stated that Qatari wild date palm (Phoenix sylvestris) displayed specific and unique bacterial operational taxonomic units (OTUs) that could improve date palm tolerance to salinity and drought. Indeed, the rhizospheric core microbiome from arid regions may improve the ability of date palm to withstand harsh environmental conditions by promoting microbe-induced systemic tolerance. To cope with abiotic stress and low organic carbon, microbes engage a multitude of direct and indirect mechanisms to support plants (Figure 1; Mohanty et al., 2021). Direct mechanisms involve the increase of vital nutrient acquisition (e.g., N, P, and Fe) (Anli et al., 2020), the accumulation of osmolytes that impart drought tolerance in plants (e.g., soluble sugars, proline, glycine, organic acids, Huang et al., 2014), the production of exopolysaccharide (Rolli et al., 2015), the regulation of phytohormone levels including auxin, gibberellin, and cytokinin, and particularly the 1-aminocyclopropane-1-carboxylate (ACC) deaminase to reduce the ethylene level in roots (Lau et al., 2022), and the induction of stress-responsive genes (e.g., NCED, P5CS) (Poudel et al., 2021). Indirect mechanisms encompass actions where microbes enhance plants’ resilience by improving soil characteristics (Ait-El-Mokhtar et al., 2020), maximizing the total area of the root, resulting in improved nutrient and water absorption (Ngumbi and Kloepper, 2016), or suppressing pathogens that may exacerbate stress conditions (Poudel et al., 2021). Through these intricate interactions, microbes play a key role in bolstering plant resilience and enabling them to thrive in challenging environments.

Next, to the advantageous ecological and protective services offered by desert plant-associated microorganisms (Köberl et al., 2016; Shilev et al., 2019; Karray et al., 2020; Gargouri et al., 2021b), few microbial profiling studies have been carried out on the rhizospheres and root systems of date palm, the iconic oasis keystone (Chebaane et al., 2020; Gagou et al., 2023; Abumaali et al., 2023a). Moreover, although high-throughput sequencing technology provides excellent opportunities for the investigation of microbiomes, studies on date palm microbiomes remain scarce.

In accordance with the available data, date palm rhizosphere soil and root systems shelter a reservoir of beneficial symbiotic microorganisms that positively regulate its homeostasis (Ferjani et al., 2015). Mosqueira et al. (2019) carried out a broad survey of bacterial diversity associated with date palm grown across the Sahara desert in Tunisia. They identified two major endophytic bacterial phyla, Gammaproteobacteria and Alphaproteobacteria, known to perform ecological functions of biopromotion and biofertilization in harsh environments. Shamim et al. (2022) demonstrated that Micromonospora and Mycobacterium bacterial taxa were effective in alleviating salinity stress when date palms were irrigated with saline water. Cherif et al. (2015) further showed that Gammaproteobacteria, a class of endophytic bacteria isolated from date palm, was also effective in improving plant drought tolerance. Using pyrosequencing, Yaish et al. (2016) revealed that the composition of endophytic bacterial and fungal communities in P. dactylifera differs according to the concentration of salt in the irrigation water.

Up-to-date, there are few reports addressing date palm microbial profiling (Ferjani et al., 2015; Yaish et al., 2016; Mosqueira et al., 2019; Chebaane et al., 2020; Al-busaidi et al., 2022; Shamim et al., 2022). Few of them go deeper beyond the species identification level. Consequently, advanced technologies, such as high-throughput sequencing, have become highly recommended to be able to characterize in depth the rhizosphere and endophytic microbiota of P. dactylifera, which would further contribute to dissecting more beneficial microbial taxa and better understanding their role in enhancing date palm stress mitigation.

The rhizosphere and endosphere of arid land habitats offer a valuable reservoir of biomolecules with fertilizing and biocontrol properties against a large spectrum of biotic and abiotic constraints (Alsharif et al., 2020). They feature a wide diversity of plant growth-promoting (PGP) microbial communities involved in vital processes, exchanging services for niches and nutrients, ultimately resulting in a win–win and high-performance partnership with the plant partner (Vacheron et al., 2013; Soussi et al., 2016). Consequently, they are regarded as potential and pertinent candidates to substitute conventional fertilizers and pesticides. This would promote food security and the sustainability of food production systems (Gargouri et al., 2021b; Ben Zineb et al., 2022).

The recent overview by Alsharif et al. (2020) on the diversity of desert plant rhizosphere microbiomes, including the latest findings and applications, reported that desert PGP microorganisms are genetically better equipped to adapt to harsh environments than those evolving in non-arid soils. Furthermore, many research teams were focusing on studying arid land-associated microbial communities to explore their beneficial agronomical contributions following their inoculation with cash crops, such as wheat (Singh and Jha, 2016), cowpea (Minaxi et al., 2012), Salicornia (Marasco et al., 2016), and date palm (Anli et al., 2020; Chebaane et al., 2020). Among the available data, a consensus emerges on the advantageous contribution provided by the inoculation of PGP bacteria on date palm to better adapt to abiotic stresses (Figure 1; Table 1).

Cultivated date palm microorganisms’ inoculum has been used to boost date palm resistance to abiotic and biotic stresses and would represent potential substitutes for conventional pest control products (Meddich et al., 2018; Omomowo et al., 2023). Nevertheless, they remain facing efficiency, technical, and sustainability challenges (Qiu et al., 2019). To reach an acceptable efficiency level on date palm, these beneficial microbes must overcome key steps: establishment, survival, colonization, and interaction with the host tree.

AB: Conceptualization, Data curation, Writing – original draft, Writing – review & editing. ML: Writing – review & editing. AK: Writing – review & editing. HH: Writing – review & editing. TA: Writing – review & editing. HA-J: Writing – review & editing. MA: Writing – review & editing. AM: Writing – review & editing. SS: Funding acquisition, Writing – review & editing. MG: Writing – original draft, Writing – review & editing.