The Potential of Biocrust-Forming Cyanobacteria to Enhance Seedling Growth of Native Semi-arid Plants Through Seed Biopriming

Vol.:(0123456789) Journal of Plant Growth Regulation https://doi.org/10.1007/s00344-024-11521-6 The Potential ofBiocrust‑Forming Cyanobacteria toEnhance Seedling Growth ofNative Semi‑arid Plants Through Seed Biopriming AitorAlameda‑Martín1,2 · SoniaChamizo3,1 · EmilioRodríguez‑Caballero1,2,6 · MiriamMuñoz‑Rojas4,5 · YolandaCantón1,2,6 Received: 21 December 2023 / Accepted: 4 October 2024 © The Author(s) 2024 Abstract In drylands, extreme environmental conditions pose a challenge for restoration, especially on a large scale. Direct seeding is the most cost-effective approach to restore large areas, but it requires improvements to enhance seedling survival and establishment. For this purpose, biopriming seeds with cyanobacteria is promising due to their plant growth-promoting properties. We evaluated the effect of seed biopriming with native biocrust-forming cyanobacteria on seed germination and radicle length of four native plant species, two perennials (Macrochloa tenacissima and Thymus hyemalis) and two annuals (Plantago ovata and Stipa capensis), chosen for their ubiquity in Mediterranean drylands. Treatments included seed biopriming with cyanobacteria inoculants (biomass + exudate), seed priming only with the cyanobacterial exudate, and controls (BG11 culture medium and distilled water). Biopriming effect was assessed individually for four native biocrust-forming cyanobacteria species: Nostoc commune, Tolypothrix distorta, Trichocoleus desertorum, and Leptolyngbya frigida. Seed biopriming showed no effect on germination with similar rates among treatments (on average, 45 ± 12.6% for M. tenacissima, 38.8 ± 12.4% for T. hyemalis, 91.7 ± 9.8% for P. ovata and 77.6 ± 10.8% for S. capensis). However, biopriming significantly affected radicle length of annual plants. Radicles were significantly increased in P. ovata when treated with cyanobacterial exudates (15–30% increase over control), and in S. capensis when treated with cyanobacterial biomass + exudate (26–42% increase over control). These results indicate that the effect of seed biopriming is species specific, but selecting the appropriate plant species and biopriming treatment can enhance plant survival and establishment in drylands, making restoration efforts more successful. Keywords Cyanobacteria exudate· Cyanobacteria biomass· Annual plants· Germination· Radicle length· Restoration Introduction Drylands, representing almost half of the Earth’s land surface and sustaining one-third of the global population, are among the most susceptible ecosystems to land degradation (Prăvălie 2016). Estimates point to 10–20% of global drylands being already degraded and around 12 million hectares being newly degraded every year due to climate change and land use intensification (Burrell etal. 2020). In this context, restoration activities aimed at preserving and restoring ecosystem services and societal goods provided by drylands are critical to the well-being of society (Yirdaw etal. 2017; Maestre etal. 2021). However, ecosystem restoration is particularly challenging for drylands, where low and unpredictable precipitation, extreme temperatures, low soil fertility, and seed quality hinder restoration efforts (Hoover etal. 2020). In fact, passive restoration of degraded drylands is Handling Editor: Abdul Latif Khan. * Sonia Chamizo [email protected] 1 Department ofAgronomy, University ofAlmería, Ctra. Sacramento SN, 04120Almería, Spain 2 Research Centre forScientific Collections fromtheUniversity ofAlmeria (CECOUAL), Ctra. Sacramento SN, 04120Almería, Spain 3 Estación Experimental de Zonas Àridas (EEZA-CSIC), Ctra. Sacramento SN, 04120Almería, Spain 4 Department ofVegetal Biology andEcology, University ofSevilla, Av. Reina Mercedes, 6, 41012Seville, Spain 5 Centre forEcosystem Science, School ofBiological, Earth andEnvironmental Sciences, UNSW, Sydney, NSW2052, Australia 6 ECO-ARID, UAL, Unidad Asociada al CSIC por la EEZA, 04120Almeria, Spain Journal of Plant Growth Regulation slow and, in many cases, hardly achievable depending on the scale and severity of degradation. On the other hand, active restoration practices often fail because of the mentioned environmental stresses (Shackelford etal. 2021), being the permanent or seasonal water scarcity one of the main factors limiting restoration success (Duncan etal. 2019). This problem will be exacerbated in the next decades given the predicted increase in aridity and drought frequency and magnitude (Mirzabaev etal. 2022), requiring the development of more efficient restoration techniques that also cope with future climatic scenarios (Zvinavashe etal. 2021). Besides, to achieve the global ecological restoration objectives, economically and logistically viable strategies should be developed to face large-scale restoration projects as well as to act on hard-to-reach areas. In this context, seeding arises as an easier and spatially manageable strategy, considered as the most cost-effective strategy for most species (Pérez etal. 2019; Shackelford etal. 2021), regardless of high seed mortality rates in drylands (James etal. 2011). The transition between germination and seedling emergence is the main bottleneck for native plant recruitment in drylands, where typically only 5–10% of seeds reach the establishment phase (Kildisheva etal. 2016). Usually, seedling mortality is extremely high during summer drought (James etal. 2011) and seedlings that overcome the critical phase of establishment increase considerably their survival probability (Chambers 2000). Seed and seedling stage are critical to enhance ecological restoration success in drylands (Brown etal. 2021) and to face the high demand of native seed within the U.N. Therefore, improvements are needed at the Decade of Ecosystem Restoration aiming to restore 350 million hectares at global scale. To advance on this line, seed enhancement technologies have emerged in the last decades. These techniques are based on physical manipulation, such as mechanical abrasion, cold and warm stratification, dry or moist heat, and dry post-ripening, or on the application of phytohormones (Kildisheva etal. 2020) and other materials to the seed to favor germination and seedling growth (Madsen etal. 2016). In particular, methods to harden and stimulate seeds in which biological components like bacteria, fungi, algae, or cyanobacteria act as boosters are recently attracting special attention (Chakraborti etal. 2022). These are commonly known as biopriming techniques. Biopriming has been used since the 1990s (Callan etal. 1990), with most studies focused on crop plants (e.g., wheat, rice, and corn) (Singh etal. 2023; Srivastava etal. 2023), especially to prevent fungal infections (Singh etal. 2020) and to combat abiotic stresses, such as salinity (Biswas etal. 2023). In contrast, research efforts on the effect of biopriming on wild plants have been marginal, mainly because the investment return does not occur in the short term. This situation is currently changing due to the benefits that biopriming can have on the germination and establishment of plants in natural ecosystems (Zulueta-Rodríguez etal. 2015; Chitra and Jijeesh 2021). This technique can be especially relevant in drylands, where biopriming using bacteria and fungi with PGP (plant growth-promoting organisms) properties can increase seed resistance to environmental stress and preadapt plants to upcoming changes in temperature and precipitation regimes due to ongoing climate change (Fazeli-Nasab etal. 2021). Among the different organisms that can be used for biopriming, cyanobacteria are emerging as one of the most interesting candidates. These organisms have been successfully used as bio-inoculants to promote seed germination and plant growth in agriculture (Essa etal. 2015; Moorthy and Delfe 2019) because of their ability to synthesize a great number of substances that act as biofertilizers and antipathogenic agents (Hashtroudi etal. 2013). These substances include growth-promoting regulators, such as cytokinins, gibberellins, or auxins (Machado‐de‐Lima etal. 2023), as well as vitamins, amino acids, polypeptides, biotin, metabolites that act as allelochemical agents, proteins, antibacterial and antifungal substances, and polymers, especially exopolysaccharides that improve exoenzyme activity (Kumar etal. 2019). Most results have been reported for cyanobacteria isolated from aquatic systems, used individually or as a consortium, and applied on agricultural plants (Prabha etal. 2019; El-Habet and Elsadany 2020), finding that the effects were greatly variable among different cyanobacterial species (Yadav etal. 2022). Since biopriming effects strongly vary depending on the cyanobacteria species used as inoculant, as well as the plant species, it is essential to consider both when evaluating the effectiveness of this technique on the performance of either agricultural or wild plants for which very few data exist (Muñoz-Rojas etal. 2018; Chua etal. 2020; Machado‐de‐Lima etal. 2023). In drylands, biopriming with cyanobacteria to promote seed germination can be especially advantageous as these organisms are ubiquitous components of soil communities that colonize the soil surface of open areas between plants, also known as biological soil crusts or biocrusts (Weber etal. 2022). Biocrust-forming cyanobacteria play a primary role as pioneer colonizers of barren soils and drivers of biocrust succession (Chilton etal. 2018) thanks to their ability to stabilize the soil surface and fix the atmospheric carbon and nitrogen, contributing to soil fertility (Xiao etal. 2022). Moreover, they exert multiple effects on plants, such as enhancing seed germination and plant growth, providing tolerance to abiotic (salinity, drought, and extreme temperatures) and biotic (pathogens that are destroyed by the defense enzymes released by cyanobacteria) stress (Kollmen and Strieth 2022). As a result, cyanobacteria species have been isolated from biocrusts and used as inoculum to restore dryland degraded soils (Román etal. 2018, 2021; Roncero-Ramos etal. 2019b). However, biocrust-forming cyanobacteria have been hardly used for seed biopriming to Journal of Plant Growth Regulation promote germination as well as plant growth in restoration assays. To our knowledge, very few studies have evaluated the impact of biopriming with biocrust-forming cyanobacteria on the germination rate and seedling development of dryland plants and all of them assessed the effects of cyanobacterial consortia on seeds from a few Australian perennial plant species (Muñoz-Rojas etal. 2018; Chua etal. 2020; Machado‐de‐Lima etal. 2023), but no attempt with plants from other different continent has been conducted. Furthermore, the isolated effect of each of the cyanobacteria species forming the inoculum was not evaluated in these studies. This aspect is crucial to screen the most viable ones in terms of seed germination and plant growth promotion. Application of seed biopriming with biocrust cyanobacteria for dryland restoration requires first to evaluate the contribution of this strategy to native plant growth promotion, including a wide range of target plant species and different life forms (i.e., annuals and perennials) used in dryland restoration. Typically, assays have been conducted with perennial species (Muñoz-Rojas etal. 2018; Chua etal. 2020; Machado‐de‐Lima etal. 2023), but the use of annual plants is certainly relevant for three reasons: (i) grow rapidly, (ii) improve soil properties and prevent erosion during first stages of restoration, and (iii) are closely associated with cyanobacteria-dominated biocrusts in drylands ecosystems, potentially involving facilitation relationships (Boeken etal. 2004; Rodríguez‐Caballero etal. 2019). Furthermore, most previous studies on seed biopriming with cyanobacteria were conducted using commercial strains from aquatic environments (Prabha etal. 2019). Therefore, the viability of native soil biocrust-forming cyanobacteria as bio-inoculants for native plant recruitment for ecosystem restoration should be evaluated. Finally, it is interesting to explore whether germination and seedling of native plants is influenced by either the cyanobacterial culture or the cyanobacterial exudates since the latter would facilitate the production and manipulation of the bioprimer and, ultimately, biopriming application. To fill in these gaps, in this study, we examined the individual effect of seed biopriming with four native biocrustforming cyanobacteria species (including N fixing and non-N fixing) on germination and radicle elongation of four indigenous plants of Mediterranean drylands. Plant selection included two annual (Plantago ovata, Stipa capensis) and two perennial (Macrochloa tenacissima, Thymus hyemalis) plant species that exhibit potential for restoration due to the ecosystem services they provide such as increased fertility, stability and infiltration (Pueyo etal. 2013), increased biodiversity and forage, reduced fire risk (Cortina etal. 2009), and reduced erosion and attraction of pollinators (Barbir etal. 2016). Additionally, we also evaluated whether the effect of seed biopriming on germination and radicle elongation was attributed to the effect of the whole cyanobacterial culture (biomass together with the cyanobacterial exudates) or exclusively to the cyanobacterial exudates. We hypothesized that seed biopriming with cyanobacteria would have a positive effect on both germination and radicle length in the four plant species, and induced effects would be greater when seeds are bioprimed with N-fixing cyanobacteria compared to non-N-fixing cyanobacteria. Materials andMethods Vegetation Species Selection andSeed Sampling andPreparation We examined the effect of biopriming with biocrust-form- ing cyanobacteria on seeds from four plant species representative of Mediterranean drylands, having different life strategies and that usually coexist with biocrusts: (i) two annual plants, i.e., Plantago ovata Forssk. and Stipa capensis Thunb. and (ii) two perennials, i.e., Thymus hyemalis Lange and Macrochloa tenacissima (L.) Kunth (Table1). Seeds from annuals were collected in the field from wild populations in Huércal de Almería (near Almería city, 36°52′52.6″N 2°27′19.3″W) in April 2020, while seeds from perennials were obtained from the germplasm bank of CECOUAL (Scientific Collection Center of University of Almeria), which includes seeds from dryland ecosystems within the province of Almeria. Seeds were stored in darkness at room temperature for 4months. Before the biopriming experiment, we assessed seed viability by carrying out germination tests on a range of seeds with different morphologies and colors (representing different degrees of maturity) for each of the plant species. These tests were conducted in a culture chamber at 25°C with a photoperiod of 16h of light and 8h of darkness (hereafter 16/8) and lasted 15days for annual species and 30days for perennial ones. Based on these results, we chose suitable seeds using a stereomicroscope (Leica MZ 12, Wetzlar, Germany). The seed selection varied depending on the species. For S. capensis, seeds of dark brown color and with more hairiness were chosen. In P. ovata, selection was based on the presence of a whitish coating externally covering the seeds. In T. hyemalis, seeds with a spherical shape and black color were chosen, and finally, for M. tenacissima, seeds without any cracks or missing parts at the ends, and with a dark green color, were selected. No pre-treatment of the seeds was necessary to break dormancy, but seed disinfection was conducted. To sterilize the seeds, they were shaken for 1min in 50-mL Falcon tubes containing a 5% (w/v) sodium hypochlorite solution. After this exposure, they were washed twice with distilled water to remove the residual sodium hypochlorite. Journal of Plant Growth Regulation Cyanobacteria Species Selection andCulture We used indigenous cyanobacteria species isolated from biocrusts located in semi-arid ecosystems of southeastern Spain, specifically in Almeria province (Roncero-Ramos etal. 2019a). From our stock cultures, we chose two nonheterocystous cyanobacteria (Leptolyngbya frigida CAU10 UAM 837 and Trichocoleus desertorum CAU7 UAM832) and two heterocystous cyanobacteria (Nostoc commune CANT2 UAM 817 and Tolypothrix distorta CANT7 UAM 825). Selection of these species was based on their different functional traits (nitrogen fixation, filamentous growth form, stress tolerance, desiccation, and UV radiation resistance), their wide distribution in arid and semi-arid ecosystems in Almeria (Roncero-Ramos etal. 2019a), and their optimized cultivation in liquid media (Roncero-Ramos etal. 2022). Each cyanobacteria species was cultured individually in sterilized flasks using a BG11 culture medium and constant temperature and light conditions (Román etal. 2018; Roncero-Ramos etal. 2019b). We monitored the growth curve of each cyanobacterial culture until they reached steady-state conditions. At that point, the biomass of each species was concentrated or diluted to obtain a concentration of 2g L−1, required for the biopriming experiments. Seed Biopriming andGermination Monitoring Seeds were bioprimed separately with each of the selected cyanobacteria species according to the following treatments: (i) biopriming with cyanobacteria biomass and the culture medium, including cyanobacterial exudates and the growth medium (hereafter “biomass + exudate”); (ii) priming with the cyanobacteria exudates, which includes both the exudates released by cyanobacteria as well as the growth medium (hereafter “exudate”); (iii) seeds immersed in distilled water; and (iv) in the culture medium BG11 as controls treatments. For biomass + exudate priming, seeds were immersed in the different inocula already prepared consisting of isolated cultures of each cyanobacterium (biomass and the medium where they were grown) at a concentration of 2g L−1. For the exudate priming, the inoculum cultures were centrifuged for 10min at 9000rpm (Wongchawalit and Premsuriya 2015) and the supernatants containing the culture medium and the substances released by each cyanobacteria species were collected and used to immerse the seeds. A total of 4000 seeds were bioprimed, 1000 of each plant species. They were separated into groups of 100 seeds, corresponding to each treatment, in small beakers containing 20mL of the different solutions. The beakers were then shaken on an orbital shaker for 24h (Prabha etal. 2019) at 180rpm (to ensure adequate mixing) at room conditions. After shaking, each group of 100 seeds was subdivided into 4 subsets of 25 seeds. These seeds were placed on filter papers in 90mm Petri dishes (4 Petri dishes per treatment) which were incubated in a growth chamber with a photoperiod of 16/8 and a temperature of 25°C. Seeds were watered with 4mL of distilled water every day. Germination was monitored daily, for 15days in the case of annuals plants, and for 30days in the case of the perennials. We defined germination as the development of a conspicuous radicle protrusion measuring at least 2mm through the seed coat (Dessì etal. 2021). We measured four variables; (i) germination percentage, which is the number of germinated seeds with respect to the number of seeds used for each subset (25 seeds) multiplied by 100; (ii) germination time, which is the average number of days it has taken for the seeds of a subset to germinate; (iii) T50, which is the number of days required for the half of Table 1 List of the four native plant species from Mediterranean drylands used in this study, specifying the type of life form and the restoration interest Sp. (Family) Life form (photosynthetic pathway) Restoration interest Reference Thymus hyemalis (Lamiaceae) Perennial shrub (C3) Attraction of pollinators Soil fertility and stability Increased infiltration Nurse plant Barbir etal. (2016) Plantago ovata (Plantaginaceae) Annual grass (C3) Soil fertility and stability Increased infiltration Pueyo etal. (2013) Macrochloa tenacissima (Poaceae) Perennial grass (C3) Fire risk reduction Source of food for grazers Soil fertility and stability Increased infiltration Nurse plant Wildlife refuge Cortina etal. (2009) Stipa capensis (Poaceae) Annual grass (C3) Soil fertility and stability Increased infiltration Pueyo etal. (2013) Journal of Plant Growth Regulation the seeds in each subset to reach germination; and (iv) slope around the inflection point of the cumulative germination curves, which was calculated by solving the b term of a loglogistic function fitted by non-linear least squares regression for each replicate of each treatment, using the drm function included in drc package (Ritz etal. 2015). The following equation was used: where G: Fraction of germinated seeds at time t; d: Germinable fraction; e: Median germination time for the germinable fraction; and b: Slope around the inflection point. Radicle Length Measurement Seven days after germination, each seedling was placed over a black cardboard with a reference scale bar to increase contrast and then photographed. Individual radicles were digitized as individual objects using BeePen tool from QGIS 3.10.7 (QGIS Development Team 2019), and from these, the total length of each radicle [mm] was obtained. Before digitization, images were rescaled to real dimensions using the reference scale added in each picture. From germination and radicle length data, we also determined the Germination Index (GI), which considers biopriming effects on both germination and radicle elongation. It was calculated according to the following equation proposed by Zucconi etal. (1981): where GI: Germination index; Ge(%): Seed germination percentage in presence of extract (exudate or biomass + exudate); Gdw(%): Seed germination percentage in distilled water; REe: Mean of radicle length (mm) in presence of extract (exudate or biomass + exudate); and REdw: Mean of radicle length (mm) in distilled water. GI values equal to 1 indicate no effect of the treatment compared to the controls. Values lower than 1 indicate inhibition by the treatment, while values higher than 1 indicate promotion on germination and radicle length by the treatment. Cyanobacteria Cultures andExudate Characterization The content of exopolysaccharides was determined in both exudates and cyanobacterial cultures (biomass + exudate). To do this, 1mL of the solutions (exudates or biomass + exudates) was placed on glass vials and the phenol–sulfuric assay was applied (DuBois etal. 1956). The absorbance G (t)= d 1+exp { −b [ log(t)−log(e) ]} GI = (Ge(%)×REe) (Gdw(%) × REdw) was measured at 488nm with a UV–vis spectrophotometer Thermo Helios Gamma 9423 UVG 1002 E (Thermo Electron Corporation, Waltham, MA, USA) (DuBois etal. 1956), and the carbohydrate content was calculated according to a calibration curve built using glucose as standard (Chamizo etal. 2020). To detect and quantify phytohormones in the exudates andcultures (biomass + exudate) of each cyanobacterial species, samples were sent to CEBAS-CSIC (Center for Applied Soil Science and Biology of the Segura) to perform ultra-performance liquid chromatography-quadrupole\ time of flight mass spectrometry (UPLC-QToF-MS/MS). Specifically, the following pool composed of salicylic acid (SA), indole-3-acetic acid (AIA), indole-3-butyric acid (IBA), gibberellic acid (GA3), 6-benzylaminopurine (BAP), abscisic acid (ABA), and jasmonic acid (JA) was determined. Phytohormone concentration was quantified in the samples, each one replicated three times, after filtering through a 0.22-µm filter. 5 µL of the filtered sample extracts were injected into a high-resolution UPLC-QToF-MS/MS equipment (UPLC equipped with a Waters Acquity I-Class Plus (Waters Corporation, Milford, MA, USA) coupled to a QToF-MS maXis Impact Series (Bruker Daltonics, Billerica, MA, USA) with a resolution of ≥ 55 000 FWHM). The chromatographic conditions tested were based on Müller and Munné-Bosch (2011). Ionization by electrospray (ESI) was used as the source MS with positive polarity. Broadband collision induced dissociation (+ bbCID) was employed for the MS/MS analysis with collision energy applied of 24eV. Additional parameters included a voltage source of 4.5kV, drying temperature of 200°C, a nebulizer pressure of 2.0bar, a N2 flow rate of 9 L/min, and a mass range of 50–1200Da. Sodium formate (HCOONa) served as the reference standard. Data Analysis We analyzed the effect of our treatments (water, culture medium, biomass + exudate, and exudate of the different cyanobacterial species) on germination percentage, germination time, median germination time (hereafter T50), slope around the inflection point (b parameter in the equation), radicle length, secondary roots and GI for each plant species, using a nested ANOVA and the Tukey’s post hoc comparison test (p < 0.05). The factors nested from most generalist to most specific were as follows: (i) priming type (no priming including water and culture medium and priming including the rest of treatments), (ii) inoculum type (water, culture medium for the no priming treatment and priming with the four cyanobacterial species, N. commune, T. distorta, T. desertorum, and L. frigida (either biomass + exudates or exudates)), and (iii) treatment type (water, culture medium for the non-priming treatment, and treatment with exudate or Journal of Plant Growth Regulation biomass + exudate for the different cyanobacteria species). Finally, a one-way ANOVA was performed to analyze the differences in EPS concentration in both exudates and biomass + exudates of the four cyanobacterial species for each plant. Post hoc comparisons were performed using Tukey’s test with a significance level set at p < 0.05. Before data analysis, variables were tested for normality and homogeneity of variance using the Shapiro–Wilk and Levene’s test. All the analyses were conducted in R version 4.2.3 (R Core Team 2023) using the stats (R Core Team 2023) and rsq (Zhang 2022) packages and the ggplot2 package (Wickham 2011) for boxplots. Results Seed Germination In absence of any priming treatment (water control), the four plant species differed in germination percentage, germination time, and slope around the inflection point of cumulative germination curves (Table2). S. capensis and P. ovata showed the highest germination percentage, the shortest germination time and the steepest slope (lowest b-value). Comparatively, M. tenacissima and T. hyemalis showed lower germination percentages. Differences were found in the time for germination between the two perennial plants, where T. hyemalis showed much longer time than M. tenacissima, which showed values closer to those shown by the annual plants (Table2). The slopes in perennial species were smoother, with T. hyemalis having the lowest slope (higher b – value) (Table2). Notably, the pattern in germination curves differed between plants (Fig.2). S. capensis, P. ovata, and M. tenacissima showed an exponential cumulative curve, while T. hyemalis showed a linear trend. The germination rate of S. capensis and P. ovata increased exponentially during the first three days, after which they reached a plateau with values between 64–86% and 82–100%, respectively. A similar response was observed in M. tenacissima (Fig.2), but in this case, stabilization occurred at day 7 with a germination rate between 35 and 54% depending on the biopriming treatment and cyanobacteria species. In the case of T. hyemalis, no plateau was reached since seeds germinated daily. With regards to the T50, we also detected differences among plant species mainly associated with their life strategy. T50 was just 1day for the annual plants, while it increased to 6days for M. tenacissima and was the highest for woody shrub T. hyemalis, which reached more than 50% of the seeds germinated after 28days (Fig.2). The nested ANOVA showed that priming, inoculum type, treatment type, as well as their interactions, had no significant effect on seed germination percentage of the four plant species tested (Fig.1; TableS1). Regardless of this lack of significance in most cases, we observed that seed priming with the exudate of the four cyanobacterial species generally performed better than priming with the biomass + exudate for the four plant species (Fig.1). Overall, exudates increased germination with respect to biomass + exudate by 11.5 ± 14.6% in S. capensis (p-value = 0.0421, etasq = 0.1306), 8.6 ± 9.4% in P. ovata (p-value = 0.0524, etasq = 0.1197), 44.2 ± 16.2% in T. hyemalis (p-value = 0.0011, etasq = 0.3014), and 3 ± 14.2% in M. tenacissima (p-value = 0.7969, etasq = 0.0022). It is worth noting that in the case of P. ovata, seed priming with T. desertorum exudates led to 100% seed germination (Fig.1). In contrast to the results of germination percentage, the nested ANOVA revealed a significant effect of the interaction between priming and inoculum on germination time in S. capensis, as well as a significant effect of priming and the interaction between priming, inoculum and treatment in M. tenacissima. In S. capensis, the water treatment resulted in the shortest germination time (1.19 ± 0.11days), while all other treatments extended it. For M. tenacissima, all treatments shortened germination time compared to water (3.31 ± 0.61days), with the biomass + exudates treatment achieving a 23% reduction. Regarding T50, nested ANOVA showed significant effects for S. capensis and M. tenacissima. In S. capensis, the significant effects were due to the interaction between priming and inoculum, as well as to the combined effect of the three factors. The treatments T. distorta biomass + exudate and culture medium significantly doubled the median germination time. For M. tenacissima, the interaction between priming and inoculum was statistically significant (TableS2). Although no effect was detected between treatments in the Tukey analysis, some trends were identified. Control Table 2 Germination percentage, germination time and slope around the inflection point of the cumulative germination curves (average [b (slope)], minimum [b min], and maximum [b max]) of each plant species for the control water Germination (%) Germination time (days) b (slope) b min b max S. capensis 82 ± 12 1.2 ± 0.1 0.46 ± 0.07 0.38 0.52 P. ovata 92 ± 6.5 1.2 ± 0.2 0.40 ± 0.04 0.33 0.43 T. hyemalis 31 ± 8.9 15.7 ± 3.7 3.70 ± 0.38 3.21 4.12 M. tenacissima 50 ± 4 3.4 ± 0.7 2.05 ± 0.47 1.68 2.71 Journal of Plant Growth Regulation water, N. commune exudate, T. desertorum exudate and biomass + exudate reduced T50 by more than half compared to the other treatments. Finally, no differences were found in the slope around the inflection point between the different cyanobacteria treatments (both exudates and biomass + exudate) compared to controls for the different plant species (Fig.2; TablesS3, S4), meaning that the priming treatments did not induce differences in the germination rate over time compared to water and medium controls. Radicle Elongation The results of the nested ANOVA showed a significant effect of priming, inoculum type and treatment type on radicle elongation. These effects varied depending on the plant and cyanobacteria species and were only detected in annual plants (Fig.3; Table3, S1). In the case of S. capensis, all biomass + exudate treatments caused a significant increase in radicle length compared to water, ranging from 26 to 42% with no significant differences between cyanobacterial species (Fig.3). Priming (p-value = 0.0058, etasq = 0.0139), inoculum (p-value = 0.0002, etasq = 0.0396), and treatment (p-value = 2.63e–8, etasq = 0.0727) alsohad a significant effect on the number of secondary or lateral roots in S. capensis. The biomass + exudates treatments produced an increase of 43% to 300% in the number of secondary roots compared to the exudates alone. Despite these differences, a significant effect was only found in the case of the biomass + exudate treatment of T. desertorum which led to a significantly higher number of secondary roots (7.5 ± 4) compared to the water (3 ± 2.5) and culture medium (2.5 ± 0.6) (Fig.S1). In P. ovata, N. commune exudate and both T. distorta exudate and T. distorta biomass + exudate had a significant positive effect on radicle elongation, showing increases of 31, 31, and 29%, respectively, with respect to water and culture medium (Fig.3). Although the exudates of the non-N-fixing species did not induce significant changes compared to the controls in P. ovata, we detected a tendency of this treatment to increase radicle length, e.g., by 16% in T. desertorum and 15% in L. frigida. Similarly, the exudate treatment showed a positive effect on radicle length compared to the biomass + exudate treatment; however, differences were not significant due to the large variability within treatments (Table3; Fig.3). N. commune exudate increased by 27%, T. distorta exudate by 1%, T. desertorum exudate by 8%, and L. frigida exudate by 83%, with respect to their corresponding biomass + exudate treatment. Finally, it is worth mentioning that L. frigida biomass + exudate showed a negative effect on radicle length, causing a Fig. 1 Biopriming effect on seed germination percentage in S. capensis, P. ovata, T. hyemalis, and M. tenacissima. Boxes represent 50% of the central data (starting at the first percentile (Q1) and ending at the third percentile (Q3)), with the black line inside representing the median and the black square representing the mean. Vertical segments arising from the boxes represent the minimum and maximum values omitting the outliers and the black dots correspond to the outliers. Blue and orange bars indicate the water and growth medium control treatments, respectively, while the green and yellow bars indicate the cyanobacteria biomass + exudate and exudate treatments, respectively. No significant differences between the treatments and the controls (water and culture medium) were found for any of the plant species. Nested ANOVA results are shown in TableS1 (Color figure online) Journal of Plant Growth Regulation decrease of 37% and 28% compared to water and culture medium, respectively (Fig.3). For the perennial species, none of the two types of inocula (exudate or biomass + exudate) promoted a significant effect on radicle elongation compared to the water treatment (Fig.3; TableS1). For T. hyemalis, the exudates from T. desertorum and L. frigida showed a positive but nonsignificant trend on radicle growth, increasing by 10 and 6%, respectively, compared to water and culture medium. In contrast, biomass + exudate of this non-heterocystous cyanobacteria species displayed an opposite effect compared to the exudates, decreasing radicle length by 39 and 48%, respectively, relative to controls (Fig.3). For M. tenacissima, none of the cyanobacteria treatments differed significantly from the water treatment, but it is noteworthy the potential inhibitory effect of the culture medium that resulted in a 33% decrease in radicle length compared to the water treatment. The summarized effects of the priming treatments on radicle elongation for the four plant species can be seen in Table3. The GI (Fig.S2; TableS5) showed a similar pattern to radicle length but no significant effect of priming, inoculum and treatment was found for any of the plant species due to large variability between replicates. Similar to the effect on radicle length, a positive trend of N. commune Fig. 2 Germination accumulation curves over time for each treatment and plant species: S. capensis (A), P. ovata (B), M. tenacissima (C), and T. hyemalis (D). The blue line corresponds to the water control, while the orange line corresponds to the culture medium. For the four cyanobacteria species, exudates are represented by continuous lines, while biomass + exudates are represented by dashed lines: N. commune (dark red), T. distorta (black), T. desertorum (fuchsia), and L. frigida (yellow). The differences in the slopes of the curves are shown in TableS3 and Nested ANOVA results are shown in TableS4 (Color figure online) Journal of Plant Growth Regulation Fig. 3 Biopriming effect on radicle elongation in S. capensis, P. ovata, T. hyemalis, and M. tenacissima. Boxes represent 50% of the central data (starting at the first percentile (Q1) and ending at the third percentile (Q3)), with the black line inside representing the median and the black square representing the mean. Vertical segments arising from the boxes represent the minimum and maximum values omitting the outliers and the black dots correspond to the outliers. Blue and orange bars indicate the water and growth medium control treatments, respectively, while the green and yellow bars indicate the cyanobacteria biomass + exudate and exudate treatments, respectively. Lower case letters indicate significant differences between exudate and biomass + exudate for each cyanobacteria (p-value < 0.05). Capital letters located above the green boxes indicate significant differences among the four biomass + exudate treatments for the same plant species, while capital letters located above the yellow boxes indicate significant differences between the four exudate treatments. Significant differences of the treatment versus water are indicated with an asterisk, while differences versus culture medium are indicated with a cross (Color figure online) Table 3 Categorical summary of the effects of different priming treatments on radicle elongation in S. capensis, P. ovata, T. hyemalis and M. tenacissima. B + Ex Cyanobacteria biomass + exudate, Ex Cyanobacteria exudate Green cells denote positive effects vs water, yellow ones denote no effect vs water, and orange ones denote negative effects vs water Journal of Plant Growth Regulation Front Microbiol 11:568224. https:// doi. org/ 10. 3389/ fmicb. 2020. 568224 Chilton AM, Neilan BA, Eldridge DJ (2018) Biocrust morphology is linked to marked differences in microbial community composition. Plant Soil 429:65–75. https:// doi. org/ 10. 1007/ s11104- 017- 3442-3 Chitra P, Jijeesh CM (2021) Biopriming of seeds with plant growth promoting bacteria Pseudomonas fluorescens for better germination and seedling vigour of the East Indian sandalwood. New for (Dordr) 52:829–841. https:// doi. org/ 10. 1007/ s11056- 020- 09823-0 Chua M, Erickson TE, Merritt DJ etal (2020) Bio-priming seeds with cyanobacteria: effects on native plant growth and soil properties. Restor Ecol 28:168–176. https:// doi. org/ 10. 1111/ rec. 13040 Cortina J, Maestre FT, Ramírez D (2009) Innovations in semiarid land restoration: the case of Stipa tenacissima L. steppes. In: Bautista S, Aronson J, Vallejo VR (eds) Land restoration to combat desertification: innovative approaches, quality control and project evaluation. Fundación Centro de Estudios Ambientales del Mediterráneo – CEAM, Valencia, pp 121–144 Costa OYA, Raaijmakers JM, Kuramae EE (2018) Microbial extracellular polymeric substances: ecological function and impact on soil aggregation. Front Microbiol 9:1636. https:// doi. org/ 10. 3389/ fmicb. 2018. 01636 De Baets S, Poesen J, Knapen A etal (2007) Root characteristics of representative Mediterranean plant species and their erosionreducing potential during concentrated runoff. Plant Soil 294:169– 183. https:// doi. org/ 10. 1007/ s11104- 007- 9244-2 Dessì L, Podda L, Brundu G etal (2021) Seed germination ecophysiology of Acacia dealbata link and Acacia mearnsii De Wild.: two invasive species in the Mediterranean Basin. Sustainability 13:11588. https:// doi. org/ 10. 3390/ su132 111588 DuBois M, Gilles KA, Hamilton JK etal (1956) Colorimetric method for determination of sugars and related substances. Anal Chem 28:350–356. https:// doi. org/ 10. 1021/ ac601 11a017 Duncan C, Schultz NL, Good MK etal (2019) The risk-takers and -avoiders: germination sensitivity to water stress in an arid zone with unpredictable rainfall. AoB Plants 11:PLZ066. https:// doi. org/ 10. 1093/ aobpla/ plz066 El-Habet H, Elsadany AY (2020) Maximize growth and productivity of rice by using N2-fixing Anabaena oryzae and Spirulina platensis extract. J Plant Prod 11:1105–1114. https:// doi. org/ 10. 21608/ jpp. 2020. 130933 Essa AMM, Ibrahim WM, Mahmud RM, ElKassim NA (2015) Potential impact of cyanobacterial exudates on seed germination and antioxidant enzymes of crop plant seedlings. Int J Curr Microbiol and Appl Sci 4:1010–1024 Fazeli-Nasab B, Sayyed RZ, Piri R, Rahmani AF (2021) Biopriming and nanopriming: green revolution wings to increase plant yield, growth, and development under stress condition and forward dimensions. In: Singh HB, Vaishnav A, Sayyed RZ (eds) Antioxidants in plant-microbe interaction. Springer, Singapore, pp 623–655 Friedman J (2020) The evolution of annual and perennial plant life histories: ecological correlates and genetic mechanisms. Annu Rev Ecol Evol Syst 51:461–481. https:// doi. org/ 10. 1146/ annur evecols ys- 110218- 024638 Ghorbanpour A, Hatami M (2014) Biopriming of Salvia officinalis seed with growth promoting rhizobacteria affects invigoration and germination indices. J Bio & Environ Sci 8:29–36 Hashtroudi MS, Ghassempour A, Riahi H etal (2013) Endogenous auxins in plant growth-promoting Cyanobacteria—Anabaena vaginicola and Nostoc calcicola. J Appl Phycol 25:379–386. https:// doi. org/ 10. 1007/ s10811- 012- 9872-7 Hnatuszko-Konka K, Gerszberg A, Weremczuk-Jeżyna I, Grzegorczyk- Karolak I (2021) Cytokinin signaling and de novo shoot organogenesis. Genes (Basel) 12:265. https:// doi. org/ 10. 3390/ genes 12020 265 Hoover DL, Bestelmeyer B, Grimm NB etal (2020) Traversing the wasteland: a framework for assessing ecological threats to drylands. Bioscience 70:35–47. https:// doi. org/ 10. 1093/ biosci/ biz126 Houida S, Yakkou L, Kaya LO etal (2022) Biopriming of maize seeds with plant growth-promoting bacteria isolated from the earthworm Aporrectodea molleri: effect on seed germination and seedling growth. Lett Appl Microbiol 75:61–69. https:// doi. org/ 10. 1111/ lam. 13693 James JJ, Svejcar TJ, Rinella MJ (2011) Demographic processes limiting seedling recruitment in arid grassland restoration. J Appl Ecol 48:961–969. https:// doi. org/ 10. 1111/j. 1365- 2664. 2011. 02009.x Jian G, Bingchang Z, Feiya S (2015) Influence of exopolysaccharides from dominant cyanobacteria in microbiotic crusts on seed germination of several desert herbaceous plants. J Desert Res 35:639– 644. https:// doi. org/ 10. 7522/j. issn. 10006 94X. 2014. 00037 Kildisheva OA, Erickson TE, Merritt DJ, Dixon KW (2016) Setting the scene for dryland recovery: an overview and key findings from a workshop targeting seed-based restoration. Restor Ecol 24:36–42. https:// doi. org/ 10. 1111/ rec. 12392 Kildisheva OA, Dixon KW, Silveira FAO etal (2020) Dormancy and germination: making every seed count in restoration. Restor Ecol 28:256–265. https:// doi. org/ 10. 1111/ rec. 13140 Kollmen J, Strieth D (2022) The beneficial effects of cyanobacterial co-culture on plant growth. Life 12:223. https:// doi. org/ 10. 3390/ life1 20202 23 Kumar M, Prasanna R, Bidyarani N etal (2013) Evaluating the plant growth promoting ability of thermotolerant bacteria and cyanobacteria and their interactions with seed spice crops. Sci Hortic 164:94–101. https:// doi. org/ 10. 1016/j. scien ta. 2013. 09. 014 Kumar G, Teli B, Mukherjee A etal (2019) Secondary metabolites from cyanobacteria: a potential source for plant growth promotion and disease management. In: Bahadur Singh H, Keswani C, Reddy MS etal (eds) Secondary metabolites of plant growth promoting rhizomicroorganisms. Springer, Singapore, pp 239–252 Laroche C (2022) Exopolysaccharides from microalgae and cyanobacteria: diversity of strains, production strategies, and applications. Mar Drugs 20:336. https:// doi. org/ 10. 3390/ md200 50336 Machado-de-Lima NM, Charlesworth J, Stewart J etal (2023) Seed biopriming at different concentrations to assess the effects of Cyanobacteria on germination and seedling performance of keystone arid species. J Sustain Agric Environ 2:266–275. https:// doi. org/ 10. 1002/ sae2. 12049 Madsen MD, Davies KW, Boyd CS etal (2016) Emerging seed enhancement technologies for overcoming barriers to restoration. Restor Ecol 24:S77–S84. https:// doi. org/ 10. 1111/ rec. 12332 Maestre FT, Benito BM, Berdugo M etal (2021) Biogeography of global drylands. New Phytol 231:540–558. https:// doi. org/ 10. 1111/ nph. 17395 Maggioli L, Chamizo S, Román R etal (2022) Coupling sewage sludge amendment with cyanobacterial inoculation to enhance stability and carbon gain in dryland degraded soils. Agriculture 12:1993. https:// doi. org/ 10. 3390/ agric ultur e1212 1993 Mahmood A, Turgay OC, Farooq M, Hayat R (2016) Seed biopriming with plant growth promoting rhizobacteria: a review. FEMS Microbiol Ecol 92:fiw112. https:// doi. or g/ 10. 1093/ femsec/ fiw112 Mazhar S, Cohen JD, Hasnain S (2013) Auxin producing non-hetero- cystous Cyanobacteria and their impact on the growth and endogenous auxin homeostasis of wheat. J Basic Microbiol 53:996–1003. https:// doi. org/ 10. 1002/ jobm. 20110 0563 Mirzabaev A, Stringer LC, Benjaminsen TA etal (2022) Cross-chapter paper 3: deserts, semiarid areas and desertification. In: Pörtner H-O, Roberts DC, Tignor M etal (eds) Climate change 2022: impacts, adaptation and vulnerability. Contribution of working group II to the sixth assessment report of the intergovernmental panel on climate change. Cambridge University Press, Cambridge, pp 2195–2232 Journal of Plant Growth Regulation Moorthy K, Delfe K (2019) Isolation and identification of cyanobacteria and its impact on seed germination potential of maize (Zea mays L.) using seed germination experiment. Int J Eng Appl Sci Tech 4:65–72. https:// doi. org/ 10. 33564/ IJEAST. 2019. v04i07. 010 Moulessehoul YI, Mehdadi Z, Benchiha W (2022) Comparative study on caryopses germination of Stipa tenacissima L. from two habitats of Western Algeria under different controlled conditions of salinity and water potential. Egypt Acad J Biol Sci C Physiol Mol Biol 14:163–174. https:// doi. org/ 10. 21608/ eajbsc. 2022. 262281 Müller M, Munné-Bosch S (2011) Rapid and sensitive hormonal profiling of complex plant samples by liquid chromatography coupled to electrospray ionization tandem mass spectrometry. Plant Methods 7:1–11. https:// doi. org/ 10. 1186/ 1746- 4811-7- 37 Muñoz-Rojas M, Chilton A, Liyanage GS etal (2018) Effects of indigenous soil cyanobacteria on seed germination and seedling growth of arid species used in restoration. Plant Soil 429:91–100. https:// doi. org/ 10. 1007/ s11104- 018- 3607-8 Nowruzi B, Bouaïcha N, Metcalf JS etal (2021) Plant-cyanobacteria interactions: beneficial and harmful effects of cyanobacterial bioactive compounds on soil-plant systems and subsequent risk to animal and human health. Phytochemistry 192:112959. https:// doi. org/ 10. 1016/j. phyto chem. 2021. 112959 Oliver TH, Heard MS, Isaac NJB etal (2015) Biodiversity and resilience of ecosystem functions. Trends Ecol Evol 30:673–684. https:// doi. org/ 10. 1016/j. tree. 2015. 08. 009 Pan VS, Girvin C, LoPresti EF (2022) Anchorage by seed mucilage prevents seed dislodgement in high surface flow: a mechanistic investigation. Ann Bot 129:817–830. https:// doi. org/ 10. 1093/ aob/ mcac0 45 Pérez DR, González F, Ceballos C etal (2019) Direct seeding and outplantings in drylands of Argentinean Patagonia: estimated costs, and prospects for large-scale restoration and rehabilitation. Restor Ecol 27:1105–1116. https:// doi. org/ 10. 1111/ rec. 12961 Prabha R, Singh DP, Yadav SK (2019) Seed biopriming with potential microbial inoculants as sustainable options for stress management in crops. In: Singh D, Prabha R (eds) Microbial interventions in agriculture and environment. Springer, Singapore, pp 211–224 Prăvălie R (2016) Drylands extent and environmental issues. A Global Approach Earth Sci Rev 161:259–278. https:// doi. org/ 10. 1016/j. earsc irev. 2016. 08. 003 Pueyo Y, Moret-Fernández D, Saiz H etal (2013) Relationships between plant spatial patterns, water infiltration capacity, and plant community composition in semi-arid Mediterranean ecosystems along stress gradients. Ecosystems 16:452–466. https:// doi. org/ 10. 1007/ s10021- 012- 9620-5 QGIS Development Team (2019) QGIS Geographic Information System. Open Source Geospatial Foundation Project R Core Team (2023) R: a language and environment for statistical computing. R Foundation for Statistical Computing, R Core Team Righini H, Francioso O, Di Foggia M etal (2021) Tomato seed biopriming with water extracts from Anabaena minutissima, Ecklonia maxima and Jania adhaerens as a new agro-ecological option against Rhizoctonia solani. Sci Hortic 281:109921. https:// doi. org/ 10. 1016/j. scien ta. 2021. 109921 Rinella MJ, Hammond DH, Bryant A-EM, Kozar BJ (2015) High precipitation and seeded species competition reduce seeded shrub establishment during dryland restoration. Ecol Appl 25:1044– 1053. https:// doi. org/ 10. 1890/ 14- 1110.1 Ritz C, Baty F, Streibig JC, Gerhard D (2015) Dose-response analysis using R. PLoS ONE 10:e0146021. https:// doi. org/ 10. 1371/ journ al. pone. 01460 21 Rodríguez-Caballero E, Román JR, Chamizo S etal (2019) Biocrust landscape-scale spatial distribution is strongly controlled by terrain attributes: topographic thresholds for colonization in a semiarid badland system. Earth Surf Process Landf 44:2771– 2779. https:// doi. org/ 10. 1002/ esp. 4706 Román JR, Roncero-Ramos B, Chamizo S etal (2018) Restoring soil functions by means of cyanobacteria inoculation: importance of soil conditions and species selection. Land Degrad Dev 29:3184– 3193. https:// doi. org/ 10. 1002/ ldr. 3064 Román JR, Chamizo S, Roncero-Ramos B etal (2021) Overcoming field barriers to restore dryland soils by cyanobacteria inoculation. Soil Tillage Res 207:104799. https:// doi. org/ 10. 1016/j. still. 2020. 104799 Roncero-Ramos B, Muñoz-Martín MÁ, Chamizo S etal (2019a) Polyphasic evaluation of key cyanobacteria in biocrusts from the most arid region in Europe. PeerJ 7:e6169. https:// doi. org/ 10. 7717/ peerj. 6169 Roncero-Ramos B, Román JR, Rodríguez-Caballero E etal (2019b) Assessing the influence of soil abiotic and biotic factors on Nostoc commune inoculation success. Plant Soil 444:57–70. https:// doi. org/ 10. 1007/ s11104- 019- 04239-y Roncero-Ramos B, Román JR, Acién G, Cantón Y (2022) Towards large scale biocrust restoration: producing an efficient and lowcost inoculum of N-fixing cyanobacteria. Sci Total Environ 848:157704. https:// doi. org/ 10. 1016/j. scito tenv. 2022. 157704 Salamah A, Purwanti D, Innaza S etal (2020) Formation of lateral roots and root hairs of Ciherang rice as a result of Nostoc colonization. IOP Conf Ser Earth Environ Sci 481:012036. https:// doi. org/ 10. 1088/ 1755- 1315/ 481/1/ 012036 Saqrane S, El Ghazali I, Oudra B etal (2008) Effects of cyanobacteria producing microcystins on seed germination and seedling growth of several agricultural plants. J Environ Sci Health, Part B 43:443–451. https:// doi. org/ 10. 1080/ 03601 23080 20623 07 Scholes RJ (2020) The future of semi-arid regions: a weak fabric unravels. Climate 8:43. https:// doi. org/ 10. 3390/ cli80 30043 Shackelford N, Paterno GB, Winkler DE etal (2021) Drivers of seedling establishment success in dryland restoration efforts. Nat Ecol Evol 5:1283–1290. https:// doi. org/ 10. 1038/ s41559- 021- 01510-3 Sharma V, Prasanna R, Hossain F etal (2020) Priming maize seeds with cyanobacteria enhances seed vigour and plant growth in elite maize inbreds. 3 Biotech 10:154. https:// doi. org/ 10. 1007/ s13205- 020- 2141-6 Singh S (2014) A review on possible elicitor molecules of cyanobacteria: their role in improving plant growth and providing tolerance against biotic or abiotic stress. J Appl Microbiol 117(5):1221– 1244. https:// doi. org/ 10. 1111/ jam. 12612 Singh R, Parihar P, Singh M etal (2017) Uncovering potential applications of cyanobacteria and algal metabolites in biology, agriculture and medicine: current status and future prospects. Front Microbiol 8:515. https:// doi. org/ 10. 3389/ fmicb. 2017. 00515 Singh V, Maharshi A, Singh DP etal (2018) Role of microbial seed priming and microbial phytohormone in modulating growth promotion and defense responses in plants. In: Rakshit A, Singh HB (eds) Advances in seed priming. Springer, Singapore, pp 115–126 Singh S, Singh UB, Malviya D etal (2020) Seed biopriming with microbial inoculant triggers local and systemic defense responses against Rhizoctonia solani causing banded leaf and sheath blight in maize (Zea mays L.). Int J Environ Res Public Health 17:1396. https:// doi. org/ 10. 3390/ ijerp h1704 1396 Singh P, Vaishnav A, Liu H etal (2023) Seed biopriming for sustainable agriculture and ecosystem restoration. Microb Biotech. https:// doi. org/ 10. 1111/ 1751- 7915. 14322 Srivastava S, Tyagi R, Sharma S (2023) Seed biopriming as a promising approach for stress tolerance and enhancement of crop productivity: a review. J Sci Food Agric. https:// doi. org/ 10. 1002/ jsfa. 13048 Tan C-Y, Dodd IC, Chen JE etal (2021) Regulation of algal and cyanobacterial auxin production, physiology, and application in Journal of Plant Growth Regulation agriculture: an overview. J Appl Phycol 33:2995–3023. https:// doi. org/ 10. 1007/ s10811- 021- 02475-3 Weber B, Belnap J, Büdel B etal (2022) What is a biocrust? A refined, contemporary definition for a broadening research community. Biol Rev 97:1768–1785. https:// doi. org/ 10. 1111/ brv. 12862 Wickham H (2011) ggplot2. Wires Comput Stat 3:180–185. https:// doi. org/ 10. 1002/ wics. 147 Wongchawalit J, Premsuriya J (2015) Screening, isolation and identification of fresh water microalgae and factors influencing of polysaccharide production. Adv Environ Biol 9:29–37 Xiao B, Bowker MA, Zhao Y etal (2022) Biocrusts: engineers and architects of surface soil properties, functions, and processes in dryland ecosystems. Geoderma 424:116015. https:// doi. org/ 10. 1016/j. geode rma. 2022. 116015 Yadav P, Singh RP, Gupta RK (2022) Role of cyanobacteria in germination and growth of paddy seedlings. Int J Phytol Res 2:11–18 Yirdaw E, Tigabu M, Monge A (2017) Rehabilitation of degraded dryland ecosystems—a review. Silva Fennica 51:1673. https:// doi. org/ 10. 14214/ sf. 1673 Zhang D (2022) rsq: R-squared and related measures. R package version 2.5 Zucconi F, Pera A, Forte M, DeBertolli M (1981) Evaluating toxicity of immature compost. Biocycle 22:54–57 Zulueta-Rodríguez R, Hernández-Montiel L, Murillo-Amador B etal (2015) Effect of hydropriming and biopriming on seed germination and growth of two Mexican fir tree species in danger of extinction. Forests 6:3109–3122. https:// doi. org/ 10. 3390/ f6093 109 Zvinavashe AT, Laurent J, Mhada M etal (2021) Programmable design of seed coating function induces water-stress tolerance in semi-arid regions. Nat Food 2:485–493. https:// doi. org/ 10. 1038/ s43016- 021- 00315-8 Publisher's Note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.