Effects of Plant Growth-promoting Microorganisms on the Early Growth of Kentucky Bluegrass under Drought and Salinity

Authors:
Qi Zhang Department of Plant Sciences, North Dakota State University, Department #7670, PO Box 6050, Fargo, ND 58108, USA

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Kevin Rue Department of Plant Sciences, North Dakota State University, Department #7670, PO Box 6050, Fargo, ND 58108, USA

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Abstract

Drought and salinity affect turfgrass growth and development adversely. Plant growth-promoting microorganisms (PGPMs) have been shown to have the capability of improving resistance to biotic stressors in plants. The objective of this research was to determine the efficacy of six commercial PGPMs on enhancing the drought and salinity resistance of kentucky bluegrass (Poa pratensis). The six PGPMs evaluated were Beauveria bassiana (strain GHA), Bacillus subtilis (strain GB03), Azadirachtin, Bacillus firmus (strain 1-582), Trichoderma harzianum Rifai (strain T-22) combined with Trichoderma virens (strain G-41), and Bacillus subtilis (strain QST713). Three cultivars—Kenblue, Moonlight, and Waterworks—were seeded in the greenhouse. Two-week seedlings were exposed to saline (sodium chloride at 6 dS⋅m–1 three times per week) or drought (tap water once per week) conditions, and no stress (irrigated with tap water three times per week) for 4 weeks. Results show that drought and salinity inhibited turf growth, with the greatest reduction in root dry weight (50.3% in drought conditions and 31.4% in saline conditions). ‘Kenblue’ performed better than ‘Waterworks’ and ‘Moonlight’ in all growth indices except for root length. Beauveria bassiana and B. subtilis had a similar or better result in enhancing turfgrass growth and development compared with the untreated turf under stress. Our results suggest that certain PGPMs have the potential to improve abiotic stress resistance in turfgrass.

The rhizosphere is the soil region largely influenced by plants through rhizodeposition of exudates and metabolites, providing rich carbon sources and colonization structures for soil microorganisms. Microorganisms in turn may have deleterious, neutral, or beneficial effects on plants. It has been well documented that plant growth-promoting microorganisms (PGPMs), including arbuscular mycorrhizal fungi (AMF) and plant growth-promoting bacteria (PGPB), can improve yield and stress resistance in field crops (Coleman-Derr and Tringe 2014). For example, Esitken et al. (2010) reported that greater yield and nutrient contents were achieved in strawberry (Fragaria ×ananassa) when three PGPB (Pseudomonas BA-8, Bacillus OSU-142, and Bacillus M-3) were applied alone or in combination as biofertilizer agents in the field. Under drought stress, citrus plants inoculated with an AMF, Glomus mosseae, showed improved plant height, stem diameter, and fresh weight (Wu et al. 2006). Azotobacter showed protection from salinity in maize (Zea mays) (Rojas-Tapias et al. 2012). Although a plant × PGPM interaction is not fully understood, some mechanisms of PGPMs enhancing plant performance and stress resistance include influencing acquisition of water and nutrients, modulating plant hormone levels, regulating source–sink relations and energetic metabolism, and inducing systemic resistance (Glick 2012).

It has been reported that fungal endophytes, such as Acremonium, enhance turfgrass performance and stress resistance (Fraser and Breen 1994). However, the beneficial effects of fungal endophytes are observed mainly in perennial ryegrass (Lolium perenne), tall fescue (Schedonorus arundinaceus), and fine fescues (Festuca sp.) as a result of the high host specificity of endophytes (Fraser and Breen 1994). Symbiotic relationships between fungal endophytes and other important turfgrass species, including kentucky bluegrass, rarely occur naturally. Recent research has shown the presence and effects of bacterial endophytes in turfgrass. Coy (2014) and Coy et al. (2014) demonstrated that PGPB blends from Paenibacillus, Bacillus, and Brevibacillus improved root and shoot growth, and reduced insect damage in ‘Tifway’ bermudagrass (Cynodon transvaalensis × Cynodon dactylon). Kentucky bluegrass seeds inoculated with Bacillus and Pantoea showed a greater seed germination rate and seedling growth than uninoculated seeds under the saline condition 100 mM NaCl (Chen et al. 2015). The aforementioned results showed that PGPMs can potentially be beneficial to nonendophytic turfgrass species, such as kentucky bluegrass. To our knowledge, the effects of commercially available PGPMs on turfgrass performance, with and without abiotic stressors, have not been documented on nonendophytic turfgrass. The objective of our research was to determine the effects of commercial PGPMs products on drought and salinity resistance of kentucky bluegrass in controlled environments.

Materials and methods

Expt. 1: Salinity

‘Kenblue’ and ‘Moonlight’ kentucky bluegrass were seeded at a rate of 3 lb pure live seeds/1000 sq ft in 4 × 4 in pots filled with a topsoil:sand mixture (1:1, v:v). A starter fertilizer, N18–P11–K4, was applied at 1 lb N/1000 sq ft at seeding. Six commercially available PGPM products labeled as biofungicides or bioinsecticides for turfgrass use were included in our study (Table 1). They were mixed with water and applied to the soil surface with a pipette (10 mL/pot) at seeding and once weekly from weeks 3 6, except for Bacillus firmus (strain 1-582), which was treated at seeding and at week 4. Pots were saturated with tap water from the bottom after seeding to minimize soil disturbance, and were kept in a tub filled with tap water (depth, 1 inch) for weeks 1 and 2 to ensure good germination. Turf pots were moved out of the tub at week 3 and were hand-watered with tap water or a NaCl treatment at 6 dS⋅m–1 three times weekly (Monday, Wednesday, and Friday) from weeks 3 to 6. Turfgrass was harvested when the experiment was ended at week 6. The experimental design was a 2 (cultivar) × 2 (salt condition) × 7 (6 PGPM products + 1 no PGPM application control) factorial design, with the experimental unit (pot) arranged in a randomized complete block design with four replicates. Data were collected on plant height, shoot and root dry weight, root length, root-to-shoot dry weight ratio, and specific root length (i.e., root length/root dry weight). Soil samples were also collected from four randomly selected pots from each combination between cultivar and salt condition (total = 16 pots) for electric conductivity (EC) and pH analysis from the saturated soil paste, following the method of Yang and Zhang (2019). Briefly, soil was sampled from the whole pot and air-dried before soil EC and pH were measured with a pH/EC meter (model 378; Hach Co., Loveland, CO, USA). Data were analyzed using PROC MIXED in SAS v9.4 (SAS Institute, Cary, NC, USA), and means were separated with Fisher’s protected least significant difference at P ≤ 0.05.

Table 1.

Six commercially available plant growth-promoting microorganism products included in our study.

Table 1.

Expt. 2: Drought

‘Kenblue’ and ‘Waterworks’ kentucky bluegrass were seeded and maintained in a greenhouse with all PGPM applications as described in Expt. 1. Half of the pots were hand-watered three times weekly from weeks 3 to 6 (i.e., nondrought) and the other half were watered once weekly (i.e., drought stress treatment). Leaf wilting was observed from the plants under the drought treatment at the end of each irrigation cycle. The experimental design, data collection, and analysis were identical to Expt. 1, with the exception that no soil samples were collected.

Results

Expt. 1: Salinity

Soil EC of the salt-treated soil was 7.9 dS⋅m–1, which was significantly greater than that of the nonsaline treatment (0.2 dS⋅m–1; P ≤ 0.05); however, soil pH was greater in the nonsaline condition compared with the saline condition (7.2 vs. 6.5; P ≤ 0.05). It was observed that salinity stress inhibited turfgrass growth, with reductions ranging from 10.2% in plant height to 31.4% in root dry weight (Table 2). In contrast, specific root length was increased under salinity as a result of a greater reduction in root dry weight than in root length (14.5%). ‘Kenblue’ seedlings outperformed ‘Moonlight’ in plant height and shoot dry weight (Table 2), whereas ‘Moonlight’ had a greater specific root length compared with ‘Kenblue’, which was the result of a lower root dry weight of ‘Moonlight’, as both cultivars had a similar root length (average, 14.8 cm). The dry weights of shoots and roots of ‘Moonlight’ were 30.2% and 27.2% less, respectively, than that of ‘Kenblue’. Thus, the root-to-shoot dry weight ratio of ‘Moonlight’ and ‘Kenblue’ was similar. No significant differences in plant growth were observed among PGPM treatments, except for plant height and shoot dry weight in which plants treated with Beauveria bassiana (strain GHA), B. firmus (strain 1-582), Trichoderma harzianum Rifai (strain T-22) combined with Trichoderma virens (strain G-41), and Bacillus subtilis (strain QST713) were similar to that of the control (i.e., no PGPM application).

Table 2.

Kentucky bluegrass seedling growth as affected by cultivar, salt condition (sodium chloride), and plant growth-promoting microorganism products, and their interactions.

Table 2.

An interaction of cultivar × salt was observed in the root dry weight and root-to-shoot dry weight ratio (Table 1). The root dry weight was reduced by salinity in both cultivars (Fig. 1A). ‘Kenblue’ had a root dry weight of 999.4 mg/pot under the nonstress condition, which was significantly greater than ‘Moonlight’ (673.5 mg/pot). However, the differences in the two cultivars were diminished under salinity (average, 574.0 mg/pot). Regarding the root-to-shoot dry weight ratio, salinity only resulted in a lower root-to-shoot dry weight ratio in ‘Kenblue’ (Fig. 1B). The averaged root-to-shoot ratio of the two cultivars was 56.1% under the nonsaline condition. Under the saline condition, ‘Moonlight’ had a root-to-shoot ratio of 53.2%, which was 24.9% higher than that of ‘Kenblue’.

Fig. 1.
Fig. 1.

The root dry weight (A) and root-to-shoot dry weight ratio (B) of kentucky bluegrass seedlings as affected by cultivar and saline conditions (sodium chloride at 0 or 6 dS⋅m–1). Means followed by the same letter are not significantly different at P ≤ 0.05. 1 mg = 3.527 × 10–5 oz; 1 dS⋅m–1 = 1 mmho/cm.

Citation: HortTechnology 34, 4; 10.21273/HORTTECH05366-23

Expt. 2: Drought

Similar to salinity stress, drought affected kentucky bluegrass growth negatively, except for specific root length (Table 3). The highest and lowest growth reduction was observed in root dry weight (50.3%) and root length (15.3%), respectively. Specific root length was increased 77.2% under drought compared with the nonstress condition. Plant height, tissue biomass, and root-to-shoot dry weight ratio were higher in ‘Kenblue’ than in ‘Waterworks’; however, ‘Waterworks’ had a longer specific root length than ‘Kenblue’ (Table 3). No difference in root length was observed between the two cultivars. Tissue biomass was affected by PGPMs. Plants treated with B. bassiana (strain GHA) and B. subtilis (strain GB03) showed a greater shoot and root dry weight than the control (i.e., no PGPM application) when data were pooled across cultivar and growth conditions. PGPM products showed no improvement of the root-to-shoot dry weight ratio compared with the control, although significant differences were observed in this growth index. Beauveria bassiana- (strain GHA) and Azadirachtin-treated turfgrass had a shorter specific root length than the untreated plants.

Table 3.

Kentucky bluegrass seedling growth as affected by cultivar, drought condition, and plant growth-promoting microorganism products, and their interactions.

Table 3.

The shoot and root dry weights were influenced by an interaction of cultivar × drought (Table 3). The shoot dry weight was less under drought than nondrought conditions in both cultivars (Fig. 2A). Under nonstress conditions, ‘Waterworks’ had a lower shoot dry weight than ‘Kenblue’, but no difference was observed between ‘Waterworks’ and ‘Kenblue’ under the drought condition. Drought caused reduced root biomass in both cultivars compared with the nonstress condition (Fig. 2B). Under either condition, ‘Kenblue’ performed better than ‘Waterworks’.

Fig. 2.
Fig. 2.

The shoot (A) and root (B) dry weight of kentucky bluegrass seedlings as affected by cultivar and drought conditions. Plants were hand-watered three times (drought) or once weekly (no drought) conditions. Means followed by the same letter are not significantly different at P ≤ 0.05. 1 mg = 3.527 × 10–5 oz.

Citation: HortTechnology 34, 4; 10.21273/HORTTECH05366-23

Discussion

Yang and Zhang (2019) reported that ‘Kenblue’ had higher values in shoot dry weight, root dry weight, and root length than ‘Moonlight’ at the germination and seedling growth stages, contributing to the differences in salinity resistance between the two cultivars at the early growth stage. Our results (Table 2) were consistent with their findings. In our study, a higher value in plant height and tissue biomass of ‘Kenblue’ over that of ‘Waterworks’ under drought was observed (Table 3). This finding suggests that ‘Kenblue’ is more drought resistant than ‘Waterworks’ at the germination and seedling growth stages. This finding is contradictory to that of the work by Morris (2017), in which the mature plants of ‘Waterworks’ performed better than ‘Kenblue’ under drought. Reverse rankings in stress resistance between the germination and seedling stages and vegetative growth stage have been reported in various turfgrass cultivars/species comparisons, including kentucky bluegrass, creeping bentgrass (Agrostis stolonifera), buffalograss (Bouteloua dactyloides), and blue grama (Bouteloua gracilis) (Dai et al. 2009; Yang and Zhang 2019; Zhang et al. 2012). Yang and Zhang (2019) suggested the discrepancy of stress resistance among turfgrass growth stages is related to the evaluation criteria used. Quick surface coverage is more important during early growth for turf, especially in the first month of development after germination. Differences in the growth rate among turf species/cultivars generally diminish 90 d after establishment. Thereafter, visual quality plays a more important role in turfgrass evaluation at the vegetative stage (>90 d after seeding) than the seedling/establishment stage (<90 d after seeding).

Among the growth indices evaluated our this study, plant height, shoot and root dry weights, root-to-shoot dry weight ratio, and root length were affected negatively by salinity and drought (Tables 2 and 3). The root dry weight was more affected by stressors than the shoot dry weight (31.4% vs. 17.0% reduction under salinity stress and 50.3% vs. 29.8% in reduction under drought stress, respectively), resulting in a lower root-to-shoot dry weight ratio (Tables 2 and 3). These results were consistent with the findings of Walter and Nagel (2006), Yang and Zhang (2019), and Nakamura et al. (2021), in which root growth was more sensitive to stressors than shoot growth. However, other research observed that shoot growth is more sensitive than root growth (Zhou et al. 2018), or both were affected equally by stressors (Hasan et al. 2017; Shahzad et al. 2012). Agathokleous et al. (2019) suggested that the root-to-shoot ratio change is dosage dependent—a typical hormesis. Photosynthetic activities generally increased by a low stress, resulting in high C allocation to roots, whereas a high level of stress reduced photosynthetic C production, which leads to the low root growth (biomass and/or elongation) (Agathokleous et al. 2019). Other factors, such as differences in stress resistance in species/cultivars and different growing media, may also influence stress dosage; thus, such factors should be taken into consideration when comparing research results. Nonetheless, the root-to-shoot ratio is an indicator of energy allocation between supportive functions (water and nutrient uptake by roots) and growth functions (light harvest by shoots) (Agathokleous et al. 2019). Similarly, specific root length indicates the potential of acquiring water and nutrients by root elongation (i.e., root length) relative to the potential of root longevity (i.e., root biomass) (Ostonen et al. 2007). In our study, specific root length increased under stressors resulting from a greater reduction in root dry weight compared with root length (Tables 2 and 3).

In the past two decades, there has been a dramatic increase in the number of commercialized PGPM products, primarily as biofertilizer, inoculants, and biopesticide, as they are much safer to the environment and human health compared with traditional synthesized products (Reed and Glick 2023). PGPMs can improve plant growth directly by interactions between the beneficial microbes and plants (e.g., nutrient/water acquisition and hormonal stimulation) and/or indirectly by suppressing activities of plant pathogens (Berg 2009). Because microorganisms have diverse functions in plants, people are interested in exploring potential additional effects of commercial PGPMs on plant growth and development. In our research, we evaluated the efficacy of six commercially available biopesticide-type PGPM products on drought and salinity enhancement in turfgrass. No PGPM products influenced plant growth negatively when exposed to salinity (except for Azadirachtin) and drought stress (Tables 2 and 3). In fact, B. bassiana (strain GHA) and B. subtilis (GB03) improved shoot and root dry weights under the drought condition compared with the control (Table 3). Hence, our findings suggest that these PGPM products can be used as effective biostimulants to enhance resistance to abiotic stressors in turfgrass. Bakhshandeh et al. (2020) evaluated the effects of 21 PGPM products on soybean (Glycine max) germination, seedling growth, and K uptake under optimum, drought, and salt conditions. Among the eight PGPMs that showed promising results under the optimal condition, four were better than others under both types of stress and one was better under salinity, whereas the rest were similar as or occasionally better than the uninoculated plants. Therefore, the beneficial effect of PGPM inoculation depends on the PGPM species (Bakhshandeh et al. 2020). Similar results were reported in other studies, including those by Estevez et al. (2009) and Widawati and Suliashih (2018).

Conclusion

Drought and salinity affect turfgrass growth and development negatively. Among the growth indices evaluated in our study, root dry weight was more sensitive than root length, shoot dry weight, and plant height at the germination and seedling growth stages. ‘Kenblue’ kentucky bluegrass showed greater resistance to drought and salinity than ‘Moonlight’ and ‘Waterworks’ because of its high initial growth rate. Beauveria bassiana (strain GHA; 4.8 × 1013 cfu/acre) and B. subtilis (strain GB03; 1.1 × 1011 cfu/acre) had promising results in improving kentucky bluegrass performance under salinity and drought conditions during its early growth phase.

References cited

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    • Search Google Scholar
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    • Search Google Scholar
    • Export Citation
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    • Search Google Scholar
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  • Fig. 1.

    The root dry weight (A) and root-to-shoot dry weight ratio (B) of kentucky bluegrass seedlings as affected by cultivar and saline conditions (sodium chloride at 0 or 6 dS⋅m–1). Means followed by the same letter are not significantly different at P ≤ 0.05. 1 mg = 3.527 × 10–5 oz; 1 dS⋅m–1 = 1 mmho/cm.

  • Fig. 2.

    The shoot (A) and root (B) dry weight of kentucky bluegrass seedlings as affected by cultivar and drought conditions. Plants were hand-watered three times (drought) or once weekly (no drought) conditions. Means followed by the same letter are not significantly different at P ≤ 0.05. 1 mg = 3.527 × 10–5 oz.

  • Agathokleous E, Belz RG, Kitao M, Koike T, Calabrese EJ. 2019. Does the root to shoot ratio show a hermetic response to stress? An ecological and environmental perspective. J For Res. 30:15691580. https://doi.org/10.1007/s11676-018-0863-7.

    • Search Google Scholar
    • Export Citation
  • Bakhshandeh E, Gholamhosseini M, Yaghoubian Y, Pirdashti H. 2020. Plant growth promoting microorganisms can improve germination, seedling growth and potassium uptake of soybean under drought and salt stress. Plant Growth Regulat. 90:123136. https://doi.org/10.1007/s10725-019-00556-5.

    • Search Google Scholar
    • Export Citation
  • Berg G. 2009. Plant-microbe interactions promoting plant growth and health: Perspectives for controlled use of microorganisms in agriculture. Appl Microbiol Biotechnol. 84:1118. https://doi.org/10.1007/s00253-009-2092-7.

    • Search Google Scholar
    • Export Citation
  • Chen Q, Bergen M, White JF Jr. 2015. Potential for application of growth-promoting bacterial endophytes in turfgrasses. SeedWorld. Sept:6467.

    • Search Google Scholar
    • Export Citation
  • Coleman-Derr D, Tringe SG. 2014. Building the crops of tomorrow: Advantages of symbiont-based approaches to improving abiotic stress tolerance. Front Microbiol. 5:16. https://doi.org/10.3389/fmicb.2014.00283.

    • Search Google Scholar
    • Export Citation
  • Coy RM. 2014. Potential of plant growth-promoting rhizobacteria (PGPR) as a biological control agent against warm-season turfgrass pests (MS Thesis). Auburn University, Auburn, AL, USA.

  • Coy RM, Held DH, Kloepper JW. 2014. Rhizobacteria inoculants increase root and shoot growth in ‘Tifway’ hybrid bermudagrass. J Environ Hortic. 32(3):149154. https://doi.org/10.24266/0738-2898.32.3.149.

    • Search Google Scholar
    • Export Citation
  • Dai J, Huff DR, Schlossberg MJ. 2009. Salinity effects on seed germination and vegetative growth of greens-type Poa annua relative to other cool-season turfgrass species. Crop Sci. 49:696703. https://doi.org/10.2135/cropsci2008.04.0221.

    • Search Google Scholar
    • Export Citation
  • Esitken A, Yildiz HE, Ercisli S, Figen Donmez M, Turan M, Gunes A. 2010. Effects of plant growth promoting bacteria (PGPB) on yield, growth and nutrient contents of organically grown strawberry. Sci Hortic. 124(1):6266. https://doi.org/10.1016/j.scienta.2009.12.012.

    • Search Google Scholar
    • Export Citation
  • Estevez J, Dardanelli M, Megías M, Rodríguez-Navarro D. 2009. Symbiotic performance of common bean and soybean co-inoculated with rhizobia and Chryseobacterium balustinum Aur9 under moderate saline conditions. Symbiosis. 49:2936. https://doi.org/10.1007/s13199-009-0008-z.

    • Search Google Scholar
    • Export Citation
  • Fraser ML, Breen JP. 1994. The role of endophytes in integrated pest management for turf, p 521–529. In: Leslie AR (ed). Handbook of integrated pest management for turf and ornamentals. CRC Press LLC, New York, NY, USA.

  • Glick BR. 2012. Plant growth-promoting bacteria: Mechanisms and applications. Scientifica. 2012:963401. https://doi.org/10.6064/2012/963401.

    • Search Google Scholar
    • Export Citation
  • Hasan MM, Baque MA, Habib MA, Yeasmin M, Hakim MA. 2017. Screening of salt tolerance capability of wheat genotypes under salt stress condition. Univ J Agric Res. 5:235249. https://doi.org/10.13189/ujar.2017.050405.

    • Search Google Scholar
    • Export Citation
  • Morris K. 2017. 2011 National kentucky bluegrass test. 2012–2016 Data. Final report NTEP no. 17-10.

  • Nakamura C, Takenaka S, Nitta M, Yamamoto M, Kawazoe K, Ono S, Takenaka M, Inoue K, Takenaka S, Kawai S. 2021. High sensitivity of roots to salt stress as revealed by novel tip bioassay in wheat seedlings. Biotechnol Biotechnol Equip. 35(1):238246. https://doi.org/10.1080/13102818.2020.1852890.

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Qi Zhang Department of Plant Sciences, North Dakota State University, Department #7670, PO Box 6050, Fargo, ND 58108, USA

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Kevin Rue Department of Plant Sciences, North Dakota State University, Department #7670, PO Box 6050, Fargo, ND 58108, USA

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Contributor Notes

We thank the US Golf Association and North Dakota Hatch Project (ND01509) for funding this project.

Q.Z. is the corresponding author. E-mail: qi.zhang.1@ndsu.edu.

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  • Fig. 1.

    The root dry weight (A) and root-to-shoot dry weight ratio (B) of kentucky bluegrass seedlings as affected by cultivar and saline conditions (sodium chloride at 0 or 6 dS⋅m–1). Means followed by the same letter are not significantly different at P ≤ 0.05. 1 mg = 3.527 × 10–5 oz; 1 dS⋅m–1 = 1 mmho/cm.

  • Fig. 2.

    The shoot (A) and root (B) dry weight of kentucky bluegrass seedlings as affected by cultivar and drought conditions. Plants were hand-watered three times (drought) or once weekly (no drought) conditions. Means followed by the same letter are not significantly different at P ≤ 0.05. 1 mg = 3.527 × 10–5 oz.

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