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. 2024 Mar 5;6:100229. doi: 10.1016/j.crmicr.2024.100229

Strigolactone GR24-mediated mitigation of phosphorus deficiency through mycorrhization in aerobic rice

Debasis Mitra a,b,1, Periyasamy Panneerselvam b,⁎, Parameswaran Chidambaranathan b, Amaresh Kumar Nayak b, Ankita Priyadarshini b, Ansuman Senapati b, Pradeep Kumar Das Mohapatra a,⁎
PMCID: PMC10958977  PMID: 38525307

Highlights

  • •

    Harnessing the potential of arbuscular mycorrhizal fungi with strigolactone GR24 in aerobic rice.

  • •

    AMF treated with 5.0 µM SL GR24 varieties CR Dhan 205 followed by CR Dhan 207 and 204 showed the best performance in plant growth and soil functional properties.

  • •

    Seed priming with 5.0 µM SL GR24 enhanced the performance of mycorrhization in varieties CR Dhan 205 followed by CR Dhan 204 and 207.

  • •

    High responsive variety CR Dhan 207 showed higher P uptake as compared to control.

  • •

    AMF intervention with SL GR24 significantly increased the environmental impacts in rice production.

Keywords: Strigolactone GR24, Mycorrhiza, Phosphorus, Stress, Aerobic rice

Abstract

Strigolactones (SLs) are a new class of plant hormones that play a significant role in regulating various aspects of plant growth promotion, stress tolerance and influence the rhizospheric microbiome. GR24 is a synthetic SL analog used in scientific research to understand the effects of SL on plants and to act as a plant growth promoter. This study aimed to conduct hormonal seed priming at different concentrations of GR24 (0.1, 0.5, 1.0, 5.0 and 10.0 µM with and without arbuscular mycorrhizal fungi (AMF) inoculation in selected aerobic rice varieties (CR Dhan 201, CR Dhan 204, CR Dhan 205, and CR Dhan 207), Kasalath-IC459373 (P-tolerant check), and IR-36 (P-susceptible check) under phosphorus (P)-deficient conditions to understand the enhancement of growth and priming effects in mycorrhization. Our findings showed that seed priming with 5.0 µM SL GR24 enhanced the performance of mycorrhization in CR Dhan 205 (88.91 %), followed by CR Dhan 204 and 207, and AMF sporulation in CR Dhan 201 (31.98 spores / 10 gm soil) and CR Dhan 207 (30.29 spores / 10 g soil), as well as rice growth. The study showed that the highly responsive variety CR Dhan 207 followed by CR Dhan 204, 205, 201, and Kasalath IC459373 showed higher P uptake than the control, and AMF treated with 5.0 µM SL GR24 varieties CR Dhan 205 followed by CR Dhan 207 and 204 showed the best performance in plant growth, chlorophyll content, and soil functional properties, such as acid and alkaline phosphatase activity, soil microbial biomass carbon (MBC), dehydrogenase activity (DHA), and fluorescein diacetate activity (FDA). Overall, AMF intervention with SL GR24 significantly increased plant growth, soil enzyme activity, and uptake of P compared to the control. Under P-deficient conditions, seed priming with 5.0 µM strigolactone GR24 and AMF inoculum significantly increased selected aerobic rice growth, P uptake, and soil enzyme activities. Application of SLs formulations with AMF inoculum in selected aerobic rice varieties, CR Dhan 207, CR Dhan 204, and CR Dhan 205, will play an important role in mycorrhization, growth, and enhancement of P utilization under P- nutrient deficient conditions.

Graphical abstract

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1. Introduction

Arbuscular mycorrhizal fungi (AMF) colonize the majority of plant roots and establish a mutualistic association with them (Besserer et al., 2006), supporting nutrient uptake (Begum et al., 2019), including phosphorus (P) from the soil under P-deficient conditions (Etesami et al., 2021). Under nutrient deficiency conditions in the soil, hormonal priming is used in agriculture to enhance seed germination, seedling emergence, and overall plant performance (Rhaman et al., 2020; Devika et al., 2021; Ibrahim et al., 2022b; Paul et al., 2023). Hormonal priming involves the application of specific plant hormones to seeds before planting to improve their ability to respond to favorable conditions and stress (Rhaman et al., 2020; Mitra et al., 2023b). Plant hormones called strigolactones (SLs) play vital roles in multiple aspects of plant growth and development, including root development, shoot branching, and AMF colonization (Smith, 2014; Mishra et al., 2017; Mitra et al., 2021c). SLs also affect plant responses to environmental cues such as nutrient availability (Marzec et al., 2013).

The application of SLs in agriculture and horticulture has gained interest because of their potential to influence plant growth and enhance crop yields (Foo, 2021). Naturally occurring SL signaling or the external application of SLs can potentially improve root system development, leading to better nutrient and water uptake by plants (Marro et al., 2022). SLs suppress shoot branching, directing the plant's energy towards main stem growth, leading to more robust and productive plants with a single dominant stem (Shinohara et al., 2013; Khuvung et al., 2022). SLs promote symbiotic relationships with mycorrhizal fungi, which helps plants increase their nutrient uptake from the soil (Yoneyama, 2019; Soliman et al., 2022; Alvi et al., 2022). The application of SLs can enhance the establishment and effectiveness of beneficial fungal associations (Lanfranco et al., 2018b). SLs are also implicated in plant responses to nutrient stress such as P deficiency (Marzec et al., 2013). SLs are naturally stimulating molecules that hold great potential for investigating plant-soil interactions in both basic and applied science (Bouwmeester et al., 2007; López-Ráez et al., 2011; Kee et al., 2023). Hence, SL can be utilized in agriculture to tackle challenges related to enhancing crop productivity and improving soil health under challenging climatic conditions.

GR-24 is a cost-effective synthetic SL molecule that is commonly used as a reference in SL research and applications (Wigchert et al., 1999; Kgosi et al., 2012; Lachia et al., 2012; Pandya‐Kumar et al., 2014; Wang and Xi, 2022). It is commercially available in racemic mixtures as a single enantiomer (Borghi et al., 2021). The structure and stereochemistry of GR-24 mimics those of natural SLs, with an ABC-ring moiety bound to the D-ring via an enol ether bridge that activates SL biosynthesis and signaling (Lopez-Obando et al., 2015; Jia et al., 2019; Borghi et al., 2021). The use of SLs improves plant resilience under adverse conditions through SL signal transduction (Foo, 2021). These synthetic compounds can be applied to plants in various ways, including foliar sprays, soil drenches, seed treatments, seed priming, but the timing, concentration, and frequency of application depending on the specific goals and the target plant species. The rac-GR24 treatment has no impact on bacterial calcium spiking/ nodulation factor production and growth, but it has been recognized as a plant hormone and play important role in rhizosphere signaling and interaction with AMF (Moscatiello et al., 2010; Soto et al., 2010; Cuyper and Goormachtig, 2017).

Therefore, this study aimed to explore potential methods for improving the association of AMF in four aerobic rice varieties using the check P-susceptible variety and P-tolerant variety by the external application of synthetic SL GR24 at different concentrations through seed priming. This study focused on the development of AMF-SL formulations and the optimum SL concentration to enhance P uptake and rice growth under P-deficient conditions.

2. Materials and methods

2.1. Experimental site

The experiment was conducted during Rabi season (2022) in a controlled net house at the Microbiology, Crop Production Division, ICAR‐ NRRI, Cuttack, India (latitude : 20°25′ N, longitude : 85°55′ E, at an altitude of 24 m above mean sea level). Low phosphorus (6.003 ± 0.59 kg ha−1) soil was collected from Krishi Vigyan Kendra (KVK), Santhpur, ICAR–NRRI, Cuttack, Odisha (20°27´45.08´´N; 85°52´58.76´´E). Each experimental pot was filled with 10 kg homogenized low-P soil.

2.2. Details of strigolactone GR24

Strigolactone GR24 has been purchased from Biosynth Carbosynth®, United Kingdom for the experiment (Table 1).

Table 1.

Details of strigolactone GR24 used in this study.

Company name
and CAS No 		Structure Chemical formula Molecular weight SMILES Melting point Storage Dissolve in
Biosynth Carbosynth Ltd, United Kingdom
[76974-79-3]		 Image, table 1 C17H14O5 298.29 g/mol CC1=C[C@@H](OC1=O)O/C=C/2\[C@H]3CC4=CC Created by potrace 1.16, written by Peter Selinger 2001-2019 CC Created by potrace 1.16, written by Peter Selinger 2001-2019 C4[C@H]3OC2=O 157 °C Store at
< -15 °C		 0.02 %
Acetone
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SMILES: Simplified molecular-input line-entry system; CAS: Chemical abstract service.

2.3. Details of AMF inoculum for experiment

The soil-based mixed AMF inoculum was obtained from Microbiology, Crop Production Division, ICAR-NRRI, India. The inoculum contained 130 AMF spores/g of soil, which was multiplied using finger millet (E. coracana) and rice as host plants in sterile soil using the trap culture method.

2.4. Seed priming of SL GR24 and experiment description

The pot experiment was conducted with five different concentrations of SL GR24 (T1: 0.1 µM, T2: 0.5 µM, T3: 1.0 µM, T4: 5.0 µM, T5: 10.0 µM, T6: 0.02 % acetone treated, T7: Control) in popular aerobic rice varieties viz. V1: CR Dhan 201, V2: CR Dhan 204, V3: CR Dhan 205, V4: CR Dhan 207, V5: P susceptible check (IR 36) and V6: P tolerant check (Kasalath IC459373), with (12,000 spores per pot) and without AMF inoculation under P-deficient conditions. Rice seeds were surface sterilized with a 5 % NaOCl solution, washed 4–5 times with distilled water. The surface sterilized seeds were immersed and primed with GR24 at different concentration, wherein the seed: solution ratio was maintained at 1:5 (w/v). Similar treatment was adopted for acetone treatment and un-inoculated control except GR24 priming. Treated seeds were air dried on blotting papers and these primed seeds were then used for experiment. Three plants per pot were maintained with three replication and a CRD design was used. Plant and soil samples were collected after 90 days from each treatment to check the AMF colonization, sporulation, growth parameters, P uptake, soil chemical, microbial, and enzymatic activity analyses.

2.5. Assessment of AMF colonization and spore count

The method developed by Phillip and Hayman (1970) was used to evaluate rice root colonization by AMF (Ganeshamurthy et al., 2017). To commence the procedure, freshly collected root samples were delicately washed to remove soil attached to the root surfaces. The samples were then submerged in a 10 % KOH solution and autoclaved for 15 min at 121 °C. Following autoclaving, the KOH solution was decanted, and the treated roots were rinsed with tap water three times until no brown color appeared in the rinsed water. The root samples were then immersed in a 2 % HCl solution for 5 min, without rinsing with water. The HCl solution was decanted, and the root samples were stained with 0.05 % trypan blue (HiMedia, India) in lacto-glycerol [lactic acid (400 mL) + glycerol (400 mL)+ water (100 mL)]. The stained samples were then autoclaved for 15 min at 121 °C, after which the staining solution was decanted, and the roots were de-stained with lacto-glycerol solution to remove excess stain. The resulting segments were observed under a compound microscope (Radical RxLr-4, India), and the method proposed by McGonigle et al. (1990) was used to calculate the percentage of root colonization.

AMF root colonization was calculated using the formula:

% of colonization = no. of root segments colonized ÷ total no. of root segments × 100

2.6. Phosphorus estimation in plant sample

The analysis of the P concentration in plant samples was carried out using the vanadomolybdo phosphoric acid method, along with a UV/Vis spectrophotometer (Analytikjena specord-200, Germany) (Arrhenius, 1927). A gram of dried plant material and 10 ml of HNO3 (69 %) were added and allowed to sit overnight, followed by the addition of 10 ml of tri-acid (HNO3, H2SO4, and HClO4 in a ratio of 9:4:1) and mixing. The mixture was then heated at 100 °C for 1 h, during which time the content reduced to 2–3 ml and turned colorless. The contents were cooled, and 10 ml of HCl (35 %) was added, followed by filtering through Whatman No. 42 filter paper. The filtrate was made up to 100 ml using distilled water, and 5 ml of the filtered sample was taken for the vanadomolybdate reagent (Merck, Germany) and incubated for 30 min. The absorption of the samples was measured at 420 nm using a UV/Vis spectrophotometer, and a standard curve was prepared with a phosphate solution (0.2195 g of KH2PO4 in 500 ml distilled water+ 25 ml of 7 N H2SO4 and made up to 1000 ml). The P content of the plant samples was calculated from the standard curve.

2.7. Estimation of soil chemical, enzymatic and microbial properties

2.7.1. Acid (AcP) and alkaline (AkP) phosphatases activity

The activity of AcP and AkP phosphatase in soil samples was determined using the method of Tabatabai and Bremner (1969) by incubating a gram of soil in a 50 ml flask with p-nitrophenyl as a substrate, modified universal buffer (MUB) (pH 6.5 for AcP assay and pH 11 for AkP assay), and 0.05 M pNP solution (Nayak et al., 2016). After incubation at 37 °C for 1 h, 1 mL of 0.5 M CaCl2 and 4 mL of 0.5 M NaOH were added, and the resulting yellow color was measured using a spectrophotometer. A standard curve was prepared with p-nitrophenol, and the amount of p-nitrophenol liberated was calculated to determine the phosphatase activity, expressed in l g of p-nitrophenyl phosphate (pNP) released per gram of soil per hour. Phosphatase activity was calculated as µg p-nitrophenol (pNP) g-1 h-1.

2.7.2. Soil microbial biomass carbon (MBC)

The chloroform fumigation extraction (CFE) method was used to determine the activity of microbial biomass carbon (MBC) using the method of Witt et al. (2000). 10 g of moist soil samples were collected and kept in oven at 105 °C for 24 h, and moisture content was calculated. A 50 ml beaker was taken and 3 g of soil was placed in a beaker (2 sets). One set was un-fumigated, while the other was fumigated in a vacuum desiccator. A vacuum was created inside the desiccator until the chloroform boiled. The desiccators were maintained in the dark for 24 h. Both fumigated and un-fumigated samples were transferred to a 250 ml conical flask and 25 ml of 0.5 M K2SO4 was added. The total organic carbon (TOC) content in the soil extracts was measured using the dichromate digestion method (Schumacher, 2002). The CFE-MBC was calculated as 2.64 times the difference in extractable organic C between fumigated and unfumigated soils and expressed as µg g-1 soil (Vance et al., 1987).

2.7.3. Soil dehydrogenase activity (DHA)

The dehydrogenase activity (DHA) was measured using the method described by Casida et al. (1964), which involved the use of triphenyltetrazolium chloride (TTC) as a substrate. The soil samples (3 g) were mixed with 0.2 g of CaCO3, 1 ml of 3 % (w/v) 2,3,5-TTC, 2.5 ml of distilled water, and incubated at 37 ºC for 24 h. After incubation, 10 ml of methanol were added, and the enzyme converted TTC to 2,3,5 triphenylformazan (TPF). The TPF formed was extracted with methanol, the extracts were filtered, and absorption was measured at 485 nm using a spectrophotometer (Analytikjena specord-200, Germany) and expressed as µg TPF h-1 g-1 soil (Nayak et al., 2016).

2.7.4. Soil fluorescein diacetate activity (FDA)

Soil fluorescein diacetate activity (FDA) measurements were performed using the method of Schnrer and Rosswall (1982), as modified by Adam and Duncan (2001). The amount of fluorescein released during the assay was determined using a calibration graph created with a 0–5 µg fluorescein mL−1 standard, and it was reported in units of µg fluorescein h-1 g-1 soil (Nayak et al., 2016).

2.8. Measures relative chlorophyll content of leaves

A chlorophyll meter (SPAD 502 Plus; Konica Minolta, Japan) was used to measure the relative chlorophyll content of the leaves (greenness) without damaging the leaves in each treatment. Reading was taken between 10:30–13.00 h of the day.

2.9. Statistical analysis

The study adopted a Completely Randomized Design (CRD) incorporating three independent factors labelled as Factor A, Factor B, and Factor C. Each factor comprised multiple levels, resulting in a total of r × s × t treatment combinations. The experiment was replicated three times to minimize experimental error. A three-way analysis of variance (ANOVA) was conducted to ascertain the influence of Factors A, B, and C on the response variable(s). The ANOVA model was fitted to the data utilizing the aov() function available in the R statistical computing environment (Team, R.C.., 2000). The data obtained were statistically analyzed using the Web-Based Agricultural Statistical Software Package (WASP 2.0) developed by the Central Coastal Agricultural Research Institute (ICAR), Ela Goa (www.ccari.res.in/waspn ew.html).

3. Results and discussion

3.1. Effect of strigolactone GR24 application with and without AMF inoculation on shoot and root length in different rice varieties under P deficiency

Strigolactones (SLs) are a group of plant hormones that control various aspects of plant development, including shoot and root growth (Agusti et al., 2011). The use of synthetic strigolactones such as GR24, rac-GR24, GR7, AB01, mimic T-010, 5-Deoxystrigol, 2′-Epi-5-deoxystrigol, RMS1, and Nijmegen-1 can affect plant growth and architecture (Xie et al., 2013; Zwanenburg et al., 2013; Yamada et al., 2014; Vurro et al., 2016; Sun et al., 2021; Ahsan et al., 2022). The effects of synthetic SLs on shoot duration vary depending on SL application concentration (Ruyter-Spira et al., 2011). It is crucial to remember that these effects depend on the concentrations and may differ depending on plant variety. According to many research, low concentrations of GR24 (10 nM, 0.1–5.0 µM) can promote shoot branching and elongation, increasing the length of the shoot (Kapulnik et al., 2011; De Cuyper et al., 2015; Jiu et al., 2022; Wani et al., 2023). This response is related to the hormone's support for the shoot architecture and growth. Higher concentrations of GR24, synthetic SL analogs, or prolonged exposure may lead to shoot elongation (Krasylenko et al., 2021). This is frequently linked to changes in the physiological responses of plants, which may entail feedback-regulatory processes. Plant growth depends on auxin transport status, which is supported by the combined effects of synthetic SL and AM symbiosis (Mitra et al., 2021a,b; Alvi et al., 2022; Kountche et al., 2018). The ability of GR24 to promote shoot and root elongation may be complemented by the capacity of AMF to enhance nutrient uptake. However, it is also possible that these two factors can be combined intricately. This precise result might be influenced by the complex interplay between GR24- and AMF-induced plant hormone signaling, nutrient availability, and growth responses. According to the present research findings, Kasalath IC459373 shown higher performance in shoot growth at the concentrations of 1.0 µM (87.191 cm) and 10.0 µM (83.143 cm) GR24 SL with combination application of AMF (Table 2). However, the priming of SL GR24 at concentrations of 5.0 and 10.0 µM for CR Dhan 207 (71.531 cm), CR Dhan 201 (76.083 cm), respectively and 1.0 µM for CR Dhan 205 (69.275 cm) resulted significant increase in shoot growth under P deficient conditions (Table 2). Where as in, CR Dhan 205 (21.131 cm) and Kasalath IC459373 (20.345 cm) the highest performance in root growth was observed at the concentration of 10.0 µM GR24 SL with AMF inoculated treatment (Supplementary Table 1). However, application of GR24 concentration with 5.0 and 10.0 µM in CR Dhan 207 and CR Dhan 205 showed significantly higher root growth as compared to the un-inoculated AMF control (Table 2). Similar results have also been found with the exogenous application of various concentrations of GR24 (0.01, 0.1, 1.0, and 10 µM) was performed with 1/2 Murashige and Skoog medium (0.8 % agar and 3 % sucrose) for plant growth (Arite et al., 2012). Similarly, increased primary root length and enhanced root system architecture have been observed in Arabidopsis treated with 1.25 µM GR24 (Ruyter-Spira et al., 2011). These findings suggest that SLs positively influence root length, and that the effect of GR24 on rice growth varies from variety to variety.

Table 2.

Effect of strigolactone GR24 on rice growth with and without application of AMF under low P available soil.

Treatments Rice varieties Shoot length (cm)
 Root length (cm)
With AMF Without AMF With AMF Without AMF
0.1µM GR24 CR Dhan 201 61.644e 60.203e 13.935d 13.461c
CR Dhan 204 62.039d 60.597d 15.759b 14.953b
CR Dhan 205 62.839c 61.394cd 14.731c 12.538d
CR Dhan 207 66.157b 64.702b 13.337e 12.927d
IR36 59.023f 57.590f 11.277f 10.484e
Kasalath IC459373 75.015a 73.534a 17.359a 16.547a
CD(0.05) 0.283 0.333 0.104 0.122
0.5µM GR24 CR Dhan 201 66.448c 65.694b 13.387d 12.588c
CR Dhan 204 60.935e 59.494de 14.432c 13.630b
CR Dhan 205 61.578d 60.137d 16.523a 15.714a
CR Dhan 207 67.152b 64.993c 16.423b 15.614a
IR36 59.163f 57.729f 12.282e 11.486d
Kasalath IC459373 78.197a 76.706a 12.342e 11.546d
CD(0.05) 0.347 0.409 0.095 0.112
1.0µM GR24 CR Dhan 201 58.028e 56.598e 14.373d 13.570d
CR Dhan 204 61.094d 59.654d 14.432d 13.630d
CR Dhan 205 69.275b 67.811bd 15.925c 15.118bc
CR Dhan 207 68.578bc 67.116c 16.264b 15.456b
IR36 68.121c 66.660c 12.382e 11.585e
Kasalath IC459373 87.191a 85.673a 16.423a 15.614a
CD(0.05) 0.506 0.597 0.077 0.091
5.0µM GR24 CR Dhan 201 60.934e 59.495b 14.482b 13.678b
CR Dhan 204 62.308d 60.865f 14.383c 13.580cd
CR Dhan 205 62.739c 61.295e 16.373a 15.565a
CR Dhan 207 71.531b 70.060c 14.482b 13.679b
IR36 59.163f 57.729d 13.158e 12.360de
Kasalath IC459373 81.505a 80.004a 13.238d 12.439d
CD(0.05) 0.427 0.504 0.058 0.069
10.0µM GR24 CR Dhan 201 76.083b 74.599f 14.930e 14.126e
CR Dhan 204 62.573f 61.129e 18.248c 17.434c
CR Dhan 205 67.185e 65.727d 21.131a 20.308a
CR Dhan 207 72.988c 71.513b 16.254d 15.446de
IR36 68.121d 66.660c 12.342f 11.546f
Kasalath IC459373 83.143a 81.638a 20.345b 19.524bc
CD(0.05) 0.365 0.431 0.167 0.197
Acetone treated CR Dhan 201 62.039f 60.597f 12.381c 11.584c
CR Dhan 204 63.270e 61.824e 13.377ab 12.578bc
CR Dhan 205 64.299d 62.849de 12.379b 11.585c
CR Dhan 207 66.223b 64.768b 12.382c 11.583c
IR36 65.035c 63.584c 11.287d 9.494d
Kasalath IC459373 79.075a 77.582a 14.263a 13.461a
CD(0.05) 0.312 0.368 0.051 0.06
Control CR Dhan 201 60.944d 59.505d 11.178a 10.385a
CR Dhan 204 63.077b 61.632b 10.282c 9.492c
CR Dhan 205 62.407c 60.964cd 10.949b 10.157b
CR Dhan 207 60.934d 59.495d 9.286d 8.499cd
IR36 61.084d 59.644d 10.252c 9.462c
Kasalath IC459373 71.883a 70.411a 11.168ab 10.375a
CD(0.05) 0.212 0.250 0.037 0.043
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Different lowercase letters represent significant variations among the treatment at p < 0.05, CD: critical difference.

3.2. Influence of SL-GR24 application with and without AMF inoculation on P-uptake in different rice varieties

AMF, especially for P uptake, are beneficial soil microorganisms that colonize plant roots to improve nutrient uptake (Perner et al., 2007; Silva et al., 2023). According to Andreo-Jimenez et al. (2015), SL plays a crucial role as a modulator of the coordinated growth of plants in response to nutrient-deficient conditions, particularly phosphorus scarcity. In addition to controlling root architecture belowground, they serve as chemical cues that allow plants to communicate with their surroundings. In the present study, we investigated the effects of different concentrations of SL-GR24 and seed priming in different rice varieties on P uptake with and without AMF inoculation. According to Czarnecki et al. (2013), SLs play dual roles in plant P uptake and utilization. This has resulted in the emergence of a signaling module that shows how P uptake, plant-microbe symbiotic relationships, and plant design are all controlled together. Seed priming with 5.0 µM GR24 and AMF inoculum resulted in the highest P uptake in Kasalath IC459373 (25.731 g pot−1), followed by CR Dhan 201 (24.631 g pot−1), and CR Dhan 205 (22.634 g pot−1) compared to the un-inoculated control. Application of 5.0 µM GR24 may attract and enhance colonization of AMF in roots and could improve nutrient uptake, particularly phosphorus. Thus, signaling for mycorrhizal interactions can be improved by SL-GR24 application, which increases AMF colonization (Makhzoum et al., 2017; Kowalczyk and Hrynkiewicz, 2018; Kaniganti et al., 2022). This combination could have a synergistic effect on nutrient uptake, in addition to the ability of AMF to enhance P uptake in aerobic rice under P-deficient conditions. Overall, in all varieties, the optimum concentration of 5.0 µM SL GR24 strongly influenced the P uptake under P-deficient conditions (Table 3; Supplementary Table 1).

Table 3.

Strigolactone GR24 seed priming and its effect on P uptake in different rice varieties with and without application AMF under P deficient condition.

Treatments Rice varieties Plant P (g.pot−1)
With AMF Without AMF
0.1µM GR24 CR Dhan 201 16.863b 16.370b
CR Dhan 204 16.186c 15.700cd
CR Dhan 205 15.235e 14.758e
CR Dhan 207 18.788a 18.276a
IR36 13.150f 12.693e
Kasalath IC459373 15.813d 15.331f
CD(0.05) 0.093 0.084
0.5µM GR24 CR Dhan 201 15.251f 14.774f
CR Dhan 204 18.661c 18.151c
CR Dhan 205 20.622b 20.093a
CR Dhan 207 17.005d 16.511b
IR36 16.875e 16.382ab
Kasalath IC459373 21.065a 20.532a
CD(0.05) 0.114 0.104
1.0µM GR24 CR Dhan 201 14.994e 14.519f
CR Dhan 204 17.901b 17.398b
CR Dhan 205 16.099d 15.614d
CR Dhan 207 16.937c 16.443c
IR36 14.478f 14.009ef
Kasalath IC459373 21.741a 21.201a
CD(0.05) 0.131 0.119
5.0µM GR24 CR Dhan 201 20.127d 19.603ab
CR Dhan 204 19.601e 19.082ab
CR Dhan 205 22.634b 22.085b
CR Dhan 207 20.411c 19.884ab
IR36 16.484f 15.995c
Kasalath IC459373 25.731a 25.152a
CD(0.05) 0.155 0.141
10.0µM GR24 CR Dhan 201 24.631a 24.063a
CR Dhan 204 18.054e 17.550cd
CR Dhan 205 19.977c 19.454c
CR Dhan 207 18.217d 17.711cd
IR36 16.186f 15.700d
Kasalath IC459373 21.360b 20.823b
CD(0.05) 0.149 0.135
Acetone treated CR Dhan 201 15.252f 14.775d
CR Dhan 204 19.009b 18.495b
CR Dhan 205 18.760c 18.249b
CR Dhan 207 18.418d 17.910cd
IR36 16.186e 15.700d
Kasalath IC459373 21.902a 21.361a
CD(0.05) 0.117 0.106
Control CR Dhan 201 12.746f 12.005d
CR Dhan 204 14.327b 13.860c
CR Dhan 205 13.937c 13.473c
CR Dhan 207 13.764d 13.302c
IR36 12.934e 15.586b
Kasalath IC459373 16.790a 15.976a
CD(0.05) 0.073 0.058
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Different lowercase letters represent significant variations among the treatment at p < 0.05.

3.3. Impact of SL-GR24 application with and without AMF inoculation on its sporulation and colonization in different rice varieties

Numerous SL activities and applications have been documented in AMF symbiosis under different crop cultivation conditions (Lanfranco et al., 2018b; Kim et al., 2022; Soliman et al., 2022). When P is limited to the soil, AMF intervention has an important impact on P utilization, soil enzyme activities, and rice growth. To address this nutrient limitation, SLs also contribute to the modification of root architecture via AMF symbiosis. The activation of the symbiotic relationship with mycorrhizal fungi is an adaptation to improve the uptake of mineral nutrients, in which SLs play a vital role not as plant hormones but as rhizosphere signaling molecules (Besserer et al., 2006). SLs help AMF to branch their hyphal structures, which promotes the growth of a mutually beneficial relationship (Akiyama et al., 2005). In the present study, application of AMF with 5.0 µM SL GR24 resulted in maximum AMF sporulation in CR Dhan 201 (31.98 spores / 10 gm soil) and CR Dhan 207 (30.29 spores / 10 g soil) (Table 4; Fig. 1; Supplementary Table 1). Similarly, the percentage of AMF colonization was significantly higher in CR Dhan 205 (88.91 %), followed by CR Dhan 204 (83.83 %), and CR Dhan 207 (78.96 %) (Table 4; Fig. 2; Supplementary Table 1).

Table 4.

Strigolactone GR24 priming effect on AMF sporulation and colonization in different rice varieties with and without application AMF under P deficient soil.

Treatments Rice varieties AMF sporulation (spores / 10gm soil)
 % of AMF colonization
With AMF Without AMF With AMF Without AMF
0.1µM GR24 CR Dhan 201 19.273e 7.053 67.118b 6.731
CR Dhan 204 21.997c 4.826 62.939c 2.886
CR Dhan 205 21.132d 3.944 67.016b 7.521
CR Dhan 207 23.221b 7.086 53.191e NC
IR36 19.240e 2.019 59.056b NC
Kasalath IC459373 24.216a 6.072 77.967a NC
CD(0.05) 0.102 NS 0.42 NS
0.5µM GR24 CR Dhan 201 26.207b 9.112 67.009c 7.037
CR Dhan 204 23.333e 6.184 68.014b 8.406
CR Dhan 205 24.316d 10.136 58.051e NC
CR Dhan 207 25.321c 8.210 69.009a 7.737
IR36 21.230f 4.046 58.058e NC
Kasalath IC459373 27.212a 7.187 59.053d NC
CD(0.05) 0.107 NS 0.266 NS
1.0µM GR24 CR Dhan 201 25.336b 4.060 67.109b 7.111
CR Dhan 204 24.226c 7.096 59.053e NC
CR Dhan 205 23.331d 6.184 62.935b 3.037
CR Dhan 207 21.244e 8.226 66.023c 6.364
IR36 20.346f 3.144 59.053e NC
Kasalath IC459373 27.312a 10.237 68.014a 7.447
CD(0.05) 0.129 NS 0.198 NS
5.0µM GR24 CR Dhan 201 31.983a 14.993 70.997e 11.330
CR Dhan 204 29.303c 12.264 83.837b NC
CR Dhan 205 28.267d 11.21 88.913a 8.813
CR Dhan 207 30.298b 13.277 78.960c NC
IR36 21.244f 4.060 69.006f 7.781
Kasalath IC459373 26.317e 9.224 74.981d 12.039
CD(0.05) 0.188 NS 0.382 NS
10.0µM GR24 CR Dhan 201 23.336d 6.184 59.053f NC
CR Dhan 204 21.240e 4.056 68.977d 8.727
CR Dhan 205 25.222c 8.109 70.997c 10.371
CR Dhan 207 28.307b 11.25 77.964a 3.021
IR36 29.297a 12.258 68.011e NC
Kasalath IC459373 29.306a 12.267 75.977b 17.761
CD(0.05) 0.169 NS 0.335 NS
Acetone treated CR Dhan 201 23.334c 6.187 69.007c NC
CR Dhan 204 28.311b 11.254 71.010b 10.450
CR Dhan 205 23.332c 6.184 75.977a NC
CR Dhan 207 22.335d 5.17 69.009c NC
IR36 21.201e 4.015 65.025d 14.408
Kasalath IC459373 29.307a 12.268 70.997b 11.041
CD(0.05) 0.167 NS 0.179 NS
Control CR Dhan 201 21.174b 4.988 60.952c 2.376
CR Dhan 204 20.241c 3.038 62.082b 5.783
CR Dhan 205 20.235c 10.159 59.053d NC
CR Dhan 207 27.235a 3.032 60.940c 2.369
IR36 21.121b 3.934 58.058e NC
Kasalath IC459373 27.246a 2.465 69.020a 3.491
CD(0.05) 0.17 NS 0.193 NS
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Different lowercase letters represent significant variations among the treatment at p < 0.05; NC: no AMF colonization.

Fig. 1.

Fig 1

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Sporulation of AMF in rice varieties treated with SL GR24.

Fig. 2.

Fig 2

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AMF colonization in different rice varieties treated with SL GR24.

3.4. Effect of GR24 priming with and without AMF inoculation on soil functional properties viz. MBC, FDA and DHA in different rice varieties

The quantifiable terrestrial labile carbon (C) component, known as microbial biomass carbon (MBC), was used to measure the soil biological activity (Wei et al., 2022). The main determining factors of MBC are soil organic carbon (SOC), water retention capability, and soil pH. MBC contributes approximately 1 –5 % C to the total SOC (Babur and Dindaroglu, 2020). Host plants provide nutrition to AMF in exchange for the carbohydrates produced during photosynthesis (Panneerselva et al., 2019; Salmeron-Santiago et al., 2021). The hyphal network of AMF can also transport soil nutrients to plants and enhance soil quality by strengthening the soil structure and its ability to retain water (Begum et al., 2019; Schütz et al., 2022). AMF are essential for P/C cycling and SOC utilization, enhancing resistance and assisting in the growth of plants under P-deficient conditions for ecosystem restoration (Begum et al., 2019; Etesami et al., 2021; Shen et al., 2023). In the present study, MBC varied with the different levels of SL GR24 and AMF. Compared to the uninoculated control, 0.5, 5.0, and 10.0 µM concentrations of GR24 treated seeds in CR Dhan 205 (485.086, 495.065, and 496.150 µg g-1 soil, respectively) resulted in higher soil MBC (Table 5; Supplementary Table 1). The soil fluorescein diacetate activity (FDA) hydrolysis assay, which analyzes the enzyme activity of soil microbes, can quantify the total amount of microbial activity in an environmental sample reported by numerous researchers (Schnrer and Rosswall, 1982; Patle et al., 2018; Panneerselvam et al., 2019). FDA and dehydrogenase enzyme activities have been reported to improve by 46.50 % and 43.70 %, respectively, with the application of AMF treatment (Jabborova et al., 2021). This study aimed to understand the effects of SL GR24 priming on the FDA in different rice varieties under P-deficient conditions. SL GR24 priming with AMF inoculation showed higher FDA at 5.0 µM GR24 treated Kasalath IC459373 (8.785 µg fluorescein h-1 g-1 soil) and 0.5 µM GR24 treated CR Dhan 204 (8.347 µg fluorescein h-1 g-1 soil) (Table 5; Supplementary Table 1). However, FDA activity in all aerobic rice varieties was lower in the 0.1 µM GR24 treatment, whereas 5.0 µM GR24 showed a higher response to AMF inoculation. Soil dehydrogenase activity (DHA) is frequently used as an indicator of cellular metabolic activity, because it catalyzes the removal of hydrogen atoms from organic molecules. This allowed for the assessment of specific dehydrogenase activities, providing insights into both soil health and microbial cell function (Wolińska and Stępniewska, 2012). Soil microbes and AMF can affect soil dehydrogenase activity by enhancing nutrient cycling and promoting microbial growth (Panneerselvam et al., 2019). According to Raghavendra et al. (2020), sodium alginate with an AMF-based product exhibited the highest dehydrogenase activity (5.12 g TPF produced g-1 soil d-1) after 45 days of growth. The main aim of this study was to understand the effects of AMF intervention with hormonal priming on soil DHA in different rice varieties. The results showed that 5.0 and 10.0 µGR24 treated CR Dhan 207 resulted in higher DHA with and without AMF treatments (Supplementary Table 1). DHA showed an effective response to AMF inoculation in all aerobic rice varieties, as well as Kasalath IC459373 at a lower dose of 0.1 µM GR24 (Table 5).

Table 5.

Strigolactone GR24 effect on soil functional properties viz. MBC, FDA and DHA in different rice varieties with and without application AMF inoculum under P deficient soil.

Treatments Rice varieties MBC (µgg−1 soil)
 FDA (µg fluoresceinh−1 g−1 soil)
 DHA (µgTPFh−1g−1 soil)
With AMF Without AMF With AMF Without AMF With AMF Without AMF
0.1µM GR24 CR Dhan 201 402.596d 385.887d 6.335b 5.097d 21.055b 19.638b
CR Dhan 204 421.499a 402.701b 6.335b 5.039c 21.082b 20.781a
CR Dhan 205 421.488a 404.779ab 7.342a 6.382a 20.236c 18.755c
CR Dhan 207 419.410b 404.789a 6.346b 5.386ab 21.121b 19.708b
IR36 399.503e 382.794e 5.999c 5.375ab 22.226a 20.757ab
Kasalath IC459373 406.468c 389.759c 6.356b 5.325b 21.012b 19.993b
CD(0.05) 0.504 0.514 0.023 0.026 0.285 0.243
0.5µM GR24 CR Dhan 201 432.338c 415.629c 7.349b 6.389b 20.235c 18.739c
CR Dhan 204 461.114b 444.405ab 8.347a 7.287a 21.045b 19.693b
CR Dhan 205 485.086a 468.377a 7.302c 7.142a 21.072b 20.671a
CR Dhan 207 407.851e 391.142b 6.344e 5.384c 18.398d 16.855d
IR36 407.453e 390.744b 6.828d 5.868c 21.345a 19.829b
Kasalath IC459373 414.407d 397.698d 7.349b 6.219b 21.284ab 19.815b
CD(0.05) 1.596 1.369 0.033 0.031 0.272 0.258
1.0µM GR24 CR Dhan 201 434.340b 417.631bc 6.306d 5.413b 22.369b 21.950a
CR Dhan 204 474.153a 457.444a 7.505a 6.478a 23.365a 20.928b
CR Dhan 205 420.780d 404.071d 6.347d 5.387b 20.281e 18.786d
CR Dhan 207 421.775d 405.067d 6.356c 5.462b 21.183d 19.712c
IR36 427.466c 410.757c 7.202c 6.242a 20.288e 18.793d
Kasalath IC459373 411.415e 394.706e 6.344b 5.417b 21.274c 19.805c
CD(0.05) 1.106 1.106 0.027 0.209 0.060 0.048
5.0µM GR24 CR Dhan 201 422.482d 405.773d 6.354e 5.413c 20.280f 18.785e
CR Dhan 204 427.372c 410.663c 6.950d 6.000b 21.236e 19.766d
CR Dhan 205 495.065a 478.356a 7.349b 7.139a 22.370c 20.929c
CR Dhan 207 436.330b 419.621ab 6.191f 5.231c 24.261a 21.921b
IR36 421.675d 404.966d 7.302c 6.311b 21.735d 20.278c
Kasalath IC459373 426.361c 409.652c 8.785a 7.387a 23.337b 22.869a
CD(0.05) 1.414 1.123 0.046 0.049 0.072 0.057
10.0µM GR24 CR Dhan 201 421.500e 409.791d 7.339a 6.383a 25.228f 23.860a
CR Dhan 204 422.495e 405.786e 6.306c 5.316c 23.365e 21.950c
CR Dhan 205 496.150a 479.441a 6.344b 5.384c 24.350c 22.961b
CR Dhan 207 484.076b 467.367ab 7.329a 6.352ab 24.260a 22.868b
IR36 480.509c 463.800c 7.339a 6.169b 21.174d 19.702d
Kasalath IC459373 426.377d 409.668d 6.354b 5.394c 21.183b 19.711d
CD(0.05) 1.755 1.252 0.027 0.053 0.086 0.068
Acetone treated CR Dhan 201 427.373c 410.664c 7.339b 6.381b 20.279a 18.784d
CR Dhan 204 425.491d 408.782d 6.344d 5.383c 20.243d 18.747d
CR Dhan 205 424.385d 407.677cd 8.334a 7.374a 20.241b 18.745d
CR Dhan 207 425.470d 408.761d 6.831c 5.879c 21.274c 19.805c
IR36 480.125b 463.416b 7.339b 6.365ab 23.265e 21.847b
Kasalath IC459373 495.065a 478.356a 6.344d 5.392c 24.261e 22.869a
CD(0.05) 1.613 1.619 0.038 0.041 0.088 0.069
Control CR Dhan 201 390.499e 373.790e 5.935e 4.953c 17.943f 16.388d
CR Dhan 204 399.162d 382.453d 5.999c 5.022ab 19.293d 17.773c
CR Dhan 205 418.339a 401.630a 6.005b 5.012c 19.193e 17.670c
CR Dhan 207 409.453c 392.744c 6.109a 5.149a 20.289b 18.794b
IR36 399.437d 382.728d 5.986d 5.081b 19.930c 18.426b
Kasalath IC459373 417.417b 400.708ab 5.998c 5.029ab 20.884a 19.405a
CD(0.05) 0.557 0.556 0.003 0.083 0.051 0.040
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Different lowercase letters represent significant variations among the treatment at p < 0.05.

3.5. Effect of GR24 priming with and without AMF inoculation on AcP and AkP activity in different rice varieties

Soil phosphatase is an enzyme that catalyzes soil organic phosphate mineralization (Nannipieri et al., 2011), which directly influences the decomposition and transformation of organic phosphate and its bioavailability (Liu et al., 2020). Activity is an indicator of the direction and intensity of soil P biotransformation. Soil phosphatase is influenced by the C, N, and available P content and pH (Wang et al., 2011; DeForest et al., 2012, 2010; Piotrowska-Długosz and Wilczewski, 2014; Hou et al., 2020). This study was conducted to understand how GR24 seed priming, with and without AMF inoculation, affects AcP and AkP activities in different rice varieties under P-deficient conditions. The effects of AcP and AkP activities on GR24 priming, with and without AMF inoculation, varied from variety to variety. However, the activity of AcP showed higher in Kasalath IC459373, CR Dhan 205, CR Dhan 204, and CR Dhan 207 at 0.5, 5.0 and 10.0 µM GR24 priming with AMF inoculation (Table 6; Supplementary Table 1). Kasalath IC459373 treated with 5.0 µM GR24 and AMF showed the highest AkP activity under P-deficient conditions (Table 6; Supplementary Table 1).

Table 6.

Strigolactone GR24 application effect on soil AcP activity in different rice varieties with and without application of AMF under P deficient soil.

Treatments Rice varieties AcP (μg p‐nitrophenol released.g−1 soil h−1)
 AkP (μg p‐nitrophenol releasedg−1 soilh−1)
With AMF Without AMF With AMF Without AMF
0.1µM GR24 CR Dhan 201 28.300b 18.281d 19.263d 18.614b
CR Dhan 204 27.249d 20.195a 21.177a 20.195a
CR Dhan 205 28.254c 18.301d 19.283d 18.635b
CR Dhan 207 29.228a 19.283b 20.265b 19.283b
IR36 27.248d 18.908c 19.890c 19.241b
Kasalath IC459373 28.244c 20.192a 21.174a 20.192a
CD(0.05) 0.037 0.043 0.043 0.758
0.5µM GR24 CR Dhan 201 29.249d 22.244b 23.226b 22.244a
CR Dhan 204 31.107c 23.278a 24.260a 22.945a
CR Dhan 205 29.249d 18.291d 19.273d 18.624b
CR Dhan 207 28.255e 19.293c 20.275c 19.293b
IR36 31.190b 19.307c 20.289c 19.173b
Kasalath IC459373 32.232a 19.309c 20.624c 19.309b
CD(0.05) 0.076 0.099 0.422 0.901
1.0µM GR24 CR Dhan 201 33.131a 20.192d 21.174d 20.192c
CR Dhan 204 29.239c 21.267c 22.249c 20.600c
CR Dhan 205 27.249d 18.303e 19.285e 18.636d
CR Dhan 207 29.226c 22.285b 23.267b 21.952b
IR36 31.130b 20.271d 21.253d 20.605c
Kasalath IC459373 29.228c 23.281a 24.262a 23.281a
CD(0.05) 0.101 0.087 0.087 1.147
5.0µM GR24 CR Dhan 201 28.243e 23.456b 24.438b 23.457b
CR Dhan 204 31.207b 20.192d 21.174d 21.092cd
CR Dhan 205 33.120a 19.293e 20.275e 19.293e
CR Dhan 207 31.229b 22.285c 23.267c 21.952c
IR36 29.239d 20.255d 21.237d 20.255d
Kasalath IC459373 30.244c 24.273a 25.255a 24.273a
CD(0.05) 0.085 0.100 0.100 0.816
10.0µM GR24 CR Dhan 201 31.229c 19.296d 20.278d 19.629c
CR Dhan 204 33.197a 20.292c 21.274c 20.292bc
CR Dhan 205 31.786b 23.259a 24.241a 22.925a
CR Dhan 207 30.244d 22.283b 23.266b 22.284a
IR36 29.249e 20.292c 21.274c 20.959b
Kasalath IC459373 30.244d 18.261e 19.243e 18.261d
CD(0.05) 0.070 0.093 0.093 0.739
Acetone treated CR Dhan 201 32.203d 19.309d 20.291d 19.643c
CR Dhan 204 33.817b 20.292c 21.274c 20.625bc
CR Dhan 205 33.341c 21.351b 22.333b 21.351ab
CR Dhan 207 39.302a 19.309d 20.291d 19.643c
IR36 29.349f 20.302c 21.284c 20.302bc
Kasalath IC459373 31.230e 23.739a 24.720a 22.739a
CD(0.05) 0.169 0.083 0.083 1.476
Control CR Dhan 201 29.199 a 17.292 c 18.274c 17.292
CR Dhan 204 23.221d 18.301b 19.283b 18.968
CR Dhan 205 28.198b 18.311b 19.293b 18.644
CR Dhan 207 26.240c 19.310a 20.292a 19.310
IR36 21.173e 16.914d 17.896d 18.247
Kasalath IC459373 29.199a 19.309a 20.291a 19.309
CD(0.05) 0.167 0.05 0.05 NS
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Different lowercase letters represent significant variations among the treatment at p < 0.05.

3.6. Effect of strigolactone GR24 priming with and without AMF inoculation on chlorophyll (SPAD), tiller number and leaf number in different rice varieties

Strigolactones are a group of phytohormones that play critical roles in plant structures. The effect of SL GR24 application in different crops has been reported by several researchers (Sedaghat et al., 2021; Sun et al., 2022; Ma et al., 2022; Ahsan et al., 2022), however, the interesting work by Yamada et al. (2014) reported the effect of SL-GR24 hormones that inhibit shoot branching and stimulate secondary stem growth, primary root growth, and root hair elongation in P-deficient soil; however, the chlorophyll levels did not differ between the sufficient and deficient phosphate conditions in the wild-type plants, but increased in the SL-deficient mutants, leading to strong promotion of leaf senescence by GR24 treatment. These results suggested that the mutants exhibited increased responsiveness to GR24 under phosphate deficiency. Furthermore, GR24 accelerated leaf senescence in both intact SL-deficient mutants and dark-induced leaf senescence under phosphate deficiency. Similarly, Krasylenko et al. (2021) conducted an experiment to understand the stimulation of both the SL and karrikin signaling pathways; 3 μM and 25 μM synthetic rac-GR24 were used to induce different physiological responses in Arabidopsis. The relationship between GR24-dependent inhibition of hypocotyl elongation and changes in cortical microtubule organization and dynamics was discovered in living wild-type and max2–1 seedlings that stably expressed genetically encoded fluorescent molecular markers for microtubules. The quantitative evaluation of microscopic datasets revealed that the chemical and/or genetic manipulation of strigolactone signaling impacted microtubule remodeling, especially under light conditions. Interestingly, the application of GR24 in dark conditions partially alleviated cytoskeletal rearrangement, suggesting a new mechanistic connection between cytoskeletal behavior and the light-dependent nature of strigolactone signaling. The analog GR24 (0, 0.5, 1, 2, 4, and 8 µM) has been studied in Artemisia annua, and 4 µM GR24 was found to be the most effective in promoting growth, photosynthesis, and other physiological indices (Wani et al., 2023). In another study, four SL GR24 levels (water, 0.001, 0.01, and 0.1 mg L-1) were applied as seed treatment, and the results showed an increase in chlorophyll fluorescence in wheat, and application of GR24 (5 and 10 µM) in Triticum aestivum L. cv. Sirvan increases photosynthesis and yield under drought stress (Sedaghat et al., 2021). Ali et al. (2021) reported that exposure to penoxsulam (PXL) and bensulfuron-methyl (BSM) significantly reduced cellular damage in both the roots and leaves of watermelon seedlings when GR24 was applied at concentrations of 0, 1, and 5 µM+ half-strength Hoagland solution. In our study, SL GR24 application with AMF in different aerobic rice varieties indicated that seed priming with 5 and 10.0 µM SL GR24 significantly increased chlorophyll (SPAD) and leaf numbers in most of selected aerobic rice varieties (Fig. 3). Fig. 4 shows the application of 5.0 µM GR24 enhanced the tiller number and suppressed outgrowth. 5.0 µM GR24 performed better in CR Dhan 207 for the enhancement of chlorophyll and the highest leaf number in CR Dhan 201, whereas in Kasalath IC459373, a significant improvement in leaf number at 10.0 µM GR24 treatment (Fig. 5).

Fig. 3.

Fig 3

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Strigolactone GR24 application effect on chlorophyll (SPAD) in different rice varieties. [T1: 0.1 µM GR24, T2: 0.5 µM GR24, T3: 1.0 µM GR24, T4: 5.0 µM GR24, T5: 10.0 µM GR24, T6: acetone treated, T7: Control, AMF (-): without AMF, AMF (+): with AMF].

Fig. 4.

Fig 4

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AMF intervention with GR24 seed priming enhanced rice tiller number under low P accessible soil.

Fig. 5.

Fig 5

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Strigolactone GR24 application effect on leaf number in different rice varieties. [T1: 0.1 µM GR24, T2: 0.5 µM GR24, T3: 1.0 µM GR24, T4: 5.0 µM GR24, T5: 10.0 µM GR24, T6: acetone treated, T7: Control, AMF (-): without AMF, AMF (+): with AMF].

4. Conclusions

The research aimed to investigate the effects of strigolactone GR24 on plant growth and development using different concentrations of GR24 (0.1, 0.5, 1.0, 5.0, and 10.0 µM) in the presence or absence of arbuscular mycorrhizal fungi (AMF) in selected rice varieties (CR Dhan 201, CR Dhan 204, CR Dhan 205, and CR Dhan 207), Kasalath-IC459373 (P-tolerant check), and IR-36 (P-susceptible check) under P-deficient conditions. Findings of the research showed that priming seeds with 5.0 µM SL GR24 improved the performance of mycorrhization in CR Dhan 205, followed by CR Dhan 204 and 207, and increased the sporulation of AMF in CR Dhan 201, as well as rice growth. AMF treated with 5.0 µM SL GR24, such as CR Dhan 205, followed by CR Dhan 207 and 204, showed the best performance in plant growth, chlorophyll content, and soil functional properties, including acid and alkaline phosphatase activity, soil microbial biomass carbon (MBC), dehydrogenase activity (DHA), and fluorescein diacetate activity (FDA). The AMF intervention with SL GR24 led to a significant increase in plant growth, soil enzyme activity, and P uptake compared to the control group. In P-deficient conditions, seed priming with 5.0 µM strigolactone GR24 and AMF inoculum significantly enhanced the growth, P uptake, and soil enzyme activities of selected aerobic rice varieties. The application of SL formulations in selected aerobic rice varieties, CR Dhan 207, CR Dhan 204, and CR Dhan 205, can promote mycorrhization and enhance P utilization under P-deficient conditions, leading to improved rice growth.

CRediT authorship contribution statement

D.M., A.S., A.P. and P.P. were involved in the sampling, analysis, visualization and manuscript writing; P.P., P.C. A.K.N. and P.K.D.M. were involved in manuscript refinement, supervision and important intellectual content discussion.

Declaration of competing interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgments

The authors are thankful to Hon'ble Director, ICAR – National Rice Research Institute, India; Hon'ble Vice-Chancellor, Raiganj University, India; Department of Biotechnology, Government of India (BT/PR36476/ NNT/28/1723/2020); and Project no 2.7 (ICAR-NRRI, Cuttack) for support. The authors wish to extend special thanks to Dr. A. Anandan, Principal Scientist (Genetics and Plant Breeding), ICAR-NRRI, and Cuttack for providing seeds and support for this experiment. The research article is a part of Mr. Debasis Mitra's Ph.D. research program, which was supervised by Dr. P. Panneerselvam, Principal Scientist, CPD, ICAR-NRRI, Cuttack, and Dr. Pradeep K. Das Mohapatra, Associate Professor and Head, Department of Microbiology, Raiganj University, India.

Footnotes

Supplementary material associated with this article can be found, in the online version, at doi:10.1016/j.crmicr.2024.100229.

Contributor Information

Periyasamy Panneerselvam, Email: panneerselvam.p@icar.gov.in.

Pradeep Kumar Das Mohapatra, Email: pkdmvu@gmail.com.

Appendix. Supplementary materials

mmc1.docx (26KB, docx)

Data availability

  • Data will be made available on request.

References

  1. Adam G., Duncan H. Development of a sensitive and rapid method for the measurement of total microbial activity using fluorescein diacetate (FDA) in a range of soils. Soil Biol. Biochem. 2001;33(7–8):943–951. [Google Scholar]
  2. Agusti J., Herold S., Schwarz M., Sanchez P., Ljung K., Dun E.A., Brewer P.B., Beveridge C.A., Sieberer T., Sehr E.M., Greb T. Strigolactone signaling is required for auxin-dependent stimulation of secondary growth in plants. Proc. Natl Acad. Sci. 2011;108(50):20242–20247. doi: 10.1073/pnas.1111902108. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Ahsan M., Zulfiqar H., Farooq M.A., Ali S., Tufail A., Kanwal S., Shaheen M.R., Sajid M., Gul H., Jamal A., Saeed M.F. Strigolactone (GR24) Application positively regulates photosynthetic attributes, stress-related metabolites and antioxidant enzymatic activities of ornamental sunflower (Helianthus annuus cv. Vincent's Choice) under salinity stress. Agriculture. 2022;13(1):50. [Google Scholar]
  4. Akiyama K., Matsuzaki K.I., Hayashi H. Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature. 2005;435(7043):824–827. doi: 10.1038/nature03608. [DOI] [PubMed] [Google Scholar]
  5. Ali A., Malangisha G.K., Yang H., Li C., Wang C., Yang Y., Mahmoud A., Khan J., Yang J., Hu Z., Zhang M. Strigolactone alleviates herbicide toxicity via maintaining antioxidant homeostasis in watermelon (Citrullus lanatus) Agriculture. 2021;11(5):419. [Google Scholar]
  6. Alvi A.F., Sehar Z., Fatma M., Masood A., Khan N.A. Strigolactone: an emerging growth regulator for developing resilience in plants. Plants. 2022;11(19):2604. doi: 10.3390/plants11192604. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Andreo-Jimenez B., Ruyter-Spira C., Bouwmeester H.J., Lopez-Raez J.A. Ecological relevance of strigolactones in nutrient uptake and other abiotic stresses, and in plant-microbe interactions below-ground. Plant Soil. 2015;394:1–19. [Google Scholar]
  8. Arite T., Kameoka H., Kyozuka J. Strigolactone positively controls crown root elongation in rice. J. Plant Growth Regul. 2012;31:165–172. [Google Scholar]
  9. Arrhenius O. Phosphorus determination by the molybdenum blue method. Archive Suikerind. 1927;35:903–911. [Google Scholar]
  10. Babur E., Dindaroglu T. Seasonal changes of soil organic carbon and microbial biomass carbon in different forest ecosystems. Environ. Factors Affect. Hum. Health. 2020;1:1–21. [Google Scholar]
  11. Begum N., Qin C., Ashraf M., Zhang L. Role of arbuscular mycorrhizal fungi in plant growth regulation: implications in abiotic stress tolerance. Front. Plant Sci. 2019;10 doi: 10.3389/fpls.2019.01068. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Besserer A., Puech-Pagès V., Kiefer P., Gomez-Roldan V., Jauneau A., Roy S., Portais J.C., Roux C., Bécard G., Séjalon-Delmas N. Strigolactones stimulate arbuscular mycorrhizal fungi by activating mitochondria. PLoS Biol. 2006;4(7):e226. doi: 10.1371/journal.pbio.0040226. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Borghi L., Screpanti C., Lumbroso A., Lachia M., Gübeli C., De Mesmaeker A. Efficiency and bioavailability of new synthetic strigolactone mimics with potential for sustainable agronomical applications. Plant Soil. 2021;465(1–2):109–123. [Google Scholar]
  14. Bouwmeester H.J., Roux C., Lopez-Raez J.A., Becard G. Rhizosphere communication of plants, parasitic plants and AM fungi. Trends Plant Sci. 2007;12(5):224–230. doi: 10.1016/j.tplants.2007.03.009. [DOI] [PubMed] [Google Scholar]
  15. Casida L.E., Jr, Klein D.A., Santoro T. Soil dehydrogenase activity. Soil Sci. 1964;98(6):371–376. 1. [Google Scholar]
  16. Czarnecki O., Yang J., Weston D.J., Tuskan G.A., Chen J.G. A dual role of strigolactones in phosphate acquisition and utilization in plants. Int. J. Mol. Sci. 2013;14(4):7681–7701. doi: 10.3390/ijms14047681. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. De Cuyper C., Goormachtig S. Strigolactones in the rhizosphere: friend or foe? Mol. Plant-Microbe Inter. 2017;30(9):683–690. doi: 10.1094/MPMI-02-17-0051-CR. [DOI] [PubMed] [Google Scholar]
  18. De Cuyper C., Fromentin J., Yocgo R.E., De Keyser A., Guillotin B., Kunert K., Boyer F.D., Goormachtig S. From lateral root density to nodule number, the strigolactone analogue GR24 shapes the root architecture of Medicago truncatula. J. Exp. Bot. 2015;66(1):137–146. doi: 10.1093/jxb/eru404. [DOI] [PubMed] [Google Scholar]
  19. Mitra D., BE G.S., Khoshru B., De Los Santos Villalobos S., Belz C., Chaudhary P., Shahri F.N., Djebaili R., Adeyemi N.O., El-Ballat E.M., El-Esawi M.A. Impacts of arbuscular mycorrhizal fungi on rice growth, development, and stress management with a particular emphasis on strigolactone effects on root development. Commun. Soil Sci. Plant Anal. 2021;52(14):1591–1621. [Google Scholar]
  20. DeForest J.L., Scott L.G. Available organic soil phosphorus has an important influence on microbial community composition. Soil Sci. Soc. Am. J. 2010;74(6):2059–2066. [Google Scholar]
  21. DeForest J.L., Smemo K.A., Burke D.J., Elliott H.L., Becker J.C. Soil microbial responses to elevated phosphorus and pH in acidic temperate deciduous forests. Biogeochemistry. 2012;109:189–202. [Google Scholar]
  22. Devika O.S., Singh S., Sarkar D., Barnwal P., Suman J., Rakshit A. Seed priming: a potential supplement in integrated resource management under fragile intensive ecosystems. Front. Sustain. Food Syst. 2021;5 [Google Scholar]
  23. Etesami H., Jeong B.R., Glick B.R. Contribution of arbuscular mycorrhizal fungi, phosphate–solubilizing bacteria, and silicon to P uptake by plant. Front. Plant Sci. 2021;12 doi: 10.3389/fpls.2021.699618. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Foo E. Strigolactones: Methods and Protocols (pp. 179-187) New York, NY: Springer US; 2021. Application of strigolactones to plant roots to influence formation of symbioses. [DOI] [PubMed] [Google Scholar]
  25. Ganeshamurthy A.N., Sharma K., Mitra D., Radha T.K., Rupa T.R. Isolation and characterization of Arbuscular mycorrhizal fungi and their role in plants growing under harsh environments. Mycorrhiza News - mycorrhizae (TERI) 2017;29(3):7–12. [Google Scholar]
  26. Hou Q., Wang W., Yang Y., Hu J., Bian C., Jin L., Li G., Xiong X. Rhizosphere microbial diversity and community dynamics during potato cultivation. Eur. J. Soil Biol. 2020;98 [Google Scholar]
  27. Ibrahim M.S., Moses N., Ikhajiagbe B. new perspectives and applications; 2022. Seed Priming With phytohormones. Plant hormones-Recent Advances. [Google Scholar]
  28. Jabborova D., Annapurna K., Al-Sadi A.M., Alharbi S.A., Datta R., Zuan A.T.K. Biochar and Arbuscular mycorrhizal fungi mediated enhanced drought tolerance in Okra (Abelmoschus esculentus) plant growth, root morphological traits and physiological properties. Saudi J. Biol. Sci. 2021;28(10):5490–5499. doi: 10.1016/j.sjbs.2021.08.016. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Jia K.P., Li C., Bouwmeester H.J., Al-Babili S. Strigolactone biosynthesis and signal transduction. Strigolactones-biol. Appl. 2019:1–45. [Google Scholar]
  30. Jiu S., Xu Y., Wang J., Haider M.S., Xu J., Wang L., Wang S., Li J., Liu X., Sun W., Xu W. Molecular mechanisms underlying the action of strigolactones involved in grapevine root development by interacting with other phytohormone signaling. Sci. Hortic. 2022;293 [Google Scholar]
  31. Kaniganti S., Bhattacharya J., Petla B.P., Reddy P.S. Strigolactone, a neglected plant hormone, with a great potential for crop improvement: crosstalk with other plant hormones. Environ. Exp. Bot. 2022;204 [Google Scholar]
  32. Kapulnik Y., Resnick N., Mayzlish-Gati E., Kaplan Y., Wininger S., Hershenhorn J., Koltai H. Strigolactones interact with ethylene and auxin in regulating root-hair elongation in Arabidopsis. J. Exp. Bot. 2011;62(8):2915–2924. doi: 10.1093/jxb/erq464. [DOI] [PubMed] [Google Scholar]
  33. Kee Y.J., Ogawa S., Ichihashi Y., Shirasu K., Yoshida S. Strigolactones in rhizosphere communication: multiple molecules with diverse functions. Plant Cell Physiol. 2023:pcad055. doi: 10.1093/pcp/pcad055. [DOI] [PubMed] [Google Scholar]
  34. Kgosi R.L., Zwanenburg B., Mwakaboko A.S., Murdoch A.J. Strigolactone analogues induce suicidal seed germination of Striga spp. in soil. Weed Res. 2012;52(3):197–203. [Google Scholar]
  35. Khuvung K., Silva Gutierrez F.A., Reinhardt D. How strigolactone shapes shoot architecture. Front. Plant Sci. 2022;13 doi: 10.3389/fpls.2022.889045. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Kim B., Westerhuis J.A., Smilde A.K., Floková K., Suleiman A.K., Kuramae E.E., Bouwmeester H.J., Zancarini A. Effect of strigolactones on recruitment of the rice root-associated microbiome. FEMS Microbiol. Ecol. 2022;98(2):fiac010. doi: 10.1093/femsec/fiac010. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Kountche B.A., Novero M., Jamil M., Asami T., Bonfante P., Al-Babili S. Effect of the strigolactone analogs methyl phenlactonoates on spore germination and root colonization of arbuscular mycorrhizal fungi. Heliyon. 2018;4(11) doi: 10.1016/j.heliyon.2018.e00936. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Kowalczyk A., Hrynkiewicz K. Strigolactones as mediators between fungi and plants. Acta Mycol. 2018;53(2) [Google Scholar]
  39. Krasylenko Y., Komis G., Hlynska S., Vavrdová T., Ovečka M., Pospíšil T., Šamaj J. GR24, a synthetic strigolactone analog, and light affect the organization of cortical microtubules in Arabidopsis hypocotyl cells. Front. Plant Sci. 2021;12 doi: 10.3389/fpls.2021.675981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Lachia M., Jung P.M., De Mesmaeker A. A novel approach toward the synthesis of strigolactones through intramolecular [2+ 2] cycloaddition of ketenes and ketene-iminiums to olefins. Application to the asymmetric synthesis of GR-24. Tetrahedron Lett. 2012;53(34):4514–4517. [Google Scholar]
  41. Lanfranco L., Fiorilli V., Venice F., Bonfante P. Strigolactones cross the kingdoms: plants, fungi, and bacteria in the arbuscular mycorrhizal symbiosis. J. Exp. Bot. 2018;69(9):2175–2188. doi: 10.1093/jxb/erx432. [DOI] [PubMed] [Google Scholar]
  42. Liu B., Wang S., Wang J., Zhang X., Shen Z., Shi L., Chen Y. The great potential for phytoremediation of abandoned tailings pond using ectomycorrhizal Pinus sylvestris. Sci. Total Environ. 2020;719 doi: 10.1016/j.scitotenv.2020.137475. [DOI] [PubMed] [Google Scholar]
  43. Lopez-Obando M., Ligerot Y., Bonhomme S., Boyer F.D., Rameau C. Strigolactone biosynthesis and signaling in plant development. Development. 2015;142(21):3615–3619. doi: 10.1242/dev.120006. [DOI] [PubMed] [Google Scholar]
  44. López-Ráez J.A., Pozo M.J., García-Garrido J.M. Strigolactones: a cry for help in the rhizosphere. Botany. 2011;89(8):513–522. [Google Scholar]
  45. Ma Q., Lin X., Zhan M., Chen Z., Wang H., Yao F., Chen J. Effect of an exogenous strigolactone GR24 on the antioxidant capacity and quality deterioration in postharvest sweet orange fruit stored at ambient temperature. Int. J. Food Sci. Technol. 2022;57(1):619–630. [Google Scholar]
  46. Makhzoum A., Yousefzadi M., Malik S., Gantet P., Tremouillaux-Guiller J. Strigolactone biology: genes, functional genomics, epigenetics and applications. Crit. Rev. Biotechnol. 2017;37(2):151–162. doi: 10.3109/07388551.2015.1121967. [DOI] [PubMed] [Google Scholar]
  47. Marro N., Lidoy J., Chico M.Á., Rial C., García J., Varela R.M., Macías F.A., Pozo M.J., Janoušková M., López-Ráez J.A. Strigolactones: new players in the nitrogen–phosphorus signalling interplay. Plant Cell Environ. 2022;45(2):512–527. doi: 10.1111/pce.14212. [DOI] [PubMed] [Google Scholar]
  48. Marzec M., Muszynska A., Gruszka D. The role of strigolactones in nutrient-stress responses in plants. Int. J. Mol. Sci. 2013;14(5):9286–9304. doi: 10.3390/ijms14059286. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. McGonigle T.P., Miller M.H., Evans D.G., Fairchild G.L., Swan J.A. A new method which gives an objective measure of colonization of roots by vesicular—Arbuscular mycorrhizal fungi. New Phytol. 1990;115(3):495–501. doi: 10.1111/j.1469-8137.1990.tb00476.x. [DOI] [PubMed] [Google Scholar]
  50. Mishra S., Upadhyay S., Shukla R.K. The role of strigolactones and their potential cross-talk under hostile ecological conditions in plants. Front. Physiol. 2017;7:691. doi: 10.3389/fphys.2016.00691. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Mitra D., Djebaili R., Pellegrini M., Mahakur B., Sarker A., Chaudhary P., Khoshru B., Gallo M.D., Kitouni M., Barik D.P., Panneerselvam P. Arbuscular mycorrhizal symbiosis: plant growth improvement and induction of resistance under stressful conditions. J. Plant Nutr. 2021;44(13):1993–2028. [Google Scholar]
  52. Mitra D., Pellegrini M., Olatunbosun A.N., Mondal R., Del Gallo M., Chattaraj S., Chakroborty D., Priyadarshini A., Khoshru B., Sierra B.G., de los Santos-Villalobos S. Microbial Inoculants. Academic Press; 2023. Seed priming with microbial inoculants for enhanced crop yield; pp. 99–123. [Google Scholar]
  53. Mitra D., Rad K.V., Chaudhary P., Ruparelia J., Sagarika M.S., Boutaj H., Mohapatra P.K.D., Panneerselvam P. Involvement of strigolactone hormone in root development, influence and interaction with mycorrhizal fungi in plant: mini-review. Curr. Res. Microb. Sci. 2021;2 doi: 10.1016/j.crmicr.2021.100026. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. Moscatiello R., Squartini A., Mariani P., Navazio L. Flavonoid‐induced calcium signalling in Rhizobium leguminosarum bv. viciae. New Phytol. 2010;188(3):814–823. doi: 10.1111/j.1469-8137.2010.03411.x. [DOI] [PubMed] [Google Scholar]
  55. Nannipieri P., Giagnoni L., Landi L., Renella G. Role of phosphatase enzymes in soil. Phos. Action Biol. Process. Soil Phos. Cycl. 2011:215–243. [Google Scholar]
  56. Nayak A.K., Bhattacharya P., Shahid M., Tripathi R. KALYANI Publisher; India: 2016. Modern Techniques in Soil and Plant Analysis; p. 272. [Google Scholar]
  57. Pandya-Kumar N., Shema R., Kumar M., Mayzlish-Gati E., Levy D., Zemach H., Belausov E., Wininger S., Abu-Abied M., Kapulnik Y., Koltai H. Strigolactone analog GR 24 triggers changes in PIN 2 polarity, vesicle trafficking and actin filament architecture. New Phytol. 2014;202(4):1184–1196. doi: 10.1111/nph.12744. [DOI] [PubMed] [Google Scholar]
  58. Panneerselvam P., Sahoo S., Senapati A., Kumar U., Mitra D., Parameswaran C., Anandan A., Kumar A., Jahan A., Nayak A.K. Understanding interaction effect of arbuscular mycorrhizal fungi in rice under elevated carbon dioxide conditions. J. Basic Microbiol. 2019;59(12):1217–1228. doi: 10.1002/jobm.201900294. [DOI] [PubMed] [Google Scholar]
  59. Patle P.N., Navnage N.P., Barange P.K. Fluorescein diacetate (FDA): measure of total microbial activity and as indicator of soil quality. Int. J. Curr. Microbiol. Appl. Sci. 2018;7:2103–2107. [Google Scholar]
  60. Paul A., Mondal S., Pal A., Biswas S., Chakraborty K., Mazumder A., Biswas A.K., Kundu R. Seed priming with NaCl helps to improve tissue tolerance, potassium retention ability of plants, and protects the photosynthetic ability in two different legumes, chickpea and lentil, under salt stress. Planta. 2023;257(6):111. doi: 10.1007/s00425-023-04150-y. [DOI] [PubMed] [Google Scholar]
  61. Perner H., Schwarz D., Bruns C., Mäder P., George E. Effect of arbuscular mycorrhizal colonization and two levels of compost supply on nutrient uptake and flowering of pelargonium plants. Mycorrhiza. 2007;17:469–474. doi: 10.1007/s00572-007-0116-7. [DOI] [PubMed] [Google Scholar]
  62. Phillips J.M., Hayman D.S. Improved procedures for clearing roots and staining parasitic and vesicular-arbuscular mycor-rhizal fungi for rapid assessment of infection. Trans. Br. Mycol. Soc. 1970;55(1):158–IN18. [Google Scholar]
  63. Piotrowska-Długosz A., Wilczewski E. Soil phosphatase activity and phosphorus content as influenced by catch crops cultivated as green manure. Polish J. Environ. Stud. 2014;23(1) [Google Scholar]
  64. Raghavendra K.S., Nirmalnath P.J., Jagadeesh K.S., Chandranath H.T., Chandrasekhar S.S. Evaluation of AMF formulations on growth, root colonization and biophysical parameters of maize (Zea mays L.) IJCS. 2020;8(2):1394–1403. [Google Scholar]
  65. Rhaman M.S., Imran S., Rauf F., Khatun M., Baskin C.C., Murata Y., Hasanuzzaman M. Seed priming with phytohormones: an effective approach for the mitigation of abiotic stress. Plants. 2020;10(1):37. doi: 10.3390/plants10010037. [DOI] [PMC free article] [PubMed] [Google Scholar]
  66. Ruyter-Spira C., Kohlen W., Charnikhova T., van Zeijl A., van Bezouwen L., De Ruijter N., Cardoso C., Lopez-Raez J.A., Matusova R., Bours R., Verstappen F. Physiological effects of the synthetic strigolactone analog GR24 on root system architecture in Arabidopsis: another belowground role for strigolactones? Plant Physiol. 2011;155(2):721–734. doi: 10.1104/pp.110.166645. [DOI] [PMC free article] [PubMed] [Google Scholar]
  67. Salmeron-Santiago I.A., Martínez-Trujillo M., Valdez-Alarcón J.J., Pedraza-Santos M.E., Santoyo G., Pozo M.J., Chávez-Bárcenas A.T. An updated review on the modulation of carbon partitioning and allocation in arbuscular mycorrhizal plants. Microorganisms. 2021;10(1):75. doi: 10.3390/microorganisms10010075. [DOI] [PMC free article] [PubMed] [Google Scholar]
  68. Schnrer J., Rosswall T. Fluorescein diacetate hydrolysis as a measure of total microbial activity in soil and litter. Appl. Environ. Microbiol. 1982;43(6):1256–1261. doi: 10.1128/aem.43.6.1256-1261.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  69. Schumacher B.A. United States Environmental Protection Agency Environmental Sciences Division National Exposure Research Laboratory P.O. Box 93478 Las Vegas,NV; 2002. Methods For the Determination of Total Organic Carbon (TOC) in Soils and Sediments. 89193-3478. [Google Scholar]
  70. Schütz L., Saharan K., Mäder P., Boller T., Mathimaran N. Rate of hyphal spread of arbuscular mycorrhizal fungi from pigeon pea to finger millet and their contribution to plant growth and nutrient uptake in experimental microcosms. Appl. Soil Ecol. 2022;169 [Google Scholar]
  71. Sedaghat M., Emam Y., Mokhtassi-Bidgoli A., Hazrati S., Lovisolo C., Visentin I., Cardinale F., Tahmasebi-Sarvestani Z. The potential of the synthetic strigolactone analogue GR24 for the maintenance of photosynthesis and yield in winter wheat under drought: investigations on the mechanisms of action and delivery modes. Plants. 2021;10(6):1223. doi: 10.3390/plants10061223. [DOI] [PMC free article] [PubMed] [Google Scholar]
  72. Shen Y., Zhang F., Yang Y., Lu G., Yang X. Arbuscular mycorrhizal fungi alter plant N and P resorption of dominant species in a degraded grassland of northern China. Ecol. Indic. 2023;150 [Google Scholar]
  73. Shinohara N., Taylor C., Leyser O. Strigolactone can promote or inhibit shoot branching by triggering rapid depletion of the auxin efflux protein PIN1 from the plasma membrane. PLoS Biol. 2013;11(1) doi: 10.1371/journal.pbio.1001474. [DOI] [PMC free article] [PubMed] [Google Scholar]
  74. Silva A.M., Jones D.L., Chadwick D.R., Qi X., Cotta S.R., Araújo V.L., Matteoli F.P., Lacerda-Júnior G.V., Pereira A.P., Fernandes-Júnior P.I., Cardoso E.J. Can arbuscular mycorrhizal fungi and rhizobacteria facilitate 33P uptake in maize plants under water stress? Microbiol. Res. 2023;271 doi: 10.1016/j.micres.2023.127350. [DOI] [PubMed] [Google Scholar]
  75. Smith S.M. QandA: what are strigolactones and why are they important to plants and soil microbes? BMC Biol. 2014;12:1–7. doi: 10.1186/1741-7007-12-19. [DOI] [PMC free article] [PubMed] [Google Scholar]
  76. Soliman S., Wang Y., Han Z., Pervaiz T., El-Kereamy A. Strigolactones in plants and their interaction with the ecological microbiome in response to abiotic stress. Plants, 2022;11(24):3499. doi: 10.3390/plants11243499. [DOI] [PMC free article] [PubMed] [Google Scholar]
  77. Soto M.J., Fernández-Aparicio M., Castellanos-Morales V., García-Garrido J.M., Ocampo J.A., Delgado M.J., Vierheilig H. First indications for the involvement of strigolactones on nodule formation in alfalfa (Medicago sativa) Soil Biol. Biochem. 2010;42(2):383–385. [Google Scholar]
  78. Sun H., Guo X., Qi X., Feng F., Xie X., Zhang Y., Zhao Q. SPL14/17 act downstream of strigolactone signalling to modulate rice root elongation in response to nitrate supply. The Plant J. 2021;106(3):649–660. doi: 10.1111/tpj.15188. [DOI] [PubMed] [Google Scholar]
  79. Sun H., Li W., Burritt D.J., Tian H., Zhang H., Liang X., Miao Y., Mostofa M.G., Tran L.S.P. Strigolactones interact with other phytohormones to modulate plant root growth and development. The Crop J. 2022;10(6):1517–1527. [Google Scholar]
  80. Tabatabai M.A., Bremner J.M. Use of p-nitrophenyl phosphate for assay of soil phosphatase activity. Soil Biol. Biochem. 1969;1(4):301–307. [Google Scholar]
  81. Team R.C. Vol. 3. Austria: R foundation for statistical computing; Vienna: 2000. (R Language Definition). [Google Scholar]
  82. Vance E.D., Brookes P.C., Jenkinson D.S. An extraction method for measuring soil microbial biomass C. Soil Biol. Biochem. 1987;19(6):703–707. [Google Scholar]
  83. Vurro M., Prandi C., Baroccio F. Strigolactones: how far is their commercial use for agricultural purposes? Pest Manag. Sci. 2016;72(11):2026–2034. doi: 10.1002/ps.4254. [DOI] [PubMed] [Google Scholar]
  84. Wang D.W., Xi Z. Advanced Agrochem; 2022. Strigolactone Agonists/Antagonists For Agricultural applications: New opportunities. [Google Scholar]
  85. Wang J.B., Chen Z.H., Chen L.J., Zhu A.N., Wu Z.J. Surface soil phosphorus and phosphatase activities affected by tillage and crop residue input amounts. Plant Soil Environ. 2011;57(6):251–257. [Google Scholar]
  86. Wani K.I., Zehra A., Choudhary S., Naeem M., Khan M.M.A., Khan R., Aftab T. Exogenous strigolactone (GR24) positively regulates growth, photosynthesis, and improves glandular trichome attributes for enhanced artemisinin production in Artemisia annua. J. Plant Growth Regul. 2023;42(8):4606–4615. doi: 10.1007/s00344-022-10654-w. [DOI] [PMC free article] [PubMed] [Google Scholar]
  87. Wei L., Ge T., Zhu Z., Ye R., Penuelas J., Li Y., Lynn T.M., Jones D.L., Wu J., Kuzyakov Y. Paddy soils have a much higher microbial biomass content than upland soils: a review of the origin, mechanisms, and drivers. Agric. Ecosyst. Environ. 2022;326 [Google Scholar]
  88. Wigchert S.C.M., Kuiper E., Boelhouwer G.J., Nefkens G.H.L., Verkleij J.A.C., Zwanenburg B. Dose− response of seeds of the parasitic weeds Striga and Orobanche toward the synthetic germination stimulants GR 24 and Nijmegen 1. J. Agric. Food Chem. 1999;47(4):1705–1710. doi: 10.1021/jf981006z. [DOI] [PubMed] [Google Scholar]
  89. Witt C., Gaunt J.L., Galicia C.C., Ottow J.C., Neue H.U. A rapid chloroform-fumigation extraction method for measuring soil microbial biomass carbon and nitrogen in flooded rice soils. Biol. Fertil. Soils. 2000;30:510–519. [Google Scholar]
  90. Wolińska A., Stępniewska Z. Dehydrogenase activity in the soil environment. Dehydrogenases, 2012;10:183–210. [Google Scholar]
  91. Xie X., Yoneyama K., Kisugi T., Uchida K., Ito S., Akiyama K., Hayashi H., Yokota T., Nomura T., Yoneyama K. Confirming stereochemical structures of strigolactones produced by rice and tobacco. Mol. Plant. 2013;6(1):153–163. doi: 10.1093/mp/sss139. [DOI] [PMC free article] [PubMed] [Google Scholar]
  92. Yamada Y., Furusawa S., Nagasaka S., Shimomura K., Yamaguchi S., Umehara M. Strigolactone signaling regulates rice leaf senescence in response to a phosphate deficiency. Planta. 2014;240:399–408. doi: 10.1007/s00425-014-2096-0. [DOI] [PubMed] [Google Scholar]
  93. Yoneyama K. How do strigolactones ameliorate nutrient deficiencies in plants? Cold Spring Harb. Perspect. Biol. 2019;11(8) doi: 10.1101/cshperspect.a034686. [DOI] [PMC free article] [PubMed] [Google Scholar]
  94. Zwanenburg B., Pospíšil T. Structure and activity of strigolactones: new plant hormones with a rich future. Mol. Plant. 2013;6(1):38–62. doi: 10.1093/mp/sss141. [DOI] [PubMed] [Google Scholar]

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