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Article

Effects of Arbuscular Mycorrhizal Fungi on Growth and Nutrient Accumulation of Oat under Drought Conditions

by
Haoqi Tian
1,
Zhifeng Jia
1,
Wenhui Liu
1,
Xiaoxin Wei
1,
Hui Wang
2,
Gensheng Bao
1,
Jin Li
1 and
Qingping Zhou
2,*
1
Key Laboratory of Superior Forage Germplasm in the Qinghai-Tibetan Plateau, Qinghai Academy of Animal Science and Veterinary Medicine, Qinghai University, Xining 810016, China
2
Sichuan Zoige Alpine Wetland Ecosystem National Observation and Research Station, Southwest Minzu University, Chengdu 610041, China
*
Author to whom correspondence should be addressed.
Agronomy 2023, 13(10), 2580; https://doi.org/10.3390/agronomy13102580
Submission received: 19 September 2023 / Revised: 27 September 2023 / Accepted: 6 October 2023 / Published: 8 October 2023
(This article belongs to the Special Issue Integrated Ways to Improve Forage Production and Nutritional Value)
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Review Reports Versions Notes

Abstract

:
Arbuscular mycorrhizal fungi (AMF) have established themselves as pivotal allies in the realm of plant physiology, renowned for their remarkable contributions to augmenting both growth and resilience against environmental stresses. In this study, we embarked on a comprehensive investigation into the discernible impact of two distinct AMF species on a widely planted oat cultivar, ‘Qingyan No. 1’, when subjected to the austere conditions of a drought. The experimental design included three distinct AMF treatments (inoculation with Rhiaophagus intraradices, Funneliformis mosseae, or not), and the three water treatments were 75% of field capacity (well watered), 50% of field capacity (moderate drought), and 30% of field capacity (severe drought). The obtained results showed that the rate of inoculation under 75% FC for both AMF species was over 74%. Drought stress limited the growth and osmotic regulation of the oat plants. However, AMF inoculation observably increased the above-ground biomass under 75% FC and increased the root biomass under 30% FC. AMF inoculation also increased the root traits under 75% FC and 50% FC. R. intraradices inoculation increased the above-ground soluble sugar and soluble protein concentrations, and both AMF species showed decreased malondialdehyde (MDA) concentrations in the roots. Furthermore, the pervasive influence of drought stress exerted a discernible stranglehold on nutrient uptake in the oat plants, profoundly impacting the distribution of nutrients within the shoots and roots. Regardless of the drought stress treatment, the inoculation with both AMF species increased the P concentrations in the roots and the K and Mg concentrations in the roots, and the inoculation with R. intraradices increased the Ca concentration in the whole oat plant. Under 75% FC, the N concentration of the whole oat plant was significantly reduced by both AMF species. However, under 50% FC and 30% FC, the N concentrations in the shoots inoculated with both AMF species were close to that of the non-inoculated shoots. In summary, AMF improved the osmotic regulation and nutrient absorption and distribution of oat plants under drought stress and thus promoted the growth and biomass accumulation of oat plants.

1. Introduction

In the world cereal production statistics, oats (Avena sativa L.) rank around sixth, be-hind wheat, corn, rice, barley, and sorghum [1]. In many parts of the world, oats are grown for use as grains as well as for forage and fodder, as straw for bedding, hay, haylage, silage, and chaff [2]. At the same time, oats are the winter reserve grass for the livestock industry [3,4]. Russia, countries of the former Soviet Union, the US, Canada, Germany, and Poland account for about 75% of the world’s supply of grain oats, seeds, and industrial-grade oats [5]. However, the rates of yield reduction related to drought disasters for major crops will increase significantly with future climate change [6]. Droughts are one of the factors restricting the growth and production of oats. At the same time, droughts also limit the sustainable development of society and the economy [7,8]. Drought-induced stress orchestrates a series of cascading effects, culminating in the diminishment of soil nutrient availability, a curtailed plant nutrient uptake, and hampered nutrient translocation from the roots to the above-ground portions of plants [9]. The repercussions extend to the cellular realm, where drought-induced cellular dehydration and constrained nutrient assimilation conspire to elevate the presence of reactive oxygen species (ROS). The outcome is a compromised cell membrane permeability, exacerbating plant cell membrane peroxidation and malondialdehyde (MDA) accumulation. Plants have evolved an array of mechanisms to contend with drought-induced damage, encompassing morphological adjustments such as stomatal closure and an augmented wax content [10], physiological adaptations including osmotic regulation and antioxidant responses [11], and molecular responses involving the up-regulation of drought resistance genes [12]. But for some water-sensitive varieties, self-regulation is far from enough to cope with drought damage. Besides variety breeding and transgenic methods, biological interaction contributes to improving plant drought resistance as well.
Arbuscular mycorrhizal fungi (AMF) have garnered attention as formidable facilitators of plant resilience in the face of droughts and other environmental stressors [13]. This biological alliance is considered a pivotal strategy for bolstering plant drought tolerance [14]. AMF enter into a symbiotic relationship with their host plants, exchanging nutrients and water in return for carbon sources such as sugars and lipids [15,16,17,18,19]. Under drought conditions, AMF significantly enhance a plant’s N (nitrogen) and P (phosphorus) utilization efficiency [20]. Mild drought stress, as evidenced in inoculation studies with Rhizophagus irregularis, notably increases the P and Ca (calcium) contents in plant leaves [21]. AMF interventions have also been shown to ameliorate the water status of crops like wheat, enhancing chlorophyll synthesis under drought conditions, and ultimately leading to increased yields and growth [22,23]. The inoculation with R. irregularis has similarly augmented the root length and root volume in Triticum aestivum ssp. spelta L. [24], while Glomus mosseae inoculation has exhibited a promotional effect on the root dry weights and the active and total absorption areas of trifoliate orange (Poncirus trifoliata (L.) Raf.) root systems under drought stress [25]. It is worth noting, however, that while a wealth of research underscores AMF’s potential to alter plant root configurations, the colonization of different strains can induce distinct responses within the same species under varying environmental conditions [26,27]. While numerous experiments have corroborated AMF’s prowess in enhancing the drought resistance of crops such as tomato [28], wheat [22,29], and rice [30], investigations on the effects of AMF on oats and other forage crops remain comparatively sparse. In the present study, we executed a meticulously designed experiment involving three distinct AMF treatments and three water treatments on cultivated oats. The objective was to assess the impacts of inoculation with Rhiaophagus intraradices and Funneliformis mosseae and no inoculation on drought resistance, as well as the nitrogen, phosphorus, and trace element contents, and any differentiations in the root configurations between the above-ground and underground components of oats.

2. Materials and Methods

2.1. Biological Materials and Experimental Design

The experiment had a complete 1 × 3 × 3 factorial design with one oat cultivar (Avena sativa cv. Qinyan No. 1), three arbuscular mycorrhizal fungi treatments (without inoculation and inoculation with Rhiaophagus intraradices or Funneliformis mosseae), and three drought treatments (75% of field capacity, well watered; 50% of field capacity, moderate drought; and 30% of field capacity, severe drought). There were twelve replicate pots in each treatment, totaling 108 pots. Two AM fungi were provided by the Institute of Root Biology, Yangtze University (Jingzhou, China), and were multiplied in our laboratory using maize (Zea mays L.) as a host plant. The experiment was conducted in a greenhouse at the Laboratory of Alpine Grass Resistance Physiological Ecology at Southwest Minzu University (Chengdu, China). The mixture of sand and soil (1:1) was autoclaved at 121 °C for 2 h under pressure (0.11 MPa), and then placed in a storage room for 1 night and oven-dried for 6 h before use. The maximum field capacity (FC) of soil is 20.54%, and the field capacity was calculated as follows:
FC = (saturated soil weight − dry soil weight)/dry soil weight × 100%.
Seeds were disinfected with 1% sodium hypochlorite (Guangzhou Testing Technology Co., Ltd., Guangzhou, China) for 10 min and washed with distilled water, and one seed was sown in each plastic pot containing 3.2 kg of a sterilized mixture of sand and soil. Each pot was supplemented with 115 g sterilized or unsterilized inoculum of R. intraradices or F. mosseae. All pots were watered regularly to 75% FC (CK, well watered) in the first 2 months, and then two-thirds of non-mycorrhizal (NM) and arbuscular mycorrhizal (R. intraradices, F. mosseae) pots were exposed to drought stress by reducing the water regime to 50% FC (MD, moderate drought) and 30% FC (SD, severe drought), while the remaining third were kept well watered (75% FC).

2.2. Mycorrhizal Colonization and Plant Growth Parameters

After 15 days of water stress treatment, plants were harvested. Shoots’ and roots’ fresh materials were separated and dried at 105 °C for 15 min and then at 75 °C for 24 h to record dry weights and conduct nutrient content analyses. Subsamples of fresh roots (0.5 g) were stored in a 4 °C refrigerator to measure mycorrhizal colonization. The rest of the roots and shoots were stored in a −80 °C refrigerator to measure the content of total soluble sugar (TSS), MDA, and soluble protein content.
The fresh, clean roots were soaked in 10% KOH solution at 90 °C for 30 min and then acidified with 1% HCL for 5 min. The cleared roots were stained with 0.05% Trypan blue in lactoglycerol (v/v) at 90 °C for 20 min [31]. The rates of AM colonization were examined using the gridline intercept method [32]. The mycorrhizal dependency was calculated according to van der Heijden method [33]. If biomass of ∑ 1 n a n   > bn, then mycorrhizal dependency was calculated as follows:
mycorrhizal   dependency = ( 1 − ( b n / ( ∑ 1 n a n ) ) ) × 100 .
If biomass of ∑ 1 n a n   < bn, then mycorrhizal dependency was calculated as follows:
mycorrhizal   dependency = ( − 1 + ( a n / ( ∑ 1 n b n ) ) ) × 100
where a is the plant dry weight of a treatment inoculated with AMF, n is the number of treatments where plants were inoculated with AMF, and b is the plant dry mass of the non-inoculated treatments.

2.3. Method for Determination of Root Architecture

The root total length, root volume, and root surface were determined using the LA-S plant root analysis system from the company Hangzhou Wseen Testing Technology Co., Ltd. (Hangzhou, China). A total of three replicates were set for the root architecture determination. The supporting roots and all fibrous roots in one root sample were scanned and measured.

2.4. TSS, MDA, and Protein Concentrations

Total soluble sugar, MDA, and soluble protein contents were measured using the assay kits from the company Suzhou Comin Biotechnology Co., Ltd. (Suzhou, China).

2.5. Macronutrient Concentrations in Oats

The concentrations of N, P, potassium (K), magnesium (Mg), and Ca were determined using homogenized dry samples of shoots and roots. The N concentration was determined as described by Kong [34] using 0.1 g of dried shoots and roots, and the P concentration was determined using 1 g of dried shoots and roots that were burned with a Muffle oven and using the vanadomolybdate method [35]. The K, Na, and Ca concentrations were determined as described by Liu and Zhang [36] using an atomic absorption spectrophotometer (Hitachi Z-2000, Tokyo, Japan).

2.6. Statistical Analysis

The effects of mycorrhizal inoculation, drought stress, and their interactions were statistically analyzed with two-way ANOVA using IBM SPSS 26. At least 3 replicates were used for each treatment of all measured parameters. The significance of differences among treatments and interaction between factors was calculated at 5%. Multiple comparisons were performed using Duncan’s (HSD) post hoc test p < 0.05. Graphpad prism 8.0 was used to make graphs, and the data in the graph were shown as mean value ± SE.

3. Results

3.1. Mycorrhizal Colonization

The mycorrhizal colonization of oats was significantly affected by the drought treatments (Figure 1). The colonization rates of R. intraradices and F. mosseae are higher than 74% under well-watered conditions. Compared with CK, the colonization rate of R. intraradices under MD and both AMF colonization rates under SD were significantly reduced. However, under MD and SD, the mycorrhizal colonization of all AMF speices was not significant (Figure 2).

3.2. Plant Growth of Shoots and Roots

The shoot and root dry weights were significantly influenced by drought treatments and AMF inoculation. However, drought and inoculation had no significant interaction effect on the shoot dry weights and root dry weights (Figure 3). Compared with the non-inoculated treatments, the inoculation with R. intraradices and F. mosseae increased the shoot dry weights under the CK and MD treatments and increased the root dry weights under the CK and SD treatments (Figure 3A,B), while drought stress decreased the shoot dry weights and root dry weights for both the non-inoculated and inoculated treatments.
Based on oat shoot and root biomasses, the mycorrhizal dependency was calculated to evaluate the contribution of two AMF inoculations to oat growth. Except for the inoculation with F. mosseae under SD in the shoots, the other inoculations under three water regimes had positive contributions to both the shoots and roots (Figure 4). Under the three irrigation regimes, the shoots showed the greatest mycorrhizal dependency on two AMF species in the MD treatment, the inoculation with R. intraradices had better mycorrhizal dependency in the shoots under three irrigation regimes, and the inoculation with F. mosseae had negative contributions in the shoots under SD. Under the three irrigation regimes, two AMF species showed positive contributions in the roots. The inoculation with R. intraradices had better mycorrhizal dependency in the root under MD and SD.
The total root length, root volume, and root surface area of the oats were significantly influenced by the drought and AMF inoculation. The drought and inoculation had significant interaction effects on the total root length and root surface area (Figure 5 and Figure 6). Under inoculated and non-inoculated treatments, the drought significantly decreased the total root length, root volume, and root surface area (Figure 5A–C). The inoculation with F. mosseae and R. intraradices significantly increased the total root length and root volume under CK and MD (Figure 5A,B). The inoculation with F. mosseae and R. intraradices significantly increased the root volume under SD (Figure 5B), and the inoculation with R. intraradices significantly increased the root surface area under SD (Figure 5C). F. mosseae had a more significant effect on the total root length under CK (Figure 5A), and R. intraradices had a more significant effect on the root surface area under MD (Figure 5C).

3.3. TSS, MDA, and Protein Contents

The concentrations of soluble sugar, soluble protein, and MDA in the leaves were significantly influenced by the drought treatment and AMF inoculation, except MDA, drought, and inoculation had significant interaction effects on the soluble sugar and soluble protein contents (Table 1). The AMF inoculation had significant effects on the soluble sugar content in the roots, which was the same as in the leaves, and drought and inoculation had significant interaction effects on the soluble sugar and soluble protein contents in the roots. Drought stress significantly increased the accumulation of soluble sugar in oats under non-inoculated and inoculated treatments with R. intraradices, and compared with the non-inoculated treatment, the inoculation with R. intraradices increased the leafsoluble sugar content by 19%, 38%, and 125% under CK, MD, and SD treatments, and the root soluble sugar content increased by 50% under MD. As a consequence of SD, the protein concentration decreased (by 13.2%) in the non-inoculated leaf. However, it significantly increased in the R. intraradices treatments in the leaves, showing increasing rates of 44.4%, and showing increasing rates of 79.2% in the roots under MD. The accumulation of MDA was steeply increased in the non-inoculated leaves as a result of water stress application. However, mycorrhizal colonization significantly reduced the MDA concentration in the leaves induced by water stress (Table 2). The MDA concentration in the leaves significantly decreased by 16% and 18% when inoculated with R. intraradices and F. mosseae under SD. The inoculation with F. mosseae decreased the MDA concentration in the roots by 38% under MD.

3.4. Macronutrient Concentrations in Oats

The concentrations of N, P, K, and Ca in all plant tissues, and the concentration of Mg in the roots were significantly influenced by AMF inoculation. The concentrations of Ca and K in all oat plant tissues, and the concentration of Mg in the roots were significantly influenced by drought treatments. Except for Mg in the shoots, the other macronutrient concentrations were significantly influenced by AMF inoculation. Meanwhile, the K and Mg contents in the roots and the Ca in all oat plant tissues were significantly influenced by drought stress, inoculation, and their interactions (Figure 7). Compared with the non-inoculated treatments, the N concentrations of the shoots in the oats were not significantly changed except under CK. The N concentrations of the roots even decreased via inoculation under CK and MD. Under different water conditions, there was no significant difference in the N concentration of the shoots under two kinds of AMF species inoculation, but F. mosseae significantly increased the N content of the roots compared with the inoculation of R. intraradices (Figure 7A). Compared with the non-inoculated treatments, only the inoculation with R. intraradices significantly increased the concentration of shoot P under CK, while both R. intraradices and F. mosseae inoculation increased the concentration of root P under different water treatments (Figure 7B). Compared with the non-inoculated treatments, the K contents of the shoots were not significantly changed except for R. intraradices inoculation under CK, and there were significant differences in the inoculated and non-inoculated root K concentrations under CK and MD; the R. intraradices and F. mosseae inoculations increased the concentrations of root K under CK, and F. mosseae inoculation increased the concentrations of root K under MD, while SD decreased the concentration of root K for both the non-inoculated and inoculated treatments (Figure 7C). Compared with the non-inoculated treatments, R. intraradices inoculation increased the concentrations of Ca in all plant tissues under MD and SD treatments (Figure 7D), and R. intraradices inoculation also increased the concentrations of root Mg under three water treatments (Figure 7E).

4. Discussion

Our experimental results align with those of previous studies, supporting the idea that droughts can decrease the infection rate of AMF [21,30,37]. Despite facing drought conditions, both AMF species had a positive influence on the oat growth, resulting in increased shoot and root biomasses as well as enhanced root architecture. It is worth noting that before the drought treatment, AMF and oat roots demonstrate symbiosis for up to two months, and establish a robust symbiotic relationship. Consequently, under normal water conditions, both AMF treatments exhibited high infection rates exceeding 74%, with G.r achieving a higher rate at 77.21%. Similar observations have been reported in wheat crops under comparable irrigation practices, where F. mosseae inoculation achieved an infection rate of 72.5% [37]. However, Zhang [38] observed a lower inoculation rate (below 40%) when oats were inoculated with Rhizophagus intraradices under 75% FC conditions. Notably, it should be acknowledged that plant mycorrhizal infection rates are influenced by various factors such as the bacterial substrate specificity [39], host genotype variations [40], soil pH levels, and even other microorganisms that are present in the soil ecosystem [41]. The relatively low infection rate observed in Zhang’s [38] study may be attributed to the influence exerted by other microorganisms present in non-sterile soil environments. In our study, both AMF species successfully established symbiotic associations with Qingyan No. 1 and positively influenced their biomass accumulation, root growth, nutrient uptake, and stress tolerance capabilities.
Consistent with most mycorrhizal studies, the two AMF species in this research increased the biomasses of different parts of the oat, especially the shoot dry weight under moderate drought conditions and the root weight under severe drought conditions. However, the oats inoculated with R. intraradices have a higher mycorrhizal dependency, especially for the shoots, which means R. intraradices inoculation has a higher mycorrhizal contribution to oats. The two AMF species also have significant effects on the root growth under well-watered and moderate drought conditions. AMF could up-regulate PtYUC3 and PtYU8 genes related to IAA synthesis, thereby increasing the IAA level, root length, and root density in trifoliate orange root [42].
Despite oats’ drought and barren resistance characteristics, water restriction reduces the utilization of N, P, and other nutrients. In this study, AMF inoculation resulted in lower N concentrations in oats compared to those without inoculation. It might be the high biomass that led to N dilution in the shoot tissues [43]. However, under water stress, AMF inoculation may promote N uptake by the roots and maintain the stability of the shoot N concentration. This result may be related to the nitrate reductase activity (NR), a key enzyme in N metabolism, which is greatly affected by droughts. Some research already showed that mycorrhizal plants had higher NR than the uninoculated treatments, particularly under water stress conditions [44,45]. Similar to most mycorrhizal studies, both AMF species enhanced the P concentration in the oat roots; the extracellular hyphae of AMF can reach the soil that cannot be reached by the root system to absorb nutrients. Additionally, the secretion of mycelia can also convert insoluble N and P nutrients into usable forms, which provide more absorbed N and P to the host plants [46].
Previous studies have shown that K plays crucial roles in enzyme activation, membrane transport, osmotic regulation, as well as protein synthesis, including starches, cellulose, and vitamins in plants [47]. Additionally, K+ also participates in stomatal opening, aiding in plant adaptation to water stress [48]. P, Ca, K, and Mg are mobile ions in the soil that rely on continuous water flow between the soil–root–shoot parts for absorption [49]. Our results demonstrated that both AMF species increased the root K concentration under well-watered conditions and were consistent with the findings of Li [21]. G. mosseae increased the K concentration in the roots under moderate drought conditions. R. irregularis increased the growth, K content, and K channel gene expression in Lycium barbarum, especially under drought conditions [50]. Compared with the well-watered treatment, the K concentration of the shoots under the drought treatment has no significant difference. Therefore, we believe that the two AMF species can maintain higher K concentrations under drought conditions, thereby reducing drought damage.
The inoculation with R. intraradices significantly increased the concentration of Ca in oat plants under all water treatments; Ca2+ can serve as a mediator for transducing signals released by the AMF to plants, thereby facilitating the establishment of a symbiotic relationship and also transmitting drought signals within mycorrhizal structures under drought conditions [51,52]. Meanwhile, Ca promoted the water retention capacity of leaves and cell membranes to alleviate plant water scarcity under drought stress [53]. In our study, the inoculation with R. intraradices had a significant influence on the oat roots under all water treatments. Mg is involved in carbon metabolism by activating the enzyme, RUBISCO, thus promoting mycorrhizal colonization and plant growth [54]. However, Lopes [55] suggested that the higher Mg accumulation in the roots of mycorrhizal plants reduces the energy required for the unnecessary transport of mineral nutrients. Overall, both AMF species had positive effects on ion nutrition accumulation, especially at root level, during drought stress due to the extraneous mycelium extending from the roots absorbing more nutrients and water.

5. Conclusions

In this study, the oats had different responses to drought stress and the colonization of the two AMF species. On the whole, AMF alleviated drought stress to a certain extent, which was manifested in the increase in the biomass, root architecture, soluble sugar, soluble protein, and the decrease in MDA. In addition, the inoculation of two kinds of AMF increased the accumulation of P, K, Ca, and Mg in different parts of the oat to different degrees, and both AMF species had significant effects on the increase in the root P concentration. Of the two types of AMF, the inoculation with R. intraradices was the most effective in the drought tolerance and nutrient absorption of the oats. The results demonstrated that the root architecture and nutrient absorption were enhanced in the mycorrhizal oats, which resulted in enhanced osmotic adjustment, shoot and root growth, and reduced biomass loss during drought stress compared with the non-mycorrhizal oats, leading to an improvement in the drought resistance of oats.

Author Contributions

Conceptualization, H.T. and Q.Z.; methodology, H.T. and W.L.; software, H.T.; validation, H.W., X.W. and G.B.; formal analysis, H.T. and J.L.; investigation, H.T.; resources, Z.J.; data curation, H.T.; writing—original draft preparation, H.T.; writing—review and editing, Q.Z.; supervision, Q.Z. and W.L.; funding acquisition, Z.J. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the Qinghai Special Project on the transformation of scientific and technological achievements (2022-NK-130).

Data Availability Statement

Not applicable.

Acknowledgments

We thank the laboratory of Alpine Grass Resistance Physiological Ecology at Southwest Minzu University for providing the laboratory equipment and venues.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Mushtaq, A.; Zaffar, G.; Dar, Z.A.; Mehfuza, H. A review on oat (Avena sativa L.) as a dual-purpose crop. Sci. Res. Essays 2014, 9, 52–59. [Google Scholar] [CrossRef]
  2. Robert, W.W. The Oat Crop: Production and Utilization; Springer: Dordrecht, The Netherlands, 1995; 584p. [Google Scholar] [CrossRef]
  3. Zhou, Q.; Gou, X.; Tian, L.; Chen, Y.; Gao, S.; Bai, W.; Zhang, W. Performances of early and late maturing oat varieties in cold regions. Chin. Sci. Bull. 2018, 63, 1722–1730. [Google Scholar] [CrossRef]
  4. Diao, X. Production and genetic improvement of minor cereals in China. Crop J. 2017, 5, 103–114. [Google Scholar] [CrossRef]
  5. USDA. World Oats Production, Consumption, and Stocks; US Department of Agriculture: Washington, DC, USA, 2014.
  6. Li, Y.; Ye, W.; Wang, M.; Yan, X. Climate change and drought: A risk assessment of crop-yield impacts. Clim. Res. 2009, 39, 31–46. [Google Scholar] [CrossRef]
  7. Stevens, E.J.; Armstrong, K.W.; Bezar, H.J.; Griffin, W.B.; Hampton, J.G. Fodder Oats: A World Overview; Food and Agricultural Organization of the United Nations: Roma, Italy, 2004; pp. 11–18. [Google Scholar]
  8. Hakala, K.; Jauhiainen, L.; Rajala, A.A.; Jalli, M.; Kujala, M.; Laine, A. Different responses to weather events may change the cultivation balance of spring barley and oats in the future. Field Crop. Res. 2020, 259, 107956. [Google Scholar] [CrossRef]
  9. Hussain, H.A.; Men, S.; Hussain, S.; Chen, Y.; Ali, S.; Zhang, S.; Liao, C.; Wang, L. Interactive effects of drought and heat stresses on morpho-physiological attributes, yield, nutrient uptake and oxidative status in maize hybrids. Sci. Rep. 2019, 9, 3890. [Google Scholar] [CrossRef] [PubMed]
  10. Yang, J.; Ordiz, M.I.; Jaworski, J.G.; Beachy, R.N. Induced accumulation of cuticular waxes enhances drought tolerance in Arabidopsis by changes in development of stomata. Plant Physiol. Bioch. 2011, 49, 1448–1455. [Google Scholar] [CrossRef]
  11. Seleiman, M.F.; Al-Suhaibani, N.; Ali, N.; Akmal, M.; Alotaibi, M.; Refay, Y.; Refay, Y.; Dindaroglu, T.; Abdul-Wajid, H.; Battaglia, M.L. Drought stress impacts on plants and different approaches to alleviate its adverse effects. Plants 2021, 10, 259. [Google Scholar] [CrossRef]
  12. Yang, Z.; Chi, X.; Guo, F.; Jin, X.; Luo, H.; Hawar, A.; Chen, Y.; Feng, K.; Wang, B.; Qi, J.; et al. SbWRKY30 enhances the drought tolerance of plants and regulates a drought stress-responsive gene, SbRD19, in sorghum. J. Plant Physiol. 2020, 246, 153142. [Google Scholar] [CrossRef]
  13. Lenoir, I.; Fontaine, J.; Sahraoui, A.L.H. Arbuscular mycorrhizal fungal responses to abiotic stresses: A review. Phytochemistry 2016, 123, 4–15. [Google Scholar] [CrossRef]
  14. Begum, N.; Qin, C.; Ahanger, M.A.; Raza, S.; Khan, M.I.; Ashraf, M.; Ahmed, N.; Zhang, L. Role of arbuscular mycorrhizal fungi in plant growth regulation: Implications in abiotic stress tolerance. Front. Plant Sci. 2019, 10, 1068. [Google Scholar] [CrossRef] [PubMed]
  15. Smith, S.E. Mycorrhizal Symbiosis. Soil Sci. 2008, 3, 273–281. [Google Scholar] [CrossRef]
  16. Atul-Nayyar, A.; Hamel, C.; Hanson, K.; Germida, J. The arbuscular mycorrhizal symbiosis links N mineralization to plant demand. Mycorrhiza 2009, 19, 239–246. [Google Scholar] [CrossRef] [PubMed]
  17. Kakouridis, A.; Hagen, J.A.; Kan, M.P.; Mambelli, S.; Feldman, L.J.; Herman, D.J.; Weber, P.K.; Pett-ridge, J.; Firestone, M.K. Routes to roots: Direct evidence of water transport by arbuscular mycorrhizal fungi to host plants. New Phytol. 2022, 236, 210–221. [Google Scholar] [CrossRef]
  18. Wang, W.; Shi, J.; Xie, Q.; Jiang, Y.; Yu, N.; Wang, E. Nutrient exchange and regulation in arbuscular mycorrhizal symbiosis. Mol. Plant 2017, 10, 1147–1158. [Google Scholar] [CrossRef]
  19. An, J.; Zeng, T.; Ji, C.; de Graaf, S.; Zheng, Z.; Xiao, T.T.; Limpens, E.; Pan, Z.A. Medicago truncatula SWEET transporter implicated in arbuscule maintenance during arbuscular mycorrhizal symbiosis. New Phytol. 2019, 224, 396–408. [Google Scholar] [CrossRef]
  20. Tang, H.; Hassan, M.U.; Feng, L.; Nawaz, M.; Shah, A.N.; Qari, S.H.; Liu, Y.; Miao, J. The critical role of arbuscular mycorrhizal fungi to improve drought tolerance and nitrogen use efficiency in crops. Front. Plant Sci. 2022, 13, 919166. [Google Scholar] [CrossRef]
  21. Li, L.; Zhang, H.; Tang, M.; Chen, H. Nutrient uptake and distribution in mycorrhizal cuttings of Populus× canadensis ‘Neva’under drought stress. J. Soil Sci. Plant Nutr. 2021, 21, 2310–2324. [Google Scholar] [CrossRef]
  22. Zhou, Q.; Ravnskov, S.; Jiang, D.; Wollenweber, B. Changes in carbon and nitrogen allocation, growth and grain yield induced by arbuscular mycorrhizal fungi in wheat (Triticum aestivum L.) subjected to a period of water deficit. Plant Growth Regul. 2015, 75, 751–760. [Google Scholar] [CrossRef]
  23. Metwally, A.; Azooz, M.; Nafady, N.; El-Enany, A. Arbuscual mycorrhizal symbiosis alleviates drought stress imposed on wheat plants (Triticum aestivum L.). Appl. Ecol. Environ. Res. 2019, 17, 13713–13727. [Google Scholar] [CrossRef]
  24. Ratajczak, K.; Sulewska, H.; Błaszczyk, L.; Basińska-Barczak, A.; Mikołajczak, K.; Salamon, S.; Szymańska, G.; Dryjański, L. Growth and Photosynthetic Activity of Selected Spelt Varieties (Triticum aestivum ssp. spelta L.) Cultivated under Drought Conditions with Different Endophytic Core Microbiomes. Int. J. Mol. Sci. 2020, 21, 7987. [Google Scholar] [CrossRef]
  25. Chen, Y.Y.; Cheng, Y.H.; Jia, X.X. Effects of arbuscular mycorrhizal fungi on the growth and zinc uptake of trifoliate orange (Poncirus trifoliata) seedlings grown in low-zinc soil. J. Plant Nutr. 2017, 40, 324–331. [Google Scholar] [CrossRef]
  26. Abdel, L.; Arafat, A.H.; He, C. Arbuscular mycorrhizal influence on growth, photosynthetic pigments, osmotic adjustment and oxidative stress in tomato plants subjected to low temperature stress. Acta Physiol. Plant. 2011, 33, 1217–1225. [Google Scholar] [CrossRef]
  27. Noshad, M.H.; Chavoshi, E.; Mosaddeghi, M.R.; Dorostkar, V.; Hosseini, F. Growth and nutrient uptake of haloxylon and atriplex as affected by mycorrhizal symbiosis under combined drought and salinity stresses. Can. J. Soil Sci. 2022, 103, 305–317. [Google Scholar] [CrossRef]
  28. Duc, N.H.; Csintalan, Z.; Posta, K. Arbuscular mycorrhizal fungi mitigate negative effects of combined drought and heat stress on tomato plants. Plant Physiol. Bioch. 2018, 132, 297–307. [Google Scholar] [CrossRef]
  29. Asadollahi, M.; Iranbakhsh, A.; Ahmadvand, R.; Ebadi, M.; Mehregan, I. Synergetic effect of water deficit and arbuscular mycorrhizal symbiosis on the expression of aquaporins in wheat (Triticum aestivum L.) roots: Insights from NGS RNA-sequencing. Physiol. Mol. Biol. Plants 2023, 29, 195–208. [Google Scholar] [CrossRef]
  30. Tisarum, R.; Theerawitaya, C.; Samphumphuang, T.; Phisalaphong, M.; Singh, H.P.; Cha-Um, S. Promoting water deficit tolerance and anthocyanin fortification in pigmented rice cultivar (Oryza sativa L. subsp. indica) using arbuscular mycorrhizal fungi inoculation. Physiol. Mol. Biol. Plants 2019, 25, 821–835. [Google Scholar] [CrossRef]
  31. Phillips, J.M. Improved procedures for clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. Trans. Br. Mycol. Soc. 1970, 55, 158–161. [Google Scholar] [CrossRef]
  32. 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 fung. New Phytol. 1990, 115, 495–501. [Google Scholar] [CrossRef]
  33. Van Der Heijden, M.G.A. Arbuscular mycorrhizal fungi as a determinant of plant diversity: In search of underlying mechanisms and general principles. In Mycorrhizal Ecology; Springer: Berlin/Heidelberg, Germany, 2002; pp. 243–265. [Google Scholar] [CrossRef]
  34. Kong, Z.; Glick, B.R.; Duan, J.; Ding, S.; Tian, J.; McConkey, B.J.; Wei, G. Effects of 1-aminocyclopropane-1-carboxylate (ACC) deaminase-overproducing Sinorhizobium meliloti on plant growth and copper tolerance of Medicago lupulina. Plant Soil 2015, 391, 383–398. [Google Scholar] [CrossRef]
  35. Sterges, A.J.; Hardin, L.J.; MacIntire, W.H. A modification of the official micro method for the determination of phosphorus content of plant tissue. J. Assoc. Off. Agric. Chem. 1950, 33, 114–121. [Google Scholar] [CrossRef]
  36. Liu, J.; Zhang, H.G. Determination of Nine Mineral Elements in Hulless Barley by Ultraviolet Spectrophotometry and Flame Atomic Absorption Spectrometry. Spectrosc. Spect. Anal. 2010, 30, 1126–1129. [Google Scholar] [CrossRef]
  37. Moradi Tarnabi, Z.; Iranbakhsh, A.; Mehregan, I.; Ahmadvand, R. Impact of arbuscular mycorrhizal fungi (AMF) on gene expression of some cell wall and membrane elements of wheat (Triticum aestivum L.) under water deficit using transcriptome analysis. Physiol. Mol. Biol. Plants 2020, 26, 143–162. [Google Scholar] [CrossRef] [PubMed]
  38. Zhang, B.; Lv, Y.F.; Li, Y.; Li, L.; Jia, J.Q.; Feng, M.C.; Fahad, S.; Zhang, M.J. Inoculation with Rhizophagus intraradices Confers Drought Stress Tolerance in Oat by Improving Nitrogen and Phosphorus Nutrition. J. Soil Sci. Plant Nutr. 2023, 23, 2039–2052. [Google Scholar] [CrossRef]
  39. Nacoon, S.; Ekprasert, J.; Riddech, N.; Mongkolthanaruk, W.; Jogloy, S.; Vorasoot, N.; Cooper Julia Boonlue, S. Growth enhancement of sunchoke by arbuscular mycorrhizal fungi under drought condition. Rhizosphere 2021, 17, 100308. [Google Scholar] [CrossRef]
  40. Baum, C.; Toljander, Y.K.; Eckhardt, K.U.; Weih, M. The significance of host-fungus combinations in ectomycorrhizal symbioses for the chemical quality of willow foliage. Plant Soil 2009, 323, 213–224. [Google Scholar] [CrossRef]
  41. Dąbrowska, G.; Baum, C.; Trejgell, A.; Hrynkiewicz, K. Impact of arbuscular mycorrhizal fungi on the growth and expression of gene encoding stress protein-metallothionein BnMT2 in the non-host crop Brassica napus L. J. Plant Nutr. Soil Sci. 2014, 177, 459–467. [Google Scholar] [CrossRef]
  42. Liu, C.Y.; Zhang, F.; Zhang, D.J.; Srivastava, A.K.; Wu, Q.S.; Zou, Y.N. Mycorrhiza stimulates root-hair growth and IAA synthesis and transport in trifoliate orange under drought stress. Sci. Rep. 2018, 8, 1978. [Google Scholar] [CrossRef]
  43. Eltigani, A.; Müller, A.; Ngwene, B.; George, E. Physiological and Morphological Responses of Okra (Abelmoschus esculentus L.) to Rhizoglomus irregulare Inoculation under Ample Water and Drought Stress Conditions Are Cultivar Dependent. Plants 2021, 11, 89. [Google Scholar] [CrossRef]
  44. Begum, N.; Ahanger, M.A.; Zhang, L. AMF inoculation and phosphorus supplementation alleviates drought induced growth and photosynthetic decline in Nicotiana tabacum by up-regulating antioxidant metabolism and osmolyte accumulation Science Direct. Environ. Exp. Bot. 2020, 176, 104088. [Google Scholar] [CrossRef]
  45. Ruiz-Lozano, J.M.; Azcón, R. Mycorrhizal colonization and drought stress as factors affecting nitrate reductase activity in lettuce plants. Agric. Ecosyst. Environ. 1996, 60, 175–181. [Google Scholar] [CrossRef]
  46. Hoang, D.T.T.; Rashtbari, M.; Anh, L.T.; Wang, S.; Tu, D.T.; Hiep, N.V.; Razavi, B.S. Mutualistic interaction between arbuscular mycorrhiza fungi and soybean roots enhances drought resistant through regulating glucose exudation and rhizosphere expansion. Soil Biol. Biochem. 2022, 171, 108728. [Google Scholar] [CrossRef]
  47. Dong, H.; Kong, X.; Li, W.; Tang, W.; Zhang, D. Effects of plant density and nitrogen and potassium fertilization on cotton yield and uptake of major nutrients in two fields with varying fertility. Field Crop. Res. 2010, 119, 106–113. [Google Scholar] [CrossRef]
  48. Aksu, G.; Altay, H. The Effects of potassium applications on srought stress in sugar beet. part ii. plant nutrition content. J. Sci. Perspect. 2020, 4, 203–216. [Google Scholar] [CrossRef]
  49. Markus, K. Water Relations and Nutrient Uptake. In The Science of Grapevines; Academic Press: Cambridge, MA, USA, 2010; pp. 85–105. [Google Scholar] [CrossRef]
  50. Zhang, H.; Wei, S.; Hu, W.; Xiao, L.; Tang, M. Arbuscular mycorrhizal fungus Rhizophagus irregularis increased potassium content and expression of genes encoding potassium channels in Lycium barbarum. Front. Plant Sci. 2017, 8, 440. [Google Scholar] [CrossRef]
  51. Lorella, N.; Moscatiello, R.; Genre, A.; Novero, M.; Baldan, B.; Bonfante, P.; Mariani, P. The arbuscular mycorrhizal fungus Glomus intraradices induces intracellular calcium changes in soybean cells. Caryologia 2007, 60, 137–140. [Google Scholar] [CrossRef]
  52. Mbengue, M.D.; Hervé, C.; Debellé, F. Nod factor signaling in symbiotic nodulation. Adv. Bot. Res. 2020, 94, 1–39. [Google Scholar] [CrossRef]
  53. Khan, A.; Anwar, Y.; Hasan, M.M.; Iqbal, A.; Ali, M.; Alharby, H.F.; Hakeem, K.R.; Hasanuzzaman, M. Attenuation of Drought Stress in Brassica Seedlings with Exogenous Application of Ca2+ and H2O2. Plants 2017, 6, 20. [Google Scholar] [CrossRef]
  54. Liu, J.; Fang, L.; Pei, W.; Li, F.; Zhao, J. Effects of magnesium application on the arbuscular mycorrhizal symbiosis in tomato. Symbiosis 2023, 89, 73–82. [Google Scholar] [CrossRef]
  55. Lopes, J.I.; Arrobas, M.; Brito, C.; Gonçalves, A.; Silva, E.; Martins, S.; Raimundo, S.; Rodrigues, M.Â.; Correia, C.M. Mycorrhizal Fungi were More Effective than Zeolites in Increasing the Growth of Non-Irrigated Young Olive Trees. Sustainability 2020, 12, 10630. [Google Scholar] [CrossRef]
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Figure 1. Frequency of mycorrhizal colonization. CK, well watered; MD, moderate drought; SD, severe drought; R.i, inoculated with Rhiaophagus intraradices; F.m, inoculated with Funneliformis mosseae. Values with different letters indicate a significant difference (Duncan’s test, p ≤ 0.05, n = 3).
Figure 1. Frequency of mycorrhizal colonization. CK, well watered; MD, moderate drought; SD, severe drought; R.i, inoculated with Rhiaophagus intraradices; F.m, inoculated with Funneliformis mosseae. Values with different letters indicate a significant difference (Duncan’s test, p ≤ 0.05, n = 3).
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Figure 2. Structures of arbuscular mycorrhizal fungi (AMF) in oat roots inoculated with AMF spores at the end of the experiment: (A) Funneliformis mosseae spores (s) and extraradical hyphae (eh); (B) Rhiaophagus intraradices vesicle (v), arbuscular (a), and intraradical hyphae (ih). Unit: μm.
Figure 2. Structures of arbuscular mycorrhizal fungi (AMF) in oat roots inoculated with AMF spores at the end of the experiment: (A) Funneliformis mosseae spores (s) and extraradical hyphae (eh); (B) Rhiaophagus intraradices vesicle (v), arbuscular (a), and intraradical hyphae (ih). Unit: μm.
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Figure 3. The effects of irrigation regime and inoculation with two AMF species on (A) shoot dry weight and (B) root dry weight of oats. CK, well watered; MD, moderate drought; SD, severe drought; NM, non-mycorrhizal, R.i, inoculated with Rhiaophagus intraradices; F.m, inoculated with Funneliformis mosseae. Values with different letters indicate a significant difference (Duncan’s test, p ≤ 0.05, n = 3). PAMF, probability value for the inoculation with the G.r and G.m species; PAMF, probability value for the inoculation with the R.i and F.m species; PD, probability value for the moisture treatment; PD×AMF, probability value for the AMF × drought stress. *** p ≤ 0.001; ns, no sigificant.
Figure 3. The effects of irrigation regime and inoculation with two AMF species on (A) shoot dry weight and (B) root dry weight of oats. CK, well watered; MD, moderate drought; SD, severe drought; NM, non-mycorrhizal, R.i, inoculated with Rhiaophagus intraradices; F.m, inoculated with Funneliformis mosseae. Values with different letters indicate a significant difference (Duncan’s test, p ≤ 0.05, n = 3). PAMF, probability value for the inoculation with the G.r and G.m species; PAMF, probability value for the inoculation with the R.i and F.m species; PD, probability value for the moisture treatment; PD×AMF, probability value for the AMF × drought stress. *** p ≤ 0.001; ns, no sigificant.
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Figure 4. The mycorrhizal dependency of two AMF species in different irrigation regimes based on shoot and root dry weights. CK, well watered; MD, moderate drought; SD, severe drought; R.i, inoculated with Rhiaophagus intraradices; F.m, inoculated with Funneliformis mosseae.
Figure 4. The mycorrhizal dependency of two AMF species in different irrigation regimes based on shoot and root dry weights. CK, well watered; MD, moderate drought; SD, severe drought; R.i, inoculated with Rhiaophagus intraradices; F.m, inoculated with Funneliformis mosseae.
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Figure 5. The effects of irrigation regime and inoculation with two AMF species on (A) total root length, (B) root volume, and (C) root surface area of oats. CK, well watered; MD, moderate drought stress; SD, severe drought; NM, non-mycorrhizal, R.i, inoculated with Rhiaophagus intraradices; F.m, inoculated with Funneliformis mosseae. Values with different letters indicate a significant difference (Duncan’s test, p ≤ 0.05, n = 3). PAMF, probability value for the inoculation with the R.i and F.m species; PD, probability value for the moisture treatment; PD×AMF, probability value for the AMF × drought stress. * p ≤0.05; ** p ≤ 0.01; *** p ≤ 0.001; ns, no sigificant.
Figure 5. The effects of irrigation regime and inoculation with two AMF species on (A) total root length, (B) root volume, and (C) root surface area of oats. CK, well watered; MD, moderate drought stress; SD, severe drought; NM, non-mycorrhizal, R.i, inoculated with Rhiaophagus intraradices; F.m, inoculated with Funneliformis mosseae. Values with different letters indicate a significant difference (Duncan’s test, p ≤ 0.05, n = 3). PAMF, probability value for the inoculation with the R.i and F.m species; PD, probability value for the moisture treatment; PD×AMF, probability value for the AMF × drought stress. * p ≤0.05; ** p ≤ 0.01; *** p ≤ 0.001; ns, no sigificant.
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Figure 6. The pictures of roots under irrigation regime and inoculation with two AMF species. (a–c) non-mycorrhizal; (d–f) i, inoculated with Rhiaophagus intraradices; (g–i) m, inoculated with Funneliformis mosseae. B, Qinyan No. 1; CK, well watered; MD, moderate drought; SD, severe drought.
Figure 6. The pictures of roots under irrigation regime and inoculation with two AMF species. (a–c) non-mycorrhizal; (d–f) i, inoculated with Rhiaophagus intraradices; (g–i) m, inoculated with Funneliformis mosseae. B, Qinyan No. 1; CK, well watered; MD, moderate drought; SD, severe drought.
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Figure 7. The effects of irrigation regime and inoculation with two AMF species on shoot and root N (A), P (B), K (C), Ca (D), and Mg (E) concentrations of oats. CK, well watered; MD, moderate drought; SD, severe drought; NM, non-mycorrhizal, R.i, inoculated with Rhiaophagus intraradices; F.m, inoculated with Funneliformis mosseae. Values with different letters indicate a significant difference (Duncan’s test, p ≤ 0.05, n = 3). PAMF, probability value for the inoculation with the R.i and F.m species; PD, probability value for the moisture treatment; PD×AMF, probability value for the AMF × drought stress. * p ≤ 0.05; ** p ≤ 0.01; *** p ≤ 0.001; ns, not significant.
Figure 7. The effects of irrigation regime and inoculation with two AMF species on shoot and root N (A), P (B), K (C), Ca (D), and Mg (E) concentrations of oats. CK, well watered; MD, moderate drought; SD, severe drought; NM, non-mycorrhizal, R.i, inoculated with Rhiaophagus intraradices; F.m, inoculated with Funneliformis mosseae. Values with different letters indicate a significant difference (Duncan’s test, p ≤ 0.05, n = 3). PAMF, probability value for the inoculation with the R.i and F.m species; PD, probability value for the moisture treatment; PD×AMF, probability value for the AMF × drought stress. * p ≤ 0.05; ** p ≤ 0.01; *** p ≤ 0.001; ns, not significant.
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Table 1. A two-way ANOVA for the effects of drought, two AMF species inoculation, and their interactions with TSS, MDA, and protein contents of oat.
Table 1. A two-way ANOVA for the effects of drought, two AMF species inoculation, and their interactions with TSS, MDA, and protein contents of oat.
PartTreatmentSoluble SugarSoluble Protein MDA
ShootsDrought10.63 **6.46 **12.13 ***
AMF110.97 ***19.08 ***8.33 **
Drought × AMF16.26 ***10.45 ***2.28 ns
RootsDrought1.94 ns2.89 ns0.54 ns
AMF6.34 **0.13 ns2.24 ns
Drought × AMF11.3 ***9.09 ***0.558 ns
ns, not significant; ** p ≤ 0.01; *** p ≤ 0.001.
Table 2. The effects of irrigation regime and inoculation with two AMF species on TSS, MDA, and protein contents.
Table 2. The effects of irrigation regime and inoculation with two AMF species on TSS, MDA, and protein contents.
PartTreatmentSoluble Sugar (mg/g)Soluble Protein (mg/g)MDA (nmol/g)
LeavesCK-NM10.78 ± 0.72 cd17.69 ± 0.52 cd8.9 ± 0.36 c
CK-R.i12.88 ± 1.59 bc18.06 ± 1.2 cd8.67 ± 0.34 c
CK-F.m8.43 ± 0.7 de16.33 ± 0.35 de8.95 ± 0.37 c
MD-NM14.58 ± 0.65 b18.49 ± 0.78 bc11.26 ± 0.54 ab
MD-R.i20.26 ± 0.42 a20.49 ± 0.68 ab9.95 ± 0.91 bc
MD-F.m6.24 ± 0.28 e16.67 ± 0.2 cde8.71 ± 0.51 c
SD-NM8.88 ± 0.62 d15.35 ± 0.76 e12.22 ± 0.35 a
SD-R.i20.06 ± 1.27 a22.17 ± 0.44 a10.27 ± 0.51 bc
SD-F.m9.27 ± 0.47 d20.18 ± 0.23 ab9.97 ± 0.18 bc
RootsCK-NM5.95 ± 0.78 ab8.36 ± 0.91 ab13.5 ± 0.3 a
CK-R.i3.83 ± 0.16 c4.77 ± 0.85 c8.27 ± 0.56 ef
CK-F.m4.65 ± 0.35 abc8.89 ± 1.07 ab11.96 ± 0.84 abc
MD-NM4.46 ± 0.21 bc6.53 ± 0.37 bc12.66 ± 0.3 ab
MD-R.i6.09 ± 0.57 a11.7 ± 1.94 a10.84 ± 1.04 bcd
MD-F.m1.69 ± 0.1 d4.17 ± 0.57 c7.8 ± 0.79 f
SD-NM4.34 ± 0.72 c9.01 ± 1.3 ab10.17 ± 0.61 cde
SD-R.i4.63 ± 0.49 abc8.28 ± 0.65 ab9.63 ± 0.46 def
SD-F.m4.83 ± 0.16 abc10.38 ± 1.1 a10.3 ± 0.9 cde
CK, well watered; MD, moderate drought; SD, severe drought; NM, non-mycorrhizal, R.i, inoculated with Rhiaophagus intraradices; F.m, inoculated with Funneliformis mosseae. Mean values ± SE with different letters indicate a significant difference (Duncan’s test, p ≤ 0.05, n = 3).
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Tian, H.; Jia, Z.; Liu, W.; Wei, X.; Wang, H.; Bao, G.; Li, J.; Zhou, Q. Effects of Arbuscular Mycorrhizal Fungi on Growth and Nutrient Accumulation of Oat under Drought Conditions. Agronomy 2023, 13, 2580. https://doi.org/10.3390/agronomy13102580

AMA Style

Tian H, Jia Z, Liu W, Wei X, Wang H, Bao G, Li J, Zhou Q. Effects of Arbuscular Mycorrhizal Fungi on Growth and Nutrient Accumulation of Oat under Drought Conditions. Agronomy. 2023; 13(10):2580. https://doi.org/10.3390/agronomy13102580

Chicago/Turabian Style

Tian, Haoqi, Zhifeng Jia, Wenhui Liu, Xiaoxin Wei, Hui Wang, Gensheng Bao, Jin Li, and Qingping Zhou. 2023. "Effects of Arbuscular Mycorrhizal Fungi on Growth and Nutrient Accumulation of Oat under Drought Conditions" Agronomy 13, no. 10: 2580. https://doi.org/10.3390/agronomy13102580

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