Effect of ectomycorrhizal fungi on the activation and uptake of phosphorus in Populus davidiana×P. bolleana mycorrhizosphere and hyphosphere

doi:10.21203/rs.3.rs-3751348/v1

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Effect of ectomycorrhizal fungi on the activation and uptake of phosphorus in Populus davidiana×P. bolleana mycorrhizosphere and hyphosphere

https://doi.org/10.21203/rs.3.rs-3751348/v1

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Ectomycorrhizal fungi (ECMF) are capable of converting phosphate in the insoluble state of the soil into effective phosphorus that can be directly absorbed and used by plants, a mechanism that is essential for promoting plant growth and development.In this study, we utilized Populus davidiana × P. bolleana tissue culture seedlings as the test material. Inoculation was performed with two ectomycorrhizal fungi: Suillus luteus and Paxillus involutus. The aim was to study the activation and uptake of soil phosphorus by ectomycorrhizal. Our results showed that inoculation of both S. luteus and P. involutus significantly increased seedling height, ground diameter, biomass and tissue phosphorus content of Populus davidiana × P. bolleana seedlings. Concurrently, it reduced soil pH, increased soil acid phosphatase activity and soil effective phosphorus content. All effects on mycorrhizosphere were better than those on hyphosphere. Therefore, this study concludes that the introduction of ectomycorrhizal acidifies the soil, increases the activity of soil acid phosphatase, promotes the decomposition of phosphate in the insoluble state of the soil, increases the content of effective phosphorus in the soil, thus promoting the uptake of phosphorus by plants, and plays a role in the growth of Populus davidiana × P. bolleana. Among them, mycorrhizal affect the soil to a greater extent than their hypha.

Ectomycorrhizal association

Growth promotion

Phosphorus activation

Soil available phosphorus

Energy spectrum analysis

Ectomycorrhizal fungi (ECMF) are beneficial microorganisms that are commonly found in rhizosphere soil. They form a reciprocal symbiosis with the plant root system (Genre et al., 2020).

It has long been a common understanding that ectomycorrhiza can promote water and nutrient uptake and transport by plants, thereby promoting plant growth (Rooney et al., 2009). It has been reported that ECMF, in influencing nutrient uptake by host plants, is mainly focused on promoting phosphorus uptake by host plants, especially in the case of phosphorus deficiency (Sato et al., 2019; Shi et al., 2021). ECMF plays an important role in plant phosphorus cycling and turnover (Song et al., 2003).

Phosphorus is an essential nutrient for plant growth and development and is at the center of nutrient metabolic exchange between mycorrhizae and plant roots (Pfeffer et al., 2001). Phosphorus moves slowly in the soil and is mostly in the form of phosphate in an insoluble state, and the amount of phosphorus available for root uptake around plant roots is usually limited. The presence of mycorrhizae, on the one hand, promotes phosphorus uptake by plants, and their extraradical hyphae extends in the soil to reach areas not reached by the root system, crossing the phosphorus deficit zone and allowing plants to take up more phosphorus (Smith et al., 2003&2004; Liu, 2021). On the other hand, mycorrhizal fungi can secrete oxalic acid, tartaric acid, malic acid, citric acid and other organic acids to acidify the soil, thus increasing the activity of acid phosphatase and converting a large amount of insoluble phosphate in the soil into effective phosphorus that can be absorbed and used by plants (Jongmans et al., 1997; Javot et al., 2007; Louche et al., 2011; Wang et al., 2021). When mycorrhiza structures are formed, soils that are affected by both plant roots and mycorrhizal fungi are called "mycorrhizosphere". Soils that are not reached by the root system, only by the extraradical hypha, and are affected only by the hyphae, are called "hypophosphere" (Rambelli, 1973; Linderman, 1988; Li&Cao, 1992).

In this study, Populus davidiana × P. bolleana seedlings were inoculated with S. luteus and P. involutus. Through "compartmented cultivation system" (Li & Cao, 1992) quantitative study of ectomycorrhiza on soil PH, soil acid phosphatase activity and soil available phosphorus content in mycorrhizosphere and hyphosphere. As well as the phosphorus content of seedling tissues and the distribution of phosphorus elements in the root system, to further reveal the effect of ECMF on the activation and uptake of soil phosphorus elements.

1.1 Test materials

Populus davidiana × P. bolleana seedlings were obtained by tissue culture. Test strains: Suillus luteus and Paxillus involutus were isolated from a forest in Zhanggutai experimental forest farm, Changwu County, Liaoning Province.

1.2 Test Preparation

Preparation of sterile soil: To prepare the soil for the purpose, we mixed grass charcoal soil and vermiculite in a ratio of 2:1. Put into sterilization bags in 120℃ autoclave sterilizer for 2 h, put into pots (diameter : 20 cm, height : 14 cm) and set aside.

Preparation of mycorrhizal reagent: About 1 month before seedling transplantation, Suillus iuteus and Paxillus involutus were previously inoculated on a PDA medium (Formula: glucose 20 g, potato 200 g, agar 20 g, KH₂PO₄ 3 g, MgSO₄ 1.5 g, peptone 1.5 g, distilled water 1000 mL). Later it was inoculated in a conical flask (500 mL) containing 200 mL of PDA liquid medium by drilling three pieces with a sterile punch (φ= 1cm). The mycorrhizal reagent was obtained by incubation on a cradle with oscillation (25 °C, 170 RPM). Before its use, we poured mycorrhizal reagent into a disintegrator to stir the mycelium for homogenization. Finally, we mixed homogenized liquid and water in a ratio of 1:3 for later use.

1.3 Experimental design

In this experiment, "compartmented cultivation system" was used to limit the growth space of seedling roots and thus exclude the influence of roots on the soil of hyphosphere, so as to quantitatively analyze the effect of extraradical hyphae of ectomycorrhiza on the relevant physicochemical properties of soil. A three-chamber culture system was made from acrylic panels, with a 30 um aperture nylon mesh separating the culture system into a plant growth compartment, a buffer compartment, and a mycelium compartment. The detailed dimensions of the culture system are shown in Fig.1.

Establish 3 treatment groups: Inoculation with S. luteus (Sl); Inoculation with P. involutus (Sl); No inoculation (CK). We made six replicates of each treatment group, total 18 seedlings.

One Populus davidiana × P. bolleana tissue cultured seedling was transplanted in each plant growth compartment, and after the seedlings were successfully transplanted. Then they were innoculated by perforated root irrigation method (Holes were punched into the rhizosphere soil, and then the bacteria solution was poured into the rhizosphere soil along the holes). Inoculation of 100 mL of bacterial solution per seedling.

The seedlings were harvested 60 d after inoculation treatment. Taking the culture system apart and the 2 cm thick soil on the surface of the root compartment and mycelium compartment was removed. The remaining soil was then well mixed and used to determine soil pH, available phosphorus content and acid phosphatase activity.

1.4 Material and methods

1.4.1 Mycorrhizal colonization rate

After harvesting the seedlings, three seedlings were randomly dug from each treatment to observe mycorrhizal morphology (under stereoscope). Mycorrhizal colonization rate was determined using statistical sampling method. The mycorrhizal colonization rate was calculated according to the following formula:

Mycorrhizal colonization rate (%) = Number of root segments colonized by mycorrhiza/Total number of root segments ×100

1.4.2 Seedling growth index measurement

Seedling height and ground diameter measurement: Three seedlings were randomly sampled from each treatment, and the plant height and ground diameter were measured using a tape measure and vernier caliper, respectively.

Biomass measurement: Electronic balance was used to weigh the fresh weight of aboveground and underground parts, and each treatment was repeated 3 times. Then dried in a constant temperature drying oven at 80 °C to a constant weight, and the dry weight was weighed.

1.4.3 Soil PH measurement

The collected soil samples were air-dried at not more than 40°C and processed through 2 mm sieve.

Preparation of suspensions：Use a measuring cylinder to take 5 ml air-dried soil sample into a 50 mL conical flask, and add 5 times the sample volume of distilled water. Using a mechanical oscillator, the suspension was continuously shaken for 60 min and then left to stand for 2 h, during which time air should be avoided from entering the conical flask.

pH measurement：At 20 ± 2 °C, the suspension was stirred before measurement so that the soil particles could be distributed relatively uniformly in the suspension without entrapping air, and then pH was measured immediately (Li et al., 2007).33

1.4.4 Soil acid phosphatase activity measurement

Soil acid phosphatase activity was measured by spectrophotometric method. 0.1g of the above fresh soil was accurately weighed and placed in a 1.5 mL centrifuge tube for measurement by Nanjing Jiancheng Kit.

1.4.5 Soil available phosphorus content measurement

Extraction and measurement of available phosphorus content: Weigh 2.50 g of air-dried soil sample after a 1mm screen, put it in a 150 mL dry conical flask, add 50 mL distilled water, keep the liquid temperature at 25℃, shake for 30 min on a 180 RPM Oscillator, filter immediately with Phosphorus-free filter paper, and leave the filtrate to be measured. Referring to the Chinese national standard (LY/T1233-1999), the molybdenum antimony anti-colorimetric method was used for the measurement.

1.4.6 Plant tissue phosphorus measurement

Extraction and measurement of tissue phosphorus content: The harvested seedlings were placed in a constant temperature drying oven at 80℃ to dry. The samples were pulverized and digested using H₂SO₄-H₂O₂. Accurately absorb 4 mL of the digestion solution into a 50 mL volumetric flask for determination of tissue phosphorus content. Referring to Li-Ping's method (Li, 2020). The molybdenum antimony anti-colorimetric method was used for the determination.

1.4.7 root system segment surface scanning electron microscope and element energy spectrum analysis

The roots were washed with tap water when the seedlings were harvested, and the roots were cut off under a stereoscope. The samples were placed in glass vials with fixation fluid, pump the air out of the bottle and stored in a 4℃ refrigerator. The samples were sent to the Analysis and Testing Center of Shenyang Agricultural University and analyzed by Hitachi Regulus 8100 electron microscope for root system segment surface scanning and phosphorus elemental energy spectrum.

1.5 Data Analysis

The obtained data were collated using Office Excel 2018; a one-way analysis of the significance of differences with SPSS 26.0, α = 0.05; plotted with GraphPad Prism 8.0.

2.1 Mycorrhizal colonization rate

Because the seedlings used in this experiment were tissue culture seedlings and the soil was sterilized sterile soil in advance, no ectomycorrhizal formation was found in the control group. As shown in Fig. 2, both ectomycorrhizal fungi could form ectomycorrhiza with Populus davidiana × P. bolleana, among which the colonization rate of S. luteus was 68.08% and that of P. involutus was 64.17%, showing no significant difference between the two treatments.

2.2 Growth indexes under different inoculation treatments

As shown in Fig. 3, inoculation with both ECMF treatments significantly increased seedling height, ground diameter and biomass of Populus davidiana × P. bolleana seedlings, with significant differences compared to the control. Inoculated S. luteus treatment was superior to inoculated P. involutus treatment, and the difference of ground diameter between the two was significant, while the other differences were not significant (P < 0.05). Compared with the control group, seedling height, ground diameter, above-ground fresh weight, above-ground dry weight, below-ground fresh weight and below-ground dry weight increased by 27.69%, 45.49%, 87.73%, 207.14%, 253.41% and 194.12%, respectively, in the S. luteus inoculation treatment. Compared with the control group, seedling height, ground diameter, aboveground fresh weight, aboveground dry weight, belowground fresh weight and belowground dry weight increased by 23.29% , 17.71%, 57.63%, 123.47%, 145.45% and 117.65%, respectively, in the P. involutus inoculation treatment.

2.3 Soil pH values under different inoculation treatments

As shown in Fig. 4, inoculation of both ECMF treatments reduced the pH values of both mycorrhizosphere and hyphosphere soils. Compared with the control group, inoculation with S. luteus treatment significantly reduced the pH value of mycorrhizosphere and hyphosphere soil ( P < 0.01); inoculation with P. involutus treatment significantly reduced the pH value of hyphosphere soil ( P < 0.05). Inoculation with S. luteus treatment had lower soil PH than inoculation with P. involutus treatment, but the difference was not significant. Compared with the control group, the mycorrhizosphere PH and hyphosphere PH of S. luteus treatment decreased by 8.92% and 2.91%, respectively. Compared with the control group, the mycorrhizosphere PH and hyphosphere PH of P. involutus treatment decreased by 4.30% and 1.98%, respectively.

2.4 Soil acid phosphatase activity under different inoculation treatments

As shown in Fig. 5, inoculation of both ECMF treatments increased the acid phosphatase activity of both mycorrhizosphere and hyphosphere soils. Compared with the control group, inoculation with S. luteus treatment significantly increased the acid phosphatase activity of mycorrhizosphere and hyphosphere soil (P＜0.001); inoculation with P. involutus treatment significantly increased the acid phosphatase activity of hyphosphere soil ( P＜0.001). Compared with P. involutus treatment, S. luteus treatment had higher acid phosphatase activity, and the difference between the two mycorrhizosphere soil acid phosphatase activity was significant (P < 0.01). Compared with the control group, the acid phosphatase activity of mycorrhizosphere and hyphosphere soil inoculated with S. luteus increased by 103.24% and 76.88%, respectively. Compared with the control group, the acid phosphatase activity of mycorrhizosphere and hyphosphere soil inoculated with P. involutus increased by 80.77% and 62.48%, respectively.

2.5 Content of available soil phosphorus under different inoculation treatments

As shown in Fig. 6, inoculation of both ECMF treatments increased the available phosphorus content of both mycorrhizosphere and hyphosphere soils. Compared with the control group, inoculation with S. luteus treatment significantly increased the available phosphorus content of mycorrhizosphere (P＜0.001) and hyphosphere soil ( P＜0.01); inoculation with P. involutus treatment significantly increased the available phosphorus content of mycorrhizosphere soil ( P＜0.05). Compared with P. involutus treatment, S. luteus treatment had higher available phosphorus content, and the difference between the two hyphosphere soil available phosphorus content was significant (P < 0.01). Compared with the control group, the available phosphorus content of mycorrhizosphere and hyphosphere soil inoculated with S. luteus increased by 60.82% and 53.84%, respectively. Compared with the control group, the available phosphorus content of mycorrhizosphere and hyphosphere soil inoculated with P. involutus increased by 46.03% and 43.21%, respectively.

2.6 Phosphorus content of tissues under different inoculation treatments

As shown in Fig. 7, inoculation of both ECMF treatments increased the phosphorus content of the roots, stems and leaves of Populus davidiana × P. bolleana seedlings. Compared with the control group, inoculation with S. luteus significantly increased the phosphorus content in roots (P < 0.05), stems (P < 0.01) and leaves (P < 0.05) . Compared with the control group, inoculation with P. involutus significantly increased the phosphorus content in stems (P < 0.01) . Compared with P. involutus treatment, S. luteus treatment had higher phosphorus content in the roots, stems and leaves of seedlings. Compared with the control group, the phosphorus content in the roots, stems and leaves of seedlings inoculated with S. luteus increased by 51.84%, 74.23% and 55.81%, respectively. Compared with the control group, the phosphorus content in the roots, stems and leaves of seedlings inoculated with P. involutus increased by 17.09%, 45.36% and 30.48%, respectively.

2.7 Scanning electron microscopy and energy spectrum analysis of root system segment surface under different inoculation treatments

The energy spectrum analysis of the root system segment surface was performed by line analysis (Fig. 8). First, a straight line is drawn on the root system segment surface, and then the line is scanned. Because each group delineates a different length of straight line, after the scan is completed, the root system segment surface is analyzed for 650 points from the center outward, where two adjacent points are separated by 0.2 μm, and the total length of the analyzed line segment is 129.8 μm.

As shown in Fig. 10, the Roi (Region of interest, Represents the level of elements that can be observed in the region) values of the root system segment surface energy spectrum analysis of the sansin Populus davidiana×P. bolleana seedlings inoculated with both ECMF treatments were higher than those of the control. Inoculation with S. luteus treatment significantly increased Roi values of root system segment surface compared to the control (P < 0.001). Inoculation with P. involutus treatment significantly increased Roi values of root system segment surface compared to the control (P＜0.05). The Roi values of the inoculated S. luteus treatment were higher than those of the inoculated P. involutus treatment. Compared to the control group, inoculation of S. luteus treatment increased the Roi value by 40.14%. Compared to the control group, inoculation of P. involutus treatment increased the Roi value by 20.74%.

According to the findings of this study, S. luteus and P. involutus can form ectomycorrhiza with Populus davidiana × P. bolleana. Inoculation with both types of ECMF significantly increased seedling height, ground diameter, biomass, and tissue phosphorus content of Populus davidiana × P. bolleana seedlings. Inoculation of both ECMF significantly reduced soil pH and increased soil acid phosphatase activity and soil available phosphorus content. Among them, mycorrhizal affect the soil to a greater extent than their hypha.

In summary, the ectomycorrhiza formed by Populus davidiana × P. bolleana with S. luteus and P. involutus and their hypha both acidified the soil, increased the activity of soil acid phosphatase, promoted the decomposition of phosphate in the insoluble state of the soil, and increased the content of available soil phosphorus, thus promoting the uptake of phosphorus elements by plants.

4.1 Effect of ECMF on the growth of Populus davidiana × P. bolleana seedlings

Poplar has a close relationship with fungi, which not only provides growth substrate for woody fungi (Dai et al., 2003), but also is a typical mycorrhizal dependent tree species, it can form ectomycorrhiza with many kinds of ECMFs (Tang et al., 1994; Yuan et al., 2014). When ECMF forms a symbiotic relationship with plants, it has a very significant contribution to plant growth and the ability to adapt to the environment.

Many reports indicate that the symbiosis of ECMF and plants can significantly increase the seedling height, ground diameter and biomass of host plants (Song et al., 2007; Zhang and Yan, 2013; Qi et al., 2019). In this study, inoculation with ECMF treatment significantly increased seedling height, ground diameter and biomass of Populus davidiana × P. bolleana seedlings (Fig. 2). This finding is the same as that reported above, which indicates that inoculation of ECMF has a significant promotion effect on seedling height and ground diameter growth of Populus davidiana × P. bolleana seedlings. The effect of ECMF on plant growth is multifaceted. First, ECMF forms a dense layer of fungal mantle on the surface of plant absorbing roots, and by extending a large number of extraradical hyphae into the soil around the roots, the large mycelial network expands the absorption area of the root system, thus enhancing the host plant's ability to absorb water and various mineral nutrients from the soil (Smith, 1997&2003; Querejeta et al., 2007; Lehto et al., 2011). Secondly, besides the wide coverage of hyphae network, the root diameter is about 1-2 times the diameter of hyphae, and the hyphae can reach into smaller soil pores to absorb nutrients, which can also expand the root uptake area (Smith et al., 2010). Finally, the uptake function of root hairs generally lasts only a few days, but the uptake function of ectomycorrhiza and its hyphae can last for a whole growing season, so the ectomycorrhiza can help the root system to absorb water and various mineral nutrients for a longer period of time (Bai, 2006). Therefore, in this study, inoculation with ECMF promoted the growth of the Populus davidiana×P. bolleana seedlings, making them significantly better than the non-inoculated seedlings in terms of seedling height, ground diameter and biomass.

4.2 ECMF promotes the activation of rhizosphere soil phosphorus

Phosphorus mostly exists in the form of inorganic PO₄^3-and organic phosphoric acid in soil, and PO₄^3- is easy to be fixed by Ca²⁺, Fe³⁺, Al³⁺ and other metal ions in soil or is chelated by soil colloid to transform into insoluble phosphate and lose its effectiveness, which is difficult to be absorbed and utilized by trees (Yang et al., 1999).

Many reports indicate that ECMF is capable of solubilizing insoluble phosphates (Lapeyrie et al., 1991; Liu et al., 2010). This is due to the ability of ECMF to secrete large amounts of various organic acids such as oxalic acid, acetic acid, malic acid, citric acid and succinic acid (Griffit et al., 1994; Xu et al., 2000; Yang et al., 2015). In the present study, both groups inoculated with ECMF treatment had significantly lower mycorrhizosphere soil and hyphosphere soil pH (Fig. 4). This finding is the same as that reported above, which has a very important role in solubilizing insoluble phosphates. ECMF secretion of large amounts of organic acids lowers soil pH, making the soil acidified and, on the one hand, promoting acidolysis of weakly acid-soluble phosphorus such as calcium phosphate and apatite (Andersoon et al., 2015). On the other hand, an acidified soil environment increases the activity of soil acid phosphatase, which converts a large amount of phosphate in the soil in an insoluble state into effective phosphorus that is available for plant uptake (Jongmans et al., 1997; Javot et al., 2007; Louche et al., 2011; Wang et al., 2021) (Fig. 11). In this study, acid phosphatase activity (Fig. 5) and effective soil phosphorus content (Fig. 6) were significantly increased in the mycorrhizosphere soil and hyphosphere soil of both groups inoculated with ECMF treatment. Therefore, ECMF promotes the activation of soil phosphorus by secreting organic acids and decomposing insoluble phosphate in soil.

It can be seen that inoculation of both ECMF treatments affected the pH, acid phosphatase activity and effective phosphorus content of both mycorrhizosphere and hyphosphere soils, but the degree of effect was more significant in mycorrhizal than hypha. Therefore, it can be inferred that inoculation of both ECMF treatments, their mycorrhizal and hypha played a role in soil phosphorus activation, but the degree of influence of mycorrhizal was greater than that of their hypha.

4.3 ECMF promotes the uptake of rhizosphere soil phosphorus by plants

Mycorrhizal symbiosis is one of the important mechanisms to improve the efficient use of phosphorus in plants (Pang et al., 2016). There are two ways for plants to absorb phosphorus in soil, one is through the root epidermis and root hairs directly, and the other way is mycorrhizal uptake (Smith et al., 2003; Liu, 2021). Mycorrhizal uptake is considered to be the most important form of phosphorus uptake under low phosphorus conditions, and almost all of the phosphorus absorbed by plant roots after mycorrhizal formation is absorbed through the hypha, while direct phosphorus uptake by root epidermis and root hairs is negligible (Smith et al., 2004).

Many reports suggest that ECMF can enhance phosphorus uptake and utilization by the host after forming a symbiosis with plant roots (Wu et al., 2008; Song et al., 2009).In the present study, the phosphorus content of seedling tissues (Fig. 7) and the level of phosphorus elements analyzed in the root system segment energy spectrum (Figs. 9 and 10) were significantly increased in both groups inoculated with ECMF treatment. This finding was the same as that reported above, and the results indicated that inoculation of ECMF promoted the uptake of soil phosphorus by Populus davidiana × P. bolleana seedlings. The main mechanisms by which ECMF promotes the uptake and utilization of phosphorus by plants are, firstly, the extension of mycorrhizal extraradical hyphae in the soil, which can reach areas not reached by the root system and cross the phosphorus deficit zone, expanding the uptake of phosphorus. Secondly, ECMF absorbs phosphorus with low Km values (H₂PO^4-/HPO₄^2-), high affinity and low critical absorption concentrations (Arocena et al., 2000). Finally, in the process of symbiosis with plants, ECMF itself and its extraradical hyphae can secrete a large amount of organic acids, which can transform weak acid-soluble phosphorus and insoluble phosphate in soil into effective phosphorus for trees to absorb and utilize (Fig. 11). Therefore, in this study, inoculation of ECMF promoted the uptake of phosphorus from soil by the seedlings of Populus davidiana × P. bolleana.

Liaoning Provincial Department of Education project(LJKZ0684)

Funding National Natural Science Foundation of China (31800542).

Compliance with Ethical Standards

Conflict of interest：The authors declare that they have no conflicts of interest

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Effect of ectomycorrhizal fungi on the activation and uptake of phosphorus in Populus davidiana×P. bolleana mycorrhizosphere and hyphosphere

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