Elsevier

Rhizosphere

Volume 19, September 2021, 100360
Rhizosphere

Effect of mycorrhizal fungi inoculation on bacterial diversity, community structure and fruit yield of blueberry

https://doi.org/10.1016/j.rhisph.2021.100360Get rights and content

Abstract

Mycorrhizal fungus is one of the most common and widespread symbiosis formed in the rhizosphere of plants which enhances the diversity and abundance of bacteria in the rhizosphere soil of plants on the basis of promoting plant growth, increasing its yield and saving costs. As an important group of soil microorganisms, bacteria can effectively promote soil material circulation and energy flow. Bacterial diversity and community structure can reflect the quality of soil. The bacterial diversity and community distribution in the rhizosphere soil of blueberry inoculated with different mycorrhizal fungi were analyzed and compared based on the bacterial 16S rRNA high-throughput sequencing technology. The membership function comprehensive evaluation method was used to find out the increase in bacterial community diversity, abundance and the most suitable inoculation strain for fruit yield. The bacterial diversity in blueberry rhizosphere soil was rich. The bacterial diversity in Cladosporium cladosporioides (ZB) and Phialocephala fortinii (DSE) treatments was significantly higher than that in other treatments. A total of 41 phyla, 107 classes, 154 orders, 289 families, 476 genera, and 476 genera were detected in the soil samples. Proteobacteria (36.5%–52.5%), of which Alphaproteobacteria (21.2%–37.9%) was the dominant subgroup, Rhizobiales (14.7%–26.7%), Burkholderiaceae (0.9%–22.1%), Acidothermus (10.3%–21.8%) was the dominant order, family and genus, respectively. The infection rate was the most significant under the DSE treatment (P < 0.05) along with increased its fruit yield. In addition, the membership function analysis showed that ZB was the best strain to improve the bacterial community diversity and fruit yield of rabbit eye blueberry rhizosphere, followed by DSE. These findings provide scientific data for the development and utilization of soil microbial resources and contribute a favorable guarantee for blueberry cultivation and production.

Introduction

Rhizosphere is one of the most important matrix of soil surrounding plant roots which is highly supportive for microbial communities (Berendsen et al., 2012; Del Carmen Orozco-Mosqueda et al., 2018). Microbial interactions present in the rhizosphere are crucial for plant growth, health, development and productivity (Philippot et al., 2013; Schmeisser et al., 2007). Plant inoculation with beneficial microbes plays a supportive role in order to enhance beneficial microbial interaction (Aeron et al., 2011). Plant growth promoting rhizobacteria (PGPR) act as functional group that is capable of promoting growth and development, disease suppression and availability of plants nutrients (Chabot et al., 1993; Kloepper et al., 1980; Edwards et al., 2015; Morrison et al., 2017). All microbes associated to a plant's endosphere, rhizosphere, and phyllosphere play a critical role in plant growth and its health (Berendsen et al., 2012; Compant et al., 2019). Rhizosphere is influenced by plant roots through secretion of various compounds, including amino acids, fatty acids, sugars and vitamins, and organic acids providing the place for microbial growth (Del Carmen Orozco-Mosqueda et al., 2018; Compant et al., 2019; Pascale et al., 2020; Saad et al., 2020). Several abiotic factors including soil pH,moisture, and soil nutrients have greater impact on rhizosphere microbiome (Lemanceau et al., 1995; Bakker et al., 2015). The rhizosphere was studied to contain a larger number of microbial species richness as compared to phyllosphere (Rodriguez et al., 2019). Previous studies were revealed the impact of PGPR on indigenous bacterial communities i.e. inoculation of Azospirillum strains in Solanum lycopersicum L., Triticum sativum L., and Zea mays L. rhizospheres (Bashan et al., 1995; Castro-Sowinski et al., 2007; Felici et al., 2008). In addition, various Pseudomonas strains effects are studied in Hordeum vulgare L., and Solanum tuberosum L. rhizospheres (Castro-Sowinski et al., 2007; Buddrus-Schiemann et al., 2010; Roquigny et al., 2018). Direct effect of bacterial inoculations were also documented on plant microbiome including Vicia faba L. (Zhang et al., 2010), Glycine max L. (Zhang et al., 2011), Brassica rapa L. (Bhattacharyya et al., 2016), and Pseudomonas species in Z. mays L. (Kozdrój et al., 2004, 2008).

Among various microorganisms, mycorrhizal fungus is one of the most common and widespread symbionts in the rhizosphere of plants (Pohjanen et al., 2014). In the symbiotic relationship, up to 80% of the nitrogen and phosphorus required for the plant are passed through the mycorrhizal fungus. (Brundrett et al., 2009; Lekberg et al., 2014; Lindahl et al., 2015). Mycorrhizal fungi can adjust the diversity and community structure of rhizosphere bacteria by changing soil enzyme activities and rhizosphere nutrition, enhance plant resistance to biotic and abiotic stresses, increase plant hormone synthesis and distribution (Bingham et al., 2012; Heinonsalo et al., 2015). The growth of most plants is greatly affected by mycorrhizal fungus, and even cannot survive. In view of its important role in the ecosystem, the study of mycorrhizal symbiosis has attracted widespread attention from scholars around the world (Hart et al., 2003; Booth et al., 2004). Therefore, studying the relationship between mycorrhiza and plant rhizosphere soil bacterial community environment is of great significance for understanding plant rhizosphere community structure, biodiversity, and improving fruit yield (Chagnon et al., 2012).

Blueberry, a vaccinium plant that belongs to Ericaceae family with high nutritional value (Zheng et al., 2017; Lin et al., 2018). In China, blueberries cultivated area was estimated 31,210 hm2 with a yield of 114,905 tons (Elks et al., 2013). Among these plants are mainly cultivated in Guizhou Province in area of 13,000 hm2 with a yield of 30,000 tons (Li et al., 2018). Several studies were reported that wild blueberry mycorrhizal fungi has infection rate of up to 75% in natural envirnment but under artificial cultivation conditions, mycorrhizal infection rate was less than 3% (Haynes et al., 1985). Further studied showed that if blueberries inoculated with artificial mycorrhiza, the mycorrhizal infection rate and biomass increased significantly compared with non-inoculation (Bizabani et al., 2016). In addition, inoculation can improve the photosynthesis and drought resistance of blueberry plants (Gui et al., 2020; Yang et al., 2019).

At present, the research of blueberry mycorrhiza mainly focused on the effects of photosynthesis and antioxidant capacity of plants (Yang et al., 2019; Gui et al., 2021). There are few reports on the changes of blueberry plant rhizosphere community environment after inoculation of mycorrhiza, especially the effect of changes in rhizosphere bacterial community diversity on plant growth and development. Bacteria are active microorganisms in the soil. Their types, population structure, and biodiversity can largely reflect the status and changes of soil fertility (Hanaka et al., 2019). By exploring the interaction between mycorrhizal fungi and rhizosphere soil bacterial communities, it will help to make better use of the rhizosphere soil bacterial environment to improve the growth-promoting effect of mycorrhiza. It plays an important role in increasing crop yields and maintaining the stability of the agricultural and forestry ecosystem. In this study, through preliminary experiments and combined with previous studies (Paul et al., 2013; Zhai et al., 2018; Li et al., 2018; Ibiang et al., 2020), we used five highly effective growth-promoting mycorrhizal fungi selected from the roots of artificially planted blueberries in Guizhou and studied the changes of blueberry rhizosphere soil enzyme activity, bacterial community structure, biodiversity and fruit yield. Combined with the analysis of the membership function, the inoculation effect of each strain was comprehensively evaluated.

Section snippets

Research area

The sampling site was located at Yanggai Blueberry Test Base, Kaili City, Guizhou Province (107°61′ E: 26°52′ N). The average temperature of sampling site recorded with max.14.9 °C, min. −2 °C and the average elevation of mountainous region with 900 m was measured. It belonging to a subtropical monsoon humid climate with frost-free period is 283 days. The annual precipitation was recorded about 1300 mm and the annual sunshine hours exceeded 1200 h, respectively. The physical and chemical

Soil enzyme activity analysis

In order to estimate the enzymatic activity of soil, blueberry experimental seedlings after different inoculation treatments were obtained the rhizosphere soil in late June 2019 (Wu et al., 2015). Rhizosphere soil was placed into the sterilized centrifuge tube and stored in refrigeration for future analysis. The soil sample was divided into two parts. One part was used for soil microbial population structure diversity analysis, while other part was air-dried to remove impurities. After sieving,

Effect of inoculation on soil enzyme activity

Inoculation had a significant effect on the content of blueberry rhizosphere soil urease (Soild urease), catalase activity (Catalase activity), soil acid phosphatase (Phosphatase activity), and sucrase activity (P < 0.05) as compared to CK. Among them, SS showed the most significant effect on catalase, while LZ improved soil urease activity, invertase activity, and acid phosphatase activity. It indicated that the inoculation of mycorrhizal fungi can significantly improve the enzyme activity of

Plant infection characteristics under different inoculation modes

Mycorrhiza plays an important role in promoting the growth of blueberries. Mycorrhizal fungi are widespread in wild blueberries with 75% infection rate. However, it is very difficult for blueberries to form mycorrhizal fungi under artificial cultivation conditions due to its long process. In North Carolina, 85% the infection rate 1%–3% in plantations of mycorrhizal fungi in wild was studied (Haynes et al., 1985). In this study, infection rate of blueberry plants inoculating with different

Conclusions

We obtained significant results with application of different inoculation methods for bacterial diversity of blueberry soils. We found that DSE and ZB mycorrhizal infection rate was significantly improved the bacterial diversity and fruit yield of blueberry rhizosphere soil. With the combination of membership function, ZB was considered the best strain to improve the bacterial community diversity and fruit yield of rabbit eye blueberry rhizosphere followed by DSE. In addition, soil properties

Author contributions

“Conceptualization, W.-D.L and G.-X.L; methodology, G.-X.L., X.-L.H. and M.S.; software, G.-X.L. and W.-Y.Q.; formal analysis, G.-X.L. and W.-Y.Q.; investigation, X.-L.H.; resources, W.-Y.Q.; data curation, M.S. and W.-Y.Q.; writing—original draft preparation, G.-X.L.; writing—review and editing, G.-X.L. M.S. and W.-D.L.; visualization, W.-Y.Q.; supervision, M.S.; All authors have read and agreed to the published version of the manuscript.“;

Funding

“This research was funded by the National Natural Science Foundation of China (grant no.31760205).

Data availability statement

The data presented in this study are available on request from the corresponding author.

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.

Acknowledgements

We are thankful to National Natural Science Foundation of China (31760205) for its financial support.

References (64)

  • Y. Lin et al.

    Comparative transcriptome analysis of genes involved in anthocyanin synthesis in blueberry

    Plant Physiol. Biochem.

    (2018)
  • P.A. Rodriguez et al.

    Systems biology of plant-microbiome interactions

    Mol. Plant

    (2019)
  • A. Aeron et al.

    Emerging role of plant growth promoting rhizobacteria in agrobiology

  • K. Ahlich et al.

    The profusion of dark septate endophytic fungi in non‐ectomycorrhizal fine roots of forest trees and shrubs

    New Phytol.

    (1996)
  • M.G. Bakker et al.

    Impacts of bulk soil microbial community structure on rhizosphere microbiomes of Zea mays

    Plant Soil

    (2015)
  • Y. Bashan et al.

    Survival of Azospirillum brasilense in the bulk soil and rhizosphere of 23 soil types

    Appl. Environ. Microbiol.

    (1995)
  • M.A. Bingham et al.

    Ectomycorrhizal networks of Pseudotsuga menziesii var. glauca trees facilitate establishment of conspecific seedlings under drought

    Ecosystems

    (2012)
  • M.G. Booth

    Mycorrhizal networks mediate overstorey‐understorey competition in a temperate forest

    Ecol. Lett.

    (2004)
  • M.C. Brundrett

    Mycorrhizal associations and other means of nutrition of vascular plants: understanding the global diversity of host plants by resolving conflicting information and developing reliable means of diagnosis

    Plant Soil

    (2009)
  • K. Buddrus-Schiemann et al.

    Root colonization by Pseudomonas sp. DSMZ 13134 and impact on the indigenous rhizosphere bacterial community of barley

    Microb. Ecol.

    (2010)
  • R.J. Case et al.

    Use of 16S rRNA and rpoB genes as molecular markers for microbial ecology studies

    Appl. Environ. Microbiol.

    (2007)
  • S. Castro-Sowinski et al.

    Effects of inoculation with plant growth-promoting rhizobacteria on resident rhizosphere microorganisms

    FEMS Microbiol. Lett.

    (2007)
  • R. Chabot et al.

    Stimulation de la croissance du maïs et de la laitue romaine par des microorganismes dissolvant le phosphore inorganique

    Can. J. Microbiol.

    (1993)
  • P.L. Chagnon et al.

    Using ecological network theory to evaluate the causes and consequences of arbuscular mycorrhizal community structure

    New Phytol.

    (2012)
  • P. Das et al.

    Root fungal associations in Gaultheria fragrantissima

    Journal of Agricultural Technology

    (2012)
  • S.N. Dedysh et al.

    NifH and NifD phylogenies: an evolutionary basis for understanding nitrogen fixation capabilities of methanotrophic bacteria

    Microbiology

    (2004)
  • M. Del Carmen Orozco-Mosqueda et al.

    Microbiome engineering to improve biocontrol and plant growth-promoting mechanisms

    Microbiol. Res.

    (2018)
  • J. Edwards et al.

    Structure, variation, and assembly of the root-associated microbiomes of rice

    Proc. Natl. Acad. Sci. Unit. States Am.

    (2015)
  • C.M. Elks et al.

    11 Overview of the Health Properties of Blueberries. Bioactives in Fruit: Health Benefits and Functional Foods

    (2013)
  • L.X. Gui et al.

    iTRAQ-based proteomic analysis reveals positive impacts of arbuscular mycorrhizal fungi inoculation on photosynthesis and drought tolerance in blueberry

    Trees (Berl.)

    (2021)
  • A. Hanaka et al.

    Relationships between the properties of Spitsbergen soil, number and biodiversity of rhizosphere microorganisms, and heavy metal concentration in selected plant species

    Plant Soil

    (2019)
  • H.U. Jun-Li et al.

    Arbuscular mycorrhizal fungal inoculation enhances suppression of cucumber Fusarium wilt in greenhouse soils

    Pedosphere

    (2010)
  • Cited by (21)

    • Cultivable rhizobacteria improve castor bean seedlings root and plant growth in Pb–Zn treated soil

      2021, Rhizosphere
      Citation Excerpt :

      In recent years, many researchers have found that culturable bacteria have higher biological and metabolic activities than strains in pure culture and are important contributors to soil ecological functions (Chen et al., 2019; Guo et al., 2021).

    View all citing articles on Scopus
    1

    These authors contributed equally to the work.

    View full text