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Evidence for a Dark Septate Endophyte (Exophiala Pisciphila, H93) Enhancing Phosphorus Absorption by Maize Seedlings

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Abstract

Background and aims

Dark septate endophytes (DSE) are a group of multifunctional fungi that ubiquitously colonize the roots of numerous plants worldwide, benefiting the nutrition and adaptation of hosts to various stressed environments. How DSE benefit phosphorus absorption by their host plants remains unclear.

Methods

We established pot cultures and compartmentalized microcosms in the greenhouse and used transcriptomic analysis to examine the response of maize to inoculation with a DSE strain, Exophiala pisciphila H93, which has been found to be capable of promoting plant growth and enhancing the tolerance of maize to heavy metals.

Results

H93 promoted the biomass, phosphorus absorption and photosynthesis of inoculated maize by enhancing phosphorus enzyme activities in the rhizosphere and by decreasing the pH of the rhizosphere compared with non-inoculated controls, either in sufficient or deficient phosphorus conditions in pot cultures. H93 inoculation changed the transcriptional pattern of maize related to 8 metabolic pathways. While H93 did not induce particular phosphate transporter gene expression under deficient phosphorus conditions, it dissolved the sparingly soluble phosphates (tricalcium phosphate) in the rhizosphere.

Conclusions

Enhanced phosphorus absorption by the host plant by DSE (H93) seemed to occur independently of DSE-induced genes involved in phosphorus absorption. The greatest contribution of DSE to phosphorus utilization of hosts might be their efficiency in transferring sparingly soluble phosphorus into soluble phosphate (Pi).

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Abbreviations

DSE:

Dark septate endophytes

P:

Phosphorus

Pi:

Inorganic orthophosphate

TCP:

Tricalcium phosphate

Pts:

Phosphate transporters

PBRMs:

Plant beneficial rhizosphere microorganisms

AMF:

Arbuscular mycorrhizal fungi

PAE:

Phosphorus acquisition efficiency

PUE:

Phosphorus use efficiency

PVK:

Pikovskaya’s medium

IR:

Inhibition rate

PR:

Promotion rate

References

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Acknowledgments

This research was financially supported by the Yunnan Provincial Science and Technology Department-Yunnan University Joint Fund, the key project (2018FY001-010), “Double First-Class” University Project of Yunnan University (C176282105) and the National Natural Science Foundation of China (31460114 and 41461073).

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Correspondence to Zhi-Wei Zhao.

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Responsible Editor: Felipe E. Albornoz.

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Fig. S1

Morphological characteristics of DSE colonizing the roots of maize inoculated with E. pisciphila in the pot culture and compartmentalized microcosm (hypha is showed by dashed arrow while microsclerotium is pointed by solid arrow; bar = 50 μm). (PNG 5915 kb)

High Resolution Image (EPS 100403 kb)

Fig. S2

Venn diagram of differentially expressed genes in maize root in response to different treatments with Pi and DSE in pot culture (+, upregulated; −, downregulated; + +, upregulated in both groups; + −, upregulated in the left group and downregulated in the right group; − +, downregulated in the left group and upregulated in the right group; − −, downregulated in both groups.) (PNG 190 kb)

High Resolution Image (EPS 1442 kb)

Fig. S3

Significantly enriched pathways in maize roots related to up/downregulated DEGs responsible for Pi deficiency and DSE inoculation in pot culture ([3.1.3.12] trehalose 6-phosphate synthase/phosphatase; [3.2.1.21] beta-glucosidase; [2.7.1.1] hexokinase; [2.7.1.11] 6-phosphofructokinase 1; [4.1.2.13] fructose-bisphosphate aldolase, class I; [5.3.1.1] triosephosphate isomerase (TIM); [2.7.1.40] pyruvate kinase; [4.1.1.1] pyruvate decarboxylase; [1.1.1.27] L-lactate dehydrogenase; [1.1.1.1] S-(hydroxymethyl) glutathione dehydrogenase / alcohol dehydrogenase; [1.4.1.13] glutamate synthase 2 (NADH); [1.4.1.14] glutamate synthase (NADH); [6.3.1.2] glutamine synthetase; [1.13.11.19] cysteamine dioxygenase; [4.1.1.15] glutamate decarboxylase. Colors from dark blue to dark red indicate gene expression from low to high.) (PNG 1078 kb)

High Resolution Image (EPS 5344 kb)

Fig. S4

Transcriptional changes in ZmPHT1 genes responsible for Pi deficiency and DSE inoculation in maize roots in pot culture (ZmPHT1;10 was not detected in the present study. Colors from dark blue to dark red indicate gene expression from low to high.) (PNG 87 kb)

High Resolution Image (EPS 836 kb)

Table S1 & S2

Table S1. Inhibition rate (IR, %) of Pi deficiency on parameters of maize growth in pot culture and promotion rate (PR, %) of DSE on the maize tested parameters in pot culture and compartmentalized microcosm. Table S2. DSE biomass and soluble P, phosphatase activity and pH in the fermentation broth (mean ± SE, n = 3) treated with different P source for 10 days. (DOCX 25 kb)

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Xu, R., Li, T., Shen, M. et al. Evidence for a Dark Septate Endophyte (Exophiala Pisciphila, H93) Enhancing Phosphorus Absorption by Maize Seedlings. Plant Soil 452, 249–266 (2020). https://doi.org/10.1007/s11104-020-04538-9

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  • DOI: https://doi.org/10.1007/s11104-020-04538-9

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