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Heat stress promotes the conversion of putrescine to spermidine and plays an important role in regulating ganoderic acid biosynthesis in Ganoderma lucidum

  • Applied Genetics and Molecular Biotechnology
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Abstract

Heat stress (HS) is inescapable environmental stress that can induce the production of ganoderic acids (GAs) in Ganoderma lucidum. Our previous studies found that putrescine (Put) played an inhibitory role in GAs biosynthesis, which appeared to be inconsistent with the upregulated transcription of the Put biosynthetic gene GlOdc under HS. To uncover the mechanism underlying this phenomenon, two spermidine (Spd) biosynthetic genes, GlSpds1 and GlSpds2, were identified and upregulated under HS. Put and Spd increased by 94% and 160% under HS, respectively, suggesting that HS induces polyamine biosynthesis and promotes the conversion of Put to Spd. By using GlSpds knockdown mutants, it is confirmed that Spd played a stimulatory role in GAs biosynthesis. In GlOdc-kd mutants, Put decreased by 62–67%, Spd decreased by approximately 34%, and GAs increased by 15–22% but sharply increased by 75–89% after supplementation with Spd. In GlSpds-kd mutants, Put increased by 31–41%, Spd decreased by approximately 63%, and GAs decreased by 24–32% and were restored to slightly higher levels than a wild type after supplementation with Spd. This result suggested that Spd, rather than Put, is a crucial factor that leads to the accumulation of GAs under HS. Spd plays a more predominant and stimulative role than Put under HS, possibly because the absolute content of Spd is 10 times greater than that of Put. GABA and H2O2, two major catabolites of Spd, had little effect on GAs biosynthesis. This study provides new insight into the mechanism by which environmental stimuli regulate secondary metabolism via polyamines in fungi.

Key points

• HS induces polyamine biosynthesis and promotes the conversion of Put to Spd in G. lucidum.

• Put and Spd played the inhibitory and stimulatory roles in regulating GAs biosynthesis, respectively.

• The stimulatory role of Spd was more predominant than the inhibitory role of Put in GAs biosynthesis.

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Data availability

All experimental data in this study will be made available upon reasonable request from readers.

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Acknowledgements

This work was supported by grants from the National Key R&D Program of China (2019YFC1710501), the China Agriculture Research System of MOF and MARA (NO. CARS-20 to Mingwen Zhao), the National Natural Science Foundation of China (81773839 to Ang Ren and 31902088 to Yongxin Tao), the Natural Science Foundation for Distinguished Young Scholar of Fujian Agriculture and Forestry University of China (xjq201919 to Yongxin Tao), and the Natural Science Foundation of Fujian Province of China (2019J01380 to Yongxin Tao).

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Authors and Affiliations

  1. College of Horticulture, Fujian Agriculture and Forestry University, Fuzhou, 350002, Fujian, China

    Yongxin Tao, Jian Li & Hanbing Song

  2. Mycological Research Center, College of Life Sciences, Fujian Agriculture and Forestry University, Fuzhou, 350002, Fujian, China

    Yongxin Tao, Jian Li, Hanbing Song & Baogui Xie

  3. College of Life Sciences, Nanjing Agricultural University, No. 1 Weigang, Nanjing, 210095, Jiangsu, China

    Xiaofei Han, Ang Ren & Mingwen Zhao

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  1. Yongxin Tao
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  2. Xiaofei Han
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  3. Ang Ren
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  4. Jian Li
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  5. Hanbing Song
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  6. Baogui Xie
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  7. Mingwen Zhao
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Contributions

TYX and ZMW conceived and designed the research. TYX, HXF, RA, LJ, and SHB conducted the experiments. TYX, HXF, RA, LJ, SHB, and XBG analyzed the data and revised the manuscript. TYX wrote the manuscript. All authors read and approved the manuscript.

Corresponding author

Correspondence to Mingwen Zhao.

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Yongxin Tao and Xiaofei Han are co-authors.

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Tao, Y., Han, X., Ren, A. et al. Heat stress promotes the conversion of putrescine to spermidine and plays an important role in regulating ganoderic acid biosynthesis in Ganoderma lucidum. Appl Microbiol Biotechnol 105, 5039–5051 (2021). https://doi.org/10.1007/s00253-021-11373-0

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  • DOI: https://doi.org/10.1007/s00253-021-11373-0

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