Age-dependent dendrobine biosynthesis in Dendrobium nobile: insights into endophytic fungal interactions

Yongxia Zhao; Xiaolong Ji; Xiaoqi Liu; Lin Qin; Daopeng Tan; Di Wu; Chaojun Bai; Jiyong Yang; Jian Xie; Yuqi He

doi:10.3389/fmicb.2023.1294402

Age-dependent dendrobine biosynthesis in Dendrobium nobile: insights into endophytic fungal interactions

Front Microbiol. 2023 Dec 8:14:1294402. doi: 10.3389/fmicb.2023.1294402. eCollection 2023.

Authors

Yongxia Zhao^{1

2

3}, Xiaolong Ji^{1

2

3}, Xiaoqi Liu^{1

2

3}, Lin Qin^{1

2

3}, Daopeng Tan^{1

2

3}, Di Wu^{1

2

3}, Chaojun Bai⁴, Jiyong Yang⁵, Jian Xie^{1

2

3}, Yuqi He^{1

2

3}

Affiliations

¹ Guizhou Engineering Research Center of Industrial Key-Technology for Dendrobium nobile, Engineering Research Center of Pharmaceutical Orchid Plant Breeding, High Efficiency Application in Guizhou Province, Zunyi Medical University, Zunyi, China.
² Key Laboratory of Basic Pharmacology of Ministry of Education, Joint International Research Laboratory of Ethnomedicine of Ministry of Education, Zunyi Medical University, Zunyi, China.
³ 2011 Cooperative Inovational Center for Guizhou Traditional Chinese Medicine and Ethnic Medicine, Zunyi Medical University, Zunyi, China.
⁴ Guangxi Shenli Pharmaceutical Co., Ltd., Yulin, China.
⁵ Chishui Xintian Chinese Medicine Industry Development Co., Ltd., Zunyi, China.

Abstract

Introduction: Dendrobium nobile (D. nobile), a valued Chinese herb known for its diverse pharmacological effects, owes much of its potency to the bioactive compound dendrobine. However, dendrobine content varies significantly with plant age, and the mechanisms governing this variation remain unclear. This study delves into the potential role of endophytic fungi in shaping host-microbe interactions and influencing plant metabolism.

Methods: Using RNA-seq, we examined the transcriptomes of 1-year-old, 2-year-old, and 3-year-old D. nobile samples and through a comprehensive analysis of endophytic fungal communities and host gene expression in D. nobile stems of varying ages, we aim to identify associations between specific fungal taxa and host genes.

Results: The results revealing 192 differentially expressed host genes. These genes exhibited a gradual decrease in expression levels as the plants aged, mirroring dendrobine content changes. They were enriched in 32 biological pathways, including phagosome, fatty acid degradation, alpha-linolenic acid metabolism, and plant hormone signal transduction. Furthermore, a significant shift in the composition of the fungal community within D. nobile stems was observed along the age gradient. Olipidium, Hannaella, and Plectospherella dominated in 1-year-old plants, while Strelitziana and Trichomerium prevailed in 2-year-old plants. Conversely, 3-year-old plants exhibited additional enrichment of endophytic fungi, including the genus Rhizopus. Two gene expression modules (mediumpurple3 and darkorange) correlated significantly with dominant endophytic fungi abundance and dendrobine accumulation. Key genes involved in dendrobine synthesis were found associated with plant hormone synthesis.

Discussion: This study suggests that the interplay between different endophytic fungi and the hormone signaling system in D. nobile likely regulates dendrobine biosynthesis, with specific endophytes potentially triggering hormone signaling cascades that ultimately influence dendrobine synthesis.

Keywords: Dendrobium nobile; age-dependent accumulation; dendrobine; endophytic fungi; transcriptomic analysis.

Grants and funding

The author(s) declare financial support was received for the research, authorship, and/or publication of this article. This research was funded by the National Nature Science Foundation of China (82160812), Guizhou Engineering Research Center of Industrial Key-technology for Dendrobium nobile [QJJ(2022)048, QJJ(2022)006], the Department of Science and Technology of Guizhou Province [QKHZC (2021)420, QKHZC (2023)261].