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The response of rhubarb to smut infection is revealed through a comparative transcriptome and metabolome study

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Abstract

Main conclusion

Integrated transcriptome and metabolome analysis have unveiled the physiological and molecular responses of rhubarb to infection by smut fungi.

Abstract

Rhubarb is an important medicinal plant that is easily infected by smut fungi during its growth. Thus far, no research on the influence of smut fungi on the growth of rhubarb and its secondary metabolism has been conducted. In this study, petioles of Chinese rhubarb (Rheum officinale) [healthy or infected with smut fungus (Thecaphora schwarzmaniana)] were characterized. Microscopic structure, global gene expression profiling, global metabolic profiling, and key enzyme activity and metabolite levels in infected plants were analyzed. Infection by smut fungi resulted in numerous holes inside the petiole tissue and led to visible tumors on the external surface of the petiole. Through metabolic changes, T. schwarzmaniana induced the production of specific sugars, lipids, and amino acids, and inhibited the metabolism of phenolics and flavonoids in R. officinale. The concentrations of key medicinal compounds (anthraquinones) were decreased because of smut fungus infection. In terms of gene expression, the presence of T. schwarzmaniana led to upregulation of the genes associated with nutrient (sugar, amino acid, etc.) transport and metabolism. The gene expression profiling showed a stimulated cell division activity (the basis of tumor formation). Although plant antioxidative response was enhanced, the plant defense response against pathogen was suppressed by T. schwarzmaniana, as indicated by the expression profiling of genes involved in biotic and abiotic stress-related hormone signaling and the synthesis of plant disease resistance proteins. This study demonstrated physiological and molecular changes in R. officinale under T. schwarzmaniana infection, reflecting the survival tactics employed by smut fungus for parasitizing rhubarb.

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Data availability

The raw sequence data reported in this paper have been deposited in the Genome Sequence Archive (Chen et al. 2021) in National Genomics Data Center (CNCB-NGDC Members and Partners 2022), China National Center for Bioinformation/Beijing Institute of Genomics, Chinese Academy of Sciences (GSA: CRA009691) that are publicly accessible at https://ngdc.cncb.ac.cn/gsa. The metabolome data reported in this paper have been deposited in the OMIX, China National Center for Bioinformation/Beijing Institute of Genomics, Chinese Academy of Sciences (https://ngdc.cncb.ac.cn/omix: accession no. OMIX002896).

Abbreviations

DEG:

Diferentially expressed gene

JA:

Jasmonic acid

ROS:

Reactive oxygen species

SA:

Salicylic acid

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Acknowledgements

This research was supported by National Natural Science Foundation of China (31901283) and Fundamental Research Funds for the Central Universities of China (Grant No. SWU-KT22045). The authors would like to express their gratitude to EditSprings for the expert linguistic services provided.

Funding

This article is funded by National Natural Science Foundation of China, 31901283, Qingwei Zhang, Fundamental Research Funds for the Central Universities, SWU-KT22045, Qingwei Zhang.

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Authors and Affiliations

  1. Key Laboratory of Eco-Environments of Three Gorges Reservoir Region, Ministry of Education, School of Life Sciences, Southwest University, Chongqing, 400715, China

    Shuangshuang Zhou, Ya Lin, Xiaohui Yao, Kuan Sun, Qin Song & Qingwei Zhang

  2. Chongqing Nanchuan Institute of Traditional Chinese Medicinal Plants, Chongqing, 408407, China

    Shuangshuang Zhou, Ya Lin, Yu Cai & Qingwei Zhang

  3. Teaching and research group of biology, Kunming No.8 High School, Kunming, China

    Linfang Li

  4. Teaching and research group of biology, Hohhot 35th Middle School, Hohhot, China

    Xiaohui Yao

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  1. Shuangshuang Zhou
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  2. Ya Lin
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  4. Linfang Li
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Contributions

QZ: designed and organized the research project; SZ, YL and YC: collected materials, conducted experiments, analyzed data, and drafted the manuscript; LL and XY contributed to pathogen culture and identification; KS and QS: performed microscopic observation of pathogen; SZ, YL and QZ: revised the manuscript. YC, LL, XY, KS and QS: participated in data analysis. All authors have read and approved the final manuscript.

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Correspondence to Qingwei Zhang.

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Supplementary file1 (DOCX 12 KB)

Supplementary file2 (XLSX 14 KB)

Supplementary file3 Details of genes in Figs. 4–9 (XLSX 51 KB)

425_2023_4306_MOESM4_ESM.tif

Supplementary file4 Activities of glutamine synthetase (GOGAT), peroxidase (POD), lipoxygenase (), phenylalanine ammonia lyase (PAL) and polyphenol oxidase (PPO). H, healthy plant; I, infected plant. “*” indicate significant (t-test, P<0.05, n = 3) differences between healthy and infected plants. The Bradford assay using BSA as a standard (Kielkopf et al. (2020) Bradford assay for determining protein concentration. Cold Spring Harb Protoc 2020(4): 102269) was utilized to estimate protein concentration and calculate specific enzyme activity (TIF 76 KB)

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Zhou, S., Lin, Y., Cai, Y. et al. The response of rhubarb to smut infection is revealed through a comparative transcriptome and metabolome study. Planta 259, 27 (2024). https://doi.org/10.1007/s00425-023-04306-w

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