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Auxin and Ethylene Play Important Roles in Parthenocarpy Under Low-Temperature Stress Revealed by Transcriptome Analysis in Cucumber (Cucumis sativus L.)

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Abstract

Although most cucumber varieties have certain parthenocarpy abilities, fruit development will still be significantly inhibited at low temperature. Therefore, it is of great significance to study the molecular mechanism of parthenocarpy regulated by low temperature and to excavate low temperature-tolerant parthenocarpic gene resources, for stable production under low-temperature stress. ‘EC5’ is a low temperature-induced parthenocarpy (LT-P) line identified by previous screening. In this study, the effect of hormones on the development of the LT-P fruit was studied by transcriptome analysis and endogenous hormone determination under two different temperature conditions. It was found that there were few differentially expressed genes between ovaries before anthesis (230 ~ 460 DEGs). However, after anthesis, the number of DEGs increased sharply, following 1, 372 DEGs at 1 day after anthesis (DAA), 6, 272 DEGs at 2 DAA, and 9, 119 DEGs at 3 DAA, respectively. At 2 DAA, DEGs were significantly enriched in the plant hormone signal transduction pathway (Ko 04075); 25% and 19% of the genes were involved in auxin and ethylene metabolism and signaling, respectively. Endogenous hormone determination indicated that the accumulation of IAA and ACC showed an inverse curve during fruit development: IAA accumulated continuously, while ACC synthesis was inhibited during parthenocarpy under low temperature. During fruit abortion at room temperature, the IAA metabolism level decreased sharply, and ACC synthesis increased. Those were consistent with the results of transcriptome analysis that auxin-related genes were significantly up-regulated, and ethylene-related genes were significantly down-regulated. qRT-PCR analysis indicated that some key auxin-related genes had an opposite expression trend compared with ethylene-related genes under two temperature conditions. Exogenous applications of auxin and ethylene showed that auxin promoted parthenocarpy while ethylene inhibited parthenocarpy. In addition, hormone-responsive transcription factors were also actively expressed, among which the DEGs of auxin signal-responsive transcription factors AUX/IAA family and ethylene signal-responsive transcription factors AP2/ERF family were the largest. During the process of LT-P, 90% ~ 100% of AUX/IAA genes were up-regulated and 15% ~ 100% of AP2/ERF genes were down-regulated. This study verified that auxin and ethylene played important roles in the process of cucumber parthenocarpy under low-temperature stress, and it was speculated that auxin positively regulated parthenocarpic fruit development, whereas ethylene negatively correlated with the developmental process.

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Data Availability

All transcriptomic sequencing data associated with this study have been submitted to the NCBI Sequence Read Archive database and can be found using accession number PRJNA874540 (https://submit.ncbi.nlm.nih.gov/subs/bioproject/SUB11978517/overview). Other data generated or analyzed during this study are included in the “Supplementary materials” part and available from the corresponding author upon reasonable request. The ‘EC5’ material is identified and stored in our laboratory.

Abbreviations

LT-P:

Low temperature-induced parthenocarpy

NT-NP:

Normal non-parthenocarpy

TFs:

Transcription factors

DAA:

Days after anthesis

DEGs:

Differentially expressed genes

IAA:

Indole acetic acid

ACC:

1-Amino cyclopropane carboxylic acid

ABA:

Abscisic acid

BR:

Brassinosteroid

JA:

Jasmonic acid

SA:

Salicylic acid

PCA:

Principal component analysis

KEGG:

Kyoto Encyclopedia of Genes and Genomes

GO:

Gene Ontology

SD:

Standard deviation

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Acknowledgements

The authors would like to thank Dr. Qinzheng Zhao for technical assistance during the manuscript revision.

Funding

This work was supported by the National Natural Science Foundation of China (32272726), the Jiangsu Belt and Road Innovation Cooperation Project (BZ2019012), the National Key Research and Development Program of China (2020YFE0202900, 2021YFD1200201), and the Jiangsu Agricultural Innovation of New Cultivars (PZCZ201719).

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Authors and Affiliations

  1. State Key Laboratory of Crop Genetics & Germplasm Enhancement and Utilization, College of Horticulture, Nan**g Agricultural University, Weigang Campus, Nan**g, 210095, China

    Yongjiao Meng, Pinyu Zhu, Chenxing Gou, Chunyan Cheng, Ji Li & **feng Chen

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  1. Yongjiao Meng
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  2. Pinyu Zhu
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  5. Ji Li
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Contributions

YM performed the experiments, analyzed the data, and wrote the manuscript. PZ and CG participated in sample collection and data analyses. CC revised the manuscript. JL provided scientific guidance and advice. JC conceived and designed the experiments. All authors have read and agreed to the published version of the manuscript.

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Correspondence to Ji Li or **feng Chen.

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All authors have read and approved this version of the article, and due care has been taken to ensure the integrity of the work. The article is original and unpublished and is not being considered for publication elsewhere. This study didn’t involve endangered or protected species and all methods were performed under the relevant guidelines and regulations.

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Supplementary Information

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344_2023_11172_MOESM1_ESM.jpg

Supplementary file1 (JPG 1708 KB)—PCA analyses of RNA-seq data from all samples of the NT-NP and LT-P fruits The PCA of gene expressions in all samples of NT-NP and LT-P. -2, -1, 0, 1, 2, 3 represents -2 DAA, -1 DAA, 0DAA (the anthesis day), 1 DAA, 2 DAA, and 3 DAA, respectively. Each sample includes three biological replicates. DAA: day after anthesis.

344_2023_11172_MOESM2_ESM.jpg

Supplementary file2 (JPG 8447 KB)—The top 30 up-regulated GO terms during the fruit developments of NT-NP and LT-P after anthesis The top 30 biological process terms of up-regulated DEGs involving NT-NP (a) and LT-P (b) after anthesis.

344_2023_11172_MOESM3_ESM.jpg

Supplementary file3 (JPG 1768 KB)—Expression analysis of the important auxin- and ethylene-related genes via qRT-PCR Relative expression of the genes associated with auxin and ethylene biosynthesis and signaling across developmental stages in the NT-NP and LT-P fruits (ovaries). The bars represent SD. *P < 0.05, **P < 0.01, ***P < 0.001, ****P< 0.0001. LT: low temperature (18°C day/10°C night), NT: normal temperature (28°C day/20°C night).

344_2023_11172_MOESM4_ESM.jpg

Supplementary file4 (JPG 368 KB)—Effects of auxin and ethylene on the fruit growth and the parthenocarpic fruit set of ‘EC5’ a: Effects of IAA, TIBA, ethylene, and STS on fruit growth of ‘EC5’ under two temperatures. b: Effects of IAA, TIBA, ethylene, and STS on parthenocarpic fruit set of ‘EC5’ under two temperatures. Data were recorded at 6 DAA. Each data point represents the means of three replicates, 10 ovaries/fruits per replicate, totaling 30 fruits. CK: no exogenous hormone treatment. The bars represent SD. Asterisks indicate a significant difference by t-test, *P < 0.05, **P < 0.01, ***P < 0.001, ****P< 0.0001. LT: low temperature (18°C day/10°C night), NT: normal temperature (28°C day/20°C night).

344_2023_11172_MOESM5_ESM.jpg

Supplementary file5 (JPG 1147 KB)—The female flowers which were wrapped with metal wires The female flowers which were wrapped with metal wires before anthesis to prevent pollination.

Supplementary file6 (DOCX 62 KB)

Supplementary file7 (XLSX 14 KB)

Supplementary file8 (XLSX 12 KB)

Supplementary file9 (XLSX 12 KB)

Supplementary file10 (XLSX 12 KB)

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Meng, Y., Zhu, P., Gou, C. et al. Auxin and Ethylene Play Important Roles in Parthenocarpy Under Low-Temperature Stress Revealed by Transcriptome Analysis in Cucumber (Cucumis sativus L.). J Plant Growth Regul 43, 1137–1152 (2024). https://doi.org/10.1007/s00344-023-11172-z

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