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Integrative transcriptome analysis uncovers common components containing CPS2 regulated by maize lncRNA GARR2 in gibberellin response

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Abstract

Main conclusion

The combined transcriptome outcome provides an important clue to the regulatory cascade centering on lncRNA GARR2 and CPS2 gene in GA response.

Abstract

Long non-coding RNAs (lncRNAs) serve as regulatory components in transcriptional hierarchy governing multiple aspects of biological processes. Dissecting regulatory mechanisms underpinning tetracyclic diterpenoid gibberellin (GA) cascade holds both theoretical and applied significance. However, roles of lncRNAs in transcriptional modulation of GA pathway remain largely elusive. Gypsy retrotransposon-derived GIBBERELLIN RESPONSIVE lncRNA2 (GARR2) has been reported as GA-responsive maize lncRNA. Here a novel GARR2-edited line garr2-1 was identified, characteristic of GA-induced phenotype of increased seedling height and elongated leaf sheath. Transcriptome analysis indicated that transcriptional abundance of five genes [ent-copalyl diphosphate synthase2 (CPS2), ent-kaurene synthase4 (KS4), ent-kaurene synthase6 (KS6), ent-kaurene oxidase2 (KO2), and ent-kaurenoic acid oxidase1/Dwarf3 (KAO1/D3)] was elevated in garr2-1 for early steps of GA biosynthesis. Five GA biosynthetic genes as hub regulators were interlaced to shape regulatory network of GA response. Different transcriptome resources were integrated to discover common differentially expressed genes (DEGs) in the independent GARR2-edited lines GARR2KO and garr2-1. A total of 320 common DEGs were retrieved. These common DEGs were enriched in diterpenoid biosynthetic pathway. Integrative transcriptome analysis revealed the common CPS2 encoding the CPS enzyme that catalyzes the conversion of the precursor trans-geranylgeranyl diphosphate to ent-copalyl diphosphate. The up-regulated CPS2 supported the GA-induced phenotype of slender seedlings observed in the independent GARR2-edited lines GARR2KO and garr2-1. Our integrative transcriptome analysis uncovers common components of the GA pathway regulated by lncRNA GARR2. These common components, especially for the GA biosynthetic gene CPS2, provide a valuable resource for further delineating the underlying mechanisms of lncRNA GARR2 in GA response.

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Data availability

Raw reads of RNA-seq can be found in the NCBI database (accession number GSE236898).

Abbreviations

CPS:

ent-Copalyl diphosphate synthase

DEG:

Differentially expressed gene

GA:

Gibberellin

lncRNA:

Long non-coding RNA

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Funding

This work was supported by the National Natural Science Foundation of China (31571671), the High-end Talent Project of Yangzhou University (18HTYZU12), and the Priority Academic Program Development of Jiangsu Higher Education Institutions (PAPD).

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Author notes

  1. Zhongtian Zheng and Wei Li have contributed equally to this work.

Authors and Affiliations

  1. Jiangsu Key Laboratory of Crop Genomics and Molecular Breeding/Key Laboratory of Plant Functional Genomics of the Ministry of Education/Jiangsu Key Laboratory of Crop Genetics and Physiology, Agricultural College of Yangzhou University, Yangzhou, 225009, China

    Zhongtian Zheng, Wei Li, Yuhang Ding, Yinting Wu, Qinyue Jiang & Yijun Wang

  2. Jiangsu Co-Innovation Center for Modern Production Technology of Grain Crops, Yangzhou University, Yangzhou, 225009, China

    Zhongtian Zheng, Wei Li, Yuhang Ding, Yinting Wu, Qinyue Jiang & Yijun Wang

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  1. Zhongtian Zheng
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  2. Wei Li
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  4. Yinting Wu
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Contributions

YJW designed the research. ZTZ and WL prepared Figs. 2–5. YHD and YTW prepared Figs. 1–2. WL and QYJ prepared Fig. 1. ZTZ and YJW wrote the manuscript. All authors reviewed the manuscript.

Corresponding author

Correspondence to Yijun Wang.

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Additional information

Communicated by Dorothea Bartels.

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Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (TIF 1384 KB) Fig. S1 Identification of GARR2-edited sites

425_2024_4425_MOESM2_ESM.tif

Supplementary file2 (TIF 208 KB) Fig. S2 Phenotype of the wild-type and garr2-1 lines. Length of the first leaf blade (a), width of the first leaf blade (b), width of the second leaf blade (c), shoot diameter (d) of the wild-type and garr2-1 lines. Data are mean ± SD (n = 3). The error bars indicate the standard deviation of the mean. Significant difference was evaluated by two-tailed Student's t-test: * P < 0.05

Supplementary file3 (TIFF 301 KB) Fig. S3 Enrichment of common DEGs and components of "diterpenoid biosynthesis" term

Supplementary file4 (XLSX 9 KB) Table S1 Statistics for RNA-seq

Supplementary file5 (XLSX 255 KB) Table S2 Information of DEGs in garr2-1 line

425_2024_4425_MOESM6_ESM.xlsx

Supplementary file6 (XLSX 11 KB) Table S3 Interactors of five GA biosynthetic components CPS2, KS4, KS6, KO2, and KAO1/D3

425_2024_4425_MOESM7_ESM.xlsx

Supplementary file7 (XLSX 9 KB) Table S4 Functional annotation of interactors of five GA biosynthetic components CPS2, KS4, KS6, KO2, and KAO1/D3

Supplementary file8 (XLSX 28 KB) Table S5 Common DEGs in GARR2KO and garr2-1 lines

Supplementary file9 (XLSX 19 KB) Table S6 Enrichment information of common DEGs in GARR2KO and garr2-1 lines

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Zheng, Z., Li, W., Ding, Y. et al. Integrative transcriptome analysis uncovers common components containing CPS2 regulated by maize lncRNA GARR2 in gibberellin response. Planta 259, 146 (2024). https://doi.org/10.1007/s00425-024-04425-y

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