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Leaf layer-based transcriptome profiling for discovery of epidermal-selective promoters in Medicago truncatula

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Abstract

Main conclusion

Transcriptomics of manually dissected leaf layers from Medicago truncatula identifies genes with preferential expression in upper and/or lower epidermis. The promoters of these genes confer epidermal-specific expression of transgenes.

Abstract

Improving the quality and quantity of proanthocyanidins (PAs) in forage legumes has potential to improve the nitrogen nutrition of ruminant animals and protect them from the risk of pasture bloat, as well as parasites. However, ectopic constitutive accumulation of PAs in plants by genetic engineering can significantly inhibit growth. We selected the leaf epidermis as a candidate tissue for targeted engineering of PAs or other pathways. To identify gene promoters selectively expressed in epidermal tissues, we performed comparative transcriptomic analyses in the model legume Medicago truncatula, using five tissue samples representing upper epidermis, lower epidermis, whole leaf without upper epidermis, whole leaf without lower epidermis, and whole leaf. We identified 52 transcripts preferentially expressed in upper epidermis, most of which encode genes involved in flavonoid biosynthesis, and 53 transcripts from lower epidermis, with the most enriched category being anatomical structure formation. Promoters of the preferentially expressed genes were cloned from the M. truncatula genome and shown to direct tissue-selective promoter activities in transient assays. Expression of the PA pathway transcription factor TaMYB14 under control of several of the promoters in transgenic alfalfa resulted in only modest MYB14 transcript accumulation and low levels of PA production. Activity of a subset of promoters was confirmed by transcript analysis in field-grown alfalfa plants throughout the growing season, and revealed variable but consistent expression, which was generally highest 3–4 weeks after cutting. We conclude that, although the selected promoters show acceptable tissue-specificity, they may not drive high enough transcription factor expression to activate the PA pathway.

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Data availability

The data that support the findings of in this study are available in the Supplementary Information of this article. Sequence data from this article can be found in the NCBI Sequence Read Archive (SRA) repository, accession number PRJNA804330 (https://dataview.ncbi.nlm.nih.gov/object/PRJNA804330?reviewer=sk6165nsvtpevq1cgeae5h25g5).

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Acknowledgements

We thank Drs Chenggang Liu, Nan Lu and Keji Yu for their suggestions on plant transformation, Tracy Kim at the UNT Genomics Facility for help with sampling and sequencing, and Wendy Rossi from the Texas Academy of Mathematics and Science for assistance on this project.

Funding

This work was supported by Forage Genetics International and the University of North Texas (UNT).

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Authors and Affiliations

  1. BioDiscovery Institute and Department of Biological Sciences, University of North Texas, 1155 Union Circle #311428, Denton, TX, 76203, USA

    Xin Cui, Ji Hyung Jun, Xiaolan Rao & Richard A. Dixon

  2. Forage Genetics International, N5292 Gills Coulee Rd S, West Salem, WI, 54669, USA

    Camille Bahr, Elisabeth Chapman & Stephen Temple

  3. Children’s Research Institute and the Department of Pediatrics, University of Texas Southwestern Medical Center, Dallas, TX, 75390, USA

    Ji Hyung Jun

  4. College of Life Sciences, Hubei University, Wuhan, 430068, Hubei, China

    Xiaolan Rao

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  1. Xin Cui
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Cui, X., Jun, J.H., Rao, X. et al. Leaf layer-based transcriptome profiling for discovery of epidermal-selective promoters in Medicago truncatula. Planta 256, 31 (2022). https://doi.org/10.1007/s00425-022-03920-4

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