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A bipartite transcription factor module controlling expression in the bundle sheath of Arabidopsis thaliana

Abstract

C4 photosynthesis evolved repeatedly from the ancestral C3 state, improving photosynthetic efficiency by ~50%. In most C4 lineages, photosynthesis is compartmented between mesophyll and bundle sheath cells, but how gene expression is restricted to these cell types is poorly understood. Using the C3 model Arabidopsis thaliana, we identified cis-elements and transcription factors driving expression in bundle sheath strands. Upstream of the bundle sheath preferentially expressed MYB76 gene, we identified a region necessary and sufficient for expression containing two cis-elements associated with the MYC and MYB families of transcription factors. MYB76 expression is reduced in mutant alleles for these transcription factors. Moreover, downregulated genes shared by both mutants are preferentially expressed in the bundle sheath. Our findings are broadly relevant for understanding the spatial patterning of gene expression, provide specific insights into mechanisms associated with the evolution of C4 photosynthesis and identify a short tuneable sequence for manipulating gene expression in the bundle sheath.

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Fig. 1: A 468-bp region from the MYB76 promoter necessary for bundle sheath expression.
Fig. 2: A DHS in the MYB76 promoter is necessary and sufficient for expression in the bundle sheath.
Fig. 3: MYC, MYB and DREB transcription factors control MYB76 expression from the DHS.
Fig. 4: The MYC–MYB module controls the bundle sheath expression of multiple genes.

Data availability

The underlying data required to generate the plots are available in the Github repository: https://github.com/hibberd-lab/Dickinson_Knerova_Arabidopsis_bipartite_transcription_factor_module. The A. thaliana transcription factor motifs were downloaded from the JASPAR motif database: http://jaspar.genereg.net/. All other data are available on request.

Code availability

All code associated with this manuscript is available in the Github repository: https://github.com/hibberd-lab/Dickinson_Knerova_Arabidopsis_bipartite_transcription_factor_module.

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Acknowledgements

The work was funded by ERC grant no. RG80867 Revolution; BBSRC grant nos BBP0031171, BB10022431 and BB/M011356 to J.M.H.; and a Derek Brewer PhD studentship to J.K. S.M.B. was partially funded by an HHMI Faculty Scholars fellowship. We thank R. Solano (Centro Nacional de Biotecnología, Madrid) for seeds of the myc2/3/4 triple mutant.

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P.J.D., J.K., M.S., S.R.S., S.J.B., H.M., A.-M.B. and A.G. carried out the work. J.K., P.J.D., S.M.B. and J.M.H. designed the work. P.J.D., J.K. and J.M.H. wrote the manuscript. J.M.H. initiated and oversaw the project.

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Correspondence to Julian M. Hibberd.

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Dickinson, P.J., Kneřová, J., Szecówka, M. et al. A bipartite transcription factor module controlling expression in the bundle sheath of Arabidopsis thaliana. Nat. Plants 6, 1468–1479 (2020). https://doi.org/10.1038/s41477-020-00805-w

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