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

Nature Plants volume 6, pages 1468–1479 (2020)Cite this article

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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.

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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.

References

  1. Hibberd, J. M., Sheehy, J. E. & Langdale, J. A. Using C4 photosynthesis to increase the yield of rice—rationale and feasibility. Curr. Opin. Plant Biol. 11, 228–231 (2008).

    Article  CAS  PubMed  Google Scholar 

  2. Von Caemmerer, S., Quick, W. P. & Furbank, R. T. The development of C4 rice: current progress and future challenges. Science 336, 1671–1672 (2012).

    Article  CAS  PubMed  Google Scholar 

  3. Hibberd, J. M. & Covshoff, S. The regulation of gene expression required for C4 photosynthesis. Annu. Rev. Plant Biol. 61, 181–207 (2010).

    Article  CAS  PubMed  Google Scholar 

  4. Wiludda, C. et al. Regulation of the photorespiratory GLDPA gene in C4 Flaveria: an intricate interplay of transcriptional and posttranscriptional processes. Plant Cell 24, 137–151 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Engelmann, S. et al. The gene for the P-subunit of glycine decarboxylase from the C4 species Flaveria trinervia: analysis of transcriptional control in transgenic Flaveria bidentis (C4) and Arabidopsis (C3). Plant Physiol. 146, 1773–1785 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Gowik, U. et al. cis-Regulatory elements for mesophyll-specific gene expression in the C4 plant Flaveria trinervia, the promoter of the C4 phosphoenolpyruvate carboxylase gene. Plant Cell 16, 1077–1090 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Akyildiz, M. et al. Evolution and function of a cis-regulatory module for mesophyll-specific gene expression in the C4 dicot Flaveria trinervia. Plant Cell 19, 3391–3402 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Williams, B. P. et al. An untranslated cis-element regulates the accumulation of multiple C4 enzymes in Gynandropsis gynandra mesophyll cells. Plant Cell 28, 454–465 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Brown, N. J. et al. Independent and parallel recruitment of preexisting mechanisms underlying C4 photosynthesis. Science 331, 1436–1439 (2011).

    Article  CAS  PubMed  Google Scholar 

  10. Reyna-Llorens, I. et al. Ancient duons may underpin spatial patterning of gene expression in C4 leaves. Proc. Natl Acad. Sci. USA 115, 1931–1936 (2018).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Matsuoka, M. et al. The promoters of two carboxylases in a C4 plant (maize) direct cell-specific, light-regulated expression in a C3 plant (rice). Plant J. 6, 311–319 (1994).

    Article  CAS  PubMed  Google Scholar 

  12. Kajala, K. et al. Multiple Arabidopsis genes primed for direct recruitment into C4 photosynthesis. Plant J. 69, 47–56 (2012).

    Article  CAS  PubMed  Google Scholar 

  13. Reyna-Llorens, I. & Hibberd, J. M. Recruitment of pre-existing networks during the evolution of C4 photosynthesis. Phil. Trans. R. Soc. B 372, 2–7 (2017).

    Article  CAS  Google Scholar 

  14. Kinsman, E. A. & Pyke, K. A. Bundle sheath cells and cell-specific plastid development in Arabidopsis leaves. Development 125, 1815–1822 (1998).

    CAS  PubMed  Google Scholar 

  15. Shatil-Cohen, A., Attia, Z. & Moshelion, M. Bundle-sheath cell regulation of xylem-mesophyll water transport via aquaporins under drought stress: a target of xylem-borne ABA? Plant J. 67, 72–80 (2011).

    Article  CAS  PubMed  Google Scholar 

  16. Leegood, R. C. Roles of the bundle sheath cells in leaves of C3 plants. J. Exp. Bot. 59, 1663–1673 (2008).

    Article  CAS  PubMed  Google Scholar 

  17. Koroleva, O., Farrar, J. F., Tomos, A. D. & Pollock, C. J. Patterns of solute in individual mesophyll, bundle sheath and epidermal cells of barley leaves induced to accumulate carbohydrate. N. Phytol. 136, 97–104 (1997).

    Article  CAS  Google Scholar 

  18. Williams, M., Thomas, B. J., Farrar, J. F. & Pollock, C. J. Visualizing the distribution of elements within barley leaves by energy dispersive X-ray image maps (EDX maps). N. Phytol. 125, 367–372 (2018).

    Article  Google Scholar 

  19. Sage, R. Environmental and evolutionary preconditions for the origin and diversification of the C4 photosynthetic syndrome. Plant Biol. 3, 202–213 (2001).

    Article  CAS  Google Scholar 

  20. Griffiths, H., Weller, G., Toy, L. F. M. & Dennis, R. J. You’re so vein: bundle sheath physiology, phylogeny and evolution in C3 and C4 plants. Plant Cell Environ. 36, 249–261 (2013).

    Article  CAS  PubMed  Google Scholar 

  21. Takahashi, H. et al. The roles of three functional sulphate transporters involved in uptake and translocation of sulphate in Arabidopsis thaliana. Plant J. 23, 171–182 (2000).

    Article  CAS  PubMed  Google Scholar 

  22. Kirschner, S. et al. Expression of SULTR2;2, encoding a low-affinity sulphur transporter, in the Arabidopsis bundle sheath and vein cells is mediated by a positive regulator. J. Exp. Bot. 69, 4897–4906 (2018).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Aubry, S., Smith-Unna, R. D., Boursnell, C. M., Kopriva, S. & Hibberd, J. M. Transcript residency on ribosomes reveals a key role for the Arabidopsis thaliana bundle sheath in sulphur and glucosinolate metabolism. Plant J. 78, 659–673 (2014).

    Article  CAS  PubMed  Google Scholar 

  24. Schweizer, F. et al. Arabidopsis basic helix-loop-helix transcription factors MYC2, MYC3, and MYC4 regulate glucosinolate biosynthesis, insect performance, and feeding behavior. Plant Cell 25, 3117–3132 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Li, B. et al. Promoter-based integration in plant defense regulation. Plant Physiol. 166, 1803–1820 (2014).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  26. Gigolashvili, T., Engqvist, M., Yatusevich, R., Müller, C. & Flügge, U.-I. HAG2/MYB76 and HAG3/MYB29 exert a specific and coordinated control on the regulation of aliphatic glucosinolate biosynthesis in Arabidopsis thaliana. N. Phytol. 177, 627–642 (2008).

    Article  CAS  Google Scholar 

  27. Ali, S. & Taylor, W. C. The 3′ non-coding region of a C4 photosynthesis gene increases transgene expression when combined with heterologous promoters. Plant Mol. Biol. 46, 325–333 (2001).

    Article  CAS  PubMed  Google Scholar 

  28. Gallegos, J. E. & Rose, A. B. Intron DNA sequences can be more important than the proximal promoter in determining the site of transcript initiation. Plant Cell 29, 843–853 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Hesselberth, J. R. et al. Global mapping of protein–DNA interactions in vivo by digital genomic footprinting. Nat. Methods 6, 283–289 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Zhang, W., Zhang, T., Wu, Y. & Jiang, J. Genome-wide identification of regulatory DNA elements and protein-binding footprints using signatures of open chromatin in Arabidopsis. Plant Cell 24, 2719–2731 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Zhang, T., Marand, A. P. & Jiang, J. PlantDHS: a database for DNase1 hypersensitive sites in plants. Nucleic Acids Res. 44, D1148–D1153 (2016).

    Article  CAS  PubMed  Google Scholar 

  32. Wysocka-Diller, J. W., Helariutta, Y., Fukaki, H., Malamy, J. E. & Benfey, P. N. Molecular analysis of SCARECROW function reveals a radial patterning mechanism common to root and shoot. Development 127, 595–603 (2000).

    CAS  PubMed  Google Scholar 

  33. Grant, C. E., Bailey, T. L. & Noble, W. S. FIMO: scanning for occurrences of a given motif. Bioinformatics 27, 1017–1018 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Fornes, O. et al. JASPAR 2020: update of the open-access database of transcription factor binding profiles. Nucleic Acids Res. https://doi.org/10.1093/nar/gkz1001 (2019).

  35. Burow, M. et al. The glucosinolate biosynthetic gene AOP2 mediates feed-back regulation of jasmonic acid signaling in Arabidopsis. Mol. Plant 8, 1201–1212 (2015).

    Article  CAS  PubMed  Google Scholar 

  36. Sønderby, I. E. et al. A systems biology approach identifies a R2R3MYB gene subfamily with distinct and overlapping functions in regulation of aliphatic glucosinolates. PLoS ONE 2, e1322 (2007).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  37. Major, I. T. et al. Regulation of growth–defense balance by the JASMONATE ZIM-DOMAIN (JAZ)-MYC transcriptional module. N. Phytol. 215, 1533–1547 (2017).

    Article  CAS  Google Scholar 

  38. Baima, S. et al. The expression of the Athb-8 homeobox gene is restricted to provascular cells in Arabidopsis thaliana. Development 121, 4171–4182 (1995).

    CAS  PubMed  Google Scholar 

  39. Levin, J. Z. & Meyerowitz, E. M. UFO—an Arabidopsis gene involved in both floral meristem and floral organ development. Plant Cell 7, 529–548 (1995).

    CAS  PubMed  PubMed Central  Google Scholar 

  40. Fletcher, J. C., Brand, U., Running, M. P., Simon, R. & Meyerowitz, E. M. Signaling of cell fate decisions by CLAVATA3 in Arabidopsis shoot meristems. Science 19, 1911–1914 (1999).

    Article  Google Scholar 

  41. Otsuga, D., DeGuzman, B., Prigge, M. J., Drews, G. N. & Clark, S. E. REVOLUTA regulates meristem initiation at lateral positions. Plant J. 25, 223–236 (2001).

    Article  CAS  PubMed  Google Scholar 

  42. Sarkar, A. K. et al. Conserved factors regulate signalling in Arabidopsis thaliana shoot and root stem cell organizers. Nature 446, 811–814 (2007).

    Article  CAS  PubMed  Google Scholar 

  43. Helariutta, Y. et al. The SHORT-ROOT gene controls radial patterning of the Arabidopsis root through radial signaling. Cell 101, 555–567 (2000).

    Article  CAS  PubMed  Google Scholar 

  44. Bonke, M., Thitamadee, S., Mähönen, A. P., Hauser, M.-T. & Helariutta, Y. APL regulates vascular tissue identity in Arabidopsis. Nature 426, 181–186 (2003).

    Article  CAS  PubMed  Google Scholar 

  45. Heidstra, R., Welch, D. & Scheres, B. Mosaic analyses using marked activation and deletion clones dissect Arabidopsis SCARECROW action in asymmetric cell division. Genes Dev. 18, 1964–1969 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Mustroph, A. et al. Profiling translatomes of discrete cell populations resolves altered cellular priorities during hypoxia in Arabidopsis. Proc. Natl Acad. Sci. USA 106, 18843–18848 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Ruzicka, D. R., Kandasamy, M. K., McKinney, E. C., Burgos-Rivera, B. & Meagher, R. B. The ancient subclasses of Arabidopsis actin depolymerizing factor genes exhibit novel and differential expression. Plant J. 52, 460–472 (2007).

    Article  CAS  PubMed  Google Scholar 

  48. Masucci, J. D. et al. The homeobox gene GLABRA2 is required for position-dependent cell differentiation in the root epidermis of Arabidopsis thaliana. Development 122, 1253–1260 (1996).

    CAS  PubMed  Google Scholar 

  49. Nakamura, R. L. et al. Expression of an Arabidopsis potassium channel gene in guard cells. Plant Physiol. 109, 371–374 (1995).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Imlau, A., Truernit, E. & Sauer, N. Cell-to-cell and long-distance trafficking of the green fluorescent protein in the phloem and symplastic unloading of the protein into sink tissues. Plant Cell 11, 309–322 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Thoma, S. et al. Tissue-specific expression of a gene encoding a cell wall-localized lipid transfer protein from Arabidopsis. Plant Physiol. 105, 35–45 (1994).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Sparks, E. E. et al. Establishment of expression in the SHORTROOT–SCARECROW transcriptional cascade through opposing activities of both activators and repressors. Dev. Cell 39, 585–596 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Neph, S. et al. An expansive human regulatory lexicon encoded in transcription factor footprints. Nature 489, 83–90 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Fryer, M. J. et al. Control of Ascorbate Peroxidase 2 expression by hydrogen peroxide and leaf water status during excess light stress reveals a functional organisation of Arabidopsis leaves. Plant J. 33, 691–705 (2003).

    Article  CAS  PubMed  Google Scholar 

  55. Bhullar, S. et al. Strategies for development of functionally equivalent promoters with minimum sequence homology for transgene expression in plants: cis-elements in a novel DNA context versus domain swapping. Plant Physiol. 132, 988–998 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Hernandez-Garcia, C. M. & Finer, J. J. Identification and validation of promoters and cis-acting regulatory elements. Plant Sci. 217–218, 109–119 (2014).

    Article  PubMed  CAS  Google Scholar 

  57. Dey, N., Sarkar, S., Acharaya, S. & Maiti, I. B. Synthetic promoters in planta. Planta 242, 1077–1094 (2015).

    Article  CAS  PubMed  Google Scholar 

  58. Shroff, R., Vergara, F., Muck, A., Svatos, A. & Gershenzon, J. Nonuniform distribution of glucosinolates in Arabidopsis thaliana leaves has important consequences for plant defense. Proc. Natl Acad. Sci. USA 105, 6196–6201 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Malitsky, S. et al. The transcript and metabolite networks affected by the two clades of Arabidopsis glucosinolate biosynthesis regulators. Plant Physiol. 148, 2021–2049 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Sønderby, I. E., Burow, M., Rowe, H. C., Kliebenstein, D. J. & Halkier, B. A. A complex interplay of three R2R3 MYB transcription factors determines the profile of aliphatic glucosinolates in Arabidopsis. Plant Physiol. 153, 348–363 (2010).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  61. Fernández-Calvo, P. et al. The Arabidopsis bHLH transcription factors MYC3 and MYC4 are targets of JAZ repressors and act additively with MYC2 in the activation of jasmonate responses. Plant Cell 23, 701–715 (2011).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  62. Howe, G. A., Major, I. T. & Koo, A. J. Modularity in jasmonate signaling for multistress resilience. Annu. Rev. Plant Biol. 69, 387–415 (2018).

    Article  CAS  PubMed  Google Scholar 

  63. Salehin, M. et al. Auxin-sensitive Aux/IAA proteins mediate drought tolerance in Arabidopsis by regulating glucosinolate levels. Nat. Commun. 10, 4021 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

  64. Agarwal, P. K., Gupta, K., Lopato, S. & Agarwal, P. Dehydration responsive element binding transcription factors and their applications for the engineering of stress tolerance. J. Exp. Bot. 68, 2135–2148 (2017).

    Article  CAS  PubMed  Google Scholar 

  65. Egawa, C. et al. Differential regulation of transcript accumulation and alternative splicing of a DREB2 homolog under abiotic stress conditions in common wheat. Genes Genet. Syst. 81, 77–91 (2006).

    Article  CAS  PubMed  Google Scholar 

  66. Qin, F. et al. Regulation and functional analysis of ZmDREB2A in response to drought and heat stresses in Zea mays L. Plant J. 50, 54–69 (2007).

    Article  CAS  PubMed  Google Scholar 

  67. Matsukura, S. et al. Comprehensive analysis of rice DREB2-type genes that encode transcription factors involved in the expression of abiotic stress-responsive genes. Mol. Genet. Genomics 283, 185–196 (2010).

    Article  CAS  PubMed  Google Scholar 

  68. Vainonen, J. P. et al. RCD1–DREB2A interaction in leaf senescence and stress responses in Arabidopsis thaliana. Biochem. J. 442, 573–581 (2012).

    Article  CAS  PubMed  Google Scholar 

  69. Liu, Q. et al. Two transcription factors, DREB1 and DREB2, with an EREBP/AP2 DNA binding domain separate two cellular signal transduction pathways in drought- and low-temperature-responsive gene expression, respectively, in Arabidopsis. Plant Cell 10, 1391–1406 (1998).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Sakuma, Y. et al. Functional analysis of an Arabidopsis transcription factor, DREB2A, involved in drought-responsive gene expression. Plant Cell 18, 1292–1309 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Theißen, G., Melzer, R. & Ruümpler, F. MADS-domain transcription factors and the floral quartet model of flower development: linking plant development and evolution. Development 143, 3259–3271 (2016).

    Article  PubMed  CAS  Google Scholar 

  72. Sarsby, J., Towers, M. W., Stain, C., Cramer, R. & Koroleva, O. A. Mass spectrometry imaging of glucosinolates in Arabidopsis flowers and siliques. Phytochemistry 77, 110–118 (2012).

    Article  CAS  PubMed  Google Scholar 

  73. Halkier, B. A. & Gershenzon, J. Biology and biochemistry of glucosinolates. Annu. Rev. Plant Biol. 57, 303–333 (2006).

    Article  CAS  PubMed  Google Scholar 

  74. Yatusevich, R. et al. Genes of primary sulfate assimilation are part of the glucosinolate biosynthetic network in Arabidopsis thaliana. Plant J. 62, 1–11 (2010).

    Article  CAS  PubMed  Google Scholar 

  75. Millard, P. S., Weber, K., Kragelund, B. B. & Burow, M. Specificity of MYB interactions relies on motifs in ordered and disordered contexts. Nucleic Acids Res. 47, 9592–9608 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Adwy, W., Laxa, M. & Peterhansel, C. A simple mechanism for the establishment of C2-specific gene expression in Brassicaceae. Plant J. 84, 1231–1238 (2015).

    Article  CAS  PubMed  Google Scholar 

  77. Mallmann, J. et al. The role of photorespiration during the evolution of C4 photosynthesis in the genus Flaveria. eLife 3, e02478 (2014).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  78. Adwy, W., Schlüter, U., Papenbrock, J., Peterhansel, C. & Offermann, S. Loss of the M-box from the glycine decarboxylase P-subunit promoter in C2 Moricandia species. Plant Gene 18, 100176 (2019).

    Article  CAS  Google Scholar 

  79. Nakagawa, T. et al. Development of series of gateway binary vectors, pGWBs, for realizing efficient construction of fusion genes for plant transformation. J. Biosci. Bioeng. 104, 34–41 (2007).

    Article  CAS  PubMed  Google Scholar 

  80. Weber, E., Engler, C., Gruetzner, R., Werner, S. & Marillonnet, S. A modular cloning system for standardized assembly of multigene constructs. PLoS ONE 6, e16765 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. Clough, S. J. & Bent, A. F. Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16, 735–743 (1998).

    Article  CAS  PubMed  Google Scholar 

  82. Feike, D. et al. Characterizing standard genetic parts and establishing common principles for engineering legume and cereal roots. Plant Biotechnol. J. 17, 2234–2245 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Patron, N. J. et al. Standards for plant synthetic biology: a common syntax for exchange of DNA parts. N. Phytol. 208, 13–19 (2015).

    Article  CAS  Google Scholar 

  84. Jefferson, R. A., Kavanagh, T. A. & Bevan, M. W. GUS fusions: β-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J. 6, 3901–3907 (1987).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. Deplancke, B. et al. A gene-centered C. elegans protein–DNA interaction network. Cell 125, 1193–1205 (2006).

    Article  CAS  PubMed  Google Scholar 

  86. Gaudinier, A. et al. Enhanced Y1H assays for Arabidopsis. Nat. Methods 8, 1053–1055 (2011).

    Article  CAS  PubMed  Google Scholar 

  87. Pruneda-Paz, J. L. et al. A genome-scale resource for the functional characterization of Arabidopsis transcription factors. Cell Rep. 8, 622–632 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Gaudinier, A., Tang, M., Bågman, A.-M. & Brady, S. M. Identification of protein–DNA interactions using enhanced yeast one-hybrid assays and a semiautomated approach. Methods Mol. Biol. 1610, 187–215 (2017).

    Article  CAS  PubMed  Google Scholar 

  89. Du, Z., Zhou, X., Ling, Y., Zhang, Z. & Su, Z. agriGO: a GO analysis toolkit for the agricultural community. Nucleic Acids Res. 38, W64–W70 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  90. Bailey, T. L. et al. MEME Suite: tools for motif discovery and searching. Nucleic Acids Res. 37, W202–W208 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  91. Castro-Mondragon, J. A., Jaeger, S., Thieffry, D., Thomas-Chollier, M. & van Helden, J. RSAT matrix-clustering: dynamic exploration and redundancy reduction of transcription factor binding motif collections. Nucleic Acids Res. 45, e119 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. Quinlan, A. R. & Hall, I. M. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 26, 841–842 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. RStudio Team. RStudio: Integrated development environment for R v.1.1.463 (2015); http://www.rstudio.com/

  94. Wickham, H. & Sievert, C. ggplot2: Elegant Graphics for Data Analysis 2nd edn (Springer, 2016).

  95. Robinson, J. T. et al. Integrative genomics viewer. Nat. Biotechnol. 29, 24–26 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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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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  1. These authors contributed equally: Patrick J. Dickinson, Jana Kneřová.

Authors and Affiliations

  1. Department of Plant Sciences, University of Cambridge, Cambridge, UK

    Patrick J. Dickinson, Jana Kneřová, Marek Szecówka, Sean R. Stevenson, Steven J. Burgess, Hugh Mulvey & Julian M. Hibberd

  2. Department of Plant Biology and Genome Center, University of California, Davis, CA, USA

    Anne-Maarit Bågman, Allison Gaudinier & Siobhan M. Brady

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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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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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