Abstract

The plant cell wall is an important factor for determining cell shape, function and response to the environment. Secondary cell walls, such as those found in xylem, are composed of cellulose, hemicelluloses and lignin and account for the bulk of plant biomass. The coordination between transcriptional regulation of synthesis for each polymer is complex and vital to cell function. A regulatory hierarchy of developmental switches has been proposed, although the full complement of regulators remains unknown. Here we present a protein–DNA network between Arabidopsis thaliana transcription factors and secondary cell wall metabolic genes with gene expression regulated by a series of feed-forward loops. This model allowed us to develop and validate new hypotheses about secondary wall gene regulation under abiotic stress. Distinct stresses are able to perturb targeted genes to potentially promote functional adaptation. These interactions will serve as a foundation for understanding the regulation of a complex, integral plant component.

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Acknowledgements

We thank M. Tierney (University of Vermont) for 35S::GFP seeds, T. Demura for VND7 resources, M.K. Barton for REV:GR seeds, E.P. Spalding for advice on manuscript revision, and C. Gutierrez for E2Fc RNAi and E2Fc N-terminal deletion overexpressor seeds and useful discussion. This research was supported by the Office of Science (BER) Department of Energy Grant DE-FG02-08ER64700DE (to S.P.H. and S.A.K.), National Institute of General Medical Sciences of the National Institutes of Health under award numbers RO1GM056006 and RC2GM092412 (to S.A.K.), National Institute of Health (R01GM107311) and National Science Foundation (IOS-1036491 and IOS-1352478) to K.D., USDA CRIS 1907-21000-030 to D.W. and L.F., a Royal Society UK Fellowship (to S.E.A.), and UC Davis Startup Funds and a Hellman Fellowship (to S.M.B).

Author information

Author notes

    • M. Taylor-Teeples
    • , L. Lin
    •  & M. de Lucas

    These authors contributed equally to this work.

    • L. Lin
    • , G. Breton
    •  & S. A. Kay

    Present addresses: Division of Plant Sciences, University of Missouri, Columbia, Missouri 65211, USA (L.L.); Department of Integrative Biology and Pharmacology, University of Texas Health Science Center at Houston, Houston, Texas 77030, USA (G.B.); Molecular and Computational Biology Section, University of Southern California, Los Angeles, California 90089, USA (S.A.K.).

Affiliations

  1. Department of Plant Biology, University of California Davis, One Shields Avenue, Davis, California 95616, USA

    • M. Taylor-Teeples
    • , M. de Lucas
    • , G. Turco
    • , T. W. Toal
    • , A. Gaudinier
    • , C. Wang
    • , K. Dehesh
    •  & S. M. Brady
  2. Genome Center, University of California Davis, One Shields Avenue, Davis, California 95616, USA

    • M. Taylor-Teeples
    • , M. de Lucas
    • , G. Turco
    • , T. W. Toal
    • , A. Gaudinier
    • , A. Tsoukalas
    • , I. Tagkopoulos
    •  & S. M. Brady
  3. Biology Department, University of Massachusetts, Amherst, Massachusetts 01003, USA

    • L. Lin
    • , N. F. Young
    • , G. M. Trabucco
    • , M. T. Veling
    • , R. Lamothe
    • , P. P. Handakumbura
    •  & S. P. Hazen
  4. Department of Plant and Microbial Biology, University of California Berkeley, Berkeley, California 94720, USA

    • G. Xiong
    •  & M. Pauly
  5. Department of Plant Sciences, University of California Davis, One Shields Avenue, Davis, California 95616, USA

    • J. Corwin
    •  & D. J. Kliebenstein
  6. Department of Computer Science, University of California Davis, One Shields Avenue, Davis, California 95616, USA

    • A. Tsoukalas
    •  & I. Tagkopoulos
  7. Cold Spring Harbor Laboratory, Cold Spring Harbor, New York 11724, USA

    • L. Zhang
    •  & D. Ware
  8. US Department of Agriculture, Agricultural Research Service, Ithaca, New York 14853, USA

    • D. Ware
  9. Section of Cell and Developmental Biology, Division of Biological Sciences, University of California San Diego, La Jolla, California 92093, USA

    • G. Breton
    • , J. L. Pruneda-Paz
    •  & S. A. Kay
  10. Theory of Condensed Matter Group, Cavendish Laboratory, University of Cambridge, Cambridge CB3 0HE, UK

    • S. E. Ahnert

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Contributions

M.T.-T., L.L. and M.d.L. contributed equally to this work. T.W.T. and A.G. contributed equally to this work. S.M.B. and S.P.H. contributed equally to this work. M.T.-T., L.L., M.d.L., S.M.B., and S.P.H. designed the research. M.T.-T., L.L., M.d.L., A.G., G.X., N.F.Y., G.M.T., M.T.V., R.L., P.P.H., C.W., and K.D. performed the research. M.T.-T., L.L., G.T., T.W.T., N.T., J.C., M.P., D.K., I.T., S.E.A., S.M.B. and S.P.H. analysed the data. L.Z., D.W., G.B., J.L.P.-P., and S.A.K. contributed new reagents/analytic tools. M.T.-T., L.L., G.M.T., S.M.B. and S.P.H. wrote the article. All authors discussed the results and commented on the manuscript.

Competing interests

The authors declare no competing financial interests.

Corresponding authors

Correspondence to S. P. Hazen or S. M. Brady.

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