An Arabidopsis Gene Regulatory Network for Secondary Cell Wall Synthesis

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Summary

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 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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Most cited references 47

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A high-resolution root spatiotemporal map reveals dominant expression patterns.

Siobhan M Brady, David A Orlando, Ji-Young Lee … (2007)

Transcriptional programs that regulate development are exquisitely controlled in space and time. Elucidating these programs that underlie development is essential to understanding the acquisition of cell and tissue identity. We present microarray expression profiles of a high-resolution set of developmental time points within a single Arabidopsis root and a comprehensive map of nearly all root cell types. These cell type-specific transcriptional signatures often predict previously unknown cellular functions. A computational pipeline identified dominant expression patterns that demonstrate transcriptional similarity between disparate cell types. Dominant expression patterns along the root's longitudinal axis do not strictly correlate with previously defined developmental zones, and in many cases, we observed expression fluctuation along this axis. Both robust co-regulation of gene expression and potential phasing of gene expression were identified between individual roots. Methods that combine these profiles demonstrate transcriptionally rich and complex programs that define Arabidopsis root development in both space and time.

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An enhanced transient expression system in plants based on suppression of gene silencing by the p19 protein of tomato bushy stunt virus.

Olivier Voinnet, Susana Rivas, Pere Mestre … (2003)

Transient gene expression is a fast, flexible and reproducible approach to high-level expression of useful proteins. In plants, recombinant strains of Agrobacterium tumefaciens can be used for transient expression of genes that have been inserted into the T-DNA region of the bacterial Ti plasmid. A bacterial culture is vacuum-infiltrated into leaves, and upon T-DNA transfer, there is ectopic expression of the gene of interest in the plant cells. However, the utility of the system is limited because the ectopic protein expression ceases after 2-3 days. Here, we show that post-transcriptional gene silencing (PTGS) is a major cause for this lack of efficiency. We describe a system based on co-expression of a viral-encoded suppressor of gene silencing, the p19 protein of tomato bushy stunt virus (TBSV), that prevents the onset of PTGS in the infiltrated tissues and allows high level of transient expression. Expression of a range of proteins was enhanced 50-folds or more in the presence of p19 so that protein purification could be achieved from as little as 100 mg of infiltrated leaf material. The effect of p19 was not saturated in cells that had received up to four individual T-DNAs and persisted until leaf senescence. Because of its simplicity and rapidity, we anticipate that the p19-enhanced expression system will have value in industrial production as well as a research tool for isolation and biochemical characterisation of a broad range of proteins without the need for the time-consuming regeneration of stably transformed plants.

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A battery of transcription factors involved in the regulation of secondary cell wall biosynthesis in Arabidopsis.

Ruiqin Zhong, Chanhui Lee, Jianli Zhou … (2008)

SECONDARY WALL-ASSOCIATED NAC DOMAIN PROTEIN1 (SND1) is a master transcriptional switch activating the developmental program of secondary wall biosynthesis. Here, we demonstrate that a battery of SND1-regulated transcription factors is required for normal secondary wall biosynthesis in Arabidopsis thaliana. The expression of 11 SND1-regulated transcription factors, namely, SND2, SND3, MYB103, MYB85, MYB52, MYB54, MYB69, MYB42, MYB43, MYB20, and KNAT7 (a Knotted1-like homeodomain protein), was developmentally associated with cells undergoing secondary wall thickening. Of these, dominant repression of SND2, SND3, MYB103, MYB85, MYB52, MYB54, and KNAT7 significantly reduced secondary wall thickening in fiber cells. Overexpression of SND2, SND3, and MYB103 increased secondary wall thickening in fibers, and overexpression of MYB85 led to ectopic deposition of lignin in epidermal and cortical cells in stems. Furthermore, SND2, SND3, MYB103, MYB85, MYB52, and MYB54 were able to induce secondary wall biosynthetic genes. Direct target analysis using the estrogen-inducible system revealed that MYB46, SND3, MYB103, and KNAT7 were direct targets of SND1 and also of its close homologs, NST1, NST2, and vessel-specific VND6 and VND7. Together, these results demonstrate that a transcriptional network consisting of SND1 and its downstream targets is involved in regulating secondary wall biosynthesis in fibers and that NST1, NST2, VND6, and VND7 are functional homologs of SND1 that regulate the same downstream targets in different cell types.

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Author and article information

Journal

Journal ID (nlm-journal-id): 0410462

Journal ID (pubmed-jr-id): 6011

Journal ID (nlm-ta): Nature

Journal ID (iso-abbrev): Nature

Title: Nature

ISSN (Print): 0028-0836

ISSN (Electronic): 1476-4687

Publication date Nihms-submitted: 26 November 2014

Publication date (Electronic): 24 December 2014

Publication date (Print): 29 January 2015

Publication date PMC-release: 29 July 2015

Volume: 517

Issue: 7536

Pages: 571-575

Affiliations

[a ]Department of Plant Biology, UC Davis, One Shields Ave, Davis, CA 95616 USA

[b ]Genome Center, UC Davis, One Shields Ave, Davis, CA 95616 USA

[c ]Biology Department, University of Massachusetts, Amherst MA 01003 USA

[d ]Section of Cell and Developmental Biology, Division of Biological Sciences, University of California San Diego, La Jolla, CA 92093 USA

[e ]Department of Plant and Microbial Biology, UC Berkeley Berkeley, CA 94720 USA

[f ]Department of Plant Sciences, UC Davis, One Shields Ave, Davis, CA 95616 USA

[g ]Department of Computer Science, UC Davis, One Shields Ave, Davis, CA 95616 USA

[h ]Cold Spring Harbor Laboratory, Cold Spring Harbor, 11724 NY, USA

[i ]US Department of Agriculture, Agricultural Research Service, Ithaca, NY 14853 USA

[j ]Theory of Condensed Matter Group, Cavendish Laboratory, University of Cambridge, Cambridge, CB3 0HE, United Kingdom

Author notes

[† ]To whom correspondence should be addressed at Department of Plant Biology, Genome Center UC Davis, One Shields Ave, Davis, CA 95616 USA, sbrady@ 123456ucdavis.edu (S.M.B.) and Biology Department, University of Massachusetts, Amherst, MA 01003 USA, hazen@ 123456bio.umass.edu (S.P.H.)

[1]

Current address, Division of Plant Sciences, University of Missouri, Columbia, MO 65211, USA

[2]

Current address, Department of Integrative Biology and Pharmacology, University of Texas Health Science Center at Houston Houston, TX 77030

[3]

Current address, Molecular and Computational Biology Section, University of Southern California, Los Angeles, CA 90089

[*]

These authors contributed equally to this work

Article

Manuscript ID: NIHMS644194

DOI: 10.1038/nature14099

PMC ID: 4333722

PubMed ID: 25533953

SO-VID: fafb3caa-17b3-4b47-98c6-af8bf3e24d04

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