Navigating the transcriptional roadmap regulating plant secondary cell wall deposition

Abstract

The current status of lignocellulosic biomass as an invaluable resource in industry, agriculture, and health has spurred increased interest in understanding the transcriptional regulation of secondary cell wall (SCW) biosynthesis. The last decade of research has revealed an extensive network of NAC, MYB and other families of transcription factors regulating Arabidopsis SCW biosynthesis, and numerous studies have explored SCW-related transcription factors in other dicots and monocots. Whilst the general structure of the Arabidopsis network has been a topic of several reviews, they have not comprehensively represented the detailed protein-DNA and protein-protein interactions described in the literature, and an understanding of network dynamics and functionality has not yet been achieved for SCW formation. Furthermore the methodologies employed in studies of SCW transcriptional regulation have not received much attention, especially in the case of non-model organisms. In this review, we have reconstructed the most exhaustive literature-based network representations to date of SCW transcriptional regulation in Arabidopsis. We include a manipulable Cytoscape representation of the Arabidopsis SCW transcriptional network to aid in future studies, along with a list of supporting literature for each documented interaction. Amongst other topics, we discuss the various components of the network, its evolutionary conservation in plants, putative modules and dynamic mechanisms that may influence network function, and the approaches that have been employed in network inference. Future research should aim to better understand network function and its response to dynamic perturbations, whilst the development and application of genome-wide approaches such as ChIP-seq and systems genetics are in progress for the study of SCW transcriptional regulation in non-model organisms.

Keywords: Arabidopsis; secondary cell wall; transcription factor; transcriptional network; wood formation.

Figure 1

The generalized Arabidopsis SCW transcriptional regulatory network in the light of vascular differentiation. Vascular meristems, representing procambiums or secondary cambiums, produce mother cells that differentiate into phloem and immature xylem tissue (gray boxes) under the influence of transcriptional, hormonal, peptide, and miRNA regulators. Terminal differentiation of immature xylem cells into vessel elements and fibers is regulated by a tiered transcriptional network regulating genes associated with secondary cell wall cellulose, hemicellulose, programmed cell death (PCD), signaling, lignin, and genes with unknown functions. Positive regulation is indicated by black arrows; negative regulation is represented by red edges. Block colors represent different biological function categories. TFs currently known to regulate only one functional category are color-matched accordingly; orange blocks denote regulation of a combination of functional categories. The same color scheme is used in Additional file 1.

Figure 2

Schematic representation of the protein–DNA interaction network underlying SCW biosynthesis in xylem fibers and vessels and anther endothecium in Arabidopsis. Interactions occurring specifically in primary cell wall tissues are also indicated. Direct protein–DNA interactions involving activation or repression are represented using solid edges, while known regulatory relationships in which the mechanism is unclear are represented with dashed edges. Repressors are denoted with red edges. Protein–protein interactions are represented as ◊; question marks represent unidentified upstream TFs; overlapping edges (MYB46, MYB83) represent redundancy. Target genes are arranged semi-hierarchically according to known functions. The complete list of supporting literature used to construct the network can be found in Data sheet 1

Figure 3

Putative modules and motifs underlying SCW transcriptional regulation. (A) Negative feedback loop regulating SND1. (B) Negative regulation of structural genes by KNAT7. (C) Positive feedback loop regulating VND6/VND7. Dashed edges indicate unknown molecular mechanisms of protein–DNA interactions. Arrows indicate positive regulation, blunt ends indicate negative interactions. Dumbbells represent protein–protein interactions. Refer to (see section Network Dynamics) for detailed discussion.