Deciphering the intricate hierarchical gene regulatory network: unraveling multi-level regulation and modifications driving secondary cell wall formation

Abstract

Wood quality is predominantly determined by the amount and the composition of secondary cell walls (SCWs). Consequently, unraveling the molecular regulatory mechanisms governing SCW formation is of paramount importance for genetic engineering aimed at enhancing wood properties. Although SCW formation is known to be governed by a hierarchical gene regulatory network (HGRN), our understanding of how a HGRN operates and regulates the formation of heterogeneous SCWs for plant development and adaption to ever-changing environment remains limited. In this review, we examined the HGRNs governing SCW formation and highlighted the significant key differences between herbaceous Arabidopsis and woody plant poplar. We clarified many confusions in existing literatures regarding the HGRNs and their orthologous gene names and functions. Additionally, we revealed many network motifs including feed-forward loops, feed-back loops, and negative and positive autoregulation in the HGRNs. We also conducted a thorough review of post-transcriptional and post-translational aspects, protein-protein interactions, and epigenetic modifications of the HGRNs. Furthermore, we summarized how the HGRNs respond to environmental factors and cues, influencing SCW biosynthesis through regulatory cascades, including many regulatory chains, wiring regulations, and network motifs. Finally, we highlighted the future research directions for gaining a further understanding of molecular regulatory mechanisms underlying SCW formation.

Figure 1

The expression patterns and direct target genes of secondary cell wall NAC TFs (SWNs) in Arabidopsis. The top panel shows the cell/tissue-selectivity of different SWNs of Arabidopsis, while the bottom panel shows the direct target genes and their functions of SWNs in the SCW formation.

Figure 2

The hierarchical gene regulatory network (HGRN) controlling secondary cell wall (SCW) formation in Arabidopsis. The first-level transcription factors (TFs), SWNs, include SND1, NST1/2, and VND1–7; first and a half-level TFs include SND2–5; the second-level master switches includes MBY46/83. Only genes that have been proven to be involved in regulation of SCW biosynthesis are included in the diagram.

Figure 3

Multi-level regulation of fourth-level structural genes by third-level TFs and some master switch TFs in the hierarchical gene regulatory network (HGRN) that governs secondary cell wall (SCW) formation in Arabidopsis. Only genes that have been proven to be involved in regulation of SCW biosynthesis are included in the diagram.

Figure 4

Complex regulatory relationships are represented by various network motifs among transcription factors (TFs) in the hierarchical gene regulatory network (HGRN) of Arabidopsis.

Figure 5

Illustrates the conversion between Arabidopsis Secondary Wall NACs (SWNs) and their poplar counterparts, referred to as Wood-Associated NAC Domain proteins (WNDs) or those with alternative names such as VNs, VNSs, or VNDs used in existing literature. It also highlights the primary functions of their target genes in Secondary Cell Wall (SCW) formation in poplar.

Figure 6

The multi-layered HGRN controlling secondary cell wall (SCW) formation in Poplar. Only genes that have been proven to be involved in regulation of SCW biosynthesis are included in the diagram.

Figure 7

Multi-level modification of hierarchical gene regulatory network (HGRN) modulate the biosynthesis of heterogenous secondary cell wall (SCW).