Abstract

In plants, GATA transcription factors (TFs) have been reported to play vital roles in to a wide range of biological processes. To date, there is still no report about the involvement and functions of woody plant GATA TFs in wood formation. In this study, we described the functional characterization of a Populus trichocarpa GATA TF, PtrGATA12, which encodes a nuclear-localized transcriptional activator predominantly expressing in developing xylem tissues. Overexpression of PtrGATA12 not only inhibited growths of most phenotypic traits and biomass accumulation, but also altered the expressions of some master TFs and pathway genes involved in secondary cell wall (SCW) and programmed cell death, leading to alternated SCW components and breaking forces of stems of transgenic lines. The significant changes occurred in the contents of hemicellulose and lignin and SCW thicknesses of fiber and vessel that increased by 13.5 and 10.8%, and 20.83 and 11.83%, respectively. Furthermore, PtrGATA12 bound directly to the promoters of a battery of TFs and pathway genes and activated them; the binding sites include two cis-acting elements that were specifically enriched in their promoter regions. Taken together, our results suggest PtrGATA12, as a higher hierarchical TF on the top of PtrWND6A, PtrWND6B, PtrMYB152, and PtrMYB21, exert a coordinated regulation of SCW components biosynthesis pathways through directly and indirectly controlling master TFs, middle-level TFs, and further downstream pathway genes of the currently known hierarchical transcription network that governs SCW formation.

Highlights

  • Wood accounts for the bulk of biomass produced by land plants, and has been considered to be an important renewable and environmentally friendly source of bioenergy (Ohlrogge et al, 2009)

  • These PtrGATA proteins contained a region with 34 aa that might serve as a nuclear location signal (NLS), and an acidic aminoterminal domain that might act as an activation domain (Figure 1B)

  • Considerable studies have revealed that the secondary cell wall (SCW) biosynthesis is mainly regulated by a multilayered hierarchical transcription regulation network with the regulatory edges, chains of command, pointing downward the pathway genes at the low hierarchy, which ensures a differential regulation on the formation of diverse SCW with varied components and thicknesses in various cells and across different tissues (Zhong et al, 2007, 2010a; Zhou et al, 2009; Du and Groover, 2010; Yamaguchi et al, 2010)

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Summary

Introduction

Wood accounts for the bulk of biomass produced by land plants, and has been considered to be an important renewable and environmentally friendly source of bioenergy (Ohlrogge et al, 2009). The currently known top-layered regulatory genes in this network are NAC SND1 (McCarthy et al, 2009), VND6/7 (Ohashi-Ito et al, 2010; Yamaguchi et al, 2010), and PtrWND2B/6B (Zhong et al, 2010a, 2011), which function as master regulators for xylem cell differentiation (Zhong et al, 2010a, 2011) Downstream of these NAC master TFs are the MYB46/83 and PtrMYB3/20, which function as intermediate level hub regulators (McCarthy et al, 2009, 2010; Ko et al, 2012), whose targets are SCW-associated genes, including other lower-level MYB TFs, such as MYB58, MYB63, PtrMYB125, PpDof, and PdOLP1 (Zhou et al, 2009; Rueda-Lopez et al, 2017; Balmant et al, 2020; Li et al, 2020). We initiated a project to identify more middle-level “hub” regulators, and high hierarchical regulators that can differentially control multiple SCW component biosynthetic pathways, and believe that they are instrumental for genetical engineering wood composition and quality

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