Abstract
Thickening of tree stems is the result of secondary growth, accomplished by the meristematic activity of the vascular cambium. Secondary growth of the stem entails developmental cascades resulting in the formation of secondary phloem outwards and secondary xylem (i.e., wood) inwards of the stem. Signaling and transcriptional reprogramming by the phytohormone ethylene modifies cambial growth and cell differentiation, but the molecular link between ethylene and secondary growth remains unknown. We addressed this shortcoming by analyzing expression profiles and co-expression networks of ethylene pathway genes using the AspWood transcriptome database which covers all stages of secondary growth in aspen (Populus tremula) stems. ACC synthase expression suggests that the ethylene precursor 1-aminocyclopropane-1-carboxylic acid (ACC) is synthesized during xylem expansion and xylem cell maturation. Ethylene-mediated transcriptional reprogramming occurs during all stages of secondary growth, as deduced from AspWood expression profiles of ethylene-responsive genes. A network centrality analysis of the AspWood dataset identified EIN3D and 11 ERFs as hubs. No overlap was found between the co-expressed genes of the EIN3 and ERF hubs, suggesting target diversification and hence independent roles for these transcription factor families during normal wood formation. The EIN3D hub was part of a large co-expression gene module, which contained 16 transcription factors, among them several new candidates that have not been earlier connected to wood formation and a VND-INTERACTING 2 (VNI2) homolog. We experimentally demonstrated Populus EIN3D function in ethylene signaling in Arabidopsis thaliana. The ERF hubs ERF118 and ERF119 were connected on the basis of their expression pattern and gene co-expression module composition to xylem cell expansion and secondary cell wall formation, respectively. We hereby establish data resources for ethylene-responsive genes and potential targets for EIN3D and ERF transcription factors in Populus stem tissues, which can help to understand the range of ethylene targeted biological processes during secondary growth.
Highlights
Woody tissue serves as plant stabilizing material, in nutrient storage and distribution of water and minerals
In the absence of ethylene, the CTR1 N-terminus binds to the receptors, while the C-terminus containing the kinase domain, prevents transcription of ethylene-regulated genes by triggering degradation of EIN2 (Clark et al, 1998; Huang et al, 2003; Ju et al, 2012)
Among them we found a homolog of VND-INTERACTING 2 (VNI2; AT5G13180) which in A. thaliana interacts with VND7 and functions to suppress xylem vessel formation (Yamaguchi et al, 2010) and NARS1/NAC2 (AT3G15510) shown to be involved in SCW development of seed coat epidermal cells (Voiniciuc et al, FIGURE 4 | EIN3 isoforms are co-expressed with TFs involved in transcriptional regulation and secondary cell wall biosynthesis. (A) Co-expression gene modules of EIN3B, EIN3C, EIN3D, and EIN3F
Summary
Woody tissue serves as plant stabilizing material, in nutrient storage and distribution of water and minerals. Powerful are the transcriptomic and proteomic datasets that have been generated in aspen (Populus tremula) and Norway spruce (Picea abies) (Obudulu et al, 2016; Bygdell et al, 2017; Jokipii-Lukkari et al, 2017; Sundell et al, 2017). Their high spatial resolution within the woody tissues allows analyses in specific phases of wood formation, from cell division to cell death. Transcriptomic datasets from aspen and Norway spruce (Picea abies) are accessible in the form of the AspWood and NorWood databases (Jokipii-Lukkari et al, 2017; Sundell et al, 2017)
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