Ethylene-Related Gene Expression Networks in Wood Formation

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.

Recent Advances in the Transcriptional Regulation of Secondary Cell Wall Biosynthesis in the Woody Plants

“… Liu et al (2017) reported that Populus ERF type TF, PsnSHN2 , is predominantly expressed in xylem tissues, and that it positively regulates cellulose and hemicellulose biosynthesis but negatively regulates lignin biosynthesis. Recently, Seyfferth et al (2018) constructed an ethylene-related gene expression network during SCW formation, ETHYLENE INSENSITIVE 3D ( EIN3D ) and 11 ERFs were identified as hub genes. Interestingly, a VNI2 homolog is highly associated with EIN3D , suggesting EIN3D may act upstream or together with VIN2 during SCW formation.…”

An AP2/ERF transcription factor ERF139 coordinates xylem cell expansion and secondary cell wall deposition

“…The APETALA2/ethylene response factors (AP2/ERFs) are TFs that have been frequently implicated in regulation of xylem differentiation and wood formation but that are functionally poorly described (Seyfferth et al ., ). Evidence is accumulating, however, that AP2/ERF TFs may play a role in lignin biosynthesis (Ambavaram et al ., ; Vahala et al ., ; Taylor‐Teeples et al ., ; Lee et al ., ).…”

Poplar carbohydrate‐active enzymes: whole‐genome annotation and functional analyses based on RNA expression data

“…Of these, PtNAC156, PtBLH3 and PtMYB128 were associated with PtGT43B, but not with PtGT43C (Figure 4a). PtGT43B was also uniquely co-expressed with an ethylene response factor (ERF) transcription factor PtERF119 homologous to AtSHINE3 (AtSHN3), which was recently found as an important hub transcription factor in secondary wall forming aspen xylem (Seyfferth et al, 2018). Overexpression of the closely related Populus SHN2/ERF118 gene induced cellulose and hemicellulose and suppressed lignin biosynthesis in Nicotiana tabacum (tobacco; Liu et al, 2017).…”