Ethylene Signaling Is Required for Fully Functional Tension Wood in Hybrid Aspen

Abstract

Tension wood (TW) in hybrid aspen trees forms on the upper side of displaced stems to generate a strain that leads to uplifting of the stem. TW is characterized by increased cambial growth, reduced vessel frequency and diameter, and the presence of gelatinous, cellulose-rich (G-)fibers with its microfibrils oriented parallel to the fiber cell axis. Knowledge remains limited about the molecular regulators required for the development of this special xylem tissue with its characteristic morphological, anatomical, and chemical features. In this study, we use transgenic, ethylene-insensitive (ETI) hybrid aspen trees together with time-lapse imaging to show that functional ethylene signaling is required for full uplifting of inclined stems. X-ray diffraction and Raman microspectroscopy of TW in ETI trees indicate that, although G-fibers form, the cellulose microfibril angle in the G-fiber S-layer is decreased, and the chemical composition of S- and G-layers is altered than in wild-type TW. The characteristic asymmetric growth and reduction of vessel density is suppressed during TW formation in ETI trees. A genome-wide transcriptome profiling reveals ethylene-dependent genes in TW, related to cell division, cell wall composition, vessel differentiation, microtubule orientation, and hormone crosstalk. Our results demonstrate that ethylene regulates transcriptional responses related to the amount of G-fiber formation and their properties (chemistry and cellulose microfibril angle) during TW formation. The quantitative and qualitative changes in G-fibers are likely to contribute to uplifting of stems that are displaced from their original position.

Genome-wide analysis of lncRNA and mRNA expression and endogenous hormone regulation during tension wood formation in Catalpa bungei

“…In our study, the vessels were smaller, and the vessel length:width ratio was significantly larger in TW than in OW and NW. Previous studies also confirmed that TW has smaller and longer vessels [10,14]. In addition, the TW of C. bungei had a thinner secondary wall without a G-layer.…”

“…The anatomy of TW is vastly different from NW. Generally, TW is described as having small vessels and a high ratio of fibers to vessels and a gelatinous layer (G-layer) is included in the fiber lumen in some tree species [13,14]. The specialization of these cells and tissues is often regulated by endogenous hormones.…”

“…Felten et al (2018) compared the xylem development of wild-type and ethylene-insensitive hybrid poplars following ethylene application and found that ethylene activated some transcription factors and triggered G-layer formation [ 16 ]. Moreover, ethylene was recently shown to be a key phytohormone regulating TW formation [ 14 ]. Gibberellin (GA) enhances the activity of cambium [ 17 ], and xylem specialization may be caused by changes in vascular cambium function.…”

Comparative transcriptomics of stem bark reveals genes associated with bast fiber development in Boehmeria nivea L. gaud (ramie)

“…Auxin is a well-known hormone crucial for plant cell wall development [21]. In addition, ethylene signaling has recently been recognized to be necessary for the deposition of gelatinous layer of fiber cells [22,23]. Ethylene signaling involves the perception of the hormone by the ER-localized receptor, and upon ethylene binding, the negative regulator CTR1 is released from the receptor, resulting in non-phosphorylation of the ER-localized EIN2.…”

Comparative transcriptomics of stem bark reveals genes associated with bast fiber development in Boehmeria nivea L. Gaud (ramie)

“…In addition, ethylene signaling has recently been recognized to be necessary for the deposition of gelatinous layer of fiber cells [22,23]. Ethylene signaling involves the perception of the hormone by the ER-localized receptor, and upon ethylene binding, the negative regulator CTR1 is released from the receptor, resulting in non-phosphorylation of the ER-localized EIN2.…”