Transcription Factor Network Gets to Heart of Wood Formation

North Carolina State University researchers have uncovered how a complex network of transcription factors switch wood formation genes on and off. Understanding this transcriptional regulatory network has applications for modifying wood properties for timber, paper and biofuels, as well as making forest trees more disease- and pest-resistant.

“We’re building a complete story, so to speak, of how wood formation
functions – all the intricate components, how they interact and how they fit
together to regulate wood formation inside the cell walls of woody plants,”
says Jack Wang, assistant professor in the College of Natural Resources and
co-lead author of a Plant Cell
article about the work.

Researchers with NC State’s Forest Biotechnology Group used transgenic
black cottonwood (Populus trichocarpa),
a species they’ve studied intensively, to identify interactions in a
transcriptional regulatory network directed by a key transcription factor,
PtrSND1-B1. The researchers documented four levels of interactions in the
network, from DNA to enzyme levels. The work is an extension of two previous
studies, in which functions of PtrSND1-B1 were discovered using a wood-forming
cell system. These early studies were published in PNAS and Plant Cell by
co-authors Quanzi Li, Ying-Chung Lin and Wei Li of the Forest Biotechnology
Group, led by Vincent Chiang.

“Transcription factors – a complex network of them – regulate which wood formation genes are turned on or off,” Wang says. “Essentially these are high-level regulatory switches.

“Understanding this network allows us to identify single switches inside that complex network of transcription factors that could simultaneously control multiple wood-forming genes. Instead of working with one, two or three genes at a time, which is our current limit, plant biologists could work with tens of genes at a time.”

The new study upends ideas about transcriptional regulatory networks
inferred from work with nonwoody species, such as Arabidopsis thaliana, a model plant.

“This network of transcription factor regulation in woody tissues is almost completely different from the regulatory processes in Arabidopsis and other plants,” says Hao Chen, co-lead author of the article and a postdoctoral researcher at NC State.

“Of 57 regulatory interactions we identified, 55 were specific to woody plant tissue, showing that herbaceous plants like Arabidopsis cannot stand in for woody plants.”

The study provides an extensive look at a transcriptional
regulatory network in woody
plants. Researchers’ goal is to provide a toolkit for building trees with
specific properties needed for commercial timber, paper, biofuel production and
conservation needs.

Plant biologists tested 42 of the interactions
they found in lines of transgenic black cottonwood, verifying the function of
about 90 percent. The network
revealed which genes are common targets for specific transcription factors. As
a result, researchers found nine new protein-protein interactions involved in
forming lignin, a component in the cell wall that gives wood its strength and
density.

Wang says several recent studies show that lignin is related to disease
and insect resistance in trees, a major concern. A 2012 U.S. Forest Service
report estimated that 7 percent of the nation’s forests are in jeopardy of
losing more than a quarter of their tree vegetation by 2027. The amount of
threatened vegetation rose by 40 percent in just six years.

“Studies like this that look at lignification and wood formation will
have great value in helping to understand how trees can be made to be more
robust and to improve forest health in general,” Wang says.

This work was supported in part by
the U.S. Office of Science (Biological and Environmental Research), Department
of Energy Grant DESC000691.

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Note: An
abstract of the paper follows.

“Hierarchical
Transcription-Factor and Chromatin Binding Network for Wood Formation in Populus trichocarpa

Authors: Hao
Chen, Jack P. Wang, Huizi Liu, Huiyu Li, Ying-Chung Jimmy Lin, Rui Shi, Chenmin
Yang, Jinghui Gao, Chenguang Zhou, Quanzi Li, Ronald R. Sederoff, Wei Li, Vincent
L. Chiang

Published: Plant Cell

DOI: https://doi.org/10.1105/tpc.18.00620

Abstract: Wood
remains the world’s most abundant and renewable resource for timber and pulp,
and an alternative to fossil fuels. Understanding the molecular regulation of wood
formation can advance the engineering of wood for more efficient material and
energy productions. We integrated a Populus
trichocarpa
wood forming cell-system with quantitative transcriptomics and
chromatin-binding assays to construct a transcriptional regulatory network
(TRN) directed by a key transcription factor (TF), PtrSND1-B1. The network
consists of 4 layers of TF-target gene interactions with quantitative
regulatory effects, describing the specificity of how the regulation is
transduced through these interactions to activate cell-wall genes (effector
genes) for wood formation. PtrSND1-B1 directs 57 TF-DNA interactions through 17
TFs transregulating 27 effector genes. Of the 57 interactions, 55 are novel. We
tested 42 of these 57 interactions in 30 genotypes of transgenic P. trichocarpa and verified that ~ 90%
of the tested interactions function in
vivo
. The TRN reveals common transregulatory targets for distinct TFs,
leading to the discovery of 9 novel TF protein-complexes (dimers and trimers)
implicated in regulating the biosynthesis of specific types of lignin. Our work
suggests that wood formation may involve regulatory homeostasis determined by
combinations of TF-DNA and TF-TF (protein-protein) regulations.