Wood development: Growth through knowledge

Abstract

Nature Plants, Published online: 5 May 2015; | doi:10.1038/nplants.2015.60

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NATURE PLANTS | VOL 1 | MAY 2015 | www.nature.com/natureplants 1
PUBLISHED: 5 MAY 2015 | ARTICLE NUMBER: 15060 | DOI: 10.1038/NPLANTS.2015.60
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Trees are important natural sources of
sustainable energy. Wood, the major
product of secondary growth, is
derived from a lateral meristem, the vascular
cambium, which gives rise to xylem (the
wood itself) inwards and phloem outwards.
Cambial activity is especially pronounced
in trees, which undergo seasonal growth
patterns involving ne-tuned and multilevel
regulation. Many attempts have been made
to promote wood production by modulating
various regulators at dierent levels, but
these have frequently aected the wood’s
properties. Writing in Current Biology,
Etchells etal.1 report that by manipulating
expression of just two genes they can make
trees that grow faster and yield more biomass
without altering the tree’s morphology.
Previously, modication of gibberellic
acid levels by ectopically overexpressing
a gibberellic acid biosynthesis enzyme
(GA20-oxidase) had been shown to greatly
increase growth rate and biomass yield
in trees2. In these trees, the xylem bre
number can be increased up to 71% while
the stem dry weight can be 126% higher
than the control plants, but the results are
variable. Alternatively secondary growth of
trees can also be enhanced by application
of ethylene, a phytohormone involved in
formation of specialized wood as a result of
mechanical tension3, however, this results
in morphological and property changes in
the wood. e expression of several ethylene
response factors (ERFs) under the control
of a xylem specic promoter (pLMX5)
indicated that, although tree diameter and
height can be increased, the outcome is
greatly aected by environmental changes.
Additionally the wood’s anatomy and
chemistry can be modied4.
e approach of Etchell and colleagues
was to co-overexpress a receptor (PXY, also
known as TDR) with its ligand (CLE41,
also known as TDIF) in a tissue-specic
manner. Aspen trees transgenic for the
receptor–ligand pair, produced 89% more
xylem cells and more than double the dry
weight in the middle and base of stems
compared to wild type. is strategy might
add robustness to the system of secondary
growth by a controlled application of our
current knowledge but due to the lack of
a standardized method to quantify the
growth traits in experimental trees, it is
dicult to compare the achievements using
dierent strategies.
e regulatory network of cambium
development and secondary growth
(Fig.1) is yet to be fully elucidated aside
from the PXY–CLE41 signalling pathway
of Arabidopsis, which has similarities to
the regulation of stem cell homeostasis
in the shoot apical meristem (SAM) by
the CLAVATA1 (CLV1) receptor kinase
and the CLV3 peptide ligand5. Phloem
derived CLE41 peptides are perceived
by cambial cells through PXY receptors.
e PXY–CLE41 pathway has two
roles in regulating secondary growth:
promotion of cambium cell proliferation
and repression of xylem dierentiation6,7.
Two transcription factors WOX4 and
WOX14 act as major downstream factors of
PXY–CLE41 to positively regulate cambial
cell proliferation6,8. Furthermore, the
PXY–WOX4 pathway appears to interact
with ethylene signalling in regulating the
division rate of cambial cells9. In addition,
GSK3 proteins have been shown to regulate
xylem cell dierentiation downstream of
the PXY–CLE41 pathway10. PXY–CLE41
also play an important role controlling the
orientation of cell division thus contributing
to vascular patterning7.
WOOD DEVELOPMENT
Growth through knowledge
Overexpressing a receptor–ligand pair specifically in their native tissue domains dramatically promotes wood
formation and biomass production in trees.
Jing Zhang, Juan Antonio Alonso Serra and Ykä Helariutta
Environmental
factors
Hormonal regulation
auxin, CK, GA
ethylene
Transcriptional
regulation
CLE41
WOX4
GSK3s WOX14
PXY
Proliferation
Dierentiation
Cambium Phloem
Xylem
100 μm
Figure 1 | Regulatory factors controlling secondary growth. The receptor–ligand node is shown within its
natural expression domains across the vascular cambium of a Populus trichocarpa stem. Hormonal and
transcriptional regulators coordinate a fine-tuned multilevel regulation to maintain undierentiated stem
cells in the cambium, and trigger dierentiation into xylem towards the centre of the stem, and phloem
toward the outside. Their potential applications towards enhanced wood/biomass production is improved
when the specific spatiotemporal expression of the receptor (PXY) and ligand (CLE41) is considered.
GA, gibberellic acid; CK, cytokinins.
© 2015 Macmillan Publishers Limited. All rights reserved

2 NATURE PLANTS | VOL 1 | MAY 2015 | www.nature.com/natureplants
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Auxin and cytokinins have been
implicated as key regulators for cambial
activity both in Arabidopsis and trees5, but
it was not known how the PXY–CLE41
pathway plays a role in regulating
cambial activity in woody species.
Etchells etal. have now demonstrated that
the PXY–CLE pathway is conserved in trees,
as overexpressing poplar CLE41 and PXY
in Arabidopsis produces disturbed vascular
patterns with increased cell numbers and
complements pxy mutants respectively1.
Previously overexpressing WOX4 under a
35S promoter could not enhance secondary
growth in Arabidopsis6 but Etchells etal.
have adopted a smart strategy to enhance
hierarchical signalling by co-overexpressing
the receptor–ligand pair. ey initially
used the 35S promoter to ubiquitously
express CLE41 and PXY, which didn’t
result in enhancement of growth but led
to disrupted growth patterns and reduced
growth in some lines. Next they employed
two tissue-specic promoters from Populus
genes, AINTEGUMENTA (ANT) and
PHLOEM PROTEIN2 (PP2), to target
receptor and ligand to tissues where they
are endogenously expressed, cambium for
the PXY and phloem for CLE41. Regular
wood morphology was thus maintained,
but more strikingly cambium activity and
secondary growth was greatly enhanced
especially when receptor and ligand are
co-overexpressed.
e necessity of phloem-specic
expression of CLE peptide for the
maintenance of proper tissue integrity
has been demonstrated previously in
Arabidopsis7, highlighting the conserved
mechanism of the PXY–CLE pathway
between herbaceous and woody species.
Although there is a negative feedback
interaction between PXY and CLE41 (PXY
expression is reduced in 35S::CLE41 plants),
by tissue specically overexpressing both
this negative loop seems to be bypassed,
as was also indicated in Arabidopsis7.
Intriguingly, overexpressing the two
components simultaneously in their own
tissues leads to synergistic and positive
eects. It is also interesting that xylem
dierentiation is not inhibited.
While it is exciting to observe the
dramatic enhancement of biomass
following coordinated overexpression of
the PXY–CLE41 regulons, the full eects
at a molecular level remain to be revealed.
Apical as well as radial growth appears to be
aected since double overexpression lines
are taller with more and longer internodes,
indicating a modication of SAM activity
and cell expansion. Given the fact that
neither PXY nor CLE41 is expressed in
apical meristem7, it will be interesting
to examine whether this global eect on
growth is the result of using the ANT
promoter, which is also expressed in the
apical shoot11. Perhaps they can functionally
swap with CLV1–CLV3 to regulate SAM
activity. Alternatively enhanced secondary
growth could be due to an increase in sink
capacity as pointed out by the authors.
Moreover, it remains to be seen whether
the wood quality is changed, or how
stable the phenotypes of transgenic trees
growing under natural environments are.
A eld test similar to that recently reported
by van Acker etal.12 would be a next
logical step.
Regulation of secondary growth is under
multiple levels of both spatial and temporal
control. is work implies that to manipulate
this process to achieve enhanced tree growth,
a protable strategy could be to intelligently
combine even more regulators from the
PXY–CLE41 and related pathways. ❐
Jing Zhang1, Juan Antonio Alonso Serra2
and Ykä Helariutta1,2 are at 1e Sainsbury
Laboratory, University of Cambridge, Bateman
Street, Cambridge CB2 1LR, UK. 2Department of
Biological and Environmental Sciences, Institute of
Biotechnology, University of Helsinki, P.O.Box65,
00014 Helsinki, Finland.
e-mail: yrjo.helariutta@slcu.cam.ac.uk
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