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Populus: A Model System for Plant Biology

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Annu. Rev. Plant Biol. 2007. 58:435–58
The Annual Review of Plant Biology is online at
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This article’s doi:
10.1146/annurev.arplant.58.032806.103956
Copyright  c 2007 by Annual Reviews.
All rights reserved
First published online as a Review in Advance on
February 5, 2007
1543-5008/07/0602-0435$20.00
Populus: A Model System
for Plant Biology
Stefan Jansson1 and Carl J. Douglas2
1
Department of Plant Physiology, Umeå Plant Science Center, Umeå University,
SE-901 87 Umeå, Sweden; email: stefan.jansson@plantphys.umu.se
2
Department of Botany, University of British Columbia, Vancouver BC V6T 1Z4,
Canada; email: cdouglas@interchange.ubc.ca
Key Words
genomics, wood formation, seasonality, flowering, biotic
interactions, natural variation
Abstract
With the completion of the Populus trichocarpa genome sequence and
the development of various genetic, genomic, and biochemical tools,
Populus now offers many possibilities to study questions that cannot
be as easily addressed in Arabidopsis and rice, the two prime model
systems of plant biology and genomics. Tree-specific traits such as
wood formation, long-term perennial growth, and seasonality are
obvious areas of research, but research in other areas such as control
of flowering, biotic interactions, and evolution of adaptive traits is
enriched by adding a tree to the suite of model systems. Furthermore,
the reproductive biology of Populus (a dioeceous wind-pollinated
long-lived tree) offers both new possibilities and challenges in the
study and analysis of natural genetic and phenotypic variation. The
relatively close phylogenetic relationship of Populus to Arabidopsis in
the Eurosid clade of Eudicotyledonous plants aids in comparative
functional studies and comparative genomics, and has the potential
to greatly facilitate studies on genome and gene family evolution in
eudicots.
435
ANRV310-PP58-19 ARI 22 March 2007 17:25
Contents
INTRODUCTION: WHY DO WE
NEED A TREE MODEL
SYSTEM? . . . . . . . . . . . . . . . . . . . . . . .
WHAT TOOLS DO WE HAVE
TO STUDY POPULUS
BIOLOGY? . . . . . . . . . . . . . . . . . . . . . .
DNA Sequence and Physical
Map . . . . . . . . . . . . . . . . . . . . . . . . . .
DNA Microarrays, Proteomics,
and Metabolomics . . . . . . . . . . . . .
Annu. Rev. Plant Biol. 2007.58:435-458. Downloaded from arjournals.annualreviews.org
Genetic Tools and
by Swedish University of Agricultural Sciences on 09/03/07. For personal use only.
Transformation. . . . . . . . . . . . . . . .
WHAT CAN WE DO WITH A
SECOND DICOT GENOME
SEQUENCE? . . . . . . . . . . . . . . . . . . .
WHAT CAN WE STUDY BETTER
IN POPULUS THAN IN
ARABIDOPSIS? . . . . . . . . . . . . . . . . . .
Wood Development . . . . . . . . . . . . . .
Seasonality/Phenology . . . . . . . . . . . .
Flowering . . . . . . . . . . . . . . . . . . . . . . . .
Interactions with Other
Organisms . . . . . . . . . . . . . . . . . . . .
Natural Variation . . . . . . . . . . . . . . . . .
FOR THE FUTURE . . . . . . . . . . . . . . .
INTRODUCTION: WHY DO WE
NEED A TREE MODEL SYSTEM?
During the last two decades, researchers have
been astonished to see the very high level
of conservation of biological function in all
living organisms. For example, a long list of
genes known to cause human heritable dis-
eases have very close homologs in the genome
of Arabidopsis thaliana (3). Nevertheless, the
striking differences in appearance and phys-
iology of different species show that a sin-
gle model system cannot be used to answer
all biological questions. In plants, Arabidopsis
has been adopted as the prime model system
and an impressive number of tools and tech-
niques are now available to understand gene
function in this plant. Arabidopsis was chosen
436 Jansson · Douglas
as a model species for obvious reasons: small
physical size, rapid generation time, straight-
forward genetics, high fecundity, and small
genome size. However, Arabidopsis is, in many
respects, an unusual plant. As an almost ob-
436
ligate inbreeder, heterozygosity has been re-
duced to a minimum. Although this greatly fa-
cilitates functional studies, most plant species
438
have different reproductive strategies, mak-
ing Arabidopsis a genetic extreme. The very
438
accelerated life cycle of Arabidopsis also makes
many traits that are essential in many (or most)
439
plants unimportant in Arabidopsis. Two obvi-
ous examples are wood formation and season-
439
ality of growth.
Physiologically and genetically, in many
respects trees represent an opposite extreme
440
to Arabidopsis in the spectrum of land plants,
with long life spans and generation times,
and woody perennial growth habits. How-
441
ever, trees do not form a monophylogenetic
441
group but are found among many higher plant
445
genera and families, and have arisen multi-
447
ple times during land plant evolution. Populus
is found in the angiosperm Euroside I clade
448
together with Arabidopsis. Thus, Arabidopsis is
449
more related to Populus than to the vast ma-
450
jority of other dicot taxa including those with
trees, not to mention monocots like rice or
gymnosperm trees such as conifers, lineages
that separated from the eudicots long before
the radiation of eudicot families 100–120 mil-
lion years ago (mya) (Figure 1). Thus, Populus,
although relatively closely related to Arabidop-
sis, offers a new model system to study an ex-
panded repertoire of biological processes that
better represent the breadth of plant biology.
The development of Populus as a model
system for tree and woody perennial plant bi-
ology has been largely driven by the rapid
development of genomic and molecular bi-
ology resources for this genus, as discussed
below, culminating in the completion of a
draft sequence of the Populus trichocarpa (black
cottonwood) genome (106). This informa-
tion will facilitate studies on the compar-
ative biology of Arabidopsis and Populus as
representatives of two angiosperm extremes,
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Figure 1
Angiosperm phylogeny showing the Eurosid clade containing Populus and Arabidopsis, relative to other
species with significant sequence information (highlighted in color). Data and images from P.F. Stevens,
Angiosperm Phylogeny Web site: http://www.mobot.org/MOBOT/research/APweb/ (Version 7,
May 2006)

www.annualreviews.org • Populus 437

ANRV310-PP58-19 ARI 22 March 2007 17:25
enabling discovery of mechanisms conserved
among eudicots. Perhaps even more im-
portantly, such studies should reveal how
Leaf senescence:
the yellowing of different lineages, subject to different se-
leaves; occurs in the lection pressures, have used common cel-
autumn in trees lular machinery in different ways. This
Whole-genome is illustrated by recent studies on the
shotgun CONSTANS(CO)/FLOWERING LOCUS
sequencing: T (FT) regulatory module. In Arabidop-
random sequencing
sis, this pathway regulates the photoperiod-
of genomic libraries
at high redundancy dependent induction of flowering (55). In Pop-
followed by ulus, however, this module regulates not only
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computer-aided flowering but also bud set in the late season
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sequence contig (9), a process absent in Arabidopsis. Obviously,
assembly
in the Populus lineage, the signal provided by
BAC: bacterial the photoperiod-dependent oscillations of CO
artificial
and FT mRNAs has been co-opted to reg-
chromosome
ulate two different developmental pathways,
whereas Arabidopsis only uses one of these.
This example illustrates the power of com-
parative biology to provide important insights
into the evolution of signal transduction path-
ways, insights that would be less obvious given
a single model. These kinds of studies can
be used to better understand the marvelous
phenotypic and functional diversification of
higher plants. They also shed light on the evo-
lution of traits that has enabled plants to col-
onize most terrestrial ecosystems, making the
existence of heterotrophic organisms like hu-
mans not only possible but also beautiful.
WHAT TOOLS DO WE HAVE TO
STUDY POPULUS BIOLOGY?
DNA Sequence and Physical Map
The major sets of tools and resources that have
propelled Populus into the set of model plants
are the genomics resources. The first set of ex-
pressed sequence tags (ESTs), 5692 sequences
from libraries made from wood-forming tis-
sues, was published in 1998 (97). Since then,
numerous groups have contributed to EST
sequencing efforts, using multiple species
or hybrids, organs, tissues, and treatments,
with 376,565 Populus sequences in the Na-
tional Center for Biotechnology Information
438 Jansson · Douglas
(NCBI) EST database as of August 2006.
These ESTs represent sequences not only
from an expanded effort to capture expressed
genes in wood-forming tissues (20, 82, 96),
but also includes sequences from, for exam-
ple, abiotic stress treatments (11, 69), plants
and cell cultures subjected to biotic stresses
such as herbivory, elicitor treatment, and sys-
temic wounding (17, 82), and leaves under-
going autumnal leaf senescence (6). From an
analysis of 102,019 ESTs, Sterky et al. (96)
identified 24,644 unique sequences, conclud-
ing that the high degree of similarity between
Arabidopsis and Populus genes would facilitate
comparative genomics approaches. Further-
more, these ESTs, as well as those provided
by other investigators and a set of over 4000
full-length cDNA sequences (106) greatly fa-
cilitated annotation of the genome, and pro-
vide relative expression data (“digital north-
ern”) for a large subset of Populus genes (96).
For sequencing of the genome, a P.
trichocarpa female individual (“Nisqually-1”),
previously used in breeding programs, was
chosen (106). The strategy employed whole-
genome shotgun sequencing of small insert
libraries, generating 4.2 × 109 high-quality
(Phred > 20) nucleotides, or a depth of
coverage of approximately 8.5 X of the
480 Mb Populus genome (106). In parallel,
a physical map derived from a 50,000-clone
Nisqually-1 bacterial artificial chromosome
(BAC) library was constructed by restric-
tion enzyme fragment fingerprinting (51a)
(http://www.bcgsc.ca/platform/mapping/
data). Including paired-end reads [BAC end
sequences (BES)] in the data set aided
large-scale assembly of the genome into
2447 major scaffolds (410 Mb), and in-
tegration of the physical map with the
genome sequence. Finally, polymorphic
microsatellite genetic markers anchored
335 Mb of genome sequence to the 19
Populus linkage groups. Annotation of the
genome assembly was carried out using a
diversity of ab initio gene calling programs,
aided by Populus EST and full-length cDNA
sequences, and the Arabidopsis genome
ANRV310-PP58-19 ARI 22 March 2007 17:25
sequence, together with manual annotation
for selected gene families, yielding 45,555
promoted gene models (http://genome.
jgi-psf.org/Poptr1 1/Poptr1 1.home.html),
the largest for any completely sequenced
plant genome to date.
DNA Microarrays, Proteomics, and
Metabolomics
Functional genomics tools such as DNA
microarrays have been developed in parallel
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with EST and genome sequencing. These
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include a 25,000-element cDNA array devel-
oped in Sweden (http://www.populus.db.
umu.se/project.html), a 27,000-element
PICME cDNA array developed in France
and available for purchase (http://www.
picme.at/), and a 15,400-element Treenomix
cDNA array developed in Canada (82).
In addition, subsequent to release of the
Populus genome sequence, Populus short
oligomer-based full-genome arrays or array
probes have been or are being commercially
developed by Affymetix, Inc., NimbleGen,
Inc., and Operon, Inc. A publicly accessible
database containing Populus DNA microar-
ray data was recently opened (93; http://
www.upscbase.db.umu.se).
Generation of proteomic data is in its in-
fancy in Populus, but annotation of 45,555
gene models from the genome sequence
should add efficiency of in silico protein pre-
dictions from mass spectrometry data. Du
et al. (25) generated a data set of 244 pro-
teins that accumulate during P. tomentosa
wood formation, Renaut et al. (83) used pro-
teomics to identify proteins associated with
cold acclimation in the stem, and Plomion
et al. (78a) cataloged more than 300 pro-
teins expressed in different tissues and in re-
sponse to drought, largely by LC-MS/MS
of spots excised from two-dimensional pro-
tein gels. Similarly, although the complex bio-
chemistry of Populus provides interesting op-
portunities for comparing biochemical phe-
notypes with genotype, environment, and
development, published metabolomic stud-
ies are few. However, Andersson-Gunnerås
et al. (2) monitored global changes in
metabolites—by gas chromatography/time-
QTL: quantitative
of-flight mass spectrometry—and transcript trait locus/loci
abundance during tension wood formation,
allowing models for reprogramming of carbo-
hydrate metabolism to be developed. Morreel
et al. (67) used a genetical metabolomics
approach to identify quantitative trait loci
(QTL) that control flux into the complex
set of flavonoids in a Populus pedigree. This
work illustrates the potential for profiling
natural variation in chemical defense com-
pounds to identify regulatory loci. Finally,
metabolic profiling of transgenic Populus lines
altered in lignin composition revealed unex-
pected changes in carbohydrates and other
metabolites relative to wild-type lines (84),
demonstrating the potential for metabolic
profiling to reveal biochemical phenotypes
and discriminate between closely related
individuals.
Genetic Tools and Transformation
Genetic resources have been developed in
Populus over decades, both in the way of F1 and
F2 populations, often derived from interspe-
cific crosses and backcrosses, and collections
of genetically diverse wild genotypes. Exam-
ples include family 331, a three-generation
pedigree derived from a P. trichocarpa female
parent and a P. deltoides male parent (28), and
F1 family 545 (99), derived from a cross be-
tween P. trichocarpa Nisqually-1 (clone 383–
2499) and a P. deltoides male parent. These
and other similar populations have allowed
genetic analysis of Mendelian and quantita-
tive trait loci.
Genetic transformation, along with the
ability to perform reverse genetic analy-
ses, is key to functional studies. Certain,
but not all, Populus genotypes can be sub-
ject to Agrobacterium-mediated transforma-
tion and overexpression or RNAi-mediated
downregulation of target genes, as reviewed
by Busov et al. (14). Naylor et al. (70)
recently demonstrated that viral-induced
www.annualreviews.org • Populus 439
ANRV310-PP58-19 ARI 22 March 2007 17:25
gene silencing (VIGS) might be possible in
Populus using PopMV as a vector. Despite lo-
gistical challenges in working with transgenic
Salicoid
duplication: a trees that require large amounts of green-
whole genome house or field space, activation tagging ap-
duplication event proaches have been successfully employed in
that occurred near Populus (15) for gene identification based on
the emergence of
mutant phenotype, and generation of inser-
Salix and Populus
lineages 60–65 mya tionally mutagenized populations hold great
promise in the future (14).
MAPK:
mitogen-activated
protein kinase
WHAT CAN WE DO WITH A
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SECOND DICOT GENOME
SEQUENCE?
The availability of a second eudicot genome
sequence has the potential to modify the
Arabidopsis-centric view of plant biology. Ge-
nomic studies in Populus can give insights into
plant genome evolution, gene family struc-
ture, and certain important biological pro-
cesses poorly developed in Arabidopsis. Some
of these processes are discussed below. In
terms of genome evolution, analysis of both
ESTs (95) and the whole genome sequence
(106) has revealed a rather recent whole
genome duplication (salicoid duplication) that
appears to have coincided with the emergence
of the Populus and Salix genera. Most in-
terestingly, the rate of gene evolution seems
to be much slower in Populus than in Ara-
bidopsis, since the molecular clock places the
time of gene duplication at 8–13 mya, in
conflict with fossil evidence for Populus 60–
65 mya (106). The greatly decelerated molec-
ular clock in Populus is perhaps a consequence
of its long generation time and contribution
of “ancient gametes” from long-lived Populus
genotypes that can clonally propagate (106),
and suggests that Populus genome reorgani-
zation following the whole genome duplica-
tion is a dynamic process that is still con-
tinuing. Gene loss after the salicoid genome
duplication has been smaller than gene loss
following a previous whole genome duplica-
tion shared by Arabidopsis and Populus, so a
single-copy gene in Arabidopsis is typically rep-
resented by two copies in Populus. Most seg-
440 Jansson · Douglas
ments of the Populus genome mapped to 1 of
19 linkage groups have a paralagous segment
located on one or more other linkage groups,
highlighting the highly duplicated nature of
the genome (Figure 2). However, some gene
families like F-box proteins have been much
more expanded in Arabidopsis relative to Pop-
ulus, and gene family expansions by tandem
duplication may be less common than in
Arabidopsis (106).
By examining differences in gene family
structure between Arabidopsis and Populus,
eudicot gene family evolution and its con-
sequences for plant function can now be
investigated in more detail. Differences in
retention and loss of duplicated gene family
members in the two species will help to
reveal genes important in common eudicot
functions, as well as genes that may have
specialized roles in the two lineages, studies
that would be impossible without a second
genome to compare to the Arabidopsis refer-
ence genome. “Classical” gene families like
those encoding expansins (89), MADS-box
(58), Lhc (CAB) proteins (53), and mitogen-
activated protein kinases (MAPKs) (36)
have been reanalyzed incorporating genome
data, and large and complex families like
carbohydrate-active enzymes (CAZymes)
have been attacked (29). Not surprisingly,
newly arisen gene duplicates may have
different evolutionary rates (102). Many
duplicate genes in the Populus genome have
undergone subfunctionalization in expres-
sion, rationalizing their retention (106), and
promotor sequences have been analyzed by
phylogenetic footprinting to yield informa-
tion about redundancy/neofunctionalization/
subfunctionalization (19). The Populus
genome has also enabled comparative anal-
ysis of less well-studied elements such as
microRNAs (miRNAs) and their potential
targets at the whole genome level. Although
the number of miRNA families is conserved
in Populus and Arabidopsis, the number of
miRNAs and miRNA targets is almost
twofold higher in Populus (106), and it has
been suggested that one function of an
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Figure 2
The 19 linkage groups (LGs) of Populus trichocarpa. Regions connected by colored bands are homologous
and retained since the salicoid genome duplication. Genes on LG annotated as those with high ( green)
and low (red ) expressed sequence tag (EST) support. Three LG pairs have been retained almost intact
after the duplication; LG VI is a fusion between LG XVI and XVIII. The remaining 10 LGs have
undergone more extensive, and complex, reorganization, as described by Tuskan et al. (106).

expanded miRNA repertoire in Populus is els are less well suited. Below, we summarize
related to wood development (60). five such general areas of investigation.

WHAT CAN WE STUDY BETTER Wood Development

IN POPULUS THAN IN
ARABIDOPSIS?
Although annuals have been essential in un-
derstanding plant development, responses to
biotic and abiotic stimuli, and trait evolution,
the biology of Populus provides an opportunity
to study processes for which herbaceous mod-
One defining characteristic of vascular land
Secondary growth
plants is the ability to undergo secondary and cambium:
growth. The evolution of the secondary radial growth
growth habit in the eudicots, and aspects brought about by the
of the regulation of vascular cambium and vascular cambium, a
cylindrical meristem
secondary xylem formation, was recently re-
in stems
viewed by Groover (34). It is clear that

www.annualreviews.org • Populus 441

ANRV310-PP58-19 ARI 22 March 2007 17:25
secondary growth has evolved multiple inde-
pendent times in eudicot lineages, and even
Arabidopsis can be induced to undergo sec-
Complementary
DNA ondary growth in certain conditions (16). Al-
(cDNA)-AFLP: though this strongly suggests conservation of
amplified fragment at least some key gene functions, secondary
length growth and the seasonal regulation of vascu-
polymorphism
lar cambium activity and wood formation are
GA: gibberellic acid still defining characteristics of the life history
of trees. Populus has provided excellent ma-
terial for experiments on xylem development
and functioning of the vascular cambium (re-
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viewed in 64) and exciting new experimental
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avenues are now available.
Formation and functioning of the vas-
cular cambium. The transition from pri-
mary to secondary growth takes place near
the shoot apex; secondary growth is evident
within the first three internodes of the upper-
most internode that can be isolated. Prassinos
et al. (80) identified 271 differentially reg-
ulated transcript-derived fragments (TDFs)
and corresponding genes by complementary
DNA-amplified fragment length polymor-
phism (cDNA-AFLP), many of which were
differentially regulated in the transition to
secondary growth, and van Raemdonck et al.
(107) identified a similar number. Unsurpris-
ingly, genes involved in secondary wall forma-
tion and lignin biosynthesis were prominent
in both sets, but several intriguing transcrip-
tion factors and other potential signaling in-
termediates were associated with transition to
secondary growth. Among these candidates,
PtaRHE1 has an apparent cell-type-specific
expression pattern in ray cell initials of the
developing vascular cambium (107).
Once the vascular cambium is established,
it can remain active for decades or centuries,
and is likely to be governed by internal regu-
latory circuitry that may be analogous to that
in apical meristems (34). A key breakthrough
in the field was microarray-based expression
profiling over the course of wood develop-
ment after isolation of cells at specific devel-
opmental stages by tangential cryo-sectioning
(40). Although other techniques for isolation
442 Jansson · Douglas
of cells at discrete stages of wood develop-
ment, such as staged sampling following re-
activation of the cambium in the spring (42)
and laser capture microdissection (71), also
hold promise, this approach gave the first
glimpse into global expression patterns that
accompany wood development, revealing, for
example, the coordinated expression of puta-
tive cyclin genes involved in cell cycle con-
trol in the zone of cell division within the
vascular cambium. Capitalizing on rapid ad-
vances in the development of microarray re-
sources, Schrader et al. (91) used a much
larger cDNA microarray and refined sampling
strategies to probe patterns of gene expression
at higher resolution, specifically in the cam-
bial zone. Of particular note is the evidence,
based on coordinated patterns of gene expres-
sion, of distinct subdomains within the 60-μm
cambial zone, including phloem mother cells,
cambial stem cells, and xylem mother cells.
From a functional point of view, analysis of
gene expression patterns at this resolution re-
vealed spatially distinct expression patterns of
homologs encoding known regulators of the
apical meristem function, such as receptor-
like kinases of the CLAVATA class (PttCLV1
and PttRLK3), and regulatory transcription
factors (WUS, ANT) (Figure 3). Based on
the opposing expression patterns of PttCLV1
(phloem side) and PttRLK3 (xylem side), an at-
tractive hypothesis is that regulatory circuits
controlled by these receptors independently
control the formation of secondary xylem and
phloem, allowing for flexibility in the rela-
tive amounts of these tissues formed in ac-
cordance with environment and seasonality
(91) (Figure 3). Based on their expression
patterns, WUS-like PttHB3 and PttANT may
also be part of feedback regulatory circuits
controlling cell proliferation at the vascular
cambium.
Secondary xylem development. Of partic-
ular interest in wood formation is the regula-
tion of fiber cell length, a trait of commercial
interest in papermaking. Eriksson et al. (26)
showed that gibberellins (GAs) play a key role
ANRV310-PP58-19 ARI 22 March 2007 17:25
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Figure 3
Model for control of xylem and phloem differentiation and cell proliferation at the Populus vascular
cambium, based on global gene expression profiling across the vascular cambium. Data taken and images
modified from Schrader et al. (91), copyright American Society of Plant Biologists. (a) Tangential
cyro-sectioning strategy across the cambial zone (shown in gray), showing tissue used for RNA isolation.
(b) Microarray expression profiles (in relative units) for selected receptor-like kinase (RLK) and
transcription factor genes. Expression patterns suggest antagonistic action of RLKs PttCLV1 and
PttRLK3 in phloem and xylem differentiation, and possible roles for Populus WUS-like and
AINTEGUMANTA-like transcription factors in cell proliferation at the cambium, and a Populus
AtHB-8-like transcription factor in secondary xylem differentiation.

in this process by overexpressing an Arabidop-
sis GA20 oxidase gene in transgenic hybrid as-
pen; 20-fold higher levels of bioactive GA1
and GA4 gave significantly enhanced height
growth and xylem fiber length. Endogenous
GA1 and GA4 levels peak sharply in the zone
of xylem cell expansion and elongation im-
mediately adjacent to the vascular cambium
(45, 46). This supports a model whereby GA1
and GA4 are key regulators of cell expan-
sion and elongation during secondary xylem
formation. Consistent with a model of GA-
controlled cell expansion and elongation, a
set of genes showing highest expression in the
zone of cell expansion was selectively upreg-
ulated in the GA1 /GA4 -enhanced trees rel-
ative to wild-type trees (45). This suggests
the existence of regulons involved in the con-
trol of cell expansion that are directly or indi-
rectly controlled by GA levels. Targets of such

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ANRV310-PP58-19 ARI 22 March 2007 17:25
regulons might include proteins such as ex-
pansins, which are important in cell wall loos-
ening. For example, a specific ∂-expansin gene
CesA: cellulose
synthase A subunit family member (PttEXP1) is expressed in the
cell expansion zone of secondary xylem and
Secondary cell wall:
formed outside the may be involved in intrusive growth of xylem
primary wall in fibers (33).
specialized cells; rich Secondary wall formation is a hugely im-
in lignin, cellulose, portant process in forest ecosystems, because
and hemicellulose
the bulk of the biomass of trees is cellulose and
AGP: encrusting lignin in secondary walls. It is now
arabinogalactan
possible to catalog the complete sets of genes
protein
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encoding lignin biosynthetic enzymes and cel-
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PCD: programmed
lulose synthase (CesA) subunits, revealing the
cell death
biosynthetic “toolboxes” for these processes.
The Populus lignin biosynthetic toolbox (106)
is roughly twice as big as that of Arabidop-
sis, and the higher number of genes encod-
ing key cytochrome P450-mediated enzymes
required for hydroxylation of the phenyl-
propanoid phenolic ring at the 4 , 3 , and 5
positions suggests a greater need for main-
taining flux into monolignol biosynthesis dur-
ing the massive commitment to secondary
wall biosynthesis. Alternatively, it could
reflect evolutionary pressure for subfunc-
tionalization, as apparent for duplicated
cinnamate-4-hydroxylase (C4H) genes (61).
Populus contains 18 apparent CesA genes (22),
relative to the 10 known in Arabidopsis. Five
of these genes are homologs of genes encod-
ing Arabidopsis CesA4, CesA7, and CesA8 sub-
units, which are dedicated to cellulose biosyn-
thesis in secondary walls (103). Expression
data support specific roles for Populus CesA
proteins in secondary wall biosynthesis dur-
ing wood formation (for example, 50), and
recent work suggests that dedication of spe-
cific CesA subunits to cellulose biosynthesis
in secondary cell walls occurred well before
divergence of angiosperms and gymnosperms
(68).
More functional information is available
for lignin biosynthesis, reviewed recently by
Boerjan et al. (8) and Li et al. (59). Cat-
alyzed in part by the importance of Populus
as a commercial plantation species, multiple
transgenic lines with modified lignin charac-
444 Jansson · Douglas
teristics have been generated by misexpres-
sion of lignin biosynthetic genes. A thorough
study of the pulping characteristics of wood
from field-tested lines showed the potential
to generate modified lignin trees with supe-
rior wood quality (78).
Functioning and regulation of the CesA
rosette complex in the plasma membrane
require numerous other proteins such as
COBRA, KORRIGAN, and sucrose synthase
(23, 88), and coexpression analyses in Ara-
bidopsis have highlighted potentially impor-
tant players such as COBRA-like 4 (COBL4),
germin-like, chitinase-like 2 (CTL2), and
fasciclin-like arabinogalactan (AGP) proteins
in cellulose secretion during secondary wall
formation (for example, 12). Homologs of
these genes are present in Populus (49, 106)
and are often coregulated with genes encod-
ing secondary wall-specific CesA genes (40).
Several studies have also highlighted the po-
tentially important role of fasciclin-like AGPs
in secondary wall formation (for example, 77).
The final step in wood development
and tracheary element differentiation, pro-
grammed cell death (PCD), has mainly been
investigated in Zinnia, but PCD in the context
of wood formation can been studied in Popu-
lus. Moreau et al. (66) isolated populations of
cells enriched for those undergoing PCD and
those still undergoing secondary wall forma-
tion, and used EST analysis and cDNA mi-
croarray expression profiling to identify novel
proteases, and potential regulatory proteins
and mechanisms involved in PCD, opening
the door to further functional studies.
The mechanisms regulating secondary
xylem formation are not yet clear. Key tran-
scriptional regulators of meristem and vas-
cular differentiation known or inferred from
Arabidopsis studies include KNOTTED-like
homeodomain proteins such as SHOOT-
MERISTEMLESS and BREVIPEDICEL-
LUS and class III HD-ZIP proteins such as
AtHB-8 and REVOLUTA (34), as well as
MYB proteins (85). Homologs of genes en-
coding these proteins are found in the Pop-
ulus genome and expression of some, such
ANRV310-PP58-19 ARI 22 March 2007 17:25
as class III HD-ZIP (54), KNOX (34a), and
MYB genes (51), are correlated with sec-
ondary xylem formation in Populus. Using the
15.4K Treenomix cDNA Populus microarray
(82), we identified a set of KNOTTED-like
and MYB transcription factors common to
Populus and Arabidopsis whose expression is
highly correlated secondary wall formation in
both species and in some cases with spruce
(M. Friedman, L. Johnson, E. Li, M. Ellis &
C. Douglas, unpublished). Interestingly, as in
Arabidopsis, there is evidence of miRNA reg-
Annu. Rev. Plant Biol. 2007.58:435-458. Downloaded from arjournals.annualreviews.org
ulation of Populus HD-ZIP proteins (54), and
by Swedish University of Agricultural Sciences on 09/03/07. For personal use only.
novel Populus miRNAs downregulated dur-
ing wood formation may play additional im-
portant regulatory roles in this process (60).
This and other data strongly suggest that
subtle changes in regulatory networks com-
Figure 4
The annual cycle of a Populus tree growing at Umeå University, Umeå, Sweden.
mon to herbaceous plants and trees, rather
than entirely new pathways, are responsible
for the elaboration of the wood-forming habit
of trees. Functional approaches performed in
parallel in Populus and Arabidopsis now have
the potential to unravel differential use of
common regulatory networks.
Seasonality/Phenology
Trees in temperate climates must not only be
able to adapt to the seasonal changes that re-
strict their growth, but they must also be able
to withstand often severe winter conditions.
As a typical deciduous tree, the yearly activ-
ity of a Populus tree in a climate of alternat-
ing summer and winter seasons is depicted in
Figure 4.
www.annualreviews.org • Populus 445
ANRV310-PP58-19
Annu. Rev. Plant Biol. 2007.58:435-458. Downloaded from arjournals.annualreviews.org
by Swedish University of Agricultural Sciences on 09/03/07. For personal use only.
ARI 22 March 2007 17:25
The ability to anticipate harsh winter con-
ditions is a highly adaptive trait, and the
shorter days in autumn are the most important
input signal. Photoreceptors detect shorten-
ing photoperiods, and both phytochrome A
and at least one of the two Populus phy-
tochrome B genes ( phyB2) have roles in this
process (73). As a first event in the preparation
for winter, trees cease growth and set dormant
buds. Time of bud set is easy to score pheno-
typically, is under very strong genetic control,
and has been a model trait studied from the
perspective of natural variation within Populus
species and pedigrees (for example, 28). Chill-
ing temperatures do not seem not to influ-
ence timing of bud set, but trees that have not
set buds when the temperature drops below
zero will stop growing and rapidly set buds (V.
Luquez, D. Hall, B. Albrectsen, J. Karlsson,
P. Ingvarsson, S. Jansson, submitted). Recent
studies have shown that bud set is under con-
trol of the CO/FT regulatory module in Popu-
lus. Expression of the Populus CO gene is sub-
ject to strong diurnal regulation, peaking in
the evening, and if CO mRNA accumulates
before dawn, it activates the FT regulatory
protein, which represses bud set. As days get
shorter, the CO protein may only accumulate
after dawn and is not able to induce the re-
pressor FT, and bud set occurs (9).
Later in the autumn, leaf senescence starts
and chlorophyll and the vast majority of the
leaf proteins are degraded. Again, day length
seems to be the main trigger in Populus. Not
all trees start senescence according to the cal-
endar but an aspen that has been studied in
detail over many years always starts chloro-
phyll degradation around September 11 in
northern Sweden (52). Leaf senescence has
been studied in many systems, but the autumn
leaf provides at attractive model; the process
seems to be similar to leaf senescence in an-
nual plants, but it is triggered in a different
way. Key cellular and transcriptional events
in autumn senescence in Populus have been
described (52). Autumn senescence has clear
adaptive value, because remobilization of ni-
trogen, in particular, is important in forest
446 Jansson · Douglas
ecosystems where nitrogen is often a limit-
ing factor for plant growth. However, perhaps
even more important are dormancy and as-
sociated cold hardiness that develop in over-
wintering aboveground parts. Using microar-
ray expression profiling of wood-forming
tissues, Schrader et al. (90) identified marker
genes for cambial dormancy. Endodormancy
refers to an initial stage in the development
of full dormancy in which presentation of fa-
vorable conditions does not result in resump-
tion of growth. Studies in Populus have shown
that once endodormancy has been induced by
short day length, extended periods of chilling
temperatures are needed to condition trees
to break dormancy (86) and put the tree in a
“standby” position, waiting for spring condi-
tions that are permissive for growth. The tools
now available in Populus make it an excellent
system to study the regulatory circuitry under-
lying these events, which likely involves ab-
scisic acid and a signaling pathway including
PtABI3, a Populus ortholog of the Arabidopsis
ABI3 gene (87).
In the buds formed in the autumn, leaf de-
velopment is arrested at an early stage. Tim-
ing of bud flush in the spring is under genetic
control; when dormancy is broken, a tree of a
given genotype has a requirement for a certain
temperature sum for bud flush. Considerable
variation in timing of bud flush often (27) ex-
ists between populations from different lati-
tudes. In a full-grown tree, at bud flush in the
spring, all leaves develop in parallel so that
at a given date, all leaves of the tree are of
the same age. Gene expression studies have
shown that the environmental influence on
gene expression during onset of leaf develop-
ment in the spring can largely be separated
from developmental and leaf-age-dependent
influences (110) in Populus, studies that would
not be possible in annuals. Gene expression in
leaves up to one month after bud flush seems
to be mainly determined by a developmen-
tal program, but later in the summer envi-
ronmental factors are much more important,
making Populus leaves an attractive system
to study environmental influences on gene
ANRV310-PP58-19 ARI 22 March 2007 17:25
expression (A. Sjödin, K. Wissel & S. Jansson,
unpublished).
Flowering
Many trees such as Populus have extended ju-
venile phases of several years before reproduc-
tive maturity and flowering (reviewed in 13).
Thus, studies of flowering time in Populus add
another dimension to the picture of regula-
tion flowering in angiosperms that could not
be obtained in annuals alone. As in annuals,
Annu. Rev. Plant Biol. 2007.58:435-458. Downloaded from arjournals.annualreviews.org
trees are under selective pressure to coordi-
by Swedish University of Agricultural Sciences on 09/03/07. For personal use only.
nate timing of annual flowering with other
trees of the same species to maximize repro-
ductive outcome. However, the juvenility to
maturity transition can be better studied in a
tree such as Populus, which lies at an extreme
relative to herbaceous weedy plants such as
Arabidopsis. It is possible that the herbaceous
growth habit is a derived state in evolution
(94), so herbs can be considered mutant trees
that flower during their first year of growth,
making typical traits found in trees, such as
woodiness, unnecessary.
Populus species flower early in the season,
often before bud burst. The overwintering
buds are either vegetative or reproductive so
the decision if, or how much, to flower next
year is taken in the summer, before bud set.
The FT gene is a regulator of FT originally
identified in Arabidopsis (55). Unlike Arabidop-
sis, Populus contains two FT genes (FT1 and
FT2; 91% amino acid identity) (41). Remark-
ably, transgenic Populus trees where ectopic
FT1 expression is driven by a constitutive pro-
moter can flower in tissue culture six weeks
after transformation (Figure 5) (9), and those
ectopically expressing FT2 flower within one
year (41). In wild-type trees, FT expression in-
creases as trees get older or reach reproductive
maturity (9, 41); therefore, FT is also a reg-
ulator of maturity. In Arabidopsis, chromatin
structure is altered by the EARLY BOLTING
IN SHORT DAYS (EBS) gene, making FT
susceptible to activation by CO, and by anal-
ogy it has been hypothesized that a grad-
ual modification of chromatin structure as a
Populus individual gets older could eventually
make FT accessible for activation by CO (9).
In contrast to the single flowers induced by
overexpression of the meristem identity gene
LEAFY (109), FT overexpressors form catkins
that look very similar to those found in wild-
type plants (9, 41).
In contrast to hermaphroditic plants such
as Arabidopsis with perfect flowers, Popu-
lus species are dioeceous and produce male
and female flowers on different individuals.
Gender is genetically determined, although
hermaphroditic flowers have been reported
in many Populus species, especially on fe-
male trees (for example, 98). New opportuni-
ties to understand the molecular mechanisms
underlying sex determination in plants have
therefore been opened up with the genome
sequence of a dioeceous plant. For exam-
ple, it may be possible to identify gender-
specific markers, as those found in Salix
(1), and gene expression profiling could re-
veal gender-biased gene expression pointing
to sex-determining loci. Several other unre-
solved matters remain regarding the control
of flowering in trees such as Populus, includ-
ing the competence of a meristem to alternate
between vegetative and reproductive growth,
and the mode of action of environmental fac-
tors such as light and temperature, that de-
termine to what extent a tree will flower the
following year.
Figure 5
Populus in tissue culture flowering six weeks after transformation with the
FLOWERING LOCUS T1 (FT1) gene. This illustrates the conservation of
flowing time regulation in annuals such as Arabidopsis and trees such as
Populus, as well as how generation times of tress can be drastically reduced
allowing for efficient tree breeding. Copyright Science, redrawn from
Reference 9.
www.annualreviews.org • Populus 447
ANRV310-PP58-19 ARI 22 March 2007 17:25

Interactions with Other Organisms of MAPKs (35). However, a diversification of

R-gene-based pathogen surveillance mecha-
Phytochemistry and chemical ecology.
nisms appears to have occurred in the Populus
Phenolic glycosides With a life span of decades, Populus faces
(PGs): phenolic lineage relative to Arabidopsis and rice (106),
challenges and opportunities with respect to
molecules with and it will be interesting to determine if this
interactions with other organisms that are
sugars attached by trait is common to perennials.
distinct from those of annual plants. Popu-
O-glycosidic bonds One of the major fungal pathogens
lus must defend itself against herbivores and
LRR: leucine-rich of the Populus species is the fungal rust
pathogens year after year in order to survive.
repeat pathogen Melampsora sp., and studies on
Furthermore, with an extensive root system
the genetics of this interaction go back at
that must maintain efficiency in water and nu-
least two decades (for example, 79). Recent
trient uptake over similar time periods, the se-
studies have revealed Mendelian loci (e.g.,
lective pressure to develop beneficial interac-
Annu. Rev. Plant Biol. 2007.58:435-458. Downloaded from arjournals.annualreviews.org

MXC3 and MER) (99, 111) and QTL for

tions with soil microflora may be greater than
by Swedish University of Agricultural Sciences on 09/03/07. For personal use only.

quantitative and qualitative resistance (48).

for short-lived organisms.
The complexity of Populus chemical ecol-
ogy is likely to greatly exceed that of Arabidop-
sis or domesticated crop plants. An important
part of this repertoire revolves around phe-
nolic metabolism. Phenolic glycosides (such
as salicin), condensed tannins, and other
flavonoids may constitute up to 35% of foliar
dry weight in some Populus species (104), and
the recent annotation of the complete set of
Populus shikimate/phenylpropanoid genes in-
volved in biosynthesis of these (104) lays the
groundwork for further studies in chemical
defense, which have great quantitative varia-
tion (38). Arimura et al. (5) showed that forest
tent caterpillars feeding on Populus leaves (but
not mechanical wounding) induced a diver-
sity of local and systemic volatile terpenoid
emissions, suggesting that terpenoid chemi-
cal diversity in Populus may have a role for po-
tential tri-trophic plant-herbivore-parasitoid
interactions.
Pathogens. The number of Populus nu-
cleotide binding site (NBS) – leucine-rich re-
peat (LRR) R resistance genes (399) is about
double the number in Arabidopsis and appears
to have increased both due to gene retention
following genome duplication and by tandem
gene duplication (106). Pathogen-induced
signaling pathways appear conserved, consis-
tent with reports of rapid transcriptional acti-
vation of phenylpropanoid in Populus by elic-
itor treatment (21), and the activation pattern
Fine mapping of R gene-containing loci com-
bined with BAC physical map and genome
sequence information should make positional
cloning of genetically identified R genes in
Populus feasible (57, 111). Future studies
on these and other host-pathogen systems
in Populus [for example, involving Septoria
(72)] provide fertile ground for biologists
interested in plant-pathogen interactions.
Sequencing of the Melampsora larici-populina
genome by the Joint Genomics Institute
(http://www.jgi.doe.gov/sequencing/why/
CSP2006/poplarrust.html) will greatly
enhance research in this area.
Beneficial interactions. Unlike Arabidop-
sis, associations with beneficial microorgan-
isms are well described in Populus. Popu-
lus is a host for ectomycorrhizal and abus-
cular mycorrhizal fungal symbionts and is
the first species with a complete genome
sequence capable of undergoing such sym-
biotic relationships. With the completion
or impending completion of the genome
sequences of two important Populus mycr-
orrhizal fungi, Laccaria bicolor (ectomycor-
rhizal) and Glomus intraradices (arbuscular my-
corrhizal) (56), interesting possibilities for
investigating the molecular, physiological,
and environmental basis for these interac-
tions are possible. QTLs controlling Populus-
mycorrhizal fungal interactions have been
identified (101), a high-affinity ammonium
transporter (PttAMT1.2) whose expression

448 Jansson · Douglas

ANRV310-PP58-19 ARI 22 March 2007 17:25
correlates with successful ectomycorrhizal
association has been found (92), and infection-
induced aquaporins involved in water trans-
port during ectomycorrhizal associations have
been identified (63).
While still in its infancy, studies on the col-
onization of internal Populus tissues by po-
tentially beneficial bacterial endophytes are
intriguing. More than 50 different fungal en-
dophytes have been isolated from a single Pop-
ulus tree (B. Albrectsen, M. Wedin, S. Jansson,
J. Karlsson, unpublished) and whole genome
Annu. Rev. Plant Biol. 2007.58:435-458. Downloaded from arjournals.annualreviews.org
shotgun sequences, derived from DNA li-
by Swedish University of Agricultural Sciences on 09/03/07. For personal use only.
braries made from surface-sterilized material
included sequences from 22 bacterial genera,
some which had thousands of sequence reads
(106), suggesting that these may represent en-
dophytes rather than contaminating surface
bacteria. Experimental evidence for efficient
bacterial endophyte colonization of Populus
exists (30), and Doty et al. (24) even identi-
fied the nitrogen-fixing bacterium Rhizobium
tropici as an endophyte of Populus.
Herbivory. As an ecologically dominant tree,
Populus is subject to herbivory by a variety
of animals. Although browsing of Populus by
mammals is particularly interesting from a
chemical ecology point of view (32) and of-
fers a system that will not soon be tackled
by Arabidopsis biologists, insect herbivory in
Populus has received the most attention. Phe-
nolic products are likely involved in defend-
ing Populus against insect herbivory. Although
genetically determined variation in phenolic
glycoside levels plays a major role in insect
performance as herbivores on Populus (74),
rapid induction of dihydroflavonol reductase
(DFR) gene expression and condensed tannin
accumulation in response to herbivory sug-
gest that these flavonoid-derived compounds
are also important (76). Potential protein-
based chemical defenses in Populus, such as
expression of genes encoding polyphenol ox-
idase (PPO) and Kunitz trypsin inhibitors,
have been studied at the molecular level (for
example, 39), and overexpression of PPO in
transgenic Populus increased insect mortality
and decreased fitness (108). Microarray stud-
ies have confirmed and extended these find-
ings, and highlighted the importance of oc-
Endophytes: fungi
tadeonoid and ethylene signaling in mediat- and bacteria that live
ing defense responses (82). internally in
association with
Natural Variation plants
Trees typically have higher levels of genetic RAPD:
random-amplified
diversity and lower levels of genetic dif-
polymorphic DNA
ferentiation between populations than other
plants (37). As a wind-pollinated obligate out-
breeder, Populus may have even higher varia-
tion than some other trees. Each year, a fe-
male Populus can produce tens of millions
of seeds that could potentially have thou-
sands of different fathers. Seeds of many Pop-
ulus species have hairs (hence the name cot-
tonwood), and can be dispersed for many
kilometers by the wind (summarized by
G.C. Wyckoff and J.C. Zasada at http://
www.nsl.fs.fed.us/wpsm/Populus.pdf ). A
high level of diversity and heterozygosity was
demonstrated early in Populus using isozyme
and random-amplified polymorphic DNA
(RAPD) markers (for example, 7), but the
genomic tools now available (for example,
31, 43) make it possible to dissect natu-
ral variation in more detail. Sequencing and
physical map construction of the highly het-
erozygous P. trichocarpa Nisqually-1 genotype
reveal extensive haplotype diversity in this sin-
gle individual (2.6 single nucleotide polymor-
phisms or small indels per kilobase) (106),
and haplotype-specific BAC clones from the
Nisqually-1 Populus physical map differ by in-
dels up to 10 kb in size (51a).
Populations of different Populus species
seem to have different levels of nucleotide di-
versity. For example, P. tremula is more vari-
able (on average, nucleotide diversity is 0.01
in genes) (43) than P. trichocarpa (on average,
0.0018) (31). Connecting phenotypic varia-
tion to genotypic variation in Populus using
traditional QTL analysis presents challenges
given its long generation time and the years
required to generate segregating populations,
as well as the logistics of maintaining large
populations in the field. The first QTLs
www.annualreviews.org • Populus 449
ANRV310-PP58-19 ARI 22 March 2007 17:25
identified in Populus, for growth, form, and
bud phenology (10, 28), were mapped in pedi-
grees established 15 to 20 years earlier. Populus
Association
mapping: process of pedigrees have subsequently been used to map
finding a genetic QTLs for numerous other traits, for exam-
marker that ple, osmotic potential (105), drought response
associates with a trait (100), and response to elevated CO2 (81), in
in a large population
addition to the uses mentioned above. Com-
pletion of the genome sequence anchored to
genetic and physical maps, combined with
other genomic tools, will facilitate analysis
of candidate genes underlying such Populus
Annu. Rev. Plant Biol. 2007.58:435-458. Downloaded from arjournals.annualreviews.org
QTLs.
by Swedish University of Agricultural Sciences on 09/03/07. For personal use only.
As an alternative to QTL analysis, as-
sociation mapping shows great promise for
exploiting natural variation to understand
phenotypic diversity. The efficient mixing of
alleles in outbreeding species ensures that
those that give the highest fitness will ac-
cumulate in a population at a given site. In
contrast to inbreeders like Arabidopsis, false
positives resulting from population structure
(4) are therefore less of a problem. How-
ever, the prospect of making genome-wide
scans for association is hampered by the low
linkage disequilibrium (LD). Even in P. tri-
chocarpa, where LD extends longer than in
Figure 6
Number of citations in National Center for Biotechnology Information
(NCBI) Medline containing the term “Populus,” from 1998 to 2006.
∗
Data for 2006 is partial (through November 2006).
450 Jansson · Douglas
P. tremula (31), scoring of close to one mil-
lion evenly distributed markers may be nec-
essary to have a reasonable chance of finding
association to a crucial polymorphism. If can-
didate genes in a QTL region can be analyzed
using association mapping, it should be pos-
sible to relatively rapidly identify SNPs or in-
dels linked to phenotypic variation. By way
of example, this approach has been used to
show that two nonsynonymous SNPs in the
phyB2 gene together explain about 10% of the
variation in critical photoperiod for bud set
(44, P. Ingvarsson and S. Jansson, unpub-
lished).
Dioecy adds another level of complexity to
natural variation in Populus. Selection can act
differently on males and females, leading to
variation between males and females in traits
such as growth rate (reviewed in 65). Thus,
there is potential for linkage of traits to sex-
determining loci not present in most other
plant species. Finally, intriguing questions re-
garding the potential role of epigenetic mech-
anisms in generating additional variation in a
perennial plant species with long generation
times can be addressed in Populus.
FOR THE FUTURE
In addition to the areas we have reviewed
here, there are many others for which Populus
provides a good model system to understand
plant biology. For example, Populus could be
used for studies on long-distance transport
of water and nutrients, studies on systemic
signaling (5, 76), studies on seasonal nitro-
gen cycling and nitrogen storage as part of
the perennial growth habit (18), studies on
adaptation to stressful environments (for ex-
ample, 11), and studies on the impact of pre-
dicted future increased CO2 levels on trees
and forest ecosystems (for example, 81). Com-
parative genomics and comparative functional
studies capitalizing on the similarities and dif-
ferences between Arabidopsis and Populus are
likely to be fruitful for studies on basic plant
processes and the evolution of plant growth
ANRV310-PP58-19 ARI 22 March 2007 17:25

and development. The high levels of natural
variation in wild populations of Populus, and
the almost infinite number of recessive alleles
in these populations, can be capitalized on for
both basic and applied research purposes, po-
tentially contributing toward domestication
of Populus (7) and the understanding of the
evolution of adaptive traits. In addition to its
traditional uses as a species for wood and fiber,
Populus, as a model and plantation tree, offers
opportunities for research into woody plants
as sources of ligno-cellulosic feedstocks for
Annu. Rev. Plant Biol. 2007.58:435-458. Downloaded from arjournals.annualreviews.org
ies, as it has over the past several years. One
measure of the increasing interest in Populus as
a model system is the nearly tenfold increase
in NCBI Medline Populus citations per year
from 1998 (the year of publication of the first
Populus EST data set, marking the beginning
of Populus genomics) (97) to 2006 (the year of
publication of the Populus genome sequence)
(106) (Figure 6). We predict that this num-
ber will continue to increase, catalyzed by the
availability of the Populus genome sequence,
the availability of Populus genomic and molec-

biofuels (for example, 75). For these reasons, ular tools, and the large number of interesting
by Swedish University of Agricultural Sciences on 09/03/07. For personal use only.

Populus will likely be a model system that will biological questions that can be addressed in
grow in importance for basic and applied stud- this plant.

SUMMARY POINTS
1. Sequencing of the Populus genome revealed that its genome has undergone a rather
recent genome duplication/polyploidization (60–65 mya; 8–12 mya by the molecular
clock), which has shaped gene family organization in the genus.
2. A suite of critical genomic and molecular tools (genome sequence, EST collections,
DNA microarrays, transformation protocols, etc.) have been developed for Populus.
3. Populus is a close relative of Arabidopsis, so gene functions are often conserved.
4. Populus provides opportunities to study important plant processes absent or poorly
developed in Arabidopsis, such as wood formation and autumn senescence, as well as
traits like flowering, sex determination, and biotic interactions from a comparative
point of view.
5. Populus exhibits an unusual amount of natural variation that now can be explored with
respect to adaptation, evolution, and biotechnology.

ACKNOWLEDGMENTS
The authors thank numerous members of the Populus research community for their ideas
and contributions to Populus genomics and biology, and apologize for their inability to in-
clude all such work in this review due to space limitations. They would like to particularly
thank Gerald Tuskan for his tireless efforts on behalf of Populus genomics and genetics, for
advice on this review, and for generating Figure 1. Bo Segerman is acknowledged for pro-
viding Figure 2. The authors’ work in Populus is funded by grants from the Knut and Alice
Wallenberg Foundation, the Swedish Foundation for Strategic Research, the Swedish Research
Council, Kempestiftelserna, and the European Commission (contract No. QLK5-CT-2002–
00953 (POPYOMICS) (S.J.), and by Genome Canada and the Province of British Columbia (to
the Treenomix project), and a Natural Sciences and Engineering Research Council of Canada
(NSERC) Discovery Grant (C.J.D.).

www.annualreviews.org • Populus 451

ANRV310-PP58-19 ARI 22 March 2007 17:25

LITERATURE CITED
1. Alstrom-Rapaport C, Lascoux M, Wang YC, Roberts G, Tuskan GA. 1998. Identification
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Annual Review of
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Contents Volume 58, 2007

Frontispiece
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Diter von Wettstein p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p pxii

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From Analysis of Mutants to Genetic Engineering

Diter von Wettstein p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p1
Phototropin Blue-Light Receptors
John M. Christie p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 21
Nutrient Sensing and Signaling: NPKS
Daniel P. Schachtman and Ryoung Shin p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 47
Hydrogenases and Hydrogen Photoproduction in Oxygenic
Photosynthetic Organisms
Maria L. Ghirardi, Matthew C. Posewitz, Pin-Ching Maness, Alexandra Dubini,
Jianping Yu, and Michael Seibert p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 71
Hidden Branches: Developments in Root System Architecture
Karen S. Osmont, Richard Sibout, and Christian S. Hardtke p p p p p p p p p p p p p p p p p p p p p p p p p p 93
Leaf Senescence
Pyung Ok Lim, Hyo Jung Kim, and Hong Gil Nam p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p115
The Biology of Arabinogalactan Proteins
Georg J. Seifert and Keith Roberts p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p137
Stomatal Development
Dominique C. Bergmann and Fred D. Sack p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p163
Gibberellin Receptor and Its Role in Gibberellin Signaling in Plants
Miyako Ueguchi-Tanaka, Masatoshi Nakajima, Ashikari Motoyuki,
and Makoto Matsuoka p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p183
Cyclic Electron Transport Around Photosystem I: Genetic Approaches
Toshiharu Shikanai p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p199
Light Regulation of Stomatal Movement
Ken-ichiro Shimazaki, Michio Doi, Sarah M. Assmann,
and Toshinori Kinoshita p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p219

v
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The Plant Heterotrimeric G-Protein Complex

Brenda R.S. Temple and Alan M. Jones p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p249
Alternative Splicing of Pre-Messenger RNAs in Plants in the
Genomic Era
Anireddy S.N. Reddy p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p267
The Production of Unusual Fatty Acids in Transgenic Plants
Johnathan A. Napier p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p295
Tetrapyrrole Biosynthesis in Higher Plants
Ryouichi Tanaka and Ayumi Tanaka p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p321
Annu. Rev. Plant Biol. 2007.58:435-458. Downloaded from arjournals.annualreviews.org

Plant ATP-Binding Cassette Transporters

by Swedish University of Agricultural Sciences on 09/03/07. For personal use only.

Philip A. Rea p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p347

Genetic and Epigenetic Mechanisms for Gene Expression and
Phenotypic Variation in Plant Polyploids
Z. Jeffrey Chen p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p377
Tracheary Element Differentiation
Simon Turner, Patrick Gallois, and David Brown p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p407
Populus: A Model System for Plant Biology
Stefan Jansson and Carl J. Douglas p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p435
Oxidative Modifications to Cellular Components in Plants
Ian M. Møller, Poul Erik Jensen, and Andreas Hansson p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p459

Indexes

Cumulative Index of Contributing Authors, Volumes 48–58 p p p p p p p p p p p p p p p p p p p p p p p p483

Cumulative Index of Chapter Titles, Volumes 48–58 p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p488

Errata

An online log of corrections to Annual Review of Plant Biology chapters

(if any, 1997 to the present) may be found at http://plant.annualreviews.org/

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