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Photoperiod- and temperature-mediated control of phenology in trees - a molecular perspective

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Contents 'Summary' I. 'Introduction' II. 'Key developmental stages of the annual growth cycle' III. 'Control of growth cessation and bud set by seasonal cues' IV. 'How does photoperiod control developmental transitions?' V. 'The role of temperature in growth cessation and bud set' VI. 'Establishment and release of bud dormancy' VII. 'Natural variation in the regulation of distinct stages of annual growth cycles in trees' VIII. 'Conclusions' Acknowledgements References Trees growing in boreal and temperate regions synchronize their growth with seasonal climatic changes in adaptive responses that are essential for their survival. These trees cease growth before the winter and establish a dormant state during which growth cessation is maintained by repression of responses to growth-promotive signals. Reactivation of growth in the spring follows the release from dormancy promoted by prolonged exposure to low temperature during the winter. The timing of the key events and regulation of the molecular programs associated with the key stages of the annual growth cycle are controlled by two main environmental cues: photoperiod and temperature. Recently, key components mediating photoperiodic control of growth cessation and bud set have been identified, and striking similarities have been observed in signaling pathways controlling growth cessation in trees and floral transition in Arabidopsis. Although less well understood, the regulation of bud dormancy and bud burst may involve cell–cell communication and chromatin remodeling. Here, we discuss current knowledge of the molecular-level regulation of the annual growth cycle of woody trees in temperate and boreal regions, and identify key questions that need to be addressed in the future.
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Tansley review
Photoperiod- and temperature-mediated
control of phenology in trees a molecular
perspective
Author for correspondence:
Rishikesh P. Bhalerao
Tel: +46 0 90 7868488
Email: rishi.bhalerao@slu.se
Received: 16 May 2016
Accepted: 7 October 2016
Rajesh Kumar Singh
1
, Tetiana Svystun
2
, Badr AlDahmash
3
, Anna Maria
Jonsson
2
and Rishikesh P. Bhalerao
1,3
1
Department of Forest Genetics and Plant Physiology, SLU, S-901 83, Umea, Sweden;
2
Department of Physical Geography and
Ecosystem Science, Lund University, Solvegatan 12, S-223 62 Lund, Sweden;
3
College of Science, King Saud University, 11451 Riyadh,
Saudi Arabia
Contents
Summary 1
I. Introduction 1
II. Key developmental stages of annual growth cycle 2
III. Control of growth cessation and bud set by seasonal cues 3
IV. How does photoperiod control developmental
transitions? 3
V. The role of temperature in growth cessation and bud set 7
VI. Establishment and release of bud dormancy 7
VII. Natural variation in the regulation of distinct stages of annual
growth cycles in trees 11
VIII. Conclusions 11
Acknowledgements 11
References 11
New Phytologist (2016)
doi: 10.1111/nph.14346
Key words: correlation analysis, evolution,
phloem, phylogeny, sieve element, sieve plate,
sieve pore, trees.
Summary
Trees growing in boreal and temperate regions synchronize their growth with seasonal climatic
changes in adaptive responses that are essential for their survival. These trees cease growth
before the winter and establish a dormant state during which growth cessation is maintained
by repression of responses to growth-promotive signals. Reactivation of growth in the spring
follows the release from dormancy promoted by prolonged exposure to low temperature
during the winter. The timing of the key events and regulation of the molecular programs
associated with the key stages of the annual growth cycle are controlled by two main
environmental cues: photoperiod and temperature. Recently, key components mediating
photoperiodic control of growth cessation and bud set have been identified, and striking
similarities have been observed in signaling pathways controlling growth cessation in trees and
floral transition in Arabidopsis. Although less well understood, the regulation of bud dormancy
and bud burst may involve cellcell communication and chromatin remodeling. Here, we
discuss current knowledge of the molecular-level regulation of the annual growth cycle of
woody trees in temperate and boreal regions, and identify key questions that need to be
addressed in the future.
I. Introduction
In contrast with annual plants, such as the model plant Arabidopsis
thaliana, perennial plants undergo repeated cycles of vegetative
growth, dormancy and flowering. Consequently, in perennials,
meristems and perennating organs, such as leaf and flower
primordia, are exposed to large seasonal fluctuations in tempera ture
and other environmental factors during post-embryonic growth.
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For example, temperatures in the boreal region may vary from +25
to 50°C during the course of the year. Trees growing in boreal
and temperate regions, the topic of this review, survive such
climatic extremes by synchronizing periods of vegetative growth
and development with periods of permissive conditions using
environmental cues, such as photoperiod and temperature (Nitsch,
1957; Weiser, 1970; Powell, 1987; Cooke et al., 2012). In recent
years, some progress has been made in the elucidation of aspects of
the molecular mechanisms underlying the seasonal control of
growth in trees (Petterle et al., 2013), largely as a result of the
development of molecular tools for the dissection of this
phenomenon in model tree genera, such as Populus spp.(hereafter
poplar) (Ellis et al., 2010), Picea spp. (hereafter spruce) (Cooke
et al., 2012) and Prunus persica (peach) (Jimenez et al., 2010). The
objectives of this review are to summarize our current understand-
ing of the cellular and molecular mechanisms involved in the
seasonal regulation of growth in apices of woody trees in temperate
and boreal regions and to identify key questions that need to be
addressed in the future.
II. Key developmental stages of the annual growth
cycle
Key stages of the annual growth cycle in the apices of trees are
outlined in Fig. 1. In order to protect the meristems and
perennating organs from harsh winter conditions, the meristematic
activity and the formation of new organs, such as leaves, are
terminated before the advent of winter and the perennating tissues
develop cold hardiness (Nitsch, 1957; Weiser, 1970; Cooke et al.,
2012). The most visible sign of growth cessation is the formation of
an apical bud, consisting of the shoot apical meristem (SAM) and
leaf primordia enclosed by protective bud scales (Nitsch, 1957;
Goffinet & Larson, 1981; Ruttink et al., 2007; El-Kayal et al.,
2011). For a brief period immediately after growth cessation,
growth can be reactivated simply by exposing plants to growth-
promotive conditions, for example long days in poplar (Saure,
1985; Espinosa-Ruiz et al., 2004; Pallardy, 2008). Traditionally,
this phase of the annual growth cycle, when growth cessatio n can be
reversed by exposure to growth-promotive signals, is defined as
ecodormancy (Lang et al., 1987), because, in this state, growth
arrest is induced and maintained by responses to external signals.
Subsequently, a transition gradually occurs in apical buds from
ecodormancy to endodormancy, in which (in contrast with
ecodormancy) growth arrest is maintained by endogenous signals
and the perennating tissues are not sensitive to growth-promotive
signals. Consequently, growth cannot be reactivated once endodor-
mancy is established by simply exposing plants to growth-
promotive conditions (Perry, 1971; Sarvas, 1974; Saure, 1985;
Battey, 2000; Espinosa-Ruiz et al., 2004; Pallardy, 2008). There-
fore, endodormancy must be broken and transition to ecodor-
mancy must occur before growth can be reactivated. The earliest
visual sign of reactivation of growth is the swelling of buds, followed
by the emergence of preformed leaf primordia and, eventually, the
formation and growth of new leaves. The sequential developmental
stages of the annual growth cycle and their timing (phenology;
Fig. 1) are associated with complex and tightly coordinated changes
in cellular, physiological and morphological processes that have
been extensively studied in various tree species (Nitsch, 1957;
Weiser, 1970; Heide, 1974; Junttila, 1976; Rinne & van der
Schoot, 1998; Druart et al., 2007; Ruttink et al., 2007; summa-
rized in Cooke et al., 2012) . These include metabolic shifts towards
the accumulation of storage compounds during the transition from
active growth to dormancy, and reversal of these shifts during
reactivation of growth after dormancy break (Druart et al., 2007;
Ruttink et al., 2007). The regulation of the metabolic shifts that
accompany distinct stages of the growth cycle and the underlying
global gene expression changes have been reviewed elsewhere and
thus will not be covered here (Welling & Palva, 2006; Cooke et al.,
2012).
Although the terms eco- and endo-dormancy have been widely
used to define dormancy states during annual growth cycles in trees
(Lang et al., 1987; Rohde & Bhalerao, 2007), they are somewhat
problematic, particularly ecodormancy. For example, the meristem
Active growth
LD
SD
SD
Growth
cessation
Bud burst
WT
Dormancy
release
LT
Dormancy
LT?
S
p
r
i
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W
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Fig. 1 Annualgrowth cycle in trees. Reduction in daylength (short days, SD)
during late summer/early autumn induces the cessation of growth and bud
set in trees such as poplar and spruce. Initially, growth cessation can be
reversed by exposing plants to growth-promotive conditions. This stage of
growth cessation is referred to as ecodormancy (as growth cessation is
induced and maintained by external signals, such as SD). Prolongedexposure
to SDs in late autumn induces the establishment of dormancy in buds. In a
dormant state, meristem and perennating organs, such as leaf primordia,
become insensitive to growth-promotive signals. Traditionally, when growth
arrest is maintained by endogenous signals, buds are described as being in an
endodormant state. Low non-lethal temperatures progressively lead to
dormancy release, following which growth arrest is primarily maintained by
low temperatures in the winter. As growth arrest is maintained by external
signals (low temperature), buds are described as being in another
ecodormant state. After release from dormancy, ‘warm’ temperatures (a few
degrees higher than the dormancy-releasing temperature) in the spring
promote bud burst in species such as poplar. In species such as birch and
apple, low temperature induces both dormancy establishment and release,
and promotes bud burst. LD, long days; LT, low temperature; WT, warm
temperature.
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and perennating tissues are described as being in an ecodormant
state both before and after release from endodormancy (Fig. 1),
giving the impression that they revert to the state they were in before
the transition to endodormancy. However, responses of perennat-
ing tissues to external signals, such as photoperiod, which have
different effects on ecodormant meristems before and after
transitions to endodormancy, show that this is not true. In
addition, there are clear differences between the two ecodormant
states (before and after endodormancy) in both global gene
expression patterns (Karlberg et al., 2010; Howe et al., 2015) and
chromatin modifications (P. Miskolczi et al., unpublished). Fur-
thermore, comparisons between bud and seed dormancy, which
obviously share several regulatory similarities (Rohde & Bhalerao,
2007), would be facilitated by the use of common terminology for
dormancy in seeds and apices of trees. For example, endodormancy
is similar to dormancy in seeds, which is defined by a failure to
activate growth under favorable conditions (Penfield & King,
2009; Graeber et al., 2012). Hence, key stages of annual growth
cycles warrant reconsideration and definition in developmental
terms rather than on the basis of growth responses to external
stimuli. Therefore, in this review, we focus on the molecu lar control
of the four key stages of the annual growth cycle in trees (Fig. 1): (1)
growth cessation and bud set; (2) establishment of bud dormancy;
(3) release of bud dormancy; and (4) bud burst and active growth.
We discuss the external and endogenous signals and response
pathways that regulate these key stages of the annual growth cycle in
the following sections.
III. Control of growth cessation and bud set by
seasonal cues
It has been shown that photoperiod plays a major role in the
regulation of growth cessation and bud set phenology invarious tree
species (Nitsch, 1957; Powell, 1987; Cooke et al., 2012; Petterle
et al., 2013; Ding & Nilsson, 2016). Changes in photoperiod
provide cues that herald the advent of winter and are used by trees to
activate mechanisms that control the timing of growth cessation in
temperate and boreal regions. The photoperiodic signal controlling
seasonal growth in trees appears to be perceived in the leaves. This is
partly because leaf extracts or grafts from plants grown under short-
day (SD) conditions (inducing growth cessation) can induce growth
cessation in plants grown under long-day (LD) conditions that
would otherwise permit continued growth (Wareing, 1956; Eagles
& Wareing, 1964). Temperature also declines as winter approaches,
and rises when it ends, but is a less robust signal of seasonal change,
because temperature (unlike photoperiod) may fluctuate strongly
diurnally as well as seasonally. It should be noted, however, that
temperature is used as a cue inthe seasonal control of growth in some
trees, for example apple and pear (Heide & Prestrud, 2005; Tanino
et al., 2010). When the transition from summer to autumn occurs,
daylength isprogressively reduced (to SDs) and, when it falls below a
growth-permitting threshold (defined as the critical daylength), a
growth cessation program is induced in the shoot apex. The growth
cessation program terminates apical elongation growth and induces
bud development (Wareing, 1956; Nitsch, 1957; Goffinet &
Larson, 1981; Powell, 1987; Thomas & Vince-Prue, 1996; Ruttink
et al., 2007; El-Kayal et al., 2011; Petterle et al., 2013). In trees such
as poplar, both cell division and cell elongation in SAM are
progressively suspended, and young leaf primordia develop into
embryonic rather than foliage leaves, and stipules develop into
enveloping bud scales (Goffinet & Larson, 1981; Rohde et al.,
2002). The developing buds gradually increase in size as a result of
the maturation of embryonic leaves and,subsequently, expansion of
the internodes of embryonic shoots emerging within bud scales is
completely inhibited, leading to the formation of a closed bud
(Goffinet & Larson, 1981; Ruttink et al., 2007; Cooke et al.,2012).
In contrast with poplar, in spruce, which has determinate
growth, the developmental pattern at the apex in response to SDs
varies and is covered in detail in Cooke et al. (2012). Briefly, in
spruce, the elongation of internodes and the formation of new
needle primordia are separated in time (El-Kayal et al., 2011;
Cooke et al., 2012; Sutinen et al., 2012), in contrast with poplar, in
which new leaves form and internodes elongate simultaneously.
Another difference between bud set in spruce and angiosperms,
such as poplar, is that stipules do not develop into bud scales in
spruce during bud formation. Despite these developmental
differences between indeterminate species, such as poplar, and
determinate species, such as spruce, photoperiod is also a primary
regulator of transition to growth cessation in spruce (Heide, 1974),
although temperature does modulate the responses (Hamilton
et al., 2016) to photoperiod, as described later.
IV. How does photoperiod control developmental
transitions?
Findings regarding the photoperiodic control of developmental
transitions in other plants, particularly flowering in the annual
model plant Arabidopsis, have provided important insights into the
general molecular basis of the photoperiodic control of develop-
mental processes (Jeong & Clark, 2005). Thus, before considering
the molecular basis of the photoperiodic control of growth in trees,
we briefly describe key features of the photoperiodic control of
flowering in Arabidopsis. A vital element of the photoperiodic
machinery is the endogenous circadian clock, which is entrained by
photoperiodic cues and has a free-running period of c. 24 h. The
clock acts like a pacemaker, and controls rhythmic outputs of
endogenous processes, such as gene expression, thereby contribut-
ing to the regulation of physiological responses to photoperiodic
signals. The clock is composed of various proteins involved in
interconnected transcriptionaltranslational feedback loops
(Greenham & McClung, 2015). In Arabidopsis, three major core
components of the central oscillator have been defined: PSEUDO-
RESPONSE REGULATOR family member PRR1/TIMING OF
CAB2 EXPRESSION 1 (TOC1) and the MYB transcription factors
CIRCADIAN CLOCK ASSOCIATED1 (CCA1) and LATE
ELONGATED HYPOCOTYL (LHY ) (Schaffer et al., 1998; Wang
& Tobin, 1998; Huang et al., 2012). In addition to the clock
components, photoreceptors also play key roles in the control of
photoperiodic responses. The perception of light signals by the
photoreceptors PHYTOCHROME A (PHYA)andPHYB and the
blue light receptor CRYPTOCHROME (CRY) entrains the
circadian clock (Somers et al., 1998), that is, allows it to maintain
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a circadian period, whereas the clock governs the rhythm and
phases of downstream gene expression (Valverde et al., 2004;
Kobayashi & Weigel, 2007).
Two models, the external and internal coincidence models, have
been proposed to explain how the central oscillator measures
daylength and mediates the photoperiodic control of various
responses, as excellently discussed by Kobayashi & Weigel (2007).
Here, we cover only the external coincidence model, as it is well
supported experimentally and more relevant for an understanding
of the photoperiodic control of growth in trees. According to this
model, originally proposed by Bunning (1946), photoperiodic
responses controlled by the circadian oscillator are sensitive to light
during a certain phase and will occur if light is perceived during this
phase (Fig. 2). Experimental evidence for the external coincidence
model has been provided by studies of the photoperiodic control of
flowering in Arabidopsis (in which flowering is promoted by LDs
and delayed by SDs). The expression of CONSTANS (CO), a key
regulator of flowering, is controlled by the circadian oscillator and
peaks at the end of the light period under LDs (16 h : 8 h,
light : dark), butin the darkin SDs(8 h : 16 h, light : dark) (Suarez-
Lopez et al., 2001). Importantly, expression of the CO target
FLOWERING LOCUS T (FT) (Samach et al., 2000) also occurs in
light periods, and peaks at the end of long photoperiods. By
contrast, when Arabidopsis is grown in SD conditions, FT
expression is weak and does not peak, as the CO protein is unstable
in the dark (Suarez-Lopez et al., 2001). These results prompted the
suggestion that the CO expression pattern provides the light-
sensitive rhythmic cue required for the photoperiodic control of
flowering, which depends on coincidence between high CO levels
and the light period.
Indications that photoperiod-controlled changes in CO levels
play a key role in photoperiod discrimination have been provided
by the analysis of toc1 mutants of Arabidopsis (Strayer et al., 2000),
which flower early in SDs (8 h : 16 h, light : dark). In key
experiments, Yanovsky & Kay (2002) showed that the toc1 mutant
has a shorter free-running period (21 h) than the wild-type (24 h)
and an earlier CO expression peak. Consequently, CO expression
coincides with the light period in toc1 mutants, even in short
photoperiods (8 h : 16 h, light : dark) as a result of the misinter-
pretation of photoperiodic inputs, because the photoperiodic
rhythm in toc1 no longer coincides with the external photoperiod of
24 h, unlike in wild-type plants. However, when toc1 mutants are
grown under a 7 h : 14 h, light : dark regime (with 21-h diurnal
cycles), CO expression peaks in the dark and the early flowering
defect is suppressed. Importantly, Yanovsky & Kay (2002) found
that FT expression was high in toc1 mutants grown under a
8 h : 16 h, light : dark regime promoting early flowering, but
reverted to low levels in toc1 mutants grown under a 7 h : 14 h,
light : dark regime, causing CO expression to peak in the dark.
Thus, CO activation of FT and the induction of flowering require
coincidence between peaks of CO expression and external light.
These results elegantly demonstrate the fundamental aspects of the
external coincidence model in the context of flowering and are
highly useful for understanding the photoperiodic control of
growth in trees, as discussed later.
1. Photoperiodic control of growth in trees
Experiments in which exposure to short days induce growth
cessation and bud set demonstrate the involvement of
Light
Day DayNight Night
Photoreceptors
PHYA/PHYB
Circadian clock
LHYs, TOC1,
CCA1
LHYs, TOC1,
CCA1
CO mRNA
CO protein
FT-mRNA
CO mRNA
CO protein
FT-mRNA
(a)
Light Photoreceptors
PHYA/PHYB
Circadian clock
(b) Day Day
Night Night
Coincidence
phase
Coincidence
phase
Fig. 2 External coincidence modelfor photoperiodic control of flowering in Arabidopsis. Transition to floweringoccurs when the expression peakof CONSTANS
(CO) coincides with the light phase. Photoreceptors (PHYA/PHYB) perceive light signals and entrain the clock. The central oscillator consisting of LATE
ELONGATED HYPOCOTYL 1 and 2 (LHYs), TIMING OF CAB EXPRESSION 1 (TOC1) and CIRCADIAN CLOCK ASSOCIATED1 (CCA1) controls the diurnal
expression of CO. In long days (left panel), the CO expression peak coincides with the light phase (coincidence phase). In light,the CO protein isstable and can
activate FLOWERING LOCUS T (FT) expression, promoting flowering.In short days (right panel),CO expression peaks in the dark (no coincidence of light phase
and CO expression). In the dark, CO protein is degraded and thus cannot induce FT expression and further processes. Redrawn from Bastow & Dean (2002).
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photoperiodic signals in these processes, and findings that inter-
rupting long nights by short pulses of light reverse SD induction of
growth in poplar (Howe et al., 1996) clearly suggest the involve-
ment of the circadian clock in the photoperiodic control of growth
in trees. Such physiological indications of photoperiodic controls in
tree growth (Nitsch, 1957) have recently been complemented with
explorations of the molecular basis of the mechanisms involved,
especially in the model organisms poplar (Olsen et al., 1997;
Bohlenius et al., 2006; Hsu et al., 2006; Takata et al., 2009, 2010;
Ibanez et al., 2010; Karlberg et al., 2010; Azeez et al., 2014;
Tylewicz et al., 2015), spruce (Gyllenstrand et al., 2007, 2014;
Karlgren et al., 2013) and peach (Li et al., 2009). These molecular
studies have shown that components of the clock and photorecep-
tors in annuals, such as Arabidopsis, have orthologs in trees, and play
key roles in the photoperiodic control of seasonal growth in trees
(Olsen et al., 1997; Takata et al., 2009, 2010; Ibanez et al., 2010;
Karlgren et al., 2013). Later, we outline findings that demonstrate
the role of the clock and photoreceptors as early components in the
photoperiodic control of growth in trees.
The involvement of phytochrome photoreceptors in the control
of SD-mediated growth cessation and bud set in poplar has been
demonstrated in several studies (Howe et al., 1996; Olsen et al.,
1997; Kozarewa et al., 2010). Olsen et al. (1997) showed that
hybrid aspen clone T89 (P. tremula 9P. tremuloides) plants
overexpressing oat phytochrome A (PHYA) cDNA failed to
undergo growth cessation in response to SDs. Kozarewa et al.
(2010) confirmed the involvement of PHYA in these processes in
hybrid aspen by showing that the downregulation of PHYA
expression resulted in faster responses to SDs, with earlier growth
cessation and bud set than in wild-type plants. In addition, they
found that the expression of LHY was repressed in PHYA-
downregulated plants, thereby establishing a link between
phytochrome and the circadian clock. In hybrid aspen, the clock’s
involvement in the photoperiodic control of growth cessation has
been demonstrated by findings that the downregulation of LHYs
and TOC1 perturbs both the phase and period of clock-controlled
gene expression, consequently delaying growth cessation and bud
set (Ibanez et al., 2010). Interestingly, dampening of circadian
rhythms has been observed in spruce under constant light
conditions: the expression of clock genes (CCA1,LHY,TOC1
and GI) oscillates in both SDs and LDs, but with lower amplitude
in the latter, and no cyclic rhythm of gene expression reportedly
occurs in constant light or dark, suggesting that circadian clock
genes are conserved but their regulation may differ in conifers and
angiosperms (Gyllenstrand et al., 2014). The implications of these
differences in the regulation of clock-related genes between poplar
and spruce for the photoperiodic regulation of growth cessation are
currently unclear.
2. FT is an early target of SD signals in the induction of gro wth
cessation
A major step towards an understanding of how photoperiod
controls growth cessation was provided by the demonstration that
the downregulation of the poplar ortholog of Arabidopsis FT
expression following exposure to SDs is necessary and sufficient to
induce growth cessation and bud set in hybrid aspen (P. tremula
9P. tremuloides) (Bohlenius et al., 2006; Hsu et al., 2011).
Further, Hsu et al. (2011) showed that FT2 (one of the two closely
related FT orthologs) is the target of SD signals in growth cessation.
In hybrid aspen, as in Arabidopsis,CO, the upstream regulator of
FT, has a diurnal expression pattern, peaking at the end of the light
phase in LDs (Bohlenius et al., 2006). Consequently, a shift from
LDs to SDs results in this expression peak of CO occurring in the
dark. The CO protein is highly unstable in the dark in Arabidopsis
(Valverde et al., 2004) and, presumably, in hybrid aspen (although
its stability in trees has not yet been determined). Therefore, on a
shift to SDs, CO cannot maintain or promote FT expression, which
thus declines in SDs. Accordingly, FT overexpression can override
the induction of growth cessation by SDs in hybrid aspen
(Bohlenius et al., 2006; Hsu et al., 2011). The model described
earlier is well supported in poplar, but, in spruce, the expression of
the FT-like gene FT4 is induced on a shift to SDs and its
overexpression results in the induction of growth cessation
(Gyllenstrand et al., 2007). This difference in growth cessation
phenotype between FT4 overexpressors in spruce and FT overex-
pressors in poplar (Bohlenius et al., 2006; Hsu et al., 2011; Azeez
et al., 2014) probably occurs because FT4 is closer to the FT
antagonist TERMINAL FLOWER 1 (TFL1) functionally, rather
than a bona fide FT, as demonstrated recently by Klintenas et al.
(2012). However, the antagonistic regulation of developmental
responses by FT genes has also been observed in other species. For
example, in sugar beet and onion, closely related FT genes are
known to have opposite effects on physiological responses (Pin
et al., 2010; Lee et al., 2013).
Bohlenius et al. (2006) also provided insight into the molecular
mechanism that may underlie latitudinal clines in the timing of bud
set by determining diurnal patterns of CO expression in aspen trees
collected across the latitudinal cline in Sweden. They showed that
the peak of CO expression shifts across the latitudinal cline and is
well correlated with the critical daylength defining the timing of
growth cessation in these genotypes. These findings imply that CO
expression will peak in the dark earlier during the year (and thus
growth should cease earlier) in northern genotypes than in southern
genotypes. The correlation between peaks in CO expression and
critical daylengths, together with the demonstration that the
downregulation of CO results in earlier growth cessation in hybrid
aspen (Bohlenius et al., 2006), provides strong, albeit correlative,
evidence for a mechanism underlying the latitudinal cline in the
timing of growth cessation.
3. Tree orthologs of APETALA1 couple the CO/FT module to
cell cycle regulation
Differences in growth cessation and bud set timing have been found
among different genotypes resulting from a cross between
P. trichocarpa 9P. deltoides with very similar patterns of FT2
downregulation following exposure to SDs (Resman et al., 2010).
This observation provides experimental confirmation that com-
ponents acting downstream of the CO/FT module also play a role in
the SD-mediated control of growth cessation. Mediators of SD
signals downstream of the CO/FT module in the photoperiodic
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control of growth have been identified recently in hybrid aspen.
The first was the AINTEGUMENTA-like 1 (AIL1) transcription
factor, which mediates SD signals downstream of FT2 in hybrid
aspen (Karlberg et al., 2011). The downregulation of AIL gene
expression was found to be necessary for growth cessation by SDs,
although it was noted that AIL1 may not be a direct target of FT2.
Accordingly, Azeez et al. (2014) identified Like-AP1 (LAP1), a tree
ortholog of the Arabidopsis floral meristem identity gene
APETALA1 (AP1), as a link between FT and AIL1, which is
probably a direct target of FT2 and, like FT2, its downregulation is
essential for SD-induced cessation of growth.Moreover, it was
shown that LAP1 binds to the promoter of AIL1 and may control its
expression. Recently, Tylewicz et al. (2015) have shown that
FD-LIKE1 (FDL1), a homolog of the Arabidopsis flowering time
gene FD (Wigge et al., 2005), also mediates the photoperiodic
control of vegetative growth by regulating LAP1 expression.
Intriguingly, although hybrid aspen has two closely related
orthologs of FD,FDL1 and FDL2, both of which physically
interact with FT, only the FTFDL1 complex appears to
participate in the photoperiodic control of growth. In addition to
the FTLAP1AIL pathway, results from studies of the evergreen
(evg) mutant of peach suggest a role for DAM genes (DORMANCY
ASSOCIATED MADS BOX) in growth cessation. This mutant fails
to cease growth and its genome harbors a deletion in a region
encompassing six DAM genes (Li et al., 2009) that belong to an
SVP/AGL24 clade (Bielenberg et al., 2008) family of MADS box
genes in Arabidopsis. These genes display seasonal- and photope-
riod-responsive expression patterns (Li et al., 2009), and, in
Arabidopsis, SVP is a known repressor of FT (Mateos et al.,
2015). Thus, it will be interesting in the future to investigate the
roles of these DAM genes in growth cessation responses and their
interactions with the CO/FT pathway.
Based on the results described so far, we propose a simple model
for SD-induced growth cessation (Fig. 3). On a shift to SDs, FT
expression is repressed, leading to the downregulation of LAP1 and
AIL expression. As AIL1 controls the expression of key cell cycle
regulators, for example D-type cyclins (Karlberg et al., 2011;
Randall et al., 2015), its downregulation results in the suppression
of cell cycling and, hence, growth cessation. Thus, according to this
model, SDs essentially induce the removal of a growth-promotive
signal rather than the generation of a growth inhibitor. As outlined
in Fig. 3, key elements of the photoperiodic signaling pathway
mediating growth control in trees have several similarities with the
flowering time pathway in Arabidopsis, and the bulbing and
tuberization pathways in onion and potato (Navarro et al., 2011;
Lee et al., 2013). The evolution of pathways that exploit the same
photoperiodic signals, but control diverse morphological processes,
clearly warrants attention, as does the somewhat unexpected
finding that signaling pathways that mediate flowering in
Arabidopsis and seasonal growth in trees deviate downstream of
the CO/FT target (AP1/LAP1), rather than immediately down-
stream of CO/FT.
4. Is gibberellin (GA) biosynthesis a target of SDs in the
induction of growth cessation?
It should be noted that the FTLAP1AIL1 pathway is the most
thoroughly studied, but certainly not the only pathway implicated
in the photoperiodic control of growth in trees. For example, there
are several indications that GAs may participate in the photope-
riodic control of growth cessation, possibly independently of the
CO/FT pathway (Eriksson et al., 2015). First, concentrations of
bioactive GAs rapidly decline on exposure to SDs (Junttila &
Jensen, 1988; Olsen et al., 1997), whereas transgenic hybrid aspen
plants that maintain high levels of GAs in SDs, for example GA20
oxidase overexpressors, do not cease growth in SDs and can thus
override SD signals (Eriksson et al., 2000). However, although
growth is more sensitive to SDs in hybrid poplar plants with
reduced GA levels or sensitivity to GAs, they disp lay little difference
from wild-type plants in the timing of bud set (Zawaski & Busov,
2014). One interpretation of these findings is that growth is more
rapidly reduced by SDs in such plants because GAs are general
promoters of growth. In summary, more evidence is needed to
firmly establish that a reduction in GA levels or sensitivity is
essential in SD-induced growth cessation or bud set sensu stricto.A
GA-deficient mutant in trees would greatly facilitate the unequiv-
ocal elucidation of the role of GAs in growth cessation or bud set, as
GA reductions in currently available transgenic trees may be
insufficient for this purpose.
5. ABI3 and FD orthologs participate in bud development
The most visible change indicating growth cessation is the
formation of a bud at the apex. On exposure to SDs (i.e. less than
critical daylength), a morphogenetic transformation of leaf
primordia occurs (Goffinet & Larson, 1981; Rohde et al., 2002).
The primordia developing after SD exposure will senesce and their
stipules will enlarge, forming bud scales in poplar. Gradually, these
bud scales will enclose the primordia that form embryonic leaves,
thereby forming a closed bud structure. In addition, bud scales
LAP1
AIL1
Long days
Growth
FT2 FDL1
Short days
ABI3
ABI3
Bud
development
and adaptive
response
D-type cyclins
FDL1
Fig. 3 Transcriptional network underlying the photoperiodic control of
growth in poplar. A shift to short days represses FT2 expression, resulting in
the downregulation of LAP1 (LIKE-AP1) and the LAP1 target AIL1
(AINTEGUMENTA-LIKE1). Downregulation of AIL1 leads to the suppression
of cell cycle-related genes and growth cessation. The expression of FD-LIKE1
(FDL1) and ABA INSENSITIVE 3 (ABI3) is induced by short days, and they
form a transcriptional complex involved in the regulation of bud maturation
and cold acclimation-related programs.
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accumulate phenylpropanoids and develop hairs (Ruttink et al.,
2007). Bud development is influenced by abscisic acid (ABA) and
ethylene signaling pathways, as well as by ABI3 (ABA
INSENSITIVE 3)andFDL1 transcription factors (Rohde et al.,
2002; Ruonala et al., 2006; Tylewicz et al., 2015). Weakened
responses to ABA (Petterle, 2011) or ethylene (Ruonala et al.,
2006) result in buds with altered, open structures, and similar
results are obtained when ABI3 (Ruttink et al., 2007) or FDL1
(Tylewicz et al., 2015) is overexpressed. Interestingly, Tylewicz
et al. (2015) have reported recently that FDL1 expression is
induced after SDs, like ABI3 expression, and ABI3 can physically
interact with FDL1. Thus, ABI3 and FDL1 probably act in concert
in bud development downstream of SDs.
V. The role of temperature in growth cessation and
bud set
As described earlier, the role of the seasonal reduction in
photoperiod as an environmental cue inducing the cessation of
apical elongation growth and bud set has been intensively studied at
the molecular level. Daylength reduction and the subsequent
responses of trees usually occur in warm, non-inductive temper-
atures, and the timing of growth cessation and bud set strongly
correlates with the latitudinal origin of trees (Bohlenius et al., 2006;
Luquez et al., 2008). To test whether temperature affects bud set,
Luquez et al. (2008) compared its timing in trees in the Swedish
Aspen collection (sampled from 12 locations in Sweden along a
latitudinal cline of 55.966.0°N) in both the field and a climate
chamber. In the growth chamber, the temperature was maintained
at a constant 20°C, whilst the photoperiod was decreased by
1hwk
1
, resembling the rate of change in the field. A tight linear
(1 : 1) relationship between photoperiods at the time of bud set in
the field and climate chamber was obtained, strongly indicating
that temperature had little or no effect on bud set phenology.
However, a caveat is that the rate of decrease in photoperiod is not
identical across latitudes, and so a uniform reduction of the
photoperiod in growth chamber studies may not faithfully
reproduce field conditions at every latitude.
The studies with poplar outlined earlier suggest that photoperiod
may be a primary cue regulating the seasonal control of growth with
little input from temperature. However, a number of studies have
indicated that low temperature can induce seasonal growth cessation
and influence bud formation in poplar, Malus (apple) and Pyrus
(pear) (Stevenson, 1994; Howe et al., 2000; Junttila et al., 2003;
Heide & Prestrud, 2005; Mølmann et al., 2005; Svendsen et al.,
2007; Kalcsits et al., 2009; Rohde et al., 2011). Although low
temperature is sufficient to induce growth cessation and bud set in
apple or pear, in poplar, temperature modulates the response to
photoperiodically controlled growth cessation and bud set, as wellas
the rate at which bud setproceeds (Rohde et al., 2011). There fore, an
interesting question is whether the signaling components mediating
the photoperiodic control of growth also mediate temperature
signals in apple and pear trees, or whether these trees have evolved
alternative signal transduction pathways for the temperature-
mediated control of seasonal growth. Interestingly, low temperature
is known to increase ABA levelsas well as responses to ABA (Welling
& Palva, 2006). Although exogenously applied ABAdoes not induce
growth cessation in hybrid aspen (R. Bhalerao, unpublished) and
ABA-insensitive hybrid aspen plants display normal growth cessa-
tion in response to SDs (A. Petterle & R. Bhalerao, unpublished),
the possibility cannot be excluded that ABA might play a role in low-
temperature-mediated growth cessation in other tree species, such as
apple and pear, in which low temperature is sufficient to induce
growth cessation and bud set. Thus, the generation of ABA-
insensitive apple trees might allow the experimental analysis of the
role of ABA in the temperature-mediated control of growth
cessation in the future. Furthermore, temperature-mediated path-
ways could also interact with photoperiodic pathway(s) in the
control of growth cessation. For example, low temperature coupled
with the blocking of GA biosynthesis can induce bud set in PHYA-
overexpressing hybrid aspen plants (Mølmann et al., 2005).
Furthermore, in chestnut, low temperature disrupts the circadian
oscillation of LHY and TOC1 expression (Ramos et al., 2005).
Thus, knowledge of the photoperiodic pathways opens up the
possibility to investigate therole of interactions between temperature
and photoperiodic signaling pathways in the future.
VI. Establishment and release of bud dormancy
Following growth cessation, dormancy is gradually established. In
both poplar and spruce, exposure to SDs after growth cessation is
sufficient to induce its establishment (Heide, 1974; Espinosa-Ruiz
et al., 2004). By contrast, in species belonging to Rosaceae, a
reduction in temperature plays a role in the establishment and
release of dormancy (Heide & Prestrud, 2005). We know
substantially less about the regulation of bud dormancy than about
the photoperiodic control of growth cessation. This is partly a result
of a lack of molecular markers. Thus, the establishment of
dormancy can only be indirectly inferred experimentally by
determining whether bud burst can occur after a shift to growth-
promotive conditions without prior exposure to dormancy-
breaking signals. In poplar, this involves a shift to LD and relatively
warm temperatures (Espinosa-Ruiz et al., 2004). It is important to
note that, when assessing dormancy in buds, bud burst should be
evaluated in the apex rather than in lateral (axillary) buds. This is
because the latter may resume growth when the apex has died or
been damaged, giving a false impression that, when lateral buds
resume growth without cold treatment, a plant has defective
dormancy regulation. Once dormancy is established, the meristem
and leaf primordia must become insensitive to external and
endogenous signals, whatever they may be. Although the molecular
basis of bud dormancy remains unknown, the identification of the
signals that activate growth and the elucidation of how the
meristem and primordia become insensitive to these signals are
crucial for an understanding of the control of bud dormancy. For
example, in the cambial meristem, dormancy establishment is
mediated by the cambial cell division machinery becoming
insensitive to indole-acetic acid, a key regulator of cambial activity
during active growth periods (Little & Bonga, 1974; Nilsson et al.,
2008; Baba et al., 2011).
Several studies have reported global transcriptomic,
metabolomic and other changes associated with transitions to
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bud dormancy (Ruttink et al., 2007; Karlberg et al., 2010; Resman
et al., 2010; Kusano et al., 2011; Shim et al., 2014; Wang et al.,
2014; Howe et al., 2015). These descriptive studies have not
provided insights into the mechanistic basis of dormancy estab-
lishment. However, an interesting hypothesis regarding bud
dormancy regulation has been proposed, based on plasmodesmatal
dynamics observed in shoot apices after SD in Betula and poplar
(Jian et al., 1997; Rinne & van der Schoot, 1998). Plasmodesmata
(PD) are intercellular conduits that connect and regulate symplastic
trafficking between adjacent cells (Maule, 2008), and play
important roles in developmental processes by controlling the
trafficking of regulatory molecules, such as hormones and
transcription factors (Urbanus et al., 2010; Yoo et al., 2013; Han
et al., 2014). PDs can be closed by the deposition of callose,
catalyzed by callose synthases and opened by its removal via the
activity of callose-degrading endoglucanases (Rinne et al., 2005;
Levy et al., 2007; Simpson et al., 2009). Moreover, several proteins
have recently been demonstrated to show associations with PDs in
Arabidopsis, and some of these, for example ParA-like division
proteins (PDLPs) and GERMIN, clearly modulate the functioning
and trafficking via PDs (Bayer et al., 2004; Thomas et al., 2008;
Raffaele et al., 2009).
In birch and poplar, the establishmentof dormancy is preceded by
the blockage of PDs with callose (1,3-b-glucan) and protein-
containing dormancy sphincter complexes (DSCs), whereas the
opening of PDs correlates with dormancy release (Jian et al., 1997;
Rinne & van der Schoot,1998; Rinne et al., 2011). These correlative
observations prompted the hypothesis that dormancy establishment
could involve the symplastic isolation of SAMs by blockage of PDs.
Based on similar observations in non-woody species, for example
winter wheat (Jian & Sun, 1992) and potato (Viola et al., 2007), the
simple rationale is that the formation of DSCs impedes the
symplastic movement of growth-promoting substances between
cells in the meristem, including nutrients and metabolites, diffusing
morphogens and transcriptional factors. Consequently, the forma-
tion of DSCs interrupts the cellcell signaling networks required to
sustain development and physically isolates SAM cells from each
other, thereby establishing dormancy (Fig. 4). The idea that the
disruption of cellcell communication by the blockage of PDs may
induce dormancy establishment is attractive, but lacks supporting
genetic and molecular evidence. For example, PD blockage could
simply be non-causally correlated with dormancy development.
Another issue with the hypothesis is that, although PD blockage can
disrupt the trafficking of many signals, several hormones (e.g. auxin)
move via specialized carriers (Robert & Friml, 2009), and this
transport may not be interrupted by PD blockage. Thus, more
functional evidence that symplastic isolation is a causal factor in the
establishment of bud dormancy isrequired. Another key aspect that
requires elucidation is the signaling involved in the establishment of
bud dormancy by SDs. It is uncertain even whether the establish-
ment of bud dormancy actually involves the generation of
dormancy-inducing signals by SDs or low temperature. For
example, removal of or insensitivity to growth-promotive signals,
as in cambial dormancy (Baba et al., 2011), could be equally
sufficient to establish dormancy in buds. In seeds, ABA is a major
regulator of dormancy (Penfield & King, 2009) and, interestingly,
increases in ABA levels following exposure to SDs have been
observed in poplar (Ruttink et al., 2007). Moreover, preliminary
data obtained from hybrid aspen studies indicate that ABA could be
involved in bud dormancy establishment, as ABA-insensitive hybrid
aspen plants fail to establish dormancy in response to SDs
(S. Tylewicz et al.,unpublished).
The role of SDs in the regulation of growth cessation, bud set and
dormancy has attracted intense interest. However, it should be
noted that, although SDs alone can induce the establishment of
dormancy under controlled growth conditions, temperature is
FT
FT
GA
Long days Short days
ABA
Callose
synthase
SAM
FT protein
Callose deposition
in plasmodesmata
SAM
Fig. 4 Hypothetical model of bud dormancy
establishment. Prolonged exposure to
dormancy-inducing signals (short days or,
possibly, low temperature) results in the
repression of growth-promoting signals, for
example FLOWERING LOCUS T (FT)
expression and bioactive gibberellic acid (GA)
levels. Simultaneously, the induction of
callose/glucan synthases after short days (SDs)
results in the closure of plasmodesmata (PDs).
Reductions in FT or GA, increases in abscisic
acid (ABA) levels and/or enhanced responses
to ABA induced by SDs could trigger the
closure of PDs, thereby mediating dormancy
establishment. SAM, shoot apical meristem.
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known to influence bud dormancy, especially in trees such as apple,
in which low temperature can also induce growth cessation and
dormancy (Heide & Prestrud, 2005). For example, Junttila et al.
(2003) observed temperature effects on dormancy establishment
during SD-induced bud set in ecotypes of different species of birch.
With a constant 12-h photoperiod, both species entered dormancy
faster at 1518°C than at either 912°Cor21°C. Thus, elucidation
of the interactions between temperature and SDs in bud dormancy
establishment is crucial to obtain deeper insights into the reg ulation
of bud dormancy, especially under field conditions.
1. A model for bud dormancy establishment
Based on current knowledge, outlined earlier, we propose the
following model for the establishment of bud dormancy, according
to which SDs could act at multiple levels (as illustrated in Fig. 4).
First, SDs induce the closure of PDs. SD-mediated downregulation
of GA levels or induction of increases in ABA levels (or enhanced
responses to ABA) could trigger the closure of PDs via the induction
of glucan synthases. The closure of PDs could then contribute to
the blockage of transport of growth-promotive signals to SAM. At
another level, SDs may block the production of growth-promotive
signals, for example GA or FT, thereby reinforcing and maintaining
dormancy. We stress that the proposed model only provides a
hypothetical framework that requires experimental validation.
However, as indicated earlier, our preliminary results from the
analysis of ABA-insensitive hybrid aspen plants lend some support
to this model. These plants not only fail to induce the establishment
of bud dormancy, but also cannot induce the closure of PDs
(S. Tylewicz et al., unpublished), suggesting possible links between
ABA, PD closure and dormancy establishment. Thus, detailed
analysis of ABA-insensitive plants may provide further insights into
the mechanisms underlying bud dormancy establishment.
2. Maintenance and release of bud dormancy
Further important aspects of dormancy to address include the
mechanisms involved in its maintenance and release, which are
poorly understood. Of course, there may be no requirement for a
mechanism to maintain dormancy: the mere absence of a signal
promoting its release may be sufficient. In other words, once
established, dormancy may become the default state until
dormancy-breaking signals are received. The investigation of
dormancy release is hindered, like the analysis of bud dormancy, by
a lack of appropriate molecular markers. As bud burst occurs only
after dormancy release, it clearly shows that dormancy has been
released. However, the use of the timing of bud burst as a marker
could lead to erroneous conclusions about the release of dormancy,
as dormancy release and bud burst are separate processes. Thus,
perturbations in bud burst phenology may be caused by defects in
dormancy release, reactivation (bud burst) after dormancy release,
or a combination of the two. For example, dormancy may be
released at the same time in two genotypes, but they may differ in
the rate at which bud burst proceeds thereafter and (hence) in bud
burst timing. Such genotypes actually differ in reactivation
processes, rather than dormancy regulation.
Prolonged exposure to low temperature induces dormancy
release in buds in species such as poplar (Saure, 1985; Hannerz
et al., 2003; Espinosa-Ruiz et al., 2004; Brunner et al., 2014; Fu
et al., 2015). However, in some taxa, for example Betula and white
spruce, the same temperature that establishes dormancy can induce
release from dormancy and reactivate growth (Heide, 1993;
Myking & Heide, 1995; Cooke et al., 2012). The optimal
temperature for breaking dormancy and reactivating growth varies
between species, and even between genotypes of the same species.
Furthermore, in some species, photoperiod (long days) can also
play a role in the reactivation of growth (Saure, 1985; Pallardy,
2008). Currently, the roles of neither temperature nor photoperiod
in dormancy release are understood at the molecular level.
The release of bud dormancy by prolonged exposure to low
temperature resembles vernalization Chouard (1960), although
there is a major difference between the processes, as vernalization
signals act in actively dividing cells (Wellensiek, 1962, 1964) unlike
dormancy-breaking signals. We know little about how low
temperature is sensed, either in these processes or more generally.
Major changes induced include shifts in gene expression profiles,
and substantial progress has been made in the elucidation of the
signaling pathways involved (Knight & Knight, 2012). However,
most relevant molecular-level studies in model plants, such as
Arabidopsis, have focused on short-term responses to rapid
reductions in temperature (Gilmour et al., 1988), rather than
prolonged exposure to low temperature. Therefore, the findings of
these studies may not necessarily be relevant to low-temperature-
induced release from dormancy in trees. However, recently, Kudoh
(2016) has reviewed how Arabidopsis can be used to investigate the
effect of seasonal changes on growth, which provides insights into
potentially similar mechanisms in trees.
Interestingly, exposure to chilling is followed by the reopening of
PDs (Rinne & van der Schoot, 1998; Levy et al., 2007). Thus, if the
closure of PDs contributes to the establishment and/or mainte-
nance of dormancy, their opening may contribute to dormancy
release by restoring the responsiveness of SAM to growth-
promotive signals, for example by providing functional routes for
the transport of growth-promoting signals to the shoot apex (Rinne
et al., 2011). However, the role of PD opening in dormancy release
has not been tested to date and the nature of the growth-promotive
signal mediating dormancy release by low temperature remains
unknown. It should also be noted that, like dormancy establish-
ment, the opening of PDs may simply be correlated with, rather
than a cause of, dormancy release.
3. Chromatin remodeling and dormancy release
Another process that has been implicated in dormancy release by
low temperature, based on its superficial similarity with vernaliza-
tion, is chromatin remodeling. In vernalization, chromatin
remodeling via evolutionarily conserved polycomb repression
complex 2 (PRC2), which deposits the repressive trimethylation
mark on lysine 27 of H3 at the FLC locus, plays a key role in
subsequent flowering (Michaels & Amasino, 1999; Gendall et al.,
2001; Bastow et al., 2004). Changes in H3K27me3 at certain loci,
such as DAM genes in peach, have been observed during bud
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dormancy release (Leida et al., 2012). Interestingly, the DAM genes
are expressed in terminal buds of pear and apricot (Yamane et al.,
2008, 2011; Li et al., 2009; Wells et al., 2015). However, their
physiological roles in bud dormancy regulation are far from clear,
and it is essential to determine whether the blocking of trimethy-
lation of H3K27 at candidate loci perturbs dormancy before
drawing definitive conclusions with regard to the roles of
H3K27me3 or DAM genes in this process. Possibly more
interesting is the upregulation of both GA20 oxidase, a key enzyme
in GA biosynthesis, and FT1 expression after low-temperature
treatment of dormant buds in hybrid aspen (Druart et al., 2007;
Karlberg et al., 2010; Rinne et al., 2011). GAs are positive
regulators of growth (Eriksson et al., 2000) and their application
to dormant axillary buds appears to eliminate the requirement for
low-temperature exposure to activate bud burst in hybrid aspen
(Rinne et al., 2011). Furthermore, as FT1 overexpression can also
override SD-induced growth cessation (Bohlenius et al., 2006;
Azeez et al., 2014), the activation of GA20 oxidase and FT1 by low-
temperature treatment indicates their potential involvement in
dormancy release in hybrid aspen, and possibly other trees. In
addition, there is some evidence for the involvement of CENL1,a
hybrid poplar (P. tremula 9P. alba) ortholog of TFL1,in
dormancy regulation. Hybrid poplar plants in which CENL1
expression is downregulated display reduced requirements for low-
temperature exposure for dormancy release, whereas CENL1
overexpressors display delayed bud burst (Mohamed et al., 2010).
The phenotypes of CENL1 plants, viewed in the context of the
antagonistic function of TFL1 to FT in flowering (Jaeger et al.,
2013) and low-temperature induction of FT1 expression (Karlberg
et al., 2010; Hsu et al., 2011; Rinne et al., 2011), suggest that
CENL1 may be a negative regulator of dormancy release. Based on
the available data, we propose a speculative model for the low-
temperature-mediated release of bud dormancy (Fig. 5). Again,
functional analysis of plants in which the expression of GA
biosynthesis and FT1 is altered may provide conclusive evidence
about their roles in dormancy release.
4. Regulation of bud burst
Once dormancy is released, ‘relatively’ warmer temperatures
promote bud burst in poplar, whereas, in other plants, for
example birch and spruce, bud burst can occur at the same low
temperature that releases dormancy (Heide, 1993; Myking &
Heide, 1995; Cooke et al., 2012). The optimum temperature
promoting bud burst and the time for which buds need to be
exposed to this temperature vary and are also related to the
temperature used for dormancy break (Cooke et al., 2012; Junttila
&Hanninen, 2012; Basler & Korner, 2014). As daylength also
increases around the time at which bud burst occurs, LDs may
also promote bud burst (Basler & Korner, 2014). However, LDs
may not be essential for bud burst; for example, in hybrid aspen
and aspen, daylength does not affect bud burst if dormancy has
been released (R. Singh & R. Bhalerao, unpublished). As outlined
earlier, a factor that complicates the investigation of bud burst is
that it is intimately connected with dormancy release, because bud
burst cannot occur until dormancy has been released. Therefore,
late bud burst may be a result of delayed dormancy release.
Nevertheless, several genes associated with perturbations in bud
burst have been identified recently in poplar, including LHY and
EBB1 (Ibanez et al., 2010; Yordanov et al., 2014). The downreg-
ulation of two LHY genes (PttLHY1 and PttLHY2, a clock
component in hybrid aspen) also results in delayed bud burst
(Ibanez et al., 2010). A genetic correlation has been noted between
bud set and bud burst in poplar (Olson et al., 2012; McKown
et al., 2014). However, it is worth noting that photoperiod does
not appear to be critical in bud burst regulation, at least under
controlled growth conditions in hybrid aspen, birch and several
other trees (S. Tylewicz & R. Bhalerao, unpublished; Myking &
Heide, 1995; Heide & Prestud, 2005). Thus, it remains to be seen
whether the downregulation of LHY delays bud burst because
LHY plays a direct role in the process or is involved indirectly. If,
however, LHY does influence bud burst, it will be important to
determine whether it is involved in dormancy release or bud burst
(Ibanez et al., 2010).
EBB1, a member of the ERF family of transcription factors, has
been identified recently by Yordanov et al. (2014) as a gene that may
participate in bud burst in poplar, by screening a population of
activation-tagged hybrid poplar lines for early bud burst. EBB1
overexpressors displayed early bud burst, whereas the downregu-
lation of EBB1 resulted in delayed bud burst and changes in the
expression of genes associated with various metabolic processes,
meristem growth and regulation of hormone levels (Yordanov et al.,
2014). Moreover, some DAM genes implicated in growth cessation
were downregulated in EBB1 overexpressors, suggesting that their
repression by EBB1 might be involved in bud burst induction
(Yordanov et al., 2014). Interestingly, EBB1 overexpression also
Bud break
Dormancy
release
LT
EBB1
FT1 CENL1 GA
Fig. 5 A hypothetical model for the transcriptional control of the release of
bud dormancy and the activation of bud burst in poplar. LT, low temperature;
FT1,FLOWERING LOCUS T; GA, gibberellin; EBB1,EARLY BUD BURST1;
CENL1,CENTRORADIALIS-LIKE1. Prolonged LT induces FT1 expression
and GA biosynthesis, which break dormancy. EBB1 subsequently promotes
meristematic activity and thus bud burst. Through unknown factors, CENL1
represses the release of dormancy and possibly delays bud break. Whether
this signaling pathway also operates in the control of bud burst in other tree
species remains unclear.
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induces precocious bud break in Japanese pear, and PpEBB1
expression peaks shortly before bud enlargement, when levels of
active histone modification (trimethylation of the histone H3 tail at
Lys4) increase in the 50 base pairs upstream and start codon regions
(Tuan et al., 2016). Furthermore, EBB1 can interact with the
promoters of, and induce the expression of, four D-type cyclin
(PpCYCD3) genes in flower buds (Tuan et al., 2016). Accordingly,
EBB1 overexpressors of hybrid poplar have enlarged meristems
(Yordanov et al., 2014), suggesting that it is a regulator of cell
proliferation. Thus, it is highly likely that EBB1 is an important
regulator of cell proliferation and a downstream target of the signal
inducing bud break. Similar functions of EBB1 in spruce, apple,
grapes and peach have been predicted by comparative and
functional genomic analyses (Busov et al., 2016).
VII. Natural variation in the regulation of distinct
stages of annual growth cycles in trees
Genomic and functional genetic analyses are yielding increasingly
detailed insights into the mechanistic aspects of the regulation of
diverse developmental events during the annual growth and
dormancy cycles of trees, as outlined earlier. However, large-scale
sequencing and phenotyping of the genotypes of trees covering
latitudinal clines is also revealing loci that contribute to geograph-
ical variation in the temporal regulation of physiological responses,
such as growth cessation, bud set and bud burst (Ingvarsson et al.,
2006; Pelgas et al., 2011; Evans et al., 2014; Holliday et al., 2016).
These studies are also revealing genetic factors associated with local
adaptation. For example, genetic variation at the FT2 locus in
Populus trichocarpa and PHYB2 loci in European aspen is associated
with variation in the timing of bud set (Ingvarsson et al., 2006;
Evans et al., 2014). Given the indications that these loci participate
in growth cessation, it is not surprising that they have been involved
in local adaptation during the course of evolution. However, the
links between genetic variation at the loci and phenotypic variation
are still correlative rather than mechanistically understood. In
Arabidopsis, allelic replacement can be used to demonstrate and
gain insights into the mechanistic roles of such genetic variation in
phenotypic variation, and the development of such techniques for
tree species would be highly valuable. Thus, natura l variation-based
analyses have considerable promise and, with further technological
breakthroughs, it seems highly likely that they will continue to
increase our knowledge of the genetic control of the annual growth
cycles of trees.
VIII. Conclusions
In conclusion, molecular genetic approaches have provided deeper
insights into the mechanisms involved in the environmental
control of the annual growth cycles of trees. Nevertheless,
substantial gaps remain in our understanding, particularly of the
regulation of post-growth cessation processes, for example the
establishment and release of bud dormancy and the control of bud
burst. Although analyses of model organisms, such as poplar,
spruce and peach, have provided major insights, it remains to be
seen whether these signaling pathways are conserved in other tree
species, such as apple, in which temperature plays a role in growth
cessation and dormancy establishment. It should also be noted that
seasonal growth cycles occur in subtropical and tropical trees, and
the regulation of these cycles warrants attention now that we have
some knowledge of the processes involved in temperate and boreal
tree species. A key aspect of annual growth cycle regulation is that
some traits, for example dormancy release and bud burst, are
quantitative. A major challenge in the future will be to explain the
molecular basis of such quantitative traits. Finally, the integration
of molecular genetics and genomic analyses with more quantitative
approaches (e.g. those used by climate modelers) will facilitate
various other efforts in addition to understanding how trees cope
with seasonal climate changes. Notably, it will aid in the
formulation of breeding programs and/or biotechnological strate-
gies to generate trees that are more productive and more capable of
adapting to anticipated climate changes (Bhalerao et al., 2003),
which are expected to impact the growth cycles and thus
productivity of trees.
Acknowledgements
The work in the laboratory of R.P.B. was funded by grants from
Berzeli/VR, Watbio, the Knut and Alice Wallenberg foundation
and Vetenskapsradet. R.K.S. is a recipient of a post-doctoral
fellowship from the Kempe Foundation.
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... After endodormancy induced by the shortened daylength and lower temperatures in autumn, budburst in temperate trees and shrubs may not occur even in a growth-promoting environment (Campoy et al., 2011;Basler and Körner, 2012;Singh et al., 2017). In the present study, the maximum dormancy generally occurred between 1 October and 3 December for all five study species. ...
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Woody plant species in temperate regions must withstand a cold winter and freezing events through cold acclimation and dormancy in autumn and winter. However, how seasonal changes in dormancy depth and cold hardiness affect the frost risk of temperate species is unclear because few studies have assessed dormancy depth and cold hardiness simultaneously. In this study, an experiment was conducted to estimate the dormancy depth and cold hardiness of five common woody temperate plant species during the winter of 2018/2019 in Beijing, China. Twigs of each species were collected at different dates during winter and the timing of budburst was monitored under the same forcing conditions. The dormancy depth was quantified as growing degree day (GDD) requirements of spring events. Simultaneously, the cold hardiness of buds at each sampling date was determined based on the electrical conductivity of the holding solution. Two indices (chilling accumulation and cold hardiness index) were used to simulate the past dynamics of dormancy depth, spring phenology, and cold hardiness from 1952 to 2021. The maximum dormancy depth of the study species was observed between early October and early December, and thereafter decreased exponentially. The cold hardiness peaked in mid-winter (end of December) through cold acclimation and thereafter decreased in spring (deacclimation). During the past 70 years, the budburst date (first flowering date or first leaf date) of five species was estimated to have advanced significantly, and dormancy depth in early spring was predicted to have increased owing to the warming-associated decrease in chilling accumulation. However, cold hardiness has decreased because of weakened acclimation and accelerated deacclimation under a warming climate. The frost risk before and after budburst remained unchanged because of the reduction in occurrence and severity of low-temperature events and earlier late spring frosts. The present methods could be generalized to estimate and predict the seasonal changes in dormancy depth and cold hardiness of temperate species in the context of climate change.
... The depth of dormancy in perennating buds and the relationship to physiology are seasonally dependent. Photoperiod and temperature signals influence the timing of dormancy onset and release (Cooke, Eriksson, & Junttila, 2012;Singh, Svystun, AlDahmash, Jönsson, & Bhalerao, 2017). We contrasted the seasonal changes in physiology of buds of cultivated table grape in Carnarvon (24° S), which has a subtropical climate, with that of the Swan Valley (31° S), which has a Mediterranean-type climate. ...
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Grapevine (Vitis vinifera L.) is the most widely cultivated fruit crop worldwide, contributing substantially to rural economies. The production cycle and productivity depend on seasonal cues and can range from a strongly deciduous habit in cool‐temperate climates to evergreen in subtropical and tropical climates. The influence of the different seasonal conditions on the dynamics of the perennating bud, including the degree of growth and metabolic quiescence, cell cycle status and internal tissue oxygen status between different climatic zones is largely unknown. This knowledge is important for adapting to changing climate conditions and for crop expansion to wider regions. This study investigated the growth and metabolic physiology of the perennating bud of commercially grown cv. Flame Seedless table grapes from Mediterranean and subtropical climate in Western Australia, from summer until late winter. Climate data were obtained, showing differences in minimum (night) temperature between the two climates, reflected by differences in calculated chilling units. Bud dormancy increased during autumn of both climates;however, the onset and depth of dormancy of buds from the subtropical region were attenuated relative to the Mediterranean condition. Stark contrasts were also observed in metabolism. The respiration of subtropical‐grown buds increased over fivefold during late autumn and winter, while that of Mediterranean‐grown buds increased less than twofold. This was also reflected in less desiccation of the subtropical‐grown buds, and an apparently greater degree of hypoxia within the bud during late winter, prior to bud burst. Collectively, these data show pronounced differences in growth and metabolic physiology of commercially grown table grapes, which provide a foundation for investigating the influence of differing climate and seasonality on the growth and productivity of table grapes and how these may be managed through breeding and agronomy. When grown in a subtropical climate, the energy metabolism of grapevine is dysregulated; the perennating bud shows negligible dormancy, and respiratory metabolism elevates three‐fold during winter, implicating a premature change in source/ sink balance that later manifests in poor production.
... In many tree species, an interaction of photoperiod and chilling is observed, as long photoperiods compensate for lack of chilling in non-chilled or partially chilled trees but have no effect after the chilling requirement has been met (Myking and Heide, 1995;Caffarra and Donnelly, 2010;Meng et al., 2021;Zhang et al., 2021b). However, there is also increasing evidence for an independent role of photoperiod in regulating the endodormancy release and leaf-out in many temperate (Zohner and Renner, 2015;Singh et al., 2016;Fu et al., 2019a;Meng et al., 2021) and subtropical (Zhang et al., 2021b) tree species. In most boreal trees, leaf-out seems to show little sensitivity to photoperiod (Zohner et al., 2016;Richardson et al., 2018). ...
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... Lang's classification is based on whether the period of rest is controlled by physiological signals in the plant, but not in the respective structure (e.g., apical dominance; paradormancy); whether the central control originates from the dormant structure itself (endodormancy); or whether the delay in growth and development is caused by unfavorable environmental conditions (e.g., cold temperatures in spring; ecodormancy) [33]. The transition from paradormancy to endodormancy initiates with the cessation of growth due to declining temperatures and photoperiods [34][35][36]. Leaves and flowers, which ensure regrowth and reproduction in spring, are formed in buds in the previous year [33]. Endodormancy is assumed to be released by the fulfillment of the chilling requirement of the respective cultivar, due to the accumulation of chilling units [37]. ...
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Hydrogen peroxide-converting enzyme activities in leaf buds of the apple cultivar Idared during the transition from dormancy release to the ontogenetic development were investigated. For this purpose, leaf buds were collected from 26 March 2021 (DOY = day of the year 85) to 23 Apirl 2021 (DOY 113) and the air temperature was continuously monitored. Enzyme assay protocols for catalase (CAT), intracellular peroxidase (POX), and cell wall-bound peroxidase (cwPOX) in apple leaf buds were successfully established based on published protocols. All enzymes showed considerable changes in activity during the observation period. Fluctuation in daily mean air temperatures seemed not to affect the activities of POX and CAT, whereas severe drops in daily mean air temperature may have interrupted the assumed trajectory of cwPOX activity during the stage of ontogenetic development. In addition, the importance of considering changes in the ratio between physiologically active tissues and bud scales when investigating physiological changes in buds during the phase of dormancy release and ontogenetic development is discussed. A new reference system, namely the “adjusted dry weight” [aDW], is proposed to circumvent this shift in ratios when working with scaled buds.
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Phenological models have become a vital tool for predicting future phenological responses to global climate change. Recently, machine learning (ML) has been used successfully to develop phenological models based on ground observations. However, fitting an observation series that has been observed for only a few years (or even a decade) can easily lead to overfitting, and it is still a great challenge to predict future phenology accurately based on a short observation series. Here, based on historical ground phenological observations, we construct an ML‐based binary classification phenological model that can be applied to temperate trees. We thoroughly describe the construction process of a species‐specific ML‐based binary classification phenological model that is suitable for phenological predictions in both spring and autumn. Through experiments, we evaluate 18 commonly used ML classification algorithms and the effects of two parameters on the prediction performance of the model. Finally, we compare the performance between the binary classification model and six widely used ecophysiological models for accuracy of spring phenological prediction. The median root mean square error (RMSE) of the binary classification model for the first flowering date (93 observation series) was only 2.99 days, which proves that it is a good method of phenological prediction for temperate trees. This model can effectively overcome the insufficient sample size of ground observations for specific species and provide new insights of phenological predictions for tropical and subtropical trees. The comparison of different ML algorithms showed that the median root mean square errors of the six algorithms were <3.5 days, and lower than those of six ecophysiological models (>3.7 days) in prediction of spring phenology. In addition, this model can help us to infer plant physiological mechanisms and drivers of phenological change and provide more accurate predictions of plant phenological responses to climate change.
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We established Silver birch phenology in the Pyrenees. We highlight real evapotranspiration as the main driver and the altitudinal effect within a north-south phenological pattern. Summary We have established the buds, leaves, and cambium activity phenological calendar of Betula pendula Roth. based on detailed ground weekly records for two years (2000-2001) in the Pyrenees. Using band dendrometers, we determined the growing period of stem radial growth, and the variation of the growth rates. The cumulative radial growth was characterized with the Gompertz model. We determined the effect of climatic variables on stem growth rates in diameter. Using data from different authors, we established a latitudinal phenological gradient along Europe. The most important cues for bud burst are heat accumulation (base temperature 5ºC) and long days that reduced the thermal time to budburst. The leaves' longevity, the period of stem cambial activity, and the variation of the stem radial growth rates throughout the year are mainly regulated by the actual evapotranspiration. We verified that leaves yellowing and shedding to advance if the hydric stress is pronounced. The latitudinal gradient of phenological events is not lineal. Spring phenology in the Pyrenees was delayed in relation to birches in central and Northern Europe due to the altitudinal effect on the birches of the Pyrenees. The south-north gradient of the maximum growth rate in diameter is not pronounced. In the Pyrenees, the cessation of stem growth in diameter takes place on similar dates to Northern Europe and earlier than in Central Europe due to water stress. The main effect of climate change might be a shorter growing period, earlier budburst but earlier growth cessation due to water stress.
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Geophytes develop underground storage organs, which help them to survive extreme environments. Besides energy resources for plants and humans, they are widely used for vegetative propagation. Naturally, these storage organs are sink tissues during the active growth cycle of the plant, but they turn into a source during vegetative propagation. Synchronized dormancy and sprouting with the environment are crucial for plant fitness and maximum yield. The active metabolic status of an underground vegetative organ determines its developmental fate. Sugars are the main components of storage organs; thus, their dynamics play an important role in controlling the dormancy-activity cycle of geophytes. Dormant buds require carbon sources (sugar) to promote growth, and the plant adjusts sugar metabolism between storage and soluble sugars to maintain dormancy and sprouting. In recent years, sugars and their derivatives, besides energy molecules, have also been considered signaling molecules involved in several plant developmental processes, including vegetative dormancy and growth. This review discusses current knowledge on the role of sugars in regulating and controlling dormancy and sprouting in geophytes. It’s regulation by external environmental factors, hormonal regulation and cross-talk. It also outlines how similar or different the regulatory mechanism controlling geophyte dormancy and sprouting is, compared to seed dormancy and germination and seasonal/annual growth in perennials that undergo dormancy-activity cycles.
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Plant dormancy has a major impact on the cultivation of plants, influencing such processes as seed germination, flowering, and vegetative growth. The diversity of plant tissues that exhibit, or contribute to the manifestation of, dormancy is great, and there appear to be numerous mechanisms of dormancy induction or release. This complexity was discussed by Romberger (55) nearly 25 years ago. Yet his analysis of the unresolved challenges in dormancy research is still valid today, for the overall understanding of dormancy is limited. This lack of understanding may be due, in part, to the abundance of terminology that has arisen without a nomenclatural framework in which to classify and relate the events being described.
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In the article “Endo-, Para-, and Ecodormancy: Physiological Terminology and Classification for Dormancy Research” by Gregory A. Lang, Jack D. Early, George C. Martin, and Rebecca L. Darnell ( HortScience 22:371–377, June 1987), in the second column of Table 5 under part III-B (paradormancy), the term “Cryogenic endodormancy” should be changed to “Cryogenic paradormancy”.
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The timing of the onset and release of dormancy impacts the survival, productivity and spatial distribution of temperate horticultural and forestry perennials and is mediated by at least three main regulatory programs involving signal perception and processing by phytochromes (PHYs) and PHY-interacting transcription factors (PIFs). PIF4 functions as a key regulator of plant growth in response to both external and internal signals. In poplar, the expression of PIF4 and PIF3-LIKE1 is upregulated in response to short days, while PHYA and PHYB are not regulated at the transcriptional level. Integration of light and environmental signals is achieved by gating the expression and transcriptional activity of PIF4. During this annual cycle, auxin promotes the degradation of Aux/IAA transcriptional repressors through the SKP–Cullin-F–boxTIR1 complex, relieving the repression of auxin-responsive genes by allowing auxin response factors (ARFs) to activate the transcription of auxin-responsive genes involved in growth responses. Analyses of transcriptome changes during dormancy transitions have identified MADS-box transcription factors associated with endodormancy induction. Previous studies show that poplar dormancy-associated MADS-box (DAM) genes PtMADS7 and PtMADS21 are differentially regulated during the growth-dormancy cycle. Endodormancy may be regulated by internal factors, which are specifically localized in buds. PtMADS7/PtMADS21 may function as an internal regulator in poplar. The control of flowering time shares certain regulatory hierarchies with control of the dormancy/growth cycle. However, the particularities of different stages of the dormancy/growth cycle warrant comprehensive approaches to identify the causative genes for the entire cycle. A growing body of knowledge also indicates epigenetic regulation plays a role in these processes in perennial horticultural and forestry plants. The increased knowledge contributes to better understanding of the dormancy process and consequently to precise manipulation of dormancy-related horticultural traits, such as flowering time.
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Morphological and anatomical changes in shoots of vigorously growing cottonwood plants (Populus deltoides Bartr.) were studied during dormancy induction in 8-hr short days (SD) and in control plants grown in 18-hr long days (LD). Pronounced structural changes occurred in terminal buds after 4 wk and full dormancy was achieved in 7 wk of SD. Leaf expansion ceased after 5 wk of SD as foliage leaves matured to the terminal bud base at leaf plastochron index 0 (LPI 0). Within the bud, total leaf length (lamina + petiole) decreased and stipule length increased progressively each week; thus, the ratio total leaf length/stipule length decreased rapidly, especially at the position of incipient bud-scale leaves LPI - 1 and LPI - 2. These bud-scale leaves were fully developed by wk 6 and were derived from enlarged stipules and aborted laminae. The full complement of primordia within the bud at the start of SD eventually matured as foliage leaves and the first bud-scale leaf (LPI - 1) was initiated immediately following transfer to SD. Acropetal advance of the primary-secondary vascular transition zone (TZ) was associated with leaf maturation. However, it did not advance throughout the entire vascular cylinder as in LD, but only in those leaf traces serving mature leaves beneath the terminal bud. In both LD and SD treatments the same linear relationship was maintained between LPI of the TZ and LPI of the most recently matured leaf; both parameters simultaneously increased in LD and decreased in SD. Thus, the relationship between leaf maturation and advance of the TZ was maintained irrespective of environment.
Article
The purpose of this study was to determine the influence of temperature applied during short day-induced budset on induction of dormancy in six ecotypes of Betula pubescens Ehrh. and two ecotypes of Betula pendula Roth. Seedlings were grown in a phytotron at constant temperatures of 9–21°C under a 12 h photoperiod (SD) during dormancy induction. Induction of dormancy was monitored by following bud flushing and shoot growth after transfer to long photoperiod conditions (24 h) at 18°C. Chilling requirement was studied in seedlings exposed to 10 weeks of SD. In both species induction of bud dormancy developed most rapidly at 15–18°C, and both 9–12°C and 21°C delayed the induction of dormancy. Raising the temperature (from 9 to 21°C) applied during induction of dormancy significantly increased the chilling requirement. These responses were noted for all ecotypes tested, but in general the northern ecotypes entered dormancy more quickly than the southern ones. No such trend was recorded for chilling requirement, although a B. pubescens ecotype from Iceland and another from the coast of northern Norway appeared to require a longer chilling treatment than the other ecotypes. In conclusion, induction and depth of bud dormancy in birch are significantly affected by temperature conditions and these effects may explain some of the annual variation in dormancy and chilling requirement observed in nature.
Article
In the Japanese pear (Pyrus pyrifolia Nakai) ‘Kosui’, three developmental stages of lateral flower buds have been proposed to occur during ecodormancy to the flowering phase, i.e., rapid enlargement, sprouting, and flowering. Here, we report an APETALA2/ethylene responsive factor (AP2/ERF) transcription factor, named EARLY BUD-BREAK (PpEBB), which was highly expressed during the rapid enlargement stage occurring prior to the onset of bud break in ‘Kosui’ lateral flower buds. Gene expression analysis revealed that PpEBB expression was dramatically increased during the rapid enlargement stage of ‘Kosui’ lateral flower buds in three successive growing seasons. PpEBB transcript levels peaked 1 week prior to onset of bud break in ‘Kosui’ potted plants treated with hydrogen cyanamide or water under forcing conditions. Chromatin immunoprecipitation quantitative polymerase chain reaction showed that higher levels of active histone modifications (trimethylation of the histone H3 tail at lysine 4 [H3K4me3]) in the 5′-upstream and start-codon regions of the PpEBB gene were associated with the induced expression level of PpEBB during the rapid enlargement stage of ‘Kosui’ lateral flower buds. In addition, we provide evidence that PpEBB may interact with and regulate four D-type cyclin genes (PpCYCD3s) during bud break in ‘Kosui’ lateral flower buds. PpEBB significantly increased the promoter activities of four PpCYCD3 genes in a dual-luciferase assay using tobacco leaves. Taken together, our findings uncovered aspects of the bud break regulatory mechanism in the Japanese pear and provided further evidence that the EBB family plays an important role in bud break in perennial plants.