Journal of Experimental Botany, Vol. 67, No. 11 pp. 3189–3203, 2016
doi:10.1093/jxb/erw138 Advance Access publication 6 April 2016
DARWIN REVIEW
On the language and physiology of dormancy and
quiescence in plants
Michael J. Considine1,2,3,* and John A. Considine1
1 School of Plant Biology, and The Institute of Agriculture, The University of Western Australia, Perth, WA 6009 Australia
Department of Agriculture and Food Western Australia, South Perth, WA 6151 Australia
3 Centre for Plant Sciences, University of Leeds, Leeds, Yorkshire LS2 9JT, UK
2 * Correspondence: [email protected]
Received 12 October 2015; Accepted 14 March 2016
Editor: Christine Foyer, Leeds University Abstract
The language of dormancy is rich and poetic, as researchers spanning disciplines and decades have attempted to
understand the spell that entranced ‘Sleeping Beauty’, and how she was gently awoken. The misleading use of ‘dormancy’, applied to annual axillary buds, for example, has confounded progress. Language is increasingly important
as genetic and genomic approaches become more accessible to species of agricultural and ecological importance.
Here we examine how terminology has been applied to different eco-physiological states in plants, and with pertinent
reference to quiescent states described in other domains of life, in order to place plant quiescence and dormancy
in a more complete context than previously described. The physiological consensus defines latency or quiescence
as opportunistic avoidance states, where growth resumes in favourable conditions. In contrast, the dormant state in
higher plants is entrained in the life history of the organism. Competence to resume growth requires quantitative and
specific conditioning. This definition applies only to the embryo of seeds and specialized meristems in higher plants;
however, mechanistic control of dormancy extends to mobile signals from peripheral tissues and organs, such as the
endosperm of seed or subtending leaf of buds. The distinction between dormancy, quiescence, and stress-hardiness
remains poorly delineated, most particularly in buds of winter perennials, which comprise multiple meristems of differing organogenic states. Studies in seeds have shown that dormancy is not a monogenic trait, and limited study
has thus far failed to canalize dormancy as seen in seeds and buds. We argue that a common language, based on
physiology, is central to enable further dissection of the quiescent and dormant states in plants. We direct the topic
largely to woody species showing a single cycle of growth and reproduction per year, as these bear the majority of
global timber, fruit, and nut production, as well being of great ecological value. However, for context and hypotheses,
we draw on knowledge from annuals and other specialized plant conditions, from a perspective of the major physical,
metabolic, and molecular cues that regulate cellular activity.
Key words: Bud, cell cycle, chromatin accessibility, dormancy, meristem, oxygen and redox signalling, plant, quiescence,
seasonality, seed.
Introduction
The language of dormancy and quiescence confers an ethereal
state. Adjectives abound, such as enigmatic and cryptic, as do
synonyms (see Table 1), but far more significant is the lack
of descriptors, measurable and testable, let alone a universal
or consensus physiology that define the phenomena. While
differentiation and senescence have definable characters that
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3190 | Considine and Considine
Table 1. Context-specific and generic terms related to quiescence and dormancy across cellular forms of life
Term
Acclimation
Definition and context
The physiological adjustment (plasticity) to environmental change to enable stress resistance.
Relates to the individual, as distinct from adaptation, which considers an evolutionary time
scale. For ‘stage I’, ‘stage II’ acclimation, see Rinne et al. (2001).
Dormancy
A developmental and entrained state of quiescence within a viable and intact meristematic
or embryonic organ. Growth is incompetent to respond to favourable conditions until after
sufficient entrainment by environmental cues.
Syn. endodormancy, true dormancy, physiological dormancy, primary dormancy, constitutive
dormancy, summer dormancy, rest, over-wintering.
Secondary dormancy
Acquired state of dormancy in already dispersed seed exposed to unfavourable conditions,
which may involve temperature, light, oxygen, or water stress. May or may not have been
imbibed. Has scarcely been described in perennial buds to date.
Physical dormancy
State of dormancy in which a physical barrier to the external environment is major limitation to
growth. For example, a seed coat that is impermeable to water or oxygen. We define this as a
mode of dormancy, as in many cases the physical barrier is not the sole limitation, but may be
source of biochemical repression.
Diapause
A programmed state of developmental arrest in vertebrate and invertebrate animals, usually in
response to a number of environmental stimuli that precede unfavourable conditions. The term
has been specifically applied to the state of the embryo but also more widely.
After-ripening
A period of entrained relief from dormancy under relatively dry conditions. May interact with
temperature or light cues according to species.
Quiescence
A condition of repressed rate of cell division which can be relieved immediately upon relief from
the source of repression. May refer to the cell, organ, organism, or community, or where the
source of repression is internal or external. Excludes senescing or terminally differentiated cells.
Correlative repression
1.A viable and intact and attached meristematic organ which is repressed by mobile signals
derived from another organ(s) of the organism.
Syn. paradormancy, apical dominance.
2.Repressed cell division and differentiation of quiescent centre stem cells by mobile signals
from adjacent proliferative cells.
Cryptobiosis
A reversible state with no visible signs of life and near metabolic inactivity.
Syn. ametabolism, abiosis, anabiosis.
Desiccation tolerance
A state of extreme but reversible desiccation, at hydration contents below 0.3g H2O g DW−1.
Syn. anhydrobiosis.
Osmobiosis
A state of repressed growth under conditions of high osmotic concentration. Has seldom been
applied in the absence of other terms or factors such as desiccation, and where that factor has
defined the authors’ approach.
Anoxybiosis
A state of repressed growth of an aerobic organism under conditions of low or zero oxygen.
Has seldom been applied in the absence of other terms or factors such as desiccation, and
where that factor has defined the authors’ approach.
Syn. anaerobiosis.
Metabolic depression
A state or reduced metabolism, commonly 5–40% of resting metabolic rate, induced in
response to, or anticipation of adverse environmental conditions or famine. Has been applied to
conditions such as diapause.
Syn. metabolic arrest, hypometabolism.
Thermal depression
A state of metabolic depression in animals under conditions of low or high ambient temperature.
Syn. cryobiosis, aestivation, torpor.
Stationery phase
The net cessation of population growth. Typically applied to unicellular organisms. Applies to
the population, not necessarily all individuals. Typically defined by optical density of the culture
as no detectable increase in OD600. Not confused with the post-diauxic shift.
Syn. saturation phase.
The hypothetical quiescent stage of the cell cycle. It is indistinguishable from G1 and defined
G0
only by the reversible absence of cell cycle division or delay in cell cycle progression.
Syn. cell cycle arrest, noting caution by Coller (2007).
Stemness, stem cell,
An undifferentiated proliferative cell which divides asymmetrically to produce at least one
initial cell
daughter stem cell and is able to divide to give rise to a differentiated cell type, noting that the
latter may undergo further division before terminal differentiation.
Quiescent centre (root), An undifferentiated cell or pool of cells which have a relatively slow mitotic rate and give rise to
organising centre (shoot) a stem cell.
Stem cell niche
A defined anatomical compartment comprising the cellular and extracellular components that
integrate local and systemic signals which regulate stem cell identity.
References
Thomashow (1999); Rinne et al.
(2001); Vitasse et al. (2014); Seo and
Mas (2015)
Amen (1968); Bewley and Black
(1994)
Bewley and Black (1994); Hilhorst
(2010)
Bewley and Black (1994)
Renfree and Shaw (2000); Podrabsky
and Hand (2015)
Bewley and Black (1994)
Keilin (1959); O’Farrell (2011)
This reference
Keilin (1959); Withers and Cooper
(2010)
Keilin (1959); Potts (1994); Leprince
and Buitink (2015)
Keilin (1959); Withers and Cooper
(2010)
Keilin (1959); Withers and Cooper
(2010)
Guppy and Withers (1999); Withers
and Cooper (2010)
Abbott (1885); Withers and Cooper
(2010)
Gershon and Gershon (2000);
Roostalu et al. (2008)
Coller (2007); Cheung and Rando
(2013)
Scheres (2007)
Scheres (2007)
Scheres (2007)
Subordinate terms are indented, i.e. secondary dormancy is subordinate to dormancy, with the exception that we consider all modes of
dormancy subordinate to quiescence.
The language and physiology of dormancy and quiescence | 3191
translate across cellular and multicellular models, quiescence
continues to intrigue researchers across kingdoms of life, even
within the more well-defined eukaryotic systems such as yeast,
insect, or human. In this regard, Theodosius Dobzhansky’s
assertion ‘nothing in biology makes sense except in the light
of evolution’ (1973) seems to be an appropriate epithet. Here,
we do not seek to define unifying modes of dormancy or quiescence, but to define the physiological distinction between
these two broader conditions, within which previous authors
have adequately defined subdivisions of dormancy in the seed
(Baskin and Baskin, 2004) and bud (Lang et al., 1987).
It is difficult to resolve when the terms quiescent (Latin
quietus, meaning at rest) or dormant (Latin dormire, meaning to sleep) first came to the study of biology; however, a
wonderful anthology is presented by David Keilin (1959) in
his Leeuwenhoek Lecture. Keilin credits the original insights
to the inventor of the microscope himself (van Leeuwenhoek,
1702, pp. 207–213). Tellingly though, van Leeuwenhoek did
not name this condition of his so-called animalcules (rotifers,
microscopic aquatic animals), which could revive after a
period of imposed desiccation. In stark contrast, by the time
of his lecture, Keilin felt it necessary to clarify confusion that
had arisen from the expansion or corruption of terms. He
cites ‘anabiosis’, coined by Wilhelm Preyer, and ‘latent life’,
by Claude Bernard, both in the late 1800s, as the earliest
terms defining a lifeless and viable organism… in a state of
absolute chemical indifference (see Keilin, 1959, pp. 165–166;
note, Preyer’s anabiosis actually referred to resurrection from,
rather than the lifeless state itself). Keilin also noted a number
of alternative terms and even coined one other, ‘cryptobiosis’, as he attempted to distinguish the various terms (Keilin,
1959, pp. 166–167). As we shall see, parallel conundrums have
vexed authors across biological disciplines. This is illustrated
in breadth in the text by Lubzens and colleagues (2010), which
was the outcome of a European Commission project named
‘Sleeping Beautyֹ’. Therein, the contributors tried more to
highlight the diversity than to seek an over-riding conceptual
resolution. Another excellent book, though confined to the
animal world, was published by Navas and Carvalho (2010).
In the plant domain, ‘quiescence’ associated with desiccation tolerance was the subject of a recent journal special issue
(Leprince and Buitink, 2015).
In this review, we give an overview of the historical and
ecological contexts of quiescence and dormancy, with primary attention to perennial plants and the terminology used
to define quiescent states in the bud and seed. Elucidating the
physiology of these phenomena remains a priority for future
research. For this, we need testable and measurable definitions at the cell, organ, and organism levels. Table 1 expands
Keilin’s own table of terminologies, and in many ways this
review begins where Keilin finished. Throughout the following discussion, terms used in their correct context as defined
in Table 1 are in bold text, otherwise the terms appear in
inverted commas.
As a foundation for these discussions, we begin with simple
definitions. Quiescence is a condition of repressed cell division (i.e. it is opportunistic and can resume division without
delay). Quiescence may also refer to a cell, organ, or whole
plant, as for example in resurrection plants. In contrast, dormancy is a quantitatively entrained state of quiescence, and,
as we define it, is exclusively seen in meristematic or embryonic organs of multicellular plants.
A diversity of terms and states; many paths
to the same phenotype
It is clear from the archaeological records that various strategies of quiescence are represented in basal life forms including
prokaryotes, preceding the Cambrian explosion of multicellular life (see, for example, Potts et al., 2005; Watanabe et al.,
2009; O’Farrell, 2011). Quiescence appears to have played an
important role in enabling species to occupy more diverse
ecological niches. This is discussed by Jones and Lennon
(2010) in terms of the contribution that ‘dormancy’ (quiescence) makes to species diversity and richness in microbial
communities. Many contexts in which we commonly discuss quiescence and dormancy appear to have derived independently, and evidence from extensive studies to define the
genetic basis of dormancy in seeds suggests that dormancy is
not a linear pathway, governed by single genes or even gene
ontologies (Alonso-Blanco et al., 2003; Clerkx et al., 2004b;
Bentsink et al., 2010).
Although Keilin refers to both ‘quiescence’ and ‘dormancy’,
the terms have become more prominent since. ‘Dormancy’
drew the interest of cancer researchers during the 1950s after
James Craigie showed that sarcoma from mice, guinea-pig,
or rat could retain viability and malignancy after years of
−70 °C storage, an insight that was related to the resumption of cancerous growth after years of patient remission (see
Hadfield, 1954). Perhaps even more attention was brought to
the biological importance of quiescence though, through the
therapeutic potential of pluripotent stem cells, as recognized
in the 1970s (see, for example, Brecher, 1977; Hellman et al.,
1978). The terms ‘dormancy’ and ‘quiescence’ have continued to proliferate in the present scientific literature on these
topics. Defining these terms experimentally, however, remains
a challenge. Keilin and others, particularly in animal studies, have expressed a preference for other terms, distinguishing two primary terms: cryptobiosis, referring to an extreme
physiological state with no activity and no apparent metabolism; and ‘dormancy’, referring to a more benign state of
depressed metabolism (Keilin, 1959; Withers and Cooper,
2010). Curiously Keilin grouped diapause with this benign
definition, despite the wealth of literature even then on the
rhythmic behaviour of, for example photoperiodism, which is
observed across several kingdoms (Way et al., 1949; Wareing,
1956; Heldmaier et al., 1989; Battey, 2000), and which we see
as congruent with the behaviour of dormancy in seeds and
perennial meristems in plants.
At the cellular level, authors refer to a definition of
‘reversible absence of proliferation’, although recognizing that the term reversible may be misleading in a context
where quiescence or dormancy is developmental and requires
maintenance (Coller, 2011; Daignan-Fornier and Sagot,
2011). Several studies have attempted to define a ‘quiescence
3192 | Considine and Considine
programme’ (see, for example, Gray et al., 2004; Coller
et al., 2006; Yanagida, 2009; Cheung and Rando, 2013), or
from another perspective the ‘desiccome’ (Potts et al., 2005).
Although some authors find common features, for example
the transcriptome of desiccating yeast resembles expression
during the stationary phase (Singh et al., 2005), others identify considerable temporal and conditional differences (Coller
et al., 2006; Coller, 2011; O’Farrell, 2011).
So, to consider the plant literature. Samish (1954) recognized that ‘dormancy’, ‘quiescence’, and ‘rest’ had been used
interchangeably. Samish argued that ‘dormancy’ was the
generic term for a transient suspension of growth, while ‘quiescence’ and ‘rest’ were more biologically meaningful. He distinguished the two latter terms by the conditions that induced or
governed them; ‘quiescence’ was induced or relieved by external, environmental constraints, while ‘rest’ was constrained
by internal factors (Samish, 1954, p. 183). Clearly, however,
Samish was not resolved. In distinguishing between ‘rest’, as
seen in deciduous trees, and cyclical growth in evergreens, he
returned to an environmental constraint, chilling. Further, he
noted that even the distinction between correlative repression
and ‘rest’ was not sharp. Subsequently, however, Vegis (1964)
returned to using the terms ‘dormancy’ and ‘rest’ interchangeably, describing ‘pre-dormancy’ (=‘pre-rest’), ‘true dormancy’
(=‘main-rest’), and ‘post-dormancy’ (=‘after-rest’). There,
the conditions of the organ in ‘pre-’ or ‘post-dormancy’ were
latent, and only constrained by unfavourable environmental
conditions. During ‘true dormancy’, Vegis argued that the
organ could not be induced to grow by any means (Vegis,
1964, p. 188). Meanwhile, Doorenbos (1953) preferred ‘winter
dormancy’ and ‘summer dormancy’, and Amen (1968) cited
even further examples of confounded terminology before settling on a distinction between ‘constitutive dormancy’ and
‘exogenous dormancy’ (=‘true dormancy’ or ‘post-dormancy’
according to Vegis), as described by Sussman and Halvorson
(1966). Here ‘constitutive dormancy’ was a state of suspended
development controlled by an innate property such as a barrier to nutrition or the presence of a repressor. Still unsatisfied,
other authors have continued to re-define dormancy, as we find
ourselves now. Lang and colleagues (1987) described ‘endo-’,
‘para-’, and ‘eco-dormancy’. Baskin and Baskin (2004)—in
homage to Russian seed physiologist Marianna Nikolaeva—
described five main strata under physiological, morphological,
and physical criteria, while Bewley (1997) and others since have
preferred the more simple definition; failure of an intact and
viable organ to resume growth under favourable conditions.
This latter definition satisfies biologists of both seed and perennial buds, with occasional refinement according to Baskin
and Baskin (2004) or Lang and colleagues (1987), respectively.
In spite of this apparent consensus, the plant literature bears
several even recent examples of ambiguous use of the term
‘dormancy’, particularly in relation to axillary buds of species
such as pea or Arabidopsis, which display no dormancy per se,
only apical dominance; that is, correlative repression or paradormancy according to Lang et al. (1987).
We consider four biophysical forces as being particularly
important for the development of quiescent strategies, including dormancy; water, oxygen, temperature, and light, or rather
desiccation, hypoxia, thermal, and photoperiod. In addition,
nutrition, hormones, and other mobile elements play key roles
as positional cues, while the epigenetic code is a key medium
between the physical environment and cellular state that enables coarse and fine tuning of gene expression. We have structured this review to articulate the central features of each of
these influences, as they relate to how we define the physiological states of quiescence and dormancy in plants. Figure 1
Fig. 1. Overview of the major states of dormancy and quiescence across kingdoms, and the conditions that define them. Epigenetic regulation may
mediate each of these conditions, but we consider epigenetic modification as a key component of entrainment. See Table 1 for definitions. (This figure is
available in colour at JXB online.)
The language and physiology of dormancy and quiescence | 3193
depicts the relationship among key terms that apply across
domains of life and conditional distinctions between them.
Desiccation tolerance and longevity
It is likely that periodic desiccation and rehydration was a
critical evolutionary force in the development of quiescence
across kingdoms (Potts et al., 2005). In the plant domain, it
is suggested to have co-evolved with the transition to life on
the land (Waters, 2003). The capacity for desiccation tolerance
is evident in even basal prokaryotes, fungi, protists, bryophytes, and in certain vascular plants, as well as arthopods
and fish. It was the subject of van Leeuwenhoek’s intrigue
with rotifers (van Leeuwenhoek, 1702), and termed ‘anhydrobiosis’ by Keilin (1959). Here we prefer desiccation tolerance.
Alpert (2000) constrained the definition to the adult form;
however, this precludes much of the relevant discussion on
quiescence and dormancy as seen in seeds, pollen, spores, and
buds, which display many of the hallmarks of desiccation
tolerance described in other domains of life. Nevertheless,
adult lichens and bryophytes, some ferns, and a few angiosperms have adapted quiescent mechanisms to survive desiccation for several years (Alpert, 2000, and references
therein). In this context, however, the state is opportunistic,
as metabolic activity and growth resume upon rehydration,
and hence we define these strategies as quiescence and not
‘dormancy’. Across the plant domain, desiccation tolerance
has been reviewed previously (see, for example, Buitink and
Leprince, 2004; Angelovici et al., 2010; Farrant and Moore,
2011), and described in the aforementioned journal special
issue (Leprince and Buitink, 2015).
Desiccation tolerance in seeds is highly correlated with dormancy, while sensitive species predominate in moist, aseasonal, vegetative habitats (Tweddle et al., 2003). Quiescence
associated with desiccation tolerance appears to confer or
be associated with the resistance to various other classes of
environmental stresses, which confounds the quest for causal
associations. Tweddle and colleagues (2003) were cautious to
indicate that desiccation tolerance was not causally associated with seed dormancy, although a desiccation-sensitive but
dormant seed would suffer negative selection pressure. When
viewed in the context of molecular water as a biochemical
requirement, the cellular alterations that define desiccation
tolerance provide the structural and conformation stability
that enable cross-tolerance to other environmental extremes.
Many of the processes associated with the acquisition of
desiccation tolerance involve the synthesis of compatible solutes that enable biophysical adjustments which maintain a
structural order within the cell. The result is often termed a
glassy state; that is, a physical solid but thermodynamic liquid (Buitink and Leprince, 2004). Compatible solutes maintain the structural integrity of proteins in one of two modes
depending on the degree of cellular desiccation: first by preferential exclusion of incompatible solutes and thereby maintaining the protein hydration; and, at levels below 0.3 g H2O g
DW−1, by chemically displacing the hydrogen bonds lost. This
maintains the ability of proteins to resume function upon
rehydration, as well as maintaining turgor in order to prevent
the collapse of cell and organelle membranes (Buitink and
Leprince, 2004; Farrant and Moore, 2011). Energy metabolism is necessarily slowed as viscosity increases, while antioxidants accumulate in order to counter the chemical generation
of molecular free radicals associated with Haber–Weiss and
Fenton reactions, or with Maillard and Amadori reactions
(Murthy and Sun, 2000; Potts et al., 2005; Angelovici et al.,
2010).
The seed of several mutants of Arabidopsis, retarded in
their ability to tolerate desiccation, also confer reduced sensitivity to abscisic acid (ABA), vivapary, and/or partly or
completely fail to acquire a dormant state (Angelovici et al.,
2010). For example, mutants of the ABA-INSENSITIVE
(ABI), LEAFY COTYLEDON (LEC), and FUSCA (FUS)
loci remain green on maturation, do not develop dormancy,
vary in their sensitivity to desiccation, and lose viability more
quickly during dry storage (Ooms et al., 1993; Wolkers et al.,
1998; Clerkx et al., 2004a). Although the abi3-1 mutant develops equivalent desiccation tolerance to the wild-type seed,
the seed deteriorate faster than those of the wild type when
stored for longer periods (Clerkx et al., 2004a). This raises
the question: is seed dormancy related to longevity? The seed
of some species are capable of remaining viable in a desiccated state for over a thousand years, although it is unlikely
they were dormant throughout, and reproductive fate was
unclear (Porsild et al., 1967; Sallon et al., 2008). More typically, long-term storage of seed results in reduced viability
associated with a loss in membrane integrity, lipid peroxidation, and accumulation of damage to proteins and nucleic
acids (Bewley, 1997; Waterworth et al., 2015). Early during
imbibition, damaged DNA is repaired prior to the resumption of the cell cycle (reviewed by Waterworth et al., 2015).
It appears logical that desiccation tolerance and dormancy
may both serve to protect and preserve macromolecules and
repair machinery. However, data from Nguyen and colleagues
(2012) indicate a negative relationship between dormancy and
seed longevity. In a long-term seed ageing study from recombinant inbred populations of Arabidopsis ecotypes, four of
the GERMINATION ABILITY AFTER STORAGE (GAAS)
loci overlapped or were in close proximity to DELAY OF
GERMINATION (DOG) loci. For example, the GAAS5 and
DOG1 loci were shown to reflect the same gene, while GAAS6
was proximal to the DNA LIGASE IV (LIG4), a key DNA
repair enzyme, mutants of which display severely retarded
longevity (Waterworth et al., 2010). These insights suggest
a fitness cost to dormancy, beyond that of the more passive
quiescence.
Oxygen and redox cues
The role of physiological oxygen tension (pO2) in shaping the
evolution of the meristem and plant embryo has yet to be
argued. pO2 plays a crucial role in defining the stem cell niche
across multicellular life. Reactive oxygen and nitrogen species
(ROS and RNS) are a central counterpart to pO2 in establishing or maintaining quiescence, and during resumption of
development (Considine and Foyer, 2014). The relationship
3194 | Considine and Considine
of pO2 and dormancy, as we define it here, requires further
investigation. Current literature suggest a complex interplay
of oxygen, ROS, RNS, and plant hormones (Gapper and
Dolan, 2006; Considine and Foyer, 2014).
Oxygen was a crucial evolutionary force shaping multicellular life. Recent geochemical data suggest that even after
the Great Oxidation Event ca. 2.1–2.4 billion years ago, the
oxygen and reduction/oxidation (redox) environments of the
oceans and atmosphere were too variable to support multicellular life, until after a further rise and stabilization, late in
the Proterozoic era, ca. 600 million years ago (Canfield and
Teske, 1996; Lyons et al., 2014); that is, despite evidence of
photosynthetic oxygen synthesis nearly 2 billion years previously. Current hypotheses suggest that the embryophytes and
the innovation of the meristem, branching, and patterning,
which are intrinsically linked to many modes of quiescence
in plants, arose ~450 million years ago (Ligrone et al., 2012;
Tomescu et al., 2014). Such recent evolution was the subject of Charles Darwin’s ‘abominable mystery’ (Darwin and
Seward, 1903; Friedman, 2009).
An understanding of the physiological role of hypoxia in
defining the stem cell niche was critical to the successful culture of animal stem cells, underpinning the revolution in stem
cell biology and medicine (Mohyeldin et al., 2010). While the
language of hypoxia deserves its own review, there is increasing acknowledgement that a degree of hypoxia (pO2 <21 kPa)
is physiologically normal (Mohyeldin et al., 2010).
It is accepted in animal biology that local tissue hypoxia
plays a central role in development and in disease (Webster,
2007). Multicellular plants differ by lacking a soluble oxygen carrier (with few exceptions, for example nitrogen-fixing
nodules of legumes), or an active vascular system. Yet, many
plants have highly dense tissues and organs, often with internal
boundaries to oxygen diffusion, as well as spatially and temporally variable metabolic rates. Many organs such as fruits
and seed are developmentally disposed to hypoxia (Considine
and Foyer, 2014; see Table 1 therein). Notwithstanding any
barriers to oxygen, the rate of diffusion is ~10 000-fold
slower in water than in air, creating extreme gradients in pO2,
where, for example, the meristem of submerged roots must be
hypoxic (Armstrong et al., 2009). In this context, it is remarkable that the primary components of plant oxygen signalling
were only revealed recently; a so-called N-end rule of proteolysis (Gibbs et al., 2011; Licausi et al., 2011).
The quiescent seed of many species (Borisjuk and
Rolletschek, 2009) and, more recently, the perennial bud of
grapevine (Meitha et al., 2015), bear an internal gradient of
pO2 towards a hypoxic core. The earlier literature suggests
that the permeability of the seed coat or bud scale to oxygen is not functionally related to dormancy per se, although
several authors report accelerated germination resulting from
removal of the outer seed coat or bud scale, or exposure to
elevated pO2 (Romberger, 1963; Amen, 1968; Edwards, 1969;
Chen, 1970). For most species, we define this as physical
dormancy (Bewley and Black, 1994; see Table 5.2 therein).
However, it is questionable whether the physical constraint
is the sole consideration, even for mutants with weakened
testa (Debeaujon et al., 2000). As an illustration, removal
of the aleurone layer of Arabidopsis or barley seed results
in increased degradation of ABA and subsequent germination (Bethke et al., 2007). This indicates that the seed coat
or aleurone layer in some species is a mechanistic source of
repressive agents, which are released by the entrainment that
overcomes dormancy. This effect was prevented by hypoxia
(Benech-Arnold et al., 2006) or scavengers of nitric oxide
(NO) (Bethke et al., 2007).
A role for glucanases in mediating physical dormancy in
seeds has been argued previously (Leubner-Metzger, 2002).
Two recent studies have added to the mechanistic understanding of tissue-specific regulation of cell wall metabolism in
physical dormancy. Jang and colleagues (2015) identified that
the gene underlying the hard-seed allele in soybean encoded
an ENDO-1,4-β-GLUCANASE, which is particularly active
in the outer palisade cells of the seed coat. More recently,
Sechet and colleagues (2016) identified an Arabidopsis mutant
which expressed no primary dormancy in the seed. They show
that the wild-type gene encodes a XYLOSIDASE involved
in xyloglucan synthesis, which when specifically expressed in
endosperm restores primary dormancy. This indicates that
the tissue-specific expression of xyloglucan metabolism is a
central feature of primary dormancy, and not limited to the
function as a physical barrier.
The influence of NO (Gibbs et al., 2014) and oxygen
(Mendiondo et al., 2015) is at least partly dependent on N-end
proteolysis (arginine-N-end pathway). However, mutants
compromised in components of the N-end proteolytic pathway still respond to chilling-induced relief of dormancy (Gibbs
et al., 2014). The dormancy-breaking effect of cyanide was also
dependent on NO (Bethke et al., 2006), and later also shown to
trigger ROS-induced carbonylation of specific proteins, which
enabled germination of sunflower seed (Oracz et al., 2007).
ROS also promoted the degradation of ABA and synthesis
of gibberellic acid (Liu et al., 2010), an effect which may also
be dependent on NO (Sarath et al., 2007). The primary source
of ROS is likely to be plasma membrane NADPH oxidases
(RBOHs). An Arabidopsis rbohb mutant showed an attenuated response to after-ripening conditions and ABA, whereby
germination was not appreciably accelerated by after-ripening,
nor repressed by ABA (Müller et al., 2009).
Across life forms, cell cycle progression at the G1/S and
G2/M checkpoints is dependent on redox cues (Rothstein and
Lucchesi, 2005). Quiescent cells are stalled in the G1 phase,
often termed G0, although distinguishable only by the failure
to progress until triggered, as distinct from senescing or terminally differentiated cells (reviewed by Coller, 2007; Cheung
and Rando, 2013). The quiescent centre cells of the root apical
meristem are oxidized, have low levels of reduced ascorbate
and glutathione, and addition of either of the latter triggers progression to the S phase (Liso et al., 1988; Kerk and
Feldman, 1995). The low redox state is functionally related
to the polar auxin gradient (Jiang and Feldman, 2003; Jiang
and Feldman, 2005). Arabidopsis mutants compromised in
glutathione synthesis fail to develop an active post-embryonic root meristem, unless glutathione is exogenously applied
(Vernoux et al., 2000). A level of redundancy exists in the
shoot with thioredoxin, as THIOREDOXIN REDUCTASE
The language and physiology of dormancy and quiescence | 3195
double mutants exhibit stunted shoot growth (Reichheld
et al., 2007). Intriguingly, the inhibition of glutathione synthesis in these mutants leads to a reversible quiescence, and
not lethal oxidative stress (Reichheld et al., 2007). It has since
been shown that glutathione is shuttled from the cytosol to
the nucleus during the G1/S transition in plants, as in animals
(Diaz Vivancos et al., 2010).
Together, these insights highlight a central function of oxygen and redox cues in calibrating cells, meristems, organs, and
whole organisms to the environment and governing quiescent
and cell fate decisions. However, no clear distinction can yet
be made in regard to oxygen and related metabolism in dormant versus quiescent organs.
Seasonal cues; temperature and
photoperiod
Relationships between temperature and photoperiod and
dormancy and quiescence have been considered and modelled
widely across plant phyla (Way et al., 1949; Wareing, 1956;
Heldmaier et al., 1989; Battey, 2000). Existing knowledge
almost wholly concerns northern hemisphere, high latitude
species, or annual, herbaceous species, endemic to a strongly
seasonal environment (Rohde and Bhalerao, 2007; Ruttink
et al., 2007; van der Schoot and Rinne, 2011; Herrmann
et al., 2015; Rinne et al., 2015). An episodic growth habit predominates in perennial species (Hallé et al., 1978; Barthélémy
and Caraglio, 2007); however, the role that dormancy per se
plays in episodic growth remains unclear for the vast majority of species. Examples where confusion has arisen include
the episodic growth of Camellia sinesis and Melaleuca viminalis (syn. Callistemon viminalis). In these species, seasonal,
episodic growth is achieved through quiescence, not meristematic dormancy (Wight and Barua, 1955; Purohit and
Nanda, 1968).
Photoperiod is the most reliable and predictable environmental cue at mid- and higher latitudes. However, it is not a
universal cue for the onset of dormancy or quiescence in perennial plants. For example, the debate regarding photoperiodism in particular members of the Rosaceae seems to have
been settled in favour of its absence (see Garner and Allard,
1923; Wareing, 1956; Heide and Prestrud, 2005; Cooke et al.,
2012).
Debate on the role of thermoperiod in quiescence and dormancy is somewhat confounded with acclimation, particularly
to water stress such as freezing or desiccation (Vitasse et al.,
2014). Perhaps an argument could be made that photoperiod
is also confounded with nutrition, at least in photoautotrophs.
Thus, in discussing the role of photoperiod and temperature
in quiescence and dormancy, we confront shades of grey,
where episodic growth and acclimation become important.
Hence some aspects of seasonality are also discussed in the
sections on epigenetic regulation and positional regulation.
However, we do not discuss acclimation per se at length.
A diversity of responses to photoperiod are apparent in the
data published by Downs and Borthwick (1956), and in numerous reviews before and since (see, for example, Doorenbos,
1953; Wareing, 1956; Nitsch, 1957a, b; Romberger, 1963;
Cooke et al., 2012). For example, Aesculus hippocastenum
appears to enter dormancy developmentally, regardless of
photoperiod and in the absence of chilling (Downs and
Borthwick, 1956). In contrast, six other species of this study
grew continuously without limit (in long days (14/10 h) or
continuous light; Downs and Borthwick, 1956]. The latter
species were more sensitive to thermoperiodism than photoperiodism, although the authors chose not to discuss the
issue (Downs and Borthwick, 1956). A further study of seven
species selected from high and low latitudes and grown in
continuous light and constant 24 °C revealed episodic growth
in each, with periods of intervening ‘dormancy’ (Lavarenne
et al., 1971). The ‘dormant’ intervals ranged from a week to
many months; however, growth was frequently abnormal,
with a terminal bud not always developing, and the authors
could not determine the nature of the ‘dormancy’, that is,
whether dormant or quiescent (Lavarenne et al., 1971). Thus,
while generalizations are frequently made about conditions
leading to the transformation of apical buds to a dormant
state, the details matter considerably.
The expression of FLOWERING LOCUS T (FT) and
CONSTANS (CO) is widely implicated in photoperiodic flowering responses in plants. In a seminal paper, Böhlenius and
colleagues (2006) also demonstrated that the CO/FT module
was a key regulator of the transition from juvenile to adult,
and in bud set (dormancy onset). RNAi-FT lines showed an
accelerated bud set in response to short days, while overexpressing lines either failed to set, or were considerably delayed
(the authors tested only 60 d of short days, Böhlenius et al.,
2006). Ecotypes sampled across 12° latitude demonstrated
that both FT and CO expression correlated with the critical
daylength for bud set, such that buds set if daylength was less
than the period required for a peak in CO and FT. As both
transcripts are expressed primarily in leaves, the transition
must be accompanied by transport of FT (see also sections on
epigenetic regulation and positional regulation). Böhlenius
and colleagues (2006) also showed that poplar overexpressing
an oat PHYTOCHROME A (PHYA) failed to repress CO or
FT in short days, and failed to set buds, as previously indicated (Olsen et al., 1997).
In species adapted to extreme cold, short days and/or cool
nights induce a transition to dormancy, which is coupled with
a ‘stage I’ acclimation to cold and desiccation, as previously
described (reviewed by Rinne et al., 2001). In species such
as Quercus, Picea, Fagus, and other boreal and cool temperature species, this state progresses to a ‘stage II’ acclimation, with induction of a suite of cold-responsive processes,
such as C-REPEAT BINDING FACTORS and LATE
EMBRYOGENESIS ACCUMULATING proteins (Welling
et al., 1997; Rinne et al., 1998; Thomashow, 1999; Welling
et al., 2004). However, while attention has focused on adaptation to extreme cold, a broader range of avoidance and adaptive processes occur across ecosystems and taxa (Levitt, 1980;
Sakai and Larcher, 1987), and much remains to be understood in the less hardy species (Wisniewski et al., 2014).
The resumption of competence to grow following dormancy is a less well studied topic. In contrast to bud set,
3196 | Considine and Considine
where the leaf may be the source of seasonal perception,
the bud meristem is the most likely sensory hub for release
of dormancy. Past research on release of dormancy has
focused on modelling rather than experimentation (Chuine
and Cour, 1999; Chuine, 2000; Schaber and Badeck, 2003).
Here again, it is difficult to uncouple dormancy from acclimation, or competence via de-acclimation. While it is generally accepted that dormancy and ‘stage I’ acclimation may be
inextricably associated at the onset of dormancy, there are
examples where de-acclimation and resumption of competence to burst by the meristem are asynchronous: competence first, then de-acclimation (Klebs, 1914; Pouget, 1963;
Nienstaedt, 1966). If this is so, then avoiding frost in spring
becomes a significant issue (Hanninen, 2006; Wisniewski
et al., 2014). Separating dormancy and acclimation remains
difficult, particularly in woody perennials, which lag progress
in forward- and reverse-genetic approaches relative to annual
species. Some species appear to be developmentally entrained
and respond to environmental cues in a facultative manner,
similar to the autonomous pathway of flowering (Lavarenne
et al., 1971; Posé et al., 2012). Further effort to dissect these
cues is needed.
Regulation of the cell cycle, and the
interface with sugar signalling
The literature is divided on the role of the cell cycle in dormancy, particularly in seeds. It is widely accepted that the cell
cycle plays a key role in the onset of dormancy during seed
maturation, and that cells of dormant seed are predominantly
arrested in the G1 phase (Raz et al., 2001). However, it is commonly understood that cell division does not occur until after
radicle emergence during germination (Bewley, 1997). The
activation of a core set of cell cycle genes very early in imbibition has been observed, sufficient for replication and presumably repair, but not for mitosis (Barrôco et al., 2005). Further,
in species such as Avena fatua, cell division was seen prior
to radicle emergence, in correlation with release of dormancy
(Cembrowska-Lech and Kepczynski, 2016). However, further
studies of the role of DNA repair and synthetic machinery
may be required to elucidate the role of cell cycle control in
seed dormancy.
The role of cell cycle control in bud dormancy is more
widely accepted, for example in buds of ash (Cottignies,
1979), potato (Campbell et al., 1996), Salix (Hansen et al.,
1999), or, more recently, in apricot, where cell division is seen
early in provascular tissue during the release from dormancy
(Julian et al., 2011). Cyclin-dependent kinases were also
implicated in cambial dormancy of poplar species (EspinosaRuiz et al., 2004; Li et al., 2009). However, there is no knowledge of the distinction in cell cycle control between dormancy
and quiescence. The cell cycle is regulated in a wide range of
quiescent conditions, both spatially and temporally, as seen
in meristems of higher plants. Metabolic depression is widely
distributed across kingdoms (Yanagida, 2009; Withers and
Cooper, 2010; O’Farrell, 2011). It is worthy of elaboration
here, because the pathways involved in metabolic depression
in plants traverse growth by extension and division, for
example in the submergence responses of Swarna-Sub1 rice
(Pucciariello and Perata, 2013).
Nutrition is perhaps the primary consideration driving quiescence in single-celled organisms. The evolutionary
significance of this was articulated by O’Farrell (2011) in
a brief exercise of arithmetic, paraphrased here: if a single Escherichia coli weighing ca. 1012 g has a doubling time
of ~20 min and growth were not limited by nutrition, then
within 2 d the culture would exceed the mass of the earth
(1.6 × 1031 g compared with 6.0 × 1027 g). Or, of course, the
whole population would die. Hence quiescence is requisite
for life at its most basic, providing a selective advantage for
evolution, and species diversity in the regulation of quiescence and dormancy provides a pathway for specialization in
ecological niches.
The TARGET OF RAPAMYCIN (TOR) pathway is a
well-conserved component of metabolic regulation across
the domains of life and particularly relevant in the context of
quiescence (reviewed by Fingar and Blenis, 2004; Henriques
et al., 2014). While several questions remain as to the role
and regulation of the TOR pathway in higher plants, and its
role in dormancy is almost completely unexplored, its relationship to nutrient sensing and the regulation of the cell
cycle are well established. An additional and interconnecting
pathway features the SNF1-RELATED KINASE1 (SnRK1)
homologue of the animal AMP-ACTIVATED PROTEIN
KINASE (AMPK). Together the plant TOR and SnRK1
pathways converge on sugar sensing, acting across the spectrum of sugar availability to limit cell division by the SnRK1
pathway where sugars are limited, or promote cell division
by the TOR pathway when sugar is abundant (reviewed by
Henriques et al., 2014; Lastdrager et al., 2014). The targets of
both pathways and their interactions pervade regulation of
cell growth as well as division. Considerably more attention
has been paid to regulation of growth, rather than division
or quiescence.
The role of sugars in regulating the cell cycle extends
beyond the TOR, SnRK1, and related pathways (Lastdrager
et al., 2014). Sugars directly induce expression of cyclins and
cyclin-dependent kinases, regulating both the G1/S and G2/M
transitions (Gaudin et al., 2000; Riou-Khamlichi et al., 2000;
Menges et al., 2006; Skylar et al., 2011). For example, sucrose
limitation results in arrest in G1 phase of the cell cycle, while
sucrose availability induces D-type cyclins, enabling progression (Riou-Khamlichi et al., 2000). The G1 arrest is mediated by the plant RETINOBLASTOMA-RELATED (RBR)
orthologue (Hirano et al., 2008), a central regulator of stem
cells across kingdoms (Scheres, 2007). RBR interacts with the
transcription factor complex SCARECROW–SHORTROOT
to co-ordinate specification of the root stem cell niche (CruzRamírez et al., 2012). Recent evidence also demonstrates
that RBR interacts with chromatin-modifying complexes,
including the PcG proteins, in regulating cell fate decisions
(reviewed by Kuwabara and Gruissem, 2014).
Currently, knowledge of the roles of sugars and the TOR,
SnRK1, and RBR pathways in regulating dormancy is nearabsent. Although several studies have implicated, for example,
The language and physiology of dormancy and quiescence | 3197
RBR (Shimizu-Sato et al., 2008), D-type cyclins (Mehrnia
et al., 2008), and BRANCHED1 in light- (Gonzalez-Grandio
et al., 2013) or sucrose-dependent (Mason et al., 2014) bud
‘dormancy’, each of these studies actually refer to correlative repression (apical dominance); that is, quiescence, not
dormancy. Notwithstanding, these are important insights
into the regulation of quiescence. While, orthologues of
BRANCHED1 have been observed in dormant buds of poplar (Rinne et al., 2015) and Jatropha curcas (Ni et al., 2015),
mechanistic relations to dormancy have yet to be established.
Epigenetics and chromatin remodelling
The regulation of the cellular chromatin state has been the
focus of recent discussions on cellular quiescence (see, for
example, Coller, 2007; Neilson, 2007; Srivastava et al., 2010;
Cheung and Rando, 2013). The roles of two protein complexes in quiescence and organism patterning, first described
in Drosophila—the Polycomb group (PcG) and Trithorax
group (TrxG)—have since defined our understanding of
cellular memory (Srivastava et al., 2010). The PcG contribute to maintaining a repressed state through trimethylation of histone-H3 lysine-27 (H3K27) and ubiquination of
H2AK118/119, while TrxG antagonizes PcG and co-ordinates the active state through trimethylation of H3K4 and
H3K36 (Srivastava et al., 2010; de la Paz Sanchez et al., 2015,
and references therein). However, repressors can also be
repressed, as seen in the vernalization response of flowering,
a well-defined example of PcG-mediated plasticity. Chilling
induced VERNALIZATION INSENSITIVE 3 (VIN3) complexes with several PcG proteins which in turn trimethylate
the H3K27 at FLOWERING LOCUS C (FLC), repressing
this central floral repressor (Sung and Amasino, 2004; Wood
et al., 2006). However, the repression is only stable if cells
have divided before warmer conditions prevail, otherwise
the trimethylation is removed, relieving repression of FLC
(Finnegan and Dennis, 2007). Hence meristem quiescence per
se precludes the floral transition.
Recent reviews highlight the evolution of knowledge on
epigenetic regulation and the parallel behaviours of dormancy
and seasonal flowering responses in particular, as a paradigm
for further exploring the crosstalk between environmental
and developmental cues (Hemming and Trevaskis, 2011; de la
Paz Sanchez et al., 2015). Packaging the genome into higher
order chromatin structures enables a regulated accessibility
to define access to transcription factors which in turn regulate expression or repression of genes. Epigenetic annotations
such as methylation and acetylation can be stably transferred
through mitotic divisions, enabling a molecular memory to
perpetuate throughout cell lineage, or be selectively curated
to enable a progressive differentiation of cell function in synchrony with seasonal or positional cues (i.e. position within an
organ). This befits the physiological behaviour of dormancy,
and particularly the patterns of quantitative entrainment.
The insight that dormancy can be at least partially uncoupled
from both desiccation and hypoxia is also suggestive of a role
for epigenetic regulation in dormancy.
Remarkably similar patterns of epigenetic control have
been defined in the chilling responses of dormant seeds
and perennial buds, although with different targets. The
DORMANCY ASSOCIATED MADS BOX (DAM) genes
are part of the MIKCC family of MADS Box transcription
factors, which includes FLC and a number of other genes
involved in floral identity and meristem plasticity and differentiation (Hemming and Trevaskis, 2011). DAM was first
identified in the evergrowing mutant of peach (Prunus persica;
evg), which is unable to form terminal buds or enter dormancy
(Rodriguez-A et al., 1994; Bielenberg et al., 2008, and references therein). The evg locus carries a deletion of six tandem
DAM orthologues. In wild-type peach, PpDAM6 in particular is induced in the buds during the onset of dormancy but
quantitatively repressed with accumulated exposure to chilling
(hours below 7 °C; Leida et al., 2012). Expression and repression correspond to the chilling requirements of several peach
cultivars. For example, after 400 chilling hours, PpDAM6 of
cv. ‘Big Top’ remains induced, reflecting a chilling requirement in excess of 600 h, while in cultivars with requirements
<400 chilling hours, PpDAM6 was repressed (Leida et al.,
2012). Similar data have been reported for Japanese apricot (Sasaki et al., 2011), Japanese pear (Saito et al., 2013),
Chinese cherry (Zhu et al., 2015), and leafy spurge, a perennial weed (Horvath et al., 2010), and orthologous genes have
been identified in numerous other woody perennials including
grapevine, apple, and poplar (Horvath et al., 2008).
Chromatin modifications of DAM orthologues have been
reported in peach and leafy spurge, consistent with methylation and deacetylation activity of PcG proteins (Horvath
et al., 2010; Leida et al., 2012). In both cases, the authors
reported increased trimethylation at H3K27 and decreased
trimethylation at H3K4 of at least one DAM orthologue,
coinciding with the decline in DAM gene expression and
release of dormancy, indicated by an increase in the rate of
bud burst under forcing conditions (Horvath et al., 2010;
Leida et al., 2012). In peach, a decline in acetylated H3 was
also reported coincident with release of bud dormancy (Leida
et al., 2012). This was also seen after storage-induced release
of dormancy in potato tubers, where multiacetylation of histone H4 dramatically declined after complete release of dormancy, and after transient increases in H3.1, H3.2, and H4
prior to complete release (Law and Suttle, 2004).
Very similar chromatin regulation has been reported for
DELAY OF GERMINATION1 (DOG1), a gene that segregates with dormancy in seeds (Alonso-Blanco et al., 2003;
Bentsink et al., 2006). DOG1 expression accumulates with the
onset of dormancy, in correlation with increased trimethylation at H3K4 (Müller et al., 2012; Molitor et al., 2014; Footitt
et al., 2015). Expression of DOG1 is further induced initially
by chilling but repressed by further exposure, in concert with
a decline in trimethylation at H3K4 and increased trimethylation at H3K27.
Together, these insights indicate a clear role for epigenetic
regulation including chromatin modifications through PcG
and TrxG proteins in determining the state of quiescence and
dormancy. Further study promises many more insights into
the molecular components of entrainment. For example, Hao
3198 | Considine and Considine
and colleagues (2015) recently provided evidence of synergies
between DAM and FT, a well-studied component of photoperiod regulation of flowering and dormancy, and which is
also regulated by PcG proteins (Romera-Branchat et al., 2014,
and references therein). It is tempting to suggest that dormancy
is governed by a higher order heterochromatin state, as an
extension of the model suggested to govern quiescence in animal cells (Coller, 2007; Neilson, 2007; Srivastava et al., 2010;
Cheung and Rando, 2013). However, here again, the distinction
between roles for epigenetic modification of PcG and TrxG in
quiescence versus dormancy requires further elucidation. Positional regulation, stem cells and
meristems
The evolution of the meristem in the byrophyte grade was
likely to be a defining event leading to the modes of dormancy
and quiescence we see in higher plants, including correlative
repression (including apical dominance), meristem patterning, and dormancy. Dormancy and quiescence need to be
viewed in the context of the organization of the apical meristem. The architecture of higher plant meristems arises during
embryogenesis, determining two polar populations of multipotent stem cells adjacent to less mitotically active quiescent
centre or organizing centre cells, within the root and shoot
apical meristems, respectively, as well as the cambium stem
cells (reviewed by Doerner, 2003; Stahl and Simon, 2010).
The two apical meristems share common regulatory functions that determine, in particular, the spatial organization
of subdomains that facilitate the developmental and environmental plasticity that defines multipotency. Intercellular
communication within and between subdomains is central
in determining cell identity and fate, as elegantly illustrated
by a series of laser ablation studies of the quiescent centre or
adjoining cells (van den Berg et al., 1995, 1997), and further,
by the near or complete lack of plasmodesmata in totipotent
embryogenic stem cells (Verdeil et al., 2007). In this way, cells
of the meristem are said to be non-cell-autonomous; that is,
there is an interdependence between quiescent, proliferating,
and differentiated cells that determines cell identity and fate,
rather than fate being defined by the progenitors. Stahl and
Simon (2013) proposed that protein complexes within plasmodesmata regulate the transport of central transcription
factors that operate in a feedback loop to control cell identity
and differentiation in the root and shoot apical meristems.
The group of Rinne and van der Schoot have progressively
illustrated the role and regulation of the plasmodesmata
in the terminal buds of the deciduous perennial trees poplar and birch and their role in maintenance of the dormant
state (see, for example, van der Schoot and Rinne, 2011; Paul
et al., 2014b; van der Schoot et al., 2014). Conductance of
plasmodesmata defines the subdomains of the meristem. This
is regulated developmentally and in synchrony with seasonal
signals. In birch, for example, transition to short days cues
the onset of bud formation and dormancy, and is accompanied by synthesis of 1,3-β-d-glucan in plasmodesmatal channels, serving to isolate further cells within subdomains of the
meristem (Rinne and van der Schoot, 1998), perhaps resembling the condition of totipotent stem cells (Verdeil et al.,
2007). Chilling and gibberellins differentially activated genes
encoding 1,3-β-GLUCANASES, leading to degradation
of the callose-obstructed plasmodesmata, and resumption
of communication, or at least competence to communicate
(Rinne et al., 2001). This seems to be a phenomenon that
is specific to the dormant state (i.e. absent from the quiescent state). Rinne and colleagues (2011) then showed that
both treatments also induced FT, expressed in the leaf and
transported to the bud and to the meristematic cells via plasmodesmata. As such, they proposed that glucanase-mediated
gating acts as a further level of control over the activity of FT
(Rinne et al., 2011), in addition to phytochrome regulation
(Böhlenius et al., 2006).
It is increasingly evident that dormant buds are also isolated from the plant (i.e. similar to the seed) and that cell wall
metabolism plays a key role in regulating the isolation and
reconnection. In fact, it is possible that this was identified
as early as the 19th century, then termed the ‘markkrone’,
as identified by Schröder (1869), although no contemporary
studies have reported on the histology and molecular characteristics of this tissue. Romberger (1963) reported the markkrone to be collenchymatous tissue, and to lack lignin or
suberin, but to be absent from some species. However, regulation of the symplastic interface between tissues by callose
deposition and removal, and the interplay with plasmodesmatal-associated lipids and proteins may suffice to enable isolation of the bud (Paul et al., 2014a, b). Such subtle changes
would not have been apparent prior to the development of
contemporary plant anatomical methods (van der Schoot
et al., 2014). Nevertheless, at least in conifers, the tissue was
seen to be a barrier to the movement of apoplastic dyes,
e.g. eosin (Lewis and Dowding, 1924), and plasmodesmatal
pit fields were also apparent (Jansson and Bornman, 1983).
Thus, developmental compartmentalization, regulated by
the conductivity of the apoplastic and symplastic pathways,
may interface with seasonal cues and with chromatin modifications, and be tied together with oxygen and redox control
of the activity and transport of plant growth regulators and
transcription factors.
Conclusions
The language of quiescence and dormancy has often been
loosely applied, and on occasion misused. There are several paths to the same phenotype, particularly in multicellular organisms. Positional cues, including distal and local
metabolic and molecular inter- and intracellular signalling
play roles that are difficult to uncouple experimentally. The
early advances in genome technologies occasionally tempted
researchers towards overly reductionist approaches at the
expense of physiology. However, the advances that have come
with second- and third-generation genomic and genetic technologies promise more cost-effective, systems approaches that
will enable elucidation of the cellular distinctions between
quiescence and dormancy in plants. However, this must
The language and physiology of dormancy and quiescence | 3199
be accompanied by sound physiological and biochemical
approaches, such as those that revealed the non-cell-autonomy of meristematic cells, the epigenetic regulation of DAM,
DOG, and FT orthologues, and the oxygen and NO signalling
via the N-end rule of proteolysis. Figure 2 provides a summary of the major cues driving quiescence and dormancy in
plants, indicating a role for non-cell-autonomous regulation
that is coupled to epigenetic regulation, in defining the dormant meristem. How these pathways might converge, particularly in a positional sense, remains to be deciphered. Several
further questions we may ask include: how is epigenetic regulation of DAM orthologues in the buds of woody perennials
coordinated spatially, within an organ of multiple meristems
of differing organogenic states? And, how does this interface
with the regulation of symplastic conductance? Does isolation, whether physical or metabolic, distinguish all modes of
dormancy from quiescence? Does the N-end rule of proteolysis
converge with redox modification of plant growth regulators,
such as auxin and ABA? How does chromatin remodelling
interface with the ‘glassy state’ of desiccated cells? Progress is
already evident towards answering some of these questions,
while others may not unravel for several years. However, the
major priority this review has highlighted, is that researchers
across disciplines pay more precise attention to the language
of dormancy and quiescence.
Acknowledgements
The authors would like to acknowledge financial support from the
Australian Research Council (LP0990355 and DP150103211). We’d also
like to thank postgraduate students Mrs K. Meitha, Miss Y. Velappan, Miss
D. Hermawaty, postdocs Dr P. Agudelo-Romero and Dr S. Signorelli, and
colleagues Mr C. Gordon and Mr I. Cameron for inspiration that underpinned the physiological and cell biological approach to this manuscript.
Authors also thank the Reviewers and Editor for constructive criticism to
help tighten the manuscript. Finally, authors wish to thank the ongoing support of the Western Australian grape and wine community for valuable inkind contributions to research. References
Fig. 2. Simplified conceptual diagram of the major physical, metabolic,
and molecular signals that govern dormancy (D), quiescence (Q),
and active (A) states in plants, and particularly relating to the nucleus.
Summarily, the cell and nucleus are in a hypoxic, oxidized, and dehydrated
state during dormancy, with low NO and low free sugars, while the
plasmodesmata are occluded with glucans. Key regulatory genes are
bound in a heterochromatin state during dormancy, more loosely
associated during quiescence, and available in a euchromatin state
when active, allowing transcription. Seasonal cues such as temperature
and photoperiod co-ordinate remodelling of the chromatin, as governed
by the activities of PcG and TrxG protein complexes, which regulate the
more dormant or active states, respectively. It is not yet known how
the chromatin state interfaces with the physical and metabolic cues
shown; however, the transitions from dormant to quiescent and active
may be accompanied by an increase in the redox state (more reduced),
particularly of the nucleus. Seasonal cues also activate transcription of
genes encoding β-GLUCANASES or GLUCAN SYNTHASES, regulating
the aperture of the plasmodesmata. The transition from dormant to
quiescent is then governed by intercellular cues via plasmodesmata,
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FLOWERING LOCUS T (FT), translated in the vasculature of leaves and
transported to the bud complex. Abbreviations: PcG, POLYCOMB GROUP
proteins; TrxG, TRITHORAX GROUP proteins; β-Gl., β-GLUCANASES
and GLUCAN SYNTHASES; PD, plasmodesmata; TOR, TARGET OF
RAPAMYCIN; SnRK, SUCROSE-NON-FERMENTING-RELATED KINASE;
redox, reduction/oxidation state (indicating more oxidized at dormant D).
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