Current Biology
Magazine
Primer
Seed dormancy and
germination
Steven Penfield
Reproduction is a critical time in plant
life history. Therefore, genes affecting
seed dormancy and germination
are among those under strongest
selection in natural plant populations.
Germination terminates seed dispersal
and thus influences the location
and timing of plant growth. After
seed shedding, germination can be
prevented by a property known as
seed dormancy. In practise, seeds
are rarely either dormant or non-
dormant, but seeds whose dormancy-
inducing pathways are activated to
higher levels will germinate in an
ever-narrower range of environments.
Thus, measurements of dormancy
must always be accompanied by
analysis of environmental contexts in
which phenotypes or behaviours are
described. At its simplest, dormancy
can be imposed by the formation of
a simple physical barrier around the
seed through which gas exchange and
the passage of water are prevented.
Seeds featuring this so-called ‘physical
dormancy’ often require either
scarification or passage through an
animal gut (replete with its associated
digestive enzymes) to disrupt the
barrier and permit germination. In other
types of seeds with ‘morphological
dormancy’ the embryo remains under-
developed at maturity and a dormant
phase exists as the embryo continues
its growth post-shedding, eventually
breaking through the surrounding
tissues. By far, the majority of seeds
exhibit ‘physiological dormancy’ — a
quiescence program initiated by
either the embryo or the surrounding
endosperm tissues. Physiological
dormancy uses germination-inhibiting
hormones to prevent germination in the
absence of the specific environmental
triggers that promote germination.
During and after germination, early
seedling growth is supported by
catabolism of stored reserves of
protein, oil or starch accumulated
during seed maturation. These reserves
support cell expansion, chloroplast
R874 Current Biology 27, R853–R909, September 11, 2017 Crown Copyright © 2017 Published by Elsevier Ltd.
development and root growth until
photoauxotrophic growth can be
resumed.
The phenomenon of seed dormancy
is best understood at three levels. At
the population level, seed dormancy
enables the formation of a soil seed
bank from which plants can emerge at
different times of year or in response to
ecosystem disturbances. At the single-
plant level, individual mothers have
evolved mechanisms for maintaining
control of progeny seed-germination
behaviour and generating heterogeneity
in progeny seed properties. This
enables mothers to hedge their bets
by producing seeds with different
propensities to germinate or that are
likely to germinate at different times
and places. Finally, at the level of the
individual progeny seed, mechanisms
exist to maintain and break dormancy,
often in response to environmental
stimuli that limit germination to specific
annual time windows, or enable seeds
to wait for gaps in the canopy to
appear.
Control of seed dormancy and
germination by the mother
Although it is tempting to think of
germination as a process that starts
and ends after seed shedding, in reality,
many of the most important aspects
of seed germination behaviour are
determined during seed maturation
and are closely linked to the control
of seed dispersal. In his pioneering
work on resource conflicts during
reproduction, W.D. Hamilton showed
that in plants the mother benefits
from diversity in seed properties. She
favours wider dispersal of progeny,
spreading individuals between safer
zones closer to the mother herself but
also to increasingly risky locations ever
further away. Increasing dispersal has
the duel benefits of discovering new
locations suitable for plant reproduction
and reducing resource conflict between
individual progeny seeds. However,
the fact that the chances of successful
reproduction decrease with distance
of germination from the mother plant
(Figure 1) creates a conflict among
individual progeny seeds who are best
served by avoiding the fate of being
included in the most risky and sacrificial
cohort. This optimum maternal strategy
therefore contrasts with the optimum
strategy for any one individual seed,
which is to germinate closer to the
location of the mother, where good
chances of reproductive success have
been convincingly demonstrated by the
mother herself.
The mother plant therefore has
evolved a number of mechanisms
for retaining control of the behaviour
of progeny seeds. These include the
maternal-derived hard outer tissues of
seeds: either the seed coat, which is
derived from the ovule integuments,
or the pericarp, which is maternal fruit
tissue. In addition, in angiosperms
the endosperm also surrounds the
embryo and has an increased dosage
of the maternal genome. Similarly,
mechanisms such as gene imprinting
allow certain genes from the mother or
father to be selectively silenced. Thus,
the maternal contribution to the seed
is substantial, and all these tissues
have been shown to be important in
the maternal control of seed dormancy.
These maternal processes do not act
alone, but instead work in concert
with a gene-expression programme in
the zygote that simultaneously blocks
growth, initiates the accumulation of
stored reserves and, in most species,
induces a low-water tolerant state that
enables the seed to survive wet or dry
for long periods in the environment.
Environmental signals are perceived
by both the mother plant and the
developing zygote, and are used to
control the germination of progeny
seed. The result is that the mother
can impart seasonal cues to progeny
and also use environmental noise to
generate variation in progeny dormancy
states. The temperature that the
mother plant experiences throughout
her life cycle, including whether or not
the plant experiences vernalisation,
both have major impacts on progeny
seed dormancy. These effects are
mediated by the same gene network
that controls the transition to flowering;
these ‘flowering time’ genes are highly
expressed in fruit and seed tissues, as
well as in leaves and the developing
shoot apex. In tomato it is clear that
photoperiod signals can be perceived
by detached fruits and information
passed to progeny seeds to control
their behaviour. The manipulation of
temperature, nitrate and light during
seed maturation also have big impacts
on progeny dormancy, and controlling
these factors is often the biggest
Current Biology

Magazine

challenge in the design and execution

of experiments analysing germination
behaviour. Seeds can be sensitive even
to 1°C changes in temperature, and
can use natural noisy environmental-
temperature variation as an important
way to generate diversity in germination
propensity in seeds on the same
inflorescence. In this way, the mother
produces cohorts of seeds with varying
strategies, for immediate germination or
to populate the soil seed bank.
There are several mechanisms Dispersal
through which maternal signals control
seed properties. Firstly, they affect Competition Risk
the developmental and metabolic
processes in the fruit- and seed-coat
tissues during seed development Dormancy
and maturation, resulting in changes
to fruit morphology (affecting
dispersal), seed-coat thickness and
the deposition of seed-coat polymers
such as tannin and suberin that in turn
affect the depth of seed dormancy.
Secondly, through specific regulation
of the maternal copies of genes in the
endosperm, the mother can control
gene expression patterns in the
endosperm during seed maturation
and even after seed shedding and Current Biology
imbibition, affecting dormancy loss,
storage-protein breakdown and
Figure 1. Kin selection and parent–offspring conflict theory applied to plant reproduction.
germination rate. Maternal effects The optimal maternal strategy (brown seeds) is to reduce competition among kin by producing
are particularly important in species progeny with a range of dormancy characters, enabling dispersal in time and space, and populat-
that exhibit what is known as coat- ing the soil seed bank. In contrast, the optimum strategy for individual progeny (white seeds) is to
imposed dormancy — that is, dormancy germinate close to the mother, where the environment must be conducive for successful repro-
that can be removed by excising duction. Because germination terminates dispersal, seed dormancy and dispersal characters are
the embryo from the seed, or even closely linked.
by simply puncturing or scarring the
seed — because of the dominant Heterogeneity in seed behaviour is to heterogeneity, but in practise it is
influence of the maternal genome achieved through varying mechanisms. challenging to separate truly stochastic
in the development and physiology First, production of seeds may events from environmental effects
of these tissues. In these cases the occur at different times of year, because of the extreme sensitivity of
mechanism of dormancy imposition or at times of year with changing seeds to micro-environmental variation.
by the seed coat and endosperm environments, leading to variation
barrier is not always entirely clear; in maternal processes controlling The induction of dormancy during
but a feature of these seeds is a low seed development and maturation. seed maturation
oxygen environment, and increasing Alternatively, there can be variation When embryogenesis is complete, the
the partial pressure of oxygen often in the degree to which seeds reach maturation programme commences
results in faster germination and higher full maturity at shedding, with seed and the seed begins to accumulate
germination rates. Oxygen levels are dormancy often declining slightly in reserves of carbon and nitrogen that
essential for the production of reactive the later stages of seed maturation. will fuel seedling establishment after
oxygen species (ROS) and nitric oxide Also, specific developmental programs germination. During the maturation
(NO) in seeds, both of which have that produce seeds of different phase, seeds of many species
important signalling roles that promote morphs, often including production also acquire the means to survive
seed germination. For instance, both of seeds of different types in different desiccation, and enter primary
ROS and NO promote the stabilisation locules of the fruit, leads to distinct dormancy. In the dormant state, the
of a group of germination-promoting VII germination behaviors. It has also cells lack hydrated vacuoles, do not
Ethylene Response Factor transcription been hypothesised that stochasticity break down stored reserves and
factors, which otherwise are rapidly in the molecular networks that control the cell cycle is suppressed. This
targeted for degradation. germination behavior may contribute developmental state is promoted by a

Current Biology 27, R853–R909, September 11, 2017 R875


in
lan
Me
Maternal
effects
Suberin
ABA
O2
GA
Wall
loosening
Figure 2. Major events in imbibed seeds.
Abscisic acid (ABA) is produced primarily in the endosperm and maintains dormancy via transport to the embryo. If ABA levels fall then the root apical
meristem (RAM) produces gibberellin (GA), which stimulates water uptake through vacuolisation, combined with cell wall loosening of the hypocotyl
and micropylar endosperm. Hypocotyl cell expansion is driven partly by endoreduplication and provides a mechanical force opposed only by the
weakening endosperm layer. ABA signalling is attenuated by ROS and NO as seed coat integrity is lost, and the oxygen content of the seed rises.
group of B3-family transcription factors
known from Arabidopsis as LEAFY
COTYLEDON 1 (LEC1), ABSCISIC
ACID INSENSITIVE 3 (ABI3), FUSCA3
(FUS3) and LEAFY COTYLEDON 2
(LEC2), often abbreviated as the ‘LAFL’
transcription factors. This same group
is also responsible for the homeotic
conversion of leaves to cotyledons,
and when any of these genes are
compromised desiccation tolerance is
reduced or absent, dormancy is lost
and accumulation of storage reserves
is incomplete. A key function of the
LAFL genes in dormancy imposition
is the induction of a high abscisic
acid (ABA) state, which is necessary
for the prevention of germination-
related processes. If ABA signalling in
developing seeds is insufficient, they
can begin to germinate on the mother
plant before shedding, a property
R876 Current Biology 27, R853–R909, September 11, 2017
Cutin Tannin
ABA synthesis
ABA transport
Suberin
ROS, NO
Cell expansion
GA
RAM
Wall loosening
mobilisa
ABA Reserve
known as vivipary. Vivipary is common
in major crops that have been bred for
vigorous stand establishment, and is
worse in environmental conditions that
lead to low dormancy, such as warm,
wet conditions. In cereals this vivipary
is known as pre-harvest sprouting,
and is accompanied by premature
production of -amylase and a sharp
reduction in grain quality. Pre-harvest
sprouting can be a major problem for
cereal production in areas of the world
with higher humidity and rainfall.
Hormones and control of seed
germination
The key roles of ABA and another,
antagonistic plant hormone, gibberellin
(GA), in the control of seed dormancy
and germination are well established.
In Arabidopsis, tomato and wheat,
ABA-deficient and GA-biosynthetic and
Current Biology
Magazine
O2
H2O
tion
Current Biology
signalling mutants have strong seed
dormancy phenotypes. LAFL mutants,
which abrogate ABA responses,
alongside ABA-deficient mutants, are
completely unable to produce dormant
seeds whatever environment seeds
are set in. The DELLA proteins are
absolutely required for seed dormancy
and growth inhibition, and as such
plants harboring mutations in these
genes are also strongly non-dormant. In
contrast, strong GA-deficient mutants
and the GA-signalling mutant sleepy 1
are unable to germinate unless the seed
coat and endosperm are removed. This
highlights the central role of GA and
ABA responses in seed dormancy and
germination control. However, other
hormones are also involved and may
be particularly important in certain
species. Ethylene is a germination
stimulant that likely promotes
Current Biology
Magazine
germination by degradation of ERF
transcription factors that mediate
reactive oxygen and reactive nitrogen
signalling in seeds. And in the parasitic
plant species Striga, germination is
strongly contingent on the perception
of secreted strigolactone from host
plant roots. It seems that evolution has
modified a common signalling network
in different species in distinct ways,
allowing the importance of different
aspects of the germination process
to vary. Natural variation in seed
dormancy also seems to be affected
by two important loci, REDUCED
DORMANCY 5 (RDO5) and DELAY OF
GERMINATON 1 (DOG1), which appear
to primarily interact with ABA signalling
pathways to modulate germination.
In temperate environments,
temperature is the dominant seasonal
signal controlling seed dormancy.
Some species have simple temperature
requirements for germination, such as
cool temperatures or a period of cold
or warm stratification. Others have
complex requirements for alternate
daily temperature fluctuations, or
prolonged incubations at cool and
warm temperatures to promote
germination. A good example is the
European ash (Fraxinus excelsior),
which requires a period of cold to
remove physiological dormancy
and a period of warm to overcome
morphological dormancy. Thus, there
is a period of the year that precedes
seedling emergence in which the seeds
lose dormancy and can germinate if
given light. If they don’t see light during
this period they will re-enter dormancy,
then known as secondary dormancy,
and wait in the seed bank for the
next emergence window. A second
dormancy-breaking process, and one
frequently in a laboratory setting, is
dry after-ripening. This is an obscure
process by which dormancy is lost over
weeks or months during dry storage,
and opinion is divided as to whether
dry after-ripening is an adaptive
response relevant to seeds in real soils,
or whether it is an artefact of storage of
seeds in very dry conditions not found
in nature, except in the most extreme
habitats. The mechanism of dry after-
ripening is unclear, but after imbibition
a signal specific to after-ripened
seeds activates ABA catabolism. A
common feature of environmental
signals that break primary dormancy,
including both temperature and after-
ripening, is a transcriptional effect
on the CYTOCHROME P450 707A
(CYP707A) gene family, members of
which catabolise the ABA necessary to
maintain dormancy. The corresponding
drop in ABA levels permits GA
synthesis and the events surrounding
germination to subsequently begin.
In addition to pure seasonal cues,
other signals are used to detect
changes in the canopy that suggest
an opportunity to establish. Nitrate is
a key signal molecule that increases
in the soil in the absence of a
growing canopy. Applying nitrate to
seeds — either during seed maturation
or after imbibition — strongly promotes
germination. As with responses to
other environmental signals, nitrate
appears to act by interacting with
hormone metabolism in seeds. In
Arabidopsis, NIN-like protein 8 (NLP8)
is a key nitrate sensor and promotes
germination in the presence of nitrate
by the direct transcriptional regulation
of CYP707A gene expression. Fire is
a second important canopy signal,
and specific compounds in smoke,
known as karrikins, have a strong
germination-promoting activity. In
ecosystems where fire is a common
disturbance, plants have evolved
to recognise these karrikins as
signals that indicate an opportunity
for seedling establishment. Karrikin
signalling appears to share elements
of the strigolactone signalling
pathway, but also appear to have
their own specific receptor. Thus,
it has been hypothesised that the
karrikin receptor recognises an as
yet unknown plant hormone, as
well as compounds from smoke.
Light is a final important cue for
germination promotion in seeds with
low dormancy. Absence of light may
indicate burial, and many plants use
the red/far red ratio detected by
phytochromes to signal the presence
of a leafy canopy and prevent
germination. Phytochrome signalling
control of germination is contingent
on the interaction of phytochromes
with specific transcription factors
that control ABA metabolism and
GA production. In contrast, for many
species darkness is more favourable
for germination, and germination
can be prevented by blue light,
perceived by cryptochromes. Such a
Current Biology 27, R853–R909, September 11, 2017 R877
mechanism is common in monocots,
including wheat and barley, where
cryptochrome signalling represses
CYP707A gene expression and lowers
seed germination rates in the light.
Functions of different seed tissues
during the decision to germinate
After imbibition of the seed, the
different seed tissues have distinct
roles in the decision to germinate
(Figure 2). For seeds with coat-
imposed dormancy, ABA is primarily
produced in the endosperm tissue;
specific transporters then export
ABA from the endosperm into the
embryo. In cereal seeds, it is especially
clear that during germination GA is
produced by the embryo, and its arrival
in the aleurone layer of the endosperm
initiates the breakdown and
mobilisation of stored endospermic
carbon reserves. Indeed, metabolic
activation, vacuolisation and reserve
mobilisation of endosperm cells are
the first visible signs that a seed has
transitioned to germination. These
events are followed by expansion
of embryo cells that lead to testa
rupture, endosperm rupture and radicle
emergence. In Arabidopsis, the root
apical meristem appears to be an
important site of GA production in
the embryo. There is good evidence
from a number of studies that a
GA-derived signal moves from the
root to activate water uptake and
metabolism in the basal cells of
the hypocotyl. The subsequent
expansion of hypocotyl cells is driven
by the GA-dependent regulation of
homeodomain transcription factors,
and is the principle cellular event in the
embryo that provides the mechanical
force for radicle emergence. At this
time, ribosome synthesis increases
and an apparent translational block
is released, allowing translation of
the key proteins at the heart of basic
metabolic processes and cell growth.
The endosperm also responds by
secreting cell wall-loosening enzymes
from the micropylar pole that weaken
the attachments between micropylar
endosperm cells to facilitate radicle
emergence. All these events are
under the inhibitory control of ABA in
dormant seeds and are promoted by
GA in germinating seeds. The relative
importance of these events in the
control of germination is likely to differ

in seeds with different ratios of embryo
and endosperm in the mature seed.
Much of our recent understanding
of germination control comes from
work in Arabidopsis, or other, highly
unnatural systems such as our major
crops. Considerably less is known
about the mechanisms underlying more
exotic seed behaviour and seasonal-
dormancy regulation in seeds present
in the soil bank. The biology of seed
germination is also highly relevant to
seed technology, the field of seed-
performance enhancement that
underpins the consistent production of
high-quality crop seeds, particularly for
the vegetable seed market. In the future it
should be possible to harness advances
in our understanding of seed germination
to make improvements to seed
performance for farmers and growers.
FURTHER READING
Bassel, G.W., Stamm, P., Mosca, G., Barbier de
Reuille, P., Gibbs, D.J., Winter, R., Janka, A.,
Holdsworth, M.J., and Smith, R.S. (2014).
Mechanical constraints imposed by 3D cellular
geometry and arrangement modulate growth
patterns in the Arabidopsis embryo. Proc. Natl.
Acad. Sci. USA 111, 8685–8690.
Chen, M., MacGregor, D.R., Dave, A., Florance,
H., Moore, K., Paszkiewicz, K., Smirnoff, N.,
Graham, I.A., and Penfield, S. (2014). Maternal
temperature history activates Flowering
Locus T in fruits to control progeny dormancy
according to time of year. Proc. Natl. Acad. Sci.
USA. 111, 18787–18792.
Chiang, G.C., Barua, D., Kramer, E.M., Amasino,
R.M., and Donohue, K. (2009). Major flowering
time gene, flowering locus C, regulates seed
germination in Arabidopsis thaliana. Proc. Natl.
Acad. Sci. USA 106, 11661–11666.
Gibbs, D.J., Lee, S.C., Isa, N.M., Gramuglia, S.,
Fukao, T., Bassel, G.W., Correia, C.S.,
Corbineau, F., Theodoulou, F.L., Bailey-
Serres, J., and Holdsworth, M.J. (2011).
Homeostatic response to hypoxia is regulated
by the N-end rule pathway in plants. Nature
479, 415–418.
Hamilton, W.D. and May, R.M. (1977). Dispersal in
stable habitats. Nature 269, 578–581.
Kang, J., Yim, S., Choi, H., Kim, A., Lee, K.P.,
Lopez-Molina, L., Martinoia, E., and Lee, Y.
(2015). Abscisic acid transporters cooperate
to control seed germination. Nat. Commun. 6,
8113.
Piskurewicz, U., Iwasaki, M., Susaki, D., Megies,
C., Kinoshita, T., and Lopez-Molina, L. (2016).
Dormancy-specific imprinting underlies
maternal inheritance of seed dormancy in
Arabidopsis thaliana. Elife 5, e19573.
Springthorpe, V., and Penfield, S. (2015). Flowering
time and seed dormancy control use external
coincidence to generate life history strategy.
eLife 4, e05557.
Yan, D., Easwaran, V., Chau, V., Okamoto, M.,
Ierullo, M., Kimura, M., Endo, A., Yano, R.,
Pasha, A., Gong, Y., et al. (2016). NIN-like
protein 8 is a master regulator of nitrate-
promoted seed germination in Arabidopsis. Nat.
Commun. 7, 13179.
Department of Crop Genetics, John Innes
Centre, Norwich, NR4 7UH, UK.
E-mail: steven.penfield@jic.ac.uk
R878 Current Biology 27, R853–R909, September 11, 2017 © 2017 Elsevier Ltd.
Primer
Radial plant growth
Nina Tonn and Thomas Greb*
One of the extraordinary features
of plants is their growth capacity.
Depending on the species and the
environment, body forms are manifold
and, at the same time, constantly
reshaped. An important basis of
this plastic variation and life-long
accumulation of biomass is radial
growth. Here, we use this term to
describe the ability to grow in girth
by the formation of wood, bast and
cork. The more technical term for
radial growth is secondary growth,
which distinguishes the process from
primary growth taking place at the
tips of stems and roots during plant
elongation.
After reaching a certain size,
most plants start producing wood
at the periphery of their organs,
which transports water and nutrients
and is also essential to support
the increasing body weight. At
the same time, bast is produced,
which transports sugars and growth
hormones throughout the entire body.
As a protective tissue, cork prevents
water loss, microbial infections and
physical damage. Illustrating the
impact of radial growth on plant
performance, there are distinct
examples having even a world-wide
reputation. The ‘Hyperion’ redwood
in Northern California is, at 115 m
tall, one of the record holders in
organismal height; the trunk girth
of the ‹Árbol del Tule› in Mexico
is 11 m; and the age of the Great
Basin bristlecone pine in the White
Mountains of California is around
5000 years. On the cellular level,
all these huge and long-lasting
structures derive from radial growth,
and seemingly non-impressive
tissues running through stems and
roots — the vascular and the cork
cambium.
In this Primer, we highlight the
evolutionary history of radial plant
growth, which underlines the
urgent need for plants to be able to
modulate long-distance transport
capacities throughout their whole life
cycle. We explain how the vascular
Current Biology
Magazine
cambium determines this growth
process and why earlier cambial
systems may have disappeared
during evolution. We also give
examples for the diversity of plant
growth forms due to variation in
cambium activity, and provide a brief
insight into the molecular players
regulating fundamental aspects of
cambium-derived tissue production.
A short glimpse on the importance
of the process for our daily life
concludes this overview.
The invention of a new skill
Nowadays, most plants grow radially
throughout their entire life. It has
been proposed that the evolution of
radial growth began during the Early
Devonian (~400 Mya), supporting the
transition from sea to land (Figure 1).
Long-distance transport of water and
nutrients and mechanical stability
in a gaseous environment were only
a few of the many challenges to be
faced during this transition. Some
extant land plants — including
liverworts, hornworts and mosses
(bryophytes) — still exclusively rely on
primary growth and, in this respect,
resemble the first land plants. Fossils
indicate that those plants had one
central strand of water-conducting
tissue which was notably small
compared with the diameter of the
whole organ. They also formed only
very simple water-conducting cells
with smooth, thickened cell walls
and pores, as found in hydroids of
today’s bryophytes. Hydroids are
elongated, dead cells often located in
the centre of organs, which lack the
more sophisticated cell-wall structure
of modern vascular elements.
They also do not deposit lignin,
a hydrophobic polymer providing
resistance against compression
and microbial decomposition in cell
walls of higher plants. Consequently,
body stability of early land plants
was predominantly based on turgor
pressure of parenchymatous cells
rather than on cell wall rigidity on its
own. Furthermore, since roots did not
yet exist, anchorage was rather poor
and uptake of water and nutrients
was achieved by simple structures
named rhizoids. Other features
present in modern land plants were
likewise missing, including stomata
as specialized structures for gas