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The effect of water motion on
short-term rates of photosynthesis
by marine phytoplankton
Hugh L. MacIntyre, Todd M. Kana and Richard J. Geider
Phytoplankton respond to variations in light intensity as they are mixed through the water
column. Changes in pigment content are characteristic of the relatively slow response of
‘sun–shade’ photoacclimation that occurs on timescales typical of mixing in the open ocean.
In estuaries, the variations are much faster and induce correspondingly rapid changes in the
activity (rather than abundance) of different components of the photosynthetic apparatus.
These components modulate light harvesting and Calvin cycle activity, or protect the pigment
bed from excess energy absorption. When the protective capacity is exceeded, photoinhibition
occurs. All these mechanisms modulate the rate of photosynthesis in situ.
P
lanktonic microalgae (phytoplankton) live in diverse and
highly variable environments. Their photosynthetic apparatus
is subject to significant stresses because of rapid changes or
imbalances in irradiance and nutrient supply imposed by the physics
and chemistry of natural water bodies. The ways in which the photosynthetic apparatus adjusts to these temporally variable and
complex environments are of interest for both practical and fundamental reasons, because phytoplankton photosynthesis is responsible for ~50% of global productivity. Modern techniques for
assessing productivity on global scales rely on remotely sensing
plankton’s optical properties, using the signature of chlorophyll as an
index of abundance (Fig. 1). The emphasis on chlorophyll is
inevitable given chlorophyll’s distinctive optical characteristics,
which enables plant material to be distinguished from other suspended matter. The relationship between chlorophyll and organic
carbon (the desired currency for productivity models) is highly
plastic, varying with growth, irradiance, nutrient availability and
temperature. However, the variability is ordered, not random, and
knowledge about the effects of environmental variables on the
efficiency of light absorption and its conversion to biomass during
photosynthesis allows estimates of chlorophyll abundance to be
translated into carbon equivalents.
Understanding the effect of varying environmental conditions
on photosynthetic rates can be considered in terms of the regulation
of the amounts and the specific activities of components of the photosynthetic apparatus. Regulation can be accomplished by variations
in the relative abundance of the constituents [e.g. chlorophyll and
ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco)] or, on
a shorter timescale, by varying the efficiency of their coupling and
activity (e.g. the activation state of Rubisco). The distinction is
blurred at some levels but serves to distinguish between those means
of photosynthetic regulation that depend on synthesis or turnover
(usually of chlorophyll) in photoacclimation, and those that
depend on more rapid changes in activation states or efficiencies,
independent of turnover. Work in this area is complicated by the
fact that phytoplankton include representatives of four kingdoms1
and are highly variable in their molecular, structural and optical
properties. Whereas physiological studies have focused largely on
taxa that are easy to maintain in culture, particularly chlorophytes
and diatoms. It has been challenging to bring qualitative information
on photosynthetic mechanisms together with quantitative kinetic
information on rates of response to understand cellular photosynthesis in the natural environment. Here we review recent
developments in our understanding of how phytoplankton photosynthesis adjusts to naturally
variable environments.
The principal environmental
factors that affect phytoplankton photosynthesis are light,
nutrient availability and temperature. In nature, these factors
operate independently on timescales that match photosynthetic
physiology, presenting a complex and unpredictable environment to the cells. Phytoplankton respond to such
stochastic environments using
a variety of physiological
processes that affect light
Fig. 1. Composite false-color image of mean annual ocean chlorophyll concentrations, as detected by satellite
remote-sensing. Chlorophyll is used as an index of biomass in seawater because, unlike other organic compounds,
harvesting efficiency and
it is unique to phytoplankton and common to all autotrophs. Note the higher concentrations near the land
photosynthetic capacity. Two
key issues are at the forefront
of ecophysiological research:
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trends in plant science
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• What are the kinetic constraints on processes that modulate
photosynthesis in rapidly fluctuating environments?
• What are the mechanisms by which cells integrate multiple environmental factors in regulating their physiological responses?
These questions are related: the photosynthetic mechanisms that
modulate energy and material flow through the cell are common
to phytoplankton in spite of their diversity. Significant conceptual
advances have been made recently that tie whole-cell physiology
with photosynthetic regulatory processes operating at the biochemical and biophysical levels.
Environmental control of photosynthetic processes
By definition, phytoplankton are incapable of sustained directional movement and therefore are subject to the environmental
conditions in their parent body of water. Photosynthesis is responsive to changes in nutrient availability on short timescales2 but in
marine systems the changes are more likely to occur over relatively long timescales (days to seasons). Although nutrient availability is critical for determining population dynamics3 and the
ultimate determinant of the geographic abundance of phytoplankton
(Fig. 1), nutrient availability is less likely to drive short-term
changes in photosynthetic rates. Because of water’s capacity for
high levels of latent heat, temperature is more likely to vary on daily
to seasonal scales, and in a manner predictable from the balance of
radiative transfer and evaporative cooling. By contrast, phytoplankton are subject to relatively rapid changes in both the intensity and the spectral quality of light as they move vertically in a
water column (Box 1). In addition to the changes imposed by
mixing, there are variations in the light field with timescales of
hours, minutes and milliseconds4 as a result of changes in solar
elevation, cloud cover and subsurface focusing by waves. Photosynthesis and growth rates appear to be insensitive to variability in
the millisecond domain5, therefore we will focus on variations that
occur on a timescale of minutes and hours.
Photoacclimation of pigment content
conditions, plastoquinone is largely oxidized, and transcription of
the mRNAs that code for the proteins that bind chlorophyll in the
antenna occurs at maximal rates. As irradiance increases, photosynthesis control passes from light harvesting to the maximum
capacity for carbon dioxide fixation, the plastoquinone becomes
increasingly reduced, and transcription of the mRNAs for pigment–protein complexes declines. The end results of this mode of
regulation can be mimicked by ‘energy balance’ models developed recently10,11. These are based on the concept of a physiological light sensor that regulates the pigment quota to maintain a
balance between the harvesting of excitation energy by means of
light absorption and photochemistry on the one hand and the energetic demands of growth on the other. Conceptually, this is comparable to the redox regulation of the antenna protein LHCII
(Refs 9,12). These models can account for steady-state responses
and for the differences in the rates of acclimation that are observed
following shifts from low-to-high versus high-to-low irradiance,
without the potential errors imposed by specifying a mathematical
function to describe the kinetics of photoacclimation13.
Photosynthetic Induction
The time-course of light intensity changes in estuarine waters is
much faster than in coastal or open-ocean waters because both the
rate of light attenuation and the rate of mixing are much higher
(Box 1). Two mechanisms, the activation and deactivation of
Rubisco and state transitions, have time constants that are comparable to the timescale of mixing in estuarine waters and probably
dominate short-term rates of photosynthesis (Fig. 2).
Photosynthetic regulation operating by means of the catalytic
activity of Rubisco can be controlled by variations in the enzyme
concentration or, in the short-term, by its activation state.
Although the enzyme cellular concentration might not be regulated during photoacclimation under nutrient-replete conditions,
depending on the taxon8, it is regulated in response to chronic
phosphorus or nitrogen limitation14. Because there is a correlation
between the maximum quantum efficiency (fm) and the ratio of
Rubisco to the PSII reaction center protein D1, changes in the pool
size of Rubisco might play a role in regulating acclimated photosynthetic rates during nutrient-limited growth.
A potential role for activation and deactivation of Rubisco
in the short-term limitation of photosynthetic rates hinges
on the assumption that at light saturation, the rate of photosynthesis depends on the enzyme’s activity. Broad conclusions are
complicated by the diversity in microalgal Rubisco structure and
For a given temperature and nutrient status, photoacclimation in
phytoplankton can be described in terms of regulation of the cell
concentrations of the catalysts that determine light-limited and
light-saturated photosynthetic rates. The rate of light absorption,
which co-varies with a cell’s chlorophyll concentration, is often
the primary determinant of light-limited photosynthesis, whereas
the maximum rate of carbon dioxide fixation, which co-varies
with Rubisco concentration, is the primary determinant of lightsaturated photosynthesis. The
cell chlorophyll content is usually higher in cells that have
Box 1. Variations in the submarine light field
grown under low light6. Variations in other constituents of
The light attenuation within any body of water follows (approximately) the Lambert–Beer law, decreasing expothe photosynthetic apparatus
nentially with depth. The rate and spectral dependence of attenuation depends on the abundance of phytoplankton,
appear to be taxon-specific: of
detritus (which includes organic material of biogenic origin and suspended sediment) and chromophoric
two studies of cells grown
dissolved organic matter (CDOM, mainly humic and fulvic acids of terrestrial origin).
under nutrient-replete condiIn estuarine waters, terrestrial runoff that is high in humics and plant nutrients, and close coupling between the
benthos and water column results in high absorption by CDOM, phytoplankton and detritus in blue light. The domtions, the concentration of
inant penetrating wavelengths are therefore red and the intermediate green (Fig. 3). Attenuation is rapid: in an
Rubisco decreased at low
extreme case, the euphotic zone (the depth to which 1% of sunlight penetrates) is ,0.5 m.
growth irradiance in a diatom7
In oceanic waters, the abundance of CDOM, detritus and phytoplankton is low and the dominant attenuator is
whereas it remained unchanged
water itself, which is highly absorbent in red light. The dominant penetrating wavelengths are therefore blue light
8
in a chlorophyte . Synthesis
(Fig. 3). The euphotic zone might be up to 140 m deep. Coastal waters are intermediate with respect to the magof pigment–protein complexes
nitude and spectral dependence of attenuation.
appears to be transcriptionally
The light regime experienced by phytoplankton also depends on the rate of mixing, which is much more rapid in
regulated by a mechanism
estuarine waters than coastal or open ocean waters. The effect of this, in combination with the more rapid attenthat is under the control of the
uation of light, means that estuarine phytoplankton can pass through a light gradient ranging from darkness to full
redox state of the plastosunlight in minutes. The same transient would take hours to days in the more stable and clearer ocean (Fig. 3).
quinone pool9. Under low-light
.
January 2000, Vol. 5, No. 1
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trends in plant science
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in illumination as it is mixed back up are
insufficient to allow much deactivation18.
There appears to be little role for Rubisco
oxygenase activity in phytoplankton.
Although the abundance of free CO2 in seawater (~10–15 mM) is well below the
half-saturation concentration of Rubisco
(30–170 mM)15,16, carbon concentrating
mechanisms that involve either active
transport of HCO32 or coupled dehydration
of HCO32 by a cell-surface carbonic anhydrase and CO2 transport, have been documented for cyanobacteria, chlorophytes19,
diatoms20 and dinoflagellates21,22. In addition, microalgal Rubiscos have high CO2
specificities compared with those from terrestrial plants. This might be because of
differences in the structure of the loop-6
region15 or in the length of the large subunit
C-terminus16, both of which appear to play
a role in the conformation of the active site
during catalysis. The dinoflagellates are
distinct from all other eukaryotes in having
a prokaryotic-type form II Rubisco23 (i.e.
one lacking the small subunit characteristic
of the eukaryotic form I). Although the specificity of dinoflagellate form II Rubisco is
higher than bacterial form II Rubisco24, it is
unlikely that it could support measured rates
Fig. 2. (a) The first-order reaction time constants (t, in minutes) of photosynthetic responses
to increases and decreases in light intensity vary from 104 min for changes in the chlorophyll
of photosynthesis without the presence of a
quota to 1021 min for inter-conversion of the xanthophylls diadinoxanthin and diatoxanthin.
carbon-concentrating mechanism.
Note that time constants for increases in irradiance (denoted ‘up’) are shorter than for
A second phenomenon that might drive
decreases (denoted ‘down’), except in the case of the chlorophyll-specific light-saturated rate
the short-term photosynthetic response in
of photosynthesis, Pm/Chl, where the kinetics are driven by changes in the chlorophyll quota.
estuarine waters is the occurrence of state
The time constant defines the rate of change of species X over a time-step of duration Dt as:
transitions25, which are rapid adjustments
Xt 1 Dt 5 Xt exp(Dt/2tdown)
in the relative magnitudes of the photosysfor a decrease in irradiance and as:
tem I (PS I) and photosystem II (PS II)
Xt 1 Dt 5 Xt [1 2 exp(Dt/2tup)]
antennae. State 2 (preferential excitation of
PS I) is favored under conditions of high
for an increase.
absolute irradiance and under darkness,
The time taken for the light level to either double or halve for cells in simulated oceanic and
estuarine water (Fig. 3) is indicated by arrows. Sources for the time constants are given in
whereas State 1 (preferential excitation of
parentheses. (b) The essence of mixing-based productivity models is defining a step-change in
PS II) is favored under conditions in which
irradiance because of a cell’s motion through a light gradient (compare with Fig. 3) and implethe spectrum is dominated by red light.
menting the time-dependence of photosynthetic response via time constants (tup and tdown) that
Consequently cells in estuarine waters are
describe the change in response to increases and decreases in light intensity (a). These contrast
driven to State 2 at aphotic depths (depths
with steady-state models (black unbroken line), in which no time-dependence is allowed (i.e.
to which light does not penetrate because
the effect of light level fluctuations is ignored). In acclimation or induction models (left),
of complete attenuation by the overlying
instantaneous estimates of productivity are almost always lower than in the steady-state rate,
water), to State 1 at intermediate depths
because of the time-lag inherent in the response as the photosynthetic mechanism adjusts to a
where the spectrum is weighted towards
change in light level. In inhibition models (right), instantaneous estimates of productivity can
long wavelengths (Fig. 3), and back to
be higher or lower than in the steady-state condition, because the steady-state rate is an empirically-derived average over a period that might be long compared with the accumulation of phoState 2 at the surface4,25. It is not clear what
effect, if any, state transitions have on photosynthetic rates, but the interchange time
constants are close enough to the rate of
catalytic characteristics15,16. However, activity changes in those mixing that the transitions can be observed in cyanobacteria and
few microalgae that have been studied are consistent with models chlorophytes from turbid waters25. State transitions are unlikely to
of regulation by means of carbamylation–decarbamylation and, in limit photosynthetic rates in the ocean because the timescale of
addition, possibly, by a tight-binding inhibitor, such as carboxy- mixing is slower, and because red light is more rapidly attenuated
arabinitol-1-phosphate17. The kinetics of activation and deacti- than blue light (Fig. 3). State transitions have yet to be docuvation could affect photosynthetic rates in response to rapid mented from chromophytic microalgae.
increases in light intensity during mixing. Because activation is
much faster than deactivation, the effect is less pronounced during Photoprotection
rapid mixing because the interval between decreases in illumi- The most complex group of photosynthetic responses includes the
nation as a cell is mixed away from the well-lit surface and increases transients associated with photoprotection and photoinhibition.
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Photoprotective mechanisms can broadly be described as those
that either decrease the absorption of light energy (by reducing the
absorption cross section or effective photosynthetic cross-section
of the reaction centers), or provide alternative energy sinks when
photosynthetic capacity is exceeded. Change in the excitation
delivery includes rapid responses, such as induction of energy-dissipating pigments in xanthophyll cycles26,27, and slower responses,
such as photoacclimative changes in the size and pigment composition of the antennae (Fig. 2). Two different xanthophyll cycles
are found in chlorophytes and chromophytes: in chlorophytes,
violaxanthin is de-epoxidated to zeaxanthin in a two-step pathway,
with antheraxanthin as an intermediate; in chromophytes diadinoxanthin is de-epoxidated to diatoxanthin in a single step. Although
the chlorophytes have a pathway that is structurally similar to vascular plants’, the relationship between non-photochemical energy
quenching and the level of de-epoxidation is different28. Conversely,
although chromophytes have a different pathway, the relationship between non-photochemical quenching and the level of
de-epoxidation is comparable to that in vascular plants.
Other electron sinks
In addition to xanthophyll cycling, there are other mechanisms
that might act as sinks for electrons when PS II activity exceeds
photosynthetic capacity. For example, cyanobacteria lack a xanthophyll cycle but exhibit strong Mehler activity at light saturation29,
and diatoms appear to be unique in using non-assimilatory nitrate
reduction as a sink30. Both pathways bleed off excess energy from
the electron transport chain when NADPH turnover is operating at
the maximum rate, preventing over-excitation of the photosynthetic antennae.
Photoinhibition
When the photoprotective mechanisms already described are
exceeded, damaged PS II reaction centers, lacking a functional D1
protein, can accumulate. The reconstitution of functional PS II
reaction centers can be described by first-order reaction kinetics
when cells are moved to non-inhibitory irradiance31. Modeling the
accumulation of damaged D1 might be more difficult because of
the diversity of photoprotective responses, the protective capacity
of which depends on both the light history and nutrient status of
the cell26. However, photo-inactivation of D1 can be modeled by
target theory32, opening the possibility that photosynthesis could
then be described using the relationship between the proportion of
inactive PS II reaction centers and the quantum efficiency.
Kinetic models and the time-dependence of
photosynthetic physiology
Short-term variability in photosynthetic rates can be accounted for in
productivity models using time-dependent relationships. Generally,
two assumptions are made, namely that the ocean can be considered
as a one-dimensional system in the vertical and (in many models)
that the time-dependence of photosynthetic processes follow firstorder reaction kinetics. With an adequate understanding of the vertical variation in mixing rate, the trajectories of groups of cells can be
described by a random walk simulation (the vertical steps of which
are defined in time by the local turbulent diffusivity) using a
Lagrangian ensemble model. Given the rate of light attenuation,
changes in light intensity can be described as a function of depth and
time (Fig. 3). The sensitivity of photosynthesis to mixing can then be
described by specifying the time-dependence of the response to
changing light intensity with one or more time constants (Fig. 2).
Separate time constants for upward and downward movements are
usually employed to account for different physiological rate constants
associated with responses to increases and decreases in irradiance.
Fig. 3. Light absorption in oceanic waters (a) is almost wholly
dependent on phytoplankton (black line) and water itself (gray
line), in contrast with estuarine waters (b), where detritus (broken
black line) and chromophoric dissolved organic material (bold,
black line) also make a substantial contribution (note different
scales). As a consequence, both the magnitude and spectral
dependence of underwater light are different. (c) The attenuation
of incident sunlight (0 m) is more pronounced in red light
(depicted by light gray) than blue light (depicted by dark gray) in
oceanic water, in contrast with estuarine water (d), were blue light
is attenuated more rapidly than red light. Light intensity is
expressed as PAR (photosynthetically active radiation), which is
the integral of irradiance between 400 and 700 nm. The blue and
red absorbance peaks of plant pigments are shown. The spectral
composition of light is shown at different depths that correspond
to either a doubling or a halving in the intensity of PAR. Higher
turbulence and more rapid attenuation in the estuarine water
results in entrained cells experiencing more rapid transients in
light intensity (f) than in the oceanic water (e). Note the difference
in scales. Exposure was calculated from the spectrally dependent
attenuation coefficient for a cell that was released into the middle
of a mixed layer and whose trajectory was based on a random
walk model.
January 2000, Vol. 5, No. 1
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The approach has been used to model the sensitivity of photosynthesis to changes that are characteristic of photoacclimation33,
photoinhibition34 and photosynthetic induction18. The relative
importance of different photosynthetic mechanisms depends on
the timescale and the magnitude of the changes in the light field
(i.e. if the time constant for the metabolic response is longer than
the characteristic timescale of change, the mechanism has the
potential to limit the reaction rate13; Fig. 2). Constructing a general model of the effect of mixing on photoinhibition that is analogous to the acclimative models depends on a somewhat arbitrary
level of calibration because both the degree and rate of accumulation of photoinhibitory damage are less constrained than acclimative changes (Fig. 2). One approach, which is based on first
principles, involves defining an action spectrum of the doseresponse of photoinhibition and using a biological weighting
function to drive the onset of photoinhibition and the subsequent
recovery as cells are mixed through a water column35.
A description based on energy-balance models is an alternative
to the descriptions of photoacclimation based on explicit timeconstants of chlorophyll-specific photosynthetic responses. In
energy-balance models, a physiological sensor regulates the pigment quota as a means of balancing excitation-energy harvesting
with the energetic demands of growth. By specifying both as rates
and using units of inverse time (which necessitates converting the
currency of electrons to carbon equivalents), the imbalance can be
used to drive changes in energy harvesting, either by inducing
chlorophyll synthesis or D1 turnover10,11 until equilibrium is reestablished. Embedding such an energy-balance model into a
physical model of mixing produces results that are consistent with
field measurements over wide temporal and spatial scales (annual
cycles from 0 to 608 N)36. Because the regulated term is the ratio
of phytoplankton chlorophyll to carbon (an index of the pigment
quota), energy-balance models can be reconciled with large-scale
estimates of phytoplankton biomass (Fig. 1), and the response has
an explicit dependence on temperature and nutrient (nitrogen)
availability. These dependencies have not been quantified for
first-order kinetic models, in which both the time constants and
the end-points of acclimation might depend on temperature and
nutrient status.
The future
It is now possible to evaluate how the photosynthetic apparatus
is regulated under complex environmental forcing. The complexity of the environment–photosynthesis relationship is
tractable using the notion of energy-balance regulation: the
redox state of the light reactions is a universal signal in microalgae for regulating cellular light harvesting efficiency. The
success of recent pigment-photoacclimation models that incorporate an energy-balance regulatory ‘signal’ based on the redox
state, holds promise for more sophisticated models that incorporate short-term energy modulation mechanisms. These models
can be made species-specific by setting parameters according to
the specific energy modulation processes that are present. Future
work on environmental effects will distinguish short-term
kinetically constrained responses from longer-term energybalance-constrained responses. This will clarify the relative
importance of kinetic versus acclimative responses to particular
environments.
Acknowledgements
We thank two anonymous reviewers for their comments on the
manuscript. This work was supported by Grants OCE-9730098
and OCE-9633633 from the National Science Foundation (USA)
and is contribution No. 3239 from Horn Point Laboratory.
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January 2000, Vol. 5, No. 1
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36 Taylor, A.H. et al. (1997) Seasonal and latitudinal dependencies of
phytoplankton carbon-to-chlorophyll a ratios: results of a modelling study.
Mar. Ecol. Prog. Ser. 152, 51–66
Hugh L. MacIntyre* and Todd M. Kana are at the University of
Maryland Center for Environmental Research, Horn Point
Laboratory, PO Box 775, Cambridge, MD 21613, USA;
Richard J. Geider is at the Dept of Biological Sciences,
University of Essex, Colchester, UK CO3 4SQ.
*Author for correspondence (tel 11 410 221 8430;
fax 11 410 221 8490; e-mail macintyr@hpl.umces.edu).
Floral induction and determination:
where is flowering controlled?
Frederick D. Hempel, David R. Welch and Lewis J. Feldman
Flowering is controlled by a variety of interrelated mechanisms. In many plants, the environment
controls the production of a floral stimulus, which moves from the leaves to the shoot apex.
Apices can become committed to the continuous production of flowers after the receipt of
sufficient amounts of floral stimulus. However, in some plants, the commitment to continued flower
production is evidently caused by a plant’s commitment to perpetually produce floral stimulus
in the leaves. Ultimately, the induction of flowering leads to the specification of flowers at the shoot
apex. In Arabidopsis, floral specification and inflorescence patterning are regulated largely by
the interactions between the genes TERMINAL FLOWER, LEAFY and APETALA1/CAULIFLOWER.
F
loral induction is the process by which stimuli originating
outside the shoot apex induce the formation of flower primordia (Fig. 1). The photoperiodic induction of flowering
was discovered 86 years ago by Julien Tornois in hops1. Shortly
afterwards, additional experiments suggested that the photoperiodic control of flowering was a general phenomenon, which controlled flowering in most plants2. Later, focused-light experiments
showed that leaves perceive photoperiodic signals3. These studies,
and numerous grafting experiments, indicate that the production
of the photoperiod-induced floral stimulus4 occurs in the leaves of
a wide variety of flowering plants5–7.
In contrast with floral induction, floral determination can be
defined as the assignment of flower(ing) fate, which is persistent
even when the flower-inducing conditions no longer exist8,9.
Assays for floral determination include:
• Changing environmental conditions (from inductive to noninductive).
• Microsurgical removal of shoot apices, and the placement of
those apices into neutral environments8,10.
However, both types of determination assay have limitations, and
it is important to note that different determination assays might
yield alternative conclusions for the same primordia (the caveats
associated with determination experiments are discussed in Ref.
11). A third type of assay has been used to test leaf commitment to
the continued production of floral stimulus: in this assay, photoinduced leaves are removed from the plant following an inductive
treatment12.
In this review we discuss firstly a variety of experiments that
indicate the site(s) that control flowering. Secondly, we review
recent studies that indicate how a few key molecular players regulate the specification of flower primordia in Arabidopsis.
Floral determination assays
Photoperiodic assays for floral determination
The simplest type of determination assay is one in which plants
are moved to non-inductive conditions after various lengths of
time under inductive conditions. Using this method, the duration
of photoinduction treatment required to produce flowers can be
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The effect of water motion on
short-term rates of photosynthesis
by marine phytoplankton
Hugh L. MacIntyre, Todd M. Kana and Richard J. Geider
Phytoplankton respond to variations in light intensity as they are mixed through the water
column. Changes in pigment content are characteristic of the relatively slow response of
‘sun–shade’ photoacclimation that occurs on timescales typical of mixing in the open ocean.
In estuaries, the variations are much faster and induce correspondingly rapid changes in the
activity (rather than abundance) of different components of the photosynthetic apparatus.
These components modulate light harvesting and Calvin cycle activity, or protect the pigment
bed from excess energy absorption. When the protective capacity is exceeded, photoinhibition
occurs. All these mechanisms modulate the rate of photosynthesis in situ.
P
lanktonic microalgae (phytoplankton) live in diverse and
highly variable environments. Their photosynthetic apparatus
is subject to significant stresses because of rapid changes or
imbalances in irradiance and nutrient supply imposed by the physics
and chemistry of natural water bodies. The ways in which the photosynthetic apparatus adjusts to these temporally variable and
complex environments are of interest for both practical and fundamental reasons, because phytoplankton photosynthesis is responsible for ~50% of global productivity. Modern techniques for
assessing productivity on global scales rely on remotely sensing
plankton’s optical properties, using the signature of chlorophyll as an
index of abundance (Fig. 1). The emphasis on chlorophyll is
inevitable given chlorophyll’s distinctive optical characteristics,
which enables plant material to be distinguished from other suspended matter. The relationship between chlorophyll and organic
carbon (the desired currency for productivity models) is highly
plastic, varying with growth, irradiance, nutrient availability and
temperature. However, the variability is ordered, not random, and
knowledge about the effects of environmental variables on the
efficiency of light absorption and its conversion to biomass during
photosynthesis allows estimates of chlorophyll abundance to be
translated into carbon equivalents.
Understanding the effect of varying environmental conditions
on photosynthetic rates can be considered in terms of the regulation
of the amounts and the specific activities of components of the photosynthetic apparatus. Regulation can be accomplished by variations
in the relative abundance of the constituents [e.g. chlorophyll and
ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco)] or, on
a shorter timescale, by varying the efficiency of their coupling and
activity (e.g. the activation state of Rubisco). The distinction is
blurred at some levels but serves to distinguish between those means
of photosynthetic regulation that depend on synthesis or turnover
(usually of chlorophyll) in photoacclimation, and those that
depend on more rapid changes in activation states or efficiencies,
independent of turnover. Work in this area is complicated by the
fact that phytoplankton include representatives of four kingdoms1
and are highly variable in their molecular, structural and optical
properties. Whereas physiological studies have focused largely on
taxa that are easy to maintain in culture, particularly chlorophytes
and diatoms. It has been challenging to bring qualitative information
on photosynthetic mechanisms together with quantitative kinetic
information on rates of response to understand cellular photosynthesis in the natural environment. Here we review recent
developments in our understanding of how phytoplankton photosynthesis adjusts to naturally
variable environments.
The principal environmental
factors that affect phytoplankton photosynthesis are light,
nutrient availability and temperature. In nature, these factors
operate independently on timescales that match photosynthetic
physiology, presenting a complex and unpredictable environment to the cells. Phytoplankton respond to such
stochastic environments using
a variety of physiological
processes that affect light
Fig. 1. Composite false-color image of mean annual ocean chlorophyll concentrations, as detected by satellite
remote-sensing. Chlorophyll is used as an index of biomass in seawater because, unlike other organic compounds,
harvesting efficiency and
it is unique to phytoplankton and common to all autotrophs. Note the higher concentrations near the land
photosynthetic capacity. Two
key issues are at the forefront
of ecophysiological research:
12
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trends in plant science
Reviews
• What are the kinetic constraints on processes that modulate
photosynthesis in rapidly fluctuating environments?
• What are the mechanisms by which cells integrate multiple environmental factors in regulating their physiological responses?
These questions are related: the photosynthetic mechanisms that
modulate energy and material flow through the cell are common
to phytoplankton in spite of their diversity. Significant conceptual
advances have been made recently that tie whole-cell physiology
with photosynthetic regulatory processes operating at the biochemical and biophysical levels.
Environmental control of photosynthetic processes
By definition, phytoplankton are incapable of sustained directional movement and therefore are subject to the environmental
conditions in their parent body of water. Photosynthesis is responsive to changes in nutrient availability on short timescales2 but in
marine systems the changes are more likely to occur over relatively long timescales (days to seasons). Although nutrient availability is critical for determining population dynamics3 and the
ultimate determinant of the geographic abundance of phytoplankton
(Fig. 1), nutrient availability is less likely to drive short-term
changes in photosynthetic rates. Because of water’s capacity for
high levels of latent heat, temperature is more likely to vary on daily
to seasonal scales, and in a manner predictable from the balance of
radiative transfer and evaporative cooling. By contrast, phytoplankton are subject to relatively rapid changes in both the intensity and the spectral quality of light as they move vertically in a
water column (Box 1). In addition to the changes imposed by
mixing, there are variations in the light field with timescales of
hours, minutes and milliseconds4 as a result of changes in solar
elevation, cloud cover and subsurface focusing by waves. Photosynthesis and growth rates appear to be insensitive to variability in
the millisecond domain5, therefore we will focus on variations that
occur on a timescale of minutes and hours.
Photoacclimation of pigment content
conditions, plastoquinone is largely oxidized, and transcription of
the mRNAs that code for the proteins that bind chlorophyll in the
antenna occurs at maximal rates. As irradiance increases, photosynthesis control passes from light harvesting to the maximum
capacity for carbon dioxide fixation, the plastoquinone becomes
increasingly reduced, and transcription of the mRNAs for pigment–protein complexes declines. The end results of this mode of
regulation can be mimicked by ‘energy balance’ models developed recently10,11. These are based on the concept of a physiological light sensor that regulates the pigment quota to maintain a
balance between the harvesting of excitation energy by means of
light absorption and photochemistry on the one hand and the energetic demands of growth on the other. Conceptually, this is comparable to the redox regulation of the antenna protein LHCII
(Refs 9,12). These models can account for steady-state responses
and for the differences in the rates of acclimation that are observed
following shifts from low-to-high versus high-to-low irradiance,
without the potential errors imposed by specifying a mathematical
function to describe the kinetics of photoacclimation13.
Photosynthetic Induction
The time-course of light intensity changes in estuarine waters is
much faster than in coastal or open-ocean waters because both the
rate of light attenuation and the rate of mixing are much higher
(Box 1). Two mechanisms, the activation and deactivation of
Rubisco and state transitions, have time constants that are comparable to the timescale of mixing in estuarine waters and probably
dominate short-term rates of photosynthesis (Fig. 2).
Photosynthetic regulation operating by means of the catalytic
activity of Rubisco can be controlled by variations in the enzyme
concentration or, in the short-term, by its activation state.
Although the enzyme cellular concentration might not be regulated during photoacclimation under nutrient-replete conditions,
depending on the taxon8, it is regulated in response to chronic
phosphorus or nitrogen limitation14. Because there is a correlation
between the maximum quantum efficiency (fm) and the ratio of
Rubisco to the PSII reaction center protein D1, changes in the pool
size of Rubisco might play a role in regulating acclimated photosynthetic rates during nutrient-limited growth.
A potential role for activation and deactivation of Rubisco
in the short-term limitation of photosynthetic rates hinges
on the assumption that at light saturation, the rate of photosynthesis depends on the enzyme’s activity. Broad conclusions are
complicated by the diversity in microalgal Rubisco structure and
For a given temperature and nutrient status, photoacclimation in
phytoplankton can be described in terms of regulation of the cell
concentrations of the catalysts that determine light-limited and
light-saturated photosynthetic rates. The rate of light absorption,
which co-varies with a cell’s chlorophyll concentration, is often
the primary determinant of light-limited photosynthesis, whereas
the maximum rate of carbon dioxide fixation, which co-varies
with Rubisco concentration, is the primary determinant of lightsaturated photosynthesis. The
cell chlorophyll content is usually higher in cells that have
Box 1. Variations in the submarine light field
grown under low light6. Variations in other constituents of
The light attenuation within any body of water follows (approximately) the Lambert–Beer law, decreasing expothe photosynthetic apparatus
nentially with depth. The rate and spectral dependence of attenuation depends on the abundance of phytoplankton,
appear to be taxon-specific: of
detritus (which includes organic material of biogenic origin and suspended sediment) and chromophoric
two studies of cells grown
dissolved organic matter (CDOM, mainly humic and fulvic acids of terrestrial origin).
under nutrient-replete condiIn estuarine waters, terrestrial runoff that is high in humics and plant nutrients, and close coupling between the
benthos and water column results in high absorption by CDOM, phytoplankton and detritus in blue light. The domtions, the concentration of
inant penetrating wavelengths are therefore red and the intermediate green (Fig. 3). Attenuation is rapid: in an
Rubisco decreased at low
extreme case, the euphotic zone (the depth to which 1% of sunlight penetrates) is ,0.5 m.
growth irradiance in a diatom7
In oceanic waters, the abundance of CDOM, detritus and phytoplankton is low and the dominant attenuator is
whereas it remained unchanged
water itself, which is highly absorbent in red light. The dominant penetrating wavelengths are therefore blue light
8
in a chlorophyte . Synthesis
(Fig. 3). The euphotic zone might be up to 140 m deep. Coastal waters are intermediate with respect to the magof pigment–protein complexes
nitude and spectral dependence of attenuation.
appears to be transcriptionally
The light regime experienced by phytoplankton also depends on the rate of mixing, which is much more rapid in
regulated by a mechanism
estuarine waters than coastal or open ocean waters. The effect of this, in combination with the more rapid attenthat is under the control of the
uation of light, means that estuarine phytoplankton can pass through a light gradient ranging from darkness to full
redox state of the plastosunlight in minutes. The same transient would take hours to days in the more stable and clearer ocean (Fig. 3).
quinone pool9. Under low-light
.
January 2000, Vol. 5, No. 1
13
trends in plant science
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in illumination as it is mixed back up are
insufficient to allow much deactivation18.
There appears to be little role for Rubisco
oxygenase activity in phytoplankton.
Although the abundance of free CO2 in seawater (~10–15 mM) is well below the
half-saturation concentration of Rubisco
(30–170 mM)15,16, carbon concentrating
mechanisms that involve either active
transport of HCO32 or coupled dehydration
of HCO32 by a cell-surface carbonic anhydrase and CO2 transport, have been documented for cyanobacteria, chlorophytes19,
diatoms20 and dinoflagellates21,22. In addition, microalgal Rubiscos have high CO2
specificities compared with those from terrestrial plants. This might be because of
differences in the structure of the loop-6
region15 or in the length of the large subunit
C-terminus16, both of which appear to play
a role in the conformation of the active site
during catalysis. The dinoflagellates are
distinct from all other eukaryotes in having
a prokaryotic-type form II Rubisco23 (i.e.
one lacking the small subunit characteristic
of the eukaryotic form I). Although the specificity of dinoflagellate form II Rubisco is
higher than bacterial form II Rubisco24, it is
unlikely that it could support measured rates
Fig. 2. (a) The first-order reaction time constants (t, in minutes) of photosynthetic responses
to increases and decreases in light intensity vary from 104 min for changes in the chlorophyll
of photosynthesis without the presence of a
quota to 1021 min for inter-conversion of the xanthophylls diadinoxanthin and diatoxanthin.
carbon-concentrating mechanism.
Note that time constants for increases in irradiance (denoted ‘up’) are shorter than for
A second phenomenon that might drive
decreases (denoted ‘down’), except in the case of the chlorophyll-specific light-saturated rate
the short-term photosynthetic response in
of photosynthesis, Pm/Chl, where the kinetics are driven by changes in the chlorophyll quota.
estuarine waters is the occurrence of state
The time constant defines the rate of change of species X over a time-step of duration Dt as:
transitions25, which are rapid adjustments
Xt 1 Dt 5 Xt exp(Dt/2tdown)
in the relative magnitudes of the photosysfor a decrease in irradiance and as:
tem I (PS I) and photosystem II (PS II)
Xt 1 Dt 5 Xt [1 2 exp(Dt/2tup)]
antennae. State 2 (preferential excitation of
PS I) is favored under conditions of high
for an increase.
absolute irradiance and under darkness,
The time taken for the light level to either double or halve for cells in simulated oceanic and
estuarine water (Fig. 3) is indicated by arrows. Sources for the time constants are given in
whereas State 1 (preferential excitation of
parentheses. (b) The essence of mixing-based productivity models is defining a step-change in
PS II) is favored under conditions in which
irradiance because of a cell’s motion through a light gradient (compare with Fig. 3) and implethe spectrum is dominated by red light.
menting the time-dependence of photosynthetic response via time constants (tup and tdown) that
Consequently cells in estuarine waters are
describe the change in response to increases and decreases in light intensity (a). These contrast
driven to State 2 at aphotic depths (depths
with steady-state models (black unbroken line), in which no time-dependence is allowed (i.e.
to which light does not penetrate because
the effect of light level fluctuations is ignored). In acclimation or induction models (left),
of complete attenuation by the overlying
instantaneous estimates of productivity are almost always lower than in the steady-state rate,
water), to State 1 at intermediate depths
because of the time-lag inherent in the response as the photosynthetic mechanism adjusts to a
where the spectrum is weighted towards
change in light level. In inhibition models (right), instantaneous estimates of productivity can
long wavelengths (Fig. 3), and back to
be higher or lower than in the steady-state condition, because the steady-state rate is an empirically-derived average over a period that might be long compared with the accumulation of phoState 2 at the surface4,25. It is not clear what
effect, if any, state transitions have on photosynthetic rates, but the interchange time
constants are close enough to the rate of
catalytic characteristics15,16. However, activity changes in those mixing that the transitions can be observed in cyanobacteria and
few microalgae that have been studied are consistent with models chlorophytes from turbid waters25. State transitions are unlikely to
of regulation by means of carbamylation–decarbamylation and, in limit photosynthetic rates in the ocean because the timescale of
addition, possibly, by a tight-binding inhibitor, such as carboxy- mixing is slower, and because red light is more rapidly attenuated
arabinitol-1-phosphate17. The kinetics of activation and deacti- than blue light (Fig. 3). State transitions have yet to be docuvation could affect photosynthetic rates in response to rapid mented from chromophytic microalgae.
increases in light intensity during mixing. Because activation is
much faster than deactivation, the effect is less pronounced during Photoprotection
rapid mixing because the interval between decreases in illumi- The most complex group of photosynthetic responses includes the
nation as a cell is mixed away from the well-lit surface and increases transients associated with photoprotection and photoinhibition.
14
January 2000, Vol. 5, No. 1
trends in plant science
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Photoprotective mechanisms can broadly be described as those
that either decrease the absorption of light energy (by reducing the
absorption cross section or effective photosynthetic cross-section
of the reaction centers), or provide alternative energy sinks when
photosynthetic capacity is exceeded. Change in the excitation
delivery includes rapid responses, such as induction of energy-dissipating pigments in xanthophyll cycles26,27, and slower responses,
such as photoacclimative changes in the size and pigment composition of the antennae (Fig. 2). Two different xanthophyll cycles
are found in chlorophytes and chromophytes: in chlorophytes,
violaxanthin is de-epoxidated to zeaxanthin in a two-step pathway,
with antheraxanthin as an intermediate; in chromophytes diadinoxanthin is de-epoxidated to diatoxanthin in a single step. Although
the chlorophytes have a pathway that is structurally similar to vascular plants’, the relationship between non-photochemical energy
quenching and the level of de-epoxidation is different28. Conversely,
although chromophytes have a different pathway, the relationship between non-photochemical quenching and the level of
de-epoxidation is comparable to that in vascular plants.
Other electron sinks
In addition to xanthophyll cycling, there are other mechanisms
that might act as sinks for electrons when PS II activity exceeds
photosynthetic capacity. For example, cyanobacteria lack a xanthophyll cycle but exhibit strong Mehler activity at light saturation29,
and diatoms appear to be unique in using non-assimilatory nitrate
reduction as a sink30. Both pathways bleed off excess energy from
the electron transport chain when NADPH turnover is operating at
the maximum rate, preventing over-excitation of the photosynthetic antennae.
Photoinhibition
When the photoprotective mechanisms already described are
exceeded, damaged PS II reaction centers, lacking a functional D1
protein, can accumulate. The reconstitution of functional PS II
reaction centers can be described by first-order reaction kinetics
when cells are moved to non-inhibitory irradiance31. Modeling the
accumulation of damaged D1 might be more difficult because of
the diversity of photoprotective responses, the protective capacity
of which depends on both the light history and nutrient status of
the cell26. However, photo-inactivation of D1 can be modeled by
target theory32, opening the possibility that photosynthesis could
then be described using the relationship between the proportion of
inactive PS II reaction centers and the quantum efficiency.
Kinetic models and the time-dependence of
photosynthetic physiology
Short-term variability in photosynthetic rates can be accounted for in
productivity models using time-dependent relationships. Generally,
two assumptions are made, namely that the ocean can be considered
as a one-dimensional system in the vertical and (in many models)
that the time-dependence of photosynthetic processes follow firstorder reaction kinetics. With an adequate understanding of the vertical variation in mixing rate, the trajectories of groups of cells can be
described by a random walk simulation (the vertical steps of which
are defined in time by the local turbulent diffusivity) using a
Lagrangian ensemble model. Given the rate of light attenuation,
changes in light intensity can be described as a function of depth and
time (Fig. 3). The sensitivity of photosynthesis to mixing can then be
described by specifying the time-dependence of the response to
changing light intensity with one or more time constants (Fig. 2).
Separate time constants for upward and downward movements are
usually employed to account for different physiological rate constants
associated with responses to increases and decreases in irradiance.
Fig. 3. Light absorption in oceanic waters (a) is almost wholly
dependent on phytoplankton (black line) and water itself (gray
line), in contrast with estuarine waters (b), where detritus (broken
black line) and chromophoric dissolved organic material (bold,
black line) also make a substantial contribution (note different
scales). As a consequence, both the magnitude and spectral
dependence of underwater light are different. (c) The attenuation
of incident sunlight (0 m) is more pronounced in red light
(depicted by light gray) than blue light (depicted by dark gray) in
oceanic water, in contrast with estuarine water (d), were blue light
is attenuated more rapidly than red light. Light intensity is
expressed as PAR (photosynthetically active radiation), which is
the integral of irradiance between 400 and 700 nm. The blue and
red absorbance peaks of plant pigments are shown. The spectral
composition of light is shown at different depths that correspond
to either a doubling or a halving in the intensity of PAR. Higher
turbulence and more rapid attenuation in the estuarine water
results in entrained cells experiencing more rapid transients in
light intensity (f) than in the oceanic water (e). Note the difference
in scales. Exposure was calculated from the spectrally dependent
attenuation coefficient for a cell that was released into the middle
of a mixed layer and whose trajectory was based on a random
walk model.
January 2000, Vol. 5, No. 1
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The approach has been used to model the sensitivity of photosynthesis to changes that are characteristic of photoacclimation33,
photoinhibition34 and photosynthetic induction18. The relative
importance of different photosynthetic mechanisms depends on
the timescale and the magnitude of the changes in the light field
(i.e. if the time constant for the metabolic response is longer than
the characteristic timescale of change, the mechanism has the
potential to limit the reaction rate13; Fig. 2). Constructing a general model of the effect of mixing on photoinhibition that is analogous to the acclimative models depends on a somewhat arbitrary
level of calibration because both the degree and rate of accumulation of photoinhibitory damage are less constrained than acclimative changes (Fig. 2). One approach, which is based on first
principles, involves defining an action spectrum of the doseresponse of photoinhibition and using a biological weighting
function to drive the onset of photoinhibition and the subsequent
recovery as cells are mixed through a water column35.
A description based on energy-balance models is an alternative
to the descriptions of photoacclimation based on explicit timeconstants of chlorophyll-specific photosynthetic responses. In
energy-balance models, a physiological sensor regulates the pigment quota as a means of balancing excitation-energy harvesting
with the energetic demands of growth. By specifying both as rates
and using units of inverse time (which necessitates converting the
currency of electrons to carbon equivalents), the imbalance can be
used to drive changes in energy harvesting, either by inducing
chlorophyll synthesis or D1 turnover10,11 until equilibrium is reestablished. Embedding such an energy-balance model into a
physical model of mixing produces results that are consistent with
field measurements over wide temporal and spatial scales (annual
cycles from 0 to 608 N)36. Because the regulated term is the ratio
of phytoplankton chlorophyll to carbon (an index of the pigment
quota), energy-balance models can be reconciled with large-scale
estimates of phytoplankton biomass (Fig. 1), and the response has
an explicit dependence on temperature and nutrient (nitrogen)
availability. These dependencies have not been quantified for
first-order kinetic models, in which both the time constants and
the end-points of acclimation might depend on temperature and
nutrient status.
The future
It is now possible to evaluate how the photosynthetic apparatus
is regulated under complex environmental forcing. The complexity of the environment–photosynthesis relationship is
tractable using the notion of energy-balance regulation: the
redox state of the light reactions is a universal signal in microalgae for regulating cellular light harvesting efficiency. The
success of recent pigment-photoacclimation models that incorporate an energy-balance regulatory ‘signal’ based on the redox
state, holds promise for more sophisticated models that incorporate short-term energy modulation mechanisms. These models
can be made species-specific by setting parameters according to
the specific energy modulation processes that are present. Future
work on environmental effects will distinguish short-term
kinetically constrained responses from longer-term energybalance-constrained responses. This will clarify the relative
importance of kinetic versus acclimative responses to particular
environments.
Acknowledgements
We thank two anonymous reviewers for their comments on the
manuscript. This work was supported by Grants OCE-9730098
and OCE-9633633 from the National Science Foundation (USA)
and is contribution No. 3239 from Horn Point Laboratory.
16
January 2000, Vol. 5, No. 1
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Hugh L. MacIntyre* and Todd M. Kana are at the University of
Maryland Center for Environmental Research, Horn Point
Laboratory, PO Box 775, Cambridge, MD 21613, USA;
Richard J. Geider is at the Dept of Biological Sciences,
University of Essex, Colchester, UK CO3 4SQ.
*Author for correspondence (tel 11 410 221 8430;
fax 11 410 221 8490; e-mail macintyr@hpl.umces.edu).
Floral induction and determination:
where is flowering controlled?
Frederick D. Hempel, David R. Welch and Lewis J. Feldman
Flowering is controlled by a variety of interrelated mechanisms. In many plants, the environment
controls the production of a floral stimulus, which moves from the leaves to the shoot apex.
Apices can become committed to the continuous production of flowers after the receipt of
sufficient amounts of floral stimulus. However, in some plants, the commitment to continued flower
production is evidently caused by a plant’s commitment to perpetually produce floral stimulus
in the leaves. Ultimately, the induction of flowering leads to the specification of flowers at the shoot
apex. In Arabidopsis, floral specification and inflorescence patterning are regulated largely by
the interactions between the genes TERMINAL FLOWER, LEAFY and APETALA1/CAULIFLOWER.
F
loral induction is the process by which stimuli originating
outside the shoot apex induce the formation of flower primordia (Fig. 1). The photoperiodic induction of flowering
was discovered 86 years ago by Julien Tornois in hops1. Shortly
afterwards, additional experiments suggested that the photoperiodic control of flowering was a general phenomenon, which controlled flowering in most plants2. Later, focused-light experiments
showed that leaves perceive photoperiodic signals3. These studies,
and numerous grafting experiments, indicate that the production
of the photoperiod-induced floral stimulus4 occurs in the leaves of
a wide variety of flowering plants5–7.
In contrast with floral induction, floral determination can be
defined as the assignment of flower(ing) fate, which is persistent
even when the flower-inducing conditions no longer exist8,9.
Assays for floral determination include:
• Changing environmental conditions (from inductive to noninductive).
• Microsurgical removal of shoot apices, and the placement of
those apices into neutral environments8,10.
However, both types of determination assay have limitations, and
it is important to note that different determination assays might
yield alternative conclusions for the same primordia (the caveats
associated with determination experiments are discussed in Ref.
11). A third type of assay has been used to test leaf commitment to
the continued production of floral stimulus: in this assay, photoinduced leaves are removed from the plant following an inductive
treatment12.
In this review we discuss firstly a variety of experiments that
indicate the site(s) that control flowering. Secondly, we review
recent studies that indicate how a few key molecular players regulate the specification of flower primordia in Arabidopsis.
Floral determination assays
Photoperiodic assays for floral determination
The simplest type of determination assay is one in which plants
are moved to non-inductive conditions after various lengths of
time under inductive conditions. Using this method, the duration
of photoinduction treatment required to produce flowers can be
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