Plant Physiology

1. Effects of Climate Change on
Mechanisms That Initiate Flowering
Donald Geiger
University of Dayton
Marianist Environmental Education Center

2. 2
 Exposure to warm temperatures over time is the main driver
for springtime plant development, particularly for perennial
plants in temperate zones.
 Plants require a certain amount of exposure to warm
temperatures before leaf out or flowering can occur.
 The required heat sum, a quantified requirement that controls
development, is a genetically controlled adaptive trait.
 One of the most obvious ways ecosystems are affected by
global climate change is through alteration of organisms’
developmental timing, their phenology.
 Onset of flowering is an important element of phenology.
Basis For Study of Flowering Phenology

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Climate Change and Flowering Phenology
 The effect of climate change on the phenology of flower
initiation was reported in the following publication:
McEwan RW, RJ Brecha, DR Geiger, GP John 2011 Flowering
phenology change and climate warming in southwestern Ohio.
Plant Ecology 212,(1) 55-61.
 The above study, based on observations of first flowering
dates for an array of species from 1976 to 2003, provided
evidence that climate change is affecting plant development.

4. Change in first flowering date over a 28–year (1976 to 2003) observation period in
southwestern Ohio, USA. Change in flowering date represents the slope of the linear
regression between first flowering date and year. Darkened symbols represent slopes
that were different from zero (P<0.05). Horizontal dashed line represents no change.
4
Spring Eph
Spring Eph
Woody Fruit
Quantitative L-D
McEwan et al. Plant Ecology (2011) 2112:55-61
In spring
In summer
Effect of Climate Warming on Flowering Phenology
Statisticaly
not
earlier.
Development
Development
Qualitative L-D
Development
Woody Ornamental
Development
Quantitative L-D
Development
Development
Quantitative L-D

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Basis For Flower Phenology Studies
 This study revealed a trend of progressively earlier flowering
time for a number of species.
 The two earliest flowering species showed the largest advance
in flowering time; advance decreased with later flowering date.
 Two species that bloomed in mid summer also had advanced
flowering dates.
 Flowering is known to be initiated by a number of different
physiological mechanisms.
 Hypothesis: The two clusters of advanced bloom dates may
result from climate change acting on two different mechanisms
that regulate initiation of flowering.

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Physiology of Floral Induction:

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Background: A Survey of Physiological
Mechanisms of Flowering Phenology
 In their discussion the authors of the flowering phenology
paper “suggest that future work is needed that bridges
the gap between pattern (plant phenology response)
and process (plant development physiology) in relation
to particular climatic cues”.
 The study that follows is a survey of process…
mechanisms that initiate flowering and investigates
possible ways in which climate change may advance
initiation mediated by these mechanisms… pattern.

8. Floral Induction
Shoot Apex Phase Changes
 Shoot apical meristems have
three developmental phases:
1. Juvenile phase
2. Adult vegetative phase
3. Adult reproductive phase
4. Flower formation
1
2
3
4
2
8

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Shoot Apex Stages for Flowering
Adult
Reproductive
state
emphasis on developmental states
 Floral evocation in the adult reproductive phase
involves three states on the way to flowering:
 Competent- Shoot apex becomes competent to respond appropriately to
a given developmental signal. E.g.- able to respond to photoperiod
 Determined- able to follow some developmental program even if shoot is
removed from its normal position and nurtured by grafting or rooting.
E.g.- able to respond to plant growth regulator.
 Expressed- apical meristem undergoes physiological steps that lead to
morphogenesis to become a flower. (Process on slide 10)

10. bract
shoot
apex
epal
shoot pex
etal
a.
b.
c.
d.
stamen
primordia
Floral Induction and Development of the Flower
Signal to apex in
determined state
Vegetative shoot apex
10

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Survey of Factors Involved In
Altering Flowering Time

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12
 Mikhail Chailakhyan in 1937 demonstrated that
floral induction can be transmitted through a graft
indicating that a signal substance is being sent.
 The hypothetical substance was named florigen.
 In 2005 an RNA was mistakenly identified as florigen.
In 2007 the paper was retracted; In 2008 florigen was
found to be a protein a translocated floral initiation signal,
florigen.
 Florigen proteins FT , Hd3a and PIF4 have been identified
as biochemical signals known to be translocated to the
apical meristem and to initiate flower formation.
Biochemical Signaling Is
Able To Initiate Flowering

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Biochemical Signaling
Involved in Flowering
Multiple development pathways for floral evocation in Arabidopsis. Part 2
Flowering is
expressed by
action of the florigen
signal in response to
photoperiod or warming
stimulus.
Mitigating factors:

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 Temperature- warming after chilling
 Temperature- vernalization = period of chilling
 Photoperiod- day length; dark period length
 Biennial life cycle- vernalization followed by lengthening days
 Carbohydrate pathway- sucrose
 Plant growth regulators- gibberellin, ethylene pathway-
 Autonomous initiation- age, size, leaf number.
 Significance:- Existence of multiple pathways provides
flexibility to produce seeds under a variety of conditions.
Which of these mechanisms are affected by climate change?
Some Factors That Initiate Flowering:
Candidates for Climate Responses

15. Photoperiodism:
Monitoring Day
Length
15
Photoperiodic regulation of flowering showing effects on short-day plants and
long-day plants. Bar graphs show the effects of the duration of dark periods on
flowering; data show the critical variable is length of the dark period.
Day long enough Night long enough
Short-Day plants Long-Day plants
“day”
“night”
too
long
too short

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Biochemical Signaling
Involved in Flowering
[pp 660 – 667]
FT protein, the “florigen” is transported to the
shoot apex to evoke flowering.
Determined by
photoperiod signal
16
Determined by
warming signal
Florigen gene
expression regulated by
warm temperature .
PIF4 protein, a florigen
Long Day Short Day

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Case Studies of Flower Types:
1. Warming Activates Florigen Gene

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Warmth Activates Flower Initiation
A period of warming over a period of time drives spring flower
development, particularly for perennial plants in temperate zones.
Plants require a critical amount of exposure to warm temperatures
before leaf out or flowering can occur; required heat sum (RHS)
 RHS for spring development is a genetically controlled, adaptive trait.
 Enables plants to survive unpredictable early onset of warmth at the
start of the growing season that does not persist.
 Warmth activates PIF4 gene which acts as a florigen; exerts
control over the flowering pathway (slide 16).
 This mechanism is likely to be encountered in a number of
species of plants but has not been studied extensively since
its recent discovery (Kumar et al. 2012).

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Mechanisms That Can
Modulate Flowering Time
The thermal control time can be modulated by conditions that
affect the rate of accumulation of the required heat sum. RHS
 Different environments may cause plants to require more or less
time to accumulate the effective heat sum under the same input rate.
 Conditions known to modulate RHS mechanism include:
snow pack depth photoperiod winter cold treatment
 For example, photoperiod can delay bud break, protecting against
responding to the threat of unusually early but intermittent warm
temperature. This effect can complicate RHS/flower induction studies.
.

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Case Studies of Flower Types:
2. Spring Ephemeral Pattern-
Altered Rate of Flower Development

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Background: Spring Ephemerals
 Spring ephemerals are species that have an active spring
growth period limited to 40 - 60 days… adapted to take
advantage of a two-month high-light before canopy closure.
 Examples: fawn lily, Dutchman’s breeches, crocus, bleeding heart, snow drops,
tulip, hyacinth, Cardamine spp (red = reported in McEwan et al.)
 Annual life cycle, Erythronium americanum- yellow fawn lily
17 April 20 April
19 April 21 April 22 April
Spring Ephemeral Flowering Cycle

22. 40 to 60 days above ground
Spring Ephemeral Developmental Life Cycle
Diagramic life cycle of Erythronium americanum .
The perennial organ is shown in radial section to show bud development
summer autumn winter spring
1 2 3 4 5 6 7
Bud
Soil temperature drives life cycle development that determines flowering time.
22

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Spring Ephemeral Life Cycle
Species that have a 40 to 60 day growth period in spring.
 Annual life cycle, Erythronium americanum- yelllow fawn lily
Dormancy is broken in autumn; bud and root growth continues through the
winter at a very slow rate due to the low soil temperatures. (stages 2, 3).
 As the soil warms shoot expansion is rapid (stages 3, 4), the long
underground growth period ends and the above ground phase begins. This
process is hastened by the warming due to climate change.
 Sexual reproduction takes place over a 5- to 6-day period (stages 4,5,6)
 Senescence of the above ground plant (stage 6) followed by senescence
of the root (stage 7) and a stage of apparent dormancy of the perennial organ
stage 1)… the end of the 40 – 60 day period. Review previous slide.
 Flowering time was advanced in crocus (Crocus flavus) and bleeding heart
(Dicentra specta sp.)the study of phenology affected by climate warming
(McEwan et al. 2010).
next
year

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Case Studies of Flower Types:
3. Flower Bud Dormancy Broken by
Spring Chilling; Woody Perennials
and Geophytes

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Breaking of Bud Dormancy: Chilling
 For a wide range of spring flowering perennials a temperature
signal typically breaks dormancy of the renewal (winter) buds.
 Renewal or winter buds form in early summer after leaf
development ends and initiate next spring’s flowering.
 In woody perennials (apple) formation next year’s leaf and flower
primordia occurs in this year’s renewal buds in fall and early winter. !!!
 Flowering is initiated by chilling during spring warming period.
 Ex. Woody ornamental:- rhododendron; tree fruit species:- apple, pear
 Flowering time was advanced in apple (Malus domestica) in the study
of phenology affected by climate warming (McEwan et al. 2010)
 In the geophytes renewal buds form on the roots; flowering is
initiated by chilling during the spring warming period.
 Ex. Geophytes:- tulip, peonie

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In woody perennials breaking of bud dormancy in spring is a
factor determining the timing of flowering... Example apple, pear
 Bud dormancy in fall is initiated by low temperatures and short
photoperiod. Fruit trees
 In spring bud dormancy is broken by environmental signals,
especially chilling during the spring warming period.
 Linear accumulation of chilling hours occurs below 7o C. 45o F.
 Short photoperiod promotes blooming.
 Phenology of spring woody perennial flower activation is complex and
still not well understood.
 Remember: flowers formed in late fall, early winter in woody
perennials. It is bud break that determined flower activation.
Breaking of Bud Dormancy: Chilling

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Case Studies of Flower Types:
4. Flowering in Qualitative,
Obligate Long-Day Plants

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Qualitative Obligate Long-Day Plants
28
Annual Phlox (Phlox drummondii) is a qualitative long-day plant.
 qualitative L-D plant:- flowers ONLY on long days… obligate; day
period must be at least a certain critical length to initiate flowering
 quantitative L-D plant:- flowering ACCELERATED by long d. ;
facultative:- long days are not required for flowering.
 Under long-day conditions leaf processes mediated by phytochrome
produce florigen that initiates flower formation by the apical meristem.
(Revisit slides 16, 15, and 10)
 At 11 hrD- 98 days to flowering; 13 hrD 87 d, 15 hrD 75 d, 17 hrD 74 d
 In Phlox drummondi flower development did not increase beyond 15hr day.
 Flowering time was advanced in annual phlox (Phlox drummondi) in the
study of phenology affected by climate warming (McEwan et al. 2010)

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Case Studies of Flower Types:
5. Flowering in Quantitative
Facultative Long-Day Plants

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Shortest time to flowering in Ranunculus asiaticus was achieved
under 16 hr photoperiod at 16oC .
 A quantitative (LD accelerates flowering), facultative (LD not
required) long day plant
 Both increased temperature + longer daylength reduce time to
flowering.
 The decreased time to flowering by lengthening the photoperiod was
due to warming advancing development triggered by photoperiod
induction of flowering. Ranunculus is a quantitative long day plant. A
day of a certain length is not required for flowering to occur.
Effect of Photoperiod and Temperature
on Flowering in Quantitative L-D Plants

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Control of time to flowering in Viola:
 Progress to flowering increases with temperature up to 28oC.
 This pattern promotes earlier flowering as a result of higher springtime
temperatures.
 Progress to flowering also increases with daylength.
 Not a photoperiod induction of flowering but the requirement pattern for
growth of a quantitative long day plant.
 Response to longer photoperiod is adaptive, lessening the lag
imposed by cooler early season temperatures.
.
Effect of Photoperiod and Temperature
on Flowering in Quantitative L-D Plants

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 A quantitative long-day plant but long photoperiod is not used as a cue.
Lengthening days promoter stem elongation.
 Flowers are formed underground during the previous winter or earlier when
the plant forms its ramets.
 In mountainous habitats the first date of bare ground in spring is a good
predictor of first flowering date, reminiscent of the winter/spring maturation of
the developing flower stalks..
 Working hypothesis: increasing soil temperature promotes the formation and
maturing of flowers initiated with the formation of ramets in the previous
fall/winter.
Effect of a Variety of Factors on Timing of
Flowering in in Quantitative L-D Plants

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Case Studies of Flower Types:
6. Flowering in Biennials

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 Biennials: First year rosette of sugar beet is unable to form
reproductive shoots during the first year of growth.
 Duplicate genes BvFT1 and BvFT2, homologs of the FT gene mediate
regulation of flowering time: BvFT2 promotes while BvFT1 represses.
 Winter vernalization lowers expression of BvFT1, which renders
shoots competent to reproduce.
 Exposure to lengthening days (quantitative long day) upregulates
BvFT2 and maintains BvFT1 in downregulated state.
 Subsequent exposure to increasing day length (qualitative
long day) causes the shoot to become determined.
 The dependence on LD puts flower induction outside the
springtime window of earlier increased temperatures.
Biennial Sugar Beet Flowering

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Case Studies of Flower Types:
7. Flower Initiation Part of a
Genetically Determined
Development Program

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 Some species of plants initiate
flowering at a specific node (leaf
location on the stem).
 For a certain variety of cotton
it occurs just after nodes
number 5 or 6.
 The program development is
driven by heat measured in
heat units. (next slide)
 Determination by stage of plant
development seems to be a
common mechanism.
Flowering Initiated At a
Specific Development Stage
Node 4
Node 3
Node 2
Node 1
Node 5
Node 6
1st Flower
Main Stem
Vegetative Branch

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Flowering Initiated At a Specific
Development Stage
Growth Stage Days Heat Units – DD60s
Planting to Emergence 4 to 9 50 to 60
Emergence to First Square 27 to 38 425 to 475
Square to Flower 20 to 25 300 to 350
Planting to First Flower 60 to 70 775 to 850
Flower to Open Boll 45 to 65 850 to 950
Planting to Harvest Ready 130 to 160 2200 to 2600
Table 1. The average number of days and heat units required for various growth
stages of cotton in the Mid-South.
Modified from Oosterhuis, D.M. 1990. Growth and development of the cotton plant. In: W.N. Miley and D.M.
Oosterhuis (eds) Nitrogen Nutrition in Cotton: Practical Issues. Proc. Southern Branch Workshop for Practicing
Agronomists. Publ. Amer. Soc. Agron., Madison, WI
Daytime high °F + Nighttime low °F -60 = DD60
2

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 Species that initiate flowering at a specific stage of
development that is promoted by spring warming would advance
flowering as a consequence of climate warming.
 Species that flower in early spring would be most reliably
advanced due to climate warming. Those blooming later likely
would show more variability.
 For tomato plants, the first flower is initiated at node 6 to 8 depending
on the earliness of the variety. In a commercial variety of tobacco the
first flower was reported to occur at or about node 41.
 In the phenology study Ageratum, Centauria, Dicentra, Hemerocallis,
and Hosta flowering appears to be regulated by developmental stage.
Flowering Initiated At a Specific
Development Stage

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Summary: Possible
Mechanisms for
Responses of Flowering
To Climate Change

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Flowering Phenology and
Climate Warming
 McEwan R, R Brecha, D Geiger, G John 2011 Flowering Phenology Change
and Climate Warming in Southwestern Ohio. Plant Ecol 212: 55-61.
Global climate change affects timing of plant development.
 Thirty years of annual botanical surveys were used to
examine impacts of climate change on plant development.
 Authors of the study found a significant relationship between
warming winter and spring temperatures and first flowering time
for 60% of the species studied.

41. Change in first flowering date over a 28–year (1976 to 2003) observation period in
southwestern Ohio, USA. Change in flowering date represents the slope of the linear
regression between first flowering date and year. Darkened symbols represent slopes
that were different from zero (P<0.05). Horizontal dashed line represents no change.
41
Spring Eph
Spring Eph
Woody Fruit
Quantitative L-D
McEwan et al. Plant Ecology (2011) 2112:55-61
In spring
In summer
Effect of Climate Warming on Flowering Phenology
Statisticaly
not
earlier.
Development
Development
Qualitative L-D
Development
Woody Ornamental
Development
Quantitative L-D
Development
Development
Quantitative L-D

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1. Warming activates florigen gene.
 Arabidopsis thaliana; newly discovered; not researched
2. Spring ephemeral pattern of flower development.
 Erythronium americanum, Cardamine sp., Galanthus sp., Allium sp.,
Anemone sp., Crocus sp.
3. Flower bud summer dormancy broken in spring by chilling.
 Woody trees and shrubs: Malus sp. Rhododendron sp.
 Geophytes: Paeonia, Tulipa
4. Long days required in qualitative, obligate long-day plants
 Phlox sp.
5. Long days accelerate flowering; quantitative L-D plants
 Ranunculus asiaticus, Viola sp, Delphinium sp.
6. Biennial species, chilling period and lengthening days
 Beta vulgaris
7. Development + warming hastens flowering.
 Dicentra, Hemerocalis, Hosta
Seven Flower Induction Mechanisms

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Advanced
Mar 2: Galanthus sp.- Spring ephemeral
Mar 6: Crocus flavus- Spring ephemeral
Apr 18: Viola pubescens- Quantitative L-D plant; LD? + warming
Apr 19: Malus sp.- Woody fruit, bud dormancy broken by chilling
Apr 25: Delphinium consolida- Quant. L-D plant; LD? + warming
Apr 27: Dicentra spectabilis- Quant L-D plant; LD? + warming
May 19: Hemerocalus lilioasphodelus- Development; Dev + warm
Jul 14: Phlox sp- Qualitative, long-day plant; LD + warming
Aug 11: Hosta plantaginea- Development; Dev + warm

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Did Not Advance
Mar 27: Forsythia sp- Flower bud dormancy broken by chilling.
Apr 23: Ajuga reptans- Development ??
Apr 27: Geranium maculatum- facult L-D plant; LD + warming
May 5: Ranunculus sp- Development
May 13: Centaurea cyanus- Development
Aug 8: Ageratum sp- Development

45. 45
 Flowering physiology
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 Zeevaart, JAD. 2008 Leaf-produced floral signals. Current Opinion in Plant Biology 11:541–
547.
 McDaniel CN, SR Singer and SME Smith. 1992 Developmental states associated with the
floral transition. Developmental Biology 153:59-69.
 Flowering phenology and climate warming
 McEwan RW, RJ Brecha, DR Geiger, GP John 2011 Flowering phenology change and
climate warming in southwestern Ohio. Plant Ecology 212,(1) 55-61.
 Conover D, S Pelikan 2010 Earlier flowering in a restored wetland-prairie correlate with
warmer temperatures (Ohio). Ecological Restoration. 28(4) : 428-430.
 Bertin RI 2008 Plant phenology and distribution in relation to recent climate change. J.
Torrey Bot. Soc. 135, 126–146.
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change in Wisconsin. Proceedings of the National Academy of Science USA 96:9701-9704
 Floral induction mechanism triggered by warming
 Kumar SV, Lucyshyn D, Jaeger KE, Alos E., Alvev E, Harberd NP, Wigge PA. 2012
Transcription factor PIF4 controls the thermosensory activation of flowering Nature March
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 Release of bud dormancy in woody perennials
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perennials: a science comes of age. Hort Science 38:911-921.
 Photoperiod and flowering phenology
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temperature. Hort Science 31:680-68
 Adams SR, Pearson S and Hadley P 1997 The effects of temperature, photoperiod and light
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 Baloch J, M Munir, M Abid and M Iqbal. 2011 Effects of different photoperiods on flowering
time of qualitative long-day ornamental annuals. Pakistan J Bot.43(3): 1485-1490.
 Modulation of flower induction mechanisms
 Inouye et al. 2002 Oecologica 130:543-550 investigate the roles of snowpack, frost, La
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 Genetic and physiological bases for phenological responses to climates
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