Temperature-dependent stomatal movement in tulip petals controls water transpiration during flower...

RESEARCH ARTICLE

Temperature-dependent stomatal movement in tulippetals controls water transpiration during floweropening and closingA.K. Azad1,2, Y. Sawa1, T. Ishikawa1 & H. Shibata1

1 Department of Life Science and Biotechnology, Shimane University, Shimane, Japan

2 Department of Biotechnology, Shah Jalal University of Science and Technology, Sylhet, Bangladesh

Keywords

Petal opening and closing; stomatal aperture;

stomatal densities; temperature; water

transpiration.

Correspondence

A.K. Azad, Department of Life Science and

Biotechnology, Shimane University, Shimane

690-8504, Japan.

Email: [email protected]

Received: 25 February 2006; revised version

accepted: 17 October 2006.

doi:10.1111/j.1744-7348.2006.00111.x

Abstract

Temperature-dependent tulip petal opening and closing movement was previ-

ously suggested to be regulated by reversible phosphorylation of a plasma

membrane aquaporin (Azad et al., 2004a). Stomatal apertures of petals were

investigated during petal opening at 20�C and closing at 5�C. In completely

open petals, the proportion of open stomata in outer and inner surfaces of the

same petal was 27 � 6% and 65 � 3%, respectively. During the course of

petal closing, stomatal apertures in both surfaces reversed, and in completely

closed petals, the proportion of open stomata in outer and inner surfaces of

the same petal was 74 � 3% and 29 � 6%, respectively, indicating an inverse

relationship between stomatal aperture in outer and inner surfaces of the

petal during petal opening and closing. Both petal opening and stomatal clo-

sure in the outer surface of the petal was inhibited by a Ca2+ channel blocker

and a Ca2+ chelator, whereas the inner surface stomata remained unaffected.

On the other hand, sodium nitroprusside, a nitric oxide donor, had no effect

on stomatal aperture of the outer surface but influenced the inner surface sto-

matal aperture during petal opening and closing, suggesting different signal-

ling pathways for regulation of temperature-dependent stomatal changes in

the two surfaces of tulip petals. Stomata were found to be differentially dis-

tributed in the bottom, middle and upper parts of tulip petals. During petal

closing, water transpiration was observed by measuring the loss of 3H2O.

Transpiration of 3H2O by petals was fivefold greater in the first 10 min than

that found after 30 min, and the transpiration rate was shown to be associated

with stomatal distribution and aperture. Thus, the stomata of outer and inner

surfaces of the petal are involved in the accumulation and transpiration of

water during petal opening.

Introduction

Stomata are small pores distributed over either one or both

surfaces of leaves that control the CO2 absorption by

photosynthesis and water loss through transpiration

(Hetherington & Woodward, 2003; Gray & Hetherington,

2004). The exchange of CO2 and water is regulated

through controlling stomatal aperture, densities and size

of stomata in the shoot epidermis (Hetherington &

Woodward, 2003). The regulation of stomatal aperture

is based on endogenous plant hormones especially ab-

scisic acid (ABA) and environmental signals, such as

light, drought, CO2 and humidity (Neill et al., 2002;

Roelfsema & Hedrich, 2005). Light and drought play

antagonistic roles in stomatal aperture. Light stimulates

stomatal opening to promote CO2 uptake, but drought

causes stomatal closure to limit water loss through

transpiration (Roelfsema & Hedrich, 2005). Reduced

Annals of Applied Biology ISSN 0003-4746

Ann Appl Biol 150 (2007) 81–87 ª 2007 The Authors

Journal compilation ª 2007 Association of Applied Biologists

81

atmospheric humidity has the same effect as that of

drought, decreasing stomatal aperture to limit water loss

(Buckley, 2005). The impact of CO2 on stomatal develop-

ment, densities and aperture has been reported in many

studies (Leymarie et al., 1999; Roelfsema et al., 2002;

Hetherington & Woodward, 2003). Although most studies

regarding stomata have been with leaves, stomata have

also been reported in nonphotosynthetic organs, such as

stem, petioles and primary roots (Christodoulakis et al.,

2002), and in nectaries (Horner et al., 2003).

Rapid stomatal response to environmental perturbations

is a crucial feature to preserve plant water balance

(Buckley, 2005). The flux of water from roots to leaves

and flowers involves aquaporins, the water channel pro-

teins (Azad et al., 2004a; Chaumont et al., 2005). Plasma

membrane aquaporins (PM-AQP) are distributed in all

plant organs including the guard cells (Chaumont et al.,

2005; Fraysse et al., 2005), which form stomata. Tulip

petals open in the morning and close in the evening. We

could reproduce this opening and closing movement in

the dark by changing the temperature from 5�C to 20�Cfor opening and from 20�C to 5�C for closing. In our

previous studies, the temperature-dependent tulip petal

opening and closing which accompanied water move-

ment was suggested to be regulated by reversible phos-

phorylation of PM-AQP (Azad et al., 2004a,b). We

propose that transpiration of water is required for petal

opening and to maintain open petals and that the accu-

mulated water in the opened petal needs to be lost for

petal closing. Stomata are the only candidates for bring-

ing about this water loss. In this study, an intriguing

inverse relationship between stomatal apertures was

observed on opposite surfaces of tulip petals during petal

opening at 20�C and closing at 5�C, indicative of water

accumulation and transpiration during petal opening and

significant transpiration of water in the early stage of

petal closing. As far as we know, reports on stomatal

responses to temperature change are very limited. This

article further shows that this inverse correlation is also

true for petals at the same temperature and shows a rela-

tionship between water transpiration and stomatal density.

Materials and methods

Source of tulips and chemicals

Tulips (Tulipa gesnerina L. cv. Ile de France) used in this

study were grown at the green house of Shimane Uni-

versity, Japan. Three-day-old flowers were used in the

experiments. All chemicals were from Wako Pure Chem-

ical Industries, Osaka, Japan, unless noted otherwise.

The 3H2O was purchased from ICN Biomedicals Inc.

(Boston, MA, USA).

Analyses of petal opening and

closing movement

Flowers with 2-cm stems immersed at the cut end in

10 mL of 10 mM potassium phosphate, pH 7.0 (KP

buffer), were incubated either at 20�C for petal opening

or at 5�C for closing. Opposite petal distances (petal aper-

ture) were measured as an indication of the degree of

opening and closing.

Observation of stomata

The epidermises of the inner and outer surfaces of petals

were peeled out, and the stomata were fixed in a solution

containing equal volumes of phenol, glycerin, lactic acid

and distilled water. Stomatal aperture, shape and densities

were observed by bright field microscope (Olympus BX

50) assembled with digital camera (Olympus C-35AD-4).

Analyses of 3H2O transpiration during

petal closing

Flowers with 2-cm stem were incubated at 20�C with

10 mL of KP buffer, containing 2.5 � 107 dpm 3H2O, for

2 h to cause the complete opening of the flowers, and

these opened flowers were transferred to 5�C, with the

same medium, for closing. The content of 3H2O in petal

or in selected portion of the petal was determined as

described previously (Azad et al., 2004a) using a liquid

scintillation counter (Backman LS6000SE, Fullerton,

CA, USA), and the transpiration was followed by the lost3H2O. To determine the transpiration rate by bottom,

middle and upper parts (based on the distribution of sto-

matal densities) of the petal, flowers with petals of simi-

lar sizes were incubated as described above. Sections

from the three parts of the same petal were used to mea-

sure the content of 3H2O. For replicas, petals of the same

flower were used. The dpm count of 3H2O was con-

verted to microlitres as follows. The 3H2O used in the

experiment was measured, 24 073 dpm lL21. In case of

water, 6.023 � 1023 molecules mol21 is equivalent to

18 g ; 18 mL, therefore, 3.34 � 1022 molecules mL21 =

3.34 � 1019 molecules lL21 ; 2.4073 � 104 dpm.

Results and discussion

To understand more fully the transpiration of water

through petals, we used the epidermis of petals to inves-

tigate the stomatal size, shape and densities (number per

unit area) in different parts (bottom, middle and upper) of

petals and the stomatal apertures during petal opening

and closing. Although kidney-shaped stomata (Fig. 1)

were found to be of similar size throughout the petal,

Stomata control water transpiration in tulip petals A.K. Azad et al.

82 Ann Appl Biol 150 (2007) 81–87 ª 2007 The Authors


stomatal densities varied in different parts of the petals

of both surfaces (inner and outer) ranging 49 ± 3 mm22

in the bottom part, 11 ± 2 mm22 in middle part and less

than 5 mm22 in the upper part, and in each part of

either surface, stomatal densities were almost homoge-

nous. Stomatal densities are not uniform in every plant

or even in every organ of the same plant (Hetherington &

Woodward, 2003), and these results further showed

that densities might be dissimilar even in different parts

of the same organ. However, a more interesting charac-

teristic was observed in stomata on both surfaces of

petals. In completely closed flowers, the proportion of

open stomata in outer and inner surfaces of the petal

was 74 ± 3% and 29 ± 6%, respectively (Fig. 2). When

the flowers were shifted from 5�C to 20�C for opening,

the stomata of the outer and inner surfaces of petals star-

ted to close and open, respectively, coinciding with the

inauguration of petal opening. After 2 h, in completely

open flowers, the proportion of open stomata on the

outer and inner surfaces of the petal was 27 ± 6% and

65 ± 3%, respectively (Fig. 2). In contrast, when the

completely open flowers were transferred from 20�C to

5�C for petal closing, stomatal aperture at both surfaces

reversed, to become open and closed in the outer and

inner surfaces, respectively, according to the time course

showed in Fig. 2. Fig. 2 also indicates that 15 min after

transferring the flowers from 20�C to 5�C, 57 ± 5% of

inner surface stomata and 39 ± 3% of outer surface sto-

mata were still open, suggesting the occurrence of a high

transpiration rate during this initial stage of petal closing.

Ruthenium red (RR), a Ca2+ channel blocker (Tsuji

et al., 2000), and O,O#-bis(2-aminophenyl)ethylene-glycol-

N,N,N#,N#-tetraacetic acid (BAPTA), a Ca2+ chelator

(Gressel et al., 2002), severely inhibited petal opening as

well as water movement at 20�C but not petal closing

(Azad et al., 2004a). This study showed that RR and

BAPTA inhibited stomatal closure in the outer surface of

the petal together with the inhibition of petal opening

at 20�C (Fig. 3). This implies that a transient change in

cytosolic free calcium concentration ([Ca2+]cyt) may be

a critical factor for temperature-dependent stomatal clo-

sure in the outer surface as well as in petal opening.

However, when the completely open flowers were incu-

bated at 5�C in the presence of RR or BAPTA, the outer

surface stomata opened as usual and no significant effect

was observed in the closing of inner surface stomata

(data not shown). Although it has been shown that sto-

matal closure can be induced by an ABA-dependent rise

in [Ca2+]cyt (McAinsh et al., 1995; Schroeder et al., 2001),

ABA-induced stomatal closure is mediated through

a complex signalling network involving both Ca2+-

dependent and Ca2+-independent pathways (Assmann &

Shimazaki, 1999; Webb et al., 2001). We found that ABA

had no significant effect either on petal opening and

closing or on stomatal aperture (data not shown). This

suggests that a temperature-dependent elevation in

[Ca2+]cyt, which does not require the intermediacy of

ABA, is sufficient to cause stomatal closure in the outer

surface and petal opening at 20�C. Interestingly, when

ABA was supplemented with RR and BAPTA, only about

30% of petal opening was inhibited after 2 h of

Figure 1 Kidney-shaped opened (A) and closed (B) stomata in tulip

petals. Stomata were collected and observed as described in Materials

and Methods.

A.K. Azad et al. Stomata control water transpiration in tulip petals



83

incubation, and the extent of closure of outer surface

stomata was greater than that of the flowers treated with

RR and BAPTA (Fig. 3A and Fig. 3B). This result sug-

gested the compensation of [Ca2+]cyt by ABA treatment,

with the uptake and intracellular release of Ca2+, and

further indicated that although an ABA-induced [Ca2+]cytsignalling pathway might be present, the transient eleva-

tion in [Ca2+]cyt induced by temperature might be suffi-

cient for temperature-dependent petal opening as well

as changes in stomatal aperture. However, opening and

closing of inner surface stomata were not significantly

affected by the supplementation of ABA with RR and

BAPTA during petal opening and closing, respectively

(data not shown), indicating that the signalling may be

different for temperature-dependent changes in stomatal

aperture in outer and inner surfaces of tulip petals.

Recently, it was shown that nitric oxide (NO) is a signal-

ling molecule in ABA-induced stomatal closure and that

it is Ca2+ independent (Neill et al., 2002). We observed

no distinguishable effect in petal opening and closing

when the flowers were treated with sodium nitroprus-

side (SNP), a NO donor, but the opening and closing of

inner surface stomata were somewhat affected after

30 min (Fig. 4), and the outer surface stomata remained

0

1

2

3

4

5

6

7

150

Incubation time (min)

Petal ap

ertu

re (cm

)

0

10

20

30

40

50

60

70

80

90

Op

en

sto

mata (%

)

0 30 60 90 120

Figure 2 Stomatal aperture conditions in inner and outer surfaces of

tulip petal during petal opening and closing. Following preincubation at

5�C, completely closed flowers were incubated with potassium phos-

phate buffer at 20�C for 2 h to cause petal opening, and completely

open flowers at 20�C were transferred to 5�C for 2 h, with the same

buffer, to cause petal closing. During petal opening and closing, petal

apertures (an index of petal opening) were measured, and the petal epi-

dermises from inner and outer surfaces were collected as the time

scale shown to fix and observe the stomata (Materials and Methods).

Petal apertures (¤, during petal opening; e, during petal closing) were

the means ± standard error (SE) of five flowers with petals of similar

sizes used in the same experiment. At least 40 individual stomata either

in the inner or outer surface of the same petal were observed to calcu-

late the percentage of open and closed stomata. The sum of percent-

age of open and closed stomata in the identical surface was considered

as 100%. The percentage of open stomata in inner (n, during petal

opening; :, during petal closing) and outer (n, during petal opening;

h, during petal closing) surfaces are shown. Data are the means ± SE

of five independent experiments. Bars represent SE.

0

1

2

3

4

5

6

7

8

0 6030 90 150120


Petal ap

ertu

re (cm

)

A

120


0

10

20

30

40

50

60

70

80

90

Op

en

sto

mata (%

)

B

0 6030 90 150

Figure 3 Effects of RR and BAPTA on outer surface stomatal closure

during tulip petal opening. Following preincubation at 5�C, completely

closed flowers immersed at the cut end in KP buffer (control), KP buffer

containing 50 lM RR or 2 mM BAPTA, KP buffer containing 50 lM RR

plus 50 lM ABA or KP buffer with 2 mM BAPTA plus 50 lM ABA were

incubated at 20�C for 2 h to cause the opening of petals. In (A), petal

apertures (¤, KP; n, KP + RR; :, KP + BAPTA; h, KP + RR + ABA; n,

KP + BAPTA + ABA) were the means ± SE of five flowers with petals of

similar sizes used in the same experiment. In (B), at least 50 stomata

from outer surface of the same petal were observed to determine the

percentages (described in legend of Fig. 2) of open stomata (¤, KP;

n, KP + RR; :, KP + BAPTA; h, KP + RR + ABA; n, KP + BAPTA + ABA).

Data are the means ± SE of five independent experiments. ABA,

abscisic acid; BAPTA, O,O#-bis(2-aminophenyl)ethylene-glycol-N,N,N#,N#-

tetraacetic acid; KP, potassium phosphate; RR, ruthenium red; SE,

standard error.




unaffected (data not shown). This result further sug-

gested the involvement of different signalling pathways

in outer and inner surfaces of tulip petals in the regu-

lation of temperature-dependent changes in stomatal

aperture. Petal opening and closing was not significantly

affected by SNP, possibly as it had no effect on closure of

outer surface stomata. It was suggested above that the

accumulation of water by closure of outer surface sto-

mata causes petal opening. Indeed, almost 50% of the

accumulated 3H2O in the petals was lost through tran-

spiration during the first 30 min of incubation (Table 1)

for petal closing. However, during this 30 min of incuba-

tion, inner surface stomatal closure was not significantly

induced by SNP (Fig. 4). NO is generated by guard cells

in response to ABA as part of the signalling pathway

(Neill et al., 2002), but in this study, ABA showed no

effect on the stomata of the inner surface of tulip petals.

One reason for this might be that the incubation time

(required to induce petal opening or closing) was insuf-

ficient to reach the level of NO sufficient to exert an

effect.

To determine how the accumulatedwater in open petals

is lost during petal closure, we measured the transpiration

of water during the course of petal closing. To determine

the transpiration rate during closure, flowers were

first incubated with 3H2O at 20�C for 2 h (for complete

opening). When fully opened, the content of 3H2O was

4.218 lL per petal. The flowers were transferred to 5�C,with the same medium, for 2 h (for closing). During the

course of petal closing, 3H2O remaining in the petal was

measured and the rate of transpiration per petal deduced

from the loss of 3H2O (Table 1), assuming negligible bulk

water movement at 5�C (Azad et al., 2004a). Table 1

shows that during the initial 10 min, the rate of loss of3H2O was approximately fivefold greater than that found

after 30 min of incubation, and after 60 min, the loss of3H2O was 10-fold less. The high rate of transpiration of3H2O during the initial phase of closing may be ex-

plained by the proportion, 57 ± 5%, of inner surface sto-

mata that were still open for up to 15 min (Fig. 2) after

transferring the flowers from 20�C to 5�C. This suggests

that the inner surface stomata contribute to water tran-

spiration during petal opening and in keeping petals

open (Azad et al., 2004a). About 60% of 3H2O was lost

by 60 min of incubation at 5�C (Table 1), and further

incubation up to 2 h resulted in very little additional

water loss rising to just 67% of the total 3H2O (Azad et

al., 2004a). This may be due in part to the closure of

about 70% of the inner surface stomata after 60 min of

incubation at 5�C (Fig. 2), but it may also be because of

the exchange of 3H2O with intracellular water, which

may only be released slowly. In a subsequent experi-

ment, we divided the petals into three parts (bottom,

middle and upper) depending on the distribution of sto-

matal densities, and the transpiration was again deduced

from the 3H2O remaining in these sections (Table 2). In

agreement with the pivotal role played by stomatal

aperture in governing the extent of water loss by

0

10

20

30

40

50

60

70

80

Op

en

sto

mata (%

)

150


0 30 60 90 120

Figure 4 Effects of SNP on inner surface stomatal aperture during tulip

petal opening and closing. Completely closed or open flowers

immersed at the cut end either in KP buffer (control) or in KP buffer

plus 100 lM SNP were incubated at 20�C for 2 h to cause the opening

of closed flowers or at 5�C for 2 h to cause the closing of open flowers.

At least 50 stomata in inner surface of the same petal were observed to

calculate the percentage of open stomata either in control flower (¤,

during petal opening; :, during petal closing) or in flowers treated with

SNP (), during petal opening; n, during petal closing). Data are the

means ± standard error of five independent experiments. KP, potassium

phosphate; SNP, sodium nitroprusside.

Table 1 3H2O transpiration by tulip petal during closing at 5�Ca

Incubation

Period (min)b

3H2O Content

(lL petal21)

3H2O Lost

Since Previous

Measurement

(lL petal21)c

3H2O Transpiration

(lL min21 petal21)

0 4.218d n.d. n.d.

10 2.751 1.467 0.147

15 2.451 0.300 0.060

30 2.106 0.346 0.023

45 1.880 0.226 0.015

60 1.677 0.203 0.014

n.d., not determined.aData are the representative of triplicate experiments.bFlowers were preincubated with 3H2O at 20�C for 2 h and then trans-

ferred to 5�C (Materials and Methods).c3H2O content shown in this column was deduced by subtracting the3H2O at any given time from the 3H2O content of the preceding time

point.d3H2O content of completely open petal.




85

transpiration (Buckley, 2005; Roelfsema & Hedrich,

2005), the transpiration rate through the bottom section

was about five and 10-fold greater than that through the

middle and upper sections, respectively. This higher 3H2O

transpiration through the bottom section was in direct

proportion to its higher densities of stomata, suggesting

the notion that the higher stomatal densities were

involved in higher rate of water transpiration. The stoma-

tal apertures of the outer and inner surfaces of the three

petal sections were investigated, and the percentage of

open stomata on both surfaces of every section were

almost the same as that shown in Fig. 2 (data not shown).

This study shows that stomatal apertures respond to

changes in temperature. This in turn is likely to influence

cell volume or turgor pressure and sowould be expected to

affect a variety of physiological functions, including plant

water balance (Buckley, 2005). However, the molecular

mechanism for sensing temperature-dependent stomatal

aperture perturbations has yet to be identified. In this

study, it was further noticeable that in the open state,

the 3H2O content per square centimetre of bottom, mid-

dle and upper petal sections was 0.39, 0.09 and 0.06 lL,respectively, which may reflect the stomatal density

and/or the abundance of aquaporins in the guard cells of

these regions – the latter owing to transcellular and

intracellular water movement being dependent on the

abundance of water channel proteins (Ohsshima et al.,

2001). Plant aquaporins located at plasma membranes

and tonoplasts are believed to ensure high water per-

meability required for cell volume perturbation. The

PM-AQP isoform in the guard cells of spinach has been

reported as being necessary for high water permeability

(Fraysse et al., 2005), and a tonoplast aquaporin in the

guard cells of sunflower has been shown to be associated

with water movement where it has been suggested to be

involved in changing stomatal aperture (Sarda et al.,

1997). Recently we have cloned four full-length comple-

mentary DNAs of PM-AQP isoforms from tulip petals for

future functional analysis and investigating such regula-

tory mechanisms (unpublished observation).

In conclusion, the present study describes for the first

time (a) the differential stomatal characteristics of each

surface of a tulip petal; (b) that stomata have an important

physiological role in petal movement and (c) that water

loss by transpiration is directly proportional to stomatal

density. These observations may apply equally to all other

flowering plants. Furthermore, this study suggests the

interplay of different signalling pathways in the tempera-

ture-dependent regulation of stomatal aperturewithin the

same organ and highlights a fruitful area for more exten-

sive molecular characterisation.

Acknowledgement

We thank Prof. Dr Sake Arase, Department of Plant

Pathology, Shimane University, Japan, for his technical

help in microscopy during this study.

References

Assmann S.M., Shimazaki K.-I. (1999) The multisensory

guard cell. Stomatal responses to blue light and abscisic

acid. Plant Physiology, 119, 809–815.

Azad A.K., Sawa Y., Ishikawa T., Shibata H. (2004a) Phos-

phorylation of plasma membrane aquaporin regulates

temperature-dependent opening of tulip petals. Plant and

Cell Physiology, 45, 608–617.

Azad A.K., Sawa Y., Ishikawa T., Shibata H. (2004b) Charac-

terization of protein phosphatase 2A acting on phosphory-

lated plasma membrane aquaporin of tulip petals.

Bioscience Biotechnology and Biochemistry, 68, 1170–1174.

Buckley T.N. (2005) The control of stomata by water

balance. New Physiologist, 168, 275–292.

Table 2 Transpiration of 3H2O by different parts of petal during closing at 5�Ca

Incubation

Period (min)b

3H2O Content (lL) 3H2O Transpiration Rate (lL min21 cm22)c

Bottom Part Middle Part Upper Part Bottom Part Middle Part Upper Part

0 3.521d 0.537d 0.251d n.d. n.d. n.d.

15 1.850 0.316 0.161 0.0124 0.0025 0.0013

30 1.583 0.289 0.147 0.0020 0.0003 0.0002

45 1.474 0.271 0.138 0.0008 0.0002 0.0001

60 1.372 0.263 0.130 0.0008 0.0001 0.0001

n.d., not determined.aThe area of each section taken from bottom, middle and upper parts of the same petal was maintained 9, 6 and 4.5 cm2, respectively.

The numerical value showing 3H2O content is the mean of three replicas. Data are the representative of three independent experiments with

comparable results.bFlowers were preincubated with 3H2O at 20�C for 2 h and then transferred to 5�C (Materials and Methods).cTo determine the transpiration rate, the 3H2O content at any given time was subtracted from that of the preceding point.d3H2O content at completely open state of petal.




Chaumont F., Moshelion M., Daniels M.J. (2005) Regulation

of plant aquaporin activity. Biology of the Cell, 97, 749–764.

Christodoulakis N.S., Menti J., Galatis B. (2002) Structure

and development of stomata on the primary root of

Ceratonia siliqua L. Annals of Botany, 89, 23–29.

Fraysse L.C., Wells B., McCann M.C., Kjellbom P. (2005)

Specific plasma membrane aquaporins of the PIP1 sub-

family are expressed in sieve elements and guard cells.

Biology of the Cell, 97, 519–534.

Gray J.E., Hetherington A.M. (2004) Plant development:

YODA the stomatal switch. Current Biology, 14,

R488–R490.

Gressel J., Michaeli D., Kampel V., Amsellem Z.,

Warshawsky A. (2002) Ultralow calcium requirements of

fungi facilitate use of calcium regulating agents to suppress

host calcium dependent defenses, synergizing infection by

a mycoherbicide. Journal of Agricultural and Food Chemistry,

50, 6353–6360.

Hetherington A.M., Woodward F.I. (2003) The role of sto-

mata in sensing and driving environmental change.

Nature, 424, 901–908.

Horner H.T., Healy R.A., Cervantes-Martinez T., Palmer R.G.

(2003) Floral nectary fine structure and development in

Glycine max L. (Fabaceae). International Journal of Plant

Science, 164, 675–690.

Leymarie J., Lasceve G., Vasasseur A. (1999) Elevated CO2

enhances stomatal responses to osmotic stress and abscisic

acid in Arabidopsis thaliana. Plant Cell and Environment, 22,

301–308.

McAinsh M.R., Webb A.A.R., Taylor J.E., Hetherington A.M.

(1995) Stimulus-induced oscillations in guard cell cyto-

plasmic free calcium. Plant Cell, 7, 1207–1219.

Neill S.J., Desikan R., Clarke A., Hancock J.T. (2002) Nitric

oxide is a novel component of abscisic acid signaling in

stomatal guard cells. Plant Physiology, 128, 13–16.

Ohshima Y., Iwasaki I., Suga S., Murakami M., Inoue K.,

Maeshima M. (2001) Low aquaporin content and low

osmotic water permeability of the plasma and vascular

membranes of a CAM plant Graptopetalum paraguayense:

comparison with radish. Plant and Cell Physiology, 42,

1119–1129.

Roelfsema R.R.G., Hedrich R. (2005) In the light of stomatal

opening: new insights into the Watergate. New Physiologist,

167, 665–691.

Roelfsema M.R.G., Hanstein S., Felle H.H., Hedrich R. (2002)

CO2 provides an intermediate link in the red light

response of guard cells. The Plant Journal, 32, 65–75.

Sarda X., Tousch D., Ferrare K., Legrand E., Dupuis J.M.,

Casse-Delbart F., Lamaze T. (1997) Two TIP-like gene

encoding aquaporins are expressed in sunflower guard

cells. Plant Journal, 12, 1103–1111.

Schroeder J.I., Allen G.J., Hugouvieux V., Kwak J.M.,

Waner D. (2001) Guard cell signal transduction. Annual

Review of Plant Physiology and Plant Molecular Biology, 52,

627–658.

Tsuji H., Nakazono M., Saisho D., Tsutsumi N., Hirai A.

(2000) Transcript levels of the nuclear-encoded respiratory

genes in rice decrease by oxygen deprivation: evidence for

involvement of calcium in expression of the alternative

oxidase 1a gene. FEBS Letters, 471, 201–204.

Webb A.A.R., Larman M.G., Montgomery L.T., Taylor J.E.,

Hetherington A.M. (2001) The role of calcium in ABA-

induced gene expression and stomatal movements.

The Plant Journal, 26, 351–361.




87

Temperature-dependent stomatal movement in tulip petals controls water transpiration during flower...

Documents

Transcript of Temperature-dependent stomatal movement in tulip petals controls water transpiration during flower...