Comparison of Physiological Properties Between Dwarf and Vine-type Cucumbers (Cucumis sativus Linn.)

June 2014

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Vol. 21 No. 2 19-27

Journal of Northeast Agricultural University (English Edition)

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Comparison of Physiological Properties Between Dwarf and Vinetype Cucumbers (Cucumis sativus Linn.) Xin Ming, Qin Zhi-wei*, Zhou Xui-yan, and Wu Tao College of Horticulture, Northeast Agricultural University, Harbin 150030, China

Abstract: Dwarfism is one of the most important traits in crop breeding. In this study, a dwarf cucumber D0462 and a vine NA129 were taken as experimental materials. The metabolism of hydrogen peroxide (H2O2) and superoxide anion radical (O2-•), activities of antioxidant enzymes, and the levels of endogenous hormones of the two cultivars were compared. In the whole growth period, D0462 maintained higher H2O2 and O2-• levels than NA129. The activities of SOD (superoxide dismutase), CAT (catalase), APX (ascorbate peroxidase) and IAAO (indoleacetic acid oxidase) in D0462 were found higher than those in NA129. The contents of gibberellic acid (GA3), indole-3-acetic acid (IAA), zeatin riboside (ZR) and jasmonic acid (JA) in internode were determined by enzyme-linked immunosorbent assay (ELISA). The internode of D0462 remained lower levels of GA3, IAA, and ZR. In contrast, JA level in internode of D0462 was higher than that of NA129. Compared with NA129, the cell mumbers in internode of D0462 did not change, but cell size evidently decreased. The chloroplasts in mature mesophyll D0462 exhibited swollen filled with starch grains instead of regular oval ones, and thylakoids of chloroplast swelled and became ambiguous. Key words: dwarf, cucumber, antioxidant enzyme, endogenous hormone CLC number: S642.2

Document code: A

Article ID: 1006-8104(2014)-02-0019-09

yield, enhance fertility, improve early maturity, and

Introduction

induce high tillering capacity (Ren et al., 2010). 　Cucumber (Cucumis sativus L. 2n=2x=14) is an

Lodging has been a problem impacting most crop

important vegetable. The compact (dwarf) charac-

and vegetable productivity (Sameri et al., 2009). The

terization is an important trait in cucumber breeding.

fungal infection and spindling extensively occur, and

Selecting directly for yield is proposed common

the inefficiency of mechanical harvesting are serious

and the most effective approach to screen excellent

problems due to plant lodging (Tar'an et al., 2003).

varieties of cucumbers (Cramer and Wehner, 2000).

However, short plant height can reduce the lodging

A large and well known dwarf genotypes or mu-

risk as well as improve yield and commodity (Hellewell

tants in agriculture attributes to hormone-deficience

et al., 2000). Dwarf is an important agronomic trait in

(Hedden et al., 2000). Many plant endogenous hor-

crop breeding. And dwarf mutants have been utilized

mones have been found to be the key elements in-

extensively in plant breeding. Dwarf genotypes have

volved in dwarfism, such as IAA, GA3, JA and ZR.

been reported to improve lodging resistance, increase

Plant development is a complicated process, which

Received 29 October 2013 Supported by the China Postdoctoral Science Foundation (2012M520701); the Key Laboratory Biology and Genetic Improvement of Horticultural Crops (Northeast Region), Ministry of Agriculture (CVB2012-001) Xin Ming (1981-), male, Ph. D, lecturer, engaged in the research of vegetable breeding. E-mail: [email protected] * Corresponding author. Qin Zhi-wei, professor, supervisor of Ph. D student, engaged in the research of cucumber breeding. E-mail: qzw303@126. com http: //publish.neau.edu.cn

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Journal of Northeast Agricultural University (English Edition)

Vol. 21 No. 2 2014

is regulated by interaction of physicochemical pro-

with 50 mmol • L-1 phosphate buffer (pH 7.5) contain-

perties, including antioxidants and hormone. The

ing 2% polyvinylpyrrolidone (PVP). SOD activity was

plant hormones have been reported to involve in

measured according to the method of Beyer and Fri-

regulating antioxidant activitiy (Buran et al., 2012). As

dovich (1987). One unit of SOD activity was defined

previously reported, the hormones such as IAA, GA,

as the amount of the extract that caused 50% nitroblue

ABA (abscisic acid), JA and salicylic acid (SA) in

tetrazolium (NBT) reduction under the experimental

plants affected the levels of antioxidase, and changed

conditions. CAT activity was assayed by monitoring

the antioxidant capacities of plants (Zhang et al.,

the consumption of H 2 O 2 as described by Aebi

2007; Sun et al., 2012; Agarwal et al., 2005). Under

(1984). One unit of CAT was expressed as l mol of

lead stress, application of exogenous hormones ABA

H2O2 oxidized mg-1 protein min-1. APX activity was

could significantly increase SOD, CAT, POD, and

determined by monitoring the decrease in absorbance

APX activities in Atractylodes macrocephala (Wang

at 290 nm, as the method given by Nakano and

et al. 2013). On the contrary, antioxidant levels acting

Asada (1981). APX activity was expressed as l mol

as free radical scavengers could affect the metabolism

ascorbate oxidized mg-1 protein min-1. IAAO activity

of hormone (Li et al., 2007). However, there are

was measured as the method of Zhang et al. (2009).

only few studies focusing on the differences between

IAAO activity was presented in μmol IAA destruct-

endogenous hormones and antiocidant of the dwarf

ed mg-1 protein min-1. The level of H2O2 and O2-• were

and vine cucumber.

determined according to the method described by Yiu et al (2009).

Materials and Methods

Determination of endogenous hormone

Plant materials and growth conditions

The extraction and purification of endogenous IAA,

The vine (NA129) and the dwarf cultivars (D0462)

GA3, JA and ZR were measured by modified method

were taken as materials in this study. D0462 has

of Arkhipova et al (2005). Homogenized internode

visible shorter height and smaller number of internode

samples were conducted in cold 80% (v/v) methanol

than NA129. Seeds of both lines were immersed in

for 4 h at 4℃. The supernatant was collected after

water overnight and sown in a nursery bed. One-month

centrifugation at 10 000 g for 15 min. Then the crude

old seedlings were transplanted to the experimental

extract was passed through a C-18 sep-column (Waters,

Station of Horticulture at Northeast Agricultural

Milford, MA). The efflux was collected and dried with

University.

a stream of N2, the residue was then dissolved in 2 mL

　The first internode samples were randomly collected

phosphate-buffered saline (PBS) containing 0.1% (v/v)

from 10 plants of D0462 and NA129 at different

Tween 20 and 0.1% (w/v) gelatin (pH 7.5). IAA,

developmental phases after germination: 23 (tropho-

GA 3, JA and ZR were determined by ELISA kits

phase), 30 (flowering phase), 37 (fruiting phase), 44

based on monoclonal antibodies (China Agricultural

(full bearing period), and 51 days (senescence phase),

University) according to the protocol provided by

respectively. Samples were immediately frozen in

the manufacturer. ELISA tests were performed with

liquid nitrogen, and then stored at –80℃. Plant height

96-well microtitration plates. Each hormone was tested

was monitored during different growth periods.

in triplicates.

Analysis of antioxidant enzyme activity and

Observation of plant structure

-

H2O2 and O2 • contents

Young internodes and leaves of D0462 and NA129

The extracts of 1.0 g young internode were suspended

were cut into small fragments (1 mm×2 mm) and

E-mail: [email protected]

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Xin Ming et al. Comparison of Physiological Properties Between Dwarf and Vine-type Cucumbers (Cucumis sativus Linn.)

doubly fixed with 2.5% glutaraldehyde (pH 6.8) and

Obvious differences in morphology were found

1.2% osmic acid. The prepared internode samples were

between D0462 and NA129. Compared with NA129,

subsequently dehydrated in a graded ethanol series and

dwarf plants D0462 had shorter and less internodes,

embedded with an Epon812 (E Micron Technologies

and less branches. However, there was no difference

Limited, China). Transverse sections were sliced

in the leaf size between the two cucumber cultivars

using a microtome RMC POWERTOME XL (RMC,

(Fig. 1). The plant heights at different development

US) and leaf ultrastructure was observed using a

stages were presented in Table 1. The result showed

transmission electron microscope H-7650 (Hitachi,

that D0462 remained significantly shorter height than

Japan).

NA129. The adult plant height of D0462 was over 60% shorter than that of NA129 at the aging stage (Table 1).

Statistical analysis SPSS 19.0 statistical software package (SPSS, Inc., Chicago, IL, USA) was used for statistical analyses. The data was represented as mean±standard deviation (SD). Differences of mean values were valued by using the one-way analysis of variance (ANOVA) and Duncan's multiple range tests. Statistically significant differences between individual means were assumed at P<0.05.

Results and Discussion Plant morphology From the seedling stage, D0462 was easily identified.

Fig. 1　Growth character of D0462 (left) and NA129 (right)

Table 1　Evaluation of plant height of D0462 and NA129 during growth stage (cm)

Cultivar

23 days (Trophophase)

30 days (Flowering phase)

37 days (Fruiting phase)

44 days (Full bearing period)

51 days (Senescence phase)

NA129

38.8±9.32Aa

58.8±11.73Aa

106.8±23.53Aa

195.5±40.36Aa

253.68±52.63Aa

D0462

20.2±5.17Bb

27±5.18Bb

36.88±8.37Bb

58.5±11.64Bb

63±14.29Bb

A and a represent significance at 0.05 and 0.01 levels, respectively.

H2O2 content of D0462 was 2.94 μmol • g-1 FW, which Contents of H2O2 and O2-•

was 23.82% more than that of NA129 at the same -

The increase in ROS, such as H 2O 2 and O 2 •, was

sampling time. H 2O 2 content of D0462 increased

concluded to play a role in cell senescence (Zhang

until full bearing period (44 days) after gernera-

et al., 2011). In our present study,

-

O2 •

and H2O2 levels

tion and then decreased (Fig. 2B). There was no

of D0462 were higher than those of NA129. The

obvious differences in O2-• contents between D0462

contents of O2-• and H2O2 in D0462 showed similar

and NA129 in the fruiting phase (37 days). The

patterns as those in NA129 (Fig. 2). The maximum

maximum O2-• content of D0462 was (49.71±5.72) http: //publish.neau.edu.cn

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Vol. 21 No. 2 2014

Journal of Northeast Agricultural University (English Edition)

μmol • g-1 FW, approximately 8.69% more than that of

high level O2-• was linked to the inhibition of internode

NA129 (Fig. 2A). Wu et al. (2008) observed that the

elongation in pumpkin.

d

3

c

2 1 0

a

b

b

b

a

60

D0462 NA129

(A)

c

O2- level (μmol• g-1 FW)

H2O2 level (μmol• g-1 FW)

4

b

a

20

30

37

44

Growth period (Day)

c

c

50

d

30 b b

20 10

D0462 NA129 d

40

0

50

(B)

b b

a a 20

30

37

44

50

Growth period (Day)

Fig. 2　Levels of superoxide radical (O2-•) (A) and hydrogen peroxide (H2O2) (B) in different growth periods of D0462 and NA129 Internodes of D0462 and NA129 are selected from 23, 30, 37, 44, and 51 days after germination, respectively. The values are means±SD of triplicates. Significant at P<0.05.

at full bearing period (44 days) and then dropped Antioxidant enzymatic activity

down a little (Fig. 3C). Maximum enhancement in the

Antioxidant enzyme system, such as SOD, CAT and

activity of IAAO (1 086±87.29 U • g-1 FW ) was observed

APX, significantly increased resulting from ROS

in leaves of D0462 at full bearing period (44 days).

overproduction (Tartoura and Youssef, 2011). The

However, IAAO activity in leaves of NA129 changed

results of the present study indicated that the activity of

little during growth (Fig. 3D). The growth and develop-

SOD, CAT and IAAO in D0462 remained much higher

ment of plants is a complicated process, which is re-

than those in NA129 during growth period (Fig. 3).

gulated by some plant regulators, such as endogenous

SOD activities of D0462 and NA129 increased gra-

hormone and antioxidant enzyme (Yan et al., 2010).

dually, and peaked at full bearing period (44 days)

It was reported that antioxidant levels acting as free

after germination. Maximum SOD activity of D0462

radical scavengers could affect the metabolism of

-1

was (293.92±45.32) U • g , which was 66.14% more than

hormone (Li et al., 2007). IAAO has been documented

that of NA129 (Fig. 3A). Similarly, maximum activity

to participate in regulating plant endogenous hormone

of CAT in D0462 and NA129 was discovered at full

content, especially IAA.

-1

bearing period (44 days), reaching (126.33±36.36) U • g

and (81.79±34.27) U • g-1, respectively. In both lines,

Endogenous hormone concentrations

the activity of CAT showed a similar tendency. CAT

Zhao et al. (2010) concluded that plant hormones

activities in D0462 and NA129 at full bearing period

interacted in a very complex way. Balancing hormone

(44 days) increased 4.48 and 7.76 times more than

metabolisms played critical roles in proper regulation

those at trophophase (23 days), respectively (Fig. 3B).

of plant growth and development, and controlled plant

APX activities in leaves of both D0462 and NA129 de-

hight, growth and development (Peng et al., 2009).

creased slightly at first, and then increased. APX acti-

Endogenous hormone contents in inernodes of both

vities of both D0462 and NA129 reached maximum

genotypes were investigated during growth. The results

-1

(617.17±32.44 and 576.49±43.65 U • g , respectively) E-mail: [email protected]

showed that the endogenous hormones (GA3, IAA, ZR

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Xin Ming et al. Comparison of Physiological Properties Between Dwarf and Vine-type Cucumbers (Cucumis sativus Linn.)

and JA) contents were found to be higher in NA129 than

that GA3 could promote cell elongation in either excised

those in D0462 at all the stages of development (Fig. 4).

or intact internode tissue (Yaxley et al., 2001) and

　In NA129, GA3 and IAA significantly increased

acted as a regulator of stem elongation (Fujioka et al.,

at fruiting phase (37 days), and then decreased. The

1988). Many dwarf mutants have been characterised as

endogenous GA 3 level in NA129 reached 571.53

gibberellic acid (GA) deficient or insensitive mutants

-1

ng • g FW, and 1.6 times higher than that in D0462

(Zhang et al., 2011). Patel and Thaker (2007) found

(Fig. 4A) at fruiting phase (37 days). It was reported

that GA3 involved in the internode elongation.

300

b a

200

b a

c a

a

b

a

a 100 0

20

30

37

200

D0462 NA129

(A)

44

CAT activity (U• g-1)

SOD activity (U• g-1)

400

c

150 100 50

a

APX activity (U• g-1)

600

c

20

1 200 c

b b 400

a a

a

c b

a

200

0

20

30

37

44

b

30

37

44

50

Growth period (Day)

50

Growth period (Day)

800 600

a

400

a

a

a

b

b

D0462 NA129

(D)

1 000 IAAO activity (U• g-1)

D0462 NA129

b

b

a

Growth period (Day) (C)

d

b

b b

0

50

D0462 NA129

(B)

a

a

a

a

200 0

20

30

37

44

50

Growth period (Day)

Fig. 3　Activities of SOD (A), CAT (B), APX (C) and IAAO (D) in internode during development period of D0462 and NA129 Internodes of bush and vine plants are selected from 23, 30, 37, 44, and 51 days after germination, respectively. The values are means±SD of triplicates. Significant at P<0.05.

　 IAA content in internode of NA129 rapidly

remained significantly greater in D0462 than those in

increased, peaked at fruiting phase (1070.23±42.47

NA129 during growth period except the full bearing

-1

ng • g FW), and then sharply decreased later. In

period (44 days). It suggested an essential involvement

D0462, however, no significant change of IAA content

of GA 3 and IAA in the height characterization of

in internode was observed, and plant hormone in

cucumber (Fig. 4B). And GA 3 and IAA probably

D0462 still remained lower level (Fig. 4B). IAA was

related to the induction elongation and plant growth.

also reported to play essential role in plant growth

　ZR content in both NA129 and D0462 increased

(Mahouachi et al., 2007). IAA was demonstrated to

and reached the peak at full bearing period (577±

promote normal stem elongation (Wu et al., 2009).

65.27 ng • g-1 FW and 379.61±20.87 ng • g-1 FW, re-

The result showed that both GA 3 and IAA levels

spectively), and then decreased slightly at the end of http: //publish.neau.edu.cn

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Vol. 21 No. 2 2014

Journal of Northeast Agricultural University (English Edition)

the experimental period (Fig. 4). These data suggested

diminished the effect of GA3 on the elongation of the

that ZR might involve in fruiting, whereas the effect

second leaf sheath of dwarf rice seedlings and lettuce

of ZR on plant height was ambiguous. The same

hypocotyls (Yamane et al., 1981), but also reduced

conclusion of rice has been described by Yang et al

IAA-induced elongation of etiolated oat coleoptile

(2000).

(Ueda et al., 1994). In this paper, JA levels in D0462

　JA was demonstrated as a significant regulator to

stems were higher than those in NA129 throughout

control the elongation growth of plants (Ueda et al.,

the growth period (Fig. 4D). This result was supported

1994; Maciejewska and Kopcewicz, 2002). In the

by Kong et al. (2005), who found that JA probably

previous reports, exogenous JA application not only

inhibited stem elongation of Pharbitis nil.

(A) a

2 000 1 500

a

a

a

b

a

a

a b

1 000 500 0

1 200

D0462 NA129 b

(B)

800

a

a

600 400

a

30

37

44

0

50

20

30

a

b b

b

b a

a

a

200

JA (ng • g-1 FW)

ZR (ng • g-1 FW)

b

400

6

D0462 NA129

c

600

37

a

44

50

Growth period (Day)

Growth period (Day) (C)

c

b c

b

a

200 20

D0462 NA129

b

1 000 IAA (ng • g-1 FW)

GA3 (ng • g-1 FW)

2 500

5

(D) a

4

a

a a

a

b

a a

D0462 NA129 a

b

3 2 1

0

20

30

37

44

50

Growth period (Day)

0

20

30

37

44

50

Growth period (Day)

Fig. 4　Leavels of GA3 (A), IAA (B), ZR (C) and JA (D) in internode of D0462 and NA129 during growth stage Internodes of D0462 and NA129 are selected from 23, 30, 37, 44, and 51 days after germination, respectively. Values are means±SD of triplicates. Significant at P<0.05.

reduced noticeably in D0462. Otherwise, the number Microstructure and ultrastructure of internode

of vascular bundle increased, as well the number of

The young internodes and leaves from D0462 and

secondary thickened vessel in D0462 increased. It

NA129 were investigated by SEM (Fig. 5). Micro-

investigated that the size of cells in internode signi-

scopic observation showed that there were no obvious

ficantly decreased, whereas the cell well thickened

differences in the number the number of collenchyma

in collenchyma cells in D0462 (Fig. 5A). Compared

cell layer and in internode between D0462 and

with NA129, elongation of parenchyma cells retarded

NA129. However, the length of cells in internode was

markedly at the early stage in D0462, which might

E-mail: [email protected]

Xin Ming et al. Comparison of Physiological Properties Between Dwarf and Vine-type Cucumbers (Cucumis sativus Linn.)

·25·

contribute to the dwarfism. Previous studies have

mature leaves (50-day-old) in NA129 were somewhat

shown that dwarfism in rice and pumpkin mutant could

vacuolated and filled with chloroplasts and grains.

be attributed to a defect in elongation of parenchyma

And nucleus was close to chloroplasts. The chloroplast

cells (Gao et al., 2009; Wu et al., 2007).

possessed well developed grana and stromal thylakoids

　When observed by TEM, the mesophyll cells of

(Fig. 6a and c).

B

A

Ve

Ve

Fig. 5　Microstructure of main stem in D0462 (A) and NA129 (B) on 40 days A, Longitudinal section of D0462; B, Longitudinal section of NA129; Scale bars=0.1 mm; Ve, Vascular bundle.

a

b c c N

Nu

S Va

Va

T

M

c

M

S

C

2 μm

2 μm c

d

c

c

S

N

c Va N

T

S

Va S N

S

C

C

Va S

Fig. 6　Transmission electron microscopy (TEM) micrographic images of D0462 and NA129 a, Magnification of mesophyll cells in D0462 showing numerous starch grains and swollen chloroplast (bar=2 μm); b, Magnification of mesophyll cells in NA129 showing numerous chloroplast and visible nucleus near the chloroplast (bar=2 μm); c, Details of mesophyll cells in D0462 with chloroplast and vacuole (bar=10 μm); d, Details of mesophyll cells of NA129 with clear chloroplast near the nuclei and nucleolus (bar=10 μm); C, Chloroplast; N, Nuclei; Nu, Nucleolus; Va, Vacuole; S, Starch grain; M, Mitochondria; T, Thylakoid. http: //publish.neau.edu.cn

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Journal of Northeast Agricultural University (English Edition)

　Chloroplast was a main producer of ROS (Sun et

Vol. 21 No. 2 2014

of the United States of America, 85: 9031-9035.

al., 2002), which was known as one of most sensitive

Gao Z, Qian Q, Liu X, et al. 2009. Dwarf 88, a novel putative esterase

organelles in leaf tissues (Krause and Santarius,

gene affecting architecture of rice plant. Plant Molecular Biology, 71:

1975). Therefore, it might be inevitably affected

265-276.

on ultrastructure of chloroplasts as a result of much accumulation of ROS (Asada et al., 1998). Therefore, an increase in the number of plastoglobuli with different shapes could be observed in chloroplasts

Hedden P, Phillips A L. 2000. Gibberellin metabolism: new insights revealed by the genes. Trends in Plant Science, 5: 523-530. Hellewell K B, Rasmusson D C, Gallo-Meagher M. 2000. Enhancing yield of semi-dwarf barley. Crop Science, 40: 352-358.

with swollen thylakoids in D0462 (Fig. 6b and d). The

Kong F J, Gao X Q, Nam K H, et al. 2005. Theobroxide inhibits

thylakoids were found ambiguous or disappeared in

stem elongation in Pharbitis nil by regulating jasmonic acid and

some chloroplasts. Compared to NA129, an increase of

gibberellin biosynthesis. Plant Science, 169: 721-725.

enlarged starch grains in the chloroplasts was detected in D0462. Finally, an increase in vacuole volume with a large quantity of electron-dense points could be seen.

Krause G H, Santarius K A. 1975. Relative thermostability of the chloroplast envelope. Planta, 127: 285-299. Li X M, He X Y, Chen W, et al. 2007. Effects of elevated CO2 and/or O 3 on hormone IAA in needles of Chinese pine. Plant Growth Regulation, 53: 25-31.

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