CSIRO PUBLISHING

Crop & Pasture Science, 2016, 67, 9198

http://dx.doi.org/10.1071/CP15110

Benecial soil microbe promotes seed germination, plant growth

and photosynthesis in herbal crop Codonopsis pilosula
Yong-Na Wu A,*, Yu-Lan Feng A,*, Paul W. ParB, Ying-Long Chen C, Rui Xu D, Shan Wu E,
Suo-Min Wang A, Qi Zhao A, Hui-Ru Li A, Yin-Quan Wang D, and Jin-Lin Zhang A,F
A

State Key Laboratory of Grassland Agro-Ecosystems, College of Pastoral Agricultural Science and Technology,
Lanzhou University, Lanzhou 730000, P. R. China.
B
Department of Chemistry and Biochemistry, Texas Tech University, Lubbock, TX 79409-1061, USA.
C
Institute of Agriculture, School of Earth and Environment, The University of Western Australia,
35 Stirling Highway Crawley, WA 6009, Australia.
D
Departments of Nurse and Chinese Medicine, Gansu University of Traditional Chinese Medicine, Lanzhou,
Gansu, 730000, P. R. China.
E
Department of Biology, School of Life Sciences, Sun Yat-sen University, Guangzhou 510275, P. R. China.
F
Corresponding author. Email: jlzhang@lzu.edu.cn

Abstract. Bacillus subtilis strain GB03 enhances growth and photosynthesis in the model plant Arabidopsis thaliana and
several crop plants. In the present study, the effects of seed soaking with GB03 suspension culture and its volatile organic
compounds on seed germination of Codonopsis pilosula (Franch.) Nannf. were investigated, and soil-grown C. pilosula
seedlings were assayed to measure growth and photosynthetic capacity after soil inoculation with GB03. Both seed soaking
with GB03 suspension culture and the presence of volatile organic compounds enhanced seed germination, especially seed
germination vigour. GB03 signicantly improved shoot and root length, branching, plant biomass (whole plant fresh and dry
weight), leaf area and chlorophyll content in C. pilosula seedlings after 20, 40 and 60 days of soil inoculation. GB03
signicantly enhanced transpiration rate, stomatal conductance and net photosynthetic rate, but decreased intercellular CO2
concentration. This study provides insight for the application of selected bacteria to improve biomass in Chinese herbal crops.
Additional keywords: Bacillus subtilis, Codonopsis pilosula, growth promotion, photosynthesis, seed germination.
Received 1 April 2015, accepted 17 August 2015, published online 14 January 2016

Introduction
Plant growth-promoting rhizobacteria (PGPRs) are naturally
occurring soil microorganisms able to colonise roots and
stimulate plant growth (de Zelicourt et al. 2013; Gao et al.
2013). PGRPs have been applied to a wide range of
agricultural crops for the purpose of growth enhancement,
including improved seed germination and establishment, plant
biomass, yield, nutrient uptake efciency, and biotic and
abiotic stress tolerance (Kloepper et al. 1991; Zhang et al.
2008a; Harvey et al. 2009; de Zelicourt et al. 2013; Song and
Ryu 2013; Han et al. 2014). PGPR colonisation has also been
shown to activate bacterial synthesis of plant hormones, including
indole-3-acetic acid, cytokinin and gibberellin, which have
been correlated with PGPR-mediated plant-growth promotion
(MacDonald et al. 1986; Timmusk et al. 1999).
As an important species among PGPRs, Bacillus subtilis can
be isolated from many environments, terrestrial and aquatic, and
can adapt to grow in diverse conditions within the biosphere
*

(Stein et al. 2002; Stein 2005; Earl et al. 2008). Bacillus

subtilis, which is not toxic to humans, widely exists in soils
and can produce a wealth of antibacterial substances including
lipopeptides, polypeptides, and phospholipids (Stein et al. 2002;
Kloepper et al. 2004; Zhang et al. 2011; Gao et al. 2013). GB03,
a commercially available B. subtilis strain that emits a complex
blend of volatile organic compounds, has been studied for its
role in inducing growth promotion and abiotic stress tolerance
in Arabidopsis (Ryu et al. 2004; Zhang et al. 2008a, 2008b,
2010). GB03 has been shown to trigger differential expression
of approximately 600 Arabidopsis transcripts related to cellwall modications, primary and secondary metabolism, stress
responses, hormone regulation and other expressed proteins
(Zhang et al. 2007). GB03 also induced growth promotion by
lowering auxin levels in shoots, with translocation to roots in
Arabidopsis (Zhang et al. 2008a). Photosynthetic capacity in
Arabidopsis is enhanced by GB03 through improvement in the
efciency of conversion of light energy, as well as through an

These authors contributed equally to this work.

Journal compilation
CSIRO 2016

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Crop & Pasture Science

Y.-N. Wu et al.

increase in chlorophyll content (Zhang et al. 2008b). Recently, we

found that GB03 promoted growth and salt tolerance in wheat
(Triticum aestivum, Zhang et al. 2014) and in white clover
(Trifolium repens, Han et al. 2014).
Codonopsis pilosula (Franch.) Nannf. is a traditional
medicinal herb crop in China, Korea, and Japan. This plant
has many kinds of biologically active components, including
polysaccharides, triterpenes, phytosterols, sesquiterpenes,
phenolic glycosides, alkaloids and a variety of essential amino
acids for human bodies (Xin et al. 2012; Wang et al. 2013).
A herbal tea prepared from the roots of this crop is prescribed for
fortifying the immune, digestive and haematopoietic systems, and
has long been used in the traditional Chinese medicines to treat
a weak spleen, stomach, lung, and immune system ailments,
energy deciency, high blood pressure, and poor appetite (Wang
et al. 2013; Kim et al. 2014).
However, there is no report that B. subtilis GB03 promotes
seed germination, plant growth and photosynthesis in traditional
Chinese herbal crops. Thus, the aim of this study was to evaluate
the effects of GB03 on growth promotion in C. pilosula. The study
shows a potential application of GB03 in growth promotion of
important Chinese herbal crops.
Materials and methods
Bacterial suspension culture
Bacillus subtilis strain GB03 and Escherichia coli DH5a were
streaked onto Luria broth (LB) agar plates and incubated at 288C
under darkness for 24 h. The bacterial cells were harvested from
LB agar plates into liquid LB media to yield 109 colony forming
units mL1, as determined by optical density and serial dilutions
with plate counts (Zhang et al. 2008b).
Seed germination experiments
Seeds of Codonopsis pilosula were surface-sterilised (10 s
of 75% (v/v) ethanol soaking followed by 10 min of 5% (v/v)
sodium hypochlorite soaking), then rinsed seven times in sterile,
distilled water.
For the rst germination experiment, sterilised seeds were
soaked in LB medium for 5 min (control) or in GB03 suspension
culture for 5, 10 or 20 min. Seeds were then placed on two layers
of lter paper wetted with 5 mL sterile, distilled water in Petri
dishes (diameter 9 cm; 100 seeds per dish with six replicates).

Germination rate (%)

120
90

The Petri dishes were sealed with sealing lm and kept in an

incubator at 258C in darkness.
The second germination experiment tested whether volatile
organic compounds affected seed germination of C. pilosula.
Sterilised seeds were placed on two layers of lter paper wetted
with 5 mL sterile, distilled water, in one side of plastic Petri dishes
that had a centre partition (diameter 12 cm; 100 seeds per dish
with six replicates). The other side of the Petri dish contained LB
solid media inoculated with 20 mL suspension culture of GB03,
DH5a, liquid LB media or sterile, distilled water. The Petri dishes
were sealed with sealing lm and kept in an incubator at 258C
in darkness.
The number of germinated seeds was recorded daily from day
1 to day 10 of germination. Germination rate (%) was estimated as
(Gt/T)
100, where Gt is the total number of germinated seeds
within 10 days and T is the number of total seeds. Germination
vigour (%) was determined as (Gmax/T)
100, where Gmax is
the maximum number of seeds germinated within 1 day during
the 10 days of germination and T is as dened above (Vicente
et al. 2007; Song et al. 2008; Han et al. 2013; Gorai et al. 2014).
Plant growth experiment
Sterilised seeds were sown in plastic pots (diameter 15 cm, height
20 cm; 1.0 kg soil and four seedlings per pot with six replicates)
containing autoclave-sterilised commercial vermiculitesoil
mix watered with half-strength modied Hoaglands nutrient
solution. After germination, the soil under each seedling was
inoculated with 1 mL bacterial suspension culture or liquid LB
media (control) near the roots (Zhang et al. 2010), and then
mulched for 24 h. Two inoculations were carried out every week
until harvest. Plants were grown in a glasshouse under metal
halide and high-pressure sodium lamps set to a cycle of 14 h light
and 10 h darkness, with a total light intensity of 800 mmol m2.s1,
an average temperature of 28  28C23  28C (daynight), and
a relative humidity of 70  10% (Han et al. 2013).
Plant growth measurements
Plants were sequentially harvested at 0 (control), 20, 40 and
60 days after germination and initial inoculation. Plants were
removed from the pots and roots were rinsed with water to remove
attached soil. Shoot height and root length were measured with
ruler and number of branches was counted. Roots and shoots

(a)
b

80
ab

60
30

Germination vigor (%)

92

(b)
a

60

b
c

40
d
20
0

Control

10

20

Control

10

20

GB03
Fig. 1. (a) Germination rate and (b) germination vigour of C. pilosula seeds soaked in water control
or Bacillus subtilis GB03 suspension culture for various periods (5, 10 and 20 min). Capped vertical lines
are standard deviations (n = 6). Means with the same letter are not signicantly different at P = 0.05
(Duncans test).

Bacillus subtilis promotes herbal crop growth

Crop & Pasture Science

5 mm

2 mm

GB03

Control

Fig. 2. Germinated C. pilosula seeds soaked in Bacillus subtilis GB03 suspension culture for 5 min (left) or in Luria broth
medium for 5 min (control, right).

100

(a)

60

a
b

80

60
40
20
0

Germination vigor (%)

Germination rate (%)

120

(b)
a

40
b

bc

DH5

LB

Water

20

0
GB03

DH5

LB

Water

GB03

Treatments
Fig. 3. (a) Germination rate and (b) germination vigour of C. pilosula seeds with exposure to Bacillus subtilis
GB03, Escherichia coli DH5a, Luria broth (LB) and water control after 10 days. Capped vertical lines are
standard deviations (n = 6). Means with the same letter are not signicantly different at P = 0.05 (Duncans test).

93

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Y.-N. Wu et al.

different periods. Leaf chlorophyll content was estimated by

using a portable chlorophyll meter (SPAD-502; Konica
Minolta, Tokyo) at 0, 20, 40 and 60 days. Transpiration rate,
stomatal conductance, intercellular CO2 and net photosynthetic
rate of 60-day-old seedlings were measured using a
photosynthetic system (GFS 3000, ZQ-WALZ009; Walz,
Effeltrich, Germany) in the greenhouse from 09 : 30 to 11 : 30.
All parameters were measured at a photosynthetic available
radiation of 800 mmol m2 s1 (saturated light intensity),
relative humidity 65  5%, leaf temperature 28  28C and CO2
concentration of 360 mmol mol1 (Liu et al. 2005; Ma et al. 2012).

were separated and blotted gently with paper towel. Fresh weights
were determined immediately and samples were oven-dried at
808C for 2 days for dry weight measurement.
Photosynthetic capacity measurements
Leaf area, chlorophyll content, transpiration rate, stomatal
conductance, intercellular CO2 and net photosynthetic rate were
determined. Whole plant leaves were harvested to measure leaf
area per plant via a leaf area meter (Perfection 4870 Photo
scanner; Epson America Inc., Long Beach, CA, USA) for the
(c)

5 cm

GB03

(a)

Control

(b)

GB03

Control

GB03

Control

Fig. 4. Growth promotion of C. pilosula plants treated with Bacillus subtilis GB03 for various periods: (a) 20 days, (b) 40 days,
(c) 60 days. GB03 suspension culture is in Luria broth (LB) medium; control is LB medium without bacteria.

Shoot height (cm)

40

(a)

30

30

a
b

20
c
10
f
0

f
0

d e
20

40

60

Root length (cm)

94

(b)

a
b

20

c
d
e

10
f
0

f
0

20

40

60

Days after inoculation

Fig. 5. (a) Shoot height and (b) root length of C. pilosula seedlings treated with Bacillus subtilis GB03 for
various periods (0, 20, 40 and 60 days). Shaded and unshaded bars represent GB03 treatment and Luria
broth control, respectively. Capped vertical lines are standard deviations (n = 6). Means with the same letter
are not signicantly different at P = 0.05 (Duncans test).

Bacillus subtilis promotes herbal crop growth

Crop & Pasture Science

Statistical analyses
Germination rate, germination vigour, shoot height, root length,
branching, fresh weight, dry weight, leaf area, chlorophyll
content, transpiration rate, stomatal conductance, intercellular
CO2 and net photosynthetic rate are presented as means with
standard deviations (n = 6). Data were subjected to analysis of
variance (ANOVA) and Duncans multiple range tests were
performed to detect differences among means at a signicance
level of P = 0.05 by using the software SPSS 13.0 (SPSS Inc.,
Chicago, IL, USA).

95

(Fig. 4). Soil inoculation of GB03 under seedlings of C. pilosula

enhanced shoot height by 36%, 82% and 92% (P < 0.05) at 20,
40 and 60 days, respectively (Fig. 5a). Root length was also
signicantly increased by 42%, 17% and 47% (P < 0.05) at 20,
40 and 60 days, respectively (Fig. 5b).
Soil inoculation with GB03 signicantly increased the number
of shoot branches by 100%, 83% and 91% (P < 0.05) at 20, 40 and
60 days, respectively (Fig. 6). Total biomass of plants with GB03
soil inoculation treatment also increased, by 85%, 79% and 210%
(P < 0.05) for fresh weight and by 133%, 82% and 205% for dry
weight at 20, 40 and 60 days, respectively (Fig. 7).

Results
GB03 augmented seed germination of C. pilosula

GB03 soil inoculation effects on photosynthetic capacity

Both seed soaking with GB03 suspension culture and exposure to

the presence of its volatile organic compounds enhanced seed
germination, especially seed germination vigour, of C. pilosula.
Of the seed-soaking treatments in GB03 suspension culture, only
the treatment with 20 min of soaking improved seed germination
signicantly (by 12%, P < 0.05) compared with the control
(Fig. 1a). However, germination vigour (Gmax was obtained
on the third day of germination) was signicantly improved, by
210%, 190% and 150% for the seeds treated with 5, 10 and 20 min
of soaking in GB03 suspension culture, respectively, compared
with control (Fig. 1b). Seed treatment with 5 min of soaking was
most effective (P < 0.05), and interestingly, hypocotyls of
germinated seeds with 5 min of soaking had more root hairs
than those of control seeds (Fig. 2).
Ten days after exposure to volatile organic compounds from
GB03, germination rate and germination vigour of C. pilosula
were signicantly improved (Fig. 3). Compared with exposure
to DH5a, LB and water, seed germination was signicantly
improved by 14.1%, 18.7%, and 23.6% (P < 0.05), respectively,
with GB03 exposure (Fig. 3a), and seed germination vigour by
94.4%, 105.9%, and 116.8% (P < 0.05) (Fig. 3b).

Soil inoculation with GB03 signicantly enhanced leaf area, by

22%, 53% and 49% (P < 0.05) at 20, 40 and 60 days, respectively.
Chlorophyll content also was improved through GB03 soil
inoculation, by 51%, 65% and 35% (P < 0.05) at 20, 40 and
60 days, respectively (Fig. 8).

Growth promotion of C. pilosula by soil inoculation

with GB03

b
2
c
1
g g
0

20

40

60

Branch number

c
c

d
e

20

40

60

Days after inoculation

Fig. 6. Number of branches of C. pilosula seedlings treated with Bacillus
subtilis GB03 for various periods (0, 20, 40 and 60 days). Shaded and
unshaded bars represent GB03 treatment and Luria broth control,
respectively. Capped vertical lines are standard deviations (n = 6). Means
with the same letter are not signicantly different at P = 0.05 (Duncans test).

0.6

(a)
a

a
6

Dry weight (g plant1)

Fresh weight (g plant1)

Compared with the control, growth of C. pilosula seedlings was

enhanced at 20, 40 and 60 days by soil inoculation with GB03

(b)
a

0.4
b
0.2

c
d e

20

40

60

Days after inoculation

Fig. 7. (a) Fresh weight and (b) dry weight of C. pilosula seedlings treated with Bacillus subtilis GB03 for
various periods (0, 20, 40 and 60 days). Shaded and unshaded bars represent GB03 treatment and Luria broth
control, respectively. Capped vertical lines are standard deviations (n = 6). Means with the same letter are not
signicantly different at P = 0.05 (Duncans test).

Crop & Pasture Science

Y.-N. Wu et al.

Discussion

Leaf area (cm2 plant1)

Seed germination is an important stage in the life cycle of plants

and determines whether the plants can establish successfully
(Song et al. 2005). PGPRs have been applied to a wide range of
agricultural crops to enhance growth, including improved
seed emergence, plant weight and crop yields (Kloepper et al.
1991, 2004; Par et al. 2011). Seed germination rate increased by
1040% for canola (Brassica napus) when seeds are coated with
PGPR before planting (Kloepper et al. 1991). In Arabidopsis,

60

(a)
a
b

40

c
d

20
e

g g
0

20

f
40

mechanistic studies revealed elevated sugar accumulation as

well as suppression of classic glucose signalling responses,
including hypocotyl elongation and seed germination, with
exposure to GB03 (Zhang et al. 2008b). In the present work,
both seed soaking with GB03 suspension culture and exposure to its
volatile organic compounds enhanced seed germination, especially
seed germination vigour, of C. pilosula. Interestingly, hypocotyls
of germinated seeds treated with 5 min of GB03 suspension
culture soaking had more root hairs than did control seeds.
Root colonisation by B. subtilis can augment plant growth
through bacterial synthesis of plant hormones, breakdown of
plant-produced ethylene, and increased mineral availability in the
soil by bacterially produced siderophores (Ali et al. 2009). Soil
inoculation with GB03 enhanced C. pilosula growth at 20, 40 and
60 days, by stimulating leaf-area enlargement and photosynthetic

Chorophyll (mg g1 FW)

Soil inoculation with GB03 enhanced transpiration rate by

41%, stomatal conductance by 38% and net photosynthetic rate
by 40%, and reduced intercellular CO2 concentration by 11%
(P < 0.05) at 60 days (Fig. 9).

50

(b)
a

40

30

10

60

20

20

40

60

Days after inoculation

Fig. 8. (a) Leaf area and (b) chlorophyll content per plant of C. pilosula seedlings treated with Bacillus
subtilis GB03 for various periods (0, 20, 40 and 60 days). Shaded and unshaded bars represent GB03 treatment
and Luria broth control, respectively. Capped vertical lines are standard deviations (n = 6). Means with the
same letter are not signicantly different at P = 0.05 (Duncans test).

(a)

150
a

2
1

Stomatal conductance
(mmol m2 s1)

Transpiration rate
(g m2 h1)

500

Intercellular CO2
(ppm)

a
100

50

(c)
a

400

(b)

300
200
100
0

Net photosynthetic rate

(mol m2 s1)

96

(d )
a

3
b
2
1
0

GB03

LB

GB03

LB

Fig. 9. (a) Transpiration rate, (b) stomatal conductance, (c) intercellular CO2 concentration and (d) net
photosynthetic rate of C. pilosula seedlings treated with Bacillus subtilis GB03 for 60 days. Shaded and
unshaded bars represent GB03 treatment and Luria broth control, respectively. Capped vertical lines are
standard deviations (n = 6). For each parameter, different letters indicate signicant difference at P = 0.05
(Duncan tests).

Bacillus subtilis promotes herbal crop growth

rate. Leaf area development is important in plant production,

being strongly related to plant growth and biomass accumulation
by improving the total photosynthetic surface area (GutirrezBoem and Thomas 2001; Baldissera et al. 2013). Increased shoot
and root growth after inoculation with B. subtilis GB03 has been
reported for some plant species such as Arabidopsis thaliana
(Zhang et al. 2009), sweet basil (Ocimum basilicum) (Banchio
et al. 2009), wheat (Zhang et al. 2014) and white clover (Han et al.
2014). However, previous studies have not provided information
on whether soil symbiosis regulates shoot branching. In this
study, GB03 increased the number of branches produced as
early as 20 days into treatment with GB03 soil inoculation.
Increased plant biomass accumulation through inoculation with
benecial soil bacteria has been reported for many plant species
(Xie et al. 2009). For instance, there was a 2-fold increase in dry
weight of sweet basil after GB03 soil inoculation (Banchio et al.
2009). Pathogen-infected cotton plants had 1.9-times higher dry
weight when treated with B. subtilis UFLA285 soil inoculation
than when untreated (Medeiros et al. 2011). In the present study,
C. pilosula plants treated with GB03 soil inoculation showed
increased biomass. Transpiration rate, stomatal conductance, net
photosynthetic rate and intercellular CO2 concentration are all
important physiological indexes directly linked to photosynthetic
capacity. Photosynthetic capacity is augmented in Arabidopsis
exposed to GB03 by increasing photosynthetic efciency and
chlorophyll content (Zhang et al. 2008b). In the present study,
soil inoculation with GB03 conferred on seedlings of C. pilosula
the ability to increase leaf photosynthesis as well as stomatal
conductance and transpiration rate, which potentially increased
water-use efciency.
In conclusion, this study demonstrated that the soil bacterium
B. subtilis GB03 enhanced seed germination, especially seed
germination vigour of C. pilosula. Furthermore, inoculation
with GB03 into the rhizosphere signicantly improved plant
growth and photosynthetic capacity, mainly through increases
in shoot height, root length, shoot branching, leaf area and net
photosynthetic rate. This study provides evidence that the
application of selected bacteria can increase seed germination,
plant growth and biomass production of Chinese herbal crops.
Acknowledgements
Professor Jairo Palta from CSIRO, Australia, is thanked for providing valuable
comments on the manuscript. This work was supported by the National Basic
Research Program of China (grantNo.2014CB138701), the National Natural
Science Foundation of China (Grant No. 31172256, 31222053 and 81260616)
and the Fundamental Research Funds for the Central Universities (Grant
No. lzujbky-2014-m01 and lzujbky-2015-194).

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