The Journal of Horticultural Science and Biotechnology

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Changes in root architecture and productivity of

melon (Cucumis melo L. cv. Hispano Nunhems)
promoted by Glomus iranicum var. tenuihypharum

Antonio Luis Alarcón, María José Gómez-Bellot, Antonio José Bernabe,

Gonzalo Calvo & Félix Fernández Martín

To cite this article: Antonio Luis Alarcón, María José Gómez-Bellot, Antonio José Bernabe,
Gonzalo Calvo & Félix Fernández Martín (2019): Changes in root architecture and productivity of
melon (Cucumis�melo L. cv. Hispano Nunhems) promoted by Glomus�iranicum var. tenuihypharum,
The Journal of Horticultural Science and Biotechnology

To link to this article: https://doi.org/10.1080/14620316.2019.1681906

Published online: 24 Oct 2019.

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THE JOURNAL OF HORTICULTURAL SCIENCE AND BIOTECHNOLOGY
https://doi.org/10.1080/14620316.2019.1681906

Changes in root architecture and productivity of melon (Cucumis melo L. cv.

Hispano Nunhems) promoted by Glomus iranicum var. tenuihypharum
Antonio Luis Alarcóna, María José Gómez-Bellotb, Antonio José Bernabec, Gonzalo Calvod
and Félix Fernández Martínc
a
Departamento de Ciencia y Tecnología Agraria, Universidad Politécnica de Cartagena (UPCT), Cartagena, Spain; bDepartamento de Riego,
Centro de Edafología y Biología Aplicada del Segura (CSIC), Murcia, Spain; cSYMBORG. SL., Campus Universitario de Espinardo, Murcia,
Spain; dTransferencia Agrotecnológica S.L. Estación experimental Agroalimentaria Tomás Ferro, Cartagena, Spain

ABSTRACT ARTICLE HISTORY

In this work, the effect of inoculation with the arbuscular mycorrhizal fungus Glomus iranicum Accepted 14 October 2019
var. tenuihypharum on the root development and yield of melon plants (Cucumis melo L. cv.
KEYWORDS
Hispano de Nunhems), grown in soil under intensive agriculture for four months, was evalu- Mycorrhizal inoculation;
ated. The parameters root length, root volume, area, number of root tips, rhizosphere activity, rhizosphere activity; root
yield, and crop quality were measured. The inoculated melon plants had an increased percen- structure; fruit quality; yield
tage of colonisation, which reached 75% at the end of experiment. As a consequence, the
inoculated plants exhibited greater rhizospheric activity with higher bacterial and fungal
population than the control plants. Inoculation produced a greater volume of roots. It was
also observed a higher area of roots with a diameter less than 0.2 mm, and a greater number of
tips in roots with a diameter less than 0.5 mm. This suggested a proliferation of lateral roots and
significant changes on the root architecture. In addition, these plants had greater fruit number
and length, yield, and fruit sugar content than untreated plants. Therefore, the mycorrhizal
association had a strong positive effect on the architecture and root activity, which stimulated
the capacity for nutrient absorption, resulting in a higher yield and fruit quality.

Introduction a protection of the plant from the negative impact of

environmental stresses and disease (Chitarra et al.,
Melon (Cucumis melo L.) is a crop of great economic
2016; Lehto & Zwiazek, 2011; Navarro-Fernández,
significance for Spain in the export trade. In southeast
Aroca, & Barea, 2011). In fact, the AMF can change
Spain, and specifically in the Murcia region with over
the composition and activity of microbial commu-
150,000 ha of crops grown with technically advanced
nities in the rhizosphere (Zhang et al., 2016). Thus,
fertigation, more than 6,000 ha are dedicated to melon
they play an essential role in the functioning of soil
production.
and in nutrient cycling (Harris, 2009). In return, the
In the management of these systems, it is essential
fungi receive plant photosynthates, which are neces-
to foster the development of an efficient root system
sary to complete their life cycle.
that enables an adequate mineral nutrition and
On the other hand, mycorrhizal inoculation may
a proper water balance. Among the options that favour
increase the fruit yield in horticultural species, includ-
the functioning of the root system, the use of arbus-
ing melon (Ortas, 2012). In most cases, an improve-
cular mycorrhizal fungi (AMF) has been proposed in
ment of fruit yield was associated with a greater plant
the recent years. These microorganisms stablish
growth. In turn, many studies have linked more rapid
mutualistic associations with 85% of the plant species
and greater crop growth with higher uptake of nutri-
of agronomic interest (Smith & Read, 2008), exhibit-
ents, mainly phosphorus through the fungus-root
ing high specificity to the soil in which they develop
association (Gholamhoseini, Ghalavand,
(Herrera, Hamel, Fernández, Ferrer, & Furazola,
Dolatabadian, Jamshidi, & Khodaei-Joghan, 2013).
2011). According to Bucher, Wegmüller, and
During this intimate association, the extraradical
Drissner (2009), an effective symbiosis allows the
hyphal mycelium acquires minerals from the soil
plants to explore a greater volume of soil, due to the
beyond the zone accessible by the root (Bonfante &
production of extramatrical mycelia connected to the
Genre 2010).
root system. As a result, nutrient and water uptake by
Some studies have shown a relationship between
the plant is increased.
mycorrhizal colonisation and changes in the struc-
Moreover, the mycorrhizal fungi produce plant
ture and morphology of the root (Yao, Wang, Zhu,
hormones, which improve the structure and quality
& Chen, 2009). It has been reported that AM
of soils, promoting a better rooting. This makes also

CONTACT María José Gómez-Bellot [email protected]

© 2019 The Journal of Horticultural Science & Biotechnology Trust
2 A. L. ALARCÓN ET AL.

colonisation itself influences the architecture of the Table 1. Physico-chemical characteristics of the soil used in the
host root system (Oláh, Brière, Bécard, Dénarié, & assay.
Gough, 2005; Paszkowski & Boller, 2002; Yano, Soil properties
Yamauchi, & Kono, 1996). However, there is no % sand 22.70
% silt 24.20
consensus on the magnitude of the relationship % clay 52.60
between these two characteristics. Several studies pH 8.66
have reported associations between thicker roots EC (dS m−1) 0.29
Assimilable Na (meq 100−1 g) 1.13
and lower root hair density with an increase in Assimilable K (meq 100−1 g) 1.05
the response of plant growth to mycorrhizal inocu- Assimilable Ca (meq 100−1 g) 8.97
Assimilable Mg (meq 100−1 g) 3.72
lation (Declerck, Plenchette, & Strullu, 1995; Assimilable P (ppm) 102.50
Jakobsen, Chen, Munkvold, Lundsgaard, & Zhu, OM (%) 1.47
Nt (%) 0.09
2005). By contrast, other comparative studies have OCt (%) 0.85
indicated that root fineness, root hair density and C/N 9.33
Carbonate (%) 44.00
root hair length are either not associated or posi- Active limestone (%) 16.30
tively associated with a plant growth response to Chloride (meq 100−1 g) 0.29
mycorrhizal inoculation (Duponnois, Plenchette, & Sulphate (meq 100−1 g) 0.41

Ba, 2001; Siqueira & Saggin-Júnior, 2001; Zangaro, EC: Electrical conductivity; OM: Organic matter. Nt: Total nitrogen. OCt: Total
organic carbon.
Nishidate, Vandresen, Andrade, & Nogueira, 2007).
Only a few studies about AMF application have
focused on the morphological changes that occur in The irrigation and fertilisation management
the root system, which make possible an increase in were the same for all plants, using the standard
the nutrient uptake capacity (Hodge, Berta, mineral fertilisation programme of the cultivation
Doussan, Merchan, & Crespi, 2009; Liu, Huang, area. The balanced nutrient solution used during
Zou, & Wu, 2014a; Wu, Zou, & He, 2010). This the growing season was (mM): N (12.8), P (1.4),
suggests a need to study the structure of the root K (7.5), Ca (4.8), and Mg (2.4), plus a standard
system of the plants and its relationship with the micronutrient complex. This nutritional balance
degree of mycorrhization. was varied to suit each phenological stage of the
Therefore, and considering the current trend crop. The average time of fertiliser application
towards the use of biological products in agricul- relative to the total irrigation application was
ture, the aim of this study was to evaluate the effect 25%. The irrigation water used in the trial came
of the application of Glomus iranicum var. tenuihy- from the Tajo-Segura transfer channel (Table 2).
pharum, contained within the product MycoUp®, On 1st April (week 1) a total of 616 melon
on the development and architecture of the root plants were transplanted to the field plot.
system of melon plants, grown under the agro- A randomised block design with four replicates
climatic conditions typical of southeast Spain. per treatment was used. On 4 April, melon plants
Likewise, yield and fruit quality of melon plants were subjected to two treatments: a control treat-
were evaluated. ment, which consisted of conventional fertigation
(Control treatment), and a treatment involving
inoculation with the fungus G. iranicum var.
Material and methods tenuihypharum (inoculated treatment). The outer
rows, as well as the beginning and the end of each
Experimental conditions and plant material row were excluded from the trial, to compensate
The experiment was carried out in a plot of the for the edge effect of the plot. The beginning of
‘Tomás Ferro’ experimental farm at La Palma the harvest was on 24 June and the experiment
(Cartagena, Spain). Nursery seedlings of Piel de ended on 4 August.
Sapo melon cv. Hispano de Nunhems (resistant to
Fusarium, mildew, tobacco mosaic virus, and Table 2. Physico-chemical characteristics of the irrigation
nematodes, and with excellent performance in water used in the assay.
tired soils) were used. The plant spacing was Water properties
pH 7.89
2 × 1.6 m with a planting density of 3130 plants EC (dS m−1) 1.33
ha−1. The soil at this site, characteristic of the Ca (mM) 2.98
agricultural zone of Campo de Cartagena, is Mg (mM) 2.37
Na (mM) 3.09
clayey, strongly calcareous, of high alkalinity (pH K (mM) 0.14
7.89), poor in organic matter (1.47%), and with HCO3− (mM) 3.04
SO42- (mM) 3.15
low levels of assimilable metal micronutrients Cl− (mM) 4.45
(Table 1). The climate in the region is semi-arid, B (μM) 36.7
with dry summers of little rainfall. EC: Electrical conductivity; HCO3: Bicarbonate; SO4: Sulphate.
 THE JOURNAL OF HORTICULTURAL SCIENCE AND BIOTECHNOLOGY 3

Characteristics, production, and application of the software (WinRHIZO, Regent Instruments, Quebec).
mycorrhizal inoculum The diameter was also grouped as <0.1 mm, 0.1 to
0.2 mm, 0.2 to 0.3 mm, 0.3 to 0.5 mm, and 0.5 to
The product MycoUp consisted of the fungus
1.4 mm, considering those with smaller diameter the
G. iranicum var. tenuihypharum, which was isolated
active roots since they have a greater capacity of nutri-
from a sodic-saline soil. It is a mycorrhizal inoculum
ent and water absorption.
based on Glomus iranicum var tenuihypharum
1,2 × 104 MPN on 100 ml substrate. It is also char-
acterised by an abundant production of external Harvest: yield and quality
mycelium, intense root colonisation, and resistance
to the high concentrations of nutrients present in the At the end of the experiment, crop yield, number of
soil solution in contact with the roots of intensive fruits per plant, and fruit length were determined in 5
crops under fertigation (Fernández & Juárez, 2012). plants per treatment and replicate. Fruit quality was
The propagation of the fungus was performed in a clay also evaluated by determination of the °Brix and, using
mineral substrate with a host plant, for 5 months. At a penetrometer, the firmness.
the end of the life cycle of the plant, the root system,
mycorrhizal propagules, spores, mycelium, and colo- Statistical analyses
nised rootlets were treated in a cryogenic mill
(Fernández & Juárez, 2012) and vacuum-packed. During the experiment, each treatment consisted of
On 4 April (Week 1) inoculation with the mycor- 260 plants, divided into four randomly distributed
rhizal fungus was performed. The product was applied blocks. The data were analysed by t-Student test, to
through the irrigation system at a dose of 3 kg ha-1, in verify whether there were significant differences, using
the area of the root system of the plants. Initially, SPSS statistics 24.
sampling was performed weekly, starting in the week
of the transplantation (week 1). From week 8 onwards,
Results
samples were taken every 15 days until harvest (week
10), on 24 June. Colonisation and rhizosphere microflora
At week 2, the roots of the inoculated melon plants
Colonisation and the rhizosphere microflora showed a higher percentage of mycorrhizal colonisa-
tion (35.4%) than those of the control plants (non-
The mycorrhizal colonisation and the rhizosphere inoculated plants) (10.2%) (Figure 1). The colonisa-
microflora were determined at the beginning of root tion of the mycorrhizal plants increased throughout
growth (week 2), at early flowering (week 4), and after the assay, reaching 75.3% at week 7, while the coloni-
fruit set (week 7); on days 15, 30, and 45 after trans- sation of the control plants remained similar to the
plantation, respectively. For each treatment and repli- initial value (Figure 1).
cate, 5 samples of young melon roots were taken at Regarding the rhizosphere microflora, significant
a depth of 15–20 cm. The percentage colonisation, differences in the amount of bacterial microflora
determined by the staining technique of Phillips and were observed between the treatments for all the
Hayman (1970), was evaluated microscopically using
the quadrant intersection method on plates
(Giovanetti & Mosse, 1980). The rhizosphere micro-
flora was evaluated, by the soil dilutions method, as
the most probable number of colony forming units per
unit of rhizosphere soil (CFU per ml of soil) (Lorch,
1995).

Development of the root architecture

The root architecture (entire root with axis and lat-
erals) was studied periodically during the experiment.
For each sampling and for each treatment and repli-
cate, 5 entire melon roots were removed, washed, and
scanned – in both greyscale (transparency adapter, 150
dpi, image file T format) and colour (reflective back-
Figure 1. Evolution of the percentage colonisation for mycor-
ground, blue, 96 dpi, TIF format). Subsequently, the rhizal plants and Control plants during the experiment.
length, volume, diameter of the roots and the number Different lower case letters indicate significant differences
of root tips, were determined with image analysis between treatments according to t-student 0.05 test.
4 A. L. ALARCÓN ET AL.

samplings (Figure 2(a)). Mycorrhizal plants had

higher values than control plants, reaching 3.3 × 107
CFU ml−1 of bacteria at week 4. The mycorrhized
plants also had a significant increase in the amount
of fungal microflora with respect to the control plants,
from the first sample onwards (Figure 2(b)). At sam-
pling 4, mycorrhizal plants had a fungal population of
5 × 105 CFU ml−1 while that of control plants was
3 × 104 CFU ml−1.

Development of the root architecture

To measure the development of the root architecture,
the root length, volume, diameter, area, and number of
tips were taken into account.
The total root length increased almost throughout
the experiment, for both treatments (Figure 3(a)).
There were two stages of significant increase for both
treatments: a rapid increase between week 4 and week
5, and another between week 8 and week 9.
Mycorrhizal plants had greater root length than con-
trol plants at three samplings (week 3, week 5 and
week 9). At the end of the experiment, mycorrhizal
Figure 2. Evolution of the bacterial (a) and fungal (b) plants had a total root length of 2915 cm while that of
microflora for mycorrhizal plants and Control plants during control plants was 2792 cm (Figure 3(a)).
the experiment. Different lower case letters indicate sig-
nificant differences between treatments according to t-stu- Concerning the evolution of the total root volume,
dent 0.05 test. there were significant differences between the two

Figure 3. Evolution of the root length (a), root volume (b), and number of root tips (c) for mycorrhizal plants and Control plants
during the experiment. Asterisks indicate statistically significant differences between treatments according to t-student 0.05 test.
 THE JOURNAL OF HORTICULTURAL SCIENCE AND BIOTECHNOLOGY 5

Photograph 1. Root architecture of Control plants in weeks 3 (a) and 11 (c) and of mycorrhizal plants in weeks 3 (b) and 11 (d).

treatments throughout the experiment, the mycorrhi- mycorrhiza treatment led to a higher number of tips
zal plants having a greater volume of roots at four of for roots in this diameter class (Figure 4(a)) compared
the samplings (week 6, 7, 9, and 10) (Figure 3(b)). The to the control treatment (Figure 4(b)).
root volume increased progressively for both treat- The root length/volume ratio of the non-
ments; at the end of the experiment the values were mycorrhizal plants tended to be higher than in the
6305 cm3 for the control plants and 6681 cm3 for the treated plants as the assay progressed. After trans-
mycorrhizal treatment plants. planting, a progressive decrease of this ratio in both
The minimum and maximum number of root tips types of plant (Figure 5) was also observed.
in the control plants were 382 and 1217, respectively, The root area corresponding to roots less than
while the corresponding values for the mycorrhizal 0.1 mm in diameter was lower than that of the roots
plants were 594 and 1751, respectively (Figure 3(c)). 0.1–0.2 mm in diameter at the start of the assay, for
For most of the experiment, the number of root tips both treatments (Figure 6(a,b)). However, from week
were significantly higher in mycorrhizal than in non- 4, the area of the roots less than 0.1 mm in diameter
mycorrhizal plants (Figure 3(c); Photograph 1). began to increase progressively, to the detriment of the
Regarding the number of tips observed in each root roots with diameter 0.1–0.2 mm. In addition, the root
diameter class throughout the experiment, a higher area corresponding to roots less than 0.1 mm was
number of tips corresponding to roots of diameter significantly higher in mycorrhizal plants than in
0.1–0.3 mm was found, for both treatments, compared non mycorrhizal plants throughout almost the whole
to the other diameters (Figure 4(a,b)). In addition, the experiment (Figure 6(a)). For roots with a diameter

Figure 4. Number of root tips according to the root diameter class during the experiment, the mycorrhizal plants (a) and Control
plants (b) during the experiment. Different lower case letters indicate significant differences between treatments according to by
t-student 0.05 test.
6 A. L. ALARCÓN ET AL.

positively affected by the inoculation of the fungus

G. iranicum var. tenuihypharum. Despite the claims
of some authors about fertilised crops (Graham,
Duncan, & Eissenstat, 1997; Smith & Smith, 1996),
AMF successfully colonised the roots of the fertigated
melon plants (Figure 1). The percentage of colonisa-
tion was similar to those found in other studies with
the same fungus – in lettuce (Vicente-Sánchez et al.,
2014), tomato (Fernández et al., 2014), grapevine
(Nicolás et al., 2015), and Laurustinus (Gómez-Bellot
et al., 2015). In melon, a similar percentage of coloni-
sation with the same genus of fungus has been found
before (Huang et al., 2011). Furthermore, colonisation
was more effective three months after inoculation
Figure 5. Relationship between the root length and volume (Fernández et al., 2014).
during the experiment, for mycorrhizal plants and Control In our study, the treatment with G. iranicum var.
plants. Asterisks indicate statistically significant differences
tenuihypharum generated greater effective colonisa-
between treatments according to t-student 0.05 test.
tion than the native soil fungi. As a result, there was
an increase in the abundance of both bacterial and
between 0.1–0.2 mm, the same trend was observed fungal microflora (Figure 2), verifying an earlier
although there were significant differences only at work on watermelon inoculated with Glomus clarum
week 2, 4 and 8. (Kaya, Higgs, Kirnak, & Tas, 2003). Wang, Srivastava,
Wu, and Fokom (2014) stated that mycorrhizal inocu-
lation increased the network of extra radicular hyphae
Harvest: yield and quality
in the rhizosphere of plants of Poncirus trifoliata
The analysis of crop yield and its quality parameters L. Raf. and raised the content of soil organic carbon.
showed that plants treated with Glomus iranicum var According to Rillig and Mummey (2006), organic
tenuihypharum produced a higher number of fruits per carbon deposition by the roots of host plants can
plant (4, 7) and a significant increase yield 28.4% com- promote the microbial activity that, in turn, contri-
pared to untreated plants. In addition, the fruits of the butes greatly to soil aggregate formation and stabilisa-
inoculated plants were more elongated and with more tion. Therefore, the mycorrhiza may affect the
ºBrix, although the firmness values were similar for the microbial population in the rhizosphere directly or
two treatments (Table 3). indirectly through changes in the composition and
quantity of root exudates, or through the exudates of
the AMF (Fernández & Juárez, 2012).
Discussion The success in melon root colonisation and
The results from this study showed that melon (cv. establishment of soil microbiota might led to
Hispano de Nunhems) plants grown in soil were changes in the root architecture, regarding length

Figure 6. Evolution of the root surface area in the active roots of <0.1 mm in diameter (a) of 0.1–0.2 mm in diameter (b) during the
experiment, for mycorrhizal plants and Control plants. Asterisks indicate statistically significant differences between treatments by
t-student 0.05 test.
 THE JOURNAL OF HORTICULTURAL SCIENCE AND BIOTECHNOLOGY 7

Table 3. Number of fruits per plant, yield, fruit length, fruit firmness, and ºBrix of mycorrhizal plants and
control plants after the growth period.
Production Yield Fruit length
(Fruits plant−1) (kg plant−1) (cm) Firmness ºBrix
Control 3.6 b 9.19 b 21.72 b 4.79 a 13.01 a
Mycorrhizal plants 4.7 a 11.8 a 22.27 a 4.82 a 13.47 b
P * * * ns *
Different lower case letters indicate significant differences between treatments according to t-student test.

(longer roots) as well as volume, area, and number which could be due to changes produced in the
of tips (Hodge et al., 2009; Sukumar et al., 2013). different stages of the plant, soil conditions and
The colonisation of roots is not distributed evenly; biotic stimuli (Gregory, 2006; Pérez, Sierra, &
mycorrhizal fungi preferably do not colonise roots Montes, 2011). The formation and function of
with an anchoring function (greater than 0.5 mm) AMF can be affected by changes in humidity, tem-
since they have a higher content of lignin. The perature, nutrient availability, and even cultural
AMF colonise tap and lateral roots (Hooker, practices, which can promote the development of
Munro, & Atkinson, 1992) as it is easier to pene- AMF at one time or reduce it at others (Augé,
trate young roots growing (Amijee, Stribley, & 2000). In our case, the architecture of the mycor-
Lane, 1993). Therefore, the increase in the number rhizal root system changed, becoming flatter and
of tips in roots with a diameter between 0.1 and closer to the soil surface – where the oxygen con-
0.3 mm (fine roots) (Figure 4) as well as the rise in centration is higher. These roots gained in volume
the root area corresponding to the finest roots and number of tips, with greater development of
(Figure 6) were directly related to the effectiveness hyphae than for non-inoculated plants (Figure 3;
of the root colonisation. The roots of smaller dia- Figure 4). Thus, they might have greater ability to
meter are considered more active than those of capture nutrients.
larger diameter, and thus, they contribute more to Several authors have claimed that a high rate of
nutrient uptake (Salgado & Cautin, 2008; Sukumar colonisation causes further soil exploration by roots,
et al., 2013). Several authors also observed leading to an increase in mineral nutrient and water
a positive relationship between the volume of soil uptake by the roots. Hence improving the water and
explored and the surface area explored with nutrient status of the plant (Gómez-Bellot et al., 2015;
increasing mycorrhization (Hodge et al., 2009). Nicolás et al., 2015). As a result, there is an increase in
This increase in root branching and volume has the contents of chlorophylls and, ultimately, in the
also been described in fruit (Bouma et al., 2001), photosynthetic rate (Feng et al., 2002; Vicente-
horticultural (Fusconi, Lingua, Trotta, & Berta, Sánchez et al., 2014). Huang et al. (2011) showed
2005), and forest trees (Orfanoudakis, Wheeler, & that melon plants inoculated with three different spe-
Hooker, 2010). cies of Glomus increased rates of gas exchange, espe-
Moreover, increased fungal and bacterial popu- cially when inoculated with G. mosseae, and enhanced
lations in the soil could also promote changes in growth. In our case, inoculation of melon plants with
the root structure. Numerous studies have G. iranicum var. tenuihypharum gave a higher number
described the role of auxins produced by microor- of fruits per plant, increased yield and fruit length, and
ganisms in root development (Liu, Srivastava, & higher ºBrix; that is, not only a greater number of
Wu, 2014b; Overvoorde, Fukaki, & Beeckman, fruits but also larger fruits (Table 3). Nicolás et al.
2010). The regulation of the transport of auxins (2015) observed that inoculation with the same
inhibits root elongation and promotes development mycorrhizal fungus had a positive effect on the yield
of lateral roots (Peret et al., 2009). Other root and ºBrix of grapes. Increases in ºBrix arising from the
exudates, such as flavonoids and strigolactone effect of mycorrhizas have been found also in tomato
(Akiyama, Matsuzaki, & Hayashi, 2005; Vierheilig (Nzanza, Marais, & Soundy, 2012). Ortas (2010)
& Piche, 2002), stimulate the growth and branching showed that mycorrhizal inoculation of soil increased
of external hyphae. These hyphae help to explore growth and fruit yield in cucumber. According to
a larger volume of soil than is possible with the Harrill (1998), a mean value for melon would be 12
root hairs alone (Rajan, Reddy, & Bagyaraj, 2000). ºBrix. The values in our study were 13.01 and 13.47
However, the molecular complexity of these pro- ºBrix for the control and inoculated plants, respec-
cesses is still far from being fully understood. tively, reflecting a high concentration of sugars in the
Fluctuations in the number of root tips and in fruit, especially for the mycorrhized plants (Harrill,
the root surface area along the assay (Figure 4; 1998). Therefore, effective mycorrhizal colonisation
Figure 6), for both treatments, were also observed, of the roots might produce a physiological
8 A. L. ALARCÓN ET AL.

improvement within the plant, resulting in an Bucher, M., Wegmüller, S., & Drissner, D. (2009). Chasing
improvement of production of assimilates – which the structures of small molecules in arbuscular mycor-
contributes to an increase in crop yield. rhizal signaling. Current Opinion on Plant Biology, 12,
500–507. doi:10.1016/j.pbi.2009.06.001
Chitarra, W., Pagliarani, C., Maserti, B., Lumini, E.,
Siciliano, I., Cascone, P.,. . . & Guerrieri, E. (2016).
Conclusions Insights on the impact of arbuscular mycorrhizal symbio-
sis on tomato tolerance to water stress. Plant Physiology,
Inoculation of soil with Glomus iranicum var.
171, 1009–1023. doi:10.1104/pp.16.00307
tenuihypharum led to successful colonisation of Declerck, S., Plenchette, C., & Strullu, D.G. (1995).
the roots of melon plants. The development of the Mycorrhizal dependency of banana (Musa acuminata,
fungus induced higher microbial activity and pro- AAA group) cultivar. Plant and Soil, 176, 183–187.
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stimulation of seventeen fallow leguminous plants inocu-
ability of the plant to capture nutrients. As lated with Glomus aggregatum in Senegal. European
a result, the plants were more productive and Journal of Soil Biology, 37, 181–186. doi:10.1016/S1164-
yielded fruit of higher quality. These results high- 5563(01)01077-9
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in mycorrhizal plants. (2002). Improved tolerance of maize plants to salt stress
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tion of soluble sugars in roots. Mycorrhiza, 12, 185–190.
doi:10.1007/s00572-002-0170-0
Acknowledgments Fernández, F., & Juárez, J. (2012). Procedimiento de
The authors wish to thank to the company SYMBORG SL obtención de un agente micorrizógeno. Patente Europea.
for its financial support to carry out this investigation as well No: ES20110030566 20110411. doi:10.1094/PDIS-11-11-
as the Polytechnic University of Cartagena (UPCT), for the 0999-PDN
use of its facilities and logistical support. Fernández, F., Vicente-Sanchez, J., Maestre-Valero, J.F.,
Bernabé, A.J., Nicolás, E., Pedrero, F., & Alarcón, J.J.
(2014). Physiological and growth responses of young
tomato seedlings to drip-irrigation containing two low
Disclosure statement doses of the arbuscular mycorrhizal fungus Glomus ira-
No potential conflict of interest was reported by the authors. nicum var. tenuihypharum sp. nova. Journal of
Horticultural Science and Biotechnology, 89, 679–685.
doi:10.1080/14620316.2014.11513137
Fusconi, A., Lingua, G., Trotta, A., & Berta, G. (2005). Effects
Funding of arbuscular mycorrhizal colonization and phosphorus
application on nuclear ploidy in Allium porrum plants.
This work was supported by the Symborg [B73574832];
Mycorrhiza, 15, 313–321. doi:10.1007/s00572-004-0338-x
Universidad Politécnica de Cartagena [Q-8050013-E];
Gholamhoseini, M., Ghalavand, A., Dolatabadian, A.,
Jamshidi, E., & Khodaei-Joghan, A. (2013). Effects of
arbuscular mycorrhizal inoculation on growth, yield,
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