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International Journal of Agriculture and Crop Sciences.

Available online at www.ijagcs.com


IJACS/2015/8-2/194-202
ISSN 2227-670X ©2015 IJACS Journal

Assessing The Native Arbuscular Mycorrhizal


Symbioses To Rehabilitate A Degraded Coastal
Sand Dune In Algeria
Bouazza Marouf K1, Ighilhariz Z1, de Lajudie P2, Duponnois R2, Bekki A1
1. Laboratoire de Biotechnologie des Rhizobiums et Amélioration des Plantes, Département de Biotechnologie,
Université d’Oran, Ahmed Ben Bella Algeria.
2. IRD, Laboratoire des Symbioses Tropicales et Méditerranéennes, UMR LSTM, Montpellier, France

Corresponding author email: [email protected]

ABSTRACT: We examined local arbuscular mycorrhizal fungal (AMF) plant symbioses for their
potential for land rehabilitation after sand industrial exploitation in a study site of the coastal sand
quarry of Terga (NW Algeria, semi-arid climate). We focused on the mycorrhizal status of five
representative plant species (Acacia saligna, Lotus creticus, Retama monosperma, Pistacia lentiscus
and Juniperus oxycedrus) present in the Terga quarry. The arbuscular mycorrhizal (AM) structures
showed significant and contrasting rates of root colonization among plant species. Spores density in
soil was generally high, but variable depending on soil disturbance and local conditions. AMF
diversity study in the rhizospheric soil fraction resulted in the distinction of eleven spore morphotypes
affiliated to four genera (Glomus, Scutellospora, Gigaspora and Acaulospora) with predominance of
Glomus. The mycorrhizal soil infectivity (MSI) level could be considered as significant except in the
rhizosphere of R. monosperma. Our results suggest that A. saligna, L. creticus and P. lentiscus are
well adapted to Terga local conditions and promote arbuscular mycorrhizal symbiosis. Management
of mycorrhizal soil potential by introducing these species is very promising approach to contribute to
degraded ecosystem rehabilitation such as in Terga. They may further constitute an important
source of AM inoculum in semi-arid ecosystems.
KEY WORDS: Glomales biodiversity; Mycorrhizal soil infectivity; Revegetation strategies; Semi-arid.

INTRODUCTION

The semi-arid ecosystems such as Mediterranean coastal areas are frequently subjected to natural and
anthropogenic disturbances (Le Houérou, 2000). This is the case of Terga coastal dunes (NW Algeria) after
massive industrial sand mining. Land degradation is further exacerbated by lower rainfall, long periods of
drought and high winds causing loss of vegetation and degradation of physical, chemical and biological soil
properties (Requina et al., 2001). All these climatic and soil disturbance conditions have severe detrimental
effect on the ecosystem restoration, for which a revegetation strategy is needed.
Among successful revegetation strategies widely reported in semi-arid ecosystem, are those including
mycorrhizal symbioses (Requina et al.,, 1996; Azcon-Aguilar et al., 2003; Sanguin et al., 2013). Two strategies
are usually offered based on the level of environmental degradation (Duponnois et al., 2013): (I) management
of the native soil mycorrhizal potential via native, drought tolerant and mycotrophic plant species establishment
(Ouahmane et al., 2006a), and/or (II) plants inoculation through selected mycosymbiots (Estaún et al., 1997;
Caravaca et al., 2003; Duponnois et al., 2007).
Arbuscular mycorrhizal fungi (AMF) can improve plants nutrient uptake efficiency in soils with low
fertility by increasing the absorption surface and nutrient sources mobilization (Smith and Read, 2008). They
help plants to tolerate biotic (Declerck et al., 2002) and abiotic stress (Mathur and Vyas, 2000; Yano-Melo et
al., 2003).They may influence on the structure and activity of microbial Communities in mycorrhizosphere
(Dabire et al., 2007) and promote coexistence between plant species (Hart et al., 2003). AMF promote plant
settlement, especially in nutrient-poor environments such as sand dunes and contribute to dune fixation by
forming aggregates of sand grains (Koske and Polson, 1984).
Although the AMF are important for vegetation persistence in semi–arid Mediterranean ecosystem
(Caravaca et al., 2003), understanding the mycorrhizal associations in Terga ecosystem and their distribution in
the soil is needed for sound sustainable restoration and management of the exploited site (Requina et al.,
Intl J Agri Crop Sci. Vol., 8 (2), 194-202, 2015

1996). Therefore, the objective of this work is to determine the mycorrhizal status of five local plant species and
studied the relationship between plant species, mycorrhizal potential and soil fertility.

MATERIALS AND METHODS


Study site and samples collection
The study was conducted in Terga coastal sand dunes, located in Northwestern Algeria submitted to
semi-arid Mediterranean climate with hot dry summers. The average annual rainfall, occurring mainly in
autumn, is 300 mm. A botanical survey was carried out. The study focused on five plant species present in the
quarry; Acacia saligna, Retama monosperma, Lotus creticus, Juniperus oxycedrus and Pistacia lentiscus.
Sampling is performed in a preserved area in two locations: (1) on a high dune facing the sea (N40 ° 37 'E0
44'), and (2) in the back of the dune which stretches a plateau characterized by dense natural vegetation (N41 °
16 E2 ° 05 '). For each target species, ten individual plants were randomly chosen. Roots and soil were
collected from the rhizosphere of each plant. The control sample was taken from the bare soil. The
physicochemical parameters of different soil composites were analyzed.

AM root colonization detection and evaluation


AM infection was observed after root staining according to Philips and Hayman (1970) under an optical
microscope to spot mycorrhizal structures and to estimate the target species AM root infection degree as
described by Trouvelot et al. (1986).

Spores density assessment


Soil samplings were performed in Spring and Winter. AM fungal spores were extracted from
rhizospheric soil of target species and bare soil using the wet sieving method described by Gerdermann and
Nicolson (1963). The spore suspension was centrifuged on a sucrose gradient to concentrate the spores and to
minimize soil particles and root fragments (Daniels and Skipper, 1982). The mixture obtained after spore
extraction was observed under a binocular microscope. The average spore number was expressed as a score
per 100 g of dry soil.

Morphological identification of spores


Spores were sorted out manually under a binocular microscope according to color and size. In each
homogeneous lot, the morphological characteristics of spores were observed under microscope (Olympus SZ
H10 research stereomicroscope, connected to computer digital image analysis software). Slides of each
different spore morphotype were prepared using either polyvinyl-alcohol alone or mixed with Melzer’s solution
(Azcon-Aguilar et al., 2003). Spores identification was mainly based on color, size, wall structure and hyphal
attachment, according to the descriptions provided by the International Culture Collection of Arbuscular
mycorrhizal Fungi (http:// www.Invam.caf.wvu.edu).

Mycorrhizal soil infectivity (MSI) determination


The method used for MSI determination was described by Plenchette et al. (1989). Young mycotrophic
plants are cultivated on a series of concentrations of rhirospheric soils and bare soil, diluted with the same
sterilized soil. Six dilutions (100, 48, 24, 12, 6 and 3%) were performed in triplicate. The seeds of sorghum
(Sorghum sudanense) were germinated for two days in Petri dishes on humid filter paper and transplanted into
small plastic pots containing 100g of each dilution with ten seeds per pot. Culture was carried out for two weeks
with 16h light and 25 ± 1 ° C. The plants were watered daily with sterile distilled water.
At harvest, the whole root system of each seedling was carefully rinsed with water and prepared
according to Phillips and Haymann (1970). Mycorrhizal structures were observed under an optical microscope.
Each root system showing at least one infection point (hyphal penetration in the root) was considered as
mycorrhizal. These results were expressed as the percentage of mycorrhizal plants per pot.
Linear regressions (Y =a X + b) was calculated from the relationship between the percentage of
mycorrhizal plants versus the logarithm of the natural soil quantity. Mycorrhizal Soil Infectivity (MSI) is
expressed as MSI50units, corresponding to the natural soil quantity required to infect 50% of a plant population
under the biological test conditions.

Statistical Analyses
Data were processed with the variance analysis (ANOVA) at p <0.05 using XL Stat software. Means
were compared by the Tukey’s HSD (Honestly Significant Difference) test (p < 0.05). Spearman correlation
coefficient was calculated between all variables. The relative abundance of spores was calculated (Johnson et
al., 1991). The Shannon diversity index (H) was calculated according to the following equation: H = −∑ (Pi ln
[Pi]) where Pi is the relative abundance (the number of individuals of the species i in relation to the total number

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of individuals of all species), and ln is the natural log. Pielou’s evenness index (E) was obtained by the following
equation: E = H/log (S) where S is the total number of species.

RESULTS
Study site characteristics
The preserved area in Terga is characterized by a large plant biodiversity of trees, shrubs and
herbaceous plants (Table 1).We chose to further focus our study on Acacia saligna, Juniperus oxycedrus,
Pistacia lentiscus, Retama monosperma, and Lotus creticus. The mined area is totally naked.
The physico-chemical parameter (Table 2) shows that all soils have a sandy soil structure, characterized by an
alkaline pH. Nitrogen, Phosphorus and organic matter are generally low.

AM Root colonization
In all plant species, root fragments microscopic examinations revealed the presence of AMF structures
like arbuscules and vesicles (Figure 1). The vesicles were widely observed compared to arbuscular structures
present only in A. saligna and P. lentiscus.
Variance analysis indicates that AM colonization depends on plant species (F = 9.904, P <0.0001). The
lowest infection frequency value (F %) was observed for J. oxycedrus (54%), while it didn’t differ significantly
among other species (72% to 82.5%). As regards the intensity of AM colonization in the root system (M %) and
in mycorrhizal fragments (m %), the difference among species was significant (Table 3).

Table1. Terga dune floristic survey.


Trees Shrubs Herbaceous
Juniperus phoenicea Calycotome villosa intermedia Ammophila arenaria
Juniperus oxycedrus Chamaerops humilis Asparagus acutifolius
Acacia saligna Cistus salviifolius Bellis sylvestris
Tamarix sp Cistus sericeus Brassica fruticulosaglabberina
Ephedra altissima Calendula tomentosa
Erica multiflora Centaurea fragilis
Genista cephalanta Centaurium umbellatum
Halimium halimifolium Clematis cirrhosa
Helianthemum origanifolium Crucianella maritima
Helianthemum racemosum Cyperus kalli
Lonicera implexa Daphne gnidium
Lycium intricatum Echinops spinosus
Osyris lanceollata Lagurus ovatus
Phillyrea angustifolia media Lavandula dentata
Pistacia lentiscus Limonium densiflorum
Quercurs coccifera Lobularia maritima
Retama monosperma bovei Lotus creticus
Rosmarinus officinalis Malcolmia arenaria
Matthiola tricuspidata
Medicago littoralis
Micromeria inodora
Ononis antennata
Ononis variegata
Orlaya maritime
Pancratium maritimum
Paronychia argentea
Prasium majus
Reicharedia tingitana
Rubia peregrine
Rumex bucephaloflorus
Senecio leucanthemifolius crassifolius
Silene ramosissima
Stipa tenacisssima
Serratula mucronata
Urginea maritimum

Table 2. Physico-chemical analysis of the target species rhizospheric soil and bare soil
Parameters Clay Loam Sand pH Organic matter Total Total
% Nitrogen% Phosphorus %

Soils origins
A. saligna 3 5 92 8.87 6.49 0.05 0.037
L. creticus 2 4 94 8.13 0.40 0.01 0.031
R. monosperma 2 4 94 8.37 0.10 0.03 0.033
P. lentiscus 5 3 92 8.45 6.47 0.07 0.035
J. oxycedrus 4 5 91 8.39 6.39 0.05 0.035
Bare soil 2 4 94 9 0.10 0.10 0.037

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Vesicule
Arbuscule

Figure 1. Arbuscular Mycorrhizal Fungi structures in target species roots

Table 3. Arbuscular mycorrhizal colonization in roots.


Species Mycorrhizal Mycorrhizal Mycorrhizal intensity Arbuscules Arbuscules
frequency (F%) intensity in root in mycorrhizal content in content in root
system (M%) fragment (m%) mycorrhizal system (A%)
fragment (a%)
a b b
A. saligna 82.50 36.25 44.17 24.86 9.00
a d d
R. monosperma 80.00 27.30 34.12 0.00 0.00
a c c
L. creticus 72.00 28.40 39.44 0.00 0.00
a a a
P. lentiscus 80.00 37.26 46.57 5.09 1.90
b e e
J. oxycedrus 54.00 14.80 27.40 0.00 0.00
For each column, values followed by the same letter are not significantly different at P <0.05

Spore density
The average spore density (Table4) varies very significantly among species (F= 34.98, P <0.0001) with
largest spore scores for R. monosperma soil (123.6 spores /100g soil) and J. oxycedrus (111.6 spores/100g
soil) and close scores for A. saligna, P. lentiscus and L. creticus (65.5, 80.8, 76.6 spores/100g soil
respectively). Bare soil had very poor spore score (12.16 spores /100g soil).
Winter and Spring samples (Table 4) showed a negative correlation (r= -0.623, α= 0.05) and a highly significant
variation between seasons (F= 33.42, P <0.0001). Thus the maximum spore score was recorded in R.
monosperma Spring soil (123.6 spores/100g soil) then decreasing to 44.8 spores /100g soil in winter. Similar
trends were also observed for the four other plant species.

Table 4. Spore densities across seasons


spores number /100g soil
Soils Origins Winter Spring
a b
A. saligna 36.33±4.16 67.33±8.02
a b
L. creticus 32.33±11.01 76.33±14.36
a a
R. monosperma 45.00±11.53 123.33±27.53
a b
P. lentiscus 32.00±8.88 80.33±4.50
a a
J. oxycedrus 41.33±5.50 110.00±18.02
b c
Bare soil 12.00±1.00 12.33±3.05
For each column, values followed by the same letter are not significantly different at P <0.05

Spores diversity
Spore morphotypes observed according to shape, color and size; vary from 4 in bare soil to 11 in
rhizospheric soil (Table 5). Most of the morphotypes are common in all soils and some are specific. The relative
abundance of the different spore types is shown in Table 5. Presence of characteristic structures (hyphae,
saccule and walls) on some spores observed allows their allocation to a genus. These spores belong to four
genera: Glomus, Scutellospora, Gigaspora and Acaulospora. The genus Glomus is the most frequent in the five
studied plant species. It varies colors among spores (black, dark brown, light brown, hyaline and orange). The
genus Gigaspora spores has yellowish white whose Gigaspora margarita (Figure 2). Brown spores and brown
with dark outline characterized by the saccule, correspond to Acaulospora (Figure 2).
Intl J Agri Crop Sci. Vol., 8 (2), 194-202, 2015

Table 5. Morphological characteristics and relative abundance of spores


Spore Morphotypes Relative abundance (%) of spores morphotypes
Color diameter (µm)
A. saligna L. creticus R. P. lentiscus J. oxycedrus Bare soil
monosperma
Black 60-100 19 14 9 4 8 32
Black 250-400 3 5 11 - 4 16
light brown 40-100 10 11 10 10 10 -
light brown 240-450 23 4 11 6 8 -
dark brown 40-100 8 7 13 4 16 3
dark brown 160-450 10 1 13 2 12 -
Cream to 240-400 6 - 6 - 2 -
yellowish
Hyaline to pale 40-80 12 9 15 9 17 49
yellow
Brown dark wall 80-120 7 19 12 3 23 -
orange 60-80 2 4 - - - -
oval brown 20-30 - - - 29 - -
irregular brown 200-360 - 15 - 26 - -
Irregular brown 200-360 - 11 - 7 - -
yellow

a b c

d e f

g Figure 2.Morphological Structures of AMF spores isolated from the target

species: (a) Scutellospora sp. in PVLG, (b) Scutellospora sp. in Melzer’s,

(c) Gigaspora margarita , (d) Glomus sp. , (e) Glomus sp. ,(f)Glomus sp. ,

(g) Acaulospora sp.

The Shannon diversity index (H) and the Pielou's evenness index (E), are parameters that express
AMF diversity (Table 6). H index ranged from 2.02 to 2.28 and follow the gradient L. creticus>R. monosperma>
A. saligna> P. lentiscus>J. oxycedrus. E index vary from 0.43 to 0.53 following the gradient L. creticus> A.
saligna> P. lentiscus> R. monosperma> J. oxycedrus.

Mycorrhizal Soil Infectivity


The MSI50 characterizes the amount of rhizospheric soil required to infect 50% of a plant population
under bioassay conditions. Here it varied significantly depending on the soil (F= 10.277, P < 0.001). Tukey test
showed three groups of rhizospheric soils compared to the level of infectivity (Table 7). A low value of MSI 50
indicates high soil infectivity. Concerning A. saligna soil, only 16.22 g of rhizospheric soil is sufficient to infect
50% of plants. In comparison, the necessary amount of R. monosperma soil is 29.50 g and over to 100 g for
bare soil. This means that there were not enough propagates of mycorrhizal fungi in 100 g of bare soil to obtain
Intl J Agri Crop Sci. Vol., 8 (2), 194-202, 2015

50% of mycorrhizal seedlings. The number of MSI50units per 100 g soil is calculated by dividing 100 by MSI 50
value (g). More the number of units MSI50 is higher, more the soil is rich in mycorrhizal propagates.

Table 6. AMF diversity as reflected by Shannon diversity and Pielou’s evenness indexes
Species H (Shannon) E (Pielou)
A. saligna 2.10 0.50
R. monosperma 2.17 0.45
L. creticus 2.28 0.53
P. lentiscus 2.05 0.47
J. oxycedrus 2.02 0.43

Table 7. Mycorrhizial soil infectivities in target species rhizospheric soil and bare soil
soils origins Regression MSI50units g per 100g Nb MSI50 units g per 100g
coefficients
b b
A. saligna 0.94 16.22 6.17
a a
R. monosperma 0.68 29.50 3.39
b b
L. creticus 0.88 18.15 5.51
b b
P. lentiscus 0.88 18.09 5.53
b b
J. oxycedrus 0.94 19.74 5.07
c
Bare soil - >100 <1

Correlation between spore density Root colonization and soil fertility


Table 8 presents the correlations between the density of spores, mycorrhizal intensity (M %) and soil
fertility in total nitrogen (N), total phosphorus (P) and organic matter (OM). The Pearson correlation coefficient
is denoted by r. Negative correlations could be observed between spore density and the content of P and
between spore density and M%.

Table 8. Correlation coefficient (r) between spore density and mycorrhiza intensity and soil fertility
Organic Total Nitrogen % Total Phosphorus% Mycorrhiza intensity Nb MSI50
matter% (M%) units /100 g
spore density -0.281 -0.091 -0.551 -0.570 -0.566
Mycorrhiza intensity (M%) 0.107 0.261 0.262 1 0.290
Values in blod are different from 0 at signification level alpha=0,05

DISCUSSION

The arbuscular mycorrhizal fungi are geographically widely distributed (Öpik et al., 2006) and almost
generally present in the plant kingdom (Trappe, 1987).Many reports showed that most plant species of semi-
arid Mediterranean environments are mycorrhized (Requena et al.,, 1996 Ferrol et al., 2004; Maremmani et al.,
2003).Here we detected the presence of arbuscular mycorrhizal fungi in roots of all target species (A. saligna,
L. creticus, R. monosperma, P. lentiscus and J. oxycedrus). Such symbiotic associations were reported
previously (Ducousso and Thoen, 1991; Escaray et al., 2010; Hatimi and Tahrouch, 2007; Ferrol et al., 2004;
Caravaca et al., 2006). AMF infection rates were high and vary depending on the studied species. Our results
are consistent with those reported by Requina et al., (1996) in South Spain. According to Diagne and Ingleby
(2003) mycorrhizal infection is affected by soil disturbances but not by the climate or the vegetation.
Despite current adverse conditions, dune soils may harbor rich and varied bacterial and fungal
microflora (Hatimi and Tahrouch 2007). Despite the total absence of vegetation in the Terga exploited area and
poor nutrients and limited water, spores could be detected in soil. The spore density is known to vary
considerably among ecosystems. Values range from a few dozen to 10,000 spores per 100 g soil (Frioni et al.,
1999; Zhao and Li, 2005; Abbas et al., 2006; Camprubí et al., 2010). Spore densities found in this study in
rhizospheric soils can be considered as relatively large compared to densities reported in semi-arid coastal
dunes (Hatimi and Tahrouch 2007; Camprubí et al., 2010), but remain relatively low compared to those
reported in other semi -arid soils (Ouahmane et al., 2006b; Abbas et al., 2006).
The spore densities observed in rhizospheric soils of R. monosperma and J. oxycedrus are
substantially higher than those of A. saligna, L. creticus and P. lentiscus. Nicolson (1960) reported that the
factors affecting the distribution of AM fungi in sand dunes are plant species, degree of dune stability, organic
matter and soil microbiological activity. Soil disturbance affect spore formation in these dunes. Indeed R.
monosperma and J. oxycedrus were found in a fixed dune protected from the wind and surrounded by dense
vegetation ; in comparison the other colonizing species were subjected to severe climatic disturbances and
limited canopy. Spore density is higher in older dunes than in the mobile and the younger dunes located near
the sea (Koske, 1975). Soil disturbance affect the AM fungi community in sand dunes systems (Beena et al.,
2000).
The seasonal variation in spore abundance has been reported by several authors (Hayman, 1970;
Sutton and Barron, 1972; Giovanetti et al., 1985; Hatimi and Tahrouch 2007). It may be attributed to the

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process of spore formation, germination and degradation (Smith, 1980). Our results show that there is a
seasonal dynamics with increase spore density during Spring, consistent with Smith (1980) observation.
In Terga ecosystem, spore density is negatively correlated to the rate of AM root colonization. Thus, the
impact of disturbances on spore production appears to be higher than on root colonization of host plants. In arid
areas, few or no sporulation is observed although roots are clearly colonized (Morton et al., 1993). Several
studies showed that there is no correlation between spore density and intensity of root infection (Mukerji and
Kapoor, 1986; Clapp et al.,, 1995;Merryweather and Fitter, 1998). In controlled conditions correlation between
spore population and root infection is often positive (Jensen and Jakobsen, 1980). The weak relationship
between the formation of endomycorrhizae and density of spores may be due to the mortality, dormant spores
(Jasper et al., 1991) and discontinuous sporulation of some Glomeromycota members (Schüßler et al., 2001).
However, the spores don’t seem to be the only ones able to infect plants but also mycorrhizal roots and
extraradical mycelia in the soil (Klironomos and Hart, 2002).
This study evidences the rich diversity of AM fungi in the sandy soil of Terga coastal dunes with eleven
spore morphotypes belonging to four genera Glomus, Acaulospora, Scutellospora, and Gigaspora. The
Shannon diversity index indicates that some fungal species are more frequent than others. Moreover this index
increases; the plant species is favorable to all fungal species, offering same survival opportunities. Therefore L.
creticus rhizospheric soil exhibit high diversity of AM species; previously observed by Camprubí et al. (2010) in
Spanish Mediterranean dunes. The values of the evenness index being in the medium of [0, 1], indicate a
variable species distribution. A high value of this index (tends to 1) would show an equitable distribution of
species. In contrast, a low value (tends to 0) means that there are in the middle several rare species and there
is disproportionate distribution of species, which therefore translates into a very selective vegetation.
Fungi belonging to the genus Glomus were predominant in samples, with the highest number of
morphotypes. According Turrini et al. (2008), the diversity of species other than Glomus in highly disturbed
ecosystems is low. This can be explained by the ability of Glomus species to initiate a colonization process
from spores, infected roots and hyphae unlike genera as Gigaspora and Scutellospora, able to initiate new root
infection only from spores (Biermann and Linderman 1983).
MSI50values in rhizospheric Terga soils are similar to those found in cultivated soils in France
(Plenchette et al., 1989b) and higher than those found in the fallows of Senegal (Duponnois et al., 2001). R.
monosperma rhizospheric soil shows the lowest mycorrhizal soil infectivity although it is the richest in spores.
Soils in disturbed ecosystems contain very few viable spores (Diop et al., 1994) which may explain the negative
correlation found between MSI50 units and spore density in Terga soils. Other rhizospheric soils have an
important mycorrhizal soil intensity compared to the infectivity potential estimated in the rhizosphere soil of the
Spanish Mediterranean dunes (Camprubí et al., 2010).
The spore density in the rhizosphere soil is negatively correlated between the phosphorus content.
Frioni et al. (1999) found a negative correlation between AM colonization and P content. Mycorrhizae have an
important role in the survival and growth of plants in soils poor in nutrient particularly phosphorus (Smith and
Read, 1997).
The overall results (soil fertility, root colonization, MSI, spores’ diversity and density) suggest that L.
creticus, A. saligna and P. lentiscus are most suitable for the rehabilitation of Terga degraded soils. Several
studies have suggested that legume with mycorrhizal dependency can improve the fertility restoration of
disturbed soils and AMF biodiversity (Duponnois et al., 2001). Ferrol et al. (2004) suggested that the mycelial
network AM colonized P. lentiscus soil could be a major source of AM inoculum.

CONCLUSION

The management of soil mycorrhizal potential by the introduction of A. saligna, L. creticus and P.
lentiscus is very promising and may validly contribute to Terga ecosystem rehabilitation, since they are adapted
to these ecosystem local conditions and have the ability to promote arbuscular mycorrhizal symbioses which
plays a key role in the ecosystem productivity and stability. They can also be an important source of AM
inoculum in semi-arid ecosystems.

ACKNOWLEDGEMENTS

We are thankful to Pr HADJAJ Aouel Segheir for his help in the botanical inventory and KADIRI Amina for her
support in the statistical analysis.

REFERENCES

Abbas Y, Ducousso M, Abourough M, Azcon R, Duponnois R. 2006. Diversity of arbuscular mycorrhizal fungi in Tetraclinis
articulata (Vahl) Masters woodlands in Morocco. Ann ForSci 63:285–291

200
Intl J Agri Crop Sci. Vol., 8 (2), 194-202, 2015

Alguacil M, Caravaca F, Dias-Vivancos P, Hernandez JA, Roldan A. 2006. Effect of arbuscular mycorrhizal and induced drought stress on
antioxidant enzyme and nitrate reductase activities in Juniperus oxycedrus L. grown in a composted sewage sludge-amended
semi- arid soil. Plant Soil 279:209-218
Azcon-Aguilar C, Palenzuela J, Roldan A, Bautist S, Vallejo R, Barea JM. 2003. Analysis of the mycorrhizal potential in the rhizosphere of
representative plant species from desertification-threatened Mediterranean shrub lands. Appl. Soil Ecol 22:29-37
Beena KR, Raviraja NS, Arun AB, Sridhar KR. 2000. Diversity of arbuscular mycorrhizal fungi on the coastal sand dunes of the west coast
of India. Current Science 79:1459-1466
Biermann BJ, Linderman RG. 1983. Use of vesicular-arbuscular mycorrhizal roots, intraradical vesicles and extraradical vesicles as
inoculum. New Phytologist 95:97-105
Brundrett MC, Abbott LK. 1994. Mycorrhizal fungal propagules in the Jarrah forest. I. Seasonal study of inoculum levels. New phytol
127:539-546
Camprubí A, Calvet C, Cabot P, Pitet M, Estaún V. 2010. Arbuscular mycorrhizal fungi associated with psammophilic vegetation in
Mediterranean coastal sand dunes. Spanish Journal of Agricultural Research 8(S1):S96-S102
Caravaca F, Barea JM, Palenzuela J, Figueroa D, Alguacil MM, Roldan A. 2003 Establishment of shrub species in a degraded semiarid site
after inoculation with native or allochthonous arbuscular mycorrhizal fungi. Applied Soil Ecology 22:103-111
Caravaca F, Alguacil MM, Azcón R, Roldán A. 2006. Formation of stable aggregates in rhizosphere soil of Juniperus oxycedrus: Effects of
AM fungi and organic amendments. Appl. Soil Ecol 33:30-38
Clapp JP, Young JPW, Merryweather JW, Fitter AH. 1995. Diversity of fungal symbionts in arbuscular mycorrhizins from a natural
community. New Phytologist 130:259-265
Dabire AP, Hien V, Kisa M, Bilgo A, Sangare KS; Plenchette C; Galiana A; Prin Y; Duponnois R. 2007. Responses of soil microbial
catabolic diversity to arbuscular mycorrhizal inoculation and soil disinfection. Mycorrhiza 17(6):537-545
Daniels BA, Skipper HD. 1982. Methods for the recovery and quantitative estimation of propagules from soil. In Methods and Principles of
Mycorrhizal Research. Ed. N. C. Schenck. The American Phytopathological Society.pp:29-36
Declerck S, Risede JM, Rufyikiri G, Delvaux B. 2002. Effects of arbuscularmycorrhizal fungi on severity of root rot of bananas caused by
Cylindrocladiumspathiphylli. Plant Pathology 51(1):109-115
Diagne O, Ingleby K. 2003. Écologie des champigions mycorhiziens arbusculaire infecant Acacia raddiana. In Un arbre au désert, Grouzis
M, Floc HL (ed) IRD Editions Paris: 205-228
Diop T, Gueye M, Dreyfus B, Plenchette C, Strullu DG. 1994. Indigenous arbuscularmycorrhizal fungi associated with Acacia albida Del. in
different areas of Senegal. Appl. Environ. Microbiol 60:3433-3436
Ducousso M, Thoen D .1991. Les types mycorhiziens des Acacieae. In :Physiologie des Arbres et Arbustes en zones arides et semi-arides.
Groupe d'Etude de l'Arbre, Paris, France, pp:175-182
Duponnois R, Plenchette C, Thioulouse J, Cadet P.2001. The mycorrhizal soil infectivity and arbuscularmycorrhizal fungal spore
communities in soils of different aged fallows in Senegal. Appl. SoilEcol 17:239-251
Duponnois R, Plenchette C, Prin Y, Ducousso M, Kisa M; Ba AM; Galiana A. 2007. Use of mycorrhizal inoculation to improve
reafforestation process with Australian Acacia in Sahelianecozones. Ecological Engineering 29(1):105-112
Duponnois R, Ramanankierana H, Hafidi M, Baohanta R, Baudoin E, Thioulouse J, Sanguin H, Bâ A, Galiana A, Bally R, Lebrun M, Prin Y.
2013. Des ressources végétales endémiques pour optimiser durablement les opérations de réhabilitation du couvert forestier en
milieu méditerranéen et tropical : exemple des plantes facilitatrices vectrices de propagation des champignons mycorhiziens
Comptes rendus biologies 336(5-6):265-272
Escaray FJ, Rosique FJC, Scambato AA, Bilenca D, Carrasco P, Matarredona AV, Ruiz OA, MenéndezAB. 2010. Evaluation of a technical
revegetation action performed on foredunes at Devesa de la Albufera, Valencia, Spain. Land Degrad. Dev 21:239-247
Estaun V, Save R, Biel C. 1997. AM inoculation as a biological tool to improve plant revegetation of a disturbed soil with
Rosmarinusofficinalis under semi-arid conditions.Applied Soil Ecology 6:223-229
Ferrol N, Calvente R, Cano C, Barea JM, Azcón-Aguilar C. 2004. Analysingarbuscular mycorrhizal fungal diversity in shrub-associated
resource islands from a desertification threatened semiarid Mediterranean ecosystem. Appl Soil Ecol 25:123-133
Frioni L, Minasian H, Volfovicz R. 1999. Arbuscular mycorrhizae and ectomycorrhizae in native tree legumes in Uruguay.For. Ecol. Manage
115:41-47
Gerdemann JW, Nicolson TH. 1963. Spores of mycorrhizalendogone species extracted form soil by wet sieving and dec anting. Trans.
Br.mycol.soc 46:235-244
Giovannetti M. 1985. Seasonal variations of vesicular-arbuscularmycorrhizae and Endogonaceous spores in a maritime sand dune. Trans.
Br. Mycol. Soc 84:485-500
Hart MM, Reader RJ, Klironomos JN. 2003. Plant coexistence mediated by arbuscular mycorrhizal fungi. Trends Ecol. Evol 18:418-423
HatimiA. 1995. Symbiotes racinaires de trois légumineuses arborescentes de dunes littorales de Souss-Massa. Ed. INRA, Paris, Les
Collogues 77:183-190
Hatimi A, Tahrouch S. 2007. Caractérisation chimique, botanique et microbiologique du sol des dunes littorales du Souss-Massa. Biomatec
Echo 2(5):85-97
Hayman DS. 1970. Endogone spores numbers in soil and vesicular-arbuscularmycorrhiza in wheat as influenced by season and soil
traitments. Trans. Br. Mycol. Soc 54(1):53-63
Jasper DA, Abbot LK, Robson AD. 1991. The effect of soil disturbance on vesicular-arbuscularmycorrhizal fungi in soils from different
vegetation types. N. Phytol 118:471-476
JeffriesP, Barea JM. 2001. Arbuscular mycorrhiza-a key component of sustainable plant–soil ecosystems inHock B (Ed.), The Mycota IX
Fungal Associations. Springer, Berlin, pp:95-113
Jensen A, Jakobsen I. 1980. The occurrence of vesicular-arbuscularmycorrhiza in barley and wheat grown in some Danish soils with
different fertilizer treatments. Plant and Soil 55:403-414
Johnson N, Zak D, Tilman D, PflegerF. 1991. Dynamics of vesicular-arbuscularmycorrhizae during old field succession. Oecologia
86(3):349-358
Klironomos JN, Hart MM. 2002. Colonisation of roots by arbuscularmycorrhizal fungi using different sources of inoculum.Mycorrhiza
12:181-184
Koske RE, Sutton JC, Sheppard BR. 1975. Ecology of Endogone in Lake Huron sand dunes. Canadian Journal of Botany 53:87-93
Koske RE, Polson WR. 1984. Are VA mycorrhizae required for sand dune stabilization? BioScience 34:420-424
Le Houerou HN. 2000. Restoration and rehabilitation of arid and semiarid Mediterranean ecosystems in North Africa and West Asia: A
review. Arid Soil Research and Rehabilitation 14:3-14
Li T, ZhaoZW. 2005. Arbuscularmycorrhizas in a hot and arid ecosystem in southwest China. Appl Soil Ecol 29:135-141
Maremmani A, Bedini S, Matoševic I, Tomei PE, Giovannetti M. 2003. Type of mycorrhizal associations in two coastal nature reserves of
the Mediterranean basin. Mycorrhiza 13:33-40

201
Intl J Agri Crop Sci. Vol., 8 (2), 194-202, 2015

Marschner P, Timonen S. 2005. Interactions between plant species and mycorrhizal colonization on the bacterial community composition in
the rhizosphere. Appl Soil Ecol 28:23–36
Mathur N, Vyas A. 2000. Influence of arbuscularmycorrhizae on biomass production, nutrient uptake and physiological changes in
Ziziphusmauritiana under water stress. J. of Arid Environ 45:191-195
Merry weather J, Fitter A. 1998. The arbuscular mycorrhizal fungi of Hyacinthoides non-scripta. II. Seasonal and spatial patterns of fungal
populations.New Phytol. 138:131-142
Morton JB, Bentivenga SP, Wheeler WW. 1993. Germ plasma in the International Collection of Arbuscular and Vesicular–
arbuscularMycorrhizal Fungi (INVAM) and procedures for culture development, documentation and storage.Mycotaxon 48:491-528
Mukerji KG, Kapoor A. 1986. Occurrence and importance of vesicular–arbuscular mycorrhizal fungi in semiarid regions of India.For. Ecol.
Manage 18:117-126
Nicolson TH. 1960. Mycorrhiza in the gramineae. II. Developpement in different habitats, particularly sand dunes. Trans. Br. Mycol. Soc,
43(1):132-145
Öpik M, Moora M, Liira J, Zobel M (2006) Composition of root-colonizing arbuscular mycorrhizal fungal communities in different
ecosystems around the globe. Journal of Ecology 94:778-790
Ouahmane L, Duponnois R, Hafidi M, Kisa M, Boumezzough A, Thioulouse J, Plenchette C.2006a. Some Mediterraneanplant species
(Lavandula spp. and Thymus satureioides) act as potential “plant nurses” for the early growth of Cupressus at lantica. Plant Ecol
185:123-124
Ouahmane L, Hafidi M, Kisa M, Boumezouch A, Thioulouse J, Duponnois R. 2006b. Lavandula species as a source of
arbuscularmycorrhizalpropagules facilitating the early development of Cupressusarizonica. Appl.Soil Ecol 34:190-199
Phillips JM, Hayman DS. 1970. Improved procedures for clearing roots and staining parasitic and vesicular-arbuscularmycorrhizal fungi for
rapid assessment of infection.Trans Br Mycol Soc 55:158-161
Plenchette C. 1989. Potentiel infectieux mycorhizogène du sol des parcelles du dispositif Dehérain. C.R. Acad. Agric. Fr 75:23-29
Plenchette C, Perrin R, Duvert P. 1989. The concept of soil infectivity and a method for its determination as applied to endomycorrhizas.
Can. J. Bot 67:112-115
Requena N, Jeffries P, Barea JM. 1996. Assessment of natural mycorrhizal potential in a desertified semiarid ecosystem. Appl. Environ.
Microbiol 62:842-847
Requena N, Perez-Solis E, Azcon-Aguilar C, Jeffries P, Barea JM. 2001. Management of indigenous Plant–Microbe Symbioses aids
restoration of desertified ecosystems.Appl. Environ. Microbiol 67:495-498
Sanguin H,Khoulissa S,Zarik L,Gryta H,Boumezzough A,Ouahmane L,Hafidi M,Ouhammou A,Prin Y,Dreyfus B,Cambecedes J,Miché
L,Gauquelin T,Duponnois R(2013) Rôles potentiels de la symbiose mycorhizienne dans la conservation des populations
méditerranéennes de Genévrier thurifère (Juniperusthurifera L.).EcologiaMediterranea. 39(1):99-107
Schubler A, Schwarzott1, Walker C. 2001. A new fungal phylum, the Glomeromycota: phylogeny and evolution. Mycol. Res. 105 (12):1413-
1421
Smith SE, Read DJ. 1997. Mycorrhizal symbiosis, 2nd Edition.Academic Press, San Diego, California, USA.
Smith SE, Read DJ. 2008. .Mycorrhizal symbiosis, 3rd edn.Clarendon Press, Oxford
Smith TF. 1980. The effect of saison and crop relation with abundance of spores of vesicular- arbuscular(VA) mycorrhizalendophytes.Plant
and soil 57:475-479
Sutton JC, Barron GL. 1972. Population dynamics of Endogone spores in soil. Can. J. Bot. 50:1909-1914
The International Culture Collection of Arbuscular and VisiculoArbuscularEndomycorrhizal Fungi (http:// www.Invam.caf.wvu.edu).
Trappe JM. 1987. Phylogenetic and ecologic aspects of mycotrophy in the angiosperms from an evolutionary standpoint. In: Safir GR (ed)
Ecophysiology of VA mycorrhizal plants. CRC, Boca Raton, FL, pp:5–26
Trouvelot A, Kough JL, Gianinazzi-Pearson V. 1986. Mesure du taux de mycorrhization d'un system radiculaire recherché de methods
d'estimation ayant une signification fonctionnelle.In: Physiological and genetical aspects of mycorrhizae. Gianinazzi-Pearson V. et
Gianinazzi S. (Eds.), INRA edition, Paris, pp:217-221
Turrini A, Avio L, Bedina S, Giovannetti M. 2008. In situ collection of endangered arbuscular mycorrhizal fungi in a Mediterranean UNESCO
Biosphere Reserve.BiodiversConserv 17:643-657
Yano-Melo AM, Saggin Jr OJ, Maia LC. 2003. Tolerance of my- corrhized banana (Musa sp. cv. Pacovan) plantlets to saline stress.
Agriculture, Ecosystems and Environment 95: 343-348

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