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Effects of arbuscular mycorrhizal fungi on Capsicum spp.

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DOI: 10.1017/S0021859615000714

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Journal of Agricultural Science (2016), 154, 828–849. © Cambridge University Press 2015
doi:10.1017/S0021859615000714

CROPS AND SOILS REVIEW

Effects of arbuscular mycorrhizal fungi on Capsicum spp.

J. A. P. PEREIRA 1 *, I. J. C. VIEIRA 2 , M. S. M. FREITAS 1 , C. L. PRINS 1 , M. A. MARTINS 1 AND

R. RODRIGUES 1
1
CCTA, Centro de Ciências e Tecnologias Agropecuárias, UENF, Campos dos Goytacazes 28013-602, RJ, Brazil
2
CCT, Centro de Ciência e Tecnologia, UENF, Campos dos Goytacazes 28013-602, RJ, Brazil

(Received 6 August 2014; revised 31 May 2015; accepted 1 July 2015;

first published online 28 July 2015)

SUMMARY
The benefits of mycorrhizal inoculation on growth, yield and nutrition of plants are well documented. However, mycor-
rhiza use in pepper and sweet pepper crops (Capsicum spp.) is still rarely exploited compared to other crops of economic
importance. The current paper reviews the main aspects of the association between arbuscular mycorrhizal (AM) fungi
and plants of pepper and sweet pepper. It includes topics about the effects of AM fungi on nutrition, growth and yield
in Capsicum spp., paying particular attention to AM fungi–pathogen interactions, responses to some environmental
stresses, as well as biochemical and physiological aspects of AM fungi–plant interaction in Capsicum annuum L.

INTRODUCTION excellent source of vitamins A and C (Miean &

Mohamed 2001), and possess medicinal properties
Pepper and sweet pepper (Capsicum spp.) have global
(Knotkova et al. 2008; Leung 2008; Oh et al. 2008;
economic importance, being grown in 116 countries
Silva et al. 2009; Wong & Gavva 2009; Costa et al.
spread over all continents. The Asian continent covers
2010; Joo et al. 2010; Thoennissen et al. 2010; Yang
0·59 of the total area under cultivation in the world,
et al. 2010; López et al. 2012).
with the main growing areas located in China (672
Like other species of plants that are able to establish a
330 ha), Indonesia (237 520 ha) and South Korea (49
symbiotic association with soil fungi, when the soil has
976 ha). Africa comes next with 0·19 of the planet’s cul-
low nutrient availability roots of Capsicum spp. typical-
tivated land (FAOSTAT 2010). The annual global pro-
ly form arbuscular mycorrhizae (Davies et al. 1992).
duction is 31·13 million t, of which China accounts for
Mycorrhiza is defined as a non-pathogenic symbiot-
0·51, followed by Mexico (0·074), Turkey (0·069) and
ic association between certain types of soil fungi and
Indonesia (0·055) (FAOSTAT 2013).
plant roots. The arbuscular mycorrhizal (AM) fungi
The Capsicum genus belongs to the Solanaceae
are of agronomic importance. They are capable of
family and comprises 36 taxa, including species and
forming mycorrhizae with >0·80 of plant species, in-
some botanical varieties, all of them native to tropical
cluding most of the cultivated species (Strack et al.
regions of the Americas (Pozzobon et al. 2006). Five
2003; Gosling et al. 2006). The AM fungi fall within
species of pepper (Capsicum annuum, Capsicum fru-
the Phylum Glomeromycota, represented by 18
tescens, Capsicum baccatum, Capsicum pubescens
genera recognized mainly by the morphological char-
and Capsicum chinense) are considered domesti-
acteristics of asexual spores. These genera include
cated, showing varied distribution throughout tropical
Redeckra, Acaulospora, Pacispora, Scutellospora,
America (Loaiza-Figueroa et al. 1989; Perry 2012).
Gigaspora, Dentiscutata, Cetraspora, Racocetra, Clar-
This genus shows great diversity in colour, size,
oideoglomus, Glomus, Funneliformis, Septoglomus,
shape, pungency and use of its fruits (Bosland 1992)
Rhizophagus, Sclerocystis, Ambispora, Geosiphon,
which impart colour, aroma and flavour to various
Archaeospora and Paraglomus, which currently com-
foods (Korel et al. 2002). In addition, the fruit is an
prise about 230 species (Schüβler et al. 2001; Peterson
* To whom all correspondence should be addressed. Email:
et al. 2004; Redecker et al. 2013). Intensive field re-
jappwar@hotmail.com search carried out in the Colombian Amazon
 Effects of AM fungi on Capsicum spp. 829

(Cardona et al. 2008), Shandong Province, China acquisition of mineral elements from the soil. This as-
(Chen et al. 2012) and West of Rajasthan, India sociation basically happens in two phases: extra-
(Vyas & Vyas 2012) showed a high diversity of AM radical, in which hyphal contact with the root cortex
fungi in rhizosphere of Capsicum spp. Glomus oc- of the host plant occurs; and intra-radical, with the de-
curred most frequently among the genera, followed velopment of intra-radical hyphae and specialized
by Acaulospora, Gigaspora and Scutellospora. structures called arbuscules (finely branched hyphae
Mycorrhizal relationships formed by AM fungi benefit involved in nutrient exchange) (Peterson et al. 2004;
their hosts by increasing the absorption of soil mineral Smith & Read 2008; Giovannetti et al. 2010). Extra-
nutrients, particularly phosphorus (P) as well as nitrogen radical mycelia continue to extend into the soil
(N), potassium (K) and micronutrients (Linderman 1992; which encourages further exploration, transferring
Perner et al. 2007). In addition to these benefits, AM water and minerals back to the plant roots (Franken
fungi improve plant–water relations, increase resistance 2010).
or tolerance to biotic and abiotic stresses and improve In the mycorrhizal association, the fungus enhances
soil structure (Smith & Read 2008). the acquisition of soil mineral nutrients, particularly
The first to establish the benefits of AM fungi in plants P and N, as well as K, sulphur (S), magnesium (Mg),
of the genus Capsicum were Hirrel & Gerdemann copper (Cu), zinc (Zn) and iron (Fe) by the host
(1980), who observed that bell pepper plants inoculated plant, which in turn provides products from carbon
with AM fungi could be more tolerant to salt stress metabolism to the fungus (Linderman 1992; Caris
than non-inoculated plants. Two years later, Bagyaraj et al. 1998; Allen & Shachar-Hill 2009).
& Sreeramulu (1982) confirmed the benefits of pre- The effects of AM fungi on the absorption of P have
inoculation with AM fungi on height, dry weight and been studied extensively and supported by several
yield of hot peppers transplanted into the field. researchers. Possible explanations for the success of
In recent years, there has been a growing interest in AM fungi on the acquisition and subsequent phos-
the associations between AM fungi and Capsicum phate nutrition improvement in their hosts are well
spp. related to P and water absorption (Estrada-Luna described by Smith & Read (2008). The AM hyphae
& Davies 2003; Sharif & Claassen 2011), growth, absorb P from soil solution and transfer it to the roots
yield, nutritional status (Boonlue et al. 2012; Franco at a speed higher than the diffusion of this element
et al. 2013), physiology (Estrada-Luna et al. 2000; by the soil. Hyphae are able to transpose the P deple-
Demir 2004) and tolerance to biotic (Ozgonen & tion regions that form around the roots. In addition, the
Erkilic 2007; Goicoechea et al. 2010; Oyetunji & smaller hyphal diameter allows greater exploration of
Salami 2011) and abiotic stresses (Mena-Violante the soil volume (Smith & Read 2008).
et al. 2006; Elahi et al. 2012; Beltrano et al. 2013). Several experiments have demonstrated the absorp-
In view of this interest, a bibliographical search on tion, transport and transfer of P and N in various plant–
the relationship between AM fungi and Capsicum AM fungi relations under different environmental
spp. resulted in 60 published works involving 33 conditions (Hattingh et al. 1973; Ames et al. 1983;
taxa of Capsicum, including crops and botanical var- George et al. 1992; Smith et al. 2000; Wang et al.
ieties and the effects of mycorrhizal associations on 2002). Other studies have also confirmed the absorp-
these species (Table 1). Thus, the current review sum- tion of Zn (Bürkert & Robson 1994; Jansa et al. 2003),
marizes the effects of AM fungi on nutrition, growth S (Rhodes & Gerdemann 1978; Allen & Shachar-Hill
and yield in Capsicum spp., paying particular atten- 2009) and Fe (Caris et al. 1998) via AM fungi. In add-
tion to AM fungi–pathogen interactions, in response ition, an increase in the absorption of Cu by mycor-
to some environmental stresses, as well as biochem- rhized plants has often been observed (Li et al.
ical and physiological aspects of AM fungi–plant inter- 1991; Lee & George 2005).
actions in C. annuum L. In Capsicum, arbuscular mycorrhizae represent an
alternative way to obtain improvements in growth
and development. The main benefits of mycorrhizal
EFFECTS OF ARBUSCULAR MYCORRHIZAL
inoculation in pepper and sweet pepper plants
F U NG I O N N U T R I T I O N , G R O W T H AN D
include improvement in seedling growth (Davies &
Y I E L D I N C AP S I CU M SP P.
Linderman 1991); economy in phosphate fertilization
The symbiotic association of roots with AM fungi is a (Bagyaraj & Sreeramulu 1982); increased seedling sur-
widespread strategy by which plants facilitate the vival and development (Estrada-Luna et al. 2000;
 830
Table 1. Effects of arbuscular mycorrhizal fungi (AM fungi) and plant growth-promoting microorganisms (PGPMs) on Capsicum spp.

Host species AM fungi/PGPMs Effect Reference

J. A. P. Pereira et al.
Capsicum annuum L. cvar Glomus fasciculatus, local isolate I4a, local Enhancement of growth, development, yield Bagyaraj & Sreeramulu 1982; Sarwade et al.
Jwala isolate I6, local isolate I14; G. fasciculatum, and improvement in P and Zn content; 2011
Trichoderma virideb, Trichoderma harzianumb Enhancement of growth and biomass
C. annuum L. cvar Byadagi G. fasciculatuma, Glomus albidum, Glomus Enhancement of growth, development, yield Sreeramulu & Bagyaraj 1986; Sreenivasa
macrocarpum, local isolate I14; G. fascicula- and improvement in P and Zn content; 1992; Sreenivasa et al. 1993
tum, Gigaspora margarita, Acaulospora laevis, Enhancement of growth and biomass,
Sclerocystis dussii, G. macrocarpuma; G. fas- yield; improvement in P, Zn, Cu, Mn and
ciculatum, G. macrocarpuma Fe levels
C. annuum L. Mixed (Acaulospora bireticulate, Acaulospora Enhancement of growth, biomass and im- Mun et al. 1990; Kim et al. 2002; Martin &
spinosa, Gigaspora decipiens, Glomus deser- provement in P level; Enhancement of Stutz 2004; Sensoy et al. 2007; Faisal et al.
ticola, Scutellospora percisa); Glomus intrara- growth, biomass and improvement in N 2010; Kim et al. 2010; Marihal et al. 2011;
dices; G. intraradicesa, Glomus ‘AZ 112’; G. and P levels; Enhancement of biomass and Sharif & Claassen 2011; Tallapragada et al.
intraradices, G. margarita; G. macrocarpum; improvement in P levels; Enhancement of 2011
Mixed (Acaulospora longula, Glomus clarum, biomass; Enhancement of biomass, yield
G. intraradices), Methylobacterium oryzaeb; and improvement in P level; Enhancement
Commercial product containing three species of growth, biomass and improvement in N,
of Glomus; Glomus mosseae; G. intraradicesa, P, K, Zn, Fe and Cu levels; Enhancement of
Azotobacter spp.b yield; Enhancement of growth and im-
provement in P level; Enhancement of
growth and biomass
C. annuum L. cvar Early G. deserticola Enhancement of growth, development, and Davies & Linderman 1991; Davies et al.
Bountiful nutrition; Resistance to water stress 1992, 1993
C. annuum L. cvar San Luis G. intraradices; G. fasciculatuma, Mixed (G. Enhancement of growth, development e gas Aguilera-Gómez et al. 1999; Davies et al.
albidum, Glomus claroides, Glomus dipha- exchange; Enhancement of growth, de- 2000, 2002; Estrada-Luna et al. 2000;
num); Not reported; G. fasciculatum, Mixeda velopment and in Fe, Mn, Zn and Cu Estrada-Luna & Davies 2003; Mena-
(G. albidum, G. claroides, G. diphanum); levels; Enhancement of growth, nutrition Violante et al. 2006
Mixed (G. albidum, G. claroides, and physiology; Resistance to water stress;
G. diphanum); G. fasciculatum, Mixed Enhancement of growth, nutrition, physi-
(Glomus constrictum, Glomus geosporum, ology and resistance to water stress;
G. fasciculatum, Glomus tortuosum), Mixeda Resistance to water stress
(Glomus aggregatum, G. deserticola,
G. geosporum, Glomus microaggregatum,
Sclerocystis coremioides)
C. annuum L. cvar Pant-C-1 Mixed (Glomus spp., Gigaspora spp., Enhancement of biomass, yield and P level Gaur et al. 1998
Scutellospora spp.), G. intraradicesa
C. annuum L. cvar Camelot G. intraradices, Mixeda (G. mosseae, Glomus Enhancement of yield Douds & Reider 2003
etunicatum, Glomus rosea)
C. annuum L. cvar Ancho, Mixeda (G. albidum, G. claroides, Glomus dia- Enhancement of growth, biomass and yield García 2003
C. annuum L. cvar Mirasol phanum), G. etunicatum, G. intraradicesa
C. annuum L. cvar Mixed (G. mosseae, G. fasciculatum, Enhancement of growth, biomass and yield Regvar et al. 2003
Californian miracle G. etunicatum, G. intraradices, Scutellospora
sp.)
C. annuum L. cvar Cetinel- G. intraradices Enhancement of growth, physiology and in P Demir 2004
150 level
C. annuum L. cvar Jupiter Mixed (G. aggregatum, G. intraradices, Without any specific improvement Russo 2006; Russo & Perkins-Veazie 2010
G. mosseae)
Capsicum chinense Jacquin Commercial product containing strains of AM Enhancement of growth and nutrition Constantino et al. 2008
fungi, Azospirillum brasilienseb, Azobacter
chroococcumb
C. annuum L. cvar Cacho de Glomus claroideuma, Mixed (native AM fungi); Enhancement of growth, biomass and in P, Castillo et al. 2009a, b
Cabra G. intraradices, G. claroideuma Ca, Mg, K, Na, Fe, Mn, Cu and Zn con-
tents; Enhancement of yield and fruit
quality
C. annuum L. cvar Mirasol, Mixed (G. intraradices, A. brasilienseb) Enhancement of growth, biomass and yield González et al. 2010
C. annuum L. cvar Puya
C. annuum L. cvar Demre G. mosseae, G. clarum, Glomus caledonium, Enhancement of biomass and in P and Zn Ortas et al. 2011
Sivrisi G. intraradices, G. etunicatum content
C. annuum L. cvar Guajillo Mixed (Rhizophagus intraradices, G. albidum, Enhancement of yield and in N, P and Ca L.G.L. Santoyo, personal communication

Effects of AM fungi on Capsicum spp.

Claroideoglomus claroideum, Rhizophagus content 2011
diaphanus, A. laevis, Glomus sp.,
Funneliformis geosporum, Glomus sinuosum)
Capsicum frutescens L. Acaulospora denticulata, Gigaspora albida, Enhancement of biomass and in P and N Dai et al. 2011; Elahi et al. 2012
G. geosporum, Scutellospora coralloideaa, levels; Tolerance to As-induced toxicity
Scutellospora scutata; Mixed (native AM fungi)
C. frutescens L. cvar Hua Acaulospora foveata, Acaulospora appendicula, Enhancement of growth, biomass and yield Boonlue et al. 2012
Rua A. denticulata, Glomus dimorphicum, Glomus and in P, N and K levels
tenerum, G. claruma, Glomus globiferum
Hibrid cvar Valeria R. intraradices Enhancement of fruit quality and in N, P, Fe Franco et al. 2013
and Zn levels
C. annuum L. var. California G. mosseae, A. laevis, Pseudomonas Enhancement of growth, development and Tanwar et al. 2013
Wonder fluorescensb yield, and in N and P levels
C. annuum L. cvar G. fasciculatusa, G. margarita Tolerance to salt stress Hirrel & Gerdemann 1980
California Wonder

831
C. annuum L. cvar Demre G. intraradicesa, G. margarita Tolerance to salt stress Türkmen et al. 2005, 2008
 832
J. A. P. Pereira et al.
Table 1. (Cont.)

Host species AM fungi/PGPMs Effect Reference

C. annuum L. cvar 11B 14 G. clarum Tolerance to salt stress Kaya et al. 2009
C. annuum L. var. aviculare G. intraradices Tolerance to salt stress Rueda-Puente et al. 2010
C. annuum L. cvar PKM1 G. intraradices Tolerance to salt stress Selvakumar & Thamizhiniyan 2011
C. annuum L. cvar G. mosseae, G. intraradicesa Tolerance to salt stress Çekiç et al. 2012
Cumaovasi
C. annuum L. cvar Piquillo G. mosseae, G. intraradices, G. deserticolaa; G. Reduction of deleterious effects of Garmendia et al. 2004a, b, 2004c, 2006
deserticola; G. deserticola; G. deserticola Verticillium dahliae
C. annuum L. cvar G. mosseaea, G. etunicatum, G. fasciculatum, Reduction of deleterious effects of Ozgonen & Erkilic 2007; Ozgonen et al.
Charliston Bagci G. margarita Phytophthora capsici 2009
C. annuum L. cvar Ancho G. fasciculatum Reduction of deleterious effects of P. capsici Alejo-Iturvide et al. 2008
C. annuum L. cvar Kandil G. intraradices Reduction of deleterious effects of P. capsici Cimen et al. 2009
C. annuum L. cvar NHU-2C G. mosseae Reduction of deleterious effects of Fusarium Oyetunji & Salami 2011
oxysporum
C. annuum L. cvar G. mosseae Reduction in copper-induced oxidative Latef 2011
Zhongjiao 105 stress
C. annuum L. cvar G. mosseae, G. intraradicesa; G. intraradices Tolerance to Cr-induced toxicity; Tolerance Ruscitti et al. 2011; Beltrano et al. 2013
California Wonder 300 to salt stress
a
Mycorrhizal inoculum with best response.
b
Plant growth-promoting microorganisms used in co-inoculation with AM fungi.
 Effects of AM fungi on Capsicum spp. 833

Estrada-Luna & Davies 2003); increased resistance or accelerates plant development, so mycorrhized
tolerance to pathogens (Garmendia et al. 2004a; plants display early maturation. Phosphate transport
Alejo-Iturvide et al. 2008); increased resistance or tol- to the roots via mycorrhizal hyphae can be a thousand
erance to abiotic stresses (Mena-Violante et al. 2006; times faster than by diffusion in soil (Bieleski 1973)
Kaya et al. 2009; Ruscitti et al. 2011); early flowering and contributes up to 0·75 of total P absorbed by the
and fruiting (Castillo et al. 2009a; Ortas et al. 2011) plant (Kothari et al. 1990). Sensoy et al. (2007)
and increased fruit yield and quality (Castillo et al. reported greater dry mass of root and shoot area in
2009b; Franco et al. 2013). C. annuum L., however AM fungi did not significantly
Several studies have reported the effects of AM fungi increase P levels due to adequate levels of P in the
on development and nutritional status of peppers. growing medium. Also, Douds & Reider (2003)
Most of the results have shown significant improve- reported an improvement of 34% in fruit yield, even
ments in yield, growth and nutrition of plants grown in soils with high levels of P.
conventionally and organically. Davies et al. (2000) reported that the improvement
in growth and development of plants under P stress
conditions (using two different P levels: 11 and
Improved pepper plant nutrition
22 µg P/ml) can be attributed to increased absorption
Seedlings pre-inoculated with AM fungi under field of Fe, Mn, Zn and Cu. The plants had, respectively, an
conditions presented a significant increase in growth increase of 30, 33, 33 and 25% of these elements.
(39%), flowering (46%), yield (39%) and contents of These elements play key roles in the photosynthetic
P (62%) and Zn (65%) (Bagyaraj & Sreeramulu process; therefore high levels of these elements in
1982; Sreeramulu & Bagyaraj 1986). Regvar et al. plant tissue can promote a greater photosynthetic
(2003) reported improved pepper plant nutrition and rate with consequent improvement in plant growth
yield of fruit under both field cultivation and in green- and development (Marschner 2012). In relation to
house experiments. Under greenhouse conditions an micronutrient levels, mycorrhized sweet pepper
increase in plant height (19%), plant biomass (38%) plants (C. annuum L. cvar Early Bountiful) showed
and fruit yield per plant (82%) was reported. Under an increase of boron (B) in foliar tissue, but a decrease
field cultivation, increases of 9, 47 and 78% in plant of molybdenum (Mo), Cu and Zn contents with
height, plant biomass and fruit yield per plant, respect- increased P fertilization (Davies & Linderman 1991).
ively, were recorded. Inoculated bell pepper plants The potential cause is due to reduced AM coloniza-
were found to be more developed and taller compared tion, which can directly affect Zn absorption (Ryan
to non-inoculated plants (Mun et al. 1990): the authors et al. 2008).
found, after 7 weeks, an increase in the shoot area Bagyaraj & Sreeramulu (1982) concluded that it is
from 9 cm in control plants to 19 cm in the most ef- possible to reduce the application of phosphate fertili-
fective mycorrhizal treatment which, according to zers by 50% through inoculation with an efficient
them, was due to an increase of P in the vegetable strain of AM fungus, as they found an increase of
tissue. 39% in fruit yield using half the recommended P
Sreenivasa (1992) observed that pepper plants level for the crop. Due to the fact that the availability
inoculated with AM fungi had an increase of 73% in of P is one of the main limiting factors for plant growth
their dry biomass as well as in the mass (64%) of the and yield, AM fungi present great potential as a bio-
green fruits from the cultivar Byadagi. In addition, logical input to agriculture, contributing significantly
mycorrhizal inoculation increased absorption of P, to a reduction in phosphate fertilizers not only in
Zn, Cu, Mn and Fe. Similar results for both growth Capsicum cultivation, but also in other crops of eco-
and nutrient uptake were obtained by Sreenivasa nomic importance.
et al. (1993) using half of the recommended dose of
superphosphate for the crop: according to the
Improved pepper fruit yield and quality
authors, the increased levels of nutrients in inoculated
plants led to improved growth and yield of the crop. In general, inoculation with AM fungi promotes an in-
Increased levels of P and Zn in shoot biomass were crease in yield of chilli (C. annuum L.) grown under
also observed by Ortas et al. (2011). In addition, plants field conditions (Marihal et al. 2011). An increase in
flowered 16 days earlier when compared to the micronutrient absorption was reported by Castillo
control treatment. In fact, mycorrhizal inoculation et al. (2009a), finding that plants presented a
834 J. A. P. Pereira et al.

significant increase in levels of Mn (59%), Cu (98%) of shoots (87%) and roots (77%), number of flowers
and Zn (87%): they found that mycorrhizal inocula- per plant (100%), number of fruits per plant (100%)
tion was positive for chilli pepper crops (cvar Cacho and uptake of N (66%), P (68%) and K (68%) com-
de Cabra), obtaining better-developed plants with pared with non-inoculated plants.
improvements in fruit quality, especially related to
fresh mass which had an increase of 55%. The yield
No arbuscular mycorrhizal fungi effect
of fruits of C. annuum L. and two of its cultivars
(Ancho and Mirasol) was positively affected by AM The positive effects of AM fungi on the production of
fungi in experiments performed by Faisal et al. sweet peppers have been observed in different
(2010) and García (2003), respectively. These studies, although some AM fungal species such as
authors reported significant increases in the number Glomus aggregatum, G. intraradices and G. mosseae
of fruits, c. 47 and 46%, respectively. Franco et al. have provided little effect on growth, yield and nutrition
(2013) reported increased levels of N, P, Fe and Zn of plants whether grown conventionally or organically
in shoot area and improvement in fruit quality: accord- (Russo 2006; Russo & Perkins-Veazie 2010). L.G.L.
ing to these authors, the impact of mycorrhizal inocu- Santoyo, personal communication 2011 reported sig-
lation on fruit quality may be closely related to better nificant effects on the number of leaves, branches,
nutritional condition of the plant caused by AM fruits, dry mass of fruits, and contents of N, P and Ca.
fungus. However, significant effects of mycorrhizal inoculation
Sharif & Claassen (2011) observed that in low P on height, dry mass of shoot and levels of K, Mg and Zn
supply the association with AM fungus increased the in the cultivar Guajillo were not found compared to
production of C. annuum L. significantly and this non-inoculated plants. Therefore, the hypothesis sus-
was related to an increased absorption of P. In add- tained by L.G.L. Santoyo, personal communication
ition, their results showed that hyphae are more effi- 2011 that AM fungi improves nutritional status,
cient in absorbing P than the root surface in soils growth and yield of cvar Guajillo can only be partly
with low levels of P. accepted, since the inoculation increased only a few
variables.

Arbuscular mycorrhizal fungi effect in organic

agricultural systems ENVIRONMENTAL FACTORS THAT
I N FL U E N C E M Y C OR R H I Z A L
Although there is little information about the benefi-
C O L ON I ZAT I O N
cial role of mycorrhizal association in pepper
species grown in soils subjected to organic manure, Most plants are capable of forming AM symbiosis, al-
favourable results have been shown in some studies. though in many cases adverse growing conditions
Gaur et al. (1998) showed that mycorrhizal inocula- may prevent the establishment of this association. In
tion increased the fresh mass of fruits from 17 g in fact, the soil system provides a constantly changing
control plants to 37 g in the most effective mycorrhizal environment for moisture, pH, temperature and nutri-
treatment. In turn, Dai et al. (2011) reported a signifi- ent availability.
cant increase in root (20%) and shoot (14%) dry mass, Arbuscular mycorrhiza formation, function and
as well as in N (12%) and P (12%) levels in the shoot. extent are clearly influenced by nutrient availability
These responses increased significantly due to the (particularly P) in soil, as reported in several studies.
amendment of soil with organic manure. Maximum Faisal et al. (2010) reported an increase in P content
root infection was seen at 100% of the recommended of plant shoots, which increased with increases in
dose of organic manure application in soil. Indeed, the levels of inoculum. According to Smith & Read
organic manure improves vegetable biomass (Ibrahim (2008) inoculum density can correlate positively
et al. 2008) and can enhance mycorrhizal infectivity with the percentage of mycorrhizal colonization of
in soil and extra-radical hyphal proliferation (St. John roots, resulting in increased acquisition of P by the my-
et al. 1983; Joner & Jakobsen 1995). In addition, celial network. It is worth noting, however, that high
Boonlue et al. (2012) observed that mycorrhizal inocu- concentrations (non-stress conditions) of P can
lation in organic systems increased growth parameters, inhibit root colonization, whereas low P concentra-
including shoot height (41%), stem diameter (39%), tions (stress conditions) favour intra-radical coloniza-
fresh mass of shoots (85%) and roots (77%), dry mass tion (Kiriachek et al. 2009). This seems to be a
 Effects of AM fungi on Capsicum spp. 835

general phenomenon, although the regulatory Among PGPMs, plant growth-promoting rhizobac-
mechanisms of this process have not been completely teria (PGPR) along with AM fungi have been recog-
elucidated (Smith & Read 2008). The P uptake is dir- nized for their potential use in agriculture (Azcón
ectly related to plant growth and when it reaches ad- 2000; Lucy et al. 2004). Some studies (Table 1) state
equate concentration levels in the soil, i.e., the plant that co-inoculation with PGPR and AM fungi can
is not under nutritional stress conditions, AM colon- produce positive synergistic effects on growth and nu-
ization is inhibited by autoregulatory mechanisms of trition of C. chinense Jacquin and C. annuum L. in
symbiosis, making AM fungi unnecessary and incom- greenhouse and field conditions (Constantino et al.
patible with non-stress conditions (Javot et al. 2007). 2008; Tallapragada et al. 2011). Favourable results
Another important factor that may influence the for the application of AM fungus and Azospirillum bra-
extent of mycorrhizal colonization is temperature. siliense in pepper crops (C. annuum L.) were demon-
Martin & Stutz (2004) observed that at moderate tem- strated by González et al. (2010). Significant
peratures (20·7–25·4 °C) mycorrhized pepper plants differences were observed in growth, vigour, number
showed improvements in shoot dry mass and concen- of fruits, fruit colour, root and shoot dry mass. On the
trations of P. These effects were reduced at elevated tem- other hand, co-inoculation with Methylobacterium
perature (32·1–38 °C). Warm soil conditions, therefore, strains and AM fungi increased the levels of N, P, K,
surely alter AM fungal activity. Root colonization by AM Zn and Fe in the roots and shoots, and Cu in the
fungi often decreases when the temperature exceeds 30 shoot, as well as growth parameters, including length
°C (Bowen 1987), and soil temperatures >40 °C are gen- and biomass of plants, and chlorophyll levels in red
erally lethal to AM fungi (Bendavid-Val el al. 1997). In peppers (Kim et al. 2010). The increase in plant
turn, Kim et al. (2002) observed that inoculum storage growth parameters and nutrient uptake has been attrib-
at low temperatures (4 °C) increased colonization of uted to the stimulatory effect of beneficial bacteria on
roots and as a result increased the growth and absorp- multiplication, spore germination and establishment
tion of N and P in hot pepper plants (C. annuum L.) as of AM fungi. In general, mycorrhizal inoculation
compared with freshly prepared soil inoculum. It is increased the proportion of mycorrhizal root coloniza-
likely that dormancy is broken by low temperature, pro- tion as well as spore numbers in the root zone soil
moting high activity of spores and propagules. compared to non-inoculated plants. The increase in
However, the effects of temperature on the rate and chlorophyll content is an important response to
extent of colonization is complex and may vary with mycorrhizal association and has been reported in
both the fungus and the plant (Smith & Read 2008). other studies involving pepper and sweet pepper
plants (Estrada-Luna et al. 2000; Kim et al. 2002;
Estrada-Luna & Davies 2003; García 2003; Demir
SYNERGISTIC EFFECTS OF CO-
2004; Kaya et al. 2009; Latef 2011; Selvakumar &
I N O C U L A T I O N WI T H P L A N T G R O W T H -
Thamizhiniyan 2011; Çekiç et al. 2012; Elahi et al.
PROMOTING MICROORGANISMS AND AM
2012; Beltrano et al. 2013; Franco et al. 2013). The in-
F U NG I O N G RO WT H AN D NU T R IT I O N O F
crease of chlorophyll content in inoculated plants can
CA PSIC UM S P P .
be attributed to good uptake of N reported in these
Certain microorganisms can stimulate root growth studies. In addition, the increase in chlorophyll con-
considerably and are often referred to as plant tents, especially chlorophyll a, is directly related to
growth-promoting microorganisms (PGPMs). These the plant’s photosynthetic efficiency, and subsequent-
microorganisms influence root growth primarily by ly to its development.
improving nutrient availability, producing phytohor- Tanwar et al. (2013) also documented that the pres-
mones and inhibiting pathogens (Lugtenberg et al. ence of PGPR (Pseudomonas fluorescens) in mycor-
1991; Dutta & Podile 2010). Many of these are diazo- rhizal inoculum can synergistically increase growth
trophic bacteria (e.g., Azospirillum, Azobacter or (64%), photosynthetic rate (75%), yield (100%) and
Pseudomonas spp.) and improve the absorption of N levels of N (37%) and P (52%) as well as leading to
(Rodrigues et al. 2008), while others increase the early flowering (28 days) in bell pepper (C. annuum
availability of P by their solubilization (Wahid & L. var. California Wonder). In addition, the inoculation
Mehana 2000). In addition, PGPMs can stimulate of AM fungi along with P. fluorescens achieved
root colonization by AM fungi, thereby increasing nu- maximum root colonization (increase of 88%). These
trient absorption by the plant (Dwivedi et al. 2009). results suggest that selected PGPR and AM fungi
836 J. A. P. Pereira et al.

could be co-inoculated to optimize the formation and stress was the development of extra-radical hyphae
functioning of the AM symbiosis. that favoured a better exploration of the soil, keeping
Although strains of Trichoderma are biological soil–root contact and consequently, root–water lin-
control agents, acting against pathogenic fungi, they kages in the soil.
can colonize plant roots to stimulate growth (Benítez The selection of AM fungi able to improve the
et al. 2004). Effects on the increase in growth para- hydric condition of peppers (cvar San Luis) is an im-
meters due to synergistic interactions between AM portant factor for the success of this crop under
fungus and Trichoderma spp. in chilli (C. annuum water-limiting conditions: Davies et al. 2002 claim
L. cvar Jwala) were reported by Sarwade et al. that AM fungi can be potentially incorporated into
(2011): their study showed that co-inoculation with pepper seedling transplantation systems, with the
AM fungus and Trichoderma spp. increased number aim of improving the absorption of P and promoting
of leaves (58%), stem diameter (22%), shoot length resistance to water stress. The positive effects of AM
(39%), number of branches (80%), fresh mass of symbiosis on San Luis crops were demonstrated
shoots (69%) and roots (83%), root length (30%), dry clearly by Mena-Violante et al. (2006), who found
mass of shoots (86%) and roots (90%) and AM fungi improvements in growth, development and quality
root colonization (40%) as compared to AM fungi- of the fruit of peppers grown under water stress. In
inoculated plants. addition, their study showed that AM fungi inocula-
tion can mitigate the adverse effects of water stress, re-
storing fruit quality parameters at levels similar to
ARBUSCULAR MYCORRHIZAL INFLUENCE
those of non-stress-treated plants.
O N C A P S I C U M AN N U U M L . : RE S P O N S E T O
Soil salinity is a limiting factor in growth, yield and
W A T E R AN D S A L T S T R E S S
quality for most non-halophytic plants (Rozema &
An emerging factor capable of impacting pepper and Flowers 2008). High levels of salt in the soil can
sweet pepper crops and agriculture in general, is the have negative effects on emergence and establish-
salinity of the soil and water (Niu 2012). There is no ment of seedlings (Niu et al. 2010), roots and shoots
doubt that AM colonization assists with the water (Niu & Cabrera 2010), membrane permeability,
balance of plants (Augé 2001). Some of the mechan- water exchange activity, ionic balance, photosyn-
isms that may be involved in the increased resistance thesis and stomatal conductance (Shannon & Grieve
of mycorrhized plants to water stress include the 1998; Navarro et al. 2003; Cabañero et al. 2004;
greater absorption of water promoted by extra- Munns & Tester 2008). However, biological strategies
radical hyphae (Hardie 1985); regulation of stomatal such as AM symbiosis have been used successfully in
conductance by hormonal signals (Allen et al. 1982); horticulture to relieve the deleterious effects of salt on
increase in hydraulic conductivity of the roots (Safir various crops, such as cucumber and zucchini
et al. 1972) or by lowered leaf osmotic potential for (Rosendahl & Rosendahl 1991; Colla et al. 2008).
greater turgor (Augé et al. 1986). Many researchers report that AM fungi could
As with other aspects of mycorrhized plant physi- improve plants’ ability to manage salt stress (Ruiz-
ology, it is relevant to distinguish direct effects of Lozano et al. 1996; Jahromi et al. 2008) by improving
fungal colonization from indirect effects resulting nutrient absorption (Cantrell & Linderman 2001),
from changes in the size of the plant or phosphate sup- maintaining ionic balance (Giri et al. 2007), protecting
plementation (Smith & Read 2008). According to Fitter enzyme activity and facilitating water absorption
(1988), AM fungi influence on plant–water relations (Colla et al. 2008). However, the mechanisms by
can be a secondary consequence of phosphate nutri- which AM fungi influence the metabolism of host
tion, although such effects are inconsistent. Davies plant under salt stress are not clear (Kaya et al. 2009;
et al. (1992, 1993) found that the resistance of bell Çekiç et al. 2012).
pepper plants (c. 7 weeks old) subjected to water Studies have classified pepper as moderately sensi-
stress conditions was not associated with the nutrition- tive to salt stress (Maas & Hoffman 1977; Pasternak &
al condition and size of the plant. Mycorrhized plants Malach 1994), although some cultivars such as Sonar
resisted stress and kept relatively high levels of water and Lamuyo can present tolerance to this kind of stress
potential, turgor potential, relative water content, tran- (Chartzoulakis & Klapaki 2000).
spiration flux and net photosynthetic flux. The pos- The advantages of mycorrhizal inoculation in bell
sible mechanism related to this resistance to water pepper crops in saline soils were first reported by
 Effects of AM fungi on Capsicum spp. 837

Hirrel & Gerdemann (1980). Other studies have Chavez et al. 2002), mainly linked to metal tolerance
shown that AM fungi inoculation can positively mechanisms in fungi (Gaur & Adholeya 2004). Elahi
affect growth parameters of peppers, such as shoot et al. (2012) demonstrated that mycorrhizal inocula-
height, root length and diameter of the stem as well tion not only mitigated the toxicity in soil amended
as nutrient acquisition of plants grown under moder- with 10 ppm arsenic (As) solution, but also increased
ate salinity (Türkmen et al. 2008). It has been noted growth and nutrient uptake in chilli (C. frutescens L.).
that the humic acid application triggered and Other studies report that AM fungi isolated from As-
increased the positive effects of AM fungi inoculation, contaminated soil were able to confer greater resist-
promoting much more growth in bell pepper plants ance to arsenate in velvet grass, suppressing As
grown under salt stress and increased root and shoot uptake (Gonzalez-Chavez et al. 2002). On the other
nutrient levels (Türkmen et al. 2005). In addition, hand, Latef (2011) observed that AM fungus was
Beltrano et al. (2013) observed that AM fungi positive- able to maintain an effective symbiosis with pepper
ly affected growth of bell pepper plants, improving dry plants (C. annuum L. cvar Zhongjiao 105) in
mass of root, shoot and leaf area, at all the experimen- Cu-contaminated soils, improving plant growth
tal levels of salinity (0, 50, 100 and 200 mM NaCl). under these conditions. Latef (2011) suggested that
The enhancement of nutritional status apparently this is probably due to the reduction of Cu-induced
plays a role in mitigation of salt stress in pepper oxidative stress and reduced accumulation of this
plants due to improvement in dry mass of shoot, metal in plant tissues. Copper immobilization by
which provide a ‘dilution effect’ of the sodium (Na) extra-radical hyphae can contribute to prevention of
(Kaya et al. 2009). In addition, Al-Karaki (2006) Cu transfer to plant tissues, so that the AM fungus
noted a high retention of Na in the roots, without acts as a biological barrier. This is supported by
transportation to the shoot in inoculated plants, sug- studies that report the high capacity of the mycorrhizal
gesting that Na could be retained in intra-radical mycelium to bind with metals (Joner et al. 2000; Toler
hyphae or compartmentalized in vacuoles of root et al. 2005). Because of the lower sensitivity of fungal
cells. Other authors propose that AM fungi exclude hyphae to metals compared with plant roots (Leyval &
Na by discrimination during their absorption from Joner 2001), a functional symbiosis with metal-
the soil or transfer to plants (Hammer et al. 2011). tolerant strains of AM fungi can provide plants
Therefore, although mycorrhizal inoculation has dis- with a survival strategy to cope with metal stress
crete effects on reducing the content of Na in the while still maintaining an adequate supply of nutrients
plant, it seems sufficient to restore the growth such as P and N, through hyphal active absorption
process at approximate levels to those of plants not (Gaur & Adholeya 2004), thus contributing to
under stress (Kaya et al. 2009). the improvement of plant performance in metal-
In studies involving pepper plants (var. aviculare) contaminated soils.
under salt stress, AM fungi positively influenced ger-
mination, plant height, root length and biomass pro-
INTERACTIONS BETWEEN ARBUSCULAR
duction (Rueda-Puente et al. 2010). In addition,
M Y C O R R H I Z A L F U N G I AN D P A T H O G E N I C
plants of the cultivar PKM1 showed better growth
F U N GI IN C A P S I C U M AN N U U M L .
when mycorrhized due to increased P content in
plant tissue (Selvakumar & Thamizhiniyan 2011). Arbuscular mycorrhizal symbiosis imparts notable
However, it is important to note that the improvement changes in host plant physiology, which have an
of growth and consequent salinity tolerance of mycor- impact on the plant response to biotic stresses (Pozo
rhized plants seems to be independent of the concen- et al. 2010). In fact, some mechanisms may be
tration of P in the growth medium (Ruiz-Lozano et al. involved in bio-protection by AM fungi against soil
1996; Feng et al. 2002). pathogens. In this sense, the improvement of plant nu-
tritional condition could be highlighted, especially
P (Azcón-Aguilar et al. 2002). However, tolerance or
METAL STRESS TOLERANCE IN
resistance to pathogen attack cannot be regarded as
M Y C O R R H I Z E D P L A N T S O F C AP S IC UM S P P .
a mere consequence of phosphate nutrition improve-
Several studies have shown that AM fungi play a role ment (Trotta et al. 1996; Fritz et al. 2006; Liu et al.
in plant protection against deleterious effects of exces- 2007). Other mechanisms may be involved in plant
sive amounts of metal (Dueck et al. 1986; Gonzalez- defence during AM symbiosis such as, for example,
838 J. A. P. Pereira et al.

differential regulation of chitinases and β-1,3-glucanase disease were observed in control plots without solar-
isoforms as a result of hormone changes and/or ization and without AM fungi. Solarization decreases
synthesis of specific elicitor/suppressor molecules crown rot disease caused by P. capsici (Yücel 1995)
(Lambais 2000). In addition, the efficiency of response through thermal inactivation, which is the most
to biotic stresses depends on the involved AM fungus, serious disease affecting pepper cultivation in
as well as on the substrate and host plant (Azcón- Turkey. However, the destruction of beneficial organ-
Aguilar & Barea 1996; Linderman 2000). isms such as AM fungus may also occur, thereby redu-
Some studies have demonstrated the effectiveness cing the positive effects of solarization (Schreiner et al.
of AM fungi as a bio-protectant in C. annuum 2001). Earlier studies suggested that eradication or re-
L. Garmendia et al. (2004a) showed that mycorrhizal duction of the mycorrhizal population in soil by solar-
inoculation has been effective in reducing disease se- ization could be recovered by artificial inoculation of
verity caused by Verticillium dahliae in pepper (cvar AM fungi, so could induce better root growth (Afek
Piquillo). The plants associated with AM fungi exhib- et al. 1991) and result in an increment in yield of
ited greater yield than non-inoculated ones despite pepper (Ortas et al. 2003). Together, the application
the lower P fertilization applied to the mycorrhizal of solarization and AM fungi in plots infested with
treatment. The maintenance of specific P uptake rate P. capsici increased plant yield by c. 43% compared
could have contributed towards diminishing the dele- with plots without the treatment in the presence of
terious effect of V. dahliae on yield in plants associated the pathogen (Cimen et al. 2009).
with AM fungus. Also, Garmendia et al. (2004b) Oyetunji & Salami (2011) showed that the inci-
observed that the effectiveness of AM fungi as a bio- dence of Fusarium wilt caused by Fusarium oxy-
protector against Verticillium wilt was influenced by sporum f. sp. lycopersici was visibly reduced in bell
the phenology of the plant at the time of pathogen pepper plants (cvar NHU-2C) inoculated with AM
attack. The highest efficacy of AM interaction oc- fungus. All the plants survived and achieved better de-
curred when V. dahliae was inoculated during the velopment compared to those of other treatments. On
vegetative stage of plants (Garmendia et al. 2004b). a microscopic level, mycorrhizal inoculation pro-
In addition, P content in leaves of plants associated motes an increase in cell-wall thickness of root cells,
with AM fungi were lower than those found in non- thus forming a barrier to pathogen attack. This contrib-
inoculated plants, reinforcing the hypothesis that the uted to the reduction in disease severity in mycor-
mechanism involved in mycorrhized plant response rhized plants (Oyetunji & Salami 2011).
to pathogenic fungus is independent of phosphate nu- Peroxidase (POX) production, which plays an im-
trition (Garmendia et al. 2004c). portant role in forming secondary cell walls and in
The reduction in disease severity caused by their suberization, can contribute to a greater resist-
Phytophthora capsici in pepper (cvar Charliston ance to subsequent invaders. Mycorrhizal inoculation
Bagci) was reported by Ozgonen & Erkilic (2007). influence on the levels of this enzyme in C. annuum
All AM fungi tested increased shoot height by 23·4– L. was demonstrated in various studies as can be
31·7% and fresh and dry weights of shoots and roots seen in the following topic.
of plants were enhanced by AM symbiosis compared
to non-inoculated plants in pot experiments. Under
greenhouse conditions AM fungi increased yield by A RBUSCULAR MY CORR HI ZA L I NFLUENCE
22%. Also, AM association reduced disease severity O N C A P S I C U M A N N U UM L . :
by 91·7, 43 and 57·2% under pot, greenhouse and PH YSI O LOGI CA L A ND BI OCH E MIC AL
field conditions, respectively. Mycorrhizal inoculation A S P E CTS
not only inhibited Phytophthora wilt caused by
Physiological and biochemical plant responses to salt
P. capsici, but also increased yield of pepper plants
and water stresses
(cvar Kandil) grown in the field (Cimen et al. 2009).
The highest yields were obtained in plots that received In plant tissue, reactive oxygen species (ROS) such as
a ‘solarization + AM fungi’ treatment (solarization is a hydrogen peroxide (H2O2), superoxide (O− 2 ) or hy-
non-chemical method for controlling soil-borne pests droxyl radicals (OH−) are continuously formed in the
using high temperatures produced using solar energy), cytosol, chloroplasts and mitochondria by a range of
in which the lowest incidence of the disease was regis- metabolic processes. Reactive oxygen species not
tered. Lower yields and the highest incidence of only play a key role in translating signals, but can
 Effects of AM fungi on Capsicum spp. 839

also cause damage to cells, for example by peroxida- water and metal-induced oxidative stress, has been
tion of membranes, protein degradation and DNA mu- documented in many plants (Kishor et al. 2005). The
tation. Plants therefore ‘kidnap’ excessive amounts of role of AM symbiosis in proline metabolism has
ROS by enzymes such as superoxide dismutase been investigated in several studies involving plants
(SOD), catalase (CAT) and glutathione peroxidase under different stress conditions, although contradic-
(GPx) (McCord 2000). However, both biotic and tory results have been obtained (Ruiz-Lozano et al.
abiotic stresses can produce changes in free radical 1995, 1996; Goicoechea et al. 1998). Some studies
kidnapper enzymes (Mittler 2002). have shown a reduction in proline levels in mycor-
Salt and water stresses can cause a rapid increase in rhized pepper (cvar 11B14) and chilli plants (cvar
free radical concentration in plant cells (Moran et al. PKM1) under salt stress (Kaya et al. 2009;
1994; Fadzilla et al. 1997; Mittler 2002), which Selvakumar & Thamizhiniyan 2011). Conversely,
seems to be due to a limitation of carbon dioxide re- Beltrano et al. (2013) demonstrate proline accumula-
duction by the Calvin cycle during the period of tion in pepper plants (cvar California Wonder 300)
osmotic stress. Also, deficiency or high amounts of grown in the presence or absence of AM fungus and
mineral elements in plant tissue can induce oxidative at all levels of salt stress: they observed that under
stress in plants (Marschner 2012). Reactive oxygen low supply of P and at all salinity levels, leaves of
species and free radicals bind to sulph–hydryl mycorrhized plants accumulated more proline when
groups of membrane proteins or increase their lipid compared with non-inoculated plants, while roots of
peroxidation. In this way, Liu et al. (2004) showed mycorrhized plants accumulated more proline only
that Cu excess can cause damage to cell membranes. at high levels of salt stress. Similarly, Ruscitti et al.
In order to overcome the harmful effects of free radi- (2011) showed that in plant roots of cvar California
cals, plants exposed to high levels of Cu show an in- Wonder 300 inoculated with AM fungi, proline con-
crease in antioxidant responses (Gratão et al. 2008) centration decreased with increasing concentration
which result from the activity of enzymes such as of chromium (Cr), while it increased in leaves.
SOD, CAT, ascorbate peroxidase (APx) and glutathi- Mycorrhizal inoculation has been suggested as a
one reductase (GR) (Schützendübel & Polle 2002). method for increasing plant resistance to water
Some studies have shown that root colonization of stress (Augé 2001). Among these, the maintenance
C. annuum L. can relieve the damage caused by oxi- of physiological parameters of plants subjected to
dative stress in plants under different environmental drought has been highlighted by several works on
conditions. Latef (2011) reported that pepper plants C. annuum L. Davies et al. (2002) observed that a
(cvar Zhongjiao 105) exposed to high levels of Cu small number of mycorrhized pepper plants (cvar
demonstrated reduced oxidative stress and lipid per- San Luis) with visible wilting during a water stress
oxidation when colonized by AM fungus. The results peak correlated with higher water potential of the
showed an increase in the enzyme activity of SOD, leaves of these plants; however, they found that P
CAT, APx and GR, which can be a manifestation of content in plant tissue was not a contributing factor
the beginning of antioxidant defence (Márquez- to the resistance to water stress. Some authors
García & Córdoba 2010). The percentage increase suggest that the resistance of pepper plants (cvar
in SOD, CAT, APx and GT, due to mycorrhizal inocu- Early Bountiful) subjected to drought is explained by
lation, was 20, 50, 16 and 29%, compared with non- the extensive network of extra-radical hyphae that
inoculated plants. Similarly, Çekiç et al. (2012) found favour a greater extraction of water in soils with low
an increase in the activity of SOD, CAT and APx in water potential, maintaining physiological parameters
mycorrhized plants under salt stress, although an im- in the plant (Davies et al. 1992, 1993). The beneficial
provement in GR activity was not observed. Çekiç effects of AM symbiosis on plant physiology, especial-
et al. (2012) also reported lower lipid peroxidation, ly related to better water use, were observed in pepper
evidenced by low content of malondialdehyde in plants (cvar Piquillo) submitted to biotic stress
inoculated plants. (Garmendia et al. 2004c).
Plants under stress conditions change their metabol- Davies et al. (1993) demonstrated that mycorrhized
ism in response to environmental adversities. The bell pepper plants (cvar Early Bountiful) are able to
accumulation of proline, an α-amino acid, due to regulate their stomata more rapidly and demonstrate
increased synthesis and decreased degradation higher photosynthetic rates compared to non-
under a variety of stress conditions, such as salt, inoculated plants during the period of adaptation to
840 J. A. P. Pereira et al.

water stress. As a consequence, improvements in Evidence suggests that the induction/suppression of

growth and development, as well as increases in nutri- plant defence mechanisms in the early stages of AM
ent absorption capacity were observed. Similar results colonization plays a key role in the establishment of
were obtained by Estrada-Luna et al. (2000) and mycorrhizal association (García-Garrido & Ocampo
Estrada-Luna & Davies (2003), who found that mycor- 2002; Yuan et al. 2007). In the host, the differential ex-
rhizal inoculation of pepper plants (cvar San Luis) pro- pression of several genes involved in plant defence
moted better responses to water deficit during the against pathogen attack, which is evaluated based
cycles of water restriction, as well as increased physio- on enzymatic activities, accumulation of protein
logical performance and growth after the adaptation of and/or RNA messengers, has been observed during
plants to water stress conditions. The results showed the development of AM fungi and may play a key
lower levels of abscisic acid (ABA) in the roots and role in controlling intra-radical colonization
stems of mycorrhized plants. This corresponded with (Lambais 2000).
high transpiration, stomatal conductance, and relative Reactive oxygen species accumulation, activation
water content, indicating that plants were not under of phenylpropanoid metabolism and the accumula-
water stress. In addition, the improvement in plant tion of specific isoforms of hydrolytic enzymes such
growth can be partly attributed to the increase of the as chitinases and glucanases, have been reported
levels of N, P and K and their influence on net in colonized roots of tomato (García-Garrido &
photosynthesis. Ocampo 2002; Pozo et al. 2002). Ozgonen et al.
(2009) demonstrated that mycorrhizal inoculation of
pepper plants (cvar Charliston Bagci) infected by
Physiological and biochemical responses to disease
P. capsici induced a significant increase in activity of
Garmendia et al. (2004c) observed that although β-1,3-glucanase and chitinase compared with non-
mycorrhized plants developed symptoms of the inoculated plants. In all treatments, the β-1,3-glucanase
disease caused by V. dahliae, they exhibited more and chitinase activities were maximum 6 days after in-
balanced activities of the enzymes SOD, CAT and oculation, decreasing at the initial and final assess-
guaiacol peroxidase during the first month after patho- ments 3 and 9 days after inoculation, respectively.
gen inoculation. This could contribute towards The levels of both, β-1,3-glucanase and chitinase
slowing the development of disease symptoms and enzymes in control plants ranged from 0 to 3 µ kat/mg
maintain controlled photosynthetic rates for longer of protein. The level of β-1,3-glucanase enzyme was
(Garmendia et al. 2004b) in mycorrhized plants. higher in P. capsici infected plants (19 µ kat/mg of
Alejo-Iturvide et al. (2008) noted that mycorrhizal in- protein) and those with combined inoculation of AM
oculation seems to have a positive influence on resist- fungi and P. capsici treatments (19–25 µ kat/mg of
ance of chilli plants (cvar Ancho), as necrotic lesions protein), as compared to that at the single mycorrhizal
caused by P. capsici were reduced by 25% compared treatments (10–16 µ kat/mg of protein) 6 days after in-
with non-inoculated infected plants. Although both oculation. Similarly, chitinase activity was higher in
treatments showed increased activity of SOD and P. capsici infected plants (11 µ kat/mg of protein) and
POX, this was best regulated by mycorrhized plants, those with combined inoculation of AM fungi and
since the changes in their activities were less varied P. capsici treatments (9–14 µ kat/mg of protein), as
compared to the variations found in non-inoculated compared to that at the single mycorrhizal treatments
plants. In addition, non-inoculated plants showed (5–7 µ kat/mg of protein) 6 days after inoculation.
greater accumulation of H2O2 than those treated Ozgonen et al. (2009) also found an increase in the
with AM fungus. According to Alejo-Iturvide et al. amount of phenolic compounds, which were highest
(2008), this observation suggests the existence of a in plants with combined inoculation of AM fungi and
local and systemic signalling process in plants colo- P. capsici treatments. Some of these compounds were
nized by AM fungus, possibly preceded by H2O2 ac- identified as: caffeic acid, trans-coumaryl, capsaicin
tivity transfer to adjacent cells and also through (CAP), p-aminobenzaldehyde, aspartic acid, chloro-
distant sites. Pozo et al. (2002) demonstrated that genic acid, glutamic acid, linoleic acid, cis-feruloyl
mycorrhizal inoculation of tomato plants induced a acid, stearic acid, capsicoside and F1 compound.
local and systemic resistance to Phytophthora parasi- Phytoalexin production during the early stages of
tica and was effective in reducing the symptoms pro- colonization could provide pepper plants (cvar
duced by this pathogen. Charliston Bagci) with a defence against P. capsici.
 Effects of AM fungi on Capsicum spp. 841

Ozgonen & Erkilic (2007) noted that infected plants reservoir causing basi-petal mobilization of photo-
inoculated with AM fungi showed improvement in synthates to roots, thus providing a stimulus for higher
capsidiol content, which may have had an influence photosynthetic activity (Bieleski 1973). Tanwar et al.
on plant response against the pathogen. (2013) demonstrated that in low doses of P, co-
Garmendia et al. (2006) also reported that pepper inoculation with PGPB and AM fungi increased the
root colonization (cvar Piquillo) by AM fungi levels of chlorophyll a and b in bell pepper var.
induced the appearance of new isoforms of acid chit- California Wonder, resulting in an increase in photo-
inases, SOD and at early stages, POXs. In addition, in- synthetic rate, and suggest that this may be due to
fection with V. dahliae slightly increased the activity of absorption of more nutrients and an increased gas ex-
both phenylalanine ammonia-lyase and POX only in change by improvement of stomatal conductance.
mycorrhized roots. These observations suggest a role
of AM fungi in biochemical-protection of plants
Physiology and biochemistry: hormonal responses to
against Verticillium wilt in pepper.
arbuscular mycorrhizal fungi colonization
Garmendia et al. (2004b) showed that the associ-
ation with AM fungi reduced the deleterious effects Arbuscular mycorrhizal fungi play a role in hormonal
on plant hydric condition caused by Verticillium balance during the adaptation of plants to adverse
wilt. The results showed that AM inoculation main- conditions, which can regulate its performance.
tained leaf water content for longer and delayed de- Several studies have demonstrated the role of AM
velopment of disease symptoms such as decreased fungi in phytohormone level changes during symbi-
photosynthesis in plants inoculated with the patho- osis, including cytokinins, gibberellins, ethylene,
gen. According to Garmendia et al. (2004b), these ABA, salicylic acid and jasmonates (Hause et al.
benefits to the physiology of the plant promoted 2007). In Capsicum sp., the AM fungi effect on the de-
improvements in its yield. velopment of pepper plants showed a positive correl-
ation with the concentration of different growth
regulators during phenological stages of the plant
Physiological and biochemical response to arbuscular
(García 2003). According to García (2003), the con-
mycorrhizal fungi in terms of improved plant health
centrations of indoleacetic acid (IAA) and gibberellic
Phosphorus plays an important role in the energy me- acid (AG3) in the shoot were higher in AM fungi colo-
tabolism of cells during photosynthesis (Marschner nized plants compared with non-inoculated ones.
2012). Studies show that AM fungi can facilitate an Also, adenine concentration (6-aminopurine) in roots
increased P absorption in pepper plants and partially showed higher values. There was also an increase of
reduce the effects of low P supply in the soil, 10% in the total chlorophyll content and 20% in the
thereby improving photosynthetic rate, stomatal con- total protein levels, which may have a direct effect
ductance and gas exchange of plants (Aguilera- on production and quality of fruit, as well as levels
Gómez et al. 1999). Mycorrhizal inoculation has of plant growth promoters. Improvements in cytokinin
also been shown to positively affect the levels of car- and gibberellin levels have been demonstrated in
otenoids in some cases (Tallapragada et al. 2011; plants inoculated with AM fungi (Allen et al. 1980,
Çekiç et al. 2012). 1982). Increases in such hormones, particularly cyto-
Aguilera-Gómez et al. (1999) showed that mycor- kinins, could elevate photosynthetic rates by stomatal
rhizal association not only relieved P-stress, but also opening, influencing the transport of ions and regulat-
increased reproductive growth of pepper plants (cvar ing the levels of chlorophyll (Allen et al. 1980, 1982).
San Luis) grown in greater availability of P (44 g P/m3) Goicoechea et al. (1997) showed that there is a posi-
by 450%. Additionally, photosynthetic rate and P tive correlation between cytokinin increase and the
levels in plant tissue were higher in mycorrhized rate of gas exchange, stomatal conductance and tran-
plants cultivated on high levels of P. Demir (2004) spiration. Moreover, evidence suggests that ABA could
found that the concentration of P was positively corre- also play a role in plant stomatal control (Zhang et al.
lated to the levels of chlorophyll (a, b and a + b) and 1987), which reinforces the results found by Estrada-
sugars (fructose, α-glucose and β-glucose) and that Luna et al. (2000) and Estrada-Luna & Davies (2003).
this had positively affected the physiological perform- Therefore, maintaining hormone levels in mycorrhized
ance in pepper plants (cvar Cetinel-150). Arbuscular plant contributes to improved photosynthesis, promot-
mycorrhizal fungi may function as a metabolic ing plant development and yield.
842 J. A. P. Pereira et al.

Physiological and biochemical response of fruit to mechanisms that control this process are still being elu-
arbuscular mycorrhizal fungi colonization cidated by several researchers. As this mutual relation-
ship is compatible with almost 0·90 of vascular plant
The effect of AM symbiosis on the quality attributes of
species, and considering the function of this symbiosis
fruits of Capsicum spp. has not been widely reported.
on plant development, nutrient cycle, carbon storage,
Castillo et al. (2009a, b) showed a slight increase in as-
disease and stress resistance and the reduced use of fer-
corbic acid concentration in fruits of colonized plants;
tilizers, AM fungi could be an important alternative to
however, no significant differences were found for
current agricultural practices that strive to be sustain-
total titratable acidity (% of citric acid) and total
able. Therefore, the potential of this symbiosis with
soluble solids (°Brix). Under drought conditions,
Capsicum spp. is of inestimable value.
Mena-Violante et al. (2006) found that the inoculation
Large-scale application of AM fungi in crops of eco-
of pepper plants (cvar San Luis) promoted significant
nomic importance, such as pepper and sweet pepper,
improvements in various fruit quality parameters,
is still a challenge due to the obligatory nature of the
such as pigment concentration. Chlorophyll content
symbiosis, which requires the presence of a host for
in fruit of mycorrhized plants under water stress
production.
were similar to those found in non-inoculated plants
Thus, AM fungi are important components of agri-
that were not subjected to drought. In addition, the
cultural production and, if managed properly, can
levels of carotenes and xanthophylls in the fruit were
substantially contribute to the sustainability of agricul-
1·4 times higher in AM inoculated plants subjected
tural systems. In addition, the development of techni-
to drought compared to that in non-inoculated
ques that aim to understand the mechanisms that
plants not exposed to drought. This could be attributed
control AM formation may contribute towards the ef-
to a mycorrhizal inoculation effect on the process of
fective large-scale application of AM fungi in
fruit maturation (Castillo et al. 2009a) and changes
agriculture.
in the concentration of photosynthetic pigments
during symbiosis (Demir 2004).
The authors are grateful to Fundação de Amparo à
Pungency is an important quality attribute in
Pesquisa do Estado do Rio de Janeiro (FAPERJ) for
peppers, and its expression is associated with the pres-
grants and a research fellowship, to Conselho
ence, in a greater or lesser proportion, of alkaloids
Nacional de Desenvolvimento Científico e
known as capsaicinoids (Appendino 2008). Among
Tecnológico (CNPq) and Coordenação de
these, CAP and its dihydro derivative (dihydrocapsai-
Aperfeiçoamento de Pessoal de Ensino Superior
cin (DHC)) constitute >0·80 of the total capsaicinoids
(CAPES) for research fellowships.
in most of the pungent varieties (Kosuge & Furuta
1970). The levels of CAP are usually higher than
DHC (Antonious et al. 2009) and these are considered
the main parameter to determine the commercial
quality of a product or derivatives (Frary & Frary R E FE R E NC E S
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