Improved pepper plant nutrition

Seedlings pre-inoculated with AM fungi under field conditions presented a significant increase in growth (39%), flowering (46%), yield (39%) and contents of P (62%) and Zn (65%) (Bagyaraj & Sreeramulu Reference Bagyaraj and Sreeramulu1982; Sreeramulu & Bagyaraj Reference Sreeramulu and Bagyaraj1986). Regvar et al. (Reference Regvar, Vogel-Mikuš and Ševerkar2003) reported improved pepper plant nutrition and yield of fruit under both field cultivation and in greenhouse experiments. Under greenhouse conditions an increase in plant height (19%), plant biomass (38%) and fruit yield per plant (82%) was reported. Under field cultivation, increases of 9, 47 and 78% in plant height, plant biomass and fruit yield per plant, respectively, were recorded. Inoculated bell pepper plants were found to be more developed and taller compared to non-inoculated plants (Mun et al. Reference Mun, Kim and Choe1990): the authors found, after 7 weeks, an increase in the shoot area from 9 cm in control plants to 19 cm in the most effective mycorrhizal treatment which, according to them, was due to an increase of P in the vegetable tissue.

Sreenivasa (Reference Sreenivasa1992) observed that pepper plants inoculated with AM fungi had an increase of 73% in their dry biomass as well as in the mass (64%) of the green fruits from the cultivar Byadagi. In addition, mycorrhizal inoculation increased absorption of P, Zn, Cu, Mn and Fe. Similar results for both growth and nutrient uptake were obtained by Sreenivasa et al. (Reference Sreenivasa, Krishnaraj, Gangadhara and Manjunathaiah1993) using half of the recommended dose of superphosphate for the crop: according to the authors, the increased levels of nutrients in inoculated plants led to improved growth and yield of the crop.

Increased levels of P and Zn in shoot biomass were also observed by Ortas et al. (Reference Ortas, Sari, Akpinar and Yetisir2011). In addition, plants flowered 16 days earlier when compared to the control treatment. In fact, mycorrhizal inoculation accelerates plant development, so mycorrhized plants display early maturation. Phosphate transport to the roots via mycorrhizal hyphae can be a thousand times faster than by diffusion in soil (Bieleski Reference Bieleski1973) and contributes up to 0·75 of total P absorbed by the plant (Kothari et al. Reference Kothari, Marschner and George1990). Sensoy et al. (Reference Sensoy, Demir, Türkmen, Erdinc and Savur2007) reported greater dry mass of root and shoot area in C. annuum L., however AM fungi did not significantly increase P levels due to adequate levels of P in the growing medium. Also, Douds & Reider (Reference Douds and Reider2003) reported an improvement of 34% in fruit yield, even in soils with high levels of P.

Davies et al. (Reference Davies, Olalde-Portugal, Alvarado, Escamilla, Ferrera-Cerrato and Espinosa2000) reported that the improvement in growth and development of plants under P stress conditions (using two different P levels: 11 and 22 µg P/ml) can be attributed to increased absorption of Fe, Mn, Zn and Cu. The plants had, respectively, an increase of 30, 33, 33 and 25% of these elements. These elements play key roles in the photosynthetic process; therefore high levels of these elements in plant tissue can promote a greater photosynthetic rate with consequent improvement in plant growth and development (Marschner Reference Marschner2012). In relation to micronutrient levels, mycorrhized sweet pepper plants (C. annuum L. cvar Early Bountiful) showed an increase of boron (B) in foliar tissue, but a decrease of molybdenum (Mo), Cu and Zn contents with increased P fertilization (Davies & Linderman Reference Davies and Linderman1991). The potential cause is due to reduced AM colonization, which can directly affect Zn absorption (Ryan et al. Reference Ryan, McInerney, Record and Angus2008).

Bagyaraj & Sreeramulu (Reference Bagyaraj and Sreeramulu1982) concluded that it is possible to reduce the application of phosphate fertilizers by 50% through inoculation with an efficient strain of AM fungus, as they found an increase of 39% in fruit yield using half the recommended P level for the crop. Due to the fact that the availability of P is one of the main limiting factors for plant growth and yield, AM fungi present great potential as a biological input to agriculture, contributing significantly to a reduction in phosphate fertilizers not only in Capsicum cultivation, but also in other crops of economic importance.

Improved pepper fruit yield and quality

In general, inoculation with AM fungi promotes an increase in yield of chilli (C. annuum L.) grown under field conditions (Marihal et al. Reference Marihal, Pradeep and Jagadeesh2011). An increase in micronutrient absorption was reported by Castillo et al. (Reference Castillo, Ortiz, Borie and Rubio2009a ), finding that plants presented a significant increase in levels of Mn (59%), Cu (98%) and Zn (87%): they found that mycorrhizal inoculation was positive for chilli pepper crops (cvar Cacho de Cabra), obtaining better-developed plants with improvements in fruit quality, especially related to fresh mass which had an increase of 55%. The yield of fruits of C. annuum L. and two of its cultivars (Ancho and Mirasol) was positively affected by AM fungi in experiments performed by Faisal et al. (Reference Faisal, Ahmad and Srivastava2010) and García (Reference García2003), respectively. These authors reported significant increases in the number of fruits, c. 47 and 46%, respectively. Franco et al. (Reference Franco, Carrillo, Chairez and Cabrera2013) reported increased levels of N, P, Fe and Zn in shoot area and improvement in fruit quality: according to these authors, the impact of mycorrhizal inoculation on fruit quality may be closely related to better nutritional condition of the plant caused by AM fungus.

Sharif & Claassen (Reference Sharif and Claassen2011) observed that in low P supply the association with AM fungus increased the production of C. annuum L. significantly and this was related to an increased absorption of P. In addition, their results showed that hyphae are more efficient in absorbing P than the root surface in soils with low levels of P.

Arbuscular mycorrhizal fungi effect in organic agricultural systems

Although there is little information about the beneficial role of mycorrhizal association in pepper species grown in soils subjected to organic manure, favourable results have been shown in some studies. Gaur et al. (Reference Gaur, Adholeya and Mukerji1998) showed that mycorrhizal inoculation increased the fresh mass of fruits from 17 g in control plants to 37 g in the most effective mycorrhizal treatment. In turn, Dai et al. (Reference Dai, Singh and Nimasow2011) reported a significant increase in root (20%) and shoot (14%) dry mass, as well as in N (12%) and P (12%) levels in the shoot. These responses increased significantly due to the amendment of soil with organic manure. Maximum root infection was seen at 100% of the recommended dose of organic manure application in soil. Indeed, organic manure improves vegetable biomass (Ibrahim et al. Reference Ibrahim, Hassan, Iqbal and Valeem2008) and can enhance mycorrhizal infectivity in soil and extra-radical hyphal proliferation (St. John et al. Reference St John, Coleman and Reid1983; Joner & Jakobsen Reference Joner and Jakobsen1995). In addition, Boonlue et al. (Reference Boonlue, Surapat, Pukahuta, Suwanarit, Suwanarit and Morinaga2012) observed that mycorrhizal inoculation in organic systems increased growth parameters, including shoot height (41%), stem diameter (39%), fresh mass of shoots (85%) and roots (77%), dry mass of shoots (87%) and roots (77%), number of flowers per plant (100%), number of fruits per plant (100%) and uptake of N (66%), P (68%) and K (68%) compared with non-inoculated plants.

No arbuscular mycorrhizal fungi effect

The positive effects of AM fungi on the production of sweet peppers have been observed in different studies, although some AM fungal species such as Glomus aggregatum, G. intraradices and G. mosseae have provided little effect on growth, yield and nutrition of plants whether grown conventionally or organically (Russo Reference Russo2006; Russo & Perkins-Veazie Reference Russo and Perkins-Veazie2010). L.G.L. Santoyo, personal communication 2011 reported significant effects on the number of leaves, branches, fruits, dry mass of fruits, and contents of N, P and Ca. However, significant effects of mycorrhizal inoculation on height, dry mass of shoot and levels of K, Mg and Zn in the cultivar Guajillo were not found compared to non-inoculated plants. Therefore, the hypothesis sustained by L.G.L. Santoyo, personal communication 2011 that AM fungi improves nutritional status, growth and yield of cvar Guajillo can only be partly accepted, since the inoculation increased only a few variables.

Physiological and biochemical plant responses to salt and water stresses

In plant tissue, reactive oxygen species (ROS) such as hydrogen peroxide (H₂O₂), superoxide (O₂ ⁻) or hydroxyl radicals (OH⁻) are continuously formed in the cytosol, chloroplasts and mitochondria by a range of metabolic processes. Reactive oxygen species not only play a key role in translating signals, but can also cause damage to cells, for example by peroxidation of membranes, protein degradation and DNA mutation. Plants therefore ‘kidnap’ excessive amounts of ROS by enzymes such as superoxide dismutase (SOD), catalase (CAT) and glutathione peroxidase (GPx) (McCord Reference McCord2000). However, both biotic and abiotic stresses can produce changes in free radical kidnapper enzymes (Mittler Reference Mittler2002).

Salt and water stresses can cause a rapid increase in free radical concentration in plant cells (Moran et al. Reference Moran, Becana, Iturbe-Ormaetxe, Frechilla, Klucas and Aparicio-Tejo1994; Fadzilla et al. Reference Fadzilla, Finch and Burdon1997; Mittler Reference Mittler2002), which seems to be due to a limitation of carbon dioxide reduction by the Calvin cycle during the period of osmotic stress. Also, deficiency or high amounts of mineral elements in plant tissue can induce oxidative stress in plants (Marschner Reference Marschner2012). Reactive oxygen species and free radicals bind to sulph–hydryl groups of membrane proteins or increase their lipid peroxidation. In this way, Liu et al. (Reference Liu, Xiong, Li and Huang2004) showed that Cu excess can cause damage to cell membranes. In order to overcome the harmful effects of free radicals, plants exposed to high levels of Cu show an increase in antioxidant responses (Gratão et al. Reference Gratão, Monteiro, Antunes, Peres and Azevedo2008) which result from the activity of enzymes such as SOD, CAT, ascorbate peroxidase (APx) and glutathione reductase (GR) (Schützendübel & Polle Reference Schützendübel and Polle2002).

Some studies have shown that root colonization of C. annuum L. can relieve the damage caused by oxidative stress in plants under different environmental conditions. Latef (Reference Latef2011) reported that pepper plants (cvar Zhongjiao 105) exposed to high levels of Cu demonstrated reduced oxidative stress and lipid peroxidation when colonized by AM fungus. The results showed an increase in the enzyme activity of SOD, CAT, APx and GR, which can be a manifestation of the beginning of antioxidant defence (Márquez-García & Córdoba Reference Márquez-García and Córdoba2010). The percentage increase in SOD, CAT, APx and GT, due to mycorrhizal inoculation, was 20, 50, 16 and 29%, compared with non-inoculated plants. Similarly, Çekiç et al. (Reference Çekiç, Unyayar and Ortas2012) found an increase in the activity of SOD, CAT and APx in mycorrhized plants under salt stress, although an improvement in GR activity was not observed. Çekiç et al. (Reference Çekiç, Unyayar and Ortas2012) also reported lower lipid peroxidation, evidenced by low content of malondialdehyde in inoculated plants.

Plants under stress conditions change their metabolism in response to environmental adversities. The accumulation of proline, an α-amino acid, due to increased synthesis and decreased degradation under a variety of stress conditions, such as salt, water and metal-induced oxidative stress, has been documented in many plants (Kishor et al. Reference Kishor, Sangam, Amrutha, Laxmi, Naidu, Rao, Rao, Reddy, Theriappan and Sreenivasulu2005). The role of AM symbiosis in proline metabolism has been investigated in several studies involving plants under different stress conditions, although contradictory results have been obtained (Ruiz-Lozano et al. Reference Ruiz-Lozano, Azcón and Gómez1995, Reference Ruiz-Lozano, Azcon and Gomez1996; Goicoechea et al. Reference Goicoechea, Szalai, Antolín, Sánchez-Díaz and Paldi1998). Some studies have shown a reduction in proline levels in mycorrhized pepper (cvar 11B14) and chilli plants (cvar PKM₁) under salt stress (Kaya et al. Reference Kaya, Ashraf, Sonmez, Aydemir, Tuna and Cullu2009; Selvakumar & Thamizhiniyan Reference Selvakumar and Thamizhiniyan2011). Conversely, Beltrano et al. (Reference Beltrano, Ruscitti, Arango and Ronco2013) demonstrate proline accumulation in pepper plants (cvar California Wonder 300) grown in the presence or absence of AM fungus and at all levels of salt stress: they observed that under low supply of P and at all salinity levels, leaves of mycorrhized plants accumulated more proline when compared with non-inoculated plants, while roots of mycorrhized plants accumulated more proline only at high levels of salt stress. Similarly, Ruscitti et al. (Reference Ruscitti, Arango, Ronco and Beltrano2011) showed that in plant roots of cvar California Wonder 300 inoculated with AM fungi, proline concentration decreased with increasing concentration of chromium (Cr), while it increased in leaves.

Mycorrhizal inoculation has been suggested as a method for increasing plant resistance to water stress (Augé Reference Augé2001). Among these, the maintenance of physiological parameters of plants subjected to drought has been highlighted by several works on C. annuum L. Davies et al. (Reference Davies, Olalde-Portugal, Aguilera-Gómez, Alvarado, Ferrera-Cerrato and Boutton2002) observed that a small number of mycorrhized pepper plants (cvar San Luis) with visible wilting during a water stress peak correlated with higher water potential of the leaves of these plants; however, they found that P content in plant tissue was not a contributing factor to the resistance to water stress. Some authors suggest that the resistance of pepper plants (cvar Early Bountiful) subjected to drought is explained by the extensive network of extra-radical hyphae that favour a greater extraction of water in soils with low water potential, maintaining physiological parameters in the plant (Davies et al. Reference Davies, Potter and Linderman1992, Reference Davies, Potter and Linderman1993). The beneficial effects of AM symbiosis on plant physiology, especially related to better water use, were observed in pepper plants (cvar Piquillo) submitted to biotic stress (Garmendia et al. Reference Garmendia, Goicoechea and Aguirreolea2004c ).

Davies et al. (Reference Davies, Potter and Linderman1993) demonstrated that mycorrhized bell pepper plants (cvar Early Bountiful) are able to regulate their stomata more rapidly and demonstrate higher photosynthetic rates compared to non-inoculated plants during the period of adaptation to water stress. As a consequence, improvements in growth and development, as well as increases in nutrient absorption capacity were observed. Similar results were obtained by Estrada-Luna et al. (Reference Estrada-Luna, Davies and Egilla2000) and Estrada-Luna & Davies (Reference Estrada-Luna and Davies2003), who found that mycorrhizal inoculation of pepper plants (cvar San Luis) promoted better responses to water deficit during the cycles of water restriction, as well as increased physiological performance and growth after the adaptation of plants to water stress conditions. The results showed lower levels of abscisic acid (ABA) in the roots and stems of mycorrhized plants. This corresponded with high transpiration, stomatal conductance, and relative water content, indicating that plants were not under water stress. In addition, the improvement in plant growth can be partly attributed to the increase of the levels of N, P and K and their influence on net photosynthesis.

Physiological and biochemical responses to disease

Garmendia et al. (Reference Garmendia, Goicoechea and Aguirreolea2004c ) observed that although mycorrhized plants developed symptoms of the disease caused by V. dahliae, they exhibited more balanced activities of the enzymes SOD, CAT and guaiacol peroxidase during the first month after pathogen inoculation. This could contribute towards slowing the development of disease symptoms and maintain controlled photosynthetic rates for longer (Garmendia et al. Reference Garmendia, Goicoechea and Aguirreolea2004b ) in mycorrhized plants. Alejo-Iturvide et al. (Reference Alejo-Iturvide, Márquez-Lucio, Morales-Ramírez, Vázquez-Garcidueñas and Olalde-Portugal2008) noted that mycorrhizal inoculation seems to have a positive influence on resistance of chilli plants (cvar Ancho), as necrotic lesions caused by P. capsici were reduced by 25% compared with non-inoculated infected plants. Although both treatments showed increased activity of SOD and POX, this was best regulated by mycorrhized plants, since the changes in their activities were less varied compared to the variations found in non-inoculated plants. In addition, non-inoculated plants showed greater accumulation of H₂O₂ than those treated with AM fungus. According to Alejo-Iturvide et al. (Reference Alejo-Iturvide, Márquez-Lucio, Morales-Ramírez, Vázquez-Garcidueñas and Olalde-Portugal2008), this observation suggests the existence of a local and systemic signalling process in plants colonized by AM fungus, possibly preceded by H₂O₂ activity transfer to adjacent cells and also through distant sites. Pozo et al. (Reference Pozo, Cordier, Dumas-Gaudot, Gianinazzi, Barea and Azcón-Aguilar2002) demonstrated that mycorrhizal inoculation of tomato plants induced a local and systemic resistance to Phytophthora parasitica and was effective in reducing the symptoms produced by this pathogen.

Evidence suggests that the induction/suppression of plant defence mechanisms in the early stages of AM colonization plays a key role in the establishment of mycorrhizal association (García-Garrido & Ocampo Reference García-Garrido and Ocampo2002; Yuan et al. Reference Yuan, Dai and Chen2007). In the host, the differential expression of several genes involved in plant defence against pathogen attack, which is evaluated based on enzymatic activities, accumulation of protein and/or RNA messengers, has been observed during the development of AM fungi and may play a key role in controlling intra-radical colonization (Lambais Reference Lambais, Podila and Douds2000).

Reactive oxygen species accumulation, activation of phenylpropanoid metabolism and the accumulation of specific isoforms of hydrolytic enzymes such as chitinases and glucanases, have been reported in colonized roots of tomato (García-Garrido & Ocampo Reference García-Garrido and Ocampo2002; Pozo et al. Reference Pozo, Cordier, Dumas-Gaudot, Gianinazzi, Barea and Azcón-Aguilar2002). Ozgonen et al. (Reference Ozgonen, Yardimci and Kilic2009) demonstrated that mycorrhizal inoculation of pepper plants (cvar Charliston Bagci) infected by P. capsici induced a significant increase in activity of β-1,3-glucanase and chitinase compared with non-inoculated plants. In all treatments, the β-1,3-glucanase and chitinase activities were maximum 6 days after inoculation, decreasing at the initial and final assessments 3 and 9 days after inoculation, respectively. The levels of both, β-1,3-glucanase and chitinase enzymes in control plants ranged from 0 to 3 µ kat/mg of protein. The level of β-1,3-glucanase enzyme was higher in P. capsici infected plants (19 µ kat/mg of protein) and those with combined inoculation of AM fungi and P. capsici treatments (19–25 µ kat/mg of protein), as compared to that at the single mycorrhizal treatments (10–16 µ kat/mg of protein) 6 days after inoculation. Similarly, chitinase activity was higher in P. capsici infected plants (11 µ kat/mg of protein) and those with combined inoculation of AM fungi and P. capsici treatments (9–14 µ kat/mg of protein), as compared to that at the single mycorrhizal treatments (5–7 µ kat/mg of protein) 6 days after inoculation. Ozgonen et al. (Reference Ozgonen, Yardimci and Kilic2009) also found an increase in the amount of phenolic compounds, which were highest in plants with combined inoculation of AM fungi and P. capsici treatments. Some of these compounds were identified as: caffeic acid, trans-coumaryl, capsaicin (CAP), p-aminobenzaldehyde, aspartic acid, chlorogenic acid, glutamic acid, linoleic acid, cis-feruloyl acid, stearic acid, capsicoside and F1 compound.

Phytoalexin production during the early stages of colonization could provide pepper plants (cvar Charliston Bagci) with a defence against P. capsici. Ozgonen & Erkilic (Reference Ozgonen and Erkilic2007) noted that infected plants inoculated with AM fungi showed improvement in capsidiol content, which may have had an influence on plant response against the pathogen.

Garmendia et al. (Reference Garmendia, Aguirreolea and Goicoechea2006) also reported that pepper root colonization (cvar Piquillo) by AM fungi induced the appearance of new isoforms of acid chitinases, SOD and at early stages, POXs. In addition, infection with V. dahliae slightly increased the activity of both phenylalanine ammonia-lyase and POX only in mycorrhized roots. These observations suggest a role of AM fungi in biochemical-protection of plants against Verticillium wilt in pepper.

Garmendia et al. (Reference Garmendia, Goicoechea and Aguirreolea2004b ) showed that the association with AM fungi reduced the deleterious effects on plant hydric condition caused by Verticillium wilt. The results showed that AM inoculation maintained leaf water content for longer and delayed development of disease symptoms such as decreased photosynthesis in plants inoculated with the pathogen. According to Garmendia et al. (Reference Garmendia, Goicoechea and Aguirreolea2004b ), these benefits to the physiology of the plant promoted improvements in its yield.

Physiological and biochemical response to arbuscular mycorrhizal fungi in terms of improved plant health

Phosphorus plays an important role in the energy metabolism of cells during photosynthesis (Marschner Reference Marschner2012). Studies show that AM fungi can facilitate an increased P absorption in pepper plants and partially reduce the effects of low P supply in the soil, thereby improving photosynthetic rate, stomatal conductance and gas exchange of plants (Aguilera-Gómez et al. Reference Aguilera-Gómez, Davies, Olalde-Portugal, Duray and Phavaphutanon1999). Mycorrhizal inoculation has also been shown to positively affect the levels of carotenoids in some cases (Tallapragada et al. Reference Tallapragada, Rajiv, Anjanappa, Sardesai, Selvaraj and Khan2011; Çekiç et al. Reference Çekiç, Unyayar and Ortas2012).

Aguilera-Gómez et al. (Reference Aguilera-Gómez, Davies, Olalde-Portugal, Duray and Phavaphutanon1999) showed that mycorrhizal association not only relieved P-stress, but also increased reproductive growth of pepper plants (cvar San Luis) grown in greater availability of P (44 g P/m³) by 450%. Additionally, photosynthetic rate and P levels in plant tissue were higher in mycorrhized plants cultivated on high levels of P. Demir (Reference Demir2004) found that the concentration of P was positively correlated to the levels of chlorophyll (a, b and a + b) and sugars (fructose, α-glucose and β-glucose) and that this had positively affected the physiological performance in pepper plants (cvar Cetinel-150). Arbuscular mycorrhizal fungi may function as a metabolic reservoir causing basi-petal mobilization of photosynthates to roots, thus providing a stimulus for higher photosynthetic activity (Bieleski Reference Bieleski1973). Tanwar et al. (Reference Tanwar, Aggarwal, Kadian and Gupta2013) demonstrated that in low doses of P, co-inoculation with PGPB and AM fungi increased the levels of chlorophyll a and b in bell pepper var. California Wonder, resulting in an increase in photosynthetic rate, and suggest that this may be due to absorption of more nutrients and an increased gas exchange by improvement of stomatal conductance.

Physiology and biochemistry: hormonal responses to arbuscular mycorrhizal fungi colonization

Arbuscular mycorrhizal fungi play a role in hormonal balance during the adaptation of plants to adverse conditions, which can regulate its performance. Several studies have demonstrated the role of AM fungi in phytohormone level changes during symbiosis, including cytokinins, gibberellins, ethylene, ABA, salicylic acid and jasmonates (Hause et al. Reference Hause, Mrosk, Isayenkov and Strack2007). In Capsicum sp., the AM fungi effect on the development of pepper plants showed a positive correlation with the concentration of different growth regulators during phenological stages of the plant (García Reference García2003). According to García (Reference García2003), the concentrations of indoleacetic acid (IAA) and gibberellic acid (AG3) in the shoot were higher in AM fungi colonized plants compared with non-inoculated ones. Also, adenine concentration (6-aminopurine) in roots showed higher values. There was also an increase of 10% in the total chlorophyll content and 20% in the total protein levels, which may have a direct effect on production and quality of fruit, as well as levels of plant growth promoters. Improvements in cytokinin and gibberellin levels have been demonstrated in plants inoculated with AM fungi (Allen et al. Reference Allen, Moore and Christensen1980, Reference Allen, Moore and Christensen1982). Increases in such hormones, particularly cytokinins, could elevate photosynthetic rates by stomatal opening, influencing the transport of ions and regulating the levels of chlorophyll (Allen et al. Reference Allen, Moore and Christensen1980, Reference Allen, Moore and Christensen1982). Goicoechea et al. (Reference Goicoechea, Antolín and Sánchez-Díaz1997) showed that there is a positive correlation between cytokinin increase and the rate of gas exchange, stomatal conductance and transpiration. Moreover, evidence suggests that ABA could also play a role in plant stomatal control (Zhang et al. Reference Zhang, Schurr and Davies1987), which reinforces the results found by Estrada-Luna et al. (Reference Estrada-Luna, Davies and Egilla2000) and Estrada-Luna & Davies (Reference Estrada-Luna and Davies2003). Therefore, maintaining hormone levels in mycorrhized plant contributes to improved photosynthesis, promoting plant development and yield.

Physiological and biochemical response of fruit to arbuscular mycorrhizal fungi colonization

The effect of AM symbiosis on the quality attributes of fruits of Capsicum spp. has not been widely reported. Castillo et al. (Reference Castillo, Ortiz, Borie and Rubio2009a , Reference Castillo, Sotomayor, Ortiz, Leonelli, Borie and Rubio b ) showed a slight increase in ascorbic acid concentration in fruits of colonized plants; however, no significant differences were found for total titratable acidity (% of citric acid) and total soluble solids (°Brix). Under drought conditions, Mena-Violante et al. (Reference Mena-Violante, Ocampo-Jiménez, Dendooven, Martínez-Soto, González-Castañeda, Davies and Olalde-Portugal2006) found that the inoculation of pepper plants (cvar San Luis) promoted significant improvements in various fruit quality parameters, such as pigment concentration. Chlorophyll content in fruit of mycorrhized plants under water stress were similar to those found in non-inoculated plants that were not subjected to drought. In addition, the levels of carotenes and xanthophylls in the fruit were 1·4 times higher in AM inoculated plants subjected to drought compared to that in non-inoculated plants not exposed to drought. This could be attributed to a mycorrhizal inoculation effect on the process of fruit maturation (Castillo et al. Reference Castillo, Ortiz, Borie and Rubio2009a ) and changes in the concentration of photosynthetic pigments during symbiosis (Demir Reference Demir2004).

Pungency is an important quality attribute in peppers, and its expression is associated with the presence, in a greater or lesser proportion, of alkaloids known as capsaicinoids (Appendino Reference Appendino, Fattorusso and Taglialatela-Scafati2008). Among these, CAP and its dihydro derivative (dihydrocapsaicin (DHC)) constitute >0·80 of the total capsaicinoids in most of the pungent varieties (Kosuge & Furuta Reference Kosuge and Furuta1970). The levels of CAP are usually higher than DHC (Antonious et al. Reference Antonious, Berke and Jarret2009) and these are considered the main parameter to determine the commercial quality of a product or derivatives (Frary & Frary Reference Frary, Frary and Russo2012). In terms of improved quality attributes, no research has been conducted on the role of AM colonization on capsaicinoid levels in pepper.

The association with AM fungi promotes physiological and biochemical changes in plants, activating diverse metabolic pathways that can result in an increase of secondary compounds (Rojas-Andrade et al. Reference Rojas-Andrade, Cerda-García-Rojas, Fríaz-Hernández, Dendooven, Olalde-Portugal and Ramos-Valdivia2003; Strack & Fester Reference Strack and Fester2006; Carlsen et al. Reference Carlsen, Understrup, Fomsgaard, Mortensen and Ravnskov2008). Therefore, the use of AM fungi seems to be a plausible strategy to obtain increases in certain compounds of interest.