Effect of Glomus mosseae and Entrophospora colombiana on plant growth, production, and fruit quality of ‘Maradol’ papaya (Carica papaya L.)

Scientia Horticulturae 128 (2011) 255–260

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Effect of Glomus mosseae and Entrophospora colombiana on plant growth, production, and fruit quality of ‘Maradol’ papaya (Carica papaya L.) Marcos V. Vázquez-Hernández a,∗ , Lourdes Arévalo-Galarza a , David Jaen-Contreras a , José L. Escamilla-García b , Antonio Mora-Aguilera a , Elías Hernández-Castro c , Juan Cibrián-Tovar a , Daniel Téliz-Ortiz a a

Colegio de Postgraduados, Km. 36.5 Carretera México-Texcoco, Montecillo, Texcoco, CP 56230, Mexico Escuela de Ciencias Agropecuarias de la Universidad Michoacana de San Nicolás de Hidalgo, Mariano Jiménez s/n colonia el Varillero, Apatzingán, CP 60660, Michoacán, Mexico Maestría en Sistemas de Producción Agropecuaria de la Universidad Autónoma de Guerrero México, Km. 273.5 Carretera México-Acapulco, Chilpancingo, CP 39090, Guerrero, Mexico b c

a r t i c l e

i n f o

Article history: Received 21 July 2010 Received in revised form 8 January 2011 Accepted 26 January 2011 Keywords: Carica papaya Mycorrhizae Production Postharvest quality

a b s t r a c t The effect of inoculating ‘Maradol’ papaya plants with arbuscular mycorrhizal fungi (AMF) Glomus mosseae (GM) and Entrophospora colombiana (EC) was assessed. The results showed that both mycorrhizae species increased the number of fruits and yield in papaya plants by 41.9 and 105.2% for GM and 22.1 and 44.1% for EC, respectively, with respect to control plants. GM significantly increased plant height. Sugar content, firmness, color (◦ Hue), and ripening process of mycorrhized plant fruits were similar to those of the control. Weight loss of mycorrhized plant fruits was considerably less than that of the control. Inoculation of papaya with AMF is recommended, particularly with GM since it increases yield, and fruit weight (45.1%), furthermore, it reduced fruit weight loss during ripening. © 2011 Elsevier B.V. All rights reserved.

1. Introduction Mexico is the second producer and the first exporter of papaya (Carica papaya L.) worldwide, with an estimated production of 919,425 tons and export value of 55 million US dollars in 2007 (FAO, 2010). In the last years, production costs have been increased because of the indiscriminate use of mineral fertilizers required by the plant for its growth and continuous production (Nakasone and Paull, 1998), which provoked the search of alternatives to diminish costs. The use of arbuscular mycorrhizal fungi (AMF) as biofertilizers increases the yield in crops like pomegranate (Punicagranatum L.) (Aseri et al., 2008), tomato (Lycopersiconesculentum Mill) (Makus, 2004), watermelon (CitrulluslanatusThunb.) (Kaya et al., 2003), and strawberry (Fragaria × ananassa Duch.) (Jaen et al., 1997). According to the aforesaid, the use of mycorrhizae in papaya production is an alternative to reduce production costs and increase productivity. AMF are key components of the rhizosphere

∗ Corresponding author. Tel.: +52 5959520233; fax: +52 5959520233. E-mail addresses: marcos [email protected], marcos [email protected] (M.V. Vázquez-Hernández), [email protected] (L. Arévalo-Galarza), [email protected] (D. Jaen-Contreras), [email protected] (J.L. Escamilla-García), [email protected] (A. Mora-Aguilera), [email protected] (E. Hernández-Castro), [email protected] (J. Cibrián-Tovar), [email protected] (D. Téliz-Ortiz). 0304-4238/$ – see front matter © 2011 Elsevier B.V. All rights reserved. doi:10.1016/j.scienta.2011.01.031

since they form a mutualistic association with the roots of 90% of the terrestrial plants (Smith and Read, 1997). They improve rooting and establishment of the crop (Alarcón and Ferrera-Cerrato, 1999), increase the absorption of mineral nutrients (especially of ions of limited mobility, such as P, Cu, and Zn) (Bethlenfalvay et al., 1988; Marschner and Dell, 1994), favor nutrient renovation (Leake et al., 2004), and promote tolerance to biotic and abiotic stress (Barea and Jeffries, 1995), mainly against the attack of some pathogens of radical habits (bacteria, nematodes, fungi, etc.) (Pozo and Azcón-Aguilar, 2007; Borowicz, 2001); they improve soil structure (Azcón-Aguilar and Barea, 1997), bring about greater vegetal diversity (Leake et al., 2004), and are sources of hormones such as abscisic acid, gibberellins, auxins, and cytokinins (Strack et al., 2003; Hirsch et al., 1997; Jaen et al., 1997). Based on the aforementioned, AMF favor plant growth and increase production (Aseri et al., 2008), however, the effects of AMF are variable, depending on the host plant and on the edaphic-environmental factors (Mueller et al., 2009). Inoculation with Glomus fasciculatum in chile ancho plants (Capsicum annum L. cv San Luis) resulted in an increase of fruit size in 25%, but with lesser color (chroma) development (Mena-Violante et al., 2006). The inoculation with Glomus mosseae increased fruit size (12%) of tomato (Lycopersiconesculentum ‘Counter’) compared to the control (Mueller et al., 2009). Trials carried out with mycorrhizae in previous years have confirmed their beneficial effects on papaya production. Nevertheless, the

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Table 1 Soil characteristics of the experimental orchard where papaya plants inoculated with Glomus mosseae and Entrophospora colombiana were grown. Soil characteristics

Units

Value

pH CE OM N P K Ca Mg Mn Cu Zn Fe B Sand Loam Clay

dS m−1 % % mg kg−1 cmol(+) kg−1 cmol(+) kg−1 cmol(+) kg−1 mg kg−1 mg kg−1 mg kg−1 mg kg−1 mg kg−1 % % %

6.30 1.20 2.23 0.14 10.00 2.10 10.20 1.00 1.21 0.30 0.93 0.41 0.53 17.20 50.25 37.52

effect of mycorrhizae on papaya quality is not known yet; therefore, the aim of the present research was to assess the effect of G. mosseae and Entrophospora colombiana on plant development, production, and quality of ‘Maradol’ papaya fruits. 2. Materials and methods 2.1. Soil analysis and treatment The experimental plantation was located in Huamuxtitlán, Gro., Mexico, (17◦ 41 –17◦ 54 N and 98◦ 26 –98◦ 40 W) at 890 m altitude. The climate is warm dry with 25.9 ◦ C mean temperature and 803.3 mm of annual mean precipitation (SMN-CONAGUA, 2009). Before sowing, three composite soil samples each one from 10 random locations of the first 40 cm were taken for nutrient analysis. The soil was air-dried and sieved through a 5 mm mesh net. The soil samples were analyzed in order to determine pH (1:2 H2 O), electrical conductivity (CE) (1:5 H2 O) and content of organic matter (OM) (Jackson, 1964); N content was determined by Kjeldahl method (Bremner and Mulvaney, 1982). The P content was estimated by extraction with NaHCO3 by Olsen method (Olsen and Dean, 1965). K, Ca, and Mg were extracted with ammonium acetate (CH3 COONH4 ) (1 N pH 7) (Chapman, 1965) and determined by spectrophotometry of atomic absorption. The content of micronutrients was quantified in the extract with diethylene-triamino-penta acetic acid (DTPA) by atomic absorption spectrophotometry. Organic matter content was verified by quick oxidation (Jackson, 1964). Finally, the soil texture was analyzed using the hydrometric method (Bouyoucos, 1936). The soil of the experimental plot is slightly acid with mean content of P, K, Ca, and organic matter, moderately rich in N and low in Mg (Benton et al., 1991). Contents of Fe, Mn, and Cu were adequate, whereas that of Zn was marginal (Reuter and Robinson, 1986) and of clay–loam texture (Table 1). Finishing harvest, the content of N, P, and K were determined taking the soil from different locations randomly chosen to get 6 replicates per treatment. Thirty days before establishing the experiment, the soil was fumigated with Metham-Sodio (BUNEMA® 55 GE; 560 L ha−1 ). The application of the compound was by irrigation system, where it was carried through the soil by the water front according to the product specifications. After the treatment the soil was left airing, and subsequently, the land was prepared for transplant. 2.2. Inoculum production G. mosseae and E. colombiana stocks were used; their identification was made based on the description of the groups of spore

walls (Schenck and Pérez, 1990). The inoculant was produced by means of the host plant method (Sieverding, 1983). Pre-germinated onion seeds (Allium cepa L.) in sterile substrate were utilized. After 6 months, harvesting was done and mycorrhizal colonization (Phillips and Hayman, 1970) and spore density in 100 g of dry soil were verified (Gerdemann and Nicolson, 1963). 2.3. Plant treatment and cultivation Papaya ‘Maradol’ seeds were soaked in clean water for 24 h with three changes of water every 8 h. The seeds were treated by immersion in benomyl solution (1 g L−1 , 8 h) and two rinses with sterile water. The treated seeds were placed on sterile towels to germinate and irrigated with manual atomizer every 2 h. When the radicle had emerged, they were sown on germination trays (60 cm × 40 cm) with autoclave sterilized sand (120 ◦ C, 3 h−1 ). Six centimeter-high seedlings were pre-transplanted in bags with 1 kg growth substrate (soil: river sand, 2:1, sterilized in autoclave sand: 120 ◦ C, 3 h−1 ) containing 100 g of inoculum of G. mosseae or E. colombiana (7300 spores kg−1 ). Transplanting was carried out when the plants reached a height of 20 cm and/or 7 true fully expanded leaves and stem diameter of 1 cm. The treatments were: Control, G. mosseae (GM), and E. colombiana (EC) with plantation density of 2857 plants ha−1 at a distance of 2.5 m between rows and 1.4 m among plants. In all the treatments the employed fertilization was 235–42–222 kg ha−1 N–P–K, distributed in transplant (117–21–0), flowering (59–21–157), and fruiting (59–0–65). At 30, 120, and 210 days after transplant, readings of plant height were taken with a flexometer (from stem base to the apical bud) and of stem diameter with a digital vernier (Caldi-6MP, Truper, USA) at 10 cm from the base. Height of the first fruit was measured from the stem base. Number of fruits per plant was determined, and yield was estimated, based on the mean weight of fruits. Two hundred and forty plants per treatment were used and 40 plants as experimental unit with 6 replications. 2.4. Mycorrhizal colonization and spore density Samples of six papaya plant roots per treatment and their soil were collected at the end of experiment. They were washed with running water, cleared with KOH (10%), stained with trypan blue (0.05%), and cut each ones into 10 segments of 1 cm considered as a replicate (Rufykiri et al., 2000). The segments were placed (at random) in parallel on a microscope slide in order to determine mycorrhizal infection (hyphae, vesicles, and arbuscular mycorrhizae) at 45×. Three visual fields in each root segment were examined to observe colonization by GM, EC, and native mycorrhizae. Colonization percentage was calculated as the ratio of the infected root sections by the observed sections per 100. The extraction and spore density were done by the method described by Gerdemann and Nicolson (1963). Pearson’s correlation analysis was done for each treatment (N = 6) and for all samples (N = 18) to determine the relationships between mycorrhizal colonization and spore density. 2.5. Mineral content in fruits At harvest, 10 fruits per treatment were used to evaluate the mineral content. Total N was determined by Microkjeldahl method (Chapman and Pratt, 1973). P was evaluated by colorimetry in Spectro-photocolorimeter (20D, Milton Roy Co., USA). K, Ca, Mg, Mn, Cu, Zn, and Fe elements were analyzed by atomic absorption spectrophotometer (IL 551, Instrumentation Laboratories, Spain) (Chapman and Pratt, 1973). Six replications per treatment were used to determine Pearson’s correlation (N = 18) between N content and fruit weight, and N content and fruit firmness.

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Table 2 Plant height, stem diameter, and height of the first fruit of papaya plants inoculated with Glomus mosseae and Entrophospora colombiana at 30, 120, and 210 days after transplant. Treatment

Plant height (cm)

Stem diameter (cm)

Days after transplant

Control G. mosseae E. colombiana

Height of the first fruit (cm)

Days after transplant

30

120

210

30

120

210

29.2 b 32.5 a 31.3 a

86.0 b 88.9 a 87.2 ab

174.9 b 180.3 a 174.9 b

1.1 b 1.3 a 1.3 a

6.5 b 6.9 a 6.6 b

10.6 a 10.8 a 10.6 a

37.5 a 36.9 a 37.2 a

Different letters in columns are significantly different. Tukey (P < 0.05).

2.6. Postharvest evaluation

3.3. Soil and mycorrhizal colonization analysis

Fruits were harvested at physiological maturity (40% of color development). They were washed and treated with sodium hypochlorite solution (200 ␮L L−1 ), submerged in Prochloraz (500 ␮L L−1 , 2 min). The assessed variables were: content of total sugars (%), firmness (Newtons, N), pulp and epidermis color (◦ Hue), and weight loss (%) during fruit ripening at 20 ± 1 ◦ C. Evaluations were carried out on days 1, 3, 5, 7, 9, and 11 after harvest. The content of total sugars was determined by antrona method (Witham et al., 1971). Fruit firmness was measured using a texturometer (FDV-30, Wagner Instrument, USA) with a 10 mm cutting pointer at 4 points of the fruit, previously eliminating epidermis in the evaluation zones. For defining color of epidermis and fruit pulp a colorimeter (Hunter Lab D-25a, USA) was utilized, obtaining values L, a and b, for tonality calculation (◦ H = tan−1 b/a). Weight loss with respect to the initial weight was assessed with a digital balance (EY-2200-A, Alsep, Japan). Each fruit was considered as experimental unit with 6 replications.

Soil analysis before and after harvest indicated that N content diminished by 42.8, 28.6, and 42.8% in the soil of the control, G. mosseae, and E. colombiana, respectively. Likewise, P level diminished in the soil of control and E. colombiana by 8.0 and 1.0% with respect to the initial value; whereas it increased by 9.0% in soil of plants inoculated with G. mosseae. K was reduced by 23.8, 15.2, and 19.5% in the soil of control, G. mosseae, and E. colombiana, respectively. Low colonization was found in control plants (Table 4). Mycorrhizal colonization and spore density were higher in plants inoculated with G. mosseae than E. colombiana (Table 4). There is high correlation between colonization of inoculated plants and spore density in soil (R2 = 0.98, P < 0.0001). The lowest correlation per treatment was for E. colombiana (R2 = 0.44, P = 0.37) compared to G. mosseae (R2 = 0.82, P = 0.043) and control (R2 = 0.76, P = 0.0756).

2.7. Statistical analysis The results were analyzed in a completely randomized experimental design. Normality of the obtained results was verified with the Kolmogorov–Smirnov test. An analysis of variance and separation of means was conducted according to Tukey’s honest significant difference (HSD) with a 0.05 probability level by means of the statistical program SAS® , version 9.1.3 (2005).

3.4. Mineral content in fruits Inoculation with G. mosseae significantly raised N and Fe contents in fruits by 150 and 21.1% compared to the control. E. colombiana increased Ca and Fe content by 75.0 and 20.5%, respectively; on the contrary, Zn level was reduced by 36.2% with respect to the control. P, K, Mg, Mn, and Cu contents were not affected by the treatments. Content of N and Zn was higher in fruits of plants inoculated with G. mosseae than in those with E. colombiana (Table 5). 3.5. Postharvest evaluation

3. Results 3.1. Plant growth Inoculation with G. mosseae significantly increased plant height with respect to the control by 11.3, 3.4, and 3.1% at 30, 120, and 210 days after transplant; stem diameter increased as well by 18.2% and 6.2% respectively, at 30 and 120 days (Table 2). Inoculation with E. colombiana only increased significantly plant height (7.2%) and stem diameter (18.2%) compared to the control at 30 days after transplant. G. mosseae showed greater effect on plant height than E. colombiana at 210 days after transplant, and on stem diameter at 120 days after transplant; none of the treatments affected height of the first fruit. 3.2. Yield Inoculation with G. mosseae increased the number of fruits per plant by 41.9%, fruit weight by 45.1% and yield by 105.2% with respect to the control (Table 3). Inoculation with E. colombiana raised the number of fruits per plant by 22.1%, fruit weight by 18.4% and yield by 44.1%.

After 11 days weight loss was lower in papaya fruits from plants inoculated with G. mosseae (22.9%) and E. colombiana (24.1%) compared to the control (Fig. 1D). Content of total sugars and color (◦ Hue) in epidermis and pulp were not affected by the treatments (Fig. 1A and C). Fruit firmness of plants with G. mosseae remained inferior to the control and E. colombiana during 7 days after harvest, but at the end of the evaluation there were no differences among treatments (Fig. 1B) Positive correlation between N content in fruits and fruit weight (R2 = 0.73, P = 0.0007) and an inverse correlation between N content and fruit firmness (R2 = −0.84, P = 0.0006) were found. Table 3 Yield, fruit weight, and fruits per papaya plant inoculated with Glomus mosseae and Entrophospora colombiana. Treatment

Yield (ton ha−1 )

Fruit weight (g)

Fruits per plant

Control G. mosseae E. colombiana

70.6 c 144.9 a 101.7 b

1432.6 c 2078.0 a 1695.5 b

17.2 c 24.4 a 21.0 b

Different letters in columns are significantly different. Tukey (P < 0.05).

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Table 4 N P, and K content, mycorrhizal colonization, and spore density of the soil at finishing the experiment of papaya plant inoculation with Glomus mosseae and Entrophospora colombiana. Treatment

Macronutrient content

Control G. mosseae E. colombiana

N (g 100 g−1 )

P (mg kg−1 )

K (cmol(+) kg−1 )

0.08 b 0.10 a 0.08 b

9.2 c 10.9 a 9.9 b

1.60 c 1.78 a 1.69 b

Mycorrhizal colonization (%)

Spore density 100 g−1 soil

16.5 c 91.5 a 58.2 b

470.0 c 2536.5 a 2030.0 b

Different letters in columns are significantly different. Tukey (P < 0.05).

Table 5 Nutrient content of papaya plant fruits inoculated with Glomus mosseae and Entrophospora colombiana. g 100 g−1

Treatment

Control G. mosseae E. colombiana

mg kg−1

N

P

K

Ca

Mg

Mn

Cu

Zn

Fe

0.4 b 1.0 a 0.6 b

0.34 a 0.39 a 0.38 a

2.9 a 3.2 a 2.9 a

0.4 b 0.5 ab 0.7 a

0.14 a 0.22 a 0.18 a

5.5 a 6.7 a 5.0 a

2.8 a 3.4 a 3.2 a

5.8 a 6.5 a 3.7 b

74.5 b 90.2 a 89.8 a

Different letters in columns are significantly different. Tukey (P < 0.05).

4. Discussion

in onion bulbs and high colonization of the same plant species (Goussous and Mohammad, 2009). In this study, high concentration of N, Ca and Fe in fruits corresponds to high colonization in papaya plants, attributed to major uptake of plant nutrients due to more soil exploration. There is plenty of evidence that AMF enhance symbiotic N fixation, AMF have also shown effect on N uptake and transport from soil via mycorrhizal hyphae (Bethlenfalvay and Schüepp, 1994) as well as mycorrhizae increasing N availability through mineralization of organic substances (Atul-Nayyar et al., 2009; Goussous and Mohammad, 2009). P content increment in the soil of plants inoculated with G. mosseae indicates the capacity of mycorrhizae of solubilizing P, normally not available (Goussous and Mohammad, 2009). Plants inoculated with G. mosseae and E. colombiana had high percentage of colonization and sporulation, compared to control

Papaya plant development has been favored by inoculation with G. mosseae and to a lesser extent with E. colombiana. The positive influence of the arbuscular mycorrhizal fungi on plant growth, fruit weight, and yield is related to the high percentage of colonization and mycorrhizal spore density in soil, which increase water supply and plant nutrients (Goussous and Mohammad, 2009; Kothamasi et al., 2001). Higher correlation of colonization and spore density could indicate a possible reinoculation and major adaptability of G. mosseae to climate and soil conditions in the study zone than that of E. colombiana, showing better efficiency in acid soils (Sieverding, 1991). There is high correlation between infectious capacity of native mycorrhizae and higher plant growth (Klironomos, 2003), likewise, direct correlation has been observed between N content

8

HSD(0.05) = 15.81 60

6 40 4 20

2 0

A

B HSD(0.05) = 17.32

140

HSD(0.05) = 1.38

8

120 100

6

Epidermis

80

Pulp

60 40 20 0

0

4

HSD(0.05) = 17.57 C

2

D 1

3

5

7

Days at 20 ºC

9

11

1

3

5

7

9

11

Weight loss (%)

Color (ºHue)

80

Control HSD(0.05) = 1.71 Glomus mosseae Entrophospora colombiana

Firmness (N)

Total sugars (%)

10

0

Days at 20 ºC

Fig. 1. Content of total sugars (A), firmness (B), color (◦ Hue in epidermis and pulp) (C), and weight loss (D) in papaya fruits of plants inoculated with Glomus mosseae or Entrophospora colombiana stored at 20 ◦ C. HSD: Tukey’s honest significant difference (P < 0.05).

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plants. Given the presence of native mycorrhizae, competition between these with G. mosseae and E. colombiana during plant development might be possible. Nevertheless G. mosseae proved to be more competitive than E. colombiana, showing greater effects on plant height, yield and N content of fruits. Competition among mycorrhizal fungi species is mainly established by the amount of inoculum and, subsequently, by growth capacity of infective hyphae (within and outside the roots), and the formation of new infection units (Wilson, 1984; Sanders and Sheikh, 1983). The significant differences in the same parameters in plants inoculated with G. mosseae compared to the control, seems to indicate that G. mosseae has better adaptability to edaphic and climatic conditions than E. colombiana. It is possible as well that better results obtained by G. mosseae are due to the high association of this genus with papaya plants (Khade and Rodrigues, 2009; Trindade et al., 2006). In this experiment, sugar content of ‘Maradol’ papaya fruit was lower than its values reported by Pérez-Carrillo and Yahia (2004) and Gayosso-García et al. (2010), attributed to a possible dilution because of rain water excess days before harvest (González et al., 2006). However Allan (2002) points out that fruit sugar content can vary depending on the season. Content of total sugars of the mycorrhizal plant fruits was slightly lower than that of the control, probably due to the fact that mycorrhizal association provokes translocation of sugars towards the root being required by the fungus (Goussous and Mohammad, 2009). The increase of fruit size, and consequently less weight loss, was another beneficial effect of mycorrhizae, since bigger fruits have less surface area/volume ratio than the smaller fruits produced by control plants (Ahmad et al., 2006; Wills et al., 1998). There was significant positive correlation between N content in fruits with fruit weight, but a reverse relation between N content with fruit firmness. Several studies show high correlation between N content and fruit size and yield; for example, high nitrogen fertilizer doses caused considerably bigger fruit growth of raspberry and increased yield (Quezada et al., 2007). In other studies, inverse correlation between N content and fruit firmness is reported on apple (Nava et al., 2008), tomato (Villarreal et al., 2002), peach (Hernández-Fuentes et al., 2004), and strawberry (Mukkun et al., 2001).

5. Conclusions Inoculation with G. mosseae and E. colombiana increased papaya yield by improving setting and fruit weight. N and Fe supply to fruits was favored by G. mosseae, and that of Ca and Fe by E. colombiana. The inoculation with both mycorrhizae species affected nutrient content in soil to a lesser degree at the end of the experiment, with respect to the control. G. mosseae increased significantly papaya plant height. Plant inoculation with G. mosseae and E. colombiana did not affect papaya fruit quality. G. mosseae and E. colombiana significantly reduced weight loss, an important aspect in papaya, given the high transpiration and perishability of the fruits. G. mosseae had better influence in various aspects, possibly due to greater association with papaya plants and better adaptability to edaphic and environmental conditions in the study region.

Acknowledgements The authors thank LPI-7 (Línea Prioritaria de Investigación en Inocuidad, Calidad de Alimentos y Bioseguridad), Colegio de Postgraduados, and Fundación Produce de Guerrero for the financial support to this project.

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References Ahmad, S., Thompson, A.K., Perviez, M.A., Anwar, N., Ahmad, F., 2006. Effect of fruit size and temperature on the shelf life and quality of ripe banana fruit. J. Agric. Res. 44, 313–324. Alarcón, A., Ferrera-Cerrato, R., 1999. Manejo de la micorriza arbuscular en sistemas de propagación de plantas frutícolas. TerraLatinoam. 17, 1979–1991. Allan, P., 2002. Carica papaya responses under cool subtropical growth conditions. Acta Hortic. 575, 757–763. Aseri, G.K., Jain, N., Panwar, J., Rao, A.V., Meghwal, P.R., 2008. Biofertilizers improve plant growth, fruit yield, nutrition, metabolism and rhizosphere enzyme activities of Pomegranate (Punicagranatum L.) in Indian Thar Desert. Sci. Hortic. 117, 130–135. Atul-Nayyar, A., Hamel, C., Hanson, K., Germida, J., 2009. The arbuscular mycorrhizal symbiosis links N mineralization to plant demands. Mycorrhiza 19, 239–249. Azcón-Aguilar, C., Barea, J.M., 1997. Applying mycorrhiza biotechnology to horticulture: significance and potentials. Sci. Hortic. 68, 1–24. Barea, J.M., Jeffries, P., 1995. Arbuscularmycorrhizas in sustainable soil plant systems. In: Varma, A., Hock, B. (Eds.), Mycorrhiza Structure, Function, Molecular Biology and Biotechnology. Springer-Verlag, Heidelberg, pp. 521–560. Benton, J.J., Wolf, J.B., Mills, H.A., 1991. Plant Analysis Handbook, a Practical Sampling, Preparation, Analysis and Interpretation Guide. Micro-Macro Publishing, Inc., USA. Bethlenfalvay, G.J., Brown, M.S., Ames, R.N., Thomas, R.S., 1988. Effects of drought on host and endophyte development in mycorrhizal soybeans in relation to water use and phosphate uptake. Physiol. Plant. 72, 565–571. Bethlenfalvay, G.J., Schüepp, H., 1994. Arbuscularmycorrhizas and agrosystemstability. In: Gianinazzi, S., Schüepp, H. (Eds.), Impact of arbuscularmycorrhizas on sustainable agriculture and natural ecosystems. BirkhäuserVerlag, Basel, pp. 117–131. Borowicz, V.A., 2001. Do arbuscular mycorrhizal fungi alter plant–pathogen relations? Ecology 82, 3057–3068. Bouyoucos, G.S., 1936. Directions for making mechanical analysis of soil by hydrometer method. Soil Sci. 4, 225–228. Bremner, J.M., Mulvaney, C.S., 1982. Nitrogen-total. In: Page, A.L., Miller, H., Keeny, D.R. (Eds.), Methods of Soil Analysis, Part 2. Agronomy Monograph 9. American Society of Agronomy, Madison, WI, USA, pp. 56–59. Chapman, H.D., Pratt, P.F., 1973. Métodos de Análisis para Suelo, Plantas y Agua. Trillas, México. Chapman, H.D., 1965. Cation exchange capacity. In: Black, C.A. (Ed.), Methods of Soil Analysis. Part 2. Agronomy Monograph 9. American Society of Agronomy, Madison, WI, USA, pp. 891–901. FAO, Food and Agriculture Organization, 2010. Statistical Database Internet http://faostat.fao.org/site/535/DesktopDefault.aspx?PageID=535#ancor (date 01.15.10). Gerdemann, J.W., Nicolson, T.H., 1963. Spores of mycorrhizalendogene species extracted from soil by wet sieving and decanting. Trans. Br. Mycol. Soc. 46, 235–244. González, M.G., Moreno, G., Giardina, E.B., Miro, M.D., 2006. Exceso de agua en el suelo: efecto sobre la calidad del fruto del duraznero Prunuspersica (L.) Batsch. Cienc. Suelo (Argentina) 24, 1–5. Goussous, S.J., Mohammad, M.J., 2009. Comparative effect of two arbuscularmycorrhizae and N and P fertilizers on growth and nutrient uptake of onions. Int. J. Agric. Biol. 11, 463–467. Gayosso-García, S.L.E., Yahia, E.M., Martínez-Téllez, M.A., González-Aguilar, G.A., 2010. Effect of maturity stage of papaya maradol on physiological and biochemical parameters. Am. J. Agric. Biol. Sci. 5, 194–203. Hernández-Fuentes, A.D., Colinas, L.M.T., Pinedo-Espinoza, J.M., 2004. Effect of fertilization on the concentration of N, P, K, Ca, Mg, Fe, Mn, Cu, Zn and phenylalanine ammoniolyase activity in fruit of ‘Zacatecas’-type peach (Prunuspersica (l.) Batsch). Acta Hortic. 636, 521–525. Hirsch, A.M., Fang, Y., Asad, S., Kapulnik, Y., 1997. The role of phytohormones in plant–microbe symbioses. Plant Soil 194, 171–184. Jackson, M.L., 1964. Chemical composition of soils. In: Bear, F.E. (Ed.), Chemistry of the Soil. , second ed. Reinhold Publ. Corp., New York, pp. 71–141. Jaen, C.D., Becerril, R.A.E., Colinas, L.M.T., Santizo, R.J.A., 1997. Crecimiento y producción de fresa inoculada con Glomus mosseae, asperjada con AG3 y fertilizada con NPK. Agrociencia 31, 165–169. Kaya, C., Higgs, D., Kirnak, H., Tas, I., 2003. Mycorrhizal colonization improves fruit yield and water use efficiency in watermelon (CitrulluslanatusThunb.) grown under well-watered and water-stressed conditions. Plant Soil 254, 287–292. Khade, S.W., Rodrigues, B.F., 2009. Spatio-temporal variations of arbuscular mycorrhizal (AM) fungi associated with Carica papaya L. in agro-based ecosystem of Goa. India Arch. Agron. Soil Sci. 56, 237–263. Klironomos, J.N., 2003. Variation in plant response to native and exotic arbuscularmycorrizhal fungi. Ecology 84, 2292–2301. Kothamasi, D., Kuhad, R.C., Babu, C.R., 2001. Arbuscularmycorrhizae in plant survival strategies. Trop. Ecol. 42, 1–13. Leake, J., Johnson, D., Donnelly, D., Muckle, G., Boddy, L., Read, D., 2004. Networks of power and influence: the role of mycorrhizal mycelium in controlling plant communities and agroecosystem functioning. Can. J. Bot. 82, 1016–1030. Makus, D.J., 2004. Mycorrhizal inoculation of tomato and onion transplants improves earlines. Acta Hortic. 631, 275–281. Marschner, H., Dell, B., 1994. Nutrient uptake in mycorrhizal symbiosis. Plant Soil 159, 89–102.

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M.V. Vázquez-Hernández et al. / Scientia Horticulturae 128 (2011) 255–260

Mena-Violante, G.H., Ocampo-Jiménez, O., Dendooven, L., Martínez-Soto, G., ˜ González-Castaneda, J., Davies Jr., F., Olalde-Portugal, V., 2006. Arbuscular mycorrhizal fungi enhance fruit growth and quality of chileancho (Capsicum annuum L. cv San Luis) plants exposed to drought. Mycorrhiza 16, 261–267. Mueller, A., Franken, P., Schwarz, D., 2009. Nutrient uptake and fruit quality of tomato colonized with mycorrhizal fungus Glomus mosseae (BEG 12) under supply of nitrogen and phosphorus. Acta Hortic. 807, 383–388. Mukkun, L., Singh, Z., Phillips, D., 2001. Nitrogen nutrition affects fruit firmness, quality and shelf life of strawberry. Acta Hortic. 553, 69–71. Nakasone, H.Y., Paull, R.E., 1998. Tropical Fruits, first ed. CAB International, Wallingford, UK. Nava, G., Dechen, A.R., Nachtigall, G.R., 2008. Nitrogen and potassium fertilization affect apple fruit quality in southern Brazil. Comm. Soil Sci. Plant Anal. 39, 96–107. Olsen, S.R., Dean, L.A., 1965. Phosphorus. In: Black, C.A. (Ed.), Methods of Soil Analysis. Part 2. Agronomy Monograph 9. American Society of Agronomy, Madison, WI, USA, pp. 1035–1049. Pérez-Carrillo, E., Yahia, E.M., 2004. Effect of postharvest hot air and fungicide treatments on the quality of ‘Maradol’ papaya (Carica papaya L.). J. Food Qual. 27, 127–139. Phillips, J.M., Hayman, D.S., 1970. Improved procedures for clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. Trans. Br. Mycol. Soc. 55, 158–160. Pozo, M.J., Azcón-Aguilar, C., 2007. Unraveling mycorrhiza-induced resistance. Curr. Opin. Plant Biol. 10, 393–398. Quezada, C., Vidal, I., Lemus, L., Sánchez, H., 2007. Efecto de la fertilización nitrogenada sobre rendimiento y calidad de fruta en frambueso (RubusidaeusL.) bajo dos programas de fertirrigación. J. Soil Sci. Plant Nutr. 7, 1–15. Reuter, D.J., Robinson, J.B., 1986. Plant Analysis and Interpretation Manual. Inkata Press, Melboune, Sidney. Rufykiri, G., Declerck, S., Dufey, J.E., Delvaux, B., 2000. Arbuscular mycorrhizal fungi might alleviate aluminium toxicity in banana plants. New Phytol. 148, 343–352.

Sanders, F.E., Sheikh, N.A., 1983. The development of vesicular-arbuscular mycorrhizal infection in plant root systems. Plant Soil 71, 223–246. SAS, Institute INC., 2005. SAS (Statistycal Analysis System) the Institute INC, Cary, NC, USA, Versión 9.1.3. Schenck, N.C., Pérez, Y., 1990. Manual for the Identification of VA Mycorrhizal Fungi, third ed. Synergistic Publications, Gainesville, FL, USA. Sieverding, E., 1991. Vesicular-arbuscularmycorrhiza Management in Tropical Agrosystems. GTZ, Eschborn, Alemania. Sieverding, E., 1983. Manual de Métodos para la Investigación de la Micorriza Versículo Arbuscular en el Laboratorio. Centro Internacional de Agricultura Tropical, Colombia. Smith, S.E., Read, D.J., 1997. Mycorrhizal Symbiosis, second ed. Academic Press, London. SMN-CONAGUA, 2009. Servicio Meteorológico Nacional. Comisión Nacional del Agua. http://smn.cna.gob.mx/ (date 01.10.10). Strack, D., Fester, T., Hause, B., Schliemann, W., Walter, M.H., 2003. Arbuscularmycorrhiza: biological, chemical, and molecular aspects. J. Chem. Ecol. 29, 1955– 1979. Trindade, A.V., Siqueira, J.O., Stürmer, S.L., 2006. Arbuscular mycorrhizalfungi in papaya plantations of Espírito Santo and Bahia, Brazil. Braz. J. Microbiol. 37, 283–289. Villarreal, R.M., García, E.R.S., Osuna, E.T., Armenta, B.A.D., 2002. Efecto de dosis y fuente de nitrógeno en rendimiento y calidad postcosecha de tomate en fertirriego. Terra Latinoam. 20, 311–320. Wills, R.B.H., McGlasson, B., Graham, D., Joyce, D., 1998. Postharvest: An Introduction to the Physiology and Handling of Fruit, Vegetables and Ornamentals, fourth ed. CAB International, Washington, DC, USA. Wilson, J.M., 1984. Comparative development of infection by three vesiculararbuscular mycorrhizal fungi. New Phytol. 97, 413–426. Witham, F.H., Blaydes, D.F., Devlin, R.M., 1971. Experiments in Plant Physiology. Van Nostrand Reinhold, New York.