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Effects of Arbuscular Mycorrhizal Fungi and Bacteria on the Biocontrol of White Root Rot in Japanese Apricot Seedlings 



Andre Freire Cruz1,2*, William Rosa de Oliveira Soares2, Luiz Eduardo Bassay Blum2



1 Kyoto Prefectural University, Graduate School of Life and Environmental Sciences, 1-5 Shimogamohangi-cho, Sakyo-ku, Kyoto 606-8522, Japan. Fax: 81-75-7035694, E mail: HYPERLINK "mailto:andre@kpu.ac.jp"andre@kpu.ac.jp

2 Universidade de Bras�lia, Departamento de Fitopatologia, Campus Universit�rio Darcy Ribeiro, CEP 70910 900 Bras�lia, DF, Brazil 



*Corresponding author



Abstract
We conducted three experiments to evaluate the synergistic effect of the arbuscular mycorrhizal fungus (AMF) Gigaspora margarita and the bacterium Paenibacillus rhizospherae on the alleviation of white root rot in Japanese apricot (Prunus mume) seedlings. In the first experiment, seedlings of the cultivar �Nanko� were inoculated with 5, 10, or 20% of vermiculite:wheat bran (7:3), containing the pathogenic ascomycete Rosellinia necatrix (NRBC 5954). In the second experiment, �Nanko� seedlings were subjected to four treatments: Control (C), AMF (A), Bacteria (B), AMF+Bacteria (A+B). On the basis of the results of the first experiment, we used 10% of inoculum concentration in the second experiment and evaluated disease severity, root infection, and AMF colonization. In the third experiment, we evaluated the same biocontrol agents by using other fruit cuttings, viz. apple (Malus domestica �Marubakaido�), fig (Ficus carica �Masui dauphine�), and grapevine ( HYPERLINK "http://en.wikipedia.org/wiki/Vitis_vinifera" \o "Vitis vinifera" Vitis vinifera �5BB�). Inoculation with A and A+B alleviated the effects of R. necatrix, compared to the controls and single inoculations of B. AMF colonization decreased after R. necatrix inoculation in both AMF and A+B roots. The presence of bacteria increased AMF colonization before and after disease infection, but R. necatrix infection rate did not change according to the treatment. The effects of biocontrol agents varied among species. Grape seedlings were affected by the AMF and bacterium, but in apple and fig seedlings, alleviation was observed only in those plants inoculated with AMF and A+B.
Key words: Bacteria, Fruit, Japanese apricot, Mycorrhiza, Rosellinia necatrix



Introduction

The Japanese apricot (Prunus mume Zieb. et Zucc.), or �ume� in Japanese, is a commercial fruit tree whose fragrant �owers bloom very early in spring in Japan. It is renowned for its attractive blossoms and longevity in Asiatic countries, mainly China and Japan  ADDIN EN.CITE <EndNote><Cite><Author>Ning</Author><Year>2007</Year><RecNum>41</RecNum><DisplayText>(Ning et al. 2007)</DisplayText><record><rec-number>41</rec-number><foreign-keys><key app="EN" db-id="5xz0rp09t0xefkedfarvwes82vrsazzsvwsw">41</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Ning, G. G.</author><author>Bai, S. P.</author><author>Bao, M. Z.</author><author>Liu, L.</author></authors></contributors><titles><title>Factors affecting plantlet regeneration from in vitro cultured immature embryos and cotyledons of Prunus mume �Xue mei�</title><secondary-title>In Vitro Cellular &amp; Developmental Biology - Plant</secondary-title><alt-title>In Vitro Cell.Dev.Biol.-Plant</alt-title></titles><periodical><full-title>In Vitro Cellular &amp; Developmental Biology - Plant</full-title><abbr-1>In Vitro Cell.Dev.Biol.-Plant</abbr-1></periodical><alt-periodical><full-title>In Vitro Cellular &amp; Developmental Biology - Plant</full-title><abbr-1>In Vitro Cell.Dev.Biol.-Plant</abbr-1></alt-periodical><pages>95-100</pages><volume>43</volume><number>2</number><keywords><keyword>Cotyledons</keyword><keyword>Direct shoot regeneration</keyword><keyword>Immature embryos</keyword><keyword>Prunus mume</keyword><keyword>Organogenesis</keyword><keyword>Rooting</keyword></keywords><dates><year>2007</year><pub-dates><date>2007/04/01</date></pub-dates></dates><publisher>Springer-Verlag</publisher><isbn>1054-5476</isbn><urls><related-urls><url>http://dx.doi.org/10.1007/s11627-007-9035-8</url></related-urls></urls><electronic-resource-num>10.1007/s11627-007-9035-8</electronic-resource-num><language>English</language></record></Cite></EndNote>( HYPERLINK \l "_ENREF_20" \o "Ning, 2007 #41" Ning et al. 2007). In addition, this tree has medicinal properties and is used to treat vomiting and fever  ADDIN EN.CITE <EndNote><Cite><Author>Chen</Author><Year>1962</Year><RecNum>15</RecNum><DisplayText>(Chen 1962)</DisplayText><record><rec-number>15</rec-number><foreign-keys><key app="EN" db-id="5xz0rp09t0xefkedfarvwes82vrsazzsvwsw">15</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Chen, JY</author></authors></contributors><titles><title>Studies on Chinese Mei (Prunus mume Sieb. et Zucc) - The origin and cultivation history</title><secondary-title>Acta Hort Sin</secondary-title></titles><periodical><full-title>Acta Hort Sin</full-title></periodical><pages>69-78</pages><volume>1</volume><dates><year>1962</year></dates><urls></urls></record></Cite></EndNote>( HYPERLINK \l "_ENREF_5" \o "Chen, 1962 #15" Chen 1962). In Japan, processed foods made from the fruit, e.g., �umeboshi,� are popular and are traditionally considered to have miscellaneous medicinal benefits, such as antibacterial and fungicidal properties  ADDIN EN.CITE  ADDIN EN.CITE.DATA ( HYPERLINK \l "_ENREF_12" \o "Fujita, 2002 #17" Fujita et al. 2002;  HYPERLINK \l "_ENREF_20" \o "Ning, 2007 #41" Ning et al. 2007). Thus, there is a great interest in this fruit tree because of its economic importance, and any kind of damage, caused either by biotic or abiotic factors, is of concern to growers.
The ascomycete fungus Rosellinia necatrix Bearl ex Prill (anamorph: Demathophora necatrix Hartig) is an important, soil-borne root pathogen that affects a wide range of commercial fruit tree species, including almond (Prunus amygdalus), peach [Prunus persica (L.) Batsch], plum (Prunus domestica L.), apple (Malus domestica Borkh.), pear (Pyrus communis L.), olive (Olea europaea L. subsp. europaea), cherry (Prunus avium L.), avocado (Persea americana Mill.), grapevine (Vitus vinifera L.), and the Japanese apricot. It is the causal agent of the white root rot disease, and host plants infected by the fungus quickly wilt and die. In Japan, this disease, which spreads rapidly, is very difficult to prevent  ADDIN EN.CITE  ADDIN EN.CITE.DATA ( HYPERLINK \l "_ENREF_16" \o "Kanda, 2003 #11" Kanda et al. 2003;  HYPERLINK \l "_ENREF_29" \o "ten Hoopen, 2006 #13" ten Hoopen and Krauss 2006). Dispersal occurs in the soil, mostly on dead wood, because of the high saprophytic ability of the fungus. The fungus attacks the roots and crowns of plants and can penetrate woody roots by invasion of aggregate organs; by doing this, it causes the disease mainly in woody plants, but also in bulbs and rhizomes  ADDIN EN.CITE <EndNote><Cite><Author>Delatour</Author><Year>1985</Year><RecNum>7</RecNum><DisplayText>(Delatour and Guillaumin 1985)</DisplayText><record><rec-number>7</rec-number><foreign-keys><key app="EN" db-id="5xz0rp09t0xefkedfarvwes82vrsazzsvwsw">7</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Delatour, C.</author><author>Guillaumin, J. J.</author></authors></contributors><titles><title>Importance des pourridies dans les r�gions temp�r�es</title><secondary-title>European Journal of Forest Pathology</secondary-title></titles><periodical><full-title>European Journal of Forest Pathology</full-title></periodical><pages>258-263</pages><volume>15</volume><number>5-6</number><dates><year>1985</year></dates><publisher>Blackwell Publishing Ltd</publisher><isbn>1439-0329</isbn><urls><related-urls><url>http://dx.doi.org/10.1111/j.1439-0329.1985.tb01097.x</url></related-urls></urls><electronic-resource-num>10.1111/j.1439-0329.1985.tb01097.x</electronic-resource-num></record></Cite></EndNote>( HYPERLINK \l "_ENREF_10" \o "Delatour, 1985 #7" Delatour and Guillaumin 1985). Normally, symptoms of the disease consist of collar and root rot (which result in different degrees of canopy decline), followed by leaf drop, wilting, and death of the tree  ADDIN EN.CITE  ADDIN EN.CITE.DATA ( HYPERLINK \l "_ENREF_25" \o "Schena, 2002 #12" Schena et al. 2002;  HYPERLINK \l "_ENREF_29" \o "ten Hoopen, 2006 #13" ten Hoopen and Krauss 2006). In Japan, economical losses attributed to R. necatrix can reach US$ 4 million per year for greenhouse grapevines in Okayama Prefecture and similar losses for Japanese pear [Pyrus pyrifolia (Burm.) Nak] in Saga Prefecture  ADDIN EN.CITE <EndNote><Cite><Author>ten Hoopen</Author><Year>2006</Year><RecNum>13</RecNum><DisplayText>(ten Hoopen and Krauss 2006)</DisplayText><record><rec-number>13</rec-number><foreign-keys><key app="EN" db-id="5xz0rp09t0xefkedfarvwes82vrsazzsvwsw">13</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>ten Hoopen, G. Martijn</author><author>Krauss, Ulrike</author></authors></contributors><titles><title>Biology and control of Rosellinia bunodes, Rosellinia necatrix and Rosellinia pepo: A review</title><secondary-title>Crop Protection</secondary-title></titles><periodical><full-title>Crop Protection</full-title></periodical><pages>89-107</pages><volume>25</volume><number>2</number><keywords><keyword>Biological control</keyword><keyword>Chemical control</keyword><keyword>Clonostachys spp.</keyword><keyword>Cultural control</keyword><keyword>Dematophora necatrix</keyword><keyword>Fungicides</keyword><keyword>Genetic resistance</keyword><keyword>Root pathogen</keyword><keyword>Rosellinia arcuata</keyword><keyword>Rosellinia bunodes</keyword><keyword>Rosellinia necatrix</keyword><keyword>Rosellinia pepo</keyword><keyword>Rosellinia spp.</keyword><keyword>Soil-borne pathogen</keyword><keyword>Solarization</keyword><keyword>Trichoderma spp.</keyword></keywords><dates><year>2006</year><pub-dates><date>2//</date></pub-dates></dates><isbn>0261-2194</isbn><urls><related-urls><url>http://www.sciencedirect.com/science/article/pii/S0261219405001109</url></related-urls></urls><electronic-resource-num>http://dx.doi.org/10.1016/j.cropro.2005.03.009</electronic-resource-num></record></Cite></EndNote>( HYPERLINK \l "_ENREF_29" \o "ten Hoopen, 2006 #13" ten Hoopen and Krauss 2006). Furthermore, we believe that there are similar losses in P. mume, because of its common occurrence in Japan. Several approaches may be attempted for the control of white root rot, but control is very difficult mainly because the different chemical treatments are not sufficiently effective. However, biological control appears to be a suitable alternative, and therefore, it is an important tool in integrated disease management. 
The effects of the association of arbuscular mycorrhizal fungi (AMF) and bacteria on plant disease control have been well documented. AMF live as obligate symbionts with the roots of about 80% of land plants, and this symbiotic relationship exists in most natural and agricultural ecosystems  ADDIN EN.CITE  ADDIN EN.CITE.DATA ( HYPERLINK \l "_ENREF_1" \o "Azc�n-Aguilar, 1997 #21" Azc�n-Aguilar and Barea 1997;  HYPERLINK \l "_ENREF_26" \o "St-Arnaud, 1994 #20" St-Arnaud et al. 1994). AMF play an important function in the reduction of plant pathogens  ADDIN EN.CITE  ADDIN EN.CITE.DATA ( HYPERLINK \l "_ENREF_1" \o "Azc�n-Aguilar, 1997 #21" Azc�n-Aguilar and Barea 1997;  HYPERLINK \l "_ENREF_26" \o "St-Arnaud, 1994 #20" St-Arnaud et al. 1994;  HYPERLINK \l "_ENREF_32" \o "Willis, 2005 #4" Willis and Memmott 2005), such as the fungi Rhizoctonia solani K�hn  ADDIN EN.CITE <EndNote><Cite><Author>Yao</Author><Year>2002</Year><RecNum>22</RecNum><DisplayText>(Yao et al. 2002)</DisplayText><record><rec-number>22</rec-number><foreign-keys><key app="EN" db-id="5xz0rp09t0xefkedfarvwes82vrsazzsvwsw">22</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Yao, M.</author><author>Tweddell, R.</author><author>D�silets, H.</author></authors></contributors><titles><title>Effect of two vesicular-arbuscular mycorrhizal fungi on the growth of micropropagated potato plantlets and on the extent of disease caused by Rhizoctonia solani</title><secondary-title>Mycorrhiza</secondary-title><alt-title>Mycorrhiza</alt-title></titles><periodical><full-title>Mycorrhiza</full-title><abbr-1>Mycorrhiza</abbr-1></periodical><alt-periodical><full-title>Mycorrhiza</full-title><abbr-1>Mycorrhiza</abbr-1></alt-periodical><pages>235-242</pages><volume>12</volume><number>5</number><keywords><keyword>Solanum tuberosum Vesicular-arbuscular mycorrhiza Rhizoctonia solani Glomus etunicatum Glomus intraradices</keyword></keywords><dates><year>2002</year><pub-dates><date>2002/10/01</date></pub-dates></dates><publisher>Springer-Verlag</publisher><isbn>0940-6360</isbn><urls><related-urls><url>http://dx.doi.org/10.1007/s00572-002-0176-7</url></related-urls></urls><electronic-resource-num>10.1007/s00572-002-0176-7</electronic-resource-num><language>English</language></record></Cite></EndNote>( HYPERLINK \l "_ENREF_33" \o "Yao, 2002 #22" Yao et al. 2002), Pythium ultimum Trow, and Phytophthora spp.  ADDIN EN.CITE  ADDIN EN.CITE.DATA ( HYPERLINK \l "_ENREF_6" \o "Cordier, 1996 #24" Cordier et al. 1996;  HYPERLINK \l "_ENREF_30" \o "Trotta, 1996 #23" Trotta et al. 1996). In different crops, AMF have also been shown to reduce bacterial diseases  ADDIN EN.CITE <EndNote><Cite><Author>Dehne</Author><Year>1982</Year><RecNum>25</RecNum><DisplayText>(Dehne 1982)</DisplayText><record><rec-number>25</rec-number><foreign-keys><key app="EN" db-id="5xz0rp09t0xefkedfarvwes82vrsazzsvwsw">25</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Dehne, HW</author></authors></contributors><titles><title> Interaction between vesicular-arbuscular mycorrhizal fungi and plant pathogens</title><secondary-title>Phytopathology</secondary-title></titles><periodical><full-title>Phytopathology</full-title></periodical><pages>1115-1119</pages><volume>72</volume><dates><year>1982</year></dates><urls></urls></record></Cite></EndNote>( HYPERLINK \l "_ENREF_9" \o "Dehne, 1982 #25" Dehne 1982); for example, the AMF Glomus mosseae (Nicol. & Gerd.) Gerd. & Trap. suppressed Ralstonia solanacearum (Smith) Yabuuchi et al., a bacterial wilt-causing organism in tomato plants  ADDIN EN.CITE <EndNote><Cite><Author>Tahat</Author><Year>2008</Year><RecNum>26</RecNum><DisplayText>(Tahat et al. 2008)</DisplayText><record><rec-number>26</rec-number><foreign-keys><key app="EN" db-id="5xz0rp09t0xefkedfarvwes82vrsazzsvwsw">26</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Tahat, MM </author><author>Kamaruzaman, S</author><author>Radziah, O</author><author>Kadir, J</author><author>Masdek, HN</author></authors></contributors><titles><title>Response of (Lycopersicum esculentum Mill.) to Different Arbuscular Mycorrhizal Fungi Species</title><secondary-title>Asian Journal of Plant Sciences</secondary-title></titles><periodical><full-title>Asian Journal of Plant Sciences</full-title></periodical><pages>479-484</pages><volume>7</volume><dates><year>2008</year></dates><urls></urls></record></Cite></EndNote>( HYPERLINK \l "_ENREF_28" \o "Tahat, 2008 #26" Tahat et al. 2008). In parallel to AMF, soil bacteria should be considered as biocontrol agents. Recently, some bacteria associated with the spores of Gigaspora margarita Becker & Hall, such as Paenibacillus polymyxa, Janthinobacterium lividum, and members of the genus Bacillus, were able to suppress diseases (antagonism) and solubilize P  ADDIN EN.CITE  ADDIN EN.CITE.DATA ( HYPERLINK \l "_ENREF_7" \o "Cruz, 2008 #10" Cruz et al. 2008;  HYPERLINK \l "_ENREF_8" \o "Cruz, 2011 #8" Cruz and Ishii 2011). Paenibacillus sp. strain B2, isolated from the mycorrhizosphere of Sorghum bicolor (L.) Moench., inoculated with G. mosseae may have antagonistic effects on soil-borne pathogens and may stimulate mycorrhization  ADDIN EN.CITE <EndNote><Cite><Author>Budi</Author><Year>1999</Year><RecNum>9</RecNum><DisplayText>(Budi et al. 1999)</DisplayText><record><rec-number>9</rec-number><foreign-keys><key app="EN" db-id="5xz0rp09t0xefkedfarvwes82vrsazzsvwsw">9</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Budi, S. W.</author><author>van Tuinen, D.</author><author>Martinotti, G.</author><author>Gianinazzi, S.</author></authors></contributors><titles><title>Isolation from the Sorghum bicolorMycorrhizosphere of a Bacterium Compatible with Arbuscular Mycorrhiza Development and Antagonistic towards Soilborne Fungal Pathogens</title><secondary-title>Applied and Environmental Microbiology</secondary-title></titles><periodical><full-title>Applied and Environmental Microbiology</full-title></periodical><pages>5148-5150</pages><volume>65</volume><number>11</number><dates><year>1999</year><pub-dates><date>November 1, 1999</date></pub-dates></dates><urls><related-urls><url>http://aem.asm.org/content/65/11/5148.abstract</url></related-urls></urls></record></Cite></EndNote>( HYPERLINK \l "_ENREF_4" \o "Budi, 1999 #9" Budi et al. 1999).
Because AMF are major components of the rhizosphere of plants, they significantly affect the incidence and severity of root diseases, which can contribute to root disease suppression in a number of ways, including improvement of nutrient uptake and competition for space  ADDIN EN.CITE <EndNote><Cite><Author>MM</Author><Year>2008</Year><RecNum>26</RecNum><DisplayText>(Tahat et al. 2008; Tahat et al. 2010)</DisplayText><record><rec-number>26</rec-number><foreign-keys><key app="EN" db-id="5xz0rp09t0xefkedfarvwes82vrsazzsvwsw">26</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Tahat, MM </author><author>Kamaruzaman, S</author><author>Radziah, O</author><author>Kadir, J</author><author>Masdek, HN</author></authors></contributors><titles><title>Response of (Lycopersicum esculentum Mill.) to Different Arbuscular Mycorrhizal Fungi Species</title><secondary-title>Asian Journal of Plant Sciences</secondary-title></titles><periodical><full-title>Asian Journal of Plant Sciences</full-title></periodical><pages>479-484</pages><volume>7</volume><dates><year>2008</year></dates><urls></urls></record></Cite><Cite><Author>MM</Author><Year>2010</Year><RecNum>27</RecNum><record><rec-number>27</rec-number><foreign-keys><key app="EN" db-id="5xz0rp09t0xefkedfarvwes82vrsazzsvwsw">27</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Tahat, MM</author><author>Kamaruzaman, S</author><author>Othman, R</author></authors></contributors><titles><title>Mycorrhizal Fungi as a Biocontrol Agent</title><secondary-title>Plant Pathology Journal</secondary-title></titles><periodical><full-title>Plant Pathology Journal</full-title></periodical><pages>198-207</pages><volume>9</volume><dates><year>2010</year></dates><urls></urls><electronic-resource-num>10.3923/ppj.2010.198.207</electronic-resource-num></record></Cite></EndNote>( HYPERLINK \l "_ENREF_28" \o "Tahat, 2008 #26" Tahat et al. 2008;  HYPERLINK \l "_ENREF_27" \o "Tahat, 2010 #27" Tahat et al. 2010). Mycorrhizal plants may also better tolerate environmental stresses, such as drought, that could predispose them to more severe fungal pathogen infections  ADDIN EN.CITE <EndNote><Cite><Author>KG</Author><Year>2002</Year><RecNum>28</RecNum><DisplayText>(Mukerji et al. 2002)</DisplayText><record><rec-number>28</rec-number><foreign-keys><key app="EN" db-id="5xz0rp09t0xefkedfarvwes82vrsazzsvwsw">28</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Mukerji, KG</author><author>Manoharachary, C</author><author>Chamola, BP</author></authors></contributors><titles><title>Techniques in Mycorrhizal Studies</title></titles><pages>285-296</pages><dates><year>2002</year></dates><pub-location>London-Netherlands</pub-location><publisher>Kluwer Academic Publishers</publisher><urls></urls></record></Cite></EndNote>( HYPERLINK \l "_ENREF_18" \o "Mukerji, 2002 #28" Mukerji et al. 2002). Other mechanisms have been reported to explain biocontrol by AMF, including biochemical changes in plant tissues, microbial changes in the rhizosphere, nutrient status, anatomical changes to cells, changes to root system morphology, and stress alleviation  ADDIN EN.CITE <EndNote><Cite><Author>Hooker</Author><Year>1994</Year><RecNum>29</RecNum><DisplayText>(Hooker et al. 1994)</DisplayText><record><rec-number>29</rec-number><foreign-keys><key app="EN" db-id="5xz0rp09t0xefkedfarvwes82vrsazzsvwsw">29</key></foreign-keys><ref-type name="Book Section">5</ref-type><contributors><authors><author>Hooker, JE</author><author>Jaizme-Vega, M</author><author>Alkinson, D</author></authors><secondary-authors><author>Gianinazzi S</author><author>Schhepp H</author></secondary-authors></contributors><titles><title>Biocontrol of Plant Pathogen Using Arbuscular Mycorrhizal Fungi</title><secondary-title>Impact of Arbuscular Mycorrhizas on Sustainable Agriculture and Natural Ecosystems</secondary-title></titles><pages>191-209</pages><dates><year>1994</year></dates><pub-location>Basle, Switzerland</pub-location><publisher>Birkhauser Verlag</publisher><urls></urls></record></Cite></EndNote>( HYPERLINK \l "_ENREF_14" \o "Hooker, 1994 #29" Hooker et al. 1994).
Extracts of rhizosphere soil from mycorrhizal plants reduced sporangia formation in Phytophthora cinnamomi Rands in comparison with extracts of rhizosphere soil from non-mycorrhizal plants  ADDIN EN.CITE <EndNote><Cite><Author>Meyer</Author><Year>1986</Year><RecNum>30</RecNum><DisplayText>(Meyer and Linderman 1986)</DisplayText><record><rec-number>30</rec-number><foreign-keys><key app="EN" db-id="5xz0rp09t0xefkedfarvwes82vrsazzsvwsw">30</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Meyer, Julie R.</author><author>Linderman, R. G.</author></authors></contributors><titles><title>Selective influence on populations of rhizosphere or rhizoplane bacteria and actinomycetes by mycorrhizas formed by Glomus fasciculatum</title><secondary-title>Soil Biology and Biochemistry</secondary-title></titles><periodical><full-title>Soil Biology and Biochemistry</full-title></periodical><pages>191-196</pages><volume>18</volume><number>2</number><dates><year>1986</year><pub-dates><date>//</date></pub-dates></dates><isbn>0038-0717</isbn><urls><related-urls><url>http://www.sciencedirect.com/science/article/pii/003807178690026X</url></related-urls></urls><electronic-resource-num>http://dx.doi.org/10.1016/0038-0717(86)90026-X</electronic-resource-num></record></Cite></EndNote>( HYPERLINK \l "_ENREF_17" \o "Meyer, 1986 #30" Meyer and Linderman 1986). The authors also found that sporulation-inducing microorganisms were missing or that the number of sporulation-inhibiting microorganisms increased. In our study, we aimed to investigate the effects of AMF and associated bacteria on the biocontrol of white root rot in Japanese apricot seedlings.
Materials & Methods
Experiment I � Inoculum test
Seedlings of 2-year-old Japanese apricot cultivar �Nanko� were used in this assay. The inoculants were prepared by autoclaving 500-mL plastic pots containing a wet mixture of vermiculite:wheat bran (7:3), placed diagonally to guarantee a larger area for fungal growth  ADDIN EN.CITE <EndNote><Cite><Author>PERC</Author><Year>2005</Year><RecNum>31</RecNum><DisplayText>(PERC 2005)</DisplayText><record><rec-number>31</rec-number><foreign-keys><key app="EN" db-id="5xz0rp09t0xefkedfarvwes82vrsazzsvwsw">31</key></foreign-keys><ref-type name="Edited Book">28</ref-type><contributors><authors><author>PERC, Annual Report</author></authors></contributors><titles><title>Development of technology to recover tree vigor and the causes of plum decline - Practice and evaluation of plant pathology in the field</title></titles><pages>204</pages><volume>1</volume><dates><year>2005</year></dates><pub-location>Kyoto, Japan</pub-location><publisher>Plant and Environment Research Center</publisher><urls></urls></record></Cite></EndNote>( HYPERLINK \l "_ENREF_22" \o "PERC, 2005 #31" PERC 2005). The fungus R. necatrix (NRBC 5954), previously grown on PDA media, was placed on this mixture and kept in the dark at 25�C for 45 d. Controls were prepared with the same mixture and media without the fungi. When the mycelium visually covered the whole pot, the inoculant was sieved (4 mm) and mixed with the substrate composed of vermiculite:cell soil:�akadam� soil:�hyouga� soil (2:1:1:1). The control (without the pathogen) pots were treated in a similar manner by using the control inoculants with only PDA media.
 Three concentrations of the inoculum (5, 10, and 20%) were prepared with 3 replicates (composed of 12 seedlings in total), which were grown in 4-L pots in a greenhouse. The disease symptoms started to appear 4 d after inoculation, and the experiment ended when the plants of one treatment wilted completely. The roots and shoots were photographed before the inoculation and at the time of harvesting to evaluate disease severity. 

Experiment II � Effect of AMF and bacteria on the biocontrol of white root rot in Japanese apricot seedlings
Cuttings (height, 15 cm; diameter, 5 mm) of the Japanese apricot cultivar �Nanko� were inserted in trays containing vermiculite for rooting. After 90 d, when the leaves were well-developed, cuttings with similar appearance were transplanted into 3.5-L pots containing the following treatments: Control (C), AMF (A), Bacteria (B), or AMF+Bacteria (A+B). Spores (n = 50) of the AMF G. margarita (Central Glass Co., Tokyo, Japan) were inserted into each pot. The bacterium Paenibacillus rhizospherae, previously isolated from G. margarita spores  ADDIN EN.CITE <EndNote><Cite><Author>Cruz</Author><Year>2011</Year><RecNum>8</RecNum><DisplayText>(Cruz and Ishii 2011)</DisplayText><record><rec-number>8</rec-number><foreign-keys><key app="EN" db-id="5xz0rp09t0xefkedfarvwes82vrsazzsvwsw">8</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Cruz, Andre Freire</author><author>Ishii, Takaaki</author></authors></contributors><titles><title>Arbuscular mycorrhizal fungal spores host bacteria that affect nutrient biodynamics and biocontrol of soil borne plant pathogens</title><secondary-title>Biology Open</secondary-title></titles><periodical><full-title>Biology Open</full-title></periodical><dates><year>2011</year><pub-dates><date>November 1, 2011</date></pub-dates></dates><urls><related-urls><url>http://bio.biologists.org/content/early/2011/10/21/bio.2011014.abstract</url></related-urls></urls><electronic-resource-num>10.1242/bio.2011014</electronic-resource-num></record></Cite></EndNote>( HYPERLINK \l "_ENREF_8" \o "Cruz, 2011 #8" Cruz and Ishii 2011), at a concentration of 3 � 108 colony-forming units (CFU) was also added to the pots. Four replicates for each treatment were prepared, comprising 16 plants in total.
The pots were grown in a greenhouse for 1 year, and then, R. necatrix was inoculated into the substrates, similar to Experiment I. An inoculum concentration of 10% was chosen in order to achieve adequate levels of infection and to observe the effects of the antagonistic microorganisms (AMF, bacteria). After 3 weeks, the experiment was terminated. Photographs and root samples were taken before and after inoculation with R. necatrix. Disease severity was evaluated by visual diagnosis, according to the following scale: 0 = no symptoms; 1 = slightly damaged; 2 = moderately damaged; 3 = strongly damaged; 4 = completely wilted. 
Roots were stained to evaluate the AMF colonization and R. necatrix infection rate, using the following procedures. Roots were cleansed using running tap water and fixed in FAA solution containing formalin (130 mL), acetic acid (50 mL), and ethanol (50%) (2 L). The roots were treated with 10% KOH for 24 h at room temperature, followed by 1 h at 90�C. They were further bleached with 10% H2O2 (1 h, room temperature). The roots were then treated with 10% HCl (v/v) (10 min, room temperature) and stained for 15 min in trypan blue (0.05% in lactic acid) at 90�C. Excess stain was removed with lactic acid, in which the samples were stored for microscopic analysis. The roots were placed on glass slides and observed using an optical microscope (100�), and those that showed AMF (hyphae and/or arbuscules) were considered. The percentage of colonization was determined according to the following equation: (% AMF) = (SA/TA) � 100, where % AMF is the percentage of colonization by AMF; SA is the number of sites with AMF; and TA is the total number of sites. A similar procedure was used to evaluate the disease in roots, where sites with septate hyphae were considered infected.

Experiment III � Observation of the effects of the biocontrol agents in other fruit seedlings
As in Experiment II, other fruit cuttings, viz. apple (�Marubakaido�), fig (Ficus carica �Masui dauphine�), and grapevine ( HYPERLINK "http://en.wikipedia.org/wiki/Vitis_vinifera" \o "Vitis vinifera" Vitis vinifera �5BB�), were inserted in trays and transplanted to 1-L pots containing the substrate and biocontrol agents. After 1 year, R. necatrix was inoculated into the substrates, and disease severity was evaluated after 2 weeks.

Results and Discussion
Experiment I
As demonstrated by the photographs of the shoots and roots, our inoculum formula caused the infection of roots (Fig. 1a), which resulted in plant damage (Fig. 1b). Even the smallest concentration (5%) was sufficient for infecting the roots. The presence of septate hyphae inside roots confirmed infection by the inoculated pathogens; these hyphae were not found in the roots of plants in the control pots. The hyphae were intercellular or intracellular. The photographs of the shoots and roots proved the pathogenicity of the fungi. In the infected pots, leaves wilted before dropping. Moreover, the dark color of the infected roots associated with a low number of new roots was clearly different from those in the control pots, which showed an abundance of new roots.
Disease severity after 2 weeks increased proportionally to the inoculum concentration, i.e., the inoculum at 20% was the most severe. Therefore, using the criteria for infection efficiency and the effect of antagonistic microorganisms, we chose a concentration of 10% for Experiments II and III.

Experiment II
Damage caused by R. necatrix in Japanese apricot seedlings was similarly severe in plants inoculated with A and A+B, but less than that in the control and B alone. The B treatment alone did not alleviate the effects of the disease in the seedlings (Table 1). AMF colonization was not found in the control and treatment B pots, and the percentage of colonization decreased after R. necatrix inoculation in both A and A+B roots. The presence of bacteria increased AMF colonization before and after disease infection (Table 1), but R. necatrix infection rate did not change according to the treatment. New roots were abundant in A and A+B pots, but were almost absent in the control pots.
Many studies have investigated the biocontrol of soil-borne diseases by AMF and bacteria. Five isolates of Trichoderma atroviride Karst and one isolate each of Trichoderma virens (Miller et al.) von Arx, Trichoderma harzianum Rifai, and Trichoderma cerinum Bissett, Kubicek & Szakacs controlled white root rot in vivo  ADDIN EN.CITE <EndNote><Cite><Author>Ruano-Rosa</Author><Year>2009</Year><RecNum>32</RecNum><DisplayText>(Ruano-Rosa and L�pez-Herrera 2009)</DisplayText><record><rec-number>32</rec-number><foreign-keys><key app="EN" db-id="5xz0rp09t0xefkedfarvwes82vrsazzsvwsw">32</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Ruano-Rosa, D</author><author>L�pez-Herrera, CJ</author></authors></contributors><titles><title>Evaluation of Trichoderma spp. as biocontrol agents against avocado white root rot</title><secondary-title>Biological Control</secondary-title></titles><periodical><full-title>Biological Control</full-title></periodical><pages>66-71</pages><volume>51</volume><number>1</number><keywords><keyword>Incompatibility in vitro</keyword><keyword>Control in vivo</keyword><keyword>Persea americana</keyword><keyword>Rosellinia necatrix</keyword><keyword>Avocado white rot</keyword><keyword>Trichoderma spp.</keyword></keywords><dates><year>2009</year><pub-dates><date>10//</date></pub-dates></dates><isbn>1049-9644</isbn><urls><related-urls><url>http://www.sciencedirect.com/science/article/pii/S1049964409001352</url></related-urls></urls><electronic-resource-num>http://dx.doi.org/10.1016/j.biocontrol.2009.05.005</electronic-resource-num></record></Cite></EndNote>( HYPERLINK \l "_ENREF_23" \o "Ruano-Rosa, 2009 #32" Ruano-Rosa and L�pez-Herrera 2009). The application of a combination of AMF and Bacillus subtilis Cohn reduced the root rot caused by Fusarium solani (Mart.) Sacc. in geranium (Pelargonium gravealens L.)  ADDIN EN.CITE <EndNote><Cite><Author>MH</Author><Year>2001</Year><RecNum>33</RecNum><DisplayText>(Wafaa and Abdel-latif 2001)</DisplayText><record><rec-number>33</rec-number><foreign-keys><key app="EN" db-id="5xz0rp09t0xefkedfarvwes82vrsazzsvwsw">33</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Wafaa, MH</author><author>Abdel-latif, FM</author></authors></contributors><titles><title>Interaction Between Vasicular Arbuscular Mycorrhizae and Antagonistic Biocontrol Micro-organisms on Controlling Root-rot Disease Incidence of Geranium Plants</title><secondary-title>Journal of Biological Sciences</secondary-title></titles><periodical><full-title>Journal of Biological Sciences</full-title></periodical><pages>1147-1153</pages><volume>1</volume><dates><year>2001</year></dates><urls></urls></record></Cite></EndNote>( HYPERLINK \l "_ENREF_31" \o "Wafaa, 2001 #33" Wafaa and Abdel-latif 2001). In contrast, Glomus intraradices Schenck & Sm and Burkholderia cepacia reduced the population density of Pythium ultimum and the biomass of B. cepacia was inhibited by the presence of mycelium of G. intraradices, suggesting that combining both agents did not enhance the biocontrol efficacy against P. ultimum compared to a single inoculation of AMF. 
Furthermore, the AMF Glomus intraradices and the rhizobacterium Pseudomonas fluorescens Migula significantly inhibited the development of the tomato leaf-speck disease caused by Pseudomonas syringae pv. tomato  ADDIN EN.CITE <EndNote><Cite><Author>SF</Author><Year>2003</Year><RecNum>34</RecNum><DisplayText>(Salem 2003)</DisplayText><record><rec-number>34</rec-number><foreign-keys><key app="EN" db-id="5xz0rp09t0xefkedfarvwes82vrsazzsvwsw">34</key></foreign-keys><ref-type name="Thesis">32</ref-type><contributors><authors><author>Salem, SF</author></authors></contributors><titles><title>Impact of mycorrhizal fungi and other symbiotic microbes as biocontrol agents on soil borne pathogens and some ecophysiological changes in tomato roots</title></titles><pages>41</pages><volume>PhD</volume><dates><year>2003</year></dates><pub-location>Godollo-Turkey</pub-location><publisher>Szentistvan University</publisher><urls><related-urls><url>https://szie.hu//file/tti/archivum/Saadallah_ertekezes.pdf</url></related-urls></urls></record></Cite></EndNote>( HYPERLINK \l "_ENREF_24" \o "Salem, 2003 #34" Salem 2003). Phytophthora parasitica Dastur proliferation greatly reduced in tomato roots colonized by Glomus mosseae  ADDIN EN.CITE <EndNote><Cite><Author>Cordier</Author><Year>1996</Year><RecNum>24</RecNum><DisplayText>(Cordier et al. 1996)</DisplayText><record><rec-number>24</rec-number><foreign-keys><key app="EN" db-id="5xz0rp09t0xefkedfarvwes82vrsazzsvwsw">24</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Cordier, C.</author><author>Gianinazzi, S.</author><author>Gianinazzi-Pearson, V.</author></authors></contributors><titles><title>Colonisation patterns of root tissues byPhytophthora nicotianae var.parasitica related to reduced disease in mycorrhizal tomato</title><secondary-title>Plant and Soil</secondary-title><alt-title>Plant Soil</alt-title></titles><periodical><full-title>Plant and Soil</full-title><abbr-1>Plant and Soil</abbr-1></periodical><pages>223-232</pages><volume>185</volume><number>2</number><keywords><keyword>biocontrol</keyword><keyword>G. mosseae</keyword><keyword>immunocytochemistry</keyword><keyword>P. nicotianae var.parasitica</keyword><keyword>tomato</keyword></keywords><dates><year>1996</year><pub-dates><date>1996/09/01</date></pub-dates></dates><publisher>Kluwer Academic Publishers</publisher><isbn>0032-079X</isbn><urls><related-urls><url>http://dx.doi.org/10.1007/BF02257527</url></related-urls></urls><electronic-resource-num>10.1007/BF02257527</electronic-resource-num><language>English</language></record></Cite></EndNote>( HYPERLINK \l "_ENREF_6" \o "Cordier, 1996 #24" Cordier et al. 1996) HYPERLINK "http://scialert.net/fulltext/?doi=ppj.2010.198.207&org=11" \l "190859_ja" . The beneficial microorganisms, including antagonistic bacteria (e.g., P. fluorescens,  HYPERLINK "http://www.scialert.net/asci/result.php?searchin=Keywords&cat=&ascicat=ALL&Submit=Search&keyword=Bacillus+subtilis" \o "" \t "_blank" B. subtilis) and fungi (e.g., AMF, Trichoderma), compete with plant pathogens for nutrients and space by producing antibiotics, parasitizing pathogens, or inducing resistance in the host plants. 
Few data are available on the compatibility between these microorganisms and AMF. Reports have indicated that biocontrol agents, like gram-negative Pseudomonas strains, do not have inhibitory effects on AM formation  ADDIN EN.CITE  ADDIN EN.CITE.DATA ( HYPERLINK \l "_ENREF_21" \o "Paulitz, 1989 #35" Paulitz and Linderman 1989;  HYPERLINK \l "_ENREF_2" \o "Barea, 1998 #36" Barea et al. 1998). Similarly, some Rhizobium leguminosarum strains have been reported to induce defense responses against Orobanche crenata Forsk in pea plants through activation of the oxidative process and production of possible toxic compounds, including phenolics  ADDIN EN.CITE <EndNote><Cite><Author>M�ller-St�ver</Author><Year>2005</Year><RecNum>5</RecNum><DisplayText>(M�ller-St�ver and Kroschel 2005)</DisplayText><record><rec-number>5</rec-number><foreign-keys><key app="EN" db-id="5xz0rp09t0xefkedfarvwes82vrsazzsvwsw">5</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>M�ller-St�ver, Dorette</author><author>Kroschel, J�rgen</author></authors></contributors><titles><title>The potential of Ulocladium botrytis for biological control of Orobanche spp</title><secondary-title>Biological Control</secondary-title></titles><periodical><full-title>Biological Control</full-title></periodical><pages>301-306</pages><volume>33</volume><number>3</number><keywords><keyword>Ulocladium botrytis</keyword><keyword>Orobanche crenata</keyword><keyword>Orobanche cumana</keyword><keyword>Orobanche aegyptiaca</keyword><keyword>Biological control</keyword><keyword>Mycoherbicide</keyword></keywords><dates><year>2005</year><pub-dates><date>6//</date></pub-dates></dates><isbn>1049-9644</isbn><urls><related-urls><url>http://www.sciencedirect.com/science/article/pii/S1049964405000599</url></related-urls></urls><electronic-resource-num>http://dx.doi.org/10.1016/j.biocontrol.2005.03.006</electronic-resource-num></record></Cite></EndNote>( HYPERLINK \l "_ENREF_19" \o "M�ller-St�ver, 2005 #5" M�ller-St�ver and Kroschel 2005). Improved nutrient status as a consequence of mycorrhizal and bacterial colonization can also result in enhanced protection against pathogens  ADDIN EN.CITE <EndNote><Cite><Author>Borowicz</Author><Year>2001</Year><RecNum>3</RecNum><DisplayText>(Borowicz 2001)</DisplayText><record><rec-number>3</rec-number><foreign-keys><key app="EN" db-id="5xz0rp09t0xefkedfarvwes82vrsazzsvwsw">3</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Borowicz, Victoria A.</author></authors></contributors><titles><title>Do Arbuscular Mycorrhizal Fungi Alter Plant-Pathogen Relations?</title><secondary-title>Ecology</secondary-title></titles><periodical><full-title>Ecology</full-title></periodical><pages>3057-3068</pages><volume>82</volume><number>11</number><dates><year>2001</year></dates><publisher>Ecological Society of America</publisher><isbn>00129658</isbn><urls><related-urls><url>http://www.jstor.org/stable/2679834</url></related-urls></urls><electronic-resource-num>10.2307/2679834</electronic-resource-num></record></Cite></EndNote>( HYPERLINK \l "_ENREF_3" \o "Borowicz, 2001 #3" Borowicz 2001). The inhibitory effects of the bacterial strains applied to fava beans could be attributed to a direct effect of the bacteria on the seeds or indirectly through the production of chemical(s) that is/are (1) toxic to the seeds; (2) inhibitors of ethylene biosynthesis; (3) inhibitors of ethylene action; (4) promoters of ethylene deactivation; and (5) promoters of ethylene biosynthesis  ADDIN EN.CITE <EndNote><Cite><Author>Imaseki</Author><Year>1991</Year><RecNum>1</RecNum><DisplayText>(Imaseki 1991)</DisplayText><record><rec-number>1</rec-number><foreign-keys><key app="EN" db-id="5xz0rp09t0xefkedfarvwes82vrsazzsvwsw">1</key></foreign-keys><ref-type name="Book Section">5</ref-type><contributors><authors><author>Imaseki, H</author></authors><secondary-authors><author>Mattoo AK</author><author>Suttle JC</author></secondary-authors></contributors><titles><title>The biochemistry of ethylene biosynthesis</title><secondary-title>The Plant Hormone Ethylene</secondary-title></titles><pages>1-21</pages><dates><year>1991</year></dates><pub-location>Boca Ratonm USA</pub-location><publisher>CRC Press</publisher><urls></urls></record></Cite></EndNote>( HYPERLINK \l "_ENREF_15" \o "Imaseki, 1991 #1" Imaseki 1991).

Experiment III
In other fruit seedlings, the effects of the biocontrol agents varied among species. In grape, all treatments decreased the disease severity, whereas in apple and fig, alleviation of R. necatrix damage was only observed in plants inoculated with A and A+B, but not in those that received only a single inoculation of the bacterium (treatment B; Fig 5).
The application of biocontrol agents has been used for many fruits worldwide. Depending on the pathogen, appropriate antagonistic microorganisms should be selected. Bio-suppression of Botrytis in strawberries was more effective and consistent when Pichia guilermondii Wick and Bacillus mycoides Flugge were applied together than when applied separately  ADDIN EN.CITE <EndNote><Cite><Author>Guetsky</Author><Year>2002</Year><RecNum>37</RecNum><DisplayText>(Guetsky et al. 2002)</DisplayText><record><rec-number>37</rec-number><foreign-keys><key app="EN" db-id="5xz0rp09t0xefkedfarvwes82vrsazzsvwsw">37</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Guetsky, Ruth</author><author>Shtienberg, D.</author><author>Elad, Y.</author><author>Fischer, E.</author><author>Dinoor, A.</author></authors></contributors><titles><title>Improving Biological Control by Combining Biocontrol Agents Each with Several Mechanisms of Disease Suppression</title><secondary-title>Phytopathology</secondary-title></titles><periodical><full-title>Phytopathology</full-title></periodical><pages>976-985</pages><volume>92</volume><number>9</number><dates><year>2002</year><pub-dates><date>2002/09/01</date></pub-dates></dates><publisher>Scientific Societies</publisher><isbn>0031-949X</isbn><urls><related-urls><url>http://dx.doi.org/10.1094/PHYTO.2002.92.9.976</url></related-urls></urls><electronic-resource-num>10.1094/PHYTO.2002.92.9.976</electronic-resource-num><access-date>2013/11/19</access-date></record></Cite></EndNote>( HYPERLINK \l "_ENREF_13" \o "Guetsky, 2002 #37" Guetsky et al. 2002). Sclerotinia sclerotiorum (Lib.) in kiwifruit was suppressed by Epicoccum nigrum Link, and Botrytis cinerea Pers, the causal agent of botrytis, has been controlled by Ulocladium oudemansii (Simmons.)  ADDIN EN.CITE <EndNote><Cite><Author>Elmer</Author><Year>2005</Year><RecNum>38</RecNum><DisplayText>(Elmer et al. 2005)</DisplayText><record><rec-number>38</rec-number><foreign-keys><key app="EN" db-id="5xz0rp09t0xefkedfarvwes82vrsazzsvwsw">38</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Elmer, R. A. G.</author><author>Hoyte, S. M.</author><author>Vanneste, J. L.</author><author>Reglinski, T.</author><author>Wood, R. N.</author><author>Parry, F. J.</author></authors></contributors><titles><title>Biological control of fruit pathogens</title><secondary-title>New Zealand Plant Protection</secondary-title></titles><periodical><full-title>New Zealand Plant Protection</full-title></periodical><pages>47-54</pages><volume>58</volume><keywords><keyword>botrytis</keyword><keyword>grapes</keyword><keyword>sclerotinia</keyword><keyword>kiwifruit</keyword><keyword>fire blight</keyword><keyword>apples</keyword><keyword>pears</keyword></keywords><dates><year>2005</year></dates><isbn>ISSN 1175-9003 (print), ISSN 1179-352X (online)</isbn><urls><related-urls><url>http://www.nzpps.org/nzpp_abstract.php?paper=580470</url></related-urls></urls></record></Cite></EndNote>( HYPERLINK \l "_ENREF_11" \o "Elmer, 2005 #38" Elmer et al. 2005).

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