Mycorrhizal relationship in lupines: A review

Transcription

1 Legume Research, 40(6)2017 : Print ISSN: / Online ISSN: AGRICULTURAL RESEARCH COMMUNICATION CENTRE Mycorrhizal relationship in lupines: A review Z.Y. Shi 1 *, X.L. Zhang, S.X. Xu, Z.J. Lan, K. Li, Y.M. Wang, F.Y. Wang and Y.L. Chen 2 * College of Agriculture, Henan University of Science and Technology, Luoyang , Henan province, China. Received: Accepted: DOI: /lr.v40i ABSTRACT Legume crops are widely cultivated with agronomical and economic significance. Majority of legume species are known to form mycorrhizal symbioses. However, plants in the genus Lupinus are generally considered as nonmycorrhizal. In this review, published researches with regards to mycorrhizal colonization and function in lupines were revisited. Research findings on mycorrhizal colonization (field or laboratory conditions) and functions (promotion in plant growth, nutrient uptake and metabolites) are summarized. These studies show that 35 out of 43 Lupinus species are colonized by mycorrhizal fungi although their root colonization rates are very low (<10%). The symbiotic status between mycorrhizal fungi and Lupinus species depend on lupine species, fungal taxa, and edaphic growth conditions. The functions of mycorrhizas on lupines exhibit more on physiology than the absorption of P. The responses of lupines to mycorrhizal fungi changed depending on mycorrhizal and Lupinus species and especially soil P concentrations. Based on current limited studies, conclusions on the nature of mycorrhizal relation in lupine could be compromised unless further studies with detailed field surveys and well-designed experiments are implemented. Key words: Arbuscular mycorrhizal fungi, Colonization rate, Lupinus, Mycorrhizal symbiosi, Mycorrhizal functions. Majority of legume plants is capable of forming mycorrhizas with arbuscular mycorrhizal (AM) fungi, and thereby benefits natural and agroecosystems. Species in the genus of Lupinus are ancient and important agricultural crops. There is no doubt that lupine roots form nodules at the presence of Rhizobia (Dudeja et al., 2012). However, the ability of lupine to form mycorrhizas and their function to benefit plant growth and nutrient acquisition remains in question. In the literature, Lupinus is considered as a nonmycorrhizal or weak mycorrhizal genus (e.g. Lambers et al., 2013) which is exceptional for Fabaceae. Schlicht (1889) first investigated colonization status of Lupins luteus by AM fungi. However, no colonization was observed in roots Lupins luteus by AM fungi. However, Trinick (1977) and Bedmar and Ocampo (1986) testified that the same species was colonization by AM fungi. Further, Bedmar and Ocampo (1986) showed that whether L. luteus was colonized or not depended on the species of AM fungi. Studies on mycorrhizal status of 43 lupine species showed that minority (8) species did not associated with AM fungi and majority (35) species formed symbioses with AM fungi with the low colonization (<10%). However, Snyder (1984) showed that L. albus was colonized by Glomus fasciculatum to the same extent as the other cover crops when they were grew as cover crops rotating with Liquidambar styracifua. As to the functions of mycorrhizal fungi, previous reports showed that the mycorrhizal fungi have not any function to improve the P absorption (Oba et al., 2001; Lambers et al., 2013). This conclusion seems to be generally accepted because almost most of reports considered mycorrhizal symbiosis as nonfunctional. However, the responses of lupines on physiological parameters to inoculate AM fungi are very significant with either positive effects (Vierheilig et al., 1994; O Dell, 1992; Lynd and Ansman, 1995; Oba et al., 2001; Hashem et al., 2016) or negative (O Dell, 1992; Vierheilig et al., 1994; Lynd and Ansman, 1995; Oba et al., 2001). From the previous studies, it is necessary to clear the mycorrhizal status and functions of lupines. With the aims, the existing reports about mycorrhizas and lupine were searched. Here, the current research progress on the relationship between mycorrhizal fungi and lupine plants were summarized. The aim is to clearly present the symbiotic status of lupine plants with mycorrhizal fungi. Further, to analyze the relationship between lupines and arbuscular mycorrhizal fungi. We searched the Web of Science database and Google Scholar for obtaining the related publications were searched. The sites, Lupinus and their colonization status for field studies were register. The Lupinus and AM fungi, *Corresponding author s shizy1116@126.com; yinglong.chen@uwa.edu.au 1 College of Agricultural, Henan University of Science and Technology, Luoyang , Henan province, China. 1 Key Laboratory of Mountain Surface Processes and Ecological Regulation, Chinese Academy of Sciences, Chengdu ,China. 2 The UWA Institute of Agriculture, & School of Agriculture and Environment, The University of Western Australia, LB 5005, Perth 6001, Australia. 2 Institute of Soil and Water Conservation, Chinese Academy of Sciences and Ministry of Water Resources, Yangling, Shaanxi , China.

2 966 LEGUME RESEARCH-An International Journal colonzaition and other conditions were collected for inoculated studies. The colonizations of Lupinus species are given according to the raw records in references. The responses of Lupinus species to AM fungi are transformed into mycorrhizal dependency for the purpose of comparability. The mycorrhizal dependency of different parameter is calculated by the following formula: Mycorrhizal dependency=(the value of inoculated AM fungi for A parameter-the value of CK for A parameter)/ the value of CK for A parameter. RESULTS AND DISCUSSION Mycorrhizal Colonization Status of Lupinus Species under Natural Conditions: The mycorrhizal status of Lupinus species in field condition were summarized in Table 1. A total 19 species or cultivated varieties was investigated in different region, which showed that 6 species or varieties were infected by AM fungi, 9 species were not colonized, and 4 species were either colonized or not depending on the different regions or elevations. For example, L. latifolius and L. lepidus could be colonized by AM fungi in some elevation sites and not in others in the same region. The results showed that whether some species formed symbiosis with AM fungi or not are affected by not only host plants but also environmental factors including all kinds of abiotic and biotic factors. Mycorrhizal Colonization Status of Lupinus Species under Cultivated Conditions: The mycorrhizal symbiotic and colonization statuses of Lupinus species were summarized (Table 2). Seventy-three species or varieties of lupines were experimented by inoculated different AM fungi, representing 140 matches of lupines and fungi. Among them, 65 matches formed symbiosis, 75 were not. When the lupines were considered in the level of species, thirty-five species were involved the inoculated studies, which 19 species were colonized by all inoculated AM fungi, 3 did not formed mycorrhizs, and whether the others were infected or not depended on AM fungal species. The results showed that the colonization of lupines was affected by hosts and AM fungi. Further, when the same Lupinus species inoculated different AM fungi, Gigaspora species were easier to infect the root of lupines than Glomus species. Table 1: The colonization status of species or cultivar varieties of lupines in changed sites under natural condition Lupine species or varieties colonization Region and elevation Sources Lupinus albicau- lis cv. Hederma + a) O Dell, 1992 L. angustifolius +V b) Trinick, 1977 L. albus + Snyder, 1984 L. caudatus - Blue Mtns of USA (1524) O Dell & Trappe, Basin and Range of USA (1280, 2377) L. cosentinii +VA c) Trinick, 1977 L. diffusus - Hood, 1964 L. latifolius - Basin and Range of USA(1676), Blue Mtn. O Dell and Trappe, of USA(1676), North Cascades of USA(900,1768, 1992/ Allen et al., , 2150), S. Wa Cascades of USA(750, 1100, 1676, 1554)/Mount St. Helens + Basin and Range of USA(1311, 1737), O Dell & Trappe, 1992 North Cascades of USA(900, 1372, 2400), Olympic Penn(1524) L. laxifloris + Blue Mtns of USA (1676) O Dell & Trappe, 1992 L. lepidus - Basin and Range of USA(2963), North Cascades O Dell & Trappe, 1992 of USA92512),S. Wa Cascades of USA(1250) + Basin and Range of USA(2347, 2585), North Cascades of USA(1829) L. leucophyllus + Blue Mtns of USA(1676), Basin and Range of O Dell & Trappe, 1992 USA(2378) L. luteus - Schlicht, 1889 L.micranthus Willamette Valley of USA(85) O Dell & Trappe, 1992 L. mutabilis - Lusnikova, 1970 L. parvifiorus - Colorado of USA Thomas,1943 L. perennis - Utah or Idaho or Montana or Michigan or Wisconsin Jones, 1924 L. polyphyllus + S. Wa Cascades of USA(1768) O Dell & Trappe, /upper Silesia Lusnikova, 1970; Pachlewski, 1958 L. rivularis - Coast range(274) O Dell & Trappe, 1992 L. sulphureus - Blue Mtns of USA(1524, 1890) O Dell & Trappe, 1992 L. wyethei - Blue Mtns of USA(1524), S. Wa Cascades of USA (1829) O Dell & Trappe, 1992 a) + and, colonization was observed or not, respectively. b) V means vesicles. c) A means arbuscules and vesicles.

3 Volume 40 Issue 6 (December 2017) 967 Table 2: The colonization status of Lupinus species or cultivar varieties with different AM fungi under inoculated condition Lupine species or varieties AMF a) C b) References c) L. albifrons Gi. m + Oba et al., 2001* L. albus, L. albus cv Gargill-1983/ Gi. m; G. m; G. f + <1~3, Bedmar and Ocampo, 1986; Lublanc/ multolup/ Blanca/ Ultra G. mi+t. m+ T. b V Lynd and Ansman, 1995; Oba et al., 2001*; Vierheilig et al., 1994*; L. albus, L. albus cv / / G. mi; G. m; G. sp 0 Avio et al., 1990 ; Bedmar and / / Arkansas/ Gala/ Gyulatanya/ Ocampo, 1986; Oba et al., 2001*; Kalina/ LA-108/ LA-109/ LA82099/ LA-82175/ Thompson and Wildermuth, 1989 LA-82233/ LA84025/ Polaca patuchy/ R-6002/ R L. andersonii G. m;gi. m 2, 3 Oba et al., 2001* L. angustifolius Gi. m; G. m+g. f <10 Oba et al., 2001*; Trinick, 1977* L. angustifolius; L. angustifolius cv G. mi; G. m;g. sp. 0 Avio et al., 1990 ; Bedmar and /112244/ E.S.Trlblue 78/ Marri/ Ocampo, 1986; Oba et al.,2001* Uniharvest/ Uniwhite L. arboreus G. m; Gi. m 2, 4 Oba et al., 2001* L. argenteus G. m; Gi. m 2, 3 Oba et al., 2001* L. aridus G. m; Gi. m +, V Oba et al., 2001* L. arizonieus G. m; Gi. m 1, 2 Oba et al., 2001* L. atlanticus G. m +, V Oba et al., 2001* L. atlanticus; L. atlanticus cv Gi.m; G. mi; G. 0 Avio et al., 1990; Oba et al., 2001* / / m;g. sp. L. bieolor Gi. m 4 Oba et al., 2001* L. cosentinii G. f; G. m; G. m+g. 2~<10 Oba et al., 2001*; Trinick, 1977*; f; Gi. m Trinick and Mosse, 1975 L. cosentinii G. f; Morley and Mosse, 1976; Oba et al., 2001*;Trinick, 1977* L. digitatus G. m; Gi. m <1, 2 Oba et al., 2001* L. elegans Gi. m; G. m <1 Oba et al., 2001* L. garifieldensis Gi. m;g. m 1, 2 Oba et al., 2001* L. hartwegii Gi. m + Oba et al., 2001* L. hirsutus Gi. m; Oba et al., 2001* L. hispanicus Gi. m; G. m + Oba et al., 2001* L. hybrid Gi. m, G. m 2, 4 Oba et al., 2001* L. latifolius G. i+g. e; G. i+g. e+ <1, 1 Oba et al., 2001*; G. d; G. m; Gi. m O Dell, 1992 L. leueophyllus Gi. m <1 Oba et al., 2001* L. littoralis Gi. m; G. m 3 Oba et al., 2001* L. luteolus Gi. m; G. m 1 Oba et al., 2001* L. luteus, L. luteus cv Barpine G. m+g. f ; G. m <10, 3 Bedmar and Ocampo, 1986; Trinick, 1977* L. luteus, L. luteus cv Portugues/ Vantus Gi. m; Bedmar and Ocampo, 1986; Oba et al., 2001* L. mexieanus Gi. m; G. m 2, 3 Oba et al., 2001* L. mieroearpus Gi. m;g. m 3 Oba et al., 2001* L. multijlorus G. m;gi. m 3, 6 Oba et al., 2001* L. mutabilis G. m + Oba et al., 2001* L. mutabilis, L. mutabilis cv / Gi.m;G.mi;G.m; G.sp. 0 Avio et al., 1990; Oba et al., 2001* / L. pilosus Gi. m; Oba et al., 2001* L. polyphyllus Gi. m + Oba et al., 2001* Table 2 continue...

4 968 LEGUME RESEARCH-An International Journal Table 2 continue... L. prineei G. m, Gi. m 2, 3 Oba et al., 2001* L. serieeus Gi. m 0 Oba et al., 2001* G. m 2 L. stiversii Gi. m; G. m <1, 3 Oba et al., 2001* L. succulentus Gi. m; G. m +, <1 Oba et al., 2001* L. sulphureus Oba et al., 2001* L. texensis G. m; Gi. m 3, 4 Oba et al., 2001* a) AMF, arbuscular mycorrhizal fungi; G. d, Glomus deserticola; G. e, Glomus etunicatum; G. f, Glomus fasciculatus; G. i, Glomus intraradices; G. m, Glomus mosseae; G. mi, Glomus microcarpus; Gi. m, Gigaspora margarita; T. b, Tuber brwnale; T. m, Tuber melanospotum. b) C, Colonization status; c) * means arbuscule and vesicle were checked; +, colonization was observed but no value was given; V vesicule was observed. The Effect of Arbuscular Mycorrhizal Fungi on Growth of Lupinus Species: It is well known that AM fungi improve the growth and nutrition status of hosts (Datta and Kulkarni, 2014). Data from previous studies about the functions of AM fungi on the growth and nutrition uptake were mined. And they were turned into the mycorrhizal dependency and summarized the effects of AM fungi on growth and nutrition uptake of lupines (Figure 1). The mycorrhizal dependencies of root fresh weight and length and shoot dry weight in 13 Lupinus species showed that the positive or negative responses and the effect degree of AM fungi depended on the changes of AM fungi and hosts. The mycorrhizal dependency of root fresh weight changed from -51% to 149% with the average of 11%. The most positive and negative effect on root fresh weight was observed in the L. mutabilis and L. angustifolius, respectively, both inoculated with Gi. margarita. When the different AM fungi were considered, the average mycorrhizal dependency of 13 Lupinus species inoculated G. mosseae (17%) was higher than that inoculated Gi. margarita (11%). However, the fluctuation of mycorrhizal dependency inoculated G. mosseae was lower than that inoculated Gi. margarita. The effect of different AM fungi on root fresh weight was also varied with the deference of AM fungal species. Mycorrhizal dependencies of root length of 13 Lupinus species to G. mosseae and Gi. margarita showed the similar tendency with root fresh weight (Figure 1 B). Further, the effect of mycorrhizal fungi on shoot dry weight of 14 Lupinus species were analyzed, which showed that mycorrhizal dependencies fluctuated with the different combination of mycorrhizal fungi and host plants. The most positive (1010 %) and negative dependency (-54 %) to mycorrhizas was observed on L. hartwegii inoculated G. mosseae and L. succulentus inoculated Gi. margarita, respectively. Moreover, the effect of mycorrhizal fungi on nodule weight and seed weight were studied, which indicated that the negative mycorrhizal dependencies of fresh and dry nodule weight of L. latifolius were presented with the mixed inocula of G. intraradices, G. etunicatum and G. intraradices. However, Lynd and Ansman (1995) showed that inocula improved the nodule weight of L. albus when inoculated the mixed AM fungi (G. faciculatum, G. microcapus) and ECM fungi (Tuber melanospotum, and T. brwnale). Further, Lynd and Ansman (1995) also studied the effect of the same mixed inocula on the seed dry weight, which showed that the function of mycorrhizal fungi varied with the different fertilizer treatments (Figure 1). Generally, the functions of mycorrhizal fungi were limited by P nutrition. So the effect of mycorrhizal fungi on seed dry weight were divided into P and non-p treatments, which indicated that the mycorrhizal dependency was much lower in P treatment (-13%) than non- P treatments (137%), which testified that abundant P concentration hampered the functions of mycorrhizal fungi on lupines. The Effect of Arbuscular Mycorrhizal Symbiosis on Nutrition Uptake of Lupinus Species: As far as the function of AM fungi on plant nutrition was concerned, the P nutrient has caused more attentions. There are numerous studies for confirming the function of AM fungi on improving P nutrition of host plants. However, as to lupines, there was only a report on improving their P nutrition by AM fungi (Oba et al., 2001). Their results showed that the P concentration in shoot of majority of 13 Lupinus species was decreased due to inoculating AM fungi (G. mosseae and Gi. margarita) (Figure 2). The mycorrhizal dependencies of 13 Lupinus species changed from -76% to 22% with the average of -13% and - 49% to 20% with the mean of 11%, respectively. The Effects of Mycorrhizal Symbiosis on Metabolities of Lupines: Lynd and Ansman (1995) studied the effect of a mixed inoculum with AM fungi (Glomus faciculatum ATCC38848, G. microcapus) and ECM fungi (Tuber melanospotum and T. brwnale) on nodule cytosol components and enzyme components governing nitrogen fixation transformations, and nitrogenase activity of L. alba cv. Ultra (Figure 3 A). The mycorrhizal dependency of Nitrate was -62% and pyruvate s dependency was 231%. As to nodule cytosol enzyme components governing nitrogen fixation transformations, nitrate oxidoreductase (NR) was reduced significantly with the mycorrhizal dependency of % and phosphoenolpyruvate carboxylase (PEPC) was

5 Volume 40 Issue 6 (December 2017) 969 Figure 1: The mycorrhizal dependency of growth of Lupinus species The figure A and B were adapted from oba et al., 2001; The figure C was comprehensively adapted from Oba et al. 2001, O Dell 1992, and Lynd and Ansman 1995; The figure D was adapted from O Dell 1992 and Lynd and Ansman 1995; The Figure E is adapted from Lynd and Ansman G.i, Glomus intraradices; G.d, G. deserticola; G.e, Glomus etunicatum; G.f, Glomus faciculatum; G.mi, G. microcapus; T. m, Tuber melanospotum; T. b, T. brwnale. L. al, Lupinus albus; L. an, L. angustifolius; L. ar, L. aridus; L. at, L. atlanticus; L. co, L. cosentinii; L. ha, L. hartwegii; L. hir, L. hirsutus; L. his, L. hispanicus; L. la, L. latifolius; L. lu, L. luteus; L. mu, L. mutabilis; L. pi, L. pilosus; L. po, L. polyphyllus; L. su, L. succulentus.

6 970 LEGUME RESEARCH-An International Journal Figure 2: The effect of mycorrhizal fungi on shoot P concentration of Lupinus species markedly improved with the mycorrhizal dependency of 302% by inoculated mixed AM and ECM fungi (Figre 3 B). The mycorrhizal dependency of nitrogenase was 96% in non- P substrate contrast to -10% in applying P treatment (Figure 3 C). The findings of Vierheilig et al. (1994) indicated that the functions of G. mosseae changed with the inoculated times (Figure 3 D). Their study showed that glucanase activity was significantly increased from the 3 days to 15 after inoculated. However, glucanase activity significantly decreased in the 30 days after inoculation. The response of ethylene production to inoculated G. mosseae was the similar trend with glucanase activity, which enhanced significantly from 6 to 15 day after inoculation, and decreased after 30 days. Chitinase activity was reduced markedly from the 6 days after inoculation. Generally, the high colonization and positive role of AM symbiosis in legume species growth, nutrition status, disease resistance, and yield are famous (Ramana et al., 2010; Indriani et al., 2016). However, the percentages of lupine roots colonization by AM fungi of majority studies have been shown either non-colonization or weak colonization (Table 1 and 2). Although the results showed that the colorizations varied with different matches of AM fungi and lupinus species, the reason had been focused on the exudation of lupine roots (Akiyama et al. 2010; Oba et al., 2002). Akiyama et al. (2010) isolated 7 pyranoisoflavones from root metabolites of Lupinus albus grown hydroponically. They were testified to inhibit the growth of germ tube of AM fungal spores, which was accorded with the finding made by Oba et al. (2002) in the other Lupinus species. However, as to Lupinus albus, the conclusion was contrary to the findings made by Oba et al. (2002) inoculated Gigaspora margarita and Gianinazzi-Pearson et al. (1993) and Gianinazzi-Pearson et al. (1989) inoculated G. mosseae, whose results showed that root exudates of L. albus did not affect hyphal growth. It was well known that the formation of mycorrhizal symbiosis included several key steps. Some previous studies had explored reasons that plants could not form mycorrhizal association (Trinick, 1977; Vierheilig et al., 1994; Oba et al., 2001; Lambers et al., 2013). Three different mechanisms were obtained. Firstly, the root exudation of non-host plants did not induce the AM fungal spore germination (Daniels and Trappe, 1980). The second idea was that the inhibitory factors in root exudates of non-host plants restricted the germination of spore and growth of hypha (Hirrel et al., 1978; Oba et al., 2002; Akiyama et al., 2010). Thirdly, the lack of stimulator hindered the hyphal growth and formation of appressorium in the exudates of non-hosts roots (Gianinazzi- Pearson and Gianinazzi, 1992). As to Lupinus species, above three mechanisms had been found in different species, even in the same species (Gianinazzi-Pearson and Gianinazzi, 1992; Gianinazzi-Pearson et al., 1993; Akiyama et al., 2010). However, the mechanisms were not consistent for lupine, even to the same species. Akiyama et al. (2010) showed that pyranoisoflavones in root exudates of L. albus inhibited hyphal development when Gigaspora margarita was employed. Contrarily, Gianinazzi-Pearson et al. (1993) indicated that the root exudates of L. albus did not hinder the hyphal growth of G. mosseae. The two conflictive conclusions were probably explained AM fungal species. However, Oba et al. (2002) showed that the root exudates

7 Volume 40 Issue 6 (December 2017) 971 Figure 3: Effect of mycorrhizal fungi on metabolites in roots or nodules of Lupinus species The figures were adapted from Lynd and Ansman 1995 and Vierheilig et al., G.f, Glomus faciculatum; G.mi, G. microcapus; T. m, Tuber melanospotum; T. b, T. brwnale. CK, means soil epipedon (0-20cm) from filed; +P means to apply 200 mg Ca(H 2 PO 4 ) 2 /kg soil. * in figure D, the effect is significant. did not restrict the hyphal growth when L. albus also inoculated Gi. margarita. Their inconsistent conclusions made us difficult explain the mechanism. Moreover, some pot culture experiments of Lupinus species inoculated AM fungi showed that fungal hypha could arrive to lupines roots and form appressorium whether the lupine roots were colonized or not (Morley And Mosse, 1976; Oba et al., 2001), which probably supported the conclusion that the germination of spores and growth of hypha were independent on the exudates of lupine roots. Further, the conformations of appressoriums of AM fungi were similar to meet a nonhost of AM fungi (Giovannetti and Sbrana, 1998). From the above descriptions about the mycorrhizal status and mechanisms of Lupinus species, the conclusion whether lupines formed mycorrhizal symbiosis or not should be considered in the level of species or even cultivars, but not to be conceded in genus level may be inferred. As a result, the relationship between Lupinus species and AM fungi need to be further studied.

8 972 LEGUME RESEARCH-An International Journal CONCLUSION In conclusion, in order to further knowledge the mycorrhizal status and their function to Lupinus species, much effort is needed (1) to explore the colonization status between specific Lupinus and AM fungal species in the same condition; (2) to probe the mechanism of lupines as either a host or non-host of AM fungi; (3) to check the changes of lupines root cortex cell in cell level because it is well known that the colonization can cause the changes of root epidermal cells;(4) to re-evaluate the functions of mycorrhizal symbiosis to Lupinus species. ACKNOWLEDGEMENT The project was supported by Key Laboratory of Mountain Surface Processes and Ecological Regulation, CAS (No ), NSFC ( , ), Program for Science & Technology Innovation Talents in Universities of Henan Province (18HASTIT013), Chinese Academy of Sciences Hundred Talent Program (A ), Laboratory for Earth Surface Processes, Ministry of Education (201612), the Innovation Team Foundation (2015TTD002) of Henan University of Science and Technology. REFERENCES Akiyama, K., Tanigawa, F., Kashihara, T. and Hayashi H. (2010). Lupin pyranoisofl avones inhibiting hyphal development in arbuscular mycorrhizal fungi. Phytochemistry, 71: Allen, M.F., Macmahon, J.A. and Ianson, D.C. (1985). Ecesis on Mount St. Helens: can mycorrhizal fun gi spread from animal- dispersed inoculum? In: Proceedings of the 6th North American Conference on Mycorrhizae (Ed. by R. Molina), pp. 291, Forestry Research Laboratory, Corvallis, Oregon. Avio, L., Sbrana, C. and Giovannetti, M. (1990). The response of different species of Lupinus to VAM endophytes. Symbiosis, 9: Bedmar, E.J. and Ocampo, J.A. (1986). Susceptibilidad de distintas variedades de guisante, veza y lupino a la infeccion por Glomus mosseae. Anales de Edalfologia Agrobiologia. 45: Datta, P. and Kulkarni M. (2014). Influence of two AM fungi in improvement of mineral profile in Arachis hypogaea L. under salinity stress. Legume Research, 37 (3): Dudeja S.S., Sheokand S. and Kumari S. (2012). Legume root nodule development and functioning under tropics and subtropics: perspectives and challenges. Legume Research, 35(2): Gianinazzi-Pearson, V. and Gianinazzi S. (1992). Influence of intergeneric grafts between host and non-host legumes on vesiculararbuscular mycorrhizal formation. New Phytologist, 120: Gianinazzi-Pearson, V., B. Branzanti. and Gianinazzi S. (1989). In vitro enhancement ot spore germmation and early hyphal growth of a vesicular -arbuscular mycorrhizal fungus by host root exudatts and plant flavonoids. Symbiosis, 1: Giovannetti, M. and Sbrana C. (1998). Meeting a non-host: the behaviour of AM fungi. Mycorrhiza, 8: Giovannetti, M., Avio, L., Sbrana, C and Citemesi A.S. (1993). Factors affecting appressorium development in the vesiculararbuscular mycorrhizal fungus Glomus mosseae (Nicol. & Gerd.) Gerd. & Trappe. New Phytologist, 123: Hashem A., Abd_Allah, E.F., Alqarawi, A.A., Wirth, S. and Egamberdieva, D. (2016). Arbuscular mycorrhizal fungi alleviate salt stress in lupine (Lupinus termis Forsik) through modulation of antioxidant defense systems and physiological traits. Legume Research, 39(2): Hood, S.C. (1964). A classification of the symbiotic relation of funlgi with plant roots. Hood Laboratory Bulletin 8, 32 pp., Tampa, Florida. Indriani N.P., Yuwariah, Y., Rochana, A., Susilawati, I. and Khairani, L. (2016). The role of Vesicular Arbuscular Mycorrhiza (VAM) and rock phosphate application on production and nutritional value of centro legumes(centrosema pubescens). Legume Research, 39(6): Jones, F.R. (1924). A mycorrhizal fungus in the roots of legumes and some other plants. Journal of Agricultural Research, 29: Lambers, H., Clements, J.C. and Nelson, M.N. (2013). How a phosphorus-acquisition strategy based on carboxylate exudation powers the success and agronomic potential of lupines (Lupinus, Fabaceae). American Journal of Botany, 100(2): Lusnikova A.A. (1970). Mikoriza dekorativnykh travyanistykh rasteniz. Uchenye Zapiski Permskii Gosvdostvennyi Pedagogicheskii Institu. 80: Lynd, J.Q. and Ansman, T.R. (1995). Mycorrhizal etiology of favorable proteoid rhizogenesis, nodulation, and nitrogenase of lupines. Journal of Plant Nutrition, 18: 11, Morley, C.D. and Mosse, B. (1976). Abnormal vesicular-arbuscular mycorrhizal infections in white clover induced by lupin. Transactions of the British Mycological Society, 67: O7: of the British Mycologic Root endophytes of lupin and some other legumes in northwestern USA. New Phytologist, 122: Oba, H., Tawaray, K. and Wagatsuma, T. (2001). Arbuscular mycorrhizal colonization in Lupinus and related genera. Soil Science and Plant Nutrition, 47: Oba, H., Tawaraya K. and Wagatsuma T. (2002). Inhibition of pre-symbiotic hyphal growth of arbuscular mycorrhizal fungus Gigaspora margarita by root exudates of Lupinus spp.. Soil Science and Plant Nutrition, 48:1,

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