Impact of wheat/faba bean mixed cropping or rotation systems on soil microbial functionalities

Frontiers in Plant Science

Volumn 7, Issue September, 2016, Pages

  Wahbi, Sanâa ^a,b   Prin, Yves ^a   Thioulouse, Jean ^c   Sanguin, Hervé ^a   Baudoin, Ezékiel ^a   Maghraoui, Tasnime ^a,b,c   Oufdou, Khalid ^b   Le Roux, Christine ^a   Galiana, Antoine ^a   Hafidi, Mohamed ^b   Duponnois, Robin ^a  

^a LABORATOIRE DES SYMBIOSES TROPICALES ET MÉDITERRANÉENNES   (France)

^b FACULTÉ DES SCIENCES SEMLALIA   (Morocco)

^c UNIVERSITÉ LYON 1   (France)

Author keywords

Arbuscular mycorrhizal fungi; Cropping systems; Mediterranean region; Microbial soil functions; Nutrient uptake efficiency

Indexed keywords

EID: 84988660439     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2016.01364     Document Type: Article

References (65)

1. Abdallah, M. E., and Abdel-Fattah, G. M. (2000). Influence of the endomycorrhizal fungus Glomus mosseae on the development of peanut pod rot disease in Egypt. Mycorrhiza 10, 29-35. doi: 10.1007/s005720050284
2. Akter, N., Alim, A. M., Islam, M. M., Naher, Z., Rahman, M., and Hossain, L. M. (2004). Evaluation of mixed and intercropping lentil and wheat. J. Agron. 3, 48-51. doi: 10.3923/ja.2004.48.51
3. Altieri, M. A. (1999). The ecological role of biodiversity in agroecosystems. Agric. Ecosyst. Environ. 74, 19-31. doi: 10.1016/S0167-8809(99)00028-6
4. Artursson, V., Finlay, R. D., and Janson, J. K. (2006). Interactions between arbuscular mycorrhizal fungi and bacteria and their potential for stimulating plant growth. Environ. Microbiol. 8, 1-10. doi: 10.1111/j.1462-2920.2005.00942.x
5. Bartelt-Ryser, J., Joshi, J., Schmid, B., Brandl, H., and Balser, T. (2005). Soil feedbacks of plant diversity on soil microbial communities and subsequent plant growth. Perspect. Plant Ecol. Evol. Syst. 7, 27-49. doi: 10.1016/j.ppees.2004.11.002
6. Bastolla, U., Fortuna, M. A., Pascal-Garcia, A., Ferrera, A., Luque, B., and Bascompte, J. (2009). The architecture of mutualistic networks minimizes competition and increases biodiversity. Nature 458, 1018-1021. doi: 10.1038/nature07950
7. Betencourt, E., Duputel, M., Colomb, B., Desclaux, D., and Hinsinger, P. (2012). Intercropping promotes the ability of durum wheat and chickpea to increase rhizosphere phosphorus availability in low P soil. Soil Biol. Biochem. 46, 21-33. doi: 10.1016/j.soilbio.2011.11.015
8. Bever, J. D., Schultz, P. A., Pringle, A., and Morton, J. B. (2001). Arbuscular mycorrhizal fungi: more diverse than meets the eye, and the ecological tale of why. Bioscience 51, 923-931. doi: 10.1641/0006-3568(2001)051[0923:AMFMDT]2.0.CO;2
9. Bulson, H. A. J., Snaydon, R. W., and Stopes, C. E. (1997). Effects of plant density on intercropped wheat and field beans in an organic farming system. J. Agric. Sci. 128, 59-71. doi: 10.1017/S0021859696003759
10. Campbell, C. D., Chapman, S. J., Cameron, C. M., Davidson, M. S., and Potts, J. M. (2003). A rapid microtiter plate method to measure carbon dioxide evolved from carbon substrate amendments so as to determine the physiological profiles of soil microbial communities by using whole soil. Appl. Environ. Microbiol. 69, 3593-3599. doi: 10.1128/AEM.69.6.3593-3599.2003
11. Chu, G. X., Shen, Q. R., and Cao, J. L. (2004). Nitrogen fixation and N transfer from peanut to rice cultivated in aerobic soil in intercropping system and its effect on soil N-fertility. Plant Soil 263, 17-27. doi: 10.1023/B:PLSO.0000047722.49160.9e
12. Corre-Hellou, G., and Crozat, Y. (2005). Assessment of root system dynamics of species grown in mixtures under field conditions using herbicide injection and 15N natural abundance methods: a case study with pea, barley and mustard. Plant Soil 276, 177-192. doi: 10.1007/s11104-005-4275-z
13. Duponnois, R., Plenchette, C., and Bâ, A. M. (2001). Growth stimulation of seventeen fallow leguminous plants inoculated with Glomus aggregatum in Senegal. Eur. J. Soil Biol. 37, 181-186. doi: 10.1016/S1164-5563(01)01077-9
14. Franquet, E., Doledec, S., and Chessel, D. (1995). Using multivariate analyses for separating spatial and temporal effects within species-environment relationships. Hydrobiologia 300, 425-431. doi: 10.1007/BF000 24484
15. Fridley, J. D. (2001). The influence of species diversity on ecosystem productivity: how, where and why? Oikos 93, 514-526. doi: 10.1034/j.1600-0706.2001.930318.x
16. Garcia-Barrios, L. (2003). “Plant-plant interactions in tropical agriculture,” in Tropical Agroecosystems, ed. J. Vandermeer (Boca Raton, FL: CRC Press), 11-58.
17. Garofalo, P., Di Paolo, E., and Rinaldi, M. (2009). Durum wheat (Triticum durum Desf.) in rotation with faba bean (Vicia faba var. minor L.): long-term simulation case study. Crop Pasture Sci. 60, 240-250. doi: 10.1071/CP08208
18. Giovannetti, M., and Mosse, B. (1980). An evaluation of techniques for measuring vesicular arbuscular mycorrhizal infection in roots. New Phytol. 84, 489-500. doi: 10.1111/j.1469-8137.1980.tb04556.x
19. Gooding, M. J., Kasyanova, E., Ruske, R., Hauggaard-Nielsen, H., Jensen, E. S., Dahlmann, C., et al. (2007). Intercropping with pulses to concentrate nitrogen and sulphur in wheat. J. Agric. Sci. 145, 469-479. doi: 10.1017/S0021859607007241
20. Gurr, G. M., Wratten, S. D., and Luna, J. M. (2003). Multi-function agricultural biodiversity: pest management and other benefits. Basic Appl. Ecol. 4, 107-116. doi: 10.1078/1439-1791-00122
21. Hafidi, M., Ouahmane, L., Thioulouse, J., Sanguin, H., Boumezzough, A., Prin, Y., et al. (2013). Managing mediterranean nurse plants-mediated effects on soil microbial functions to improve rock phosphate solubilization processes and early growth of Cupressus atlantica G. Ecol. Eng. 57, 57-64. doi: 10.1016/j.ecoleng.2013.04.006
22. Hauggaard-Nielsen, H., Ambus, P., and Jensen, E. S. (2001). Temporal and spatial distribution of roots and competition for nitrogen in pea-barley intercrops - a field study employing 32P technique. Plant Soil 236, 63-74. doi: 10.1023/A:1011909414400
23. Hauggaard-Nielsen, H., Jornsgaard, B., Kinane, J., and Jensen, E. S. (2007). Grain legume-cereal intercropping: the practical application of diversity, competition and facilitation in arable andorganic cropping systems. Renew. Agric. Food Syst. 23, 3-12. doi: 10.1017/S1742170507002025
24. Hinsinger, P., Bettencourt, E., Bernard, L., Brauman, A., Plassard, C., Shen, J., et al. (2011). P for two sharing a scarce resource: soil phosphorus acquisition in the rhizosphere of intercropped species. Plant Physiol. 156, 1075-1086. doi: 10.1104/pp.111.175331
25. Hooper, D. U., and Vitousek, P. M. (1997). The effects of plant composition and diversity on ecosystem processes. Science 277, 1302-1305. doi: 10.1126/science.277.5330.1302
26. Jakobsen, I., Gazey, C., and Abbott, L. K. (2001). Phosphate transport by communities of arbuscular mycorrhizal fungi in intact soil cores. New Phytol. 149, 95-103. doi: 10.1046/j.1469-8137.2001.00006.x
27. Jakobsen, I., and Rosendahl, L. (1990). Carbon flow into soil and external hyphae from roots of mycorrhizal cucumber plants. New Phytol. 115, 77-83. doi: 10.1111/j.1469-8137.1990.tb00924.x
28. Jansa, J., Mozafar, A., and Frossard, E. (2005). Phosphorus acquisition strategies within arbuscular mycorrhizal fungal community of a single field site. Plant Soil 276, 163-176. doi: 10.1007/s11104-005-4274-0
29. Jensen, E. S., Bedoussac, L., Carlsson, G., Journet, E. P., Justes, E., and Hauggaard-Nielsen, H. (2015). Enhancing yields in organic crop production by eco-functional intensification. Sustain. Agric. Res. 4, 42-50. doi: 10.5539/sar.v4n3p42
30. Johansson, J. F., Paul, L. R., and Finlay, R. D. (2004). Microbial interactions in the mycorrhizosphere and their significance for sustainable agriculture. FEMS Microbiol. Ecol. 48, 1-13. doi: 10.1016/j.femsec.2003.11.012
31. John, M. K. (1970). Colorimetric determination in soil and plant material with ascorbic acid. Soil Sci. 68, 171-177.
32. Kaya, C., Higgs, D., Kirnak, H., and Tas, I. (2003). Mycorrhizal colonization improves fruit yield and water use efficiency in water melon (Citrullus lanatus Thumb) grown under well-watered and water-stressed conditions. Plant Soil 253, 287-292. doi: 10.1023/A:1024843419670
33. Kisa, M., Sanon, A., Thioulouse, J., Assigbetse, K., Sylla, S., Spichiger, R., et al. (2007). Arbuscular mycorrhizal symbiosis can counterbalance the negative influence of the exotic tree species Eucalyptus camaldulensis on the structure and functioning of soil microbial communities in a sahelian soil. FEMS Microbiol. Ecol. 62, 32-44. doi: 10.1111/j.1574-6941.2007.00363.x
34. Klironomos, J. N. (2002). Feedback with soil biota contributes to plant rarity and invasiveness in communities. Nature 417, 67-70. doi: 10.1038/417067a
35. Köpke, U., and Nemecek, T. (2010). Ecological services of faba bean. Field Crops Res. 115, 217-233. doi: 10.1016/j.fcr.2009.10.012
36. Latati, M., Blavet, D., Alkama, N., Laoufi, H., Drevon, J. J., Gérard, F., et al. (2014). The intercropping cowpea-maize improves soil phosphorus availability and maize yields in an alkaline soil. Plant Soil 85, 181-191. doi: 10.1007/s11104-014-2214-6
37. Latati, M., Pansu, M., Drevon, J. J., and Ounane, S. M. (2013). Advantage of intercropping maize (Zea mays L.) and common bean (Phaseolus vulgaris L.) on yield and nitrogen uptake in Northeast Algeria. Int. J. Res. Appl. Sci. 01, 1-7.
38. Lebart, L., Morineau, A., and Warwick, K. M. (1984). Multivariate Descriptive Statistical Analysis. New York, NY: Wiley.
39. Li, L., Tang, C., Rengel, Z., and Zhang, F. (2005). Chickpea facilitates phosphorus uptake by intercropped wheat from an organic phosphorus source. Plant Soil 248, 297-303. doi: 10.1023/A:1022389707051
40. Li, W., Li, L., Sun, J., Zhang, F. S., and Christie, P. (2003). Effects of nitrogen and phosphorus fertilizers and intercropping on uptake of nitrogen and phosphorus by wheat, maize, and faba bean. J. Plant Nutr. 26, 629-642. doi: 10.1081/PLN-120017670
41. Linderman, R. G. (1988). Mycorrhizal interactions with the rhizosphere microflora: the mycorrhizosphere effect. Phytopathology 78, 366-371.
42. Lovelock, C. E., Andersen, K., and Morton, J. B. (2003). Arbuscular mycorrhizal communities in tropical forests are affected by host tree species and environment. Oecologia 135, 268-297. doi: 10.1007/s00442-002-1166-3
43. Magurran, A. E. (1988). Ecological Diversity and its Measurement. London: Croom Helm.
44. Malézieux, E., Crozat, Y., Dupraz, C., Laurans, M., Makowski, D., Ozier- Lafontaine, H., et al. (2009). Mixing plant species in cropping systems: concepts, tools and models. A review. Agron. Sustain. Dev. 29, 43-62. doi: 10.1051/agro:2007057
45. Naeem, S., Thompson, L. J., Lawler, S. P., Lawton, J. H., and Woodfin, R. M. (1994). Declining biodiversity can alter the performance of ecosystems. Nature 368, 734-737. doi: 10.1038/368734a0
46. Ofori, F., and Stern, W. R. (1987). Cereal-legume intercropping systems. Adv. Agron. 41, 41-90. doi: 10.1016/S0065-2113(08)60802-0
47. Orrell, P., and Bennett, E. (2013). How can we exploit above-belowground interactions to assist in addressing the challenges of food security. Front. Plant Sci. 4:432. doi: 10.3389/fpls.2013.00432
48. Ouahmane, L., Thioulouse, J., Hafidi, M., Prin, Y., Ducousso, M., Galiana, A., et al. (2007). Soil functional diversity and P solubilization from rock phosphate after inoculation with native or exotic arbuscular mycorrhizal fungi. Forest Ecol. Manage. 241, 200-208. doi: 10.1016/j.foreco.2007.01.015
49. Phillips, J. M., and Hayman, D. S. (1970). Improved procedures for clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. Trans. British Mycol. Soc. 55, 158-161. doi: 10.1016/S0007-1536(70)80110-3
50. Rambelli, A. (1973). “The rhizosphere of mycorrhizae,” in Ectomycorrhizae: Their Ecology and Physiology, eds G. C. Marks and T. T. Kozlowski (New York, NY: Academic Press), 299-343.
51. Schnitzer, S. A., Klironomos, J. N., Hille Ris Lambers, J., Kinkel, L. L., Reich, P. B., Xiao, K., et al. (2011). Soil microbes drive the classic plant diversity-productivity pattern. Ecology 92, 296-303. doi: 10.1890/10-0773.1
52. Soler, R., van der Putten, W. H., Harvey, J. A., Vet, L. E. M., Dickie, M., and Bezemer, T. M. (2012). Root herbivore effects on aboveground multitrophic interactions: patterns, processes and mechanisms. J. Chem. Ecol. 38, 755-767. doi: 10.1007/s10886-012-0104-z
53. Tang, X., Bernard, L., Brauman, A., Daufresne, T., Deleporte, P., Desclaux, D., et al. (2014). Increase in microbial biomass and phosphorus availability in the rhizosphere of intercropped cereal and legumes under field conditions. Soil Biol. Biochem. 75, 86-93. doi: 10.1016/j.soilbio.2014.04.001
54. Thioulouse, J. (2011). Simultaneous analysis of a sequence of paired ecological tables: a comparison of several methods. Annals Appl. Stat. 5, 2300-2325. doi: 10.1214/10-AOAS372
55. Thioulouse, J., and Dray, S. (2007). Interactive multivariate data analysis in R with the ade4 and ade4TkGUI packages. J. Stat. Soft. 5, 1-14.
56. Thioulouse, J., Prin, Y., and Duponnois, R. (2012). Multivariate analyses in soil microbial ecology: a new paradigm. Environ. Ecol. Stat. 19, 499-520. doi: 10.1007/s10651-012-0198-z
57. Tilman, D., and Downing, J. A. (1994). Biodiversity and stability in grasslands. Nature 367, 363-365. doi: 10.1038/367363a0
58. Tilman, D., Knops, J., Wedin, D., Reich, P., Ritchie, M., and Siemann, E. (1997). The influence of functional diversity and composition on ecosystem processes. Science 277, 1300-1302. doi: 10.1126/science.277.5330.1300
59. Tilman, D., Wedin, D., and Knops, J. (1996). Productivity and sustainability influenced by biodiversity in grassland ecosystems. Nature 379, 718-720. doi: 10.1038/379718a0
60. van der putten, W. H., Bardgett, R. D., Bever, J. D., Bezemer, T. M., Casper, B. B., Fukami, T., et al. (2013). Plant-Soil Feedbacks: the past, the present and future challenges. J. Ecol. 101, 265-276. doi: 10.1111/1365-2745.12054
61. Vandermeer, J. H. (1989). The Ecology of Intercropping. Cambridge: Cambridge University Press.
62. Wagg, C., Jansa, J., Stadler, M., Schmid, B., and van der Heijden, M. G. A. (2011). Mycorrhizal fungal identity and diversity relaxes plant-plant competition. Ecology 92, 1303-1313. doi: 10.1890/10-1915.1
63. Wang, D., Marschner, P., Solaiman, Z., and Rengel, Z. (2007). Growth, P uptake and rhizosphere properties in intercropped wheat and chickpea in soil amended with iron phosphate or phytate. Soil Biol. Biochem. 39, 249-256. doi: 10.1016/j.soilbio.2006.07.013
64. Wolters, V., Silver, W. L., Bignell, D. E., Coleman, D. C., Lavelle, P., van der Putten, W. H., et al. (2000). Effects of global changes on above- and belowground biodiversity in terrestrial ecosystems: implications for ecosystem functioning. Bioscience 50, 1089-1098. doi: 10.1641/0006-568(2000)050[1089:EOGCOA]2.0.CO;2
65. Zhou, L. L., Cao, J., Zhang, F. S., and Li, L. (2009). Rhizosphere acidification of faba bean, soybean and maize. Sci. Tot. Environ. 407, 4356-4362. doi: 10.1016/j.scitotenv.2009.02.006