Some soil microorganisms are involved in the complex interactions with plants and earthworms, through the production of indole acetic acid (IAA) which modifies plant growth and development. In a factorial experiment testing the impact of the presence/absence of plants and earthworms on IAA production by cultivable bacteria, we observed that plants were decreasing IAA production of 43%, whereas earthworms were increasing it of 46%. In the presence of both plant and earthworms, IAA production was as low as in the presence of plant control, showing that plants influence on IAA production by microorganisms prevails on earthworm influence. We discuss functional reasons which could explain this result. 1. Introduction Soil microorganisms can be closely associated with soil animals such as earthworms for the delivery of ecosystem functions such as organic matter mineralization [1–3]. The release of nutrients due to this dual interaction has consequences on plant growth [4–6]. In addition to nutrients, interdependence between microorganisms, plants, and earthworms has led to the selection of diversified signal molecules, from low-molecular weight compounds such as auxin (e.g., IAA), amino acids, and secondary metabolites, to high-molecular weight compounds such as proteins and polysaccharides (for review see [7]). Emission of signal molecules by microorganisms can be deleterious for plants in the case of pathogenic bacteria and invertebrate herbivores, or positive with mycorrhizas, nitrogen-fixing symbiotic bacteria, or free living bacteria such as plant growth promoting rhizobacteria (PGPR) [7–9]. Auxin-like compounds have also been detected in earthworm dejections [10, 11], and could be responsible for the positive effect of earthworms [12] and vermicompost [10] on plant growth. The same molecule can have positive or negative effects according to its concentration and plant sensitivity [13]. There are very few studies which consider simultaneously the impact of plants and earthworms on microbial activities. However, it is of prior importance to establish a hierarchy in biotic factors influencing soil microorganisms. The purpose of our study was to determine the hierarchy of biotic factors on IAA-producing bacteria: do microorganisms obey to plants or earthworms? 2. Materials and Methods To answer this question, we set up an experiment with 4 treatments: soil without macroorganisms (S), with the plant Arabidopsis thaliana (P), and with the earthworm Aporrectodea caliginosa (E), with both plant and earthworms (PE). Nine cm diameter-10?cm high PVC experimental
References
[1]
G. G. Brown, I. Barois, and P. Lavelle, “Regulation of soil organic matter dynamics and microbial activity in the drilosphere and the role of interactions with other edaphic functional domains,” European Journal of Soil Biology, vol. 36, no. 3-4, pp. 177–198, 2000.
[2]
P. Lavelle, “Functional domains in soils,” Ecological Research, vol. 17, no. 4, pp. 441–450, 2002.
[3]
P. Lavelle and A. V. Spain, Soil Ecology, Kluwer Scientific Publications, Amsterdam, The Netherlands, 2001.
[4]
R. E. Ingham, J. A. Trofymow, E. R. Ingham, and D. C. Coleman, “Interactions of bacteria, fungi, and their nematode grazers: effects on nutrient cycling and plant growth,” Ecological Monographs, vol. 55, no. 1, pp. 119–140, 1985.
[5]
M. Blouin, S. Barot, and P. Lavelle, “Earthworms (Millsonia anomala, Megascolecidae) do not increase rice growth through enhanced nitrogen mineralization,” Soil Biology and Biochemistry, vol. 38, no. 8, pp. 2063–2068, 2006.
[6]
U. Jana, S. Barot, M. Blouin, P. Lavelle, D. Laffray, and A. Repellin, “Earthworms influence the production of above- and belowground biomass and the expression of genes involved in cell proliferation and stress responses in Arabidopsis thaliana,” Soil Biology and Biochemistry, vol. 42, no. 2, pp. 244–252, 2010.
[7]
H. P. Bais, T. L. Weir, L. G. Perry, S. Gilroy, and J. M. Vivanco, “The role of root exudates in rhizosphere interactions with plants and other organisms,” Annual Review of Plant Biology, vol. 57, pp. 233–266, 2006.
[8]
D. V. Badri and J. M. Vivanco, “Regulation and function of root exudates,” Plant, Cell & Environment, vol. 32, no. 6, pp. 666–681, 2009.
[9]
F. Persello-Cartieaux, L. Nussaume, and C. Robaglia, “Tales from the underground: molecular plant-rhizobacteria interactions,” Plant, Cell & Environment, vol. 26, no. 2, pp. 189–199, 2003.
[10]
L. P. Canellas, F. L. Olivares, A. L. Okorokova-Fa?anha, and A. R. Fa?anha, “Humic acids isolated from earthworm compost enhance root elongation, lateral root emergence, and plasma membrane H+-ATPase activity in maize roots,” Plant Physiology, vol. 130, no. 4, pp. 1951–1957, 2002.
[11]
A. Muscolo, S. Cutrupi, and S. Nardi, “IAA detection in humic substances,” Soil Biology and Biochemistry, vol. 30, no. 8-9, pp. 1199–1201, 1998.
[12]
G. G. Brown, C. A. Edwards, and L. Brussaard, “How earthworms affect plant growth: burrowing into the mechanisms,” in Earthworm Ecology, pp. 13–49, CRC Press, Boca Raton, Fla, USA, 2004.
[13]
O. Barazani and J. Friedman, “Is IAA the major root growth factor secreted from plant-growth-mediating bacteria?” Journal of Chemical Ecology, vol. 25, no. 10, pp. 2397–2406, 1999.
[14]
L. Taiz and E. Zeiger, Plant Physiology, Sinauer Associates, Sunderland, Mass, USA, 3rd edition, 2010.
[15]
S. Quaggiotti, B. Ruperti, D. Pizzeghello, O. Francioso, V. Tugnoli, and S. Nardi, “Effect of low molecular size humic substances on nitrate uptake and expression of genes involved in nitrate transport in maize (Zea mays L.),” Journal of Experimental Botany, vol. 55, no. 398, pp. 803–813, 2004.
[16]
D. B. Nehl, S. J. Allen, and J. F. Brown, “Deleterious rhizosphere bacteria: an integrating perspective,” Applied Soil Ecology, vol. 5, no. 1, pp. 1–20, 1997.
[17]
B. Schippers, A. W. Bakker, and P. Bakker, “Interactions of deleterious and beneficial rhizosphere microorganisms and the effect of cropping practices,” Annual Review of Phytopathology, vol. 25, pp. 339–358, 1987.
[18]
T. V. Suslow and M. N. Schroth, “Role of deleterious rhizobacteria as minor pathogens in reducing crop growth,” Phytopathology, vol. 72, no. 1, pp. 111–115, 1982.
[19]
Y. Bashan and G. Holguin, “Proposal for the division of plant growth-promoting rhizobacteria into two classifications: biocontrol-PGPB (plant growth-promoting bacteria) and PGPB,” Soil Biology and Biochemistry, vol. 30, no. 8-9, pp. 1225–1228, 1998.
[20]
J. W. Kloepper and M. N. Schroth, “Plant growth-promoting rhizobacteria on radishes,” in Proceedings of the 4th International Conference on Plant Pathogenic Bacteria, pp. 879–882, Station de Pathologie Vegetale et Phytobacteriologie, 1978.
[21]
A. M. Hirsch, Y. Fang, S. Asad, and Y. Kapulnik, “The role of phytohormones in plant-microbe symbioses,” Plant and Soil, vol. 194, no. 1-2, pp. 171–184, 1997.
[22]
P. E. Jameson, “Cytokinins and auxins in plant-pathogen interactions—an overview,” Plant Growth Regulation, vol. 32, no. 2-3, pp. 369–380, 2000.
[23]
M. Bonkowski, “Protozoa and plant growth: the microbial loop in soil revisited,” New Phytologist, vol. 162, no. 3, pp. 617–631, 2004.
[24]
N. Q. Arancon, C. A. Edwards, S. Lee, and R. Byrne, “Effects ofhumic acids from vermicomposts onplant growth,” European Journal of Soil Biology, vol. 42, no. 1, pp. S65–S69, 2006.
[25]
R. M. Atiyeh, N. Arancon, C. A. Edwards, and J. D. Metzger, “Influence of earthworm-processed pig manure on the growth and yield of greenhouse tomatoes,” Bioresource Technology, vol. 75, no. 3, pp. 175–180, 2000.
[26]
H. Chaoui, C. A. Edwards, M. Brickner, S. Lee, and N. Q. Arancon, “Suppression of the plant deseases Pythium, Rhizoctonia, and Verticillium by vermicompost,” Proceedings of the Brighton Crop Protection Conference on Pests Diseases, vol. 2, no. 8B-3, pp. 711–715, 2002.
[27]
M. T. Brandl and S. E. Lindow, “Environmental signals modulate the expression of an indole-3-acetic acid biosynthetic gene in Erwinia herbicola,” Molecular Plant-Microbe Interactions, vol. 10, no. 4, pp. 499–505, 1997.
[28]
Y. Kuzyakov and G. Domanski, “Carbon input by plants into the soil. Review,” Journal of Plant Nutrition and Soil Science, vol. 163, no. 4, pp. 421–431, 2000.
[29]
J. M. Lynch and J. M. Whipps, “Substrate flow in the rhizosphere,” Plant and Soil, vol. 129, no. 1, pp. 1–10, 1990.
[30]
L. Brussaard, “On the mechanisms of interactions between earthworms and plants,” Pedobiologia, vol. 43, no. 6, pp. 880–885, 1999.
[31]
M. J. Zarea, A. Ghalavand, E. M. Goltapeh, F. Rejali, and M. Zamaniyan, “Effects of mixed cropping, earthworms (Pheretima sp.), and arbuscular mycorrhizal fungi (Glomus mosseae) on plant yield, mycorrhizal colonization rate, soil microbial biomass, and nitrogenase activity of free-living rhizosphere bacteria,” Pedobiologia, vol. 52, no. 4, pp. 223–235, 2009.
[32]
J. Alphei, M. Bonkowski, and S. Scheu, “Protozoa, nematoda and lumbricidae in the rhizosphere of Hordelymus europaeus (Poaceae): faunal interactions, response of microorganisms and effects on plant growth,” Oecologia, vol. 106, no. 1, pp. 111–126, 1996.
[33]
R. Milleret, R. C. Le Bayon, F. Lamy, J. M. Gobat, and P. Boivin, “Impact of roots, mycorrhizas and earthworms on soil physical properties as assessed by shrinkage analysis,” Journal of Hydrology, vol. 373, no. 3-4, pp. 499–507, 2009.