Advertisement

Plant and Soil

, Volume 440, Issue 1–2, pp 277–292 | Cite as

Bioirrigation: a common mycorrhizal network facilitates the water transfer from deep-rooted pigeon pea to shallow-rooted finger millet under drought

  • Devesh Singh
  • Natarajan Mathimaran
  • Thomas Boller
  • Ansgar KahmenEmail author
Regular Article

Abstract

Background and aim

Hydraulically lifted water can be redistributed to a neighbouring plant, a process referred to as “bioirrigation”. Facilitation of bioirrigation by beneficial microbes such as arbuscular mycorrhizal (AM) fungi that form a common mycorrhizal network (CMN) between neighbouring plants has often been suggested but is not yet well explored. In this study, we tested if the presence of a CMN can facilitate the transfer of hydraulically lifted water from pigeon pea (PP) to finger millet (FM) and ameliorate thereby the water relations of the shallow-rooted FM during drought.

Methods

In a compartmented microcosm set up, PP roots were grown up to the bottom layer of the pot to access the soil moisture. Whereas FM roots were restricted into a shallow compartment, separated through a 21 μm nylon mesh, without access to the moist bottom layer. We applied deuterium labelled water to the bottom layer of the pot to test if PP can perform hydraulic lift (HL) and if hydraulically lifted water is transferred to FM via a CMN. During the drought period we also assessed the water relations of FM to determine if bioirrigation mediated through a CMN can support the water relations of FM.

Results

Application of deuterium-enriched water to the moist bottom layer of the microcosms demonstrated the capability of PP to hydraulically lift water to the drier topsoil through an insulation layer of coarse gravel. Only FM plants that were connected to PP via a CMN were able to utilize HL water. As a consequence, FM bioirrigated by PP in the presence of a CMN was able to maintain its water relations during drought conditions and showed higher rates of survival than FM plants in monoculture.

Conclusions

Connecting the rhizosphere of two intercropping partners with a CMN can improve the water relations of shallow-rooted crops by bioirrigation. This finding has great potential for reducing drought induced crop yield loss in arid and semi-arid tropics.

Keywords

AM fungi Bioirrigation Drought Finger millet Intercropping PGPR Pigeon pea Water relations 

Notes

Acknowledgements

This research work was funded by Swiss Agency for Development and Cooperation (SDC) under the Indo-Swiss Collaboration in Biotechnology (The BIOFI project). We are thankful to Dr. M. N. Thimmegowda, All India Coordinated Research Project on Small Millets, University of Agricultural Sciences, Bengaluru India, for providing the PP and FM seeds. Dr. D. J. Bagyaraj, Centre for Natural Biological Resources and Community Development (CNBRCD), Bengaluru, India) for providing AMF culture for research work at University of Basel, Switzerland.

References

  1. Armas C, Kim JH, Bleby TM, Jackson RB (2012) The effect of hydraulic lift on organic matter decomposition, soil nitrogen cycling, and nitrogen acquisition by a grass species. Oecologia 168:11–22.  https://doi.org/10.1007/s00442-011-2065-2 CrossRefPubMedGoogle Scholar
  2. Artursson V, Finlay RD, Jansson JK (2006) Interactions between arbuscular mycorrhizal fungi and bacteria and their potential for stimulating plant growth. Environ Microbiol 8:1–10.  https://doi.org/10.1111/j.1462-2920.2005.00942.x CrossRefPubMedGoogle Scholar
  3. Augé RM (2001) Water relations, drought and vesicular-arbuscular mycorrhizal symbiosis. Mycorrhiza 11:3–42.  https://doi.org/10.1007/s005720100097
  4. Augé RM, Stodola JW, Tims JE, Saxton AM (2001) Moisture retention properties of a mycorrhizal soil. Plant Soil 230:87–97.  https://doi.org/10.1023/A:1004891210871
  5. Augé RM, Sylvia DM, Park S, Buttery BR, Saxton AM, Moore JL, Cho K (2004) Partitioning mycorrhizal influence on water relations of Phaseolus vulgaris into soil and plant components. Can J Bot 82:503–514.  https://doi.org/10.1139/b04-020 CrossRefGoogle Scholar
  6. Augé RM, Toler HD, Saxton AM (2015) Arbuscular mycorrhizal symbiosis alters stomatal conductance of host plants more under drought than under amply watered conditions: a meta-analysis. Mycorrhiza 25:13–24.  https://doi.org/10.1007/s00572-014-0585-4 CrossRefPubMedGoogle Scholar
  7. Barea JM, Azcen-Aguilar C, Azcen R (1991) The role of vesicular-arbuscular mycorrhizae in improving plant N acquisition from soil as assessed with 15N. In: Stable isotopes in plant nutrition, soil fertility and environmental studies. International Atomic Energy Agency, Vienna, pp 209–216Google Scholar
  8. Barnard RL, Bello F, Gilgen AK, Buchmann N (2006) The δ18O of root crown water best reflects source water δ18O in different types of herbaceous species. Rapid Commun Mass Spectrom 20:3799–3802.  https://doi.org/10.1002/rcm.2778
  9. Beggi F, Hamidou F, Hash CT, Buerkert A (2016) Effects of early mycorrhization and colonized root length on low-soil-phosphorus resistance of West African pearl millet. J Plant Nutr Soil Sci 179:466–471.  https://doi.org/10.1002/jpln.201500501 CrossRefGoogle Scholar
  10. Bingham MA, Simard S (2012) Ectomycorrhizal networks of Pseudotsuga menziesii var. glauca trees facilitate establishment of conspecific seedlings under drought. Ecosystems 15:188–199.  https://doi.org/10.1007/s10021-011-9502-2 CrossRefGoogle Scholar
  11. Bleby TM, Mcelrone AJ, Jackson RB (2010) Water uptake and hydraulic redistribution across large woody root systems to 20 m depth. Plant Cell Environ 33:2132–2148.  https://doi.org/10.1111/j.1365-3040.2010.02212.x CrossRefPubMedGoogle Scholar
  12. Bogie NA, Bayala R, Diedhiou I, Dick RP, Ghezzehei TA (2018a) Intercropping with two native woody shrubs improves water status and development of interplanted groundnut and pearl millet in the Sahel. Plant Soil 435:143–159.  https://doi.org/10.1007/s11104-018-3882-4 CrossRefGoogle Scholar
  13. Bogie NA, Bayala R, Diedhiou I, Conklin MH, Fogel ML, Dick RP, Ghezzehei TA (2018b) Hydraulic redistribution by native sahelian shrubs: bioirrigation to resist in-season drought. Front Environ Sci 6:1–12.  https://doi.org/10.3389/fenvs.2018.00098 CrossRefGoogle Scholar
  14. Brooks JR, Meinzer FC, Coulombe ROB, Gregg J (2002) Hydraulic redistribution of soil water during summer drought in two contrasting pacific northwest coniferous forests. Tree Physiol 22:1107–1117CrossRefPubMedGoogle Scholar
  15. Brooks JR, Meinter FC, Warren JM et al (2005) Hydraulic redistribution in a Douglas-fir forest: lessons from system manipulations. Plant Cell Environ 29:138–150.  https://doi.org/10.1111/j.1365-3040.2005.01409.x CrossRefGoogle Scholar
  16. Brundrett M (1994) Estimation of root length and colonization by mycorrhizal fungi. In: Brundrett, M., Melville, L., Peterson (Eds.), Practical Methods in Mycorrhiza Research. Waterloo, pp 51–59Google Scholar
  17. Burgess SSO (2011) Can hydraulic redistribution put bread on our table? Plant Soil 341:25–29.  https://doi.org/10.1007/s11104-010-0638-1 CrossRefGoogle Scholar
  18. Burgess SSO, M a A, Turner NC, Ong CK (1998) The redistribution of soil water by tree root systems. Oecologia 115:306–311.  https://doi.org/10.1007/s004420050521 CrossRefPubMedGoogle Scholar
  19. Byra RMS, Bagyaraj DJ (1991) The symbiotic efficiency of pigeonpea to VA mycorrhizal inoculation in an Alfisol and a vertisol. Biol Agric Hortic 8:177–182.  https://doi.org/10.1080/01448765.1991.9754588 CrossRefGoogle Scholar
  20. Caldwell MM (1990) Water parasitism stemming from hydraulic lift: a quantitative test in the field. Isr J Bot 39:395–402.  https://doi.org/10.1080/0021213X.1990.10677163 CrossRefGoogle Scholar
  21. Caldwell MM, Manwaring JH (1994) Hydraulic lift and soil nutrient heterogeneity. Isr J Plant Sci 42:321–330.  https://doi.org/10.1080/07929978.1994.10676583 CrossRefGoogle Scholar
  22. Caldwell MM, Dawson TE, Richards JH (1998) Hydraulic lift: consequences of water efflux from the roots of plants. Oecologia 113:151–161.  https://doi.org/10.1007/s004420050363 CrossRefPubMedGoogle Scholar
  23. Carminati A, Moradi AB, Vetterlein D, Vontobel P, Lehmann E, Weller U, Vogel HJ, Oswald SE (2010) Dynamics of soil water content in the rhizosphere. Plant Soil 332:163–176.  https://doi.org/10.1007/s11104-010-0283-8 CrossRefGoogle Scholar
  24. Dawson TE (1993) Hydraulic lift and water use by plants: implications for water balance, performance and plant-plant interactions. Oecologia 95:565–574CrossRefPubMedGoogle Scholar
  25. Dohn J, Demgele F, Karembe M, Moustakas A, Amevor KA, Hanan NP (2013) Tree effects on grass growth in savannas: competition, facilitation and the stress-gradient hypothesis. J Ecol 101:202–209CrossRefGoogle Scholar
  26. Egerton-Warburton LM, Querejeta JI, Allen MF (2007) Common mycorrhizal networks provide a potential pathway for the transfer of hydraulically lifted water between plants. J Exp Bot 58:1473–1483.  https://doi.org/10.1093/jxb/erm009 CrossRefPubMedGoogle Scholar
  27. Egerton-Warburton LM, Querejeta JI, Allen MF (2008) Efflux of hydraulically lifted water from mycorrhizal fungal hyphae during imposed drought. Plant Signal Behav 3:68–71.  https://doi.org/10.4161/psb.3.1.4924 CrossRefPubMedPubMedCentralGoogle Scholar
  28. Espeleta JF, West JB, Donovan LA (2004) Species-specific patterns of hydraulic lift in co-occurring adult trees and grasses in a sandhill community. Oecologia 138:341–349.  https://doi.org/10.1007/s00442-003-1460-8 CrossRefPubMedGoogle Scholar
  29. Fu YJ, Liu W, Zu YG, Tong MH, Li SM, Yan MM, Efferth T, Luo H (2008) Enzyme assisted extraction of luteolin and apigenin from pigeonpea [Cajanus cajan (L.) Millsp.] leaves. Food Chem 111:508–512.  https://doi.org/10.1016/j.foodchem.2008.04.003 CrossRefPubMedGoogle Scholar
  30. Gamborg OL, Wetter LR (1975) Plant tissue culture methods. Saskatoon: National Research CouncilGoogle Scholar
  31. Govinda RYS, Bagyaraj DJ, Rai PV (1983) Selection of an efficient VA mycorrhizal fungus for finger millet: II. Screening under field conditions. Zentralbl Mikrobiol 138:415–419.  https://doi.org/10.1016/S0232-4393(83)80039-0 CrossRefGoogle Scholar
  32. Hetrick BAD, Wilson GWT, Todd TC (1996) Mycorrhizal response in wheat cultivars: relationship to phosphorus. Can J Bot 74:19–25.  https://doi.org/10.1139/b96-003 CrossRefGoogle Scholar
  33. Hirota I, Sakuratani T, Sato T, Higuchi H, Nawata E (2004) A split-root apparatus for examining the effects of hydraulic lift by trees on the water status of neighbouring crops. Agrofor Syst 60:181–187.  https://doi.org/10.1023/B:AGFO.0000013293.77907.64 CrossRefGoogle Scholar
  34. Höflich G, Wiehe W, Kühn G (1994) Plant growth stimulation by inoculation with symbiotic and associative rhizosphere microorganisms. Experientia 50:897–905.  https://doi.org/10.1007/BF01923476 CrossRefGoogle Scholar
  35. Horton JL, Hart SC (1998) Hydraulic lift: a potentially important ecosystem process. Trends Ecol Evol 13:232–235.  https://doi.org/10.1016/S0169-5347(98)01328-7 CrossRefPubMedGoogle Scholar
  36. Johnson D, Vandenkoornhuyse PJ, Leake JR, Gilbert L, Booth RE, Grime JP, Young JPW, Read DJ (2004) Plant communities affect arbuscular mycorrhizal fungal diversity and community composition in grassland microcosms. New Phytol 161:503–515.  https://doi.org/10.1046/j.1469-8137.2003.00938.x CrossRefGoogle Scholar
  37. Khalvati MA, Hu Y, Mozafar A, Schmidhalter U (2005) Quantification of water uptake by arbuscular mycorrhizal hyphae and its significance for leaf growth, water relations, and gas exchange of barley subjected to drought stress. Plant Biol 7:706–712.  https://doi.org/10.1055/s-2005-872893 CrossRefPubMedGoogle Scholar
  38. Kothari SK, Marschner H, George E (1990) Effect of VA mycorrhizal fungi and rhizosphere microorganisms on root and shoot morphology, growth and water relations in maize. New Phytol 116:303–311.  https://doi.org/10.1111/j.1469-8137.1990.tb04718.x CrossRefGoogle Scholar
  39. Lee J-E, Oliveira RS, Dawson TE, Fung I (2005) Root functioning modifies seasonal climate. Proc Natl Acad Sci U S A 102:17576 LP-17581Google Scholar
  40. Liste H-H (1993) Förderung von symbiose und Wachstum bei Luzerne durch kombinierte Beimpfung mit Rhizobium meliloti und Pseudomonas fluorescens. Zentralbl Mikrobiol 148:163–176.  https://doi.org/10.1016/S0232-4393(11)80085-5 CrossRefGoogle Scholar
  41. Ludwig F, Dawson TE, Kroon H et al (2003) Hydraulic lift in Acacia tortilis trees on an east African savanna. Oecologia 134:293–300.  https://doi.org/10.1007/s00442-002-1119-x CrossRefPubMedGoogle Scholar
  42. Ludwig F, de-Kroon H, Berendse F, Prins HHT (2004a) The influence of savanna trees on nutrient, water and light availability and the understorey vegetation. Plant Ecol 170:93–105CrossRefGoogle Scholar
  43. Ludwig F, Dawson TE, Prins HHT, Berendse F, de-Kroon H (2004b) Below-ground competition between trees and grasses may overwhelm the facilitative effects of hydraulic lift. Ecol Lett 7:623–631CrossRefGoogle Scholar
  44. Mathimaran N, Srivastava R, Wiemken A, Sharma AK, Boller T (2012) Genome sequences of two plant growth-promoting fluorescent pseudomonas strains, R62 and R81. J Bacteriol 194:3272–3273.  https://doi.org/10.1128/JB.00349-12 CrossRefPubMedPubMedCentralGoogle Scholar
  45. Meinzer FC, Brooks JR, Bucci S, Goldstein G, Scholz FG, Warren JM (2004) Converging patterns of uptake and hydraulic redistribution of soil water in contrasting woody vegetation types. Tree Physiol 24:919–928.  https://doi.org/10.1093/treephys/24.8.919 CrossRefPubMedGoogle Scholar
  46. Mikkelsen BL, Rosendahl S, Jakobsen I (2008) Underground resource allocation between individual networks of mycorrhizal fungi. New Phytol 180:890–898.  https://doi.org/10.1111/j.1469-8137.2008.02623.x CrossRefPubMedGoogle Scholar
  47. Nadeem SM, Ahmad M, Zahir ZA, Javaid A, Ashraf M (2014) The role of mycorrhizae and plant growth promoting rhizobacteria (PGPR) in improving crop productivity under stressful environments. Biotechnol Adv 32:429–448.  https://doi.org/10.1016/j.biotechadv.2013.12.005 CrossRefPubMedGoogle Scholar
  48. Newberry SL, Nelson DB, Kahmen A (2017) Cryogenic vacuum artifacts do not affect plant water-uptake studies using stable isotope analysis. Ecohydrology 10:1–10.  https://doi.org/10.1002/eco.1892 CrossRefGoogle Scholar
  49. Parniske M (2008) Arbuscular mycorrhiza: the mother of plant root endosymbioses. Nat Rev Microbiol 6:763–775.  https://doi.org/10.1038/nrmicro1987 CrossRefPubMedGoogle Scholar
  50. Peñuelas J, Filella I, Lloret F et al (2000) Effects of a severe drought on water and nitrogen use by Quercus ilex and Phyllyrea latifolia. Biol Plant 43:47–53.  https://doi.org/10.1023/A:1026546828466 CrossRefGoogle Scholar
  51. Plamboeck AH, Dawson TE, Egerton-Warburton LM, North M, Bruns TD, Querejeta JI (2007) Water transfer via ectomycorrhizal fungal hyphae to conifer seedlings. Mycorrhiza 17:439–447.  https://doi.org/10.1007/s00572-007-0119-4 CrossRefPubMedGoogle Scholar
  52. Prieto I, Padilla FM, Armas C, Pugnaire FI (2011) The role of hydraulic lift on seedling establishment under a nurse plant species in a semi-arid environment. Perspect Plant Ecol Evol Syst 13:181–187.  https://doi.org/10.1016/j.ppees.2011.05.002 CrossRefGoogle Scholar
  53. Prieto I, Roldán A, Huygens D, del Mar Alguacil M, Navarro-Cano JA, Querejeta JI (2016) Species-specific roles of ectomycorrhizal fungi in facilitating interplant transfer of hydraulically redistributed water between Pinus halepensis saplings and seedlings. Plant Soil 406:15–27.  https://doi.org/10.1007/s11104-016-2860-y CrossRefGoogle Scholar
  54. Querejeta JI (2017) Soil water retention and availability as influenced by mycorrhizal symbiosis: consequences for individual plants, communities, and ecosystems. In: Johnson NC, Gehring C, Jansa JBT-MM of S (eds). Elsevier, pp 299–317Google Scholar
  55. Querejeta JI, Egerton-Warburton LM, Prieto I, Vargas R, Allen MF (2012) Changes in soil hyphal abundance and viability can alter the patterns of hydraulic redistribution by plant roots. Plant Soil 355:63–73.  https://doi.org/10.1007/s11104-011-1080-8 CrossRefGoogle Scholar
  56. Richards JH, Caldwell MM (1987) Hydraulic lift: substantial nocturnal water transport between soil layers by Artemisia tridentata roots. Oecologia 73:486–489.  https://doi.org/10.1007/BF00379405 CrossRefPubMedGoogle Scholar
  57. Saharan K, Schütz L, Kahmen A, Wiemken A, Boller T, Mathimaran N (2018) Finger millet growth and nutrient uptake is improved in intercropping with pigeon pea through “biofertilization” and “bioirrigation” mediated by arbuscular mycorrhizal fungi and plant growth promoting rhizobacteria. Front Environ Sci 6:1–11.  https://doi.org/10.3389/fenvs.2018.00046 CrossRefGoogle Scholar
  58. Sauer DB, Burroughs R (1986) Disinfection of seed surfaces with sodium hypochlorite. Phytopathol 76:745–749CrossRefGoogle Scholar
  59. Schenck NC, Smith GS (1982) Responses of six species of vesicular-arbuscular mycorrhizal fungi and their effects on soybean at four soil temperatures. New Phytol 92:193–201CrossRefGoogle Scholar
  60. Schenk HJ (2006) Root competition: beyond resource depletion. J Ecol 94:725–739.  https://doi.org/10.1111/j.1365-2745.2006.01124.x CrossRefGoogle Scholar
  61. Scholes R, Archer SR (1997) Tree-grass interactions in savannas. Annu Rev Ecol Syst 28:527–544CrossRefGoogle Scholar
  62. Schoonmaker AL, Teste FP, Simard SW, Guy RD (2007) Tree proximity, soil pathways and common mycorrhizal networks: their influence on the utilization of redistributed water by understory seedlings. Oecologia 154:455–466.  https://doi.org/10.1007/s00442-007-0852-6 CrossRefPubMedGoogle Scholar
  63. Schütz L, Gattinger A, Meier M, Müller A, Boller T, Mäder P, Mathimaran N (2018) Improving crop yield and nutrient use efficiency via biofertilization—a global meta-analysis. Front Plant Sci 8:2204.  https://doi.org/10.3389/fpls.2017.02204 CrossRefPubMedPubMedCentralGoogle Scholar
  64. Sekiya N, Yano K (2004) Do pigeon pea and sesbania supply groundwater to intercropped maize through hydraulic lift? - hydrogen stable isotope investigation of xylem waters. F Crop Res 86:167–173.  https://doi.org/10.1016/j.fcr.2003.08.007 CrossRefGoogle Scholar
  65. Simard SW, Beiler KJ, Bingham MA, Deslippe JR, Philip LJ, Teste FP (2012) Mycorrhizal networks: mechanisms, ecology and modelling. Fungal Biol Rev 26:39–60.  https://doi.org/10.1016/j.fbr.2012.01.001 CrossRefGoogle Scholar
  66. Smith DM, Jackson N a, Roberts JM, Ong CK (1999) Reverse flow of sap in tree roots and downward siphoning of water by Grevillea robusta. Funct Ecol 13:256–264.  https://doi.org/10.1046/j.1365-2435.1999.00315.x CrossRefGoogle Scholar
  67. Sorensen JN, Larsen J, Jakobsen I (2005) Mycorrhiza formation and nutrient concentration in leeks (Allium porrum) in relation to previous crop and cover crop management on high P soils. Plant Soil 273:101–114.  https://doi.org/10.1007/s11104-004-6960-8 CrossRefGoogle Scholar
  68. Subbarao MVSST, MUralikrishna G (2001) Non-starchy polysaccharides and bound phenolics acids from native and malted finger millet (Eleusine coracan Indaf-15). Food Chem 72:187–192CrossRefGoogle Scholar
  69. Vanaja M, Reddy PRR, Lakshmi NJ et al (2010) Response of seed yield and its components of red gram (Cajanus cajan L. Millsp.) to elevated CO2. Plant Soil Environ 56:458–462CrossRefGoogle Scholar
  70. Walder F, Niemann H, Natarajan M, Lehmann MF, Boller T, Wiemken A (2012) Mycorrhizal networks: common goods of plants shared under unequal terms of trade. Plant Physiol 159:789–797.  https://doi.org/10.1104/pp.112.195727 CrossRefPubMedPubMedCentralGoogle Scholar
  71. Warren JM, Brooks JR, Meinzer FC, Eberhart JL (2008) Hydraulic redistribution of water from Pinus ponderosa trees to seedlings: evidence for an ectomycorrhizal pathway. New Phytol 178:382–394.  https://doi.org/10.1111/j.1469-8137.2008.02377.x CrossRefPubMedGoogle Scholar
  72. Wu Q-S, Xia R-X (2006) Arbuscular mycorrhizal fungi influence growth, osmotic adjustment and photosynthesis of citrus under well-watered and water stress conditions. J Plant Physiol 163:417–425.  https://doi.org/10.1016/j.jplph.2005.04.024 CrossRefPubMedGoogle Scholar
  73. Zarebanadkouki M, Kim YX, Carminati A (2013) Where do roots take up water? Neutron radiography of water flow into the roots of transpiring plants growing in soil. New Phytol 199:1034–1044.  https://doi.org/10.1111/nph.12330 CrossRefPubMedGoogle Scholar
  74. Zhu YG, Smith FA, Smith SE (2003) Phosphorus efficiencies and responses of barley (Hordeum vulgare L.) to arbuscular mycorrhizal fungi grown in highly calcareous soil. Mycorrhiza 13:93–100.  https://doi.org/10.1007/s00572-002-0205-6 CrossRefPubMedGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Department of Environmental Sciences – BotanyUniversity of BaselBaselSwitzerland

Personalised recommendations