Species-specific roles of ectomycorrhizal fungi in facilitating interplant transfer of hydraulically redistributed water between Pinus halepensis saplings and seedlings

Plant and Soil

Volumn 406, Issue 1-2, 2016, Pages 15-27

  Prieto, Iván ^a   Roldán, Antonio ^a   Huygens, Dries ^b   del Mar Alguacil, María ^a   Navarro Cano, José A ^c   Querejeta, José I ^a  

^a RESEARCH GROUP ON QUALITY   (Spain)

^b GHENT UNIVERSITY   (Belgium)

^c Atmosphere and Ocean Laboratory   (Spain)

Author keywords

Aleppo pine; Ectomycorrhizal pathways; Hydraulic redistribution; Interplant water transfer; Specific root length

Indexed keywords

ABUNDANCE; CONIFEROUS TREE; ECTOMYCORRHIZA; FACILITATION; FACULTATIVE BEHAVIOR; FUNGUS; HOST-SYMBIONT INTERACTION; HYDRAULICS; MESOCOSM; ROOT ARCHITECTURE; SAPLING; SEEDLING; TRANSLOCATION; WATER UPTAKE;

FUNGI; PINUS HALEPENSIS; SUILLUS GRANULATUS; THELEPHORA TERRESTRIS;

EID: 84961207320     PISSN: 0032079X     EISSN: 15735036     Source Type: Journal    
DOI: 10.1007/s11104-016-2860-y     Document Type: Article

References (60)

1. Agerer R (ed) (1987–2006) Colour Atlas of Ectomycorrhizae. Einhorn-Verlag, Schwäbisch Gmünd
2. Agerer R (2001) Exploration types of ectomycorrhizae. Mycorrhiza 11:107–114
3. 18O in dry soils 2. Experimental. J Hydrol 64:377–397
4. Amaranthus MP, Perry D (1989) Rapid root tip and mycorrhiza formation and increased survival of Douglas-fir seedlings after soil transfer. New Forest 3:259–264
5. 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
6. Augé RM (2004) Arbuscular mycorrhizae and soil/plant water relations. Can J Soil Sci 84:373–381
7. Augé RM, Stodola AJW, Tims JE, Saxton AM (2001) Moisture retention properties of a mycorrhizal soil. Plant Soil 230:87–97
8. Bardgett RD (1991) The use of the membrane filter technique for comparative measurements of hyphal lengths in different grassland sites. Agr Ecosyst Environ 34:115–119
9. Bauerle TL, Richards JH, Smart DR, Eissenstat DM (2008) Importance of internal hydraulic redistribution for prolonging the lifespan of roots in dry soil. Plant Cell Environ 31:177–186
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
11. Bogeat-Triboulot MB, Bartoli F, Garbaye J, Marmeisse R, Tagu D (2004) Fungal ectomycorrhizal community affect root hydraulic properties and soil adherence to roots of Pinus pinaster seedlings. Plant Soil 267:213–223
12. Booth MG, Hoeksema JD (2010) Mycorrhizal networks counteract competitive effects of canopy trees on seedling survival. Ecology 91:2294–2302
13. Brooks JR, Meinzer FC, Coulombe R, Gregg J (2002) Hydraulic redistribution of soil water during summer drought in two contrasting Pacific Northwest coniferous forests. Tree Physiol 22:1107–1117
14. Brownlee C, Duddridge JA, Malibari A, Read DJ (1983) The structure and function of mycelial systems of ectomycorrhizal roots with a special reference to their role in forming inter-plant connections and providing pathways for assimilate and water transport. Plant Soil 71:433–443
15. Brundrett MC (2009) Mycorrhizal associations and other means of nutrition of vascular plants: understanding the global diversity of host plants by resolving conflicting information and developing reliable means of diagnosis. Plant Soil 320:37–77
16. Caldwell MM, Richards JH (1989) Hydraulic lift: water efflux from upper roots improves effectiveness of water uptake by deep roots. Oecologia 79:1–5
17. Caldwell MM, Dawson TE, Richards JH (1998) Hydraulic lift: consequences of water efflux from the roots of plants. Oecologia 113:151–161
18. Cardon ZG, Stark JM, Herron PM, Rasmussen JA (2013) Sagebrush carrying out hydraulic lift enhances surface soil nitrogen cycling and nitrogen uptake into inflorescences. Proc Natl Acad Sci USA 110:18988–18993
19. Dawson TE (1993) Hydraulic lift and water use by plants: implications for water balance, performance, and plant–plant interactions. Oecologia 95:565–574
20. Dawson TE (1996) Determining water use by trees and forests from isotopic, energy balance, and transpiration analyses: the roles of tree size and hydraulic lift. Tree Physiol 16:263–272
21. Domec JC, King JS, Noormets A, Treasure E, Gavazzi MJ, Sun G, McNulty SG (2010) Hydraulic redistribution of soil water by roots affects whole-stand evapotranspiration and net ecosystem carbon exchange. New Phytol 187:171–183
22. Duddridge JA, Malibari A, Read DJ (1980) Structure and function of mycorrhizal rhizomorphs with special reference to their role in water transport. Nature 287:834–836
23. 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
24. 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
25. Ehleringer JR, Osmond CB (1989) Stable isotopes. In: Pearcy RW, Ehleringer JR, Mooney HA, Rundel PW (eds) Plant physiological ecology. Kluwer Academic Publishers, London, pp 281–300
26. Eissenstat DM (1991) On the relationship between specific root length and the rate of root proliferation: a field study using citrus rootstocks. New Phytol 118:63–68
27. Filella I, Peñuelas J (2003) Indications of hydraulic lift by Pinus halepensis and its effects on the water relations of neighbour shrubs. Biol Plantarum 47:209–214
28. Flanagan LB, Ehleringer JR (1991) Stable isotope composition of stem and leaf water: applications to the study of plant water use. Funct Ecol 5:270–277
29. Fuentes D, Valdecantos A, Llovet J, Cortina J, Vallejo VR (2010) Fine-tuning of sewage sludge application to promote the establishment of Pinus halepensis seedlings. Ecol Eng 36:1213–1221
30. Gardes M, Bruns TD (1993) ITS primers with enhanced specificity for basidiomycetes—application to the identification of mycorrhizae and rusts. Mol Ecol 2:113–118
31. Grand LF, Harvey AE (1982) Quantitative measurements of ectomycorrhizae on plant roots. methods and principles of mycorrhizal research. Am Phytopathol Soc, St Paul
32. Hoagland DR, Arnon DI (1950) The water-culture method of growing plants without soil. Calif Aes Bull 347:31
33. Huang B, Eissenstat DM (2000) Linking hydraulic conductivity to anatomy in plants that vary in specific root length. J Am Soc Hortic Sci 125:260–264
34. Hummel I, Vile D, Violle C, Devaux J, Ricci B, Blanchard A, Garnier E, Roumet C (2007) Relating root structure and anatomy to whole-plant functioning in 14 herbaceous Mediterranean species. New Phytol 173:313–321
35. Kummerow J, Krause D, Jow W (1978) Seasonal changes of fine root density in the Southern Californian chaparral. Oecologia 37:201–212
36. Lehto T, Zwiazek J (2011) Ectomycorrhizas and water relations of trees: a review. Mycorrhiza 21:71–90
37. Maestre FT, Cortina J (2004) Are Pinus halepensis plantations useful as a restoration tool in semiarid Mediterranean areas? For Ecol Manag 198:303–317
38. Marjanović Ž, Uehlein N, Kaldenhoff R, Zwiazek JJ, Weiß M, Hampp R, Nehls U (2005) Aquaporins in poplar: what a difference a symbiont makes! Planta 222:258–268
39. Muhsin TM, Zwiazek JJ (2002) Ectomycorrhizas increase apoplastic water transport and hydraulic conductivity in Ulmus americana seedlings. New Phytol 153:153–158
40. Plamboeck AH, Dawson TE, Egerton-Warburton LE, North M, Bruns TD, Querejeta JI (2007) Water transfer via ectomycorrhizal fungal hyphae to conifer seedlings. Mycorrhiza 17:439–447
41. Prieto I, Ryel RJ (2014) Internal hydraulic redistribution prevents the loss of root conductivity during drought. Tree Physiol 34:39–48
42. 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
43. Prieto I, Armas C, Pugnaire FI (2012) Water release through plant roots: new insights into its consequences at the plant and ecosystem level. New Phytol 193:830–841
44. Querejeta JI, Roldan A, Albaladejo J, Castillo V (2001) Soil water availability improved by site preparation in a Pinus halepensis afforestation under semiarid climate. For Ecol Manag 149:115–128
45. Querejeta JI, Egerton-Warburton LM, Allen MF (2003) Direct nocturnal transfer from oaks to their mycorrhizal symbionts during severe soil drying. Oecologia 134:55–64
46. Querejeta JI, Egerton-Warburton LM, Allen MF (2009) Topographic position modulates the mycorrhizal response of oak trees to interannual rainfall variability. Ecology 90:649–662
47. 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
48. Richter H (1997) Water relations of plants in the field: some comments on the measurement of selected parameters. J Exp Bot 48:1–7
49. Roberts J (1976) A study of root distribution and growth in a Pinus sylvestris L. (Scots Pine) plantation in East Anglia. Plant Soil 44:607–621
50. Schoonmaker A, Teste F, Simard S, Guy R (2007) Tree proximity, soil pathways and common mycorrhizal networks: their influence on the utilization of redistributed water by understory seedlings. Oecologia 154:455–466
51. Sylvia DM (1992) Quantification of external hyphae of vesicular-arbuscular mycorrhizal fungi. Method Microbiol 24:53–65
52. Tennant D (1975) A test of the modified root intersect method of estimating root length. J Ecol 63:995–1001
53. Teste F, Simard S (2008) Mycorrhizal networks and distance from mature trees alter patterns of competition and facilitation in dry Douglas-fir forests. Oecologia 158:193–203
54. Teste F, Karst J, Jones MD, Simard S, Durall DM (2006) Methods to control ectomycorrhizal colonization: effectiveness of chemical and physical barriers. Mycorrhiza 17:51–65
55. Torres P, Honrubia M (1991) In vitro synthesis of ectomycorrhizae between Suillus collinitus (Fr.) O Kuntze and Rhizopogon roseolus (Corda) Th M Fr. with Pinus halepensis Miller. Mycotaxon 41:437–443
56. Torres P, Honrubia M (1994) Ectomycorrhizal associations proven for Pinus halepensis. Israel J Plant Sci 42:51–58
57. Unestam T (1991) Water repellency, mat formation and leaf-stimulated growth of some ectomycorrhizal fungi. Mycorrhiza 1:13–20
58. Unestam T, Sun YP (1995) Extramatrical structures of hydrophobic and hydrophilic ectomycorrhizal fungi. Mycorrhiza 5:301–311
59. 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
60. White TJ, Bruns T, Lee S et al. (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ and White TJ (Eds.). PCR protocols. a guide to methods and applications, San Diego, pp. 315–322