Exploring the role of root anatomy in P-mediated control of colonization by arbuscular mycorrhizal fungi

Botany

Volumn 88, Issue 2, 2010, Pages 165-173

  Sharda, J N ^a   Koide, R T ^a  

^a PENNSYLVANIA STATE UNIVERSITY   (United States)

Author keywords

Arbuscular mycorrhizal colonization; Intercellular air space; Passage cells; Phosphorus; Root anatomy; Suberized hypodermis

Indexed keywords

ANATOMY; ARBUSCULAR MYCORRHIZA; PHOSPHORUS; ROOT COLONIZATION;

ARBUSCULAR; FUNGI; MAGNOLIOPHYTA;

EID: 77449135637     PISSN: 19162804     EISSN: None     Source Type: Journal    
DOI: 10.1139/B09-105     Document Type: Article

References (55)

1. Abbott, L.K., Robson, A.D., and De Boer, G. 1984. The effect of phosphorus on the formation of hyphae in soil by the vesicular-arbuscular mycorrhizal fungus, Glomus fasciculatum. New Phytol. 97(30): 437-446. doi:10.1111/j.1469-8137.1984.tb03609.x.
2. Akiyama, K., Matsuoka, H., and Hayashi, H. 2002. Isolation and identification of a phosphate deficiency-induced C-glycosylflavonoid that stimulates arbuscular mycorrhiza formation in melon roots. Mol. Plant Microbe Interact. 15(4): 334-340. doi:10.1094/ MPMI.2002.15.4.334. PMID:12026171.
3. Amijee, F., Tinker, P.B., and Stribley, D.P. 1989. The development of endomycorrhizal root systems. VII. A detailed study of effects of soil phosphorus on colonization. New Phytol. 111(3): 435-446. doi:10.1111/j.1469-8137.1989.tb00706.x.
4. APG II. 2003. An update of the Angiosperm Phylogeny Group classification for orders and families of flowering plants: APG II. Bot. J. Linn. Soc. 141(4): 399-436. doi:10.1046/j.1095-8339. 2003.t01-1-00158.x.
5. Baylis, G.T.S. 1967. Experiments on the ecological significance of phycomycetous mycorrhizas. New Phytol. 66(2): 231-243. doi:10.1111/j.1469-8137.1967.tb06001.x.
6. Bécard, G., Douds, D.D., and Pfeffer, P.E. 1992. Extensive in vitro hyphal growth of vesicular-arbuscular mycorrhizal fungi in the presence of CO2 and flavonols. Appl. Environ. Microbiol. 58(3): 821-825. PMID:16348673.
7. Bonfante-Fasolo, P. 1984. Anatomy and morphology of VA mycorrhizae. In VA Mycorrhizas. Edited by C.L. Powell and D.J. Bagyaraj. CRC Press, Boca Raton, Fla. pp. 5-33.
8. Brundrett, M., and Kendrick, B. 1990. The roots and mycorrhizas of herbaceous woodland plants.II. Structural aspects of morphology. New Phytol. 114(3): 469-479. doi:10.1111/j.1469-8137.1990.tb00415.x.
9. Brundrett, M.C., Piché, Y., and Peterson, R.L. 1985. A developmental-study of the early stages in vesicular-arbuscular mycorrhiza formation. Can. J. Bot. 63(2): 184-194. doi:10.1139/b85-021.
10. Brundrett, M.C., Kendrick, B., and Peterson, C.A. 1991. Efficient lipid staining in plant material with Sudan red 7B or Fluorol yellow 088 in polyethylene glycol-glycerol. Biotech. Histochem. 66(3): 111-116. doi:10.3109/10520299109110562. PMID:1716161.
11. Clarke, C., and Mosse, B. 1981. Plant growth responses to vesicular-arbuscular mycorrhiza. XII. Field inoculation responses of barley at two soil P levels. New Phytol. 87(4): 695-703. doi:10. 1111/j.1469-8137.1981.tb01704.x.
12. Daft, M.J., and Nicolson, T.H. 1969. Effect of Endogone mycorrhiza on plant growth. II. Influence of soluble phosphate on endophyte and host in maize. New Phytol. 68(4): 945-952. doi:10.1111/j.1469-8137.1969.tb06494.x.
13. Dickson, S. 2004. The Arum-Paris continuum of mycorrhizal symbioses. New Phytol. 163(1): 187-200. doi:10.1111/j.1469-8137.2004.01095.x.
14. Elias, K.S., and Safir, G.R. 1987. Hyphal elongation of Glomus fasciculatus in response to root exudates. Appl. Environ. Microbiol. 53(8): 1928-1933. PMID:16347418.
15. Enstone, D.E., and Peterson, C.A. 1997. Suberin deposition and band plasmolysis in the corn (Zea mays) root exodermis. Can. J. Bot. 75(7): 1188-1199. doi:10.1139/b97-832.
16. Enstone, D.E., Peterson, C.A., and Ma, F.S. 2003. Root endodermis and exodermis: Structure, function, and responses to the environment. J. Plant Growth Regul. 21(4): 335-351. doi:10.1007/s00344-003-0002-2.
17. Garriock, M.L., Peterson, R.L., and Ackerley, C.A. 1989. Early stages in colonization of Allium porrum (leek) roots by the vesicular arbuscular mycorrhizal fungus, Glomus versiforme. New Phytol. 112(1): 85-92. doi:10.1111/j.1469-8137.1989.tb00312.x.
18. Gianinazzi-Pearson, V., Branzanti, B., and Gianinazzi, S. 1989. In vitro enhancement of spore germination and early hyphal growth of a vesicular-arbuscular mycorrhizal fungus by host root exudates and plant flavonoids. Symbiosis, 7(3): 243-255.
19. Graham, J.H., Leonard, R.T., and Menge, J.A. 1981. Membrane-mediated decrease in root exudation responsible for phosphorus inhibition of vesicular-arbuscular mycorrhiza formation. Plant Physiol. 68(3): 548-552. doi:10.1104/pp.68.3.548. PMID:16661955.
20. Hayman, D.S. 1983. The physiology of vesicular-arbuscular endo-mycorrhizal symbiosis. Can. J. Bot. 61(3): 944-963. doi:10.1139/b83-105.
21. Jasper, D.A., Robson, A.D., and Abbott, L.K. 1979. Phosphorus and the formation of vesicular-arbuscular mycorrhizas. Soil Biol. Biochem. 11(5): 501-505. doi:10.1016/0038-0717(79)90009-9.
22. Koide, R.T. 1985. The nature of growth depressions in sunflower caused by vesicular-arbuscular mycorrhizal infection. New Phytol. 99(3): 449-462. doi:10.1111/j.1469-8137.1985.tb03672.x.
23. Koide, R.T., and Li, M. 1990. On host regulation of the vesicular-arbuscular mycorrhizal symbiosis. New Phytol. 114(1): 59-74. doi:10.1111/j.1469-8137.1990.tb00373.x.
24. Koide, R.T., and Mooney, H.A. 1987. Spatial variation in inoculum potential of vesicular arbuscular mycorrhizal fungi caused by formation of gopher mounds. New Phytol. 107(1): 173-182. doi:10.1111/j.1469-8137.1987.tb04891.x.
25. Koide, R.T., and Schreiner, R.P. 1992. Regulation of the vesicular-arbuscular mycorrhizal symbiosis. Annu. Rev. Plant Physiol. Plant Mol. Biol. 43(: 557-581.
26. Machlis, L., and Torrey, J.G. 1956. Plants in action. Freeman, San Francisco,Calif.
27. Matsubara, Y., Uetake, Y., and Peterson, R.L. 1999. Entry and colonization of Asparagus officinalis roots by arbuscular mycorrhizal fungi with emphasis on changes in host microtubules. Can. J. Bot. 77(8): 1159-1167. doi:10.1139/cjb-77-8-1159.
28. McArthur, D.A.J., and Knowles, N.R. 1992. Resistance responses of potato to vesicular-arbuscular mycorrhizal fungi under varying abiotic phosphorus levels. Plant Physiol. 100(1): 341-351. doi:10.1104/pp.100.1.341. PMID:16652967
29. MINITAB. 1998. Release 12 for Windows. Minitab. Penn State University, Penn.
30. Modjo, H.S., and Hendrix, J.W. 1986. The mycorrhizal fungus Glomus macrocarpum as a cause of tobacco stunt disease. Phytopathology, 76(7): 688-691. doi:10.1094/Phyto-76-688.
31. Mosse, B. 1973. Plant growth responses to vesicular-arbuscular mycorrhiza.IV. In soil given additional phosphate. New Phytol. 72(1): 127-136. doi:10.1111/j.1469-8137.1973.tb02017.x.
32. Nagahashi, G., and Douds, D.D., Jr. 1997. Appressorium formation by AM fungi on isolated cell walls of carrot roots. New Phytol. 136(2): 299-304. doi:10.1046/j.1469-8137.1997.00739.x.
33. Nagahashi, G., Douds, D.D., Jr., and Abney, G.D. 1996. Phosphorus amendment inhibits hyphal branching of the VAM fungus Gigaspora margarita directly and indirectly through its effect on root exudation. Mycorrhiza, 6(5): 403-408. doi:10.1007/s005720050139.
34. Olsson, P.A., van Aarle, I.M., Allaway, W.G., Ashford, A.E., and Rouhier, H. 2002. Phosphorus effects on metabolic processes in monoxenic arbuscular mycorrhiza cultures. Plant Physiol. 130(3): 1162-1171. doi:10.1104/pp.009639. PMID:12427983.
35. Peng, S., Eissenstat, D.M., Graham, J.H., Williams, K., and Hodge, N.C. 1993. Growth depression in mycorrhizal citrus at high-phosphorus supply: analysis of carbon costs. Plant Physiol. 101(3): 1063-1071. PMID:12231758.
36. Perumalla, C.J., Peterson, C.A., and Enstone, D.E. 1990. A survey of angiosperm species to detect hypodermal Casparian bands. I. Roots with a uniseriate hypodermis and epidermis. Bot. J. Linn. Soc. 103(2): 93-112. doi:10.1111/j.1095-8339.1990.tb00176.x.
37. Peterson, C.A. 1989. Significance of the exodermis in root function. In Structural and functional aspects of transport in roots. Edited by B.C. Loughman, O. Gasparikova and J. Kolek. Kluwer Academic Publishers, Dordrecht, the Netherlands. pp. 35-40.
38. Peterson, C.A., and Enstone, D.E. 1996. Functions of passage cells in the endodermis and exodermis of roots. Physiol. Plant. 97(3): 592-598. doi:10.1111/j.1399-3054.1996.tb00520.x.
39. Pinior, A., Wyss, U., Piche, Y., and Vierheilig, H. 1999. Plants colonized by AM fungi regulate further root colonization by AM fungi through altered root exudation. Can. J. Bot. 77(6): 891-897. doi:10.1139/cjb-77-6-891.
40. Raskin, I. 1983. Volume, density, thickness, and internal gas volume. HortScience, 18(5): 698-699.
41. Ratnayake, M., Leonard, R.T., and Menge, J.A. 1978. Root exudation in relation to supply of phosphorus and its possible relevance to mycorrhizal formation. New Phytol. 81(3): 543-552. doi:10.1111/j.1469-8137.1978.tb01627.x.
42. Same, B.I., Robson, A.D., and Abbott, L.K. 1983. Phosphorus, soluble carbohydrates and endomycorrhizal infection. Soil Biol. Biochem. 15(5): 593-597. doi:10.1016/0038-0717(83)90055-X.
43. Schwab, S.M., Menge, J.A., and Leonard, R.T. 1983. Quantitative and qualitative effects of phosphorus on extracts and exudates of sudangrass roots in relation to vesicular-arbuscular mycorrhiza formation. Plant Physiol. 73(3): 761-765. doi:10.1104/pp. 73.3.761. PMID:16663297.
44. Sharda, J.N., and Koide, R.T. 2008. Can hypodermal passage cell distribution limit root penetration by mycorrhizal fungi? New Phytol. 180(3): 696-701. doi:10.1111/j.1469-8137.2008.02600.x. PMID:18761635.
45. Shishkoff, N. 1987. Distribution of the dimorphic hypodermis of roots in angiosperm families. Ann. Bot. (Lond.), 60(1): 1-15.
46. Shishkoff, N. 1989. Zoospore encystment pattern and germination on onion roots, and the colonization of hypodermal cells by Pythium coloratum. Can. J. Bot. 67(1): 258-262. doi:10.1139/ b89-035.
47. Smith, S.E., and Read, D.J. 1997. Mycorrhizal Symbiosis. 2nd ed. Academic Press, London, UK.
48. Smith, F.A., and Smith, S.E. 1997. Structural diversity in (vesicular)-arbuscular mycorrhizal symbioses. New Phytol. 137(3): 373-388. doi:10.1046/j.1469-8137.1997.00848.x.
49. Smith, S.E., Smith, F.A., and Jakobsen, I. 2003. Mycorrhizal fungi can dominate phosphate supply to plants irrespective of growth responses. Plant Physiol. 133(1): 16-20. doi:10.1104/pp.103.024380. PMID:12970469.
50. Takemoto, D., and Hardham, A.R. 2004. The cytoskeleton as a regulator and target of biotic interactions in plants. Plant Physiol. 136(4): 3864-3876. doi:10.1104/pp.104.052159. PMID:15591444.
51. Tawaraya, K., Watanabe, S., Yoshida, E., and Wagatsuma, T. 1996. Effect of onion (Allium cepa) root exudates on the hyphal growth of Gigaspora margarita. Mycorrhiza, 6(1): 57-59. doi:10.1007/s005720050106.
52. Tawaraya, K., Hashimoto, K., and Wagatsuma, T. 1998. Effect of root exudate fractions from P-deficient and P-sufficient onion plants on root colonisation by the arbuscular mycorrhizal fungus Gigaspora margarita. Mycorrhiza, 8(2): 67-70. doi:10.1007/s005720050214.
53. Thomson, B.D., Robson, A.D., and Abbott, L.K. 1986. Effects of phosphorus on the formation of mycorrhizas by Gigaspora calospora and Glomus fasciculatum in relation to root carbohydrates. New Phytol. 103(4): 751-765. doi:10.1111/j.1469-8137. 1986.tb00850.x.
54. Wang, X.L., McCully, M.E., and Canny, M.J. 1995. Branch roots of Zea. V. Structural features that may influence water and nutrient transport. Bot. Acta, 108: 209-219.
55. Watanabe, F.S., and Olsen, S.R. 1965. Test of an ascorbic acid method for determining phosphorus in water and NaHCO3 extracts from soil. Soil Sci. Soc. Proc. 29: 677-678.