Plant and Soil

, Volume 248, Issue 1–2, pp 21–30 | Cite as

The evolution of physiology and development in the cluster root: teaching an old dog new tricks?

  • Keith R. Skene


In this paper we examine the key elements of cluster or proteoid roots, and trace their origins back to regular root properties. By viewing the root system as being composed of two categories of surface, the high transport capacity (HTC) area, just behind the meristem, and the low transport capacity (LTC) area (the rest of the root system), based on export and import capacities, we examine root system architecture in terms of structure–function relationships, and conclude that measuring total root exudation per unit area, volume or mass will not give useful comparative data for root transport properties. Furthermore, the cluster root represents a manipulation of the HTC to LTC root surface area ratio. Increased exudation and P uptake may be no higher in individual rootlets than in other HTC regions of the root system. We also examine the transformation theory (the theory of form resulting from a series of forces, which, when altered, lead to a change, or transformation in form) as an explanation of cluster root evolution, and conclude that the cluster root requires only a change in pericycle response to depleted internal nutrient levels, with the other characteristics representing consequences stemming from the form and constraints of the root system.

cluster roots high transport capacity (HTC) low transport capacity (LTC) morphogenesis proteoid roots pseudo-cluster root root architecture transformation theory 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Armbuster W S 1997 Exaptations link evolution of plant-herbivore and plant-pollinator interactions: a phylogenetic inquiry. Ecology 78, 1661–1672.Google Scholar
  2. Arnold E N 1994 Investigating the origin of performance advantage: adaptation, exaptation and lineage effects. In Phylogenetics and Ecology. Eds. P Eggleton and R Vane-Wright. pp. 123–168. Academic Press, London.Google Scholar
  3. Barlow P W 1976 Towards an understanding of the behaviour of root meristems. J. Theor. Biol. 57, 433–451.PubMedGoogle Scholar
  4. Beeckman T, Burssens S and Inzé D 2001 The peri-cell-cycle in Arabidopsis. J. Exp. Bot. 52, 403–412.PubMedGoogle Scholar
  5. Bertrand H, Pinochet X, Cleyet Marel JC 1996 Inducing pseudonodules on colza roots by hormone treatment and the accompanying morphological changes in the root system. Ocl-Oleagineux Corps Gras Lipides 3, 213–219.Google Scholar
  6. Bolton H, Fredrickson JK and Elliot LF 1992 Microbial ecology of the rhizosphere. In Soil Microbial Ecology. Ed. F B Metting. pp. 27–63. Marcel Dekker, New York.Google Scholar
  7. Bowen G D 1968 Phosphate uptake by mycorrhizas and uninfected roots of Pinus radiata in relation to root distribution. Int. Cong. Soil Sci. Trans. No. 9 Vol. II, 219–228.Google Scholar
  8. Bowen G D and Rovira A D 1991 The rhizosphere: the hidden half of the hidden half. In Plant roots — the Hidden Half. Eds. Y Waisel, A Eshel and U Kafkafi. pp. 641–649. Marcel Dekker, New York.Google Scholar
  9. Cowling R M, Mustart P J, Laurie H and Richards M B 1994 Species diversity: functional diversity and functional redundancy in fynbos communities. S. Afr. J. Sci. 90, 333–337.Google Scholar
  10. Curio E 1973 Towards a methodology of teleonomy. Experientia 29, 1045–1058.PubMedGoogle Scholar
  11. Diem H G and Arahou M 1996 A review of cluster root formation: a primary strategy of Casuarinaceae to overcome soil nutrient deficiency. In Recent Casuarina Research and Development. Eds. K Pinyopusarek, J W Turnbull and S J Midgley. pp. 51–58. CSIRO, Canberra.Google Scholar
  12. Dinkelaker B, Hengeler C and Marschner H 1995 Distribution and function of proteoid roots and other root clusters. Bot. Acta 108, 183–200.Google Scholar
  13. Goodwin BC 1985 What are the causes of morphogenesis? BioEssays 3, 32–36PubMedGoogle Scholar
  14. Gould S J and Lewontin R C 1979 The spandrels of San Marco and the Panglossian paradigm: a critique of the adaptionist argument. Proc. R. Soc. London B 205, 581–598.Google Scholar
  15. Gould S J and Vrba E S 1982 Exaptation — a missing term in the science of form. Palaeobiology. 8: 4–15.Google Scholar
  16. Grayston S J, Vaughan D and Jones D 1996 Rhizosphere carbon flow in trees, in comparison with annual plants: the importance of root exudation and its impact onmicrobial activity and nutrient availability. Appl. Soil Ecol. 5, 29–56.Google Scholar
  17. Gunning BES 1978 Age related and origin-related control of the numbers of plasmodesmata in cell walls of developing Azolla roots. Planta 143, 181–190.Google Scholar
  18. Hagstrom J, James W M and Skene KR 2000 A comparison of structure, development and function in cluster roots of Lupinus albus L. under phosphate and iron stress. Plant Soil 232, 81–90.Google Scholar
  19. Jain P S, Shrivastava P, Narayana H S 1983 Pseudo-nodules in Cicer arietinum L. Curr. Sci. India 52, 889–890.Google Scholar
  20. Jing Y, Zhang B T and Shan X Q 1990 Pseudo-nodules formation on barley roots induced by rhizobium astragali. FEMS Microbiol. Lett. 69, 123–127.Google Scholar
  21. Leisen E, Häussling M and Marschner H 1990 Einfluss von Stickstoff-Form und-Konzentration und saurer Benebelung auf pH-Veränderungen in der Rhizosphäre von Fichten (Picea abies (L.) Karst.). Forstwiss. Cbl. 109, 275–286.Google Scholar
  22. Marschner H 1995 Mineral Nutrition of Higher Plants. Academic Press, London.Google Scholar
  23. Marschner H, Romheld V and Cakmak I 1987. Root-induced changes in the rhizosphere: importance for the mineral nutrition of plants. J. Plant Nutr. 10, 1175–1184.Google Scholar
  24. McDougall B M and Rovira A D 1970Sites of exudation of 14C-labelled compounds from wheat roots. New Phytol. 69, 999–1003.Google Scholar
  25. Neumann G, Massonneau A, Martinoia E and Romheld V 1999 Physiological adaptations to phosphorus deficiency during proteoid root development in white lupin. Planta 208, 373–382.Google Scholar
  26. Neumann G, Massonneau A, Dinkelaker B, Hengeler C, Romheld V and Martinoia E 2000 Physiological aspects of cluster root function and development in phosphorus-deficient white lupin (Lupinus albus L.). Ann. Bot. 85, 909–920.Google Scholar
  27. Porat R, Lu PZ and O'Neill SD 1998 Arabidopsis SKP1, a homologue of a cell cycle regulator gene, is predominantly expressed in meristematic cells. Planta 204, 345–351.PubMedGoogle Scholar
  28. Skene K R 1998 Cluster roots: some ecological considerations. J. Ecol. 86, 1060–1064.Google Scholar
  29. Skene K R 2000 Pattern formation in cluster roots: some developmental and evolutionary considerations. Ann. Bot. 85, 901–908.Google Scholar
  30. Skene K R 2001 Cluster roots: model experimental tools for key biological problems. J. Exp. Bot. 52, 479–485.Google Scholar
  31. Skene K R and James W M 2000 A comparison of the effects of auxin on cluster root initiation and development on Grevillea robusta Cunn. Ex R. Br. (Proteaceae) and in the genus Lupinus (Leguminosae). Plant Soil 219, 221–229.Google Scholar
  32. Skene K R, Raven J A and Sprent J I 1998 Aspects of cluster root development in Grevillea robusta (Proteaceae). I. Xylem, pericycle, cortex and epidermis in a determinate root and in an indeterminate, lateral root. New Phytol. 138, 733–742.Google Scholar
  33. Tinbergen N 1967 Adaptive features of the black-headed gull, Larus ridibandus. Proc. 14th Int. Ornithol. Cong. 43–59.Google Scholar
  34. Thompson D W 1917 On Growth and Form. First Edition. Cambridge University Press, Cambridge.Google Scholar
  35. Thomas H 1994 Resource rejection by higher plants. In Resource Capture by Crops. Eds. J L Monteith, R K Scott and M H Unsworth. pp. 375–385. Nottingham University Press, Nottingham.Google Scholar
  36. Turing A M 1952 The chemical basis of morphogenesis. Phil. Trans. R. Soc. B 237, 37–72.Google Scholar
  37. Wang H, Qi Q, Schorr P, Cutler AJ, Crosby WL and Fowke LC 1998 ICK1, a cyclin-dependent protein kinase inhibitor from Arabidopsis thaliana interacts with with Cdc2a and CycD3, and its expression is induced by abscisic acid. Plant J. 15, 501–510.PubMedGoogle Scholar
  38. Watt M and Evans J R 1999 Linking development and determinancy with organic acid efflux from proteoid roots of white lupin grown with low phosphorus and ambient or elevated atmospheric CO2 concentration. Plant Physiol. 120, 705–716.PubMedGoogle Scholar
  39. Williams G C 1966 Adaptation and Natural Selection. Princeton University Press, Princeton.Google Scholar
  40. Wolpert L 1971 Positional information and pattern formation. Curr. Top. Dev. Biol. 6, 183–224.PubMedGoogle Scholar

Copyright information

© Kluwer Academic Publishers 2003

Authors and Affiliations

  • Keith R. Skene
    • 1
  1. 1.Division of Environmental and Applied Biology, Institute of Biological SciencesUniversity of DundeeDundeeScotland

Personalised recommendations