Plant and Soil

, Volume 371, Issue 1–2, pp 167–177 | Cite as

Interspecific competition in Arabidopsis thaliana: root hairs are important for competitive effect, but not for competitive response

Regular Article

Abstract

Background and aims

The role of root hairs in intraspecific competition for Phosporus (P) is well examined, but their importance during interaction with other plant species is unknown, as is the differential meaning for competitive effect and response. This study aims to fill this gap of knowledge.

Methods

Competitive abilities of Arabidopsis thaliana wildtype and mutants with aberrant root hair phynotypes (root hair deficient, rhd2-1 or excessive root hair density, prc1-1) were examined in a pot-experiment with P-deficient sand. Competitive effects on a phytometer (Hieracium pilosella) or on A. thaliana itself were assessed as well as competitive responses to species mixtures.

Results

In intraspecific interaction, the competitive effect of wildtype was superior to that of rhd2-1 or prc1-1. This was much less pronounced in interspecific interaction. Competitive response was entirely uniform between Arabidopsis root phenotypes.

Conclusions

The notion that root hairs are important for competition for P should be differentiated. With A. thaliana root hairs less important in inter- than in intraspecific interaction and with root hairs entirely unimportant for competitive response, functional mechanisms of competition for P appear quite complex. Such differential importance of root traits in different facets of competition might well be more common than previously thought.

Keywords

Arabidopsis thaliana Competitive effect Competitive response Interspecific interaction Root hair deficiency Species mixture 

Abbreviations

P

Phosphorus

PFD

Photon flux density

SRA

Specific root area

TDW

Total dry weight

ZOI

Zone of influence

Notes

Acknowledgement

The authors would like to thank their colleagues at the Institute of Botany in Regensburg for support and helpful contributions to the project, especially Ingeborg Lauer for assistance with plant harvest and root photography. We are grateful to Iris Finkemeier (LMU Munich) and two anonymous reviewers for helpful comments on an earlier draft.

References

  1. Akaike H (1978) A Bayesian analysis of the minimum AIC procedure. Ann Inst Stat Math 30:9–14CrossRefGoogle Scholar
  2. Armas C, Pugnaire FI (2011) Plant neighbour identity matters to belowground interactions under controlled conditions. PLoS One 6:e27791PubMedCrossRefGoogle Scholar
  3. Bates TR, Lynch JP (2000) Plant growth and phosphorus accumulation of wild type and two root hair mutants of Arabidopsis thaliana (Brassicaceae). Am J Bot 87:958–963PubMedCrossRefGoogle Scholar
  4. Bates TR, Lynch JP (2001) Root hairs confer a competitive advantage under low phosphorus availability. Plant Soil 236:243–250CrossRefGoogle Scholar
  5. Bolan NS (1991) A critical review on the role of mycorrhizal fungi in the uptake of phosphorus by plants. Plant Soil 134:189–207CrossRefGoogle Scholar
  6. Brachi B, Aimé C, Glorieux C, Roux F (2012) Adaptive value of phenological traits in stressful environments: predictions based on seed production and laboratory natural selection. PLoS One 7:e32069PubMedCrossRefGoogle Scholar
  7. Brown LK, George TS, Thompson JA, Wright G, Lyon J, Dupuy L, Hubbard SF, White PJ (2012) What are the implications of variation in root hair length in tolerance to phosphorus deficiency in combination with water stress in barley (Hordeum vulgare)? Ann Bot 110:319–328PubMedCrossRefGoogle Scholar
  8. Cahill JF Jr, Kembel SW, Gustafson DJ (2005) Differential genetic influences on competitive effect and response in Arabidopsis thaliana. J Ecol 93:958–967CrossRefGoogle Scholar
  9. Casper BB, Jackson RB (1997) Plant competition underground. Annu Rev Ecol Syst 28:545–570CrossRefGoogle Scholar
  10. Casper BB, Schenk HJ, Jackson RB (2003) Defining a plant’s belowground zone of influence. Ecol 84:2313–2321CrossRefGoogle Scholar
  11. Clarkson DT (1985) Factors affecting nutrient acquisition by plants. Annu Rev Plant Physiol 36:77–115CrossRefGoogle Scholar
  12. Dodd AN, Salathia N, Hall A, Kevei E, Toth R, Nagy F, Hibberd MJ, Millar AJ, Webb AAR (2005) Plant circadian clocks increase photosynthesis, growth survival, and competitive advantage. Science 309:630–633PubMedCrossRefGoogle Scholar
  13. Elser JJ, Bracken MES, Cleland EE, Gruner DS, Harpole WS, Hillebrand H, Ngai JT, Seabloom EW, Shurin JB, Smith JE (2007) Global analysis of nitrogen and phosphorus limitation of primary producers in freshwater, marine and terrestrial ecosystemes. Ecol Lett 10:1135–1142PubMedCrossRefGoogle Scholar
  14. Esch JJ, Oppenheimer DG, Marks MD (1994) Characterization of a weak allele of teh GL1 gene of Arabidopsis thaliana. Plant Mol Biol 24:203–207PubMedCrossRefGoogle Scholar
  15. Fagard M, Desnos T, Desprez T, Goubet F, Refregier G, Mouille G, McCann M, Rayon C, Vernhettes S, Höfte H (2000) PROCUSTE1 encodes a cellulose synthase required for normal cell elongation specifically in dark-grown hypocotyls of Arabidopsis. Plant Cell 12:2409–2423PubMedGoogle Scholar
  16. Fitter AH, Williamson L, Linkohr B, Leyser O (2002) Root system architecture determines fitness in an Arabidopsis mutant in competition for immobile phosphate ions but not for nitrate ions. Proc R Soc Lond 269:2017–2022CrossRefGoogle Scholar
  17. Fynn RWS, Morris CD, Kirkman KP (2005) Plant strategies and trait-offs influence trends in competitive ability along gradients of soil fertility and disturbance. J Ecol 93:384–394CrossRefGoogle Scholar
  18. Gages DJ, Westcott M (1978) Zone of influence models for competition in plantations. Adv Appl Probab 10:499–537CrossRefGoogle Scholar
  19. Gahoonia TS, Nielsen NE (1997) Variation in root hairs of barley cultivars doubled soil phosphorus uptake. Euphytica 98:177–182CrossRefGoogle Scholar
  20. Gahoonia TS, Nielsen NE, Joshi PA, Jahoor A (2001) A root hairless barley mutant for elucidating genetic of root hairs and phosphorus uptake. Plant Soil 235:211–219CrossRefGoogle Scholar
  21. Gibson DJ, Conolly J, Hartnett DC, Weidenhamer JD (1999) Designs for greenhouse studies of interactions between plants. J Ecol 87:1–16CrossRefGoogle Scholar
  22. Gidman E, Goodacre R, Emmett B, Smith AR, Gwynn-Jones D (2003) Investigating plant-plant interference by metabolic fingerprinting. Phytochemistry 63:705–710PubMedCrossRefGoogle Scholar
  23. Gilbert N (2009) The disappearing nutrient. Nature 461:716–718PubMedCrossRefGoogle Scholar
  24. Goldberg DE (1990) Components of resource competition in plant communities. In: Grace JB, Tilman D (eds) Perspectives on plant competition. Academic Press, San Diego, pp 27–49Google Scholar
  25. Goldberg DE, Landa K (1991) Competitive effect and response: hierarchies and correlated traits in the early stages of competition. J Ecol 79:1013–1030CrossRefGoogle Scholar
  26. Grime JP (1973) Competitive exclusion in herbaceous vegetation. Nature 242:344–347CrossRefGoogle Scholar
  27. Grime JP, Hodgson JG, Hunt R (2007) Comparative plant biology—a functional approach to common British species. Castlepoint Press, Colvend, 748 pGoogle Scholar
  28. Grubb PJ (1977) The maintenance of species-richness in plant communities: the importance of the regeneration niche. Biol Rev 52:107–145CrossRefGoogle Scholar
  29. Ho MD, Rosas JC, Brown KM, Lynch JP (2005) Root architectural tradeoffs for water and phosphorus acquisition. Funct Plant Biol 32:737–748CrossRefGoogle Scholar
  30. Holford ICR (1997) Soil phosphorus: its measurement, and its uptake by plants. Aust J Soil Res 35:227–239CrossRefGoogle Scholar
  31. Ishida T, Kurata T, Okada K, Wada T (2008) A genetic regulatory network in the development of trichomes and root hairs. Annu Rev Plant Biol 59:365–386PubMedCrossRefGoogle Scholar
  32. Itoh S, Barber SA (1983) Phosphorus uptake by six plant species as related to root hairs. Agron J 75:457–461CrossRefGoogle Scholar
  33. Jakobsen I, Chen B, Munkvold L, Lundsgaard T, Zhu Y-D (2005) Contrasting phosphate acquisition of mycorrhizal fungi with that of root hairs using the root barley mutant. Plant Cell Environ 28:928–938CrossRefGoogle Scholar
  34. Jones MA, Raymond MJ, Yang Z, Smirnoff N (2007) NADPH oxidase-dependent reactive oxygen species formation required for root growth depends on ROP GTPase. J Exp Bot 58:1261–1270PubMedCrossRefGoogle Scholar
  35. Kandlbinder A, Finkemeier I, Wormuth D, Hanitzsch M, Dietz K-J (2004) The antioxidant status of photosynthesizing leaves under nutrient deficiency: redox regulation, gene expression and antioxidant activity in Arabidopsis thaliana. Physiol Plant 120:63–73PubMedCrossRefGoogle Scholar
  36. Lamb EG, Cahill JF Jr (2006) Consequences of differing competitive abilities between junvenile and adult plants. Oikos 112:502–512CrossRefGoogle Scholar
  37. Larkin JC, Oppenheimer DG, Lloyd AM, Paparozzi ET, Marks MD (1994) Roles of the GLABROUS1 and TRANSPARENT TESTA GLABRA genes in Arabidopsis trichome development. Plant Cell 6:1065–1076PubMedGoogle Scholar
  38. Lau JA, Shaw RG, Reich PB, Tiffin P (2010) Species interactions in a changing environment: elevated CO2 alters the ecological and potential evolutionary consequences of competition. Evol Ecol Res 12:435–455Google Scholar
  39. Li L, Yang S, Li X, Zhang F, Christie P (1999) Interspecific complementarity and competitive interactions between intercropped maize and faba bean. Plant Soil 212:105–114CrossRefGoogle Scholar
  40. Lynch JP (2007) Roots of the second green revolution. Aust J Bot 55:493–512CrossRefGoogle Scholar
  41. Marks MD, Feldmann KA (1989) Trichome development of Arabidopsis thaliana. I. T-DNA tagging of the GLABROUS1 gene. Plant Cell 1:1043–1050PubMedGoogle Scholar
  42. Oberdorfer E (2001) Pflanzensoziologische Exkursionsflora für Deutschland und angrenzende Gebiete. Ulmer, StuttgartGoogle Scholar
  43. Oppenheimer DG, Herman PL, Sivakumaran S, Esch J, Marks MD (1991) A myb gene required for leaf trichome differentiation in Arabidopsis is expressed in stipules. Cell 67:483–493PubMedCrossRefGoogle Scholar
  44. Paredez A, Persson S, Ehrhardt DW, Somerville CR (2008) Genetic evidence that cellulose synthase activity influences microtubule cortical array organization. Plant Physiol 147:1723–1734PubMedCrossRefGoogle Scholar
  45. Persson S, Paredez A, Carroll A, Palsdottir H, Doblin M, Poindexter P, Khitrov N, Auer M, Somerville CR (2007) Genetic evidence for three unique components in primary cell-wall cellulose synthase complexes in Arabidopsis. Proc Natl Acad Sci USA 25:15566–15571CrossRefGoogle Scholar
  46. Sánchez-Rodríguez C, Bauer S, Hématy K, Saxe F, Ibàñez AB, Vodemaier V, Konlechner C, Sampathkumar A, Rüggeberg M, Aichinger E, Neumetzler L, Burgert I, Somerville C, Hauser M-T, Persson S (2012) CHITINASE-LIKE/POM-POM1 and its homolog CTL2 are glucan-interacting proteins important for cellulose biosynthesis in Arabidopsis. Plant Cell 24:589–607PubMedCrossRefGoogle Scholar
  47. Schiefelbein J, Somerville S (1990) Genetic control of root hair development in Arabidopsis thaliana. Plant Cell 2:235–243PubMedGoogle Scholar
  48. Shindo C, Bernasconi G, Hardtke CS (2008) Intraspecific competition reveals conditional fitness effects of single gene polymorphism at the Arabidopsis root growth regulator BRX. New Phytol 180:71–80PubMedCrossRefGoogle Scholar
  49. Singh SK, Fischer U, Singh M, Grebe M, Marchant A (2008) Insight into the early steps of root hair formation revealed by the procuste I cellulose synthase mutant of Arabidopsis thaliana. BMC Plant Biol 8, doi: 10.1186/1471-2229-8-57
  50. Smith SE, Smith FA, Jakobsen I (2003) Mycorrhizal fungi can dominate phosphate supply to plants irrespective of growth responses. Plant Physiol 133:16–20PubMedCrossRefGoogle Scholar
  51. Suding KN, Goldberg DE (2001) Do disturbances alter competitive hierarchies? Mechanisms of change following gap creation. Ecology 82:2133–2149CrossRefGoogle Scholar
  52. Tilman D (1982) Resource competition and community structure. Princeton University Press, PrincetonGoogle Scholar
  53. Tinker PB, Nye PH (2000) Solute movement in the rhizosphere. Oxford University Press, New YorkGoogle Scholar
  54. Walk TC, Jaramillo R, Lynch JP (2006) Architectural tradeoffs between adventitious and basal roots for phosphorus acquisition. Plant Soil 279:347–366CrossRefGoogle Scholar
  55. Wang X, Tang C, Guppy CN, Sale PWG (2008) Phosphorus acquisition characteristics of cotton (Gossypium hirsutum L.), wheat (Triticum aestivum L.) and white lupin (Lupinus albus L.) under P deficient conditions. Plant Soil 312:117–128CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  1. 1.Institute of Botany, Faculty of Biology and Preclinical MedicineUniversity of RegensburgRegensburgGermany
  2. 2.Cell Biology and Plant Biochemistry, Faculty of Biology and Preclinical MedicineUniversity of RegensburgRegensburgGermany

Personalised recommendations