Root hair morphology and mycorrhizal colonisation of pasture species in response to phosphorus and nitrogen nutrition
J. O. Hill A B , R. J. Simpson A D , M. H. Ryan A C and D. F. Chapman BA CSIRO Plant Industry, PO Box 1600, Canberra, ACT 2601, Australia.
B School of Land and Environment, University of Melbourne, Parkville, Vic. 3010, Australia.
C Present address: School of Plant Biology, University of Western Australia, Crawley, WA 6009, Australia.
D Corresponding author. Email: Richard.Simpson@csiro.au
Crop and Pasture Science 61(2) 122-131 https://doi.org/10.1071/CP09217
Submitted: 23 July 2009 Accepted: 13 November 2009 Published: 8 February 2010
Abstract
Root hairs and arbuscular mycorrhizal fungi (AMF) increase the absorptive surface area of a root and the volume of soil explored and as such are important for nutrient acquisition in infertile soil. Root hair morphology and colonisation by AMF were compared for 10 temperate pasture species, and responses to N and P deficiency characterised. Vulpia spp., Holcus lanatus, and Lolium rigidum had the longest root hairs (range 1.02–2.36 mm) while Trifolium subterraneum had the shortest (~0.27 mm). In contrast, T. subterraneum had a much higher density of root hairs than any of the other species. In response to P deficiency, the length and density of root hairs generally increased; in response to N deficiency, both increases and decreases in the length and density of root hairs were observed. The annual dicotyledons T. subterraneum and Arctotheca calendula had much higher mycorrhizal colonisation on roots grown at low P availability than the grasses. Root colonisation decreased with increasing P availability in all species. A yield advantage from mycorrhizal colonisation was demonstrated only for T. subterraneum when P was deficient. The potential root cylinder volume of each species was calculated as an index of the ability of the species to explore soil. Although all plant species were colonised by AMF, a positive linear relationship was observed between relative P uptake rate from the soil and the rate at which potential root cylinder volumes were developed by most species. Development of potential root cylinder volume also largely explained the critical external P requirements of most species. No such relationships were observed for N. It was concluded that knowledge of root length and the length of root hairs grown in nutrient-poor conditions may be used to predict the potential of many plant species to acquire P, and also their critical external P requirement for maximum growth. However, the study also highlighted some exceptional species.
Additional keywords: Austrodanthonia richardsonii, Bromus molliformis, critical P, Hordeum leporinum, Microleana stipoides, Phalaris aquatica, root cylinder volume.
Acknowledgments
We thank Dr Lyn Abbot and Dr Zakaria Solomain for providing mycorrhizal inoculum, and Anne Cowling for statistical advice. David Marshall and Adam Stefanski provided invaluable technical assistance for some experiments.
Ali B
(1976) Influence of the endophytes of Nardus on plant growth. Plant and Soil 44, 329–340.
| Crossref | GoogleScholarGoogle Scholar |
Barrett DJ, Gifford RM
(1999) Increased C-gain by an endemic Australian pasture grass at elevated atmospheric CO2 concentration when supplied with non-labile inorganic phosphorus. Australian Journal of Plant Physiology 26, 443–451.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Bates TR, Lynch JP
(1996) Stimulation of root hair elongation in Arabidopsis thaliana by low phosphorus availability. Plant, Cell & Environment 19, 529–538.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Bates TR, Lynch JP
(2000) The efficiency of Arabidopsis thaliana (Brassicaceae) root hairs in phosphorus acquisition. American Journal of Botany 87, 964–970.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Bates TR, Lynch JP
(2001) Root hairs confer a competitive advantage under low phosphorus availability. Plant and Soil 236, 243–250.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Bhat KKS,
Nye PH, Brereton AJ
(1979) The possibility of predicting solute uptake and plant growth response from independently measured soil and plant characteristics VI. The growth and uptake of rape in solutions of constant nitrate concentration. Plant and Soil 53, 137–167.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Bolan NS,
Robson AD, Barrow NJ
(1983) Plant and soil factors including mycorrhizal infection causing sigmoidal response of plants to applied phosphorus. Plant and Soil 73, 187–201.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Bolan NS,
Robson AD, Barrow NJ
(1987) Effects of phosphorus application and mycorrhizal inoculation on root characteristics of subterranean clover and ryegrass in relation to phosphorus uptake. Plant and Soil 104, 294–298.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Boot GA, Mensink M
(1990) Size and morphology of root systems of perennial grasses from contrasting habitats as affected by nitrogen supply. Plant and Soil 129, 291–299.
|
CAS |
Campbell BD,
Grime JP, Mackey JML
(1991) A trade-off between scale and precision in resource foraging. Oecologia 87, 532–538.
| Crossref | GoogleScholarGoogle Scholar |
Caradus JR
(1980) Distinguishing between grass and legume species for efficiency of phosphorus use. New Zealand Journal of Agricultural Research 23, 75–81.
|
CAS |
Colwell JD
(1963) The estimation of the phosphorus fertiliser requirements of wheat in southern New South Wales by soil analysis. Australian Journal of Experimental Agriculture 3, 190–198.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Dazzo FB,
Truchet GL,
Sherwood JE,
Hrabak EM,
Abe M, Pankratz SH
(1984) Specific phases of root hair attachment in the Rhizobium trifolii-clover symbiosis. Applied and Environmental Microbiology 48, 1140–1150.
|
CAS |
PubMed |
Dinkelaker B,
Hengeler C, Marschner H
(1995) Distribution and function of proteoid roots and other root clusters. Botanica Acta 108, 183–200.
Dittmer HJ
(1949) Root hair variations in plant species. American Journal of Botany 36, 152–155.
| Crossref | GoogleScholarGoogle Scholar |
Fohse D,
Claassen N, Jungk A
(1991) Phosphorus efficiency of plants II. Significance of root radius, root hairs and cation-anion balance for phosphorus influx in seven plant species. Plant and Soil 132, 261–272.
Fohse D, Jungk A
(1983) Influence of phosphate and nitrate supply on root hair formation of rape, spinach and tomato plants. Plant and Soil 74, 359–368.
| Crossref | GoogleScholarGoogle Scholar |
Gahoonia TS,
Care D, Nielsen NE
(1997) Root hairs and phosphorus acquisition of wheat and barley cultivars. Plant and Soil 191, 181–188.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Gahoonia TS, Nielsen NE
(1997) Variation in root hairs of barley cultivars doubled soil phosphorus uptake. Euphytica 98, 177–182.
| Crossref | GoogleScholarGoogle Scholar |
Gahoonia TS, Nielsen NE
(1998) Direct evidence on participation of root hairs in phosphorus (32P) uptake from soil. Plant and Soil 198, 147–152.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Gahoonia TS, Nielsen NE
(2004) Barley genotypes with long root hairs sustain high grain yields in low-P field. Plant and Soil 262, 55–62.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Gahoonia TS,
Nielsen NE,
Joshi PA, Jahoor A
(2001) A root hairless barley mutant for elucidating genetics of root hairs and phosphorus uptake. Plant and Soil 235, 211–219.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Gahoonia TS,
Nielsen NE, Lyshede OB
(1999) Phosphorus (P) acquisition of cereal cultivars in the field at three levels of P fertilisation. Plant and Soil 211, 269–281.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Gifford RM,
Lutze JL, Barrett DJ
(1996) Global atmospheric change effects on terrestrial carbon sequestration: exploration with a global C- and N-cycle model (CQUESTN). Plant and Soil 187, 369–387.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Giovannetti M, Mosse B
(1980) An evaluation of techniques for measuring vesicular-arbuscular mycorrhizal infection in roots. New Phytologist 84, 489–500.
| Crossref | GoogleScholarGoogle Scholar |
Grace C, Stribley DR
(1991) A safer procedure for routine staining of vesicular-mycorrhizal fungi. Mycological Research 95, 1160–1162.
| Crossref | GoogleScholarGoogle Scholar |
Hall IR
(1978) Effects of endomycorrhizas on the competitive ability of white clover. New Zealand Journal of Agricultural Research 21, 509–515.
Hill JO,
Simpson RJ,
Moore AD, Chapman DF
(2006) Morphology and response of roots of pasture species to phosphorus and nitrogen nutrition. Plant and Soil 286, 7–19.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Hill JO,
Simpson RJ,
Wood JT,
Moore AD, Chapman DF
(2005) The phosphorus and nitrogen requirements of temperate pasture species and their influence on grassland botanical composition. Australian Journal of Agricultural Research 56, 1027–1039.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Itoh S, Barber SA
(1983) Phosphorus uptake by six plant species as related to root hairs. Agronomy Journal 75, 457–461.
Jakobsen I,
Abbott LK, Robson AD
(1992) External hyphae of vescicular arbuscular mycorrhizal fungi associated with Trifolium subterraneum L. 2. Hyphal transport of 32P over defined distances. New Phytologist 120, 509–516.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Jakobsen I,
Chen B,
Munkvold L,
Lundsgaard T, Zhu Y-G
(2005) Contrasting phosphate acquisition of mycorrhizal fungi with that of root hairs using the root hairless barley mutant. Plant, Cell & Environment 28, 928–938.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Joner EJ, Jakobsen I
(1995) Uptake of 32P from labelled organic matter by mycorrhizal and non-mycorrhizal subterranean clover (Trifolium subterraneum L.). Plant and Soil 172, 221–227.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Kohls SJ, Baker DD
(1989) Effects of substrate nitrate concentration on symbiotic nodule formation in actinorhizal plants. Plant and Soil 118, 171–179.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Koucheki HK, Read DJ
(1976) Vesicular-arbuscular mycorrhiza in natural vegetation systems. II. The relationship between infection and growth in Festuca ovina L. New Phytologist 77, 655–666.
| Crossref | GoogleScholarGoogle Scholar |
Ma Z,
Bielenberg DG,
Brown KM, Lynch JP
(2001a) Regulation of root hair density by phosphorus availability in Arabidopsis thaliana. Plant, Cell & Environment 24, 459–467.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Ma Z,
Walk TC,
Marcus A, Lynch JP
(2001b) Morphological synergism in root hair length, density, initiation and geometry for phosphorus acquisition in Arabidopsis thaliana: A modeling approach. Plant and Soil 236, 221–235.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Plenchette C, Morel C
(1996) External phosphorus requirement of mycorrhizal and non-mycorrhizal barley and soybean plants. Biology and Fertility of Soils 21, 303–308.
| Crossref | GoogleScholarGoogle Scholar |
Robinson D, Rorison IH
(1985) A quantitative analysis of the relationships between root distribution and nitrogen uptake from soil by two grass species. Journal of Soil Science 36, 71–85.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Robinson D, Rorison IH
(1987) Root hairs and plant growth at low nitrogen availabilities. New Phytologist 107, 681–693.
| Crossref | GoogleScholarGoogle Scholar |
Robinson D, Rorison IH
(1988) Plasticity in grass species in relation to nitrogen supply. Functional Ecology 2, 249–257.
| Crossref | GoogleScholarGoogle Scholar |
Ryan M,
Small DR, Ash JE
(2000) Phosphorus controls the level of colonisation by arbuscular mycorrhizal fungi (AMF) in conventional and biodynamic irrigated dairy pastures. Australian Journal of Experimental Agriculture 40, 663–670.
| Crossref | GoogleScholarGoogle Scholar |
Ryan MH, Angus JF
(2003) Arbuscular mycorrhizae in wheat and field pea crops on a low P soil: increased Zn-uptake but no increase in P uptake or yield. Plant and Soil 250, 225–239.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Sano SM,
Abbot LK,
Solaiman MZ, Robson AD
(2002) Influence of liming, inoculum level and inoculum placement on root colonisation of subterranean clover. Mycorrhiza 12, 285–290.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Schweiger PF,
Robson AD, Barrow NJ
(1995) Root hair length determines beneficial effect of a Glomus species on shoot growth of some pasture species. New Phytologist 131, 247–254.
| Crossref | GoogleScholarGoogle Scholar |
Stribley DP,
Read DJ, Hunt R
(1975) The biology of mycorrhiza in the Ericaceae. V. The effects of mycorrhizal infection, soil type, and partial soil sterilisation (by gamma-irradiation) on growth of Cranberry (Vaccinium macrocarpon, Ait.). New Phytologist 75, 119–130.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Thomson BD,
Robson AD, Abbott LK
(1992) The effect of long-term applications of phosphorus fertiliser on populations of vesicular-arbuscular mycorrhizal fungi in pastures. Australian Journal of Agricultural Research 43, 1131–1142.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Thompson JP
(1990) Soil sterilisation methods to show VA-mycorrhizae aid P and Zn nutrition of wheat in vertisols. Soil Biology & Biochemistry 22, 229–240.
| Crossref | GoogleScholarGoogle Scholar |
CAS |