ong>Theong> ong>localisedong> ong>effectong> ong>ofong> ong>graniteong> on root proliferation and dauciform root
production in Carex caryophyllea and its ong>effectong> on feldspar weathering.
1. Where phosphorus is limiting, some species ong>ofong> the family Cyperaceae have been found to
increase root proliferation and produce dauciform roots in response to ong>localisedong> nutrient
2. Carex caryophyllea plants were grown with different treatment bands to see if the P limitation
response could be initiated by a patch ong>ofong> feldspar-rich ong>graniteong> and if this response
would differ if soil was present in the treatment band.
3. C. caryophyllea produced the greatest root biomass and density ong>ofong> dauciform roots when
grown with a treatment band ong>ofong> mineral and sand. ong>Theong> highest amount ong>ofong> root biomass and
length was allocated to the depth ong>ofong> tube containing the treatment band in all P limited
plants not treated with 10ml P solution per tube once a week.
4. No dauciform roots were produced by plants that were treated with P solution, and there
was no increase in root proliferation in the treatment bands. ong>Theong>re was no significant ong>effectong>
ong>ofong> treatment on shoot dry weight.
5. Etch-pits weathered in the feldspar were detected in tubes containing plants grown with
ong>graniteong> and sand. ong>Theong>se plants produced a high density ong>ofong> dauciform roots and the weathering
is thought to be caused by the high concentration ong>ofong> organic acid exudation from
Plants living on nutrient impoverished soils are ong>ofong>ten stress tolerators, well adapted to take up
the limited amount ong>ofong> nutrients available (Grime, 1986). In soils with low phosphorus (P)
concentrations most plants (~ 80%) have mycorrhizal associations to enable uptake ong>ofong> P from
the soil. Those that lack these have other means ong>ofong> increasing uptake, usually involving alterations
in the morphology ong>ofong> their root systems by increased carbon allocation to roots
(Vance et al., 2003), to increase their growth and proliferation. Some plants, e.g. Arabidopsis
thaliana, rely on increasing their root hair density and length in reduced P availability to increase
the surface area ong>ofong> roots available to take up the limited P (Ma et al., 2001). Plants can
also enhance P acquisition biochemically, by modifying the rhizosphere to overcome deficiency
in the soil. ong>Theong> release ong>ofong> hydrogen ions, organic acids and phosphatases increases
plant uptake ong>ofong> phosphorus (Jones, 1998). Organic acids chelate metal cations such as iron,
aluminium and calcium which bind P, causing its desorption by increasing its solubility and
therefore increasing its uptake into plants (Marschner, 1995). Phosphatases, such as phosphomonoesterase
and phosphodiesterase, are produced when P is limited in the soil (Leake &
Miles, 1996) and mineralize organic P converting it into an inorganic form available for plant
uptake (Tarafdar & Jungk, 1987). In P deficient soils, released phosphatases and organic acids
work together to increase the mobility ong>ofong> inorganic P (Neumann et al., 2000).
ong>Theong> development ong>ofong> specialized roots is another way ong>ofong> overcoming P deficiency. Cluster
roots are found in species ong>ofong> Proteaceae and in Lupinus albus, among others, their production
peaking at suboptimal levels ong>ofong> P (Neumann et al., 2000). Cluster roots increase the soil volume
covered by the roots by 300 times more than the same length ong>ofong> a normal root, thus increasing
the surface area ong>ofong> root for carboxylate exudation and subsequent solubilisation ong>ofong>
nutrients and uptake by the plant (Lamont, 2003).
Like Proteaceae species, some sedge species also produce modified roots, called dauciform
roots, in response to phosphorous deficiency. This adaptation is important as they are ong>ofong>ten
found in P limited calcareous soils. ong>Theong>se were first observed by Davies et al. (1973), who
described these roots as short, carrot-shaped branches ong>ofong>f the main roots, with very long and
dense root hairs. ong>Theong>y form mats in the surface layers ong>ofong> the soil, where P inputs are the
greatest from falling litter, and bind soil particles, so they become ensheathed in soil material.
Like cluster roots, the development ong>ofong> dauciform roots shows a lot ong>ofong> plasticity depending on
the availability ong>ofong> phosphorus (Shane et al., 2006). Dauciform root production is caused by
limiting P concentrations (Ballard, 2001). If the availability ong>ofong> phosphorous is increased, it
will be sensed by an increase in the concentration ong>ofong> P in the leaf and the production ong>ofong> dauciform
roots will be suppressed (Shane et al., 2005). This minimizes energy expenditure; the
synthesis ong>ofong> modified roots is not initiated when it is unnecessary. Similarly, the addition ong>ofong> P
causes a decrease in the concentration ong>ofong> phosphatase on the surface the root (Hedley et al,
1983). However in P starvation, phosphatase activity is increased, both by an increase in root
density and by the production ong>ofong> dauciform roots, which have higher levels ong>ofong> phosphatase
activity than the same area ong>ofong> an unmodified root (Ballard, 2001).
ong>Theong> abundance ong>ofong> root hairs and highly branched morphology ong>ofong> dauciform roots enables
them to extract more P from the soil than normal roots, giving an overlap in the areas ong>ofong> soil
each root hair is able to deplete P from, thus allowing a concentrated release ong>ofong> carboxylates
(mainly citric acid) and phosphatases into a particular area. ong>Theong>se are released in a single
pulse at the point ong>ofong> dauciform root maturity (Shane et al., 2006), this may be to overwhelm
microorganisms which can use root exudates as an energy source and allow for increased hydrolysis
ong>ofong> organic P esters to allow P uptake (Playstead et al., 2006).
Johnson (2007) found that certain species ong>ofong> sedge (e.g. Carex caryophyllea and Carex
flacca) are spatially precise in their foraging. When grown in a tube ong>ofong> sand with a band ong>ofong>
soil making up 3% ong>ofong> the total volume ong>ofong> the growth medium, they show a ong>localisedong> increase
in root proliferation and turn on the expression ong>ofong> dauciform roots in the soil patch. He found
that 90% ong>ofong> the total dauciform roots produced were allocated to this small area as was 40%
ong>ofong> the total root biomass. This is a response to the P present in small quantities in the soil but
absent in the sand. ong>Theong>y are able to sense the environment before producing dauciform roots
and releasing exudates.
ong>Theong> aim ong>ofong> this study is to find out if C. caryophyllea would produce dauciform roots and
increase their root proliferation in a ong>localisedong> response to a band ong>ofong> ong>graniteong>, which would
suggest they are able to uptake P from the mineral. This will be compared to the number ong>ofong>
dauciform roots produced and increase in root proliferation in a band ong>ofong> soil and a band ong>ofong>
mineral and soil together. Rock is P limiting (Hong>ofong>fland et al., 2004) so it is hypothesised that
C. caryophyllea will locally increase root proliferation and dauciform root production in response
to a band ong>ofong> mineral as it does to a band ong>ofong> soil, as shown by Johnson (2007). It is hypothesized
that the plants grown with a mineral and sand band will produce the highest number
ong>ofong> dauciform roots and the greatest amount ong>ofong> root biomass overall. ong>Theong>y are also likely
to increase ong>localisedong> root proliferation and dauciform root production in the treatment band
the most as they are probably more P limited than plants grown with the other treatment
bands. In all P limited plants, it is predicted that root biomass and dauciform root production
will be lower in all areas ong>ofong> the tube that do not contain the treatment band.
Plants grown with mineral and soil bands and soil and sand bands were hypothesized to show
a ong>localisedong> increase in root proliferation and modified root production in response to their
treatment bands also, but to a lesser extent, as they are less P limited due to the presence ong>ofong>
soil in their treatment band.
Two controls with added P fertilizer will be used as a comparison to see the difference in root
proliferation down the sections ong>ofong> the tube. P limitation is ameliorated by the addition ong>ofong> P
fertilizer, thus inhibiting P limitation responses from the plant such as dauciform root production
and ong>localisedong> root proliferation to a P source. It is predicted that the tubes treated with P
fertilizer will produce no dauciform roots and have a relatively uniform distribution ong>ofong> root
biomass, decreasing towards the bottom ong>ofong> the tube, with no ong>localisedong> increase in root proliferation
where the treatment band is located. ong>Theong>y are predicted to have a lower root biomass
and length overall, as fewer resources need to be allocated to root growth as P is not in limiting
supply. It is also predicted that the plants treated with P fertilizer will produce the highest
shoot weights as less resources are being allocated to the root system and released in exudates
in order to uptake P.
Feldspar crystals contain apatite inclusions, the weathering ong>ofong> which is known to release P
(Hong>ofong>fland et al., 2004). Feldspars will be placed within bands containing ong>graniteong> to see if
there is any ong>effectong> ong>ofong> weathering from the dauciform roots. This will be compared with the
ong>effectong> ong>ofong> unmodified roots on the surface ong>ofong> the feldspar crystals and 2 other controls where
no plants were grown in the tubes. It has been found that certain plant species can take up
phosphate from rocks. Hong>ofong>fland et al., (1989) documented the mobilisation ong>ofong> P from phosphate
in the rock by rape (Brassica napus), probably due to its production ong>ofong> long fine root
hairs in P deficiency. Weathering ong>ofong> rocks releases the phosphate bound in them (Griffith et
al., 1977). Organic acids released by plants have a small role in mineral weathering, which is
thought to increase nutrient availability to the plant, and increase feldspar dissolution rates
below a certain acidity. ong>Theong>y may play a greater role in the areas closer to the plant roots
where there is more ong>localisedong> exudation (Drever & Stillings, 1997). However, plants themselves
probably contribute much more to weathering, through binding soil particles and
breaking down the parent material (Drever, 1994). It is predicted that where there is a ong>localisedong>
increase ong>ofong> dauciform roots and root proliferation in the treatment band there will be a
greater extent ong>ofong> weathering as there is a higher surface area ong>ofong> roots to release organic acids
and bind the rock. Treatments with added P fertilizer were used as controls, as they it would
produce no dauciform roots nor increase their root proliferation in the treatment band as they
would not be limited in P. Unmodified roots are predicted to have less ong>ofong> a weathering ong>effectong>
and where no plant was grown it is predicted that the surface ong>ofong> the feldspar will have barely
changed at all.
Materials and Methods
Carex caryophyllea is a sedge ong>ofong> the family Cyperaceae. It is found in grasslands in most areas
ong>ofong> the UK, mainly on calcareous soils. (Jermy & Tutin, 1968). ong>Theong>y are short plants and
have keeled leaves which curve outwards. ong>Theong> C.caryophyllea plants and the soil used in this
experiment were obtained from Redmire Moor in the Yorkshire Dales, from a roadside quarry
in carboniferous limestone.
Tubes were made for the plants to be grown in, 2 halves ong>ofong> the tube were taped together at the
sides and a mesh was glued to the bottom ong>ofong> the tube to prevent the sand and treatments from
falling out. ong>Theong> tubes were put in an oven overnight at 40ºC, to get rid ong>ofong> the glue fumes so as
not to cause damage to the plants. ong>Theong>re was a hole on one side ong>ofong> the tube, approximately
1cm from the top. In this was inserted a plastic plug, to keep a standard volume ong>ofong> 1.91cm³
free for the input ong>ofong> the treatment bands. ong>Theong> tubes were filled with sand and in some, C.
caryophyllea was planted. As they were grown in sand, there were no areas ong>ofong> increased nutrients
like in the field, so the production ong>ofong> modified roots in response to surface horizons
was eradicated. All modified roots, and the majority ong>ofong> the root system was removed before
Granite was obtained from Shap quarry in Cumbria. Pink feldspar crystals which had flat
shiny surfaces were picked out ong>ofong> the 2-4mm ong>graniteong> and the rest was ground down to 0.5-
1mm pieces using a ball mill and 2 sieves. Treatment bands were made up, according to volume
ong>ofong> material to be put in them. ong>Theong> treatment bands with ong>graniteong> in also had three feldspar
crystals in which came to the weight ong>ofong> 0.16998 ± 0.01 g.
ong>Theong> treatment bands were inserted into the tubes on the 28/10/08. Combinations ong>ofong> treatments
are shown in figure 1. Sedges planted with a band ong>ofong> soil and sand were used as comparisons
to ones with mineral in their treatment band, in terms ong>ofong> root proliferation and dauciform root
production. Treatments with added P fertilizer were used as controls to see the distribution ong>ofong>
roots and ong>effectong>s ong>ofong> unmodified roots on feldspar weathering. Treatments with no plants were
used as controls to see the ong>effectong> ong>ofong> feldspar weathering where no roots are present.
Figure 1. C.caryophyllea grown in sand with different treatment bands and controls: 1. Grown
with a band ong>ofong> soil and sand. 2. Grown with a band ong>ofong> mineral and soil. 3.Grown with a band ong>ofong>
mineral and sand. 4.Grown awith same treatment band as 2 but with added P fertilizer. 5 Grown
with same treatment band as 3 but with added P fertilizer. 6. No plant grown, band ong>ofong> mineral
and soil. 7. No plant grown, band ong>ofong> mineral and sand.
= Band ong>ofong> soil and sand
= Band ong>ofong> mineral and soil
= Band ong>ofong> mineral and sand
ong>Theong> tubes were left for around a month to grow in a growth chamber with a propagator over
them to reduce water loss from the plants by evapo-transpiration so they would not dry out.
ong>Theong>y were watered every day except for weekends and when they were fertilized. 10ml ong>ofong>
nutrient solution made up ong>ofong> 1ml ong>ofong> N, K, Mg, Ca diluted in a litre ong>ofong> distilled water was
added to each tube for 3 days in a row in the first week, and from then on once a week until
harvesting. 10ml P solution made up ong>ofong> 50ml P added to 950ml distilled water was added to
treatments 4 and 5 (Figure 1.) once every week.
Plants were harvested from 28/11/08 - 5/12/08. ong>Theong> two sides ong>ofong> the tubes were split apart
and the sand containing roots was cut into sections for analysis (Figure 2.). ong>Theong> roots in each
section were extracted, cut up and spread around a square dish with a 0.5 x 0.5cm grid on the
bottom. This was put under a microscope and the number ong>ofong> times a root crossed a grid line
and the number ong>ofong> dauciform roots produced was recorded for each section. Number ong>ofong> grid
intersects crossed was used to estimate the length ong>ofong> the roots (Tennant, 1975). ong>Theong> shoots
and roots from each section were dried in an oven at 80ºC, put in a desiccator overnight and
Pieces ong>ofong> feldspar were extracted from the treatment bands and scanned using vertical scanning
inferometry VSI (Veeco Instruments) to map the surface topography ong>ofong> crystals at
nanometric scale. 3D images were compared to see if there were any noticeable ong>effectong>s ong>ofong> the
different treatments on the feldspar surface.
Dauciform roots could be seen to bind the soil and mineral particles ensheathing themselves
in the material in order to access P (Figure 3).
1 2 3 4
1.5cm 1.5cm 1.5cm 10.4cm
Figure 2. Lengths ong>ofong> sections cut in the growth medium for root extraction
Dauciform roots were produced by C.caryophyllea in all tubes except those treated with P
fertilizer (Figure 4.). Where this was added, no dauciform roots were seen in any ong>ofong> the sections,
and these were therefore not included in the statistical analysis as they were obviously
ong>Theong> production ong>ofong> dauciform roots per cm 3 growth substrate varied significantly between
depths ong>ofong> substrate (Figure 4) (Two-way ANOVA, F=25.48, d.f.=3, p
Number ong>ofong> dauciform roots produced/cm 3
Mean no. dauciform roots/cm 3
1 2 3 4 5
Figure 4.ong>Theong> ong>effectong> ong>ofong> treatment on the number ong>ofong>
dauciform roots/cm 3 Treatment
produced in each section
Mean no.dauciform roots/cm 3
1 2 3 4
Figure 5. Tukey comparison ong>ofong> ong>effectong>s. Means with different letter codes do not differ significantly
(tukey test p>0.05).(A) ong>Theong> ong>effectong> ong>ofong> treatment on the number ong>ofong> dauciform roots
produced/cm3. (B) ong>Theong> ong>effectong> ong>ofong> section on mean number ong>ofong> dauciform roots produced/cm3
Treatments: 1)Soil and sand band.
2)Mineral and soil band. 3) mineral and sand
band. 4) mineral and soil band + P fertilizer.
5) Mineral and sand band + P fertilizer.
Sections: 1) 0 - 1.5cm deep. 2) 1.5 – 3.0cm
deep. 3) 3.0 – 4.5cm deep. 4) 4.5 10.4cm
Mean no. dauciform roots produced per cm root length
Mean no. dauciform roots per cm root length
1 2 3 4 5
Figure 6. ong>Theong> ong>effectong> ong>ofong> treatment on the mean number ong>ofong>
dauciform roots produced per unit root length in each section.
1 2 3
Figure7. Effect ong>ofong> treatment on the mean number ong>ofong>
dauciform roots produced per cm root length. Means
having the same letter code do not differ significantly
(Tukey test p>0.05)
ong>Theong> treatment band had a very significant
ong>effectong> on the number ong>ofong> dauciform roots
produced per cm root length (Two-way
ANOVA, F=9.05, d.f.= 2, p
Mean root dry weight (g/cm 3 )
Mean root length per volume growth substrate (cm/cm 3 )
= 12, p = 0.716).
In treatments 1, 2 and 3 the highest amount
ong>ofong> root biomass was allocated to the section
containing the treatment band, as hypothesized.
ong>Theong> amount ong>ofong> root biomass produced
was lower above and much lower below this
section. In P fertilized treatments, the
amount ong>ofong> biomass produced decreased with
depth, and there was no increase in root
biomass at depths 1.5 – 3.0cm, where the
treatment band was contained, as expected
(Figure 9). ong>Theong>re was a highly significant
ong>effectong> ong>ofong> section on the amount ong>ofong> root biomass
produced (two-way ANOVA, F= 62.78,
would reduce shoot biomass.
Observations from the VSI scanning suggest that the sedges grown with the treatment band ong>ofong>
mineral and sand weathered the feldspar to a much greater extent than any ong>ofong> the other treatments.
At 50x and 100x magnification, etch pits ong>ofong> an approximate depth ong>ofong> 0.3μm and diameter
ong>ofong> 0.5μm are clearly visible, and in some areas, lateral lines ong>ofong> these pits have formed.
Etch pits were not observed on the feldspar surfaces in any other treatment, and their surfaces
appeared much smoother (Figure 11.).
This experiment has shown that C.caryophyllea will produce a ong>localisedong> response in its root
system to low concentrations ong>ofong> phosphorus in its growth medium, supporting the work ong>ofong>
Johnson (2007). ong>Theong> production ong>ofong> dauciform roots and increased root growth in tubes containing
the mineral and sand band suggest that C.caryophyllea can directly uptake P from the
mineral, supporting the initial predictions. ong>Theong> direct uptake ong>ofong> P from rock has also been
seen in other plant species. Wallander et al.’s (1997) experiment on Pinus sylvestris seedlings
showed that they could weather apatite, by which they were able to increase their nutrient
supply. This challenges the general conceptions ong>ofong> P acquisition, suggesting that
C.caryophyllea may be able to take up organic P, bypassing the mineralization process to
PO4, which could have important implications for their fitness in the field.
Plants which produced modified roots increased root hair proliferation in zones ong>ofong> nutrient
availability in order to compensate for the rest ong>ofong> the root system which subjected to infertile
Figure 11. VSI images ong>ofong> surface layers ong>ofong> feldspars from different treatments. (A) Non
reacted feldspar. 100x. (B) mineral and soil band, no plant grown. 100x. (C)Mineral and
sand, no plant grown. 50x. (D) Mineral and soil band, plant grown.100x. (E) mineral and
sand and plant (i) 100x (ii) 50x. (F) Mineral and soil and P fertilizer. 50x. (G) Mineral
and sand and P fertilizer. 100x.
conditions. Net absorption in these ong>localisedong> patches is increased in order to maintain their
relative growth rate (Drew & Saker, 1978). Plants grown with the treatment band ong>ofong> ong>graniteong>
and sand showed the greatest extent ong>ofong> dauciform root production, suggesting that
C.caryophyllea finds the phosphorous in the mineral more inaccessible than in the soil. However
the production ong>ofong> dauciform roots is not as ong>localisedong> to the resource patch as it is with
the other two treatments. Dauciform roots are produced at high levels all down the root prong>ofong>ile.
This was not predicted, it was thought that the mineral band would cause just a ong>localisedong>
production ong>ofong> dauciform roots in a similar way to a band ong>ofong> soil. In the field, the high exudation
ong>ofong> organic acids by these highly modified roots can cause mineral weathering and the
release ong>ofong> P into the bulk soil (van Breemen et al., 2000). A similar process may have occurred
in the tubes, allowing P to be released into the sand, so it is not just concentrated in the
treatment band, accounting for the high number ong>ofong> dauciform roots per unit root length in all
As predicted, the sedges treated with P fertilizer did not produce dauciform roots anywhere in
the growth medium, nor did they increase their root proliferation in response to any treatment
band. Root biomass and proliferation was greatest at the nearest to the plant, and decreased
with depth. ong>Theong>se were not limited by P and so it would be a waste ong>ofong> energy for them to produce
structures to facilitate P uptake, and excess P may cause toxicity.
ong>Theong> roots ong>ofong> plants deficient in P become a dominant sink ong>ofong> photosynthates from the shoots
(Marschner, 1995). Sedges that were P limited allocated a higher amount ong>ofong> their dry weight
to their root system than those supplied with sufficient P, the highest allocation being to the
section containing the treatment band, as predicted. ong>Theong> production ong>ofong> shoot biomass did not
appear to be altered by different treatments; therefore it appears that changes in the root systems
were produced without any significant ong>effectong> on above ground biomass. This result has
also been seen in barley where plants treated with extra phosphates produced similar shoot
weights to those that were untreated (Drew, 1975). This was not predicted; it was thought that
the sedges treated with P solution, which were therefore not P limited, would have a greater
shoot dry weight as fewer resources would be allocated to the root system in order to take up
P. Perhaps this is a limitation ong>ofong> the low growing mechanism ong>ofong> C.caryophyllea. Plants growing
on low nutrient soils, such as the calcareous soils low in plant-available P where
C.caryophyllea are ong>ofong>ten found, generally produce dry matter at low rates. ong>Theong>y also tend to
accumulate mineral nutrients when they are more readily available as their demands for the
use ong>ofong> the nutrient in growth have been exceeded (Grime, 1986). High amounts ong>ofong> P supplied
to plants which typically grow on infertile soils have also been seen to accumulate to toxic
amounts, to the detriment ong>ofong> the plants growth (Jones, 1974).
Dauciform roots exude a burst ong>ofong> organic acids to mobilize P bound in the soil. This causes
the local rhizosphere to be subjected to intense chemical extraction (Marschner, 1995). Organic
acids have been documented to cause weathering to some extent (Drever, 1994) and
observations from the VSI scanning suggested that where the highest density ong>ofong> dauciform
roots are produced, the weathering ong>effectong>s are the strongest, as etch pits were only seen in
feldspars that had been in the mineral and sand treatment band. This confirms the initial predictions
as the higher the density ong>ofong> dauciform roots, the greater the concentration ong>ofong> organic
In this experiment the weathering ong>effectong> observed on the feldspar was only very small compared
to ong>effectong>s shown by Smith et al. (1999), as unfortunately the time constraints meant that
the plants had to be harvested after 1 month. If plants had been left to grow for longer they
may have had a more prominent ong>effectong> on feldspar weathering. In future work it may be useful
to scan the feldspar before input into treatment bands, and then again after plant harvest
and statistically compare the two to see the ong>effectong> ong>ofong> the plant on the feldspar surface.
In future, aseptic culture ong>ofong> the sedges may be useful, to determine whether the weathering is
in fact due entirely to the plant or if microorganisms in the growth medium also play a role.
As microorganisms deplete organic acids, feldspars in treatment bands containing soil and
therefore potentially soil bacteria, may not have been as intensely weathered, as the bacteria
may have got rid ong>ofong> the acids before they could do much damage to the feldspar surface. In
addition, microorganisms may also have played a part in the weathering ong>ofong> the feldspars from
the mineral bands, as they may also use the feldspar as a P source.
Jonathan Leake obtained all materials needed and assisted throughout the experiment and
write-up. Megan Andrews, Ben Palmer, Irene Johnson and Adele Duran helped with technical
aspects ong>ofong> the experiment including the VSI scanning, sieving and grinding the ong>graniteong>, assembling
the tubes, and photographing the dauciform roots.
Ballard, S. (2001) Dauciform roots in sedges: their role in nutrition and response to environmental
change. PHD ong>Theong>sis, University ong>ofong> Sheffield, UK. P45-70
Davies, J., Briarty, L.G., Rieley, J.O. (1973) Observations on the swollen lateral roots ong>ofong> the
Cyperaceae. New Phytologist. 72 167-174
Drever, J.I. (1994). ong>Theong> ong>effectong> ong>ofong> land plants on the weathering rates ong>ofong> silicate minerals.
Geochimica et Cosmochimica Acta. 58 2325-2332
Drever, J.I., Stillings, L.L. (1997). ong>Theong> role ong>ofong> organic acids in mineral weathering. Colloids
and Surfaces A - Physiochemical and Engineering Aspects. 120 167-181
Drew, M.C. (1975). Comparison ong>ofong> the ong>effectong>s ong>ofong> a localized supply ong>ofong> phosphate, nitrate,
ammonium and potassium on the growth ong>ofong> the seminal root system, and the shoot, in barley.
New Phytologist, 75 479-490
Drew, M.C. & Saker, L.R. (1978). Nutrient supply and the growth ong>ofong> the seminal root system
in barley III. Compensatory increases in growth ong>ofong> lateral roots and in rates ong>ofong> phoshorus uptake,
in response to a ong>localisedong> supply ong>ofong> phosphate. Journal ong>ofong> Experimental Botany. 29 435-
Griffith,E.J., Ponnamperuma, C. & Gabel, N.W. (1977). Phosphorus, a key to life on the
primitive earth. Origins ong>ofong> Life and Evolution ong>ofong> Biospheres. 8 71-85
Grime, J.P. (1986). Plant strategies and vegetation processes. John Wiley and sons. p31-32
Hedley, M.J., Nye, P.H., White, R.E. (1983) Plant-induced changes in the rhizosphere ong>ofong> rape
(Brassica napus var. emerald) seedlings. IV. ong>Theong> ong>effectong> ong>ofong> rhizosphere phosphorus status on
the pH, phosphatase activity and depletion ong>ofong> soil phosphorus fractions in the rhizosphere and
on the cation-anion balance in the plants. New Phytologist, 95 69-82
Hong>ofong>fland, E., Findenegg, G.R., Nelemans, J.A. (1989) Solubilisation ong>ofong> rock phosphate by
rape. 1. Evaluation ong>ofong> the role ong>ofong> the nutrient-uptake pattern. Plant and soil. 113 155-160
Hong>ofong>fland, E., Kuyper. T.W., Wallander, H., Plassard, C., Gorbushina, A.A., Haselwandter K.,
Holmström, S., Landeweert, R., Lundström, U.S., Rosling, A., Sen, R., Smits, M.M., van
Hees, P.A.W., van Breemen, N. (2004). ong>Theong> role ong>ofong> fungi in weathering. Frontiers in Ecology
and the Environment.2 258-264
Jermy, A.C. & Tutin, T.G. (1968). British sedges. A handbook to the species ong>ofong> Carex found
growing in the British Isles. Botanical society ong>ofong> the British Isles. p122
Johnson, D.A. (2007). Specialised root functioning in sedges: physiological activity and ecological
significance. PhD ong>Theong>sis, University ong>ofong> Sheffield, UK
Jones, D.L. (1998) Organic acids in the rhizosphere. Plant and Soil, 205 25-44.
Jones, R.K. (1974). Study ong>ofong> phosphorus responses ong>ofong> a wide-range ong>ofong> accessions from genus
Stylosanthes. Australian Journal ong>ofong> Agricultural Research. 25 847-862
Lamont, B.B. (2003). Structure, ecology and physiology ong>ofong> root clusters - a review. Plant and
soil. 248 1-19
Leake, J.R., Miles, W. (1996) Phosphodiesters as mycorrhizal P sources. I. Phosphodiesterase
production and the utilization ong>ofong> DNA as a phosphorus source by the ericoid mycorrhizal
fungus Hymenoscyphus ericae. New Phytologist, 132 435-443
Ma, Z., Walk, T.C., Marcus, A., Lynch, J.P. (2001).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
Marschner, H. (1995) Mineral nutrition ong>ofong> higher plants. 2 nd edition. Academic press. P554
Neumann, G, Massonneu, A.S., Langlade, N. Dinkelaker, B., Hengeler, C., Roemheld, V.
Martinoi, E (2000). Physiological aspects ong>ofong> cluster root function and development in phosphorus-deficient
White Lupin (Lupinus albus L.). Annals ong>ofong> Botany 85 909-919
Playstead,, C.W.S., Johnston, M.E., Ramage, C.M., Edwards, D.G., Cawthray, G.R., Lambers,
H. (2006) Functional significance ong>ofong> dauciform roots: exudation ong>ofong> carboxylates and acid
phosphatase under phosphorus deficiency in Caustis blakei (Cyperaceae). New Phytologist
Shane, M.W., Cawthray, G.R., Cramer, M.D., Kuo, J., Lambers, H. (2006) Specialized ‘dauciform’
roots ong>ofong> Cyperaceae are structurally distinct, but functionally analogous with ‘cluster’
roots. Plant, Cell and Environment. 29 1989-1999
Shane, M.W., Dixon, K. W., Lambers, H. (2005). ong>Theong> occurrence ong>ofong> dauciform roots amongst
Western Australian reeds, rushes and sedges, and the impact ong>ofong> phosphorus supply on dauciform-root
development in Schoenus unispiculatus (Cyperaceae). New Phytologist. 165 887-
Smith, J.V., Arnold, F.P., Parsons, I., Lee, M.R. (1999). Biochemical evolution III: Polymerization
on organophilic silica-rich surfaces, crystal–chemical modeling, formation ong>ofong> first
cells, and geological clues. Proceedings ong>ofong> the National Academy ong>ofong> Sciences ong>ofong> the United
States ong>ofong> America. 95 15173-15176
Tarafdar, J.C. & Jungk, A. (1987). Phosphatase activity in the rhizosphere and its relation to
the depletion ong>ofong> soil organic phosphorus. Biology and Fertility ong>ofong> Soils. 3 199-204
Tennant, D. (1975). A test ong>ofong> a modified line intersect method ong>ofong> estimating root length. ong>Theong>
Journal ong>ofong> Ecology. 63 995-1001
Van Breemen, N., Finlay, R. Lundstrom, U., Jongmans, A.G., Giesler, R. Olsson, M. (2000). Mycorrhizal
weathering: A true case ong>ofong> mineral plant nutrition? Biogeochemistry. 49 53-67
Vance, C.P., Uhde-Stone, C., Allen, D.L. (2003) Phosphorus acquisition and use: critical adaptations
by plants for securing a non-renewable resource. New Phytologist 157 423–447
Wallander, H., Wickman, T. Jacks, G. (1997). Apatite as a P source in mycorrhizal and nonmycorrhizal
Pinus sylvestris seedlings. Plant and Soil. 196 123-131