Turgor, solute import and growth in maize roots treated with galactose
Jeremy Pritchard A , A. Deri Tomos B , John F. Farrar B , Peter E. H. Minchin C D , Nick Gould C , Matthew J. Paul E , Elspeth A. MacRae F , Richard A. Ferrieri G , Dennis W. Gray H and Michael R. Thorpe C IA School of Biosciences, University of Birmingham, Edgbaston, Birmingham B15 2TT, UK.
B Ysgol Gwyddorau Bioleg, Prifysgol Cymru Bangor, Bangor, Gwynedd, LL57 2UW, Wales, UK.
C Horticulture and Food Research Institute, Ruakura, Hamilton, New Zealand.
D Current address: ICG-III Phytosphäre, Forschungszentrum Jülich, D 52425, Jülich, Germany.
E Rothamsted Research, Harpenden, Hertfordshire AL5 2JQ, UK.
F Horticulture and Food Research Institute, Private Bag 92 169, Auckland, New Zealand.
G Brookhaven National Laboratory, Upton, NY 11973, USA.
H University of Connecticut, Department of Ecology and Evolutionary Biology, Storrs, CT 06269, USA.
I Current address: Brookhaven National Laboratory, Upton, NY 11973, USA. Corresponding author. Email: thorpe@bnl.gov
Functional Plant Biology 31(11) 1095-1103 https://doi.org/10.1071/FP04082
Submitted: 28 April 2004 Accepted: 21 September 2004 Published: 18 November 2004
Abstract
It has been observed that extension growth in maize roots is almost stopped by exposure to 5 mm d-galactose in the root medium, while the import of recent photoassimilate into the entire root system is temporarily promoted by the same treatment. The aim of this study was to reconcile these two apparently incompatible observations. We examined events near the root tip before and after galactose treatment since the tip region is the site of elongation and of high carbon deposition in the root. The treatment rapidly decreased root extension along the whole growing zone. In contrast, turgor pressure, measured directly with the pressure probe in the cortical cells of the growing zone, rapidly increased by 0.15 MPa within the first hour following treatment, and the increase was maintained over the following 24 h. Both tensiometric measurements and a comparison of turgor pressure with local growth rate demonstrated that a rapid tightening of the cell wall caused the reduction in growth. Single cell sampling showed cell osmotic pressure increased by 0.3 MPa owing to accumulation of both organic and inorganic solutes. The corresponding change in cell water potential was a rise from –0.18 MPa to approximately zero. More mature cells at 14 mm from the root tip (just outside the growing region) showed a qualitatively similar response.
Galactose treatment rapidly increased the import of recently fixed carbon (RFC) into the whole root as deduced by 11C labelling of photoassimilate. In contrast, there was a significant decrease in import of recently fixed carbon into the apical 5mm concomitant with the increase in turgor in this region. No decrease in import of recently fixed carbon was observed 5–15 mm from the root tip despite the increase in cortical cell turgor. These data are consistent with direct symplastic connections between the growing cells and the phloem supplying the solutes in the apical, but not the basal, regions of the growing zone. Hence, the inhibition of growth and the elevation of solute import induced by galactose are spatially separated within the root.
Keywords: cell solutes, cell wall, cell water relations, osmotic pressure, phloem transport, pressure probe, root growth, tissue mapping, turgor pressure, 11C.
Acknowledgments
This work was supported by: NZ Foundation for Research Science and Technology Contract C06X0001; International Science and Technology Linkages Fund of The Royal Society of New Zealand Contract 03-CSP-22-THOR; Leverhulme Trust Fellowship, UK to JP; Biotechnological and Biological Sciences Research Council of the United Kingdom via grant-aid to Rothamsted Research; Brookhaven National Laboratory Directed Research and Development Grant; USA Department of Energy, Office of Biological and Environmental Research Contract DE-ACO2–98CH10886.
Bret-Harte MS, Silk WK
(1994) Nonvascular, symplastic diffusion of sucrose cannot satisfy the carbon demands of growth in the primary root tip of Zea mays L. Plant Physiology 105, 19–33.
| PubMed |
Burström H
(1948) Observation on the influence of galactose on wheat roots. Physiologia Plantarum 1, 209–215.
Cheung SP, Cleland RE
(1991) Galactose inhibits auxin-induced growth of Avena coleoptiles by two mechanisms. Plant and Cell Physiology 32, 1015–1019.
| PubMed |
Clarke LJ,
Whalley WR,
Dexter AR,
Barraclough PB, Leigh RA
(1996) Complete mechanical impedance increases the turgor of the cells in the apex of pea roots. Plant, Cell and Environment 19, 1099–1102.
Clipson NJW,
Tomos AD,
Flowers TJ, Jones RGW
(1985) Salt tolerance in the halophyte Suaeda-maritima (L.) Dum. — the maintenance of turgor pressure and water-potential gradients in plants growing at different salinities. Planta 165, 392–396.
| Crossref |
Cosgrove DJ
(1987) Wall relaxation and the driving forces for cell expansive growth. Plant Physiology 84, 561–564.
| PubMed |
Croser C,
Bengough AG, Pritchard J
(2000) The effect of mechanical impedance on root growth in pea (Pisum sativum L.). 2. Cell expansion and wall rheology during expansion. Physiologia Plantarum 109, 150–159.
| Crossref | GoogleScholarGoogle Scholar |
Dick PES, ap Rees T
(1975) The pathway of sugar transport in Pisum sativum. Journal of Experimental Botany 26, 305–314.
Duckett CM,
Oparka KJ,
Prior DAM,
Dolan L, Roberts K
(1994) Dye-coupling in the root epidermis of Arabidopsis is progressively reduced during development. Development 120, 3247–3255.
Farrar, JF (1992). The whole plant: carbon partitioning during development. In ‘Carbon partitioning within and between organisms’. pp. 163–179. (Bios Scientific publishers: Oxford)
Farrar JF,
Minchin PEH, Thorpe MR
(1994) Carbon import into barley roots — stimulation by galactose. Journal of Experimental Botany 45, 17–22.
Ferrieri RA,
Gray DW,
Babst BA,
Schueller MJ,
Schlyer DJ,
Thorpe MR,
Orians CM, Lerdau M
(2005) Use of 11C in Populus shows that exogenous jasmonic acid increases biosynthesis of isoprene from recently fixed carbon. Plant, Cell and Environment (In press). ,
Giaquinta RT,
Lin W,
Sadler N, Franceschi VR
(1983) Pathway of phloem unloading of sucrose in corn roots. Plant Physiology 72, 362–367.
Hughes R, Street HE
(1974) Galactose as an inhibitor of the expansion of root cells. Annals of Botany 38, 555–564.
Hukin D,
Doering-Saad C,
Thomas CR, Pritchard J
(2002) Sensitivity of cell hydraulic conductivity to mercury is coincident with symplastic isolation and expression of plasmalemma aquaporin genes in growing maize roots. Planta 215, 1047–1056.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Hüsken D,
Zimmermann U, Steudle E
(1978) Pressure probe technique for measuring water relations of cells in higher plants. Plant Physiology 61, 158–163.
Lalonde S,
Tegeder M,
Throne-Holst M,
Frommer WB, Patrick JW
(2003) Phloem loading and unloading of sugars and amino acids. Plant, Cell and Environment 26, 37–56.
| Crossref | GoogleScholarGoogle Scholar |
Loughman BC,
Ratcliffe RG, Schwabe JWR
(1989) Galactose metabolism in Zea mays root tissues observed by P-31 NMR spectroscopy. Plant Science 59, 11–23.
| Crossref | GoogleScholarGoogle Scholar |
Malone M,
Leigh RA, Tomos AD
(1989) Extraction and analysis of sap for individual wheat leaf cells: the effect of sampling speed on the osmotic pressure of extracted sap. Plant, Cell and Environment 12, 919–926.
Minchin PEH, Thorpe MR
(1996) A method for monitoring γ-radiation from an extended source with uniform sensitivity. Applied Radiation and Isotopes 47, 693–696.
| Crossref | GoogleScholarGoogle Scholar |
Minchin PEH, Thorpe MR
(2003) Using the short-lived isotope 11C in mechanistic studies of photosynthate transport. Functional Plant Biology 30, 831–841.
| Crossref | GoogleScholarGoogle Scholar |
More RD, Troughton JH
(1973) Production of 11CO2 for use in plant translocation studies. Photosynthetica 7, 271–274.
Patrick JW
(1997) Phloem unloading: Sieve element unloading and post-sieve element transport. Annual Review of Plant Physiology and Plant Molecular Biology 48, 191–222.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Patrick JW, Offler CE
(1996) Post-sieve element transport of photoassimilates in sink regions. Journal of Experimental Botany 47, 1165–1177.
Pritchard J
(1994) The control of cell expansion in roots. New Phytologist 127, 3–26.
Pritchard J,
Tomos AD, Wyn Jones RG
(1987) Effects of ions on growth rate, wall rheology and cell water relations. Journal of Experimental Botany 38, 948–959.
Pritchard J,
Wyn Jones RG, Tomos AD
(1988) Control of wheat root growth. The effect of excision on growth, wall rheology and root anatomy. Planta 176, 399–405.
| Crossref |
Pritchard J,
Adams JS,
Barlow PW, Tomos AD
(1990) Biophysics of inhibition of root growth by low temperature. Plant Physiology 93, 222–230.
Pritchard J,
Wyn Jones RG, Tomos AD
(1991) Turgor, growth and rheological gradients of wheat roots following osmotic stress. Journal of Experimental Botany 42, 1043–1049.
Pritchard J,
Hetherington PR,
Fry SC, Tomos AD
(1993) Xyloglucan endotransglycosylase activity, microfibril orientation and the profiles of cell wall properties along growing regions of maize roots. Journal of Experimental Botany 44, 1281–1289.
Pritchard J,
Fricke W, Tomos AD
(1996) Turgor-regulation during extension growth and osmotic stress of maize roots. An example of single cell mapping. Plant and Soil 187, 11–21.
Pritchard J,
Winch S, Gould N
(2000) Phloem water relations and root growth. Australian Journal of Plant Physiology 27, 539–548.
Pritchard, J ,
Ford-Lloyd, B ,
and
Newbury, HJ (In press). Roots as an integrated part of the translocation pathway. In ‘Vascular transport in plants’. (Elsevier: Oxford)
Roberts PM, Butt VS
(1969) Patterns of incorporation of d-galactose into cell-wall polysaccharide of growing maize roots. Planta 84, 250–262.
| Crossref |
Sharp RE,
Hsiao TC, Silk WK
(1990) Growth of the primary root at low water potentials. II. Role of growth and deposition of hexose and potassium in osmotic adjustment. Plant Physiology 93, 1337–1346.
Spollen WG, Sharp RE
(1991) Spatial distribution of turgor and root growth at low water potentials. Plant Physiology 96, 438–443.
Tanimoto E,
Scott TK, Masuda Y
(1989) Inhibition of acid-enhanced elongation of Zea mays root segments by galactose Plant Physiology 90, 440–444.
Thorpe MR,
MacRae EA,
Minchin PEH, Edwards CM
(1999) Galactose stimulation of carbon import into roots is confined to the Poaceae. Journal of Experimental Botany 50, 1613–1618.
| Crossref | GoogleScholarGoogle Scholar |
Tomos AD, Leigh RA
(1999) The pressure probe: a versatile tool in plant cell physiology. Annual Review of Plant Physiology and Plant Molecular Biology 50, 447–472.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Tomos, AD ,
Hinde, PSS ,
Richardson, PBR ,
Pritchard, J ,
and
Fricke, W (1994). Microsampling and measurements of solutes in single cells. In ‘Plant cell biology: a practical approach’. pp. 297–314. (IRL Press: Oxford)
Triboulot MB,
Pritchard J, Tomos AD
(1995) Stimulation and inhibition of pine root growth by osmotic-stress. New Phytologist 130, 169–175.
Van Volkenburgh E,
Hunt S, Davies WJ
(1983) A simple instrument for measuring cell-wall extensibility. Annals of Botany 51, 669–672.
Verslues PE, Sharp RE
(1999) Proline accumulation in maize (Zea mays L.) primary roots at low water potentials. II. Metabolic source of increased proline deposition in the elongation zone. Plant Physiology 119, 1349–1360.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Williams JHH,
Minchin PEH, Farrar JF
(1991) Carbon partitioning in split root systems of barley — the effect of osmotica. Journal of Experimental Botany 42, 453–460.
Winch SK, Pritchard J
(1999) Acid-induced wall loosening is confined to the accelerating region of the root growing zone. Journal of Experimental Botany 50, 1481–1487.
| Crossref | GoogleScholarGoogle Scholar |
