Abstract
Background and aims
Close regulation of cellular Ca in roots is required in the face of marked changes in soil solution Ca over time and space. This study’s aims were to quantify and gain insights into the ways in which roots respond to changes in solution Ca.
Methods
Root elongation rate (RER) of cowpea (Vigna unguiculata (L.) Walp.) seedlings was determined at 0.05 to 15 mM Ca for up to 24 h both without and with added K, Mg, or Na. Root tip concentrations of Ca, K, Mg, and Na were determined and binding of cations by root tips estimated by subsequent Cu sorption.
Results
Transfer from higher to lower Ca solutions (and with added K at high Ca) resulted in RER ≥ 2 mm h−1 within minutes. This was attributed to greater cell wall relaxation through lower Ca binding aided by a decrease to pH ≤ 5.1 in solution. Transfer to higher Ca solutions, which remained at ~pH 5.6, led to an equally rapid decrease in RER to ~0.5 mm h−1, an effect ascribed to greater cell wall binding of Ca. Thereafter, a gradual increase in RER to ~1.8 mm h−1 occurred over 24 h, an effect likely due to reduced cell wall Ca binding as shown by decreasing Cu sorption at a rate of 0.027 mmol Cu kg−1 FM h−1 over 24 h.
Conclusion
The kinetics of changes in RER and cations in root tips suggest that roots respond to changes in solution Ca through effects on cell wall relaxation of the rhizodermis and outer cortex in the elongation zone.
Similar content being viewed by others
References
Albenne C, Canut H, Jamet E (2013) Plant cell wall proteomics: the leadership of Arabidopsis thaliana. Front Plant Sci 4:111. doi:10.3389/fpls.2013.00111
Baluška F, Volkman D, Barlow PW (1996a) Specialised zones of development in roots: view from the cellular level. Plant Physiol 112:3–4
Baluška F, Volkman D, Hauskrecht M, Barlow PW (1996b) Root cap mucilage and extracellular calcium as modulators of cellular growth in postmitotic growth zones of the maize root apex. Bot Acta 109:25–34
Bell RW, Edwards DG, Asher CJ (1989) Effects of calcium supply on uptake of calcium and selected mineral nutrients by tropical food legumes in solution culture. Aust J Agric Res 40:1003–1013
Blamey FPC, Dowling AJ (1995) Antagonism between aluminium and calcium for sorption by calcium pectate. Plant Soil 171:137–140
Blamey FPC, Nishizawa NK, Yoshimura E (2004) Timing, magnitude, and location of initial soluble aluminum injuries to mungbean roots. Soil Sci Plant Nutr 50:67–76
Braybrook SA, Peaucelle A (2013) Mechano-chemical aspects of organ formation in Arabidopsis thaliana: the relationship between auxin and pectin. PLoS ONE 8(3):e57813. doi:10.1371/journal.pone.0057813
Brett CT, Waldron KW (1996) Physiology and biochemistry of plant cell walls, 2nd edn. Chapman and Hall, London
Bruce RC, Warrell LA, Edwards DG, Bell LC (1988) Effects of aluminium and calcium in the soil solution of acid soils on root elongation of Glycine max cv. Forrest. Aust J Agric Res 39:319–338
Carpita NC, Gibeaut DM (1993) Structural models of primary cell walls of flowering plants: consistency of molecular structure with the physical properties of the walls during growth. Plant J 3:1–30
Cleland RE, Rayle DL (1977) Re-evaluation of the effect of calcium ions on auxin-induced elongation. Plant Physiol 60:709–712
Cosgrove DJ (2005) Growth of the plant cell wall. Nat Rev Mol Cell Biol 6:850–861
Dyer CL, Kopittke PM, Sheldon AR, Menzies NW (2008) Influence of soil moisture content on soil solution composition. Soil Sci Soc Am J 72:355–361
Eder M, Lütz-Meindl U (2008) Pectin-like carbohydrates in the green alga Micrasterias characterized by cytochemical analysis and energy filtering TEM. J Microsc 231:201–214
Edmeades DC, Wheeler DM, Clinton OE (1985) The chemical composition and ionic strength of soil solutions from New Zealand topsoils. Aust J Soil Res 23:151–165
Goldbach HE, Yu Q, Wingender R, Schulz M, Wimmer M, Findeklee P, Baluška F (2001) Rapid reaction of roots to boron deprivation. J Plant Nutr Soil Sci 164:173–181
Hasenstein KH, Evans ML (1986) Calcium dependence of rapid auxin action in maize roots. Plant Physiol 81:439–443
Hawkesford M, Horst W, Kichey T, Lambers H, Schjoerring J, Møller IS, White P (2012) Functions of macronutrients. In: Marschner P (ed) Marschner’s mineral nutrition of higher plants. Elsevier, Amsterdam, pp 135–189
Kinraide TB (1991) Identity of the rhizotoxic aluminium species. In: Wright RJ, Baligar VC Murrmann RP (eds) Plant-Soil Interactions at Low pH. Developments in Plant and Soil Sciences, vol 45. Kluwer Academic Publishers, Dordrecht, pp 717–728
Kinraide TB (2006) Plasma membrane surface potential (ΨPM) as a determinant of ion bioavailability: a critical analysis of new and published toxicological studies and a simplified method for the computation of plant ΨPM. Environ Toxicol Chem 25:3188–3198
Kinraide TB, Wang P (2010) The surface charge density of plant cell membranes (σ): an attempt to resolve conflicting values for intrinsic σ. J Exp Bot 61:2057–2518
Kobayashi M, Nakagawa H, Asaka T, Matoh T (1999) Borate-rhamnogalacturan II bonding reinforced by Ca2+ retains pectic polysaccharides in higher-plant cell walls. Plant Physiol 119:199–203
Kopittke PM, Blamey FPC, Menzies NW (2008) Toxicities of soluble Al, Cu, and La include ruptures to rhizodermal and root cortical cells of cowpea. Plant Soil 303:217–227
Kopittke PM, Blamey FPC, Kinraide TB, Wang P, Reichman SM, Menzies N (2011a) Separating multiple, short-term, deleterious effects of saline solutions on the growth of cowpea seedlings. New Phytol 189:1110–1121
Kopittke PM, Menzies NW, de Jonge MD, McKenna BA, Donner E, Webb RI, Paterson DJ, Howard DL, Ryan CG, Glover CJ, Scheckel KG, Lombi E (2011b) In situ distribution and speciation of toxic copper, nickel, and zinc in hydrated roots of cowpea. Plant Physiol 156:663–673
Kopittke PM, Wang P, Menzies NW, Naidu R, Kinraide TB (2013) A web-accessible computer program for calculating electrical potentials and ion activities at cell-membrane surfaces. Plant Soil 375(1–2):35–46
MacDougall AJ, Ring SG (2003) The hydration behaviour of pectin networks and plant cell walls. In: Voragen F, Schols H, Visser R (eds) Advances in pectin and pectinase research. Kluwer Academic Publishers, Dordrecht, pp 123–135
Marcus SE, Verhertbruggen Y, Hervé C, Ordaz-Ortiz JJ, Farkas V, Pedersen HL, Willats WGT, Knox JP (2008) Pectic homogalacturonan masks abundant sets of xyloglucan epitopes in plant cell walls. BMC Plant Biol 8:60. doi:10.1186/1471-2229-8-60
Marschner H, Romheld V, Horst WJ, Martin P (1986) Root-induced changes in the rhizosphere: importance for the mineral nutrition of plants. Z Pflanz Bodenk 149:441–456
McKenna BA, Nicholson TM, Wehr JB, Menzies NW (2010) Effects of Ca, Cu, Al and La on pectin gel strength: implications for plant cell walls. Carbohydr Res 345:1174–1179
McQueen-Mason SJ, Durachko DM, Cosgrove DJ (1992) Two endogenous proteins that induce cell wall extension in plants. Plant Cell 4:1425–1433
Mehrnoush A, Mustafa S, Yazid AMM (2012) Characterization of pectinase from mango (Mangifera indica cv. Chokanan) peel. J Food Agric Environ 10:85–88
Menzies NW, Edwards DG, Bell LC (1994) Effects of calcium and aluminium in the soil solution of acid, surface soils on root elongation of mungbean. Aust J Soil Res 32:721–737
Mondal K, Malhotra S, Jain V, Singh R (2009) Partial purification and characterization of pectinmethylesterase from ripening guava (Psidium guajava L.) fruits. Acta Physiol Plant 31:81–87
Morris ER, Powell DA, Gidley MJ, Rees DA (1982) Conformations and interactions of pectins. I. Polymorphism between gel and solid states of calcium polygalacturonate. J Mol Biol 155:507–516
Nantawisarakul T, Newman IA (1992) Growth and gravitropism of corn roots in solution. Plant Cell Environ 15:693–701
Rayle D, Cleland RE (1970) Enhancement of wall loosening and elongation by acid solutions. Plant Physiol 46:250–253
Ryan PR, Newman IA, Arif I (1992) Rapid calcium exchange for protons and potassium in cell walls of Chara. Plant Cell Environ 15:675–683
Sampedro J, Cosgrove DJ (2005) The expansin superfamily. Genome Biol 6:242. doi:10.1186/gb-2005-6-12-242
Sattelmacher B, Horst WJ (2007) The apoplast of higher plants: compartment of storage, transport, and reactions. Springer, Dordrecht
Shaff JE, Schultz BA, Craft EJ, Clark RT, Kochian LV (2010) GEOCHEM-EZ: a chemical speciation program with greater power and flexibility. Plant Soil 330:207–214
Spehar CR, Galwey NW (1997) Screening soya beans [Glycine max (L.) Merill] for calcium efficiency by root growth in low-Ca nutrient solution. Euphytica 94:113–117
Stael S, Wurzinger B, Mair A, Mehlmer N, Vothknecht UC, Teige M (2012) Plant organellar calcium signalling: an emerging field. J Exp Bot 63:1525–1542
Sun L, Peng XX, Sun P, Shi JH, Yuan XW, Zhu JJ, Tai GH, Zhou YF (2012) Structural characterization and immunostimulatory activity of a novel linear alpha-(1–6)-D-glucan isolated from Panax ginseng C. A. Meyer. Glycoconj J 29:357–364
Vandevenne E, Van Buggenhout S, Duvetter T, Brouwers E, Declerck PJ, Hendrickx ME, Van Loey A, Gils A (2009) Development and evaluation of monoclonal antibodies as probes to assess the differences between two tomato pectin methylesterase isoenzymes. J Immunol Methods 349:18–27
Walkinshaw MD, Arnott S (1981) Conformations and interactions of pectins. II. Models for junction zones in pectinic acid and calcium pectate gels. J Mol Biol 153:1075–1085
Wehr JB, Menzies NW, Blamey FPC (2004) Inhibition of cell-wall autolysis and pectin degradation by cations. Plant Physiol Bioch 42:485–492
Wehr JB, Blamey FPC, Menzies NW (2010) Comparison between methods using copper, lanthanum, and colorimetry for the determination of the cation exchange capacity of plant cell walls. J Agric Food Chem 58:4554–4559
Willats WGT, McCartney L, Mackie W, Knox JP (2001) Pectin: cell biology and prospects for functional analysis. Plant Mol Biol 47:9–27
Winch S, Pritchard J (1999) Acid-induced wall loosening is confined to the accelerating region of the root growing zone. J Exp Bot 50:1481–1487
Yang ZB, Eticha D, Albacete A, Rao IM, Roitsch T, Horst WJ (2012) Physiological and molecular analysis of the interaction between aluminium toxicity and drought stress in common bean (Phaseolus vulgaris). J Exp Bot 63:3109–3125
Acknowledgements
We thank D. Greenway for advice on statistical analyses. This research was supported in part by an Australian Research Council (ARC) DECRA Award (DE130100943) to Peng Wang and an ARC Future Fellowship (FT120100277) awarded to Peter Kopittke.
Author information
Authors and Affiliations
Corresponding author
Additional information
Responsible Editor: Ismail Cakmak.
Electronic supplementary material
Below is the link to the electronic supplementary material.
ESM 1
(XLSX 40 kb)
Rights and permissions
About this article
Cite this article
Blamey, F.P.C., Wehr, J.B., Wang, P. et al. Kinetics and mechanisms of cowpea root adaptation to changes in solution calcium. Plant Soil 379, 301–314 (2014). https://doi.org/10.1007/s11104-014-2065-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11104-014-2065-1