Abstract
Aims
The rhizosheath is defined as the weight of soil adhering strongly to roots on excavation, and current interest in this trait as a potential tolerance mechanism to abiotic stress has prompted us to explore the extent of its occurrence throughout the angiosperm phylogeny.
Methods
Here we describe a robust, novel method which was used to screen species for the presence/absence and strength of a rhizosheath. We correlate the latter with root hair length to provide insight into some of the factors affecting its formation. We go on to compare experimental data with previous observations in the literature.
Results
Results of a glasshouse screen demonstrate that rhizosheaths exist in species from many angiosperm orders, and the frequency of their occurrence and their strength and size are related. No correlation between root hair length and rhizosheath size was found, except when root hairs were extremely short, but the presence of root hairs was required for rhizosheath formation.
Conclusions
The rhizosheath is present in species from many angiosperm orders. Potential to enhance the trait is likely to exist in a range of crop species and could help contribute to future agricultural sustainability.
Similar content being viewed by others
References
Angiosperm Phylogeny Group [APG IV] (2016) An update of the angiosperm phylogeny group classification for the orders and families of flowering plants: APG IV. Bot J Linn Soc 181:1–20
Albalasmeh AA, Ghezzehei TA (2014) Interplay between soil drying and root exudation in rhizosheath development. Plant Soil 374:739–751
Ghezzehei TA, Albalasmeh AA (2015) Spatial distribution of rhizodeposits provides built-in water potential gradient in the rhizosphere. Ecol Model 298:53–63
Bailey C, Scholes M (1997) Rhizosheath occurrence in south African grasses. S Afr J Bot 63:484–490
Barre P, Hallett PD (2009) Rheological stabilization of wet soils by model root and fungal exudates depends on clay mineralogy. Eur J Sol Sci 60:525–538
Benard P, Kroener E, Vontobel P, Kaestner A, Carminati A (2016) Water percolation through the root-soil interface. Adv Water Res 95:190–198
Bennett AE, Daniell TJ, White PJ (2013) Benefits of breeding crops for yield response to soil organisms. In: de Bruijn FJ (ed) Molecular microbial ecology of the rhizosphere. Wiley-Blackwell, pp 17–27
Bergmann D, Zehfus M, Zierer L, Smith B, Gabel M (2009) Grass rhizosheaths: associated bacterial communities and potential for nitrogen fixation. West N Am Nat 69:105–114
Bristow CE, Campbell GS, Wullstein LH, Neilson R (1985) Water-uptake and storage by rhizosheaths of Oryzopsis hymenoides – a numerical simulation. Physiol Plantarum 65:228–232
Brown LK, George TS, Thompson JA, Wright G, Lyon J, Hubbard SF, White PJ (2012) What are the implications of variation in root hair length on P-limited yield in barley (Hordeum vulgare L.)? Ann Bot 10:319–328
Buckley R (1982) Sand rhizosheath of an arid zone grass. Plant Soil 66:417–421
Bulgarelli D, Schlaeppi K, Spaepen S, Ver Loren van Themaat E, Schulze-Lefert P (2013) Structure and functions of the bacterial microbiota of plants. Annu Rev Plant Biol 64:807–838
Bulgarelli D, Rott M, Schlaeppi K, Ver Loren van Themaat E, Ahmadinejad N, Assenza F, Rauf P, Huettel B, Reinhardt R, Schmelzer E et al (2012) Revealing structure and assembly cues for Arabidopsis root-inhabiting bacterial microbiota. Nature 488:91–95
Carminati A, Moradi AB, Vetterlein D, Vantobel P, Lehmann E, Weller U, Vogel H-J, Oswald SE (2010) Dynamics of soil water content in the rhizosphere. Plant Soil 332:163–176
Czarnes S, Dexter AR, Bartoli F (2000) Wetting and drying cycles in the maize rhizosphere under controlled conditions. Mechanics of the root-adhering soil. Plant Soil 221:253–271
Danin A (1996a) Adaptations of Stipagrostis species to desert dunes. J Arid Environ 34:297–311
Danin A (1996b) Plants of desert dunes. Springer-Verlag, Berlin
Davies TJ, Barraclough TG, Chase MW, Soltis PS, Soltis DE, Savolainen V (2004) Darwin’s abominable mystery: insights from a supertree of the angiosperms. Proc Natl A Sci USA 101:1904–1909
Delhaize E, Rathjen TM, Cavanagh CR (2015) The genetics of rhizosheath size in a multiparent mapping population of wheat. J Exp Bot 66:4527–4536
Delhaize E, James RA, Ryan PR (2012) Aluminium tolerance of root hairs underlies genotypic differences in rhizosheath size of wheat (Triticum aestivum) grown on acid soils. New Phytol 195:609–619
Downie HF, Adu MO, Schmidt S, Otten W, Dupuy LX, White PJ, Valentine TA (2015) Challenges and opportunities for quantifying roots and rhizosphere interactions through imaging and image analysis. Plant Cell Environ 38:1213–1232
Duell RW, Peacock GR (1985) Rhizosheaths on mesophytic grasses. Crop Sci 25:880–883
George TS, Brown LK, Ramsay L, White PJ, Newton AC, Bengough AG, Russell J, Thomas WTB (2014) Understanding the genetic control and physiological traits associated with rhizosheath production in barley (Hordeum vulgare). New Phytol 203:195–205
Goodchild DJ, Myers LF (1987) Rhizosheaths - a neglected phenomenon in Australian agriculture. Aust J Agric Res 38:559–563
Gregory PJ, Bengough AG, Grinev D, Schmidt S, Thomas WTB, Wojciechowski T, Young IM (2009) Root phenomics of crops: opportunities and challenges. Funct Plant Biol 36:922–929
Haling RE, Brown LK, Bengough AG, Valentine TA, White PJ, Young IM, George TS (2014) Effect of soil physical properties and soil water on root hair and rhizosheath development of barley mutants differing in root hair traits. Planta 239:643–651
Haling RE, Brown LK, Bengough AG, Young IM, Hallett PD, White PJ, George TS (2013) Root hairs improve root penetration, root-soil contact and phosphorus acquisition in soils of different strength. J Exp Bot 64:3711–3721
Haling RE, Richardson AE, Culvenor RA, Lambers H, Simpson RJ (2010) Root morphology, root-hair development and rhizosheath formation on perennial grass seedlings is influenced by soil acidity. Plant Soil 327:199–212
Harris PJ, Trethewey JAK (2010) The distribution of ester-linked ferulic acid in the cell walls of angiosperms. Phytochem Rev 9:19–33
James AR, Wellgama C, Verbyla K, Ryan PR, Rebetzke GJ, Rattey A, Richardson AE, Delhaize E (2016) Rhizosheaths on wheat grown in acid soils: phosphorus acquisition efficiency and genetic control. J Exp Bot 67:3709–3718
Jungk A (2001) Root hairs and the acquisition of plant nutrients from soil. J Plant Nutr Soil Sci 164:121–129
Koebernick N, Wellerc U, Huberd K, Schlutera S, Vogela HJ, Jahnb R, Vereeckend H, Vetterleina D (2014) In situ visualization and quantification of three-dimensional root system architecture and growth using X-Ray computed tomography. Vadose Zone J 13(8). doi:10.2136/vzj2014.03.0024
Lynch JP (2007) Roots of the second green revolution. Aust J Bot 55:493–512
McCully ME (1999) Roots in soil: unearthing the complexities of roots and their rhizospheres. Annu Rev Plant Phys 50:695–718
Moreno-Espíndola IP, Rivera-Becerrilb F, Ferrara-Guerrerob M d J, León-Gonzálezc F d (2007) Role of root-hairs and hyphae in adhesion of sand particles. Soil Biol Biochem 39:2520–2526
Nambiar EKS (1976) The uptake of zinc-65 by oats in relation to soil water content and root growth. Aust J Soil Res 14:67–74
North GB, Nobel PS (1997) Drought-induced changes in soil contact and hydraulic conductivity for roots of Opuntia ficus-indica with and without rhizosheaths. Plant Soil 191:249–258
Othman AA, Amer WM, Fayez M, Hegazi NA (2004) Rhizosheath of Sinai desert plants is a potential repository for associative diazotrophs. Microbiol Res 159:285–293
Pate JS, Dixon KW (1996) Convergence and divergence in the southwestern Australian flora in adaptations of roots to limited availability of water and nutrients, fire and heat stress. In: Hopper SD, Chappill JA, Harvey MS, George AS (eds) Gondwanan Heritage. Surrey Beatty & Sons, Chipping Norton, New South Wales, pp 249–258
Price SR (1911) The roots of some north African desert-grasses. New Phytol 10:328–340
Shane MW, McCully ME, Canny MJ, Pate JS, Lambers H (2011) Development and persistence of sandsheaths of Lyginia barbata (Restionaceae): relation to root structural development and longevity. Ann Bot 108:1307–1322
Shane MW, McCully ME, Canny MJ, Pate JS, Huang C, Ngo H, Lambers H (2010) Seasonal water relations of Lyginia barbata (southern rush) in relation to root xylem development and summer dormancy of root apices. New Phytol 185:1025–1037
Shane MW, McCully ME, Canny MJ, Pate JS, Ngo H, Mathesius U, Cawthray GR, Lambers H (2009) Summer dormancy and winter growth: root survival strategy in a perennial monocotyledon. New Phytol 183:1085–1096
Smith RJ, Hopper SD, Shane MW (2011) Sand-binding roots in Haemodoraceae global survey and morphology in a phylogenetic context. Plant Soil 348:453–470
Sprent JI (1975) Adherence of sand particles to soybean roots under water stress. New Phytol 74:461–463
The Plant List (2013) A working list of all plant species [WWW document] http://www.theplantlist.org/. Accessed 14 Mar 2017
Unno Y, Okubo K, Wasaki J, Shinano T, Osaki M (2005) Plant growth promotion abilities and microscale bacterial dynamics in the rhizosphere of lupin analysed by phytate utilization ability. Environ Microbiol 7:396–404
Volkens G (1887) Die Flora der Aegyptisch-arabischen Wuste auf Grundlage anatomisch-physiologischer Forschungen. Gerbruger Borntraeger, Berlin pp 156
Watt M, McCully ME, Canny MJ (1994) Formation and stabilization of rhizosheaths of Zea mays L. (effect of soil water content). Plant Physiol 106:179–186
Watt M, McCully ME, Jeffree CE (1993) Plant and bacterial mucilages of the maize rhizosphere: comparison of their soil binding properties and histochemistry in a model system. Plant Soil 151:151–165
White PJ, George TS, Gregory PJ, Bengough AG, Hallett PD, McKenzie BM (2013) Matching roots to their environment. Ann Bot 112:207–222
Wullstein LH (1991) Variation in N2 fixation (C2 H2 reduction) associated with rhizosheaths of Indian ricegrass (Stipa hymenoides). Am Mdl Nat 126:76–81
Young IM (1995) Variation in moisture contents between bulk soil and the rhizosheath of wheat (Triticum-aestivum L cv Wembley). New Phytol 130:135–139
Acknowledgements
This work was funded by the Rural & Environment Science & Analytical Services Division of the Scottish Government. We acknoweldge the suggestions made by the editor and reviewers of an earlier version of this manuscript.
Author information
Authors and Affiliations
Corresponding author
Additional information
Responsible Editor: Hans Lambers.
Rights and permissions
About this article
Cite this article
Brown, L.K., George, T.S., Neugebauer, K. et al. The rhizosheath – a potential trait for future agricultural sustainability occurs in orders throughout the angiosperms. Plant Soil 418, 115–128 (2017). https://doi.org/10.1007/s11104-017-3220-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11104-017-3220-2