Lawrie K. Brown1, Timothy S. George1, Konrad Neugebauer1,3, Philip J. White1,2

The Rhizosheath – A potential trait for future agricultural sustainability occurs in orders throughout the angiosperms.

Lawrie K. Brown1, Timothy S. George1, Konrad Neugebauer1,3, Philip J. White1,2

1The James Hutton Institute, Dundee, DD2 5DA, UK

2King Saud University, Riyadh 12372, Saudi Arabia

3University of Nottingham, Loughborough, LE12 5RD, UK

Corresponding author:

Timothy S. George

Tel:+44 1382 568700

Email:

Supplementary Material List S1: References for published data on the rhizosheath which were included in the meta-analysis and are referred to in Supplementary Material Table S2.

Abrahao A, Lambers H, Sawaya ACHF, Mazzafera P, Oliveira RS (2014) Convergence of a specialized root trait in plants from nutrient-impoverished soils: phosphorus-acquisition strategy in a nonmycorrhizal cactus. Oecologia 176: 345-355

Alami Y, Achouak W, Marol C, Heulin T (2000) Rhizosphere soil aggregation and plant growth promotion of sunflowers by an exopolysaccharide-producing Rhizobium sp. strain isolated from sunflower roots. Appl Environ Microbiol 66: 3393-3398

Ashraf M, Hasnain S, Berge O (2006) Effect of exo-polysaccharides producing bacterial inoculation on growth of roots of wheat (Triticum aestivum L.) plants grown in a salt-affected soil. Int J Environ Sci Tech 3: 43-51

Bailey C, Scholes M (1997) Rhizosheath occurrence in South African grasses. S Afr J Bot 63: 484-490

Bergmann D, Zehfus M, Zierer L, Smith B, Gabel M (2009) Grass rhizosheaths: associated bacterial communities and potential for nitrogen fixation. West N Am Naturalist 6:, 105-114

Blydenstein J (1966) Root systems of four desert grassland species on grazed and protected sites. J Range Manage 2: 93-95

Brejda JJ, Moser LE, Waller SS (1989) Rhizome and tiller development of three Nebraska sandhills warm-season grasses. Proceedings of the Eleventh North American Prairie Conference, 1989.

Bristow, C.E., Campbell, G.S., Wullstein, L.H., Neilson, R., 1985. A finite element simulation of water uptake through rhizosheaths of Oryzopsis hymenoides. Physiol Plantarum 65: 228-232

Brown LK, George TS, Thompson JA, Wright G, Lyon J, Dupuy L, Hubbard SF, White PJ (2012) What are the implications of variation in root hair length on tolerance to phosphorus deficiency in combination with water stress in barley (Hordeum vulgare)? Ann Bot 11: 319-328

Brown LK, George TS, White PJ (2013) Rhizosheaths of common plants in their natural environment. Personal observations (unplublished)

Buckley R (1982) Sand rhizosheath of an arid zone grass. Plant Soil 66: 417-421

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. 22: 253-271

Danin A (1996a) Adaptations of Stipagrostis species to desert dunes. Jl Arid Environ 34: 297-311

Danin A (1996b) Plants of Desert Dunes. Berlin and Heidelberg: Springer-Verlag.

Danin A, Kukkonen I (1995) Contributions to the flora of Israel. VIII. New Cyperus from Israel, Cyperus sharonensis Danin et Kukkonen Sp. N. Israel J Plant Sci 43: 77-82

De León-González F, Celada TE, Hidalgo-Moreno CI, Etchevers-Barra JD, Gutiérrez-Castorena MC, Flores-Macías A (2006) Root-soil adhesion in a volcanic sandy soil of Mexico. Soil Till Res 90: 77-83

Delhaize E, Taylor P, Hocking PJ, Simpson RJ, Ryan PR, Richardson AE (2009) Transgenic barley (Hordeum vulgare L.) expressing the wheat aluminium resistance gene (TaALMT1) shows enhanced phosphorus nutrition and grain production when grown on an acid soil. Plant Biotech J 7: 391-400

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 soil. New Phytol 195: 609-619

Dodd J, Heddle EM, Pate JS, Dixon KW. 1984. Rooting patterns of sandplain plants and their functional significance. In: Pate JS, Beard JS. eds. Kwongan - plant life of the sandplain: biology of a south-west Australian shrubland ecosystem. Nedlands, Australia: University of Western Australia Press, pp. 146-177.

Dubrovsky JG, North GB (2002) Root structure and function. In: Cacti: Biologi and Uses. PS Nobel (ed). Regents of the University of California.

Duell RW, Peacock GR (1985) Rhizosheaths on mesophytic grasses. Crop Sci 2: 880-883

Ebner M, Miranda T, Roth-Nebelsick A (2011) Efficient fog harvesting by Stipagrostis sabulicola (Namib dune bushman grass). J Arid Environ 75: 524-531

Ellis RP (2002) EcoPort Image ID 27667 Centropodia glauca, Rhizosheath. http://ecoport.org/ep?SearchType=pdb&PdbID=27667

Ennos AR (1991) The mechanics of anchorage in wheat Triticum aestivum L. II. Anchorage of mature wheat against lodging. J Exp Bot 42: 1607-1613

Fahn A, Cutler DF (1992) Xerophytes. Encyclopaedia of Plant Anatomy 13, 1-176. Gebrüder Borntraeger, Berlin.

Felger RS, Rutman S, Malusa J (2014) Ajo Peak to Tinajas Altas: A flora of southwestern Arizona. Part 6. Poaceae – grass family. Phytoneuron 2014-35: 1–139

Fyson A, Oaks A (1987) Physical factors involved in the formation of soil sheaths on corn seedling roots. Can. J Soil Sci. 67: 591-600

Fyson A, Kerr P, Lott JNA, Oaks A (1988) The structure of the rhizosphere of maize seedling roots: a cryogenic scanning electron microscopy study. Can J Bot 66: 2431-2435

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 by barley (Hordeum vulgare). New Phytol 203:195-205

Goodchild DJ, Myers LF (1987) Rhizosheaths - a neglected phenomenon in Australian agriculture. Aust J Agric Res 3: 559-63

Gouzou L, Burtin G, Philippy R, Bartoli F, Heulin T (1993) Effect of inoculation with Bacillus polymyxa on soil aggregation in the wheat rhizosphere: preliminary examination. Geoderma 56:479–490

Haling RE, Simpson RJ, Delhaize E, Hocking PJ, Richardson, AE (2010a) Effect of lime on root growth, morphology and the rhizosheath of cereal seedlings growing in an acid soil. Plant Soil 327: 199-212

Haling RE, Richardson AE, Culvenor RA, Lambers H, Simpson RJ (2010b) Root morphology, root-hair development and rhizosheath formation on perennial grass seedlings is influenced by soil acidity. Plant Soil 335: 457-468

Haling RE, Simpson RJ, Culvenor RA, Lambers H, Richardson AE (2011) Effect of soil acidity, soil strength and macropores on root growth and morphology of perennial grass species differing in acid-soil resistance. Plant Cell Environ 34: 444-456

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

Hanna AL, Youssef HH, Amer WM, Monib M, Fayez M, Hegazi NA (2013) Diversity of bacteria nesting the plant cover of north Sinai deserts, Egypt. Journal of Advanced Research 4, 13-26.

Harper KT, Pendleton RL (1993) Cyanobacteria and cyanolichens: Can they enhance availability of essential minerals for higher plants. Great Basin Nat 53: 59-72

Hartnett DC, Wilson GWT, Ott JP, Setshogo M (2013) Variation in root system traits among African semi-arid savanna grasses: Implications for drought tolerance. Austral Ecol 38: 383-392

Hayes P, Turner BL, Lambers H, Laliberté E (2014) Foliar nutrient concentrations and resorption efficiency in plants of contrasting nutrient-acquisition strategies along a 2-million-year dune chronosequence. J Ecol 102: 396-410

Hinsinger P (2012) EURoot Gallery. http://www.euroot.eu/gallery/album1/?page=viewall

Hinsinger P, Gobran GR, Gregory PJ, Wenzel WW (2005) Rhizosphere geometry and heterogeneity arising from root-mediated physical and chemical processes. New Phytol 168: 293–303

Huang, B, North GB, Nobel PS (1993) Soil sheaths, photosynthate distribution to roots, and rhizosphere water relations for Opuntia ficus-indica. Int J Plant Sci 154: 425-431

Körner C (2011) Alpandino. University of Basel: Basel. http://alpandino.org/en/course/07/07bh.htm

Kukkonen I (1995) New taxa, new combinations and notes on the treatment of Cyperaceae for Flora Iranica. Ann Bot Fenn 32: 153-164

Kukkonen I, Lye KA (1996) Cyperus medusaeus (Cyperaceae) redescribed. Annales Botanici Fennici 33: 21-27

Luo LM, Wang J, Wang LX, Qin LG, Wang K (2013) Comparison of physicochemical properties and microbe population between the surrounding soil and rhizosheath of Agropyron cristatum L. Acta Agr Sin 21: 1109-1112

Marshall AH, Howarth C, Cowan AA, Langdon T, Valentine J, McDevitt J, Macleod M, Clarke S, Bounds P (2010) Project Report 469: The incorporation of important traits underlying sustainable development of the oat crop through combining ‘conventional’ phenotypic selection with molecular marker technologies (OatLINK).

Masart J (1898) Un voyage botanique au Sahara. Bulletin de la Societe [Royale] Botanique de Belgique 37: - [pp. 237-240. In French]

McCully ME (1995a) How do real roots work? Some new views of root structure. Plant Physiol 109: 1-6

McCully ME (1995b) Water efflux from the surface of field-grown grass roots. Observations by cryo-scanning electronmicroscopy. Physiol Plantarum 95: 217-224

McCully ME (1999) Roots in soil: Unearthing the complexities of roots and their rhizospheres. Annu Rev Plant Physiol Plant Mol Biol. 50: 695-718

McCully ME (2005) The rhizosphere: the key functional unit in plant/soil/microbial interactions in the field. Implications for the understanding of allelopathic effects. http://www.regional.org.au/au/allelopathy/2005/1/1/2726_mccullyme.htm, last accessed 24/06/16.

McCully ME, Canny MJ (1988) Pathways and processes of water and nutrient movement in roots. Plant Soil 111: 159-170

McCully ME, Canny MJ, Huang CX (2009) Cryo-scanning electron microscopy (CSEM) in the advancement of functional plant biology. Morphological and anatomical applications. Funct Plant Biol 36: 97-124

Moreno- Espíndola IP, Rivera-Becerril F, Ferrara-Guerrero MJ, De León-González F (2007) Role of root hairs and hyphae in adhesion of sand particles. Soil Biol Biochem 39: 2520–2526

Moreno-Espíndola IP, Ferrara-Guerrero MJ, De León-González F, Rivera-Becerril F, González-Halphen D (2013) Cultivable bacterial community from the rhizosheath of Amaranthus hypochondriacus. Terra Latinoamericana 31: 57-69 [In Spanish]

Nambiar EKS (1976a) Uptake of Zn65 from dry soil by plants. Plant Soil 44: 267-271

Nambiar EKS (1976b) 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 (1992) Drought-induced changes in hydraulic conductivity and structure in roots of Ferocactus acanthodes and Opuntia ficus-indica. New Phytol 120: 9-19

North GB, Nobel PS (1994) Changes in root hydraulic conductivity for two tropical epiphytic cacti as soil moisture varies. Am J Bot 81: 46-53

North GB, Nobel PS (1997a) Drought-induced changes in soil contact and hydraulic conductivity for roots of Opuntia ficus-indica with and without rhizosheaths. Plant Soil, 191: 249-258.

North GB, Nobel PS (1997b) Root–soil contact for the desert succulent Agave deserti Engelm. in wet and drying soil. New Phytol 135: 21-29

Oliveira RS, Galvão HC, de Campos MCR, Eller CB, Pearse SJ, Lambers H (2015) Mineral nutrition of campos rupestres plant species on contrasting nutrient-impoverished soil types. New Phytol 205: 1183-1194

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

Parke JL, Liddell CM, Clayton MK (1990) Relationship between soil mass adhering to pea taproots and recovery of Pseudomonas fluorescens from the rhizosphere. Soil Biol Biochem 22: 495-499

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: Past, Present and Future of the western Australian Biota. Surrey Beatty & Sons, Chipping Norton, New South Wales, pp 249-258.

Peacock JM (1999) In: Breeding for low-nutrient environments: Is it sustainable? Adu-Gyamfi, J.J. (ed.) Food security in nutrient-stressed environments, exploiting plants' genetic capabilities: summary and recommendations of an International Workshop, 27-30 Sep 1999, ICRISAT, Patancheru, India.

Price SR (1911) The roots of some North American desert-grasses. New Phytol 10: 328-339

Pritchard SG, Rogers HH (2000) Spatial and temporal deployment of crop roots in CO2-enriched environments. New Phytol 147: 55-71

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

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, Lambers H (2011) Development and persistence of sandsheaths of Lyginia barbata (Restionaceae): relation to root structural development and longevity. Ann Bot 108: 1307-1322

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

Swanson MM, Fraser G, Daniell TJ, Torrance L, Gregory PJ, Taliansky M (2009) Viruses in soils: morphological diversity and abundance in the rhizosphere. Ann Appl Biol 155: 51-60

Thomas HH (1922) Some observations of plants in the Libyan desert. Journal of Ecology 9: 75-89

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

Vermeer J, McCully ME (1982) The rhizosphere in Zea: new insight into its structure and development. Planta 156: 45-61

Volkens G (1887) Die Flora der aegyptisch-arabischen Wuste auf Grundlage anatomisch-physiologischer Forschungen. Gebruder Borntraeger, Berlin.

Wang X-L, Canny MJ, McCully ME (1991) The water status of the roots of soil-grown maize in relation to the maturity of their xylem. Physiol Plantarum 82: 157-162

Watt M, McCully ME, Canny MJ (1994) Formation and stabilization of rhizosheaths of Zea mays L. Effect of soil water content. Plant Physiol 106: 1179-1186

Watt M, McCully ME, Kirkegaard, JA (2003) Soil strength and rate of root elongation alter the accumulation of Pseudomonas spp. and other bacteria in the rhizosphere of wheat. Funct Plant Biol 30; 483-491

Wenzel CL, McCully ME, Canny MJ (1989) Development of water conducting capacity in the root systems of young plants of corn and some other C4 grasses. Plant Physiol 89: 1094-1101

Wullstein LH (1980) Nitrogen fixation (acetylene reduction) associated with rhizosheaths of Indian ricegrass used in the stabilization of the Slick Rock, Colorado Tailings Pile. J Range Manage 33: 204-206

Wullstein LH (1991) Variation in N2 fixation (C2H2 reduction) associated with rhizosheaths of Indian ricegrass (Stipa hymenoides). Am Midl Nat 126: 76-81

Wullstein LH, Pratt SA (1981) Scanning electron microscopy of rhizosheaths of Oryzopsis hymenoides. Am J Bot 68: 408-19

Wullstein L H, Bruening ML, Bollen WB (1979) Nitrogen fixation associated with sand grain root sheaths (rhizosheaths) of certain xeric grasses. Physiol Plant 46: 1-4

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