Abstract
Background
First discovered on desert plants by Volkens 1887, rhizosheath formation, i.e. soil aggregation at the root surface, is now considered as a very promising adaptive trait to deal with abiotic stress. Indeed, the rhizosheath could help plants better cope with water stress, nitrogen and phosphorus deficiencies, and soil acidity.
Scope
We have reviewed studies on the biological factors involved in rhizosheath formation, the methods used to quantify it, and its importance in plant nutrition. Thus, we have collected recent evidence that shows that the rhizosheath is an important trait arising from the morphology and physiology of plant root system, and the cooperation between plant root and its associated microbiota. In particular, the transformation of root exudates by exopolysaccharide-producing bacteria effectively contributes to soil aggregation and thus to increases the volume of the rhizosheath (i.e. root-adhering soil), thereby improving the absorption of minerals and water by plants. The growing interest for this process has led to the genetic mapping of potential plant QTLs controlling this trait in order to provide new tools for the selection of plant varieties with improved tolerance to abiotic stresses.
Conclusion
Finally, we discussed some important issues that need to be addressed in order to develop an appropriate selection strategy focused on the rhizosheath, such as the relationship between the genes controlling rhizosheath formation and those controlling other root traits, but also the impact of rhizosheath formation on soil carbon sequestration, a potential strategy for mitigating climate change.
Similar content being viewed by others
References
Adu MO, Asare PA, Yawson DO, Ackah FK, Amoah KK, Nyarko MA, Andoh DA (2017) Quantifying variations in rhizosheath and root system phenotypes of landraces and improved varieties of juvenile maize. Rhizosphere 3:29–39. https://doi.org/10.1016/j.rhisph.2016.12.004
Akhtar J, Galloway AF, Nikolopoulos G, Field KJ, Knox P (2018) A quantitative method for the high throughput screening for the soil adhesion properties of plant and microbial polysaccharides and exudates. Plant Soil 428:57–65. https://doi.org/10.1007/s11104-018-3670-1
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. https://doi.org/10.1128/AEM.66.8.3393-3398.2000
Amellal N, Burtin G, Bartoli F, Heulin T (1998) Colonization of wheat roots by an exopolysaccharide-producing Pantoea agglomerans strain and its effect on rhizosphere soil aggregation. Appl Environ Microbiol 64:3740–3747
Ashraf M, Hasnain S, Berge O, Mahmood T (2004) Inoculating wheat seedlings with exopolysaccharide-producing bacteria restricts sodium uptake and stimulates plant growth under salt stress. Biol Fertil Soils 40:157–162. https://doi.org/10.1007/s00374-004-0766-y
Badri DV, Loyola-Vargas VM, Broeckling CD, de-la-Peña C, Jasinski M, Santelia D, Martinoia E, Sumner LW, Banta LM, Stermitz F, Vivanco JM (2008) Altered profile of secondary metabolites in the roote exudates of Arabidopsis ATP-binding cassette transporter mutants. Plant Physiol 146:762–771. https://doi.org/10.1104/pp.107.109587
Badri DV, Quintana N, Kassis EGE et al (2009) An ABC transporter mutation alters root exudation of phytochemicals that provoke an overhaul of natural soil microbiota. Plant Physiol 151:2006–2017. https://doi.org/10.1104/pp.109.147462
Bais HP, Weir TL, Perry LG, Gilroy S, Vivanco JM (2006) The role of root exudates in rhizosphere interactions with plants and other organisms. Annu Rev Plant Biol 57:233–266. https://doi.org/10.1146/annurev.arplant.57.032905.105159
Basirat M, Mousavi SM, Abbaszadeh S, Ebrahimi M, Zarebanadkouki M (2019) The rhizosheath: a potential root trait helping plants to tolerate drought stress. Plant Soil 445:565–575. https://doi.org/10.1007/s11104-019-04334-0
Bavel V, CH M (1950) Mean weight-diameter of soil aggregates as a statistical index of aggregation 1. Soil Sci Soc Am J 14:20–23. https://doi.org/10.2136/sssaj1950.036159950014000C0005x
Bedini S, Pellegrino E, Avio L, Pellegrini S, Bazzoffi P, Argese E, Giovannetti M (2009) Changes in soil aggregation and glomalin-related soil protein content as affected by the arbuscular mycorrhizal fungal species Glomus mosseae and Glomus intraradices. Soil Biol Biochem 41:1491–1496. https://doi.org/10.1016/j.soilbio.2009.04.005
Benard P, Kroener E, Vontobel P, Kaestner A, Carminati A (2016) Water percolation through the root-soil interface. Adv Water Resour 95:190–198. https://doi.org/10.1016/j.advwatres.2015.09.014
Bengough AG (2012). Water dynamics of the root zone: rhizosphere biophysics and its control on soil hydrology. Vadose zone J 11:vzj2011.0111. https://doi.org/10.2136/vzj2011.0111
Berge O, Lodhi A, Brandelet G, Santaella C, Roncato MA, Christen R, Heulin T, Achouak W (2009) Rhizobium alamii sp. nov., an exopolysaccharide-producing species isolated from legume and non-legume rhizospheres. Int J Syst Evol Microbiol 59:367–372. https://doi.org/10.1099/ijs.0.000521-0
Bezzate S, Aymerich S, Chambert R, Czarnes S, Berge O, Heulin T (2000) Disruption of the Paenibacillus polymyxa levansucrase gene impairs its ability to aggregate soil in the wheat rhizosphere. Environ Microbiol 2:333–342. https://doi.org/10.1046/j.1462-2920.2000.00114.x
Broadley MR, White PJ, Hammond JP, Zelko I, Lux A (2007) Zinc in plants. New Phytol 173:677–702. https://doi.org/10.1111/j.1469-8137.2007.01996.x
Broersma K, Robertson JA, Chanasyk DS (1997) The effects of diverse cropping systems on aggregation of a Luvisolic soil in the Peace River region. Can J Soil Sci 77:323–329. https://doi.org/10.4141/S96-013
Bronick CJ, Lal R (2005) Soil structure and management: a review. Geoderma 124:3–22. https://doi.org/10.1016/j.geoderma.2004.03.005
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 110:319–328. https://doi.org/10.1093/aob/mcs085
Brown LK, George TS, Neugebauer K, White PJ (2017) The rhizosheath – a potential trait for future agricultural sustainability occurs in orders throughout the angiosperms. Plant Soil 418:115–128. https://doi.org/10.1007/s11104-017-3220-2
Burak E, Dodd I, Quinton J (2018) Does root architecture influence the formation of rhizosheath? In: EGU general assembly conference abstracts. 20th EGU general assembly, EGU2018. Proceedings from the conference, Vienna, p 13505
Celik I, Ortas I, Kilic S (2004) Effects of compost, mycorrhiza, manure and fertilizer on some physical properties of a Chromoxerert soil. Soil Tillage Res 78:59–67. https://doi.org/10.1016/j.still.2004.02.012
Debieu M, Kanfany G, Laplaze L (2017) Pearl millet genome: lessons from a tough crop. Trends Plant Sci 22:911–913. https://doi.org/10.1016/j.tplants.2017.09.006
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. https://doi.org/10.1111/j.1469-8137.2012.04183.x
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. https://doi.org/10.1093/jxb/erv223
Drury CF, Stone JA, Findlay WI (1991) Microbial biomass and soil structure associated with corn, grasses, and legumes. Soil Sci Soc Am J 55:805–811. https://doi.org/10.2136/sssaj1991.03615995005500030029x
Duell RW, Peacock GR (1985) Rhizosheaths on mesophytic grasses. Crop Sci 25:880–883. https://doi.org/10.2135/cropsci1985.0011183X002500050036x
Fageria NK, Baligar VC, Jones CA (2010). Growth and mineral nutrition of field crops, Third edition, CRC Press
Fernández Bidondo L, Bompadre J, Pergola M, Silvani V, Colombo R, Bracamonte F, Godeas A (2012) Differential interaction between two Glomus intraradices strains and a phosphate solubilizing bacterium in maize rhizosphere. Pedobiologia 55:227–232. https://doi.org/10.1016/j.pedobi.2012.04.001
Figueiredo MVB, Burity HA, Martínez CR, Chanway CP (2008) Alleviation of drought stress in the common bean (Phaseolus vulgaris L.) by co-inoculation with Paenibacillus polymyxa and rhizobium tropici. Appl Soil Ecol 40:182–188. https://doi.org/10.1016/j.apsoil.2008.04.005
Galloway AF, Pedersen MJ, Merry B, Marcus SE, Blacker J, Benning LG, Field KJ, Knox JP (2018) Xyloglucan is released by plants and promotes soil particle aggregation. New Phytol 217:1128–1136. https://doi.org/10.1111/nph.14897
Garland G, Bünemann EK, Oberson A et al (2017) Plant-mediated rhizospheric interactions in maize-pigeon pea intercropping enhance soil aggregation and organic phosphorus storage. Plant Soil 415:37–55. https://doi.org/10.1007/s11104-016-3145-1
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. https://doi.org/10.1111/nph.12786
Gong X, McDonald G (2017) QTL mapping of root traits in phosphorus-deficient soils reveals important genomic regions for improving NDVI and grain yield in barley. Theor Appl Genet 130:1885–1902. https://doi.org/10.1007/s00122-017-2931-3
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 56:479–491. https://doi.org/10.1016/0016-7061(93)90128-8
Grover M, Ali SZ, Sandhya V, Rasul A, Venkateswarlu B (2011) Role of microorganisms in adaptation of agriculture crops to abiotic stresses. World J Microbiol Biotechnol 27:1231–1240. https://doi.org/10.1007/s11274-010-0572-7
Haichar FZ, Santaella C, Heulin T, Achouak W (2014) Root exudates mediated interactions belowground. Soil Biol Biochem 77:69–80. https://doi.org/10.1016/j.soilbio.2014.06.017
Haling RE, Richardson AE, Culvenor RA, Lambers H, Simpson RJ (2010a) Root morphology, root-hair development and rhizosheath formation on perennial grass seedlings is influenced by soil acidity. Plant Soil 335:457–468. https://doi.org/10.1007/s11104-010-0433-z
Haling RE, Simpson RJ, Delhaize E, Hocking PJ, Richardson AE (2010b) Effect of lime on root growth, morphology and the rhizosheath of cereal seedlings growing in an acid soil. Plant Soil 327:199–212. https://doi.org/10.1007/s11104-009-0047-5
Harrison MT, Tardieu F, Dong Z, Messina CD, Hammer GL (2014) Characterizing drought stress and trait influence on maize yield under current and future conditions. Glob Chang Biol 20:867–878. https://doi.org/10.1111/gcb.12381
Haynes RJ, Francis GS (1993) Changes in microbial biomass C, soil carbohydrate composition and aggregate stability induced by growth of selected crop and forage species under field conditions. Eur J Soil Sci 44:665–675. https://doi.org/10.1111/j.1365-2389.1993.tb02331.x
Hiltner L (1904). Uber neue erfahrungen und probleme auf dem gebiete der bodenbakteriologie. Arbeiten der Deutschen Landwirtschaft Gesellschaft 98,59–78 -. Arbeiten der Deutschen Landwirtschaft Gesellschaft 59–78
Hinsinger P (2001) Bioavailability of soil inorganic P in the rhizosphere as affected by root-induced chemical changes: a review. Plant Soil 237:173–195. https://doi.org/10.1023/A:1013351617532
Hochholdinger F, Yu P, Marcon C (2018) Genetic control of root system development in maize. Trends Plant Sci 23:79–88. https://doi.org/10.1016/j.tplants.2017.10.004
Holz M, Zarebanadkouki M, Kuzyakov Y, Pausch J, Carminati A (2018) Root hairs increase rhizosphere extension and carbon input to soil. Ann Bot 121:61–69. https://doi.org/10.1093/aob/mcx127
Ismail AM, Heuer S, Thomson MJ, Wissuwa M (2007) Genetic and genomic approaches to develop rice germplasm for problem soils. Plant Mol Biol 65:547–570. https://doi.org/10.1007/s11103-007-9215-2
James RA, Weligama 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. https://doi.org/10.1093/jxb/erw035
Kaci Y, Heyraud A, Barakat M, Heulin T (2005) Isolation and identification of an EPS-producing rhizobium strain from arid soil (Algeria): characterization of its EPS and the effect of inoculation on wheat rhizosphere soil structure. Res Microbiol 156:522–531. https://doi.org/10.1016/j.resmic.2005.01.012
Kemper WD, Rosenau RC (1986). Aggregate stability and size distribution. In: methods of soil analysis, part 1, physical and mineralogical methods. Pp 425–442
Kirkby EA, Johnston AEJ (2008). Soil and fertilizer phosphorus in relation to crop nutrition. In: the ecophysiology of plant-phosphorus interactions, plant Ecophysiology. Springer, p 177
Kohler-Milleret R, Le Bayon R-C, Chenu C et al (2013) Impact of two root systems, earthworms and mycorrhizae on the physical properties of an unstable silt loam Luvisol and plant production. Plant Soil 370:251–265. https://doi.org/10.1007/s11104-013-1621-4
Lesk C, Rowhani P, Ramankutty N (2016) Influence of extreme weather disasters on global crop production. Nature 529:84–87. https://doi.org/10.1038/nature16467
Li J, Zhu S, Song X, Shen Y, Chen H, Yu J, Yi K, Liu Y, Karplus VJ, Wu P, Deng XW (2006) A rice glutamate receptor–like gene is critical for the division and survival of individual cells in the root apical meristem. Plant Cell 18:340–349. https://doi.org/10.1105/tpc.105.037713
Liu M, Rathjen T, Weligama K, Forrest K, Hayden M, Delhaize E (2017) Analysis of aneuploid lines of bread wheat to map chromosomal locations of genes controlling root hair length. Ann Bot 119:1333–1341. https://doi.org/10.1093/aob/mcx030
Liu T-Y, Ye N, Song T, Cao Y, Gao B, Zhang D, Zhu F, Chen M, Zhang Y, Xu W, Zhang J (2018) Rhizosheath formation and involvement in foxtail millet (Setaria italica) root growth under drought stress. J Integr Plant Biol 61:449–462. https://doi.org/10.1111/jipb.12716
Liu T-Y, Chen M-X, Zhang Y, Zhu FY, Liu YG, Tian Y, Fernie AR, Ye N, Zhang J (2019) Comparative metabolite profiling of two switchgrass ecotypes reveals differences in drought stress responses and rhizosheath weight. Planta. 250:1355–1369. https://doi.org/10.1007/s00425-019-03228-w
Lynch JP (2007) Roots of the second green revolution. Aust J Bot 55:493–512. https://doi.org/10.1071/BT06118
Lynch JP (2011) Root phenes for enhanced soil exploration and phosphorus acquisition: tools for future crops. Plant Physiol 156:1041–1049. https://doi.org/10.1104/pp.111.175414
Lynch JP (2019) Root phenotypes for improved nutrient capture: an underexploited opportunity for global agriculture. New Phytol 223:548–564. https://doi.org/10.1111/nph.15738
Milleret R, Le Bayon R-C, Lamy F et al (2009) Impact of roots, mycorrhizas and earthworms on soil physical properties as assessed by shrinkage analysis. J Hydrol 373:499–507. https://doi.org/10.1016/j.jhydrol.2009.05.013
Morel JL, Habib L, Plantureux S, Guckert A (1991) Influence of maize root mucilage on soil aggregate stability. Plant Soil 136:111–119. https://doi.org/10.1007/BF02465226
Moreno-Espíndola IP, Rivera-Becerril F, de Jesús F-GM, De León-González F (2007) Role of root-hairs and hyphae in adhesion of sand particles. Soil Biol Biochem 39:2520–2526. https://doi.org/10.1016/j.soilbio.2007.04.021
Mueller ND, Gerber JS, Johnston M et al (2012) Closing yield gaps through nutrient and water management. Nature 490:254–257. https://doi.org/10.1038/nature11420
Ndour PMS, Gueye M, Barakat M, Ortet P, Bertrand-Huleux M, Pablo AL, Dezette D, Chapuis-Lardy L, Assigbetsé K, Kane NA, Vigouroux Y, Achouak W, Ndoye I, Heulin T, Cournac L (2017) Pearl millet genetic traits shape rhizobacterial diversity and modulate rhizosphere aggregation. Front Plant Sci 8. https://doi.org/10.3389/fpls.2017.01288
Nguyen C (2003) Rhizodeposition of organic C by plants: mechanisms and controls. Agron Sustain Dev 23:22–396. https://doi.org/10.1051/agro:2003011
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. https://doi.org/10.1023/A:1004213728734
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. https://doi.org/10.1016/j.micres.2004.05.004
Pang J, Ryan MH, Siddique KHM, Simpson RJ (2017) Unwrapping the rhizosheath. Plant Soil 418:129–139. https://doi.org/10.1007/s11104-017-3358-y
Peng S, Guo T, Liu G (2013) The effects of arbuscular mycorrhizal hyphal networks on soil aggregations of purple soil in Southwest China. Soil Biol Biochem 57:411–417. https://doi.org/10.1016/j.soilbio.2012.10.026
Peterson RL, Farquhar ML (1996) Root hairs: specialized tubular cells extending root surfaces. Bot Rev 62:1–40
Phillips RP, Brzostek E, Midgley MG (2013) The mycorrhizal-associated nutrient economy: a new framework for predicting carbon–nutrient couplings in temperate forests. New Phytol 199:41–51. https://doi.org/10.1111/nph.12221
Price SR (1911) The roots of some north African desert-grasses. New Phytol 10:328–340. https://doi.org/10.1111/j.1469-8137.1911.tb06524.x
Rebetzke GJ, Verbyla AP, Verbyla KL, Morell MK, Cavanagh CR (2014) Use of a large multiparent wheat mapping population in genomic dissection of coleoptile and seedling growth. Plant Biotechnol J 12:219–230. https://doi.org/10.1111/pbi.12130
Richards RA, Watt M, Rebetzke GJ (2007) Physiological traits and cereal germplasm for sustainable agricultural systems. Euphytica 154:409–425. https://doi.org/10.1007/s10681-006-9286-1
Robertson-Albertyn S, Alegria Terrazas R, Balbirnie K, Blank M, Janiak A, Szarejko I, Chmielewska B, Karcz J, Morris J, Hedley PE, George TS, Bulgarelli D (2017) Root hair mutations displace the barley rhizosphere microbiota. Front Plant Sci 8. https://doi.org/10.3389/fpls.2017.01094
Rodriguez RJ, Redman RS, Henson JM (2004) The role of fungal symbioses in the adaptation of plants to high stress environments. Mitig Adapt Strateg Glob Chang 9:261–272. https://doi.org/10.1023/B:MITI.0000029922.31110.97
Saijo Y, Hata S, Kyozuka J, Shimamoto K, Izui K (2000) Over-expression of a single Ca2+−dependent protein kinase confers both cold and salt/drought tolerance on rice plants. Plant J 23:319–327. https://doi.org/10.1046/j.1365-313x.2000.00787.x
Salazar-Henao JE, Vélez-Bermúdez IC, Schmidt W (2016) The regulation and plasticity of root hair patterning and morphogenesis. Development 143:1848–1858. https://doi.org/10.1242/dev.132845
Sandhya V, AS Z, Grover M et al (2009) Alleviation of drought stress effects in sunflower seedlings by the exopolysaccharides producing Pseudomonas putida, strain GAP-P45. Biol Fertil Soils 46:17–26. https://doi.org/10.1007/s00374-009-0401-z
Sasse J, Martinoia E, Northen T (2018) Feed your friends: do Plant exudates shape the root microbiome? Trends Plant Sci 23:25–41. https://doi.org/10.1016/j.tplants.2017.09.003
Shane MW, McCully ME, Canny MJ et al (2009) Summer dormancy and winter growth: root survival strategy in a perennial monocotyledon. New Phytol 183:1085–1096. https://doi.org/10.1111/j.1469-8137.2009.02875.x
Sherwood S, Fu Q (2014) A drier future? Science 343:737–739. https://doi.org/10.1126/science.1247620
Singh U, Wilkens P, Chude V, Oikeh S (1999). Predicting the effect of nitrogen deficiency on crop growth duration and yield. In: Precision Agriculture. pp. 1379–1393
Six J, Frey SD, Thiet RK, Batten KM (2006) Bacterial and fungal contributions to carbon sequestration in agroecosystems. Soil Sci Soc Am J 70:555–569. https://doi.org/10.2136/sssaj2004.0347
Smith S, Read D (2008). Mycorrhizal Symbiosis - 3rd edition. In: academic press. New York, USA, p 800
Traoré O, Groleau-Renaud V, Plantureux S, Tubeileh A, Boeuf-Tremblay V (2000) Effect of root mucilage and modelled root exudates on soil structure. Eur J Soil Sci 51:575–581. https://doi.org/10.1111/j.1365-2389.2000.00348.x
Varshney RK, Shi C, Thudi M, Mariac C, Wallace J, Qi P, Zhang H, Zhao Y, Wang X, Rathore A, Srivastava RK, Chitikineni A, Fan G, Bajaj P, Punnuri S, Gupta SK, Wang H, Jiang Y, Couderc M, Katta MAVSK, Paudel DR, Mungra KD, Chen W, Harris-Shultz KR, Garg V, Desai N, Doddamani D, Kane NA, Conner JA, Ghatak A, Chaturvedi P, Subramaniam S, Yadav OP, Berthouly-Salazar C, Hamidou F, Wang J, Liang X, Clotault J, Upadhyaya HD, Cubry P, Rhoné B, Gueye MC, Sunkar R, Dupuy C, Sparvoli F, Cheng S, Mahala RS, Singh B, Yadav RS, Lyons E, Datta SK, Hash CT, Devos KM, Buckler E, Bennetzen JL, Paterson AH, Ozias-Akins P, Grando S, Wang J, Mohapatra T, Weckwerth W, Reif JC, Liu X, Vigouroux Y, Xu X (2017) Pearl millet genome sequence provides a resource to improve agronomic traits in arid environments. Nat Biotech advance online publication 35:969–976. https://doi.org/10.1038/nbt.3943
Villain-Simonnet A, Milas M, Rinaudo M (2000a) A new bacterial polysaccharide (YAS34). I. Characterization of the conformations and conformational transition. Int J Biol Macromol 27:65–75. https://doi.org/10.1016/S0141-8130(99)00120-8
Villain-Simonnet A, Milas M, Rinaudo M (2000b) A new bacterial exopolysaccharide (YAS34). II. Influence of thermal treatments on the conformation and structure. Relation with gelation ability. Int J Biol Macromol 27:77–87. https://doi.org/10.1016/S0141-8130(99)00119-1
Volkens G (1887). Die Flora der aegyptisch-arabischen Wüste: auf Grundlage anatomisch-physiologischer Forschungen. Gebrüder Borntraeger 156 p
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. https://doi.org/10.1007/BF00016280
Wen T-J, Schnable PS (1994) Analyses of mutants of three genes that influence root hair development in Zea mays (Gramineae) suggest that root hairs are dispensable. Am J Bot 81:833–842. https://doi.org/10.1002/j.1537-2197.1994.tb15564.x
Wojciechowski T, Gooding MJ, Ramsay L, Gregory PJ (2009) The effects of dwarfing genes on seedling root growth of wheat. J Exp Bot 60:2565–2573. https://doi.org/10.1093/jxb/erp107
Wu Q-S, Cao M-Q, Zou Y-N, He X (2014). Direct and indirect effects of glomalin, mycorrhizal hyphae, and roots on aggregate stability in rhizosphere of trifoliate orange. Sci Rep 4:. https://doi.org/10.1038/srep05823
Wu Q-S, Srivastava AK, Cao M-Q, Wang J (2015) Mycorrhizal function on soil aggregate stability in root zone and root-free hyphae zone of trifoliate orange. Arch Agron Soil Sci 61:813–825. https://doi.org/10.1080/03650340.2014.952226
Wullstein LH (1991) Variation in N2 fixation (C2 H2 reduction) associated with rhizosheaths of Indian ricegrass (Stipa hymenoides). Am Midl Nat 126:76–81. https://doi.org/10.2307/2426151
Yan X, Liao H, Beebe SE, Blair MW, Lynch JP (2004) QTL mapping of root hair and acid exudation traits and their relationship to phosphorus uptake in common bean. Plant Soil 265:17–29. https://doi.org/10.1007/s11104-005-0693-1
Yu P, Gutjahr C, Li C, Hochholdinger F (2016) Genetic control of lateral root formation in cereals. Trends Plant Sci 21:951–961. https://doi.org/10.1016/j.tplants.2016.07.011
Zhao D, Reddy KR, Kakani VG, Reddy VR (2005) Nitrogen deficiency effects on plant growth, leaf photosynthesis, and hyperspectral reflectance properties of sorghum. Eur J Agron 22:391–403. https://doi.org/10.1016/j.eja.2004.06.005
Zhu J, Kaeppler SM, Lynch JP (2005) Mapping of QTL controlling root hair length in maize (Zea mays L.) under phosphorus deficiency. Plant Soil 270:299–310. https://doi.org/10.1007/s11104-004-1697-y
Zou Y-N, Chen X, Srivastava A, Wang P, Xiang L, Wu QS (2016) Changes in rhizosphere properties of trifoliate orange in response to mycorrhization and sod culture. Appl Soil Ecol 107:307–312. https://doi.org/10.1016/j.apsoil.2016.07.004
Acknowledgments
This work was supported by the French National Research Institute for Sustainable Development (IRD), the Make Our Planet Great Again (MOPGA) initiative of the French government (PMS Ndour postdoctoral fellowship), and by the Agence Nationale de la Recherche (ANR) through the RootAdapt grant (N° ANR-17-CE20-0022).
Author information
Authors and Affiliations
Corresponding author
Additional information
Responsible Editor: Tim S. George
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Ndour, P.M.S., Heulin, T., Achouak, W. et al. The rhizosheath: from desert plants adaptation to crop breeding. Plant Soil 456, 1–13 (2020). https://doi.org/10.1007/s11104-020-04700-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11104-020-04700-3