Root Hair Growth and Development in Response to Nutrients and Phytohormones

  • De-Jian Zhang
  • Yu-Jie Yang
  • Chun-Yan Liu
  • Fei Zhang
  • Qiang-Sheng Wu
Part of the Soil Biology book series (SOILBIOL, volume 52)


Root hair is tubular projections from the root epidermal cell. In general, root hair formation results in a significant increase in root surface area, which plays the important roles in nutrient and water uptake, plant anchorage, and interaction with soil microorganisms. In this chapter, we discussed the effects of mineral nutrients (nitrogen, phosphorus, potassium, calcium, iron, and magnesium) and phytohormones (auxin, ethylene, jasmonic acid, methyl jasmonate, strigolactones, and brassinosteroids) on root hair growth and their relevant mechanisms. Interaction exists between nutrients and phytohormones on root hair growth and development. Especially, the interaction between auxin and ethylene plays an important role in regulation of root hair development. The effects of jasmonic acid, strigolactone, and brassinosteroids on root hair growth partly depend on the way of auxin and ethylene. As a result, more works are needed to clone the genes of additional root hair mutants and elucidate their roles, as well as undertaking reverse genetics and mutant complementation studies to add the current knowledge of the signaling networks, which are involved in root hair cell fate specification, initiation, tip growth, and maturation regulated by nutrients and phytohormones.


Auxin Calcium Ethylene Phosphorus Root hair Phytohormones 



This study was supported by the Yangtze Youth Fund (2016cqn64) and the Yangtze Initial Fund (801190010132) of Yangtze University and the Plan in Scientific and Technological Innovation Team of Outstanding Young, Hubei Provincial Department of Education (T201604).


  1. Bai L, Ma X, Zhang G, Song S, Zhou Y, Gao L, Miao Y, Song CP (2014) A receptor-like kinase mediates ammonium homeostasis and is important for the polar growth of root hairs in Arabidopsis. Plant Cell 26:1497–1511PubMedPubMedCentralCrossRefGoogle Scholar
  2. Bates TR, Lynch JP (1996) Stimulation of root hair elongation in Arabidopsis thaliana by low phosphorus availability. Plant Cell Environ 19:529–538CrossRefGoogle Scholar
  3. Bates TR, Lynch JP (2000) The efficiency of Arabidopsis thaliana (Brassicaceae) root hairs in phosphorus acquisition. Am J Bot 87:964–970PubMedCrossRefGoogle Scholar
  4. Bibikova TN, Zhigilei A, Gilroy S (1997) Root hair growth in Arabidopsis thaliana is directed by calcium and an endogenous polarity. Planta 203:495–505PubMedCrossRefGoogle Scholar
  5. Bloch D, Monshausen G, Gilroy S, Yalovsky S (2011) Co-regulation of root hair tip growth by ROP GTPases and nitrogen source modulated pH fluctuations. Plant Signal Behav 6:426–429PubMedPubMedCentralCrossRefGoogle Scholar
  6. 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 110:319–328PubMedPubMedCentralCrossRefGoogle Scholar
  7. Bruex A, Kainkaryam RM, Wieckowski Y, Kang YH, Bernhardt C, Xia Y, Zheng X, Wang JY, Lee MM, Benfey P et al (2012) A gene regulatory network for root epidermis cell differentiation in Arabidopsis. PLoS Genet 8:e1002446PubMedPubMedCentralCrossRefGoogle Scholar
  8. Bush DS (1995) Calcium regulation in plant cells and its role in signaling. Annu Rev Plant Biol 9:95–122CrossRefGoogle Scholar
  9. Cakmak I, Yazici AM (2010) Magnesium: a forgotten element in crop production. Better Crops 11:23–25Google Scholar
  10. Cao X, Chen CL, Zhang DJ, Shu B, Xiao J, Xia RX (2013) Influence of nutrient deficiency on root architecture and root hair morphology of trifoliate orange (Poncirus trifoliata L. Raf.) seedlings under sand culture. Scientia Horticulturae 162:100–105CrossRefGoogle Scholar
  11. Carol RJ, Dolan L (2002) Building a hair: tip growth in Arabidopsis thaliana root hairs. Philos Trans R Soc Lond B Biol Sci 357:815–821PubMedPubMedCentralCrossRefGoogle Scholar
  12. Carol RJ, Dolan L (2006) The role of reactive oxygen species in cell growth: lessons from root hairs. J Exp Bot 57:1829–1834PubMedCrossRefGoogle Scholar
  13. Cho M, Lee SH, Cho HT (2007a) P-glycoprotein4 displays auxin efflux transporter-like action in Arabidopsis root hair cells and tobacco cells. Plant Cell 19:3930–3943PubMedPubMedCentralCrossRefGoogle Scholar
  14. Cho M, Lee OR, Ganguly A, Cho HT (2007b) Auxin-signaling: short and long. J Plant Biol 50:79–89CrossRefGoogle Scholar
  15. Clowes FAL (2000) Pattern in root meristem development in angiosperms. New Phytol 146:83–94CrossRefGoogle Scholar
  16. Cormack RGH (1947) A comparative study of developing epidermal cells in white mustard and tomato roots. Am J Bot 34:310–314CrossRefGoogle Scholar
  17. Curie C, Mari S (2017) New routes for plant iron mining. New Phytol 214:521PubMedCrossRefGoogle Scholar
  18. Derevyanchuk M, Litvinovskaya R, Khripach V, Martinec J, Kravets V (2015) Effect of 24-epibrassinolide on Arabidopsis thaliana alternative respiratory pathway under salt stress. Acta Physiol Plant 37:1–10CrossRefGoogle Scholar
  19. Di CM et al (1996) The Arabidopsis ATHB10 (GLABRA2) is a HD-ZIP protein required for repression of ectopic root hair formation. Plant J 10:393–402CrossRefGoogle Scholar
  20. Dolan L (2001) The role of ethylene in root hair growth in Arabidopsis. J Plant Nutr Soil Sci 164:141–145CrossRefGoogle Scholar
  21. Dolan L (2017) Root hair development in grasses and cereals (Poaceae). Curr Opin Genet Dev 45:76–81PubMedCrossRefGoogle Scholar
  22. Dolan L, Costa S (2001) Evolution and genetics of root hair stripes in the root epidermis. J Exp Bot 52(suppl 1):413–417PubMedCrossRefPubMedCentralGoogle Scholar
  23. Dolan L, Janmaat K, Willemsen V, Linstead P, Poethig S, Roberts K, Scheres B (1993) Cellular organisation of the Arabidopsis thaliana root. Development 119:71–84PubMedGoogle Scholar
  24. Duckett CM, Grierson C, Linstead P, Schneider K, Lawson E, Dean C, Poethig S, Roberts K (1994) Clonal relationships and cell patterning in the root epidermis of Arabidopsis. Development 120:2465–2474Google Scholar
  25. Felle HH, Hepler PK (1997) The cytosolic Ca2+-concentration gradient of Sinapis alba root hairs as revealed by Ca2+-selective microelectrode tests and fura-dextran ratio imaging. Plant Physiol 114:39–45PubMedPubMedCentralCrossRefGoogle Scholar
  26. Föhse D, Claassen N, Jungk A (1991) Phosphorus efficiency of plants: II. Significance of root radius, root hairs and cation-onion balance for phosphorus influx in seven plant species. Plant Soil 132:261–272CrossRefGoogle Scholar
  27. Forde BG (2002) Local and long-range signaling pathways regulating plant responses to nitrate. Annu Rev Plant Biol 53:203–224PubMedCrossRefGoogle Scholar
  28. Foreman J, Demidchik V, Bothwell JH, Mylona P, Miedema H, Torres MA, Linstead P, Costa S, Brownlee C, Jones JD, Davies JM, Dolan L (2003) Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. Nature 422:442–446PubMedCrossRefGoogle Scholar
  29. Frahry G, Schopfer P (1998) Inhibition of O2-reducing activity of horseradish peroxidase by diphenyleneiodonium. Phytochemistry 48:223–227PubMedCrossRefGoogle Scholar
  30. Gahoonia TS, Nielsen NE (1998) Direct evidence on participation of root hair in phosphorus (32P) uptake from soil. Plant Soil 198:147–152CrossRefGoogle Scholar
  31. Gahoonia TS, Care D, Nielsen NE (1997) Root hairs and phosphorus acquisition of wheat and barley cultivars. Plant Soil 191:181–188CrossRefGoogle Scholar
  32. Galway ME, Masucci JD, Lloyd AM, Walbot V, Davis RW (1994) The TTG gene is required to specify epidermal cell fate and cell patterning in the Arabidopsis root. Dev Biol 166:740–754PubMedCrossRefPubMedCentralGoogle Scholar
  33. Galway ME, Heckman JW Jr, Schiefelbein JW (1997) Growth and ultrastructure of Arabidopsis root hairs: the rhd3 mutation alters vacuole enlargement and tip growth. Planta 201:209–218PubMedCrossRefGoogle Scholar
  34. Ganguly A, Lee SH, Cho M, Lee OR, Yoo H, Cho HT (2010) Differential auxin-transporting activities of PIN-FORMED proteins in Arabidopsis root hair cells. Plant Physiol 153:1046–1061PubMedPubMedCentralCrossRefGoogle Scholar
  35. Gassmann W, Schroeder JI (1994) Inward-rectifying K+ channels in root hairs of wheat: a mechanism for aluminum-sensitive low-affinity K+ uptake and membrane potential control. Plant Physiol 105:1399–1408PubMedPubMedCentralCrossRefGoogle Scholar
  36. Gilroy S, Jones DL (2000) Through form to function: root hair development and nutrient uptake. Trends Plant Sci 5:56–60PubMedCrossRefGoogle Scholar
  37. Gomezroldan V, Fermas S, Brewer PB et al (2008) Strigolactone inhibition of shoot branching. Nature 455:189–194CrossRefGoogle Scholar
  38. Gransee A, Führs H (2013) Magnesium mobility in soils as a challenge for soil and plant analysis, magnesium fertilization and root uptake under adverse growth conditions. Plant Soil 368:5–21CrossRefGoogle Scholar
  39. Grierson C, Schiefelbein J (2002) Root hairs. In: Somerville C, Meyerowitz EM (eds) The Arabidopsis book, vol 1. American Society of Plant Biologists, RockvilleGoogle Scholar
  40. Hardtke CS, Dorcey E, Osmont KS, Sibout R (2007) Phytohormone collaboration: zooming in on auxin-brassinosteroid interactions. Trends Cell Biol. 17:485–492PubMedCrossRefGoogle Scholar
  41. Hentrich M, Böttcher C, Düchting P, Cheng Y, Zhao Y, Berkowitz O, Masle J, Medina J, Pollmann S (2013) The jasmonic acid signaling pathway is linked to auxin homeostasis through the modulation of YUCCA8 and YUCCA9 gene expression. Plant J 74:626–637PubMedPubMedCentralCrossRefGoogle Scholar
  42. Hepler PK, Vidali L, Cheung AY (2001) Polarized cell growth in higher plants. Annu Rev Cell Dev Biol 17:159–187PubMedCrossRefGoogle Scholar
  43. Herrmann A, Felle HH (1995) Tip growth in root hair cells of Sinapis alba L.: significance of internal and external Ca21 and pH. New Phytol 129:523–533CrossRefGoogle Scholar
  44. Hoffmann C, Jungk A (1995) Growth and phosphorus supply of sugar beet as affected by soil compaction and water tension. Plant Soil 176:15–25CrossRefGoogle Scholar
  45. Jones DL, Shaff JE, Kochian LV (1995) Role of calcium and other ions in directing root hair tip growth in Limnobium stoloniferum. I. Inhibition of tip growth by aluminum. Planta 197:672–680CrossRefGoogle Scholar
  46. Jones AR, Kramer EM, Knox K, Swarup R, Bennett MJ, Lazarus CM, Leyser HMO, Grierson CS (2009) Auxin transport through non-hair cells sustains root-hair development. Nat Cell Biol 11:78–84PubMedCrossRefGoogle Scholar
  47. Jung JY, Shin R, Schachtman DP (2009) Ethylene mediates response and tolerance to potassium deprivation in Arabidopsis. Plant Cell 21:607PubMedPubMedCentralCrossRefGoogle Scholar
  48. Jungk A (2015) Root hairs and the acquisition of plant nutrients from soil. J Plant Nutr Soil Sci 164:121–129CrossRefGoogle Scholar
  49. Kadota Y, Goh T, Tomatsu H et al (2004) Cryptogein-induced initial events in tobacco BY-2 cells: pharmacological characterization of molecular relationship among cytosolic Ca2+ transients, anion efflux and production of reactive oxygen species. Plant Cell Physiol 45:160–170PubMedCrossRefGoogle Scholar
  50. Kapulnik Y, Delaux PM, Resnick N et al (2011) Strigolactones affect lateral root formation and root-hair elongation in Arabidopsis. Planta 233:209–216PubMedCrossRefGoogle Scholar
  51. Kieber JJ, Rothenberg M, Roman G, Feldmann KA, Ecker JR (1993) CTR1, a negative regulator of the ethylene response pathway in Arabidopsis, encodes a member of the Raf family of protein kinases. Cell 72:427–441PubMedCrossRefGoogle Scholar
  52. Kim CM, Dolan L (2011) Root hair development involves asymmetric cell division in Brachypodium distachyon and symmetric division in Oryza sativa. New Phytol 192:601–610PubMedCrossRefGoogle Scholar
  53. Kim DW, Lee SH, Choi SB, Won SK, Heo YK, Cho M, Park YI, Cho HT (2006a) Functional conservation of a root hair cell-specific cis-element in angiosperms with different root hair distribution patterns. Plant Cell 18:2958–2970PubMedPubMedCentralCrossRefGoogle Scholar
  54. Kim H, Park PJ, Hwang HJ, Lee SY, Oh MH, Kim SG (2006b) Brassinosteroid signals control expression of the AXR3/IAA17 gene in the cross-talk point with auxin in root development. Biosci Biotechnol Biochem 70:768–773PubMedCrossRefGoogle Scholar
  55. Kim MC, Chung WS, Yun D, Cho MJ (2009) Calcium and calmodulin-mediated regulation of gene expression in plants. Mol Plant 2:13–21PubMedPubMedCentralCrossRefGoogle Scholar
  56. Knox K, Grierson CS, Leyser O (2003) AXR3 and SHY2 interact to regulate root hair development. Development 130:5769–5777PubMedCrossRefGoogle Scholar
  57. Koltai H, Dor E, Hershenhorn J et al (2010) Strigolactones’ effect on root growth and root-hair elongation may be mediated by Auxin-efflux carriers. J Plant Growth Regul 29:129–136CrossRefGoogle Scholar
  58. Kuhn BM, Nodzyński T, Errafi S et al (2017) Flavonol-induced changes in PIN2 polarity and auxin transport in the Arabidopsis thaliana rol1-2 mutant require phosphatase activity. Sci Rep 7:41906PubMedPubMedCentralCrossRefGoogle Scholar
  59. Kwasniewski M, Chwialkowska K, Kwasniewska J et al (2013) Accumulation of peroxidase-related reactive oxygen species in trichoblasts correlates with root hair initiation in barley. J Plant Physiol 170:185PubMedCrossRefGoogle Scholar
  60. LaňKová M, Smith RS, Pešek B et al (2010) Auxin influx inhibitors 1-NOA, 2-NOA, and CHPAA interfere with membrane dynamics in tobacco cells. J Exp Bot 61:3589–3598PubMedPubMedCentralCrossRefGoogle Scholar
  61. Lee SH, Cho HT (2009) Auxin and root hair morphogenesis. Plant Cell Monogr 12:45–64CrossRefGoogle Scholar
  62. Lee RDW, Cho HT (2013) Auxin, the organizer of the hormonal/environmental signals for root hair growth. Front Plant Sci 4:448PubMedPubMedCentralGoogle Scholar
  63. Li S, Yu JL, Zhu M, Zhao F, Luan S (2012) Cadmium impairs ion homeostasis by altering K+, and Ca2+, channel activities in rice root hair cells. Plant Cell Environ 35:1998–2013PubMedCrossRefGoogle Scholar
  64. Li TC, Yang HY, Zhang W, Xu DF, Dong Q, Wang F, Lei YL, Liu GH, Zhou YB, Chen HJ, Li C (2017) Comparative transcriptome analysis of root hairs proliferation induced by water deficiency in maize. J Plant Biol 60:26–34CrossRefGoogle Scholar
  65. Libault M, Brechenmacher L, Cheng J, Xu D, Stacey G (2010) Root hair systems biology. Trends Plant Sci 15:641–650PubMedCrossRefGoogle Scholar
  66. Lima JV, Lobato AKS (2017) Brassinosteroids improve photosystem II efficiency, gas exchange, antioxidant enzymes and growth of cowpea plants exposed to water deficit. Physiol Mol Biol Plants 23:59–72PubMedPubMedCentralCrossRefGoogle Scholar
  67. Lin CY, Huang LY, Chi WC, Huang TL, Kakimoto T, Tsai CR, Huang HJ (2015) Pathways involved in vanadate-induced root hair formation in Arabidopsis. Physiol Plant 153:137–148PubMedCrossRefGoogle Scholar
  68. Mano Y, Nemoto K (2012) The pathway of auxin biosynthesis in plants. J Exp Bot 63:2853–2872PubMedCrossRefGoogle Scholar
  69. Marchant A, Kargul J, May ST, Muller P, Delbarre A, Perrot-Rechenmann C, Bennett MJ (1999) AUX1 regulates root gravitropism in Arabidopsis by facilitating auxin uptake within root apical tissues. EMBO J 18:2066–2073PubMedPubMedCentralCrossRefGoogle Scholar
  70. Marschner A (1995) Mineral nutrition of higher plants. Academic, San Diego, CAGoogle Scholar
  71. Masucci JD, Schiefelbein JW (1994) The rhd6 mutation of Arabidopsis thaliana alters root-hair initiation through an Auxin- and Ethylene-associated process. Plant Physiol 106:1335–1346PubMedPubMedCentralCrossRefGoogle Scholar
  72. Masucci JD, Schiefelbein JW (1996) Hormones act downstream of TTG and GL2 to promote root hair outgrowth during epidermis development in the Arabidopsis root. Plant Cell 8:1505–1517PubMedPubMedCentralCrossRefGoogle Scholar
  73. Masucci JD et al (1996) The homeobox gene GLABRA2 is required for position-dependent cell differentiation in the root epidermis in Arabidopsis thaliana. Development 122:1253–1260PubMedGoogle Scholar
  74. Mayzlish-Gati E, De-Cuyper C, Goormachtig S, Beeckman T, Vuylsteke M, Brewer PB, Beveridge CA, Yermiyahu U, Kaplan Y, Enzer Y, Wininger S, Resnick N, Cohen M, Kapulnik Y, Koltai H (2012) Strigolactones are involved in root response to low phosphate conditions in Arabidopsis. Plant Physiol 160:1329–1341PubMedPubMedCentralCrossRefGoogle Scholar
  75. Meharg AA, Blatt MR (1995) NO3 - transport across the plasma-membrane of Arabidopsis thaliana root hairs-kinetic control by pH and membrane voltage. J Membr Biol 145:49–66PubMedCrossRefGoogle Scholar
  76. Miao BH, Han XG, Zhang WH (2010) The ameliorative effect of silicon on soybean seedlings grown in potassium-deficient medium. Ann Bot 105:967PubMedPubMedCentralCrossRefGoogle Scholar
  77. Michael G (2001) The control of root hair formation: suggested mechanisms. J Plant Nutr Soil Sci 164:111–119CrossRefGoogle Scholar
  78. Miller DD, Callaham DA, Gross DJ, Hepler PK (1992) Free Ca2+ gradient in growing pollen tubes of Lilium. J Cell Sci 101:7–12Google Scholar
  79. Moeder W, Barry CS, Tauriainen AA, Betz C, Tuomainen J, Utriainen M, Grierson D, Sandermann H, Langebartels C, Kangasjärvi J (2002) Ethylene synthesis regulated by biphasic induction of 1-aminocyclopropane-1-carboxylic acid synthase and 1-aminocyclopropane-1-carboxylic acid oxidase genes is required for hydrogen peroxide accumulation and cell death in ozone-exposed tomato. Plant Physiol 130:1918–1926PubMedPubMedCentralCrossRefGoogle Scholar
  80. Mouchel CF et al (2004) Natural genetic variation in Arabidopsis identifies BREVIS RADIX, a novel regulator of cell proliferation and elongation in the root. Genes Dev 18:700–714PubMedPubMedCentralCrossRefGoogle Scholar
  81. Mouchel CF et al (2006) BRX mediates feedback between brassinosteroid levels and auxin signalling in root growth. Nature 443:458–461PubMedCrossRefGoogle Scholar
  82. Muday GK, Rahman A, Binder BM (2012) Auxin and ethylene: collaborators or competitors. Trends Plant Sci 17:181–195PubMedCrossRefGoogle Scholar
  83. Muller M, Schmidt W (2004) Environmentally induced plasticity of root hair development in Arabidopsis. Plant Physiol 134:409–419PubMedPubMedCentralCrossRefGoogle Scholar
  84. Nestler J, Liu S, Wen TJ, Paschold A, Marcon C, Tang HM, Li D, Li L, Meeley RB, Sakai H, Bruce W, Schnable PS, Hochholdinger F (2014) Roothairless5, which functions in maize (Zea mays L.) root hair initiation and elongation encodes a monocot-specific NADPH oxidase. Plant J 79:729–740PubMedCrossRefGoogle Scholar
  85. Niu Y, Jin CW, Jin G, Zhou Q, Lin X, Tang C, Zhang Y (2011) Auxin modulates the enhanced development of root hairs in Arabidopsis thaliana (L.) Heynh. under elevated CO2. Plant Cell Environ 34:1304–1317PubMedCrossRefGoogle Scholar
  86. Niu Y, Jin G, Yong SZ (2014) Root development under control of magnesium availability. Plant Signal Behav 9:e29720PubMedPubMedCentralCrossRefGoogle Scholar
  87. Parimalan R, Giridhar P, Ravishankar GA (2011) Enhanced shoot organogenesis in Bixa orellana L: in the presence of putrescine and silver nitrate. Plant Cell Tissue Organ Cult 105:285–290CrossRefGoogle Scholar
  88. Parker JS, Cavell AC, Dolan L et al (2000) Genetic interactions during root hair morphogenesis in Arabidopsis. Plant Cell 12:1961–1974PubMedPubMedCentralCrossRefGoogle Scholar
  89. Peret B, Clement M, Nussaume L, Desnos T (2011) Root developmental adaptation to phosphate starvation: better safe than sorry. Trends Plant Sci 16:442–450PubMedCrossRefGoogle Scholar
  90. Pettigrew WT (2008) Potassium influences on yield and quality production for maize, wheat, soybean and cotton. Physiologia Plantarum 133:670–681PubMedCrossRefGoogle Scholar
  91. Pierson ES, Miller DD, Callaham DA et al (1994) Pollen tube growth is coupled to the extracellular calcium ion flux and the intracellular calcium gradient: effect of BAPTA-type buffers and hypertonic media. Plant Cell 6:1815–1828PubMedPubMedCentralCrossRefGoogle Scholar
  92. Pierson ES, Miller DD, Callaham DA, van Aken J, Hackett G, Hepler PK (1996) Tip-localized calcium entry fluctuates during pollen tube growth. Dev Biol 174:160–173PubMedCrossRefGoogle Scholar
  93. Pitts RJ, Cernac A, Estelle M (1998) Auxin and ethylene promote root hair elongation in Arabidopsis. Plant J 16:553–560PubMedCrossRefGoogle Scholar
  94. Raghothama KG, Karthikeyan AS (2005) Phosphate acquisition. Plant Soil 274:37–49CrossRefGoogle Scholar
  95. Rahman A, Hosokawa S, Oono Y, Amakawa T, Goto N, Tsurumi S (2002) Auxin and ethylene response interactions during Arabidopsis root hair development dissected by auxin influx modulators. Plant Physiol 130:1908–1917PubMedPubMedCentralCrossRefGoogle Scholar
  96. Ribaudo CM, Krumpholz EM, Cassán FD, Bottini R, Cantore ML, Curá JA (2006) Azospirillum sp: promotes root hair development in tomato plants through a mechanism that involves ethylene. J Plant Growth Regul 25:175–185CrossRefGoogle Scholar
  97. Rigas S, Debrosses G, Haralampidis K, Vicente-Agullo F, Feldmann KA, Grabov A, Dolan L, Hatzopoulos P (2001) TRH1 encodes a potassium transporter required for tip growth in Arabidopsis root hairs. Plant Cell 13:139–151PubMedPubMedCentralCrossRefGoogle Scholar
  98. Rigas S, Ditengou FA, Ljung K, Daras G, Tietz O, Palme K, Hatzopoulos P (2013) Root gravitropism and root hair development constitute coupled developmental responses regulated by auxin homeostasis in the Arabidopsis root apex. New Phytol 197:1130–1141PubMedCrossRefGoogle Scholar
  99. Růžička R, Ljung K, Vanneste S, Podhorská R, Beeckman T, Friml J, Benková E (2007) Ethylene regulates root growth through effects on auxin biosynthesis and transport-dependent auxin distribution. Plant Cell 19:2197–2212PubMedPubMedCentralCrossRefGoogle Scholar
  100. Sanders D, Pelloux J, Brownlee C, Harper JF (2002) Calcium at the crossroads of signaling. Plant Cell 14:S401–S417PubMedPubMedCentralCrossRefGoogle Scholar
  101. Savage NS, Walker T, Wieckowski Y, Schiefelbein J, Dolan L, Monk NA (2008) A mutual support mechanism through intercellular movement of CAPRICE and GLABRA3 can pattern the Arabidopsis root epidermis. PLoS Biol 6:e235PubMedPubMedCentralCrossRefGoogle Scholar
  102. Schellmann S, Schnittger A, Kirik V, Wada T, Okada K, Beermann A, Thumfahrt J, Jürgens G, Hülskamp M (2002) TRIPTYCHON and CAPRICE mediate lateral inhibition during trichome and root hair patterning in Arabidopsis. EMBO J 21:5036–5046PubMedPubMedCentralCrossRefGoogle Scholar
  103. Schiefelbein J (2003) Cell-fate specification in the epidermis: a common patterning mechanism in the root and shoot. Curr Opin Plant Biol 6:74–78PubMedCrossRefGoogle Scholar
  104. Schiefelbein JW, Shipley A, Rowse P (1992) Calcium influx at the tip of growing root-hair cells of Arabidopsis thaliana. Planta 187:455–459PubMedCrossRefGoogle Scholar
  105. Schmidt W, Schikora A (2001) Different pathways are involved in phosphate and iron stress-induced alterations of root epidermal cell development. Plant Physiol 125:2078–2084PubMedPubMedCentralCrossRefGoogle Scholar
  106. Shah SH, Ali S, Jan SA, Din JU, Ali GM (2014) Assessment of silver nitrate on callus induction and in vitro shoot regeneration in tomato (Solanum lycopersicum Mill.) Pak J Bot 46:2163–2172Google Scholar
  107. Shin R, Schachtman DP (2004) Hydrogen peroxide mediates plant root response to nutrient deprivation. Proc Natl Acad Sci USA 101:8827–8832PubMedPubMedCentralCrossRefGoogle Scholar
  108. Shin R, Berg RH, Schachtman DP (2005) Reactive oxygen species and root hairs in Arabidopsis root response to nitrogen, phosphorus and potassium deficiency. Plant Cell Physiol 46:1350–1357PubMedCrossRefGoogle Scholar
  109. Shin LJ, Huang HE, Chang H, Lin YH, Feng TY, Ger MJ (2011) Ectopic ferredoxin I protein promotes root hair growth through induction of reactive oxygen species in Arabidopsis thaliana. J Plant Physiol 168:434–440PubMedCrossRefGoogle Scholar
  110. Siminis CI, Stavrakakis MN (2008) Iron induces root and leaf ferric chelate reduction activity in grapevine rootstock 140 Ruggeri. Hortscience 43:685–690Google Scholar
  111. Strader LC, Bartel B (2009) The Arabidopsis PLEIOTROPIC DRUG RESISTANCE8/ABCG36 ATP binding cassette transporter modulates sensitivity to the auxin precursor indole-3-butyric acid. Plant Cell 21:1992–2007PubMedPubMedCentralCrossRefGoogle Scholar
  112. Strader LC, Chen GL, Bartel B (2010) Ethylene directs auxin to control root cell expansion. Plant J 64:874–884PubMedPubMedCentralCrossRefGoogle Scholar
  113. Sundaravelpandian K, Chandrika NNP, Schmidt W (2013) PFT1, a transcriptional Mediator complex subunit, controls root hair differentiation through reactive oxygen species (ROS) distribution in Arabidopsis. New Phytol 197:151–161PubMedCrossRefGoogle Scholar
  114. Swarup R, Péret B (2012) AUX/LAX family of auxin influx carriers-an overview. Front Plant Sci 3:225PubMedPubMedCentralCrossRefGoogle Scholar
  115. Takahashi H, Kawahara A, Inoue Y (2003) Ethylene promotes the induction by auxin of the cortical microtubule randomization required for low-pH-induced-root hair initiation in lettuce (Lactuca sativa L.) seedlings. Plant Cell Physiol 44:932–940PubMedCrossRefGoogle Scholar
  116. Takeda S, Gapper C, Kaya H, Bell E, Kuchitsu K, Dolan L (2008) Local positive feedback regulation determines cell shape in root hair cells. Science 319:1241–1244PubMedCrossRefGoogle Scholar
  117. Tanaka N, Kato M, Tomioka R, Kurata R, Fukao Y, Aoyama T, Maeshima M (2014) Characteristics of a root hair-less line of Arabidopsis thaliana under physiological stresses. J Exp Bot 65:1497–1512PubMedPubMedCentralCrossRefGoogle Scholar
  118. Tanimoto M, Roberts K, Dolan L (1995) Ethylene is a positive regulator of root hair development in Arabidopsis thaliana. Plant J 8:943–948PubMedCrossRefGoogle Scholar
  119. Tromas A, Perrot-Rechenmann C (2010) Recent progress in auxin biology. CR Biol 333:297–306CrossRefGoogle Scholar
  120. Tsai HH, Schmidt W (2017) Mobilization of iron by plant-borne coumarins. Trends Plant Sci 22:538–548PubMedCrossRefGoogle Scholar
  121. Vandamme E, Renkens M, Pypers P, Smolders E, Vanlauwe B, Merckx R (2013) Root hairs explain P uptake efficiency of soybean genotypes grown in a P-deficient Ferralsol. Plant Soil 369:269–282CrossRefGoogle Scholar
  122. Vicente-Agullo F, Rigas S, Desbrosses G, Dolan L, Hatzopoulos P, Grabov A (2004) Potassium carrier TRH1 is required for auxin transport in Arabidopsis roots. Plant J 40:523–535PubMedCrossRefGoogle Scholar
  123. Vincent C, Rowland D, Na C, Schaffer B (2017) A high-throughput method to quantify root hair area in digital images taken in situ. Plant Soil 412:61–80CrossRefGoogle Scholar
  124. Wada T, Tachibana T, Shimura Y, Okada K (1997) Epidermal cell differentiation in Arabidopsis is determined by a Myb homolog, CPC. Science 227:1113–1116CrossRefGoogle Scholar
  125. Wang Y, Kristian TK, Stoumann JL, Jakob M (2016) Vigorous root growth is a better indicator of early nutrient uptake than root hair traits in spring wheat grown under low fertility. Front Plant Sci 7:865PubMedPubMedCentralGoogle Scholar
  126. Waters MT, Gutjahr C, Bennett T et al (2017) Strigolactone signaling and evolution. Annu Rev Plant Biol 68:291PubMedCrossRefGoogle Scholar
  127. Weinl S, Kudla J (2009) The CBL-CIPK Ca2+-decoding signaling network: function and perspectives. New Phytol 184:517–528PubMedCrossRefGoogle Scholar
  128. White PJ, Broadley MR (2003) Calcium in plants. Ann Bot 92:487–511PubMedPubMedCentralCrossRefGoogle Scholar
  129. Wu Y, He D (2011) Advances in root hairs in Gramineae and Triticum aestivum. Afr J Agric Res 6:1047–1050Google Scholar
  130. Wu QS, Liu CY, Zhang DJ et al (2016) Mycorrhiza alters the profile of root hairs in trifoliate orange. Mycorrhiza 26:237–247PubMedCrossRefGoogle Scholar
  131. Wymer CL, Bibikova TN, Gilroy S (1997) Cytoplasmic free calcium distribution during the development of root hairs of Arabidopsis thaliana. Plant J 12:427–439PubMedCrossRefGoogle Scholar
  132. Xie X, Yoneyama K, Yoneyama K (2010) The strigolactone story. Annu Rev Phytopathol 48:93PubMedCrossRefGoogle Scholar
  133. Yan XL, 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 265:17–29CrossRefGoogle Scholar
  134. Yang HB, Murphy AS (2009) Functional expression and characterization of Arabidopsis ABCB, AUX1 and PIN auxin transporters in Schizosaccharomyces pombe. Plant J 59:179–191PubMedCrossRefGoogle Scholar
  135. Yang N, Zhu C, Gan L, Ng D, Xia K (2011) Ammonium-stimulated root hair branching is enhanced by methyl jasmonate and suppressed by ethylene in Arabidopsis thaliana. J Plant Biol 54:92–100CrossRefGoogle Scholar
  136. Yoshii H, Imaseki H (1982) Regulation of auxin-induced ethylene biosynthesis: repression of inductive formation of 1-Aminocyclopropane-1-carboxylate synthase by ethylene. Plant Cell Physiol 23:639–649Google Scholar
  137. Yoshioka H, Sugie K, Park HJ et al (2001) Induction of plant gp91 phox homolog by fungal cell wall, arachidonic acid, and salicylic acid in potato. Mol Plant Microbe Interact 14:725–736PubMedCrossRefGoogle Scholar
  138. Zhang YY, Zhu HY, Zhang Q et al (2009) Phospholipase Dα1 and phosphatidic acid regulate NADPH oxidase activity and production of reactive oxygen species in ABA-mediated stomatal closure in Arabidopsis. Plant Cell 21:2357–2377PubMedPubMedCentralCrossRefGoogle Scholar
  139. Zhang DJ, Xia RX, Cao X, Shu B, Chen CL (2013) Root hair development of Poncirus trifoliata grown in different growth cultures and treated with 3-indolebutyric acid and ethephon. Scientia Horticulturae 160:389–397CrossRefGoogle Scholar
  140. Zhang D, Xia R, Cao X (2016) Ethylene modulates root hair development in trifoliate orange through auxin-signaling pathway. Scientia Horticulturae 213:252–259CrossRefGoogle Scholar
  141. Zhao Y, Christensen SK, Fankhauser C, Cashman JR, Cohen JD, Weigel D et al (2001) A role for flavin monooxygenase-like enzymes in auxin biosynthesis. Science 291:306–309PubMedCrossRefGoogle Scholar
  142. Zheng Y, Zhu Z (2016) Relaying the ethylene signal: new roles for EIN2. Trends Plant Sci 21:2–4PubMedCrossRefGoogle Scholar
  143. Zhu J, Kaeppler SM, Lynch JP (2005) Mapping of QTL controlling root hair length in maize (Zea mays L.) under phosphorus deficiency. Plant Soil 270:299–310CrossRefGoogle Scholar
  144. Zhu C, Gan L, Shen Z, Xia K (2006) Interactions between jasmonates and ethylene in the regulation of root hair development in Arabidopsis. J Exp Bot 57:1299–1308PubMedCrossRefGoogle Scholar
  145. Zhu Y, Rong L, Luo Q et al (2017) The histone chaperone NRP1 interacts with WEREWOLF to activate GLABRA2 in Arabidopsis root hair development. Plant Cell 29:260–276PubMedPubMedCentralCrossRefGoogle Scholar
  146. Zou YN, Wang P, Liu CY, Ni QD, Zhang DJ, Wu QS (2017) Mycorrhizal trifoliate orange has greater root adaptation of morphology and phytohormones in response to drought stress. Sci Rep 7:41134PubMedPubMedCentralCrossRefGoogle Scholar
  147. Zuchi S, Cesco S, Gottardi S, Pinton R, Römheld V, Astolfi S (2011) The root-hairless barley mutant brb used as model for assessment of role of root hairs in iron accumulation. Plant Physiol Biochem 49:506–512PubMedCrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • De-Jian Zhang
    • 1
    • 2
  • Yu-Jie Yang
    • 1
    • 2
  • Chun-Yan Liu
    • 1
    • 2
  • Fei Zhang
    • 1
    • 2
  • Qiang-Sheng Wu
    • 1
    • 2
  1. 1.College of Horticulture and GardeningYangtze UniversityJingzhouChina
  2. 2.Institute of Root BiologyYangtze UniversityJingzhouChina

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