Advertisement

Journal of Plant Research

, Volume 131, Issue 3, pp 543–554 | Cite as

Effects of glucose and ethylene on root hair initiation and elongation in lettuce (Lactuca sativa L.) seedlings

  • Wakana Harigaya
  • Hidenori Takahashi
Regular Paper

Abstract

Root hair formation occurs in lettuce seedlings after transfer to an acidic medium (pH 4.0). This process requires cortical microtubule (CMT) randomization in root epidermal cells and the plant hormone ethylene. We investigated the interaction between ethylene and glucose, a new signaling molecule in plants, in lettuce root development, with an emphasis on root hair formation. Dark-grown seedlings were used to exclude the effect of photosynthetically produced glucose. In the dark, neither root hair formation nor the CMT randomization preceding it occurred, even after transfer to the acidic medium (pH 4.0). Adding 1-aminocyclopropane-1-carboxylic-acid (ACC) to the medium rescued the induction, while adding glucose did not. Although CMT randomization occurred when glucose was applied together with ACC, it was somewhat suppressed compared to that in ACC-treated seedlings. This was not due to a decrease in the speed of randomization, but due to lowering of the maximum degree of randomization. Despite the negative effect of glucose on ACC-induced CMT randomization, the density and length of ACC-induced root hairs increased when glucose was also added. The hair-cell length of the ACC-treated seedlings was comparable to that in the combined-treatment seedlings, indicating that the increase in hair density caused by glucose results from an increase in the root hair number. Furthermore, quantitative RT-PCR revealed that glucose suppressed ethylene signaling. These results suggest that glucose has a negative and positive effect on the earlier and later stages of root hair formation, respectively, and that the promotion of the initiation and elongation of root hairs by glucose may be mediated in an ethylene-independent manner.

Keywords

Cortical microtubule Ethylene Glucose Lettuce (Lactuca sativa L.) Root hair 

Notes

Acknowledgements

We thank Prof. Y. Inoue in Tokyo University of Science for providing lettuce seeds.

References

  1. Balasubramanian R, Karve A, Kandasamy M, Meagher RB, Moore B (2007) A role for F-actin in hexokinase-mediated glucose signaling. Plant Physiol 145:1423–1434CrossRefPubMedPubMedCentralGoogle Scholar
  2. Baluška F, Salaj J, Mathur J, Braun M, Jasper F, Šamaj J, Chua NH, Barlow PW, Volkmann D (2000) Root hair formation: F-actin-dependent tip growth is initiated by local assembly of profilin-supported F-actin meshworks accumulated within expansin-enriched bulges. Dev Biol 227:618–632CrossRefPubMedGoogle Scholar
  3. Bao Y, Kost B, Chua NH (2001) Reduced expression of α-tubulin genes in Arabidopsis thaliana specifically affects root growth and morphology, root hair development and root gravitropism. Plant J 28:145–157CrossRefPubMedGoogle Scholar
  4. Berger F, Haseloff J, Schiefelbein J, Dolan L (1998) Positional information in root epidermis is defined during mbryogenesis and acts in domains with strict boundaries. Curr Biol 8:421–430CrossRefPubMedGoogle Scholar
  5. Bibikova TN, Blancaflor EB, Gilroy S (1999) Microtubules regulate tip growth and orientation in root hairs of Arabidopsis thaliana. Plant J 17:657–665CrossRefPubMedGoogle Scholar
  6. Chao Q, Rothenberg M, Solano R, Roman G, Terzaghi W, Ecker JR (1997) Activation of the ethylene gas response pathway in Arabidopsis by the nuclear protein ETHYLENE-INSENSITIVE3 and related proteins. Cell 89:1133–1144CrossRefPubMedGoogle Scholar
  7. Cheng WH, Endo A, Zhou L, Penney J, Chen HC, Arroyo A, Leon P, Nambara E, Asami T, Seo M, Koshiba T, Sheen J (2002) A unique short-chain dehydrogenase/reductase in Arabidopsis glucose signaling and abscisic acid biosynthesis and functions. Plant Cell 14:2723–2743CrossRefPubMedPubMedCentralGoogle Scholar
  8. Clarkson DT (1985) Factors affecting mineral nutrient acquisition by plants. Annu Rev Plant Physiol 36:77–115CrossRefGoogle Scholar
  9. Collings DA, Lill AW, Himmelspach R, Wasteneys GO (2006) Hypersensitivity to cytoskeletal antagonists demonstrates microtubule-microfilament cross-talk in the control of root elongation in Arabidopsis thaliana. New Phytol 170:275–290CrossRefPubMedGoogle Scholar
  10. De Simone S, Oka Y, Nishioke N, Tadano S, Inoue Y (2000) Evidence of phytochrome mediation in the low-pH-induced root hair formation process in lettuce (Lactuca sativa L. cv. Grand Rapids) seedlings. J Plant Res 113:45–53CrossRefGoogle Scholar
  11. Dolan L, Duckett CM, Grierson C, Linstead P, Schneider K, Lawson E, Dean C, Roberts K, Poethig S (1994) Clonal relationships and cell patterning in the root epidermis of Arabidopsis. Development 120:2465–2474Google Scholar
  12. Emons AMC, Derksen J (1986) Microfibrils, microtubules and microfilaments of the trichoblast of Equisetum hyemale. Acta Bot Neerl 35:311–320CrossRefGoogle Scholar
  13. Favery B, Ryan E, Foreman J, Linstead P, Boudonck K, Steer M, Shaw P, Dolan L (2001) KOJAK encodes a cellulose synthase-like protein required for root hair cell morphogenesis in Arabidopsis. Genes Dev 15:79–89CrossRefPubMedPubMedCentralGoogle Scholar
  14. Fu Y, Li H, Yang Z (2002) The ROP2 GTPase controls the formation of cortical fine F-actin and the early phase of directional cell expansion during Arabidopsis organogenesis. Plant Cell 14:777–794CrossRefPubMedPubMedCentralGoogle Scholar
  15. Gális I, Šimek P, Van Onckelen HA, Kakiuchi Y, Wabiko H (2002) Resistance of transgenic tobacco seedlings expressing the Agrobacterium tumefaciens C58-6b gene, to growth-inhibitory levels of cytokinin is associated with elevated IAA levels and activation of phenylpropanoid metabolism. Plant Cell Physiol 43:939–950CrossRefPubMedGoogle Scholar
  16. Gancedo JM (2008) Early steps of glucose signalling in yeast. FEMS Microbiol Rev 32:673–704CrossRefPubMedGoogle Scholar
  17. Gazzarrini S, McCourt P (2001) Genetic interactions between ABA, ethylene and sugar signaling pathways. Curr Opin Plant Biol 4:387–391CrossRefPubMedGoogle Scholar
  18. Gibson SI (2004) Sugar and phytohormone response pathways: navigating a signalling network. J Exp Bot 55:253–264CrossRefPubMedGoogle Scholar
  19. Gibson SI, Laby RJ, Kim D (2001) The sugar-insensitive1 (sis1) mutant of Arabidopsis is allelic to ctr1. Biochem Biophys Res Commun 280:196–203CrossRefPubMedGoogle Scholar
  20. Gu Y, Wang Z, Yang Z (2004) ROP/RAC GTPase: an old new master regulator for plant signaling. Curr Opin Plant Biol 7:527–536CrossRefPubMedGoogle Scholar
  21. Guo H, Ecker JR (2003) Plant responses to ethylene gas are mediated by SCFEBF1/EBF2-dependent proteolysis of EIN3 transcription factor. Cell 115:667–677CrossRefPubMedGoogle Scholar
  22. Hong JH, Cowan AK, Lee SK (2004) Glucose inhibits ACC oxidase activity and ethylene biosynthesis in ripening tomato fruit. Plant Growth Regul 43:81–87CrossRefGoogle Scholar
  23. Honkanen S, Dolan L (2016) Growth regulation in tip-growing cells that develop on the epidermis. Curr Opin Plant Biol 34:77–83CrossRefPubMedGoogle Scholar
  24. Inoue Y, Hirota K (2000) Low pH-induced root hair formation in lettuce (Lactuca sativa L. cv. Grand Rapids) seedlings: determination of root hair-forming site. J Plant Res 113:245–251CrossRefGoogle Scholar
  25. Inoue Y, Yamaoka K, Kimura K, Sawai K (1995) Image processing-aided simple analysis method for root hair formation in plants. Bioimages 3:31–36Google Scholar
  26. Inoue Y, Yamaoka K, Kimura K, Sawai K, Arai T (2000) Effect of low pH on the induction of root hair formation in young lettuce (Lactuca sativa L. cv. Grand Rapids) seedlings. J Plant Res 113:39–44CrossRefGoogle Scholar
  27. Ishida T, Kurata T, Okada K, Wada T (2008) A genetic regulatory network in the development of trichomes and root hairs. Ann Rev Plant Bio 59:365–386CrossRefGoogle Scholar
  28. Jones MA, Shen JJ, Fu Y, Li H, Yang Z, Grierson CS (2002) The Arabidopsis Rop2 GTPase is a positive regulator of both root hair initiation and tip growth. Plant Cell 14:763–776CrossRefPubMedPubMedCentralGoogle Scholar
  29. Ju C, Chang C (2015) Mechanistic insights in ethylene perception and signal transduction. Plant Physiol 169:85–95CrossRefPubMedPubMedCentralGoogle Scholar
  30. Karve A, Moore BD (2009) Function of Arabidopsis hexokinase-like1 as a negative regulator of plant growth. J Exp Bot 60:4137–4149CrossRefPubMedPubMedCentralGoogle Scholar
  31. Karve A, Xia X, Moore BD (2012) Arabidopsis Hexokinase-Like1 and Hexokinase1 form a critical node in mediating plant glucose and ethylene responses. Plant Physiol 158:1965–1975CrossRefPubMedPubMedCentralGoogle Scholar
  32. Kende H (1993) Ethylene biosynthesis. Annu Rev Plant Physiol Plant Mol Biol 44:283–307CrossRefGoogle Scholar
  33. Kieber JJ (1997) The ethylene response pathway in Arabidopsis. Annu Rev Plant Physiol Plant Mol Biol 48:277–296CrossRefPubMedGoogle Scholar
  34. Kim CM, Park SH, Je BI, Park SJ, Piao HL, Eun MY, Dolan L, Han CD (2007) OsCSLD1, a cellulose synthase-like D1 gene, is required for root hair morphogenesis in rice. Plant Physiol 143:1220–1230CrossRefPubMedPubMedCentralGoogle Scholar
  35. León P, Sheen J (2003) Sugar and hormone connections. Trends Plant Sci 8:110–116CrossRefPubMedGoogle Scholar
  36. Leyser HM, Pickett FB, Dharmasiri S, Estelle M (1996) Mutations in the AXR3 gene of Arabidopsis result in altered auxin response including ectopic expression from the SAUR-AC1 promoter. Plant J 10:403–413CrossRefPubMedGoogle Scholar
  37. Li Y, Lee KK, Walsh S, Smith C, Hadingham S, Sorefan K, Cawley G, Bevan MW (2006) Establishing glucose- and ABA-regulated transcription networks in Arabidopsis by microarray analysis and promoter classification using a relevance vector machine. Genome Res 16:414–427CrossRefPubMedPubMedCentralGoogle Scholar
  38. Libault M, Brechenmacher L, Cheng J, Xu D, Stacey G (2010) Root hair systems biology. Trends Plant Sci 15:641–650CrossRefPubMedGoogle Scholar
  39. Lincoln C, Britton JH, Estelle M (1990) Growth and development of the axr1 mutants of Arabidopsis. Plant Cell 2:1071–1080CrossRefPubMedPubMedCentralGoogle Scholar
  40. Masucci JD, Schiefelbein JW (1994) The rhd6 mutation of Arabidopsis thaliana alters root-hair initiation through an auxin- and ethylene-associated process. Plant Physiol 106:1335–1346CrossRefPubMedPubMedCentralGoogle Scholar
  41. 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 8:1505–1517CrossRefPubMedPubMedCentralGoogle Scholar
  42. McFarlane HE, Döring A, Persson S (2014) The cell biology of cellulose synthesis. Annu Rev Plant Biol 65:69–94CrossRefPubMedGoogle Scholar
  43. Mishra BS, Singh M, Aggrawal P, Laxmi A (2009) Glucose and auxin signaling interaction in controlling Arabidopsis thaliana seedlings root growth and development. PLoS One 4:e4502CrossRefPubMedPubMedCentralGoogle Scholar
  44. Molendijk AJ, Bischoff F, Rajendrakumar CS, Friml J, Braun M, Gilroy S, Palme K (2001) Arabidopsis thaliana Rop GTPases are localized to tips of root hairs and control polar growth. EMBO J 20:2779–2788CrossRefPubMedPubMedCentralGoogle Scholar
  45. Moore B, Zhou L, Rolland F, Hall Q, Cheng WH, Liu YX, Hwang I, Jones T, Sheen J (2003) Role of the Arabidopsis glucose sensor HXK1 in nutrient, light, and hormonal signaling. Science 300:332–336CrossRefPubMedGoogle Scholar
  46. Narukawa M, Watanabe K, Inoue Y (2010) Light-induced root hair formation in lettuce (Lactuca sativa L. cv. Grand Rapids) roots at low pH is brought by chlorogenic acid synthesis and sugar. J Plant Res 123:789–799CrossRefPubMedGoogle Scholar
  47. Peterson RL, Farquhar ML (1996) Root hairs: Specialized tubular cells extending root surfaces. Bot Rev 62:1–40CrossRefGoogle Scholar
  48. Pietra S, Lang P, Grebe M (2015) SABRE is required for stabilization of root hair patterning in Arabidopsis thaliana. Physiol Plant 153:440–453CrossRefPubMedGoogle Scholar
  49. Pitts RJ, Cernac A, Estelle M (1998) Auxin and ethylene promote root hair elongation in Arabidopsis. Plant J 16:553–560CrossRefPubMedGoogle Scholar
  50. Price J, Laxmi A, St Martin SK, Jang JC (2004) Global transcription profiling reveals multiple sugar signal transduction mechanisms in Arabidopsis. Plant Cell 16:2128–2150CrossRefPubMedPubMedCentralGoogle Scholar
  51. 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 130:1908–1917CrossRefPubMedPubMedCentralGoogle Scholar
  52. Rolland F, Baena-Gonzalez E, Sheen J (2006) Sugar sensing and signaling in plants: conserved and novel mechanisms. Annu Rev Plant Biol 57:675–709CrossRefPubMedGoogle Scholar
  53. Rowe JH, Topping JF, Liu J, Lindsey K (2016) Abscisic acid regulates root growth under osmotic stress conditions via an interacting hormonal network with cytokinin, ethylene and auxin. New Phytol 211:225–239CrossRefPubMedPubMedCentralGoogle Scholar
  54. Salazar-Henao JE, Vélez-Bermúdez IC, Schmidt W (2016) The regulation and plasticity of root hair patterning and morphogenesis. Development 143:1848–1858CrossRefPubMedGoogle Scholar
  55. Schaefer AW, Kabir N, Forscher P (2002) Filopodia and actin arcs guide the assembly and transport of two populations of microtubules with unique dynamic parameters in neuronal growth cones. J Cell Biol 158:139–152CrossRefPubMedPubMedCentralGoogle Scholar
  56. Sheen J (2014) Master regulators in plant glucose signaling networks. J Plant Biol 57:67–79CrossRefPubMedPubMedCentralGoogle Scholar
  57. Smeekens S, Ma J, Hanson J, Rolland F (2010) Sugar signals and molecular networks controlling plant growth. Curr Opin Plant Biol 13:274–279CrossRefPubMedGoogle Scholar
  58. Song SH, Vieille C (2009) Recent advances in the biological production of mannitol. Appl Microbiol Biotechnol 84:55–62CrossRefPubMedGoogle Scholar
  59. Stonier T, Macgladrie K, Shaw G (1979) Studies on auxin protectors XIV. Chlorogenic acid, a low molecular weight auxin protector in sunflower. Plant Cell Environ 2:79–82CrossRefGoogle Scholar
  60. Sulmon C, Gouesbet G, El Amrani A, Couée I (2007) Involvement of the ethylene-signalling pathway in sugar-induced tolerance to the herbicide atrazine in Arabidopsis thaliana seedlings. J Plant Physiol 164:1083–1092CrossRefPubMedGoogle Scholar
  61. Swarup R, Perry P, Hagenbeek D, Van Der Straeten D, Beemster GTS, Sandberg G, Bhalerao R, Ljung K, Bennett MJ (2007) Ethylene upregulates auxin biosynthesis in Arabidopsis seedlings to enhance inhibition of root cell elongation. Plant Cell 19:2186–2196CrossRefPubMedPubMedCentralGoogle Scholar
  62. Takahashi H, Inoue Y (2008) Stage-specific crosstalk between light, auxin, and ethylene during low-pH-induced root hair formation in lettuce (Lactuca sativa L.) seedlings. Plant Growth Regul 56:31–41CrossRefGoogle Scholar
  63. Takahashi H, Hirota K, Kawahara A, Hayakawa E, Inoue Y (2003a) Randomization of cortical microtubules in root epidermal cells induces root hair initiation in lettuce (Lactuca sativa L.) seedlings. Plant Cell Physiol 44:350–359CrossRefPubMedGoogle Scholar
  64. Takahashi H, Iwasa T, Shinkawa T, Kawahara A, Kurusu T, Inoue Y (2003b) Isolation and characterization of the ACC synthase genes from lettuce (Lactuca sativa L.), and the involvement in low pH-induced root hair initiation. Plant Cell Physiol 44:62–69CrossRefPubMedGoogle Scholar
  65. Takahashi H, Kawahara A, Inoue Y (2003c) 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 44:932–940CrossRefPubMedGoogle Scholar
  66. Tanimoto M, Roberts K, Dolan L (1995) Ethylene is a positive regulator of root hair development in Arabidopsis thaliana. Plant J 8:943–948CrossRefPubMedGoogle Scholar
  67. Timmers AC, Vallotton P, Heym C, Menzel D (2007) Microtubule dynamics in root hairs of Medicago truncatula. Eur J Cell Biol 86:69–83CrossRefPubMedGoogle Scholar
  68. Van Bruaene N, Joss G, Van Oostveldt P (2004) Reorganization and in vivo dynamics of microtubules during Arabidopsis root hair development. Plant Physiol 136:3905–3919CrossRefPubMedPubMedCentralGoogle Scholar
  69. Wang X, Cnops G, Vanderhaeghen R, De Block S, Van Montagu M, Van Lijsebettens M (2001) AtCSLD3, a cellulose synthase-like gene important for root hair growth in Arabidopsis. Plant Physiol 126:575–586CrossRefPubMedPubMedCentralGoogle Scholar
  70. Wilson AK, Pickett FB, Turner JC, Estelle M (1990) A dominant mutation in Arabidopsis confers resistance to auxin, ethylene and abscisic acid. Mol Gen Genet 222:377–383CrossRefPubMedGoogle Scholar
  71. Yanagisawa S, Yoo SD, Sheen J (2003) Differential regulation of EIN3 stability by glucose and ethylene signalling in plants. Nature 425:521–525CrossRefPubMedGoogle Scholar
  72. Yang SF, Hoffman NE (1984) Ethylene biosynthesis and its regulation in higher plants. Ann Rev Plant Physiol 35:155–189CrossRefGoogle Scholar
  73. Yuan K, Wysocka-Diller J (2006) Phytohormone signalling pathways interact with sugars during seed germination and seedling development. J Exp Bot 57:3359–3367CrossRefPubMedGoogle Scholar
  74. Zenk MH, Muller G (1963) In vivo destruction of exogenously applied indol-3-acetic acid as influenced by naturally occurring phenolic acids. Nature 200:761–763CrossRefGoogle Scholar
  75. Zhang S, Huang L, Yan A, Liu Y, Liu B, Yu C, Zhang A, Schiefelbein J, Gan Y (2016) Multiple phytohormones promote root hair elongation by regulating a similar set of genes in the root epidermis in Arabidopsis. J Exp Bot 67:6363–6372CrossRefPubMedPubMedCentralGoogle Scholar
  76. Zhou L, Jang JC, Jones TL, Sheen J (1998) Glucose and ethylene signal transduction crosstalk revealed by an Arabidopsis glucose-insensitive mutant. Proc Natl Acad Sci USA 95:10294–10299CrossRefPubMedGoogle Scholar

Copyright information

© The Botanical Society of Japan and Springer Japan KK, part of Springer Nature 2017

Authors and Affiliations

  1. 1.Department of Biology, Faculty of ScienceToho UniversityFunabashiJapan

Personalised recommendations