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Planta

, 225:451 | Cite as

Actin is bundled in activation-tagged tobacco mutants that tolerate aluminum

  • Abdul Ahad
  • Peter Nick
Original Article

Abstract

A panel of aluminum-tolerant (AlRes) mutants was isolated by protoplast-based T-DNA activation tagging in the tobacco cultivar SR1. The mutants fell into two phenotypic classes: a minority of the mutants were fertile and developed similarly to the wild type (type I), the majority was male-sterile and grew as semi-dwarfs (type II). These traits, along with the aluminum tolerance, were inherited in a monogenic dominant manner. Both types of mutants were characterized by excessive bundling of actin microfilaments and by a strongly increased abundance of actin, a phenotype that could be partially phenocopied in the wild type by treatment with aluminum chloride. The actin bundles could be dissociated into finer strands by addition of exogenous auxin in both types of mutants. However, actin microfilaments and leaf expansion were sensitive to blockers of actin assembly in the wild type and in the mutants of type I, whereas they were more tolerant in the mutants of type II. The mutants of type II displayed a hypertrophic development of vasculature, manifest in form of supernumerary leaf veins and extended xylem layers in stems and petioles. Whereas mutants of type I were characterized by a normal, but aluminum-tolerant polar auxin-transport, auxin-transport was strongly promoted in the mutants of type II. The phenotype of these mutants is discussed in terms of reduced endocytosis leading, concomitantly with aluminum tolerance, to changes in polar auxin transport.

Keywords

Actin microfilaments Activation tagging Aluminum tolerance Auxin transport male sterility tobacco (Nicotiana tabacum L.) 

Abbreviations

Al

Aluminum

AlRes

Aluminum tolerance

MS

Murashige and Skoog medium

Notes

Acknowledgments

This work was supported by a Volkswagen-Foundation Young Researcher Group Grant (Nachwuchsgruppe) to PN.

References

  1. Ahad A, Wolf J, Nick P (2003) Isolation of tobacco mutants with increased tolerance to low temperature and anticytoskeletal herbicides by activation tagging. Trans Res 12:615–629CrossRefGoogle Scholar
  2. Bennet RJ, Breen CM (1991) The aluminum signal: new dimensions to mechanisms of aluminum tolerance. Plant Soil 134:153–166Google Scholar
  3. Bennett MJ, Marchant A, Green HG, May ST, Ward SP, Millner PA, Walker AR, Schulz B, Feldmann KA (1996) Arabidopsis AUX1 gene: a permease-like regulator of root gravitropism. Science 273:948–950PubMedCrossRefGoogle Scholar
  4. Blancaflor EB, Jones DL, Gilroy S (1998) Alteration in the cytoskeleton accompany aluminum-induced growth inhibition and morphological changes in primary roots of maize. Plant Physiol 118:159–172PubMedCrossRefGoogle Scholar
  5. Breitling F, Little M (1986) Carboxy-terminal regions on the surface of tubulin and microtubules. Epitope Locations of YOL1/34, DM1A and DM1B. J Mol Biol 189:367–370PubMedCrossRefGoogle Scholar
  6. Chang C, Kwok SF, Bleecker AB, Myerowitz EM (1993) Arabidopsis ethylene/response gene ETR1: similarity of product to two-component regulators. Science 262:539–544PubMedCrossRefGoogle Scholar
  7. Chenery EM, Sporne KR (1976). A note on the evolutionary status of aluminum-accumulators among dicotyledons. New Phytol 76:551–554CrossRefGoogle Scholar
  8. Coué M, Brenner SL, Spector I, Korn ED (1987) Inhibition of actin polymerization by latrunculin A. FEBS Lett 213:316–318PubMedCrossRefGoogle Scholar
  9. De la Fuente JM, Ramirez-Rodriguez V, Carbera-Ponce JL, Herrera-Estrella L (1997) Aluminum tolerance in transgenic plants by alteration of citrate synthesis. Science 276:1566–1568CrossRefGoogle Scholar
  10. Delhaize E, Ryan PR (1995) Aluminum toxicity and tolerance in plants. Plant Physiol 107:315–321PubMedGoogle Scholar
  11. Delhaize E, Hebb DM, Ryan PR (2001) Expression of a pseudomonas aeruginosa citrate synthase gene in tobacco is not associated with either enhanced citrate accumulation or efflux. Plant Physiol 125:2059–2067PubMedCrossRefGoogle Scholar
  12. Doncheva S, Amenós M, Poschenrieder C, Barceló J (2005) Root cell patterning: a primary target for aluminium toxicity in maize. J Exp Bot 56: 1213–1220PubMedCrossRefGoogle Scholar
  13. Foey CD, Chaney RL, White MS (1978) The physiology of metal toxicity in plants. Annu Rev Plant Physiol 29:511–566CrossRefGoogle Scholar
  14. Friml J (2003) Auxin transport—shaping the plant. Curr Opin Plant Biol 6:7–12PubMedCrossRefGoogle Scholar
  15. Frantzios G, Galatis B, Apostolakos P (2005) Aluminium causes variable responses in actin filament cytoskeleton of the root tip cells of Triticum turgidum. Protoplasma 225:129–140PubMedCrossRefGoogle Scholar
  16. Geisler M, Blakeslee JJ, Bouchard R, Lee OR, Vincenzetti V, Bandyopadhyay A, Titapiwatanakun B, Peer WA, Bailly AI, Richards EL, Ejendal KFK, Smith AP, Baroux C, Grossniklaus U, Müller A, Hrycyna CA, Dudler R, Murphy AS, Martinoia E (2005) Cellular efflux of auxin catalyzed by the Arabidopsis MDR/PGP transporter AtPGP1. Plant J 44:179–194PubMedCrossRefGoogle Scholar
  17. Geldner N, Friml J, Stierhof YD, Jürgens G, Palme K (2001) Auxin transport inhibitors block PIN1 cycling and vesicle trafficking. Nature 413:425–428PubMedCrossRefGoogle Scholar
  18. Geldner N, Richter S, Vieten A, Marquardt S, Torres-Ruiz RA, Mayer U, Jürgens G (2003) Partial loss of function alleses reveal a role for GNOM in auxin transport-related, post-embryonic development of Arabidopsis. Development 131:380–400CrossRefGoogle Scholar
  19. Godbolé R, Michalke W, Nick P, Hertel R (2000) Cytoskeletal drugs and gravity-induced lateral auxin transport in rice coleoptiles. Plant Biol 2:176–181CrossRefGoogle Scholar
  20. Grabski S, Schindler M (1995) Aluminum induces rigor within the actin network of soybean cells. Plant Physiol 108:897–901PubMedGoogle Scholar
  21. Hasenstein KH, Evans ML (1988) Effects of cations on hormone transport in primary roots of Zea mays. Plant Physiol 86:890–894PubMedCrossRefGoogle Scholar
  22. Hayashi H, Czaja I, Schell J, Walden R (1992) Activation of plant gene by T-DNA tagging: Auxin independent growth in vitro. Science 258:1350–1353PubMedCrossRefGoogle Scholar
  23. Holweg C, Nick P (2004) Arabidopsis myosin XI mutant is defective in organelle movement and polar auxin transport. Proc Natl Acad Sci USA 101:10488–10493PubMedCrossRefGoogle Scholar
  24. Holweg C, Süßlin C, Nick P (2004) Capturing in-vivo dynamics of the actin cytoskeleton stimulated by auxin or light. Plant Cell Physiol 45:855–863PubMedCrossRefGoogle Scholar
  25. Kakimoto T (1996) CKI1, a histidine kinase homologue implicated in cytokinin signal transduction. Science 274:982–985PubMedCrossRefGoogle Scholar
  26. Kerven GL, Edwards DG, Asher CJ, Hallman PS, Kokot S (1989) Aluminum determination in soil solution. II. Short term calorimetric procedures for the measurement of inorganic monomeric aluminium in the presence of organic acid ligands. Austr J Soil Res 27:91–102CrossRefGoogle Scholar
  27. Kochian LV, Hoekenga OA, Piñeros MA (2005) How do crop plants tolerate acid soil? Mechanisms of aluminum tolerance and phosphorus efficiency. Annu Rev Plant Biol 55:459–493CrossRefGoogle Scholar
  28. Kollmeier M, Hubert HF, Horst JW (2000) Genotypical differences in aluminum resistance of maize are expressed in the distal part of the transition zone. Is reduced basipetal auxin flow involved in inhibition of root elongation by aluminum? Plant Physiol 122:945–956PubMedCrossRefGoogle Scholar
  29. Koncz C, Mayerhofer R, Konct-Kalman Z, Nawrath C, Reiss B, Redei GP, Schell J (1990) Isolation of a gene encoding a novel chloroplast protein by T-DNA tagging in Arabidopsis thaliana. EMBO J 9:1337–1346PubMedGoogle Scholar
  30. Koncz C, Martini N, Szabados L, Hrouda M, Bachmair A, Schell J (1994) Specialized vectors for gene tagging and expression studies. In: Gelvin SB, Schilperoort RA, Verma DPS (eds) Plant molecular biology manual, vol B2. Kluwer Academic Publishers, Netherlands, pp 1–22Google Scholar
  31. Koop H-U, Steinmüller K, Wagner H, Rössler C, Eibil C, Sacher L (1996) Integration of foreign sequences into the tobacco plastome via polyethylene glycol-mediated protoplast transformation. Planta 199:193–201PubMedCrossRefGoogle Scholar
  32. MacDonald TL, Martin RB (1988) Aluminum ion in biological systems. Trends Biochem Sci 13:15–19 PubMedCrossRefGoogle Scholar
  33. Mattson J, Sung ZR, Berleth T (1999) Responses of plant vascular systems to auxin transport inhibition. Development 126:2979–2991Google Scholar
  34. Murashige T, Skoog F (1962) A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol Plant 15:473–497CrossRefGoogle Scholar
  35. Nakazawa M, Ichikawa T, Ishikawa A, Kobayashi H, Tsuhara Y, Kawashima M, Suzuki K, Muto S, Mastui M (2003) Activation tagging, a novel tool to dissect the functions of a gene family. Plant J 34:741–750PubMedCrossRefGoogle Scholar
  36. Nick P. (2006) Noise yields order: auxin, actin, and polar patterning. Plant Biol 8:360–370PubMedCrossRefGoogle Scholar
  37. Nick P, Lambert AM, Vantard M (1995) A microtubules-associated protein in maize is induced during phytochrome-dependent cell elongation. Plant J 8:835–844PubMedGoogle Scholar
  38. Nick P, Heuing A, Ehmann B (2000) Plant chaperonins: a role in microtubule-dependent wall formation. Protoplasma 211:234–244CrossRefGoogle Scholar
  39. Popov N, Schmitt S, Matthices H (1975) Eine störungsfreie Mikromethode zur Bestimmung des Proteingehalts in Gewebshomogenaten. Acta Biol Ger 31:1441–1446Google Scholar
  40. Piñeros MA, Shaff JE; Manslank HS, Alves VM, Kochian LV (2005) Aluminum resistance in maize cannot solely explained by root organic acid exudation. A comparative physiological study. Plant Physiol 137:231–241PubMedCrossRefGoogle Scholar
  41. Rengel Z, Zhang W-H (2003) Role of dynamics of intracellular calcium in aluminium-toxicity syndrome. New Phytol 159:295–314CrossRefGoogle Scholar
  42. Ryan PR, Delhaize E, Randall PJ (1995) Malate efflux from root apices and tolerance to Al are highly correlated in wheat. Austr J Plant Physiol 22:531–536CrossRefGoogle Scholar
  43. Sachs T (2000) Integrating cellular and organismic aspects of vascular differentiation. Plant Cell Physiol 41:649–656PubMedGoogle Scholar
  44. Sasaki T, Yamamoto Y, Ezaki B, Katsuhara M, Ahn SJ, Ryan PR, Delhaize E, Matsumoto H (2004) A wheat gene encoding an aluminum activated malate transporter. Plant J 37:645–653PubMedCrossRefGoogle Scholar
  45. Schmidt R, Bohm K, Vater W, Unger E (1991) Aluminum-induced osteomalacia and encelopathy: an aberration of the tubulin assembly into microtubules by Al3+. Prog Histochem Cytochem 23:355–364PubMedGoogle Scholar
  46. Schwarzerová K, Zelenková S, Nick P, Opartrný Z (2002) Aluminum induced rapid changes in the microtubular cytoskeleton of tobacco cell lines. Plant Cell Physiol 43:207–216PubMedCrossRefGoogle Scholar
  47. Sivaguru M, Matsumoto H, Horst WJ (2000) Control of the response to aluminium stress. In: Nick P (ed) Plant microtubules—potential for biotechnology, Springer, Berlin Heidelberg New York , pp 103–120Google Scholar
  48. Sivaguru M, Ezaki B, He Zh-H, Tong H, Osawa H, Baluška F, Volkmann D, Matsumoto H (2003a) Aluminum-induced gene expression and protein localization of a cell wall-associated receptor kinase in Arabidopsis. Plant Physiol 132:2256–2266CrossRefGoogle Scholar
  49. Sivaguru M, Pike S, Gassmann W, Baskin TI (2003b) Aluminum rapidly depolymerizes cortical microtubules and depolarizes the plasma membrane: evidence that these responses are mediated by a glutamate receptor. Plant Cell Physiol 44:667–675CrossRefGoogle Scholar
  50. Steinmann T, Geldner N, Grebe M, Mangold S, Jackson CL, Paris S, Galweiler L, Palme K, Jurgens G (1999) Coordinated polar localization of auxin efflux carrier PIN1 by GNOM ARF GEF. Science 286:316–318PubMedCrossRefGoogle Scholar
  51. Strzelecka-Golaszewska H (2001) Divalent cations, nucleotides, and actin structure. Res Probl Cell Differ 32:23–41Google Scholar
  52. Swarup R, Friml J, Marchant A, Ljung K, Sandberg G, Palme K, Bennett M (2001) Localization of the auxin permease AUX1 suggests two functionally distinct hormone transport pathways operate in the Arabidopsis root apex. Genes Dev 15:2648–2653PubMedCrossRefGoogle Scholar
  53. Tani H, Chen X, Nurmberg P, Grant JJ, SantaMaria M, Chini A, Gilroy E, Birch PRJ, Loake GJ (2004) Activation tagging in plants: a tool for gene discovery. Funct Integr Genomics 0:1–9Google Scholar
  54. Vitorello VA, Haug A (1999) Capacity for aluminium uptake depends on brefeldin A-sensitive membrane traffic in tobacco (Nicotiana tabacum L. cv. BY-2) cells. Plant Cell Rep 18:733–736CrossRefGoogle Scholar
  55. Wagatsuma T, Kaneko M, Hayasaka Y (1995) Destruction process of plant root cells by aluminium. Soil Sci Plant Nutr 33:161–175Google Scholar
  56. Waller F, Nick P (1997) Response of actin microfilaments during phytochrome-controlled growth of maize seedlings. Protoplasma 200:154–162CrossRefGoogle Scholar
  57. Waller F, Riemann M, Nick P (2002) A role for actin-driven secretion in auxin-induced growth. Protoplasma 219:72–81PubMedCrossRefGoogle Scholar
  58. Watt DA (2003) Aluminium-responsive genes in sugarcane: identification and analysis of expression under oxidative stress. J Exp Bot 54:1163–1174PubMedCrossRefGoogle Scholar
  59. Weigel D, Ahn JH, Blazquez MA et al (2000) Activation tagging in Arabidopsis. Plant Physiol 122:1003–1013PubMedCrossRefGoogle Scholar
  60. Xia Y, Suzuki H, Borevitz J, Blount J, Guo Z, Patel K, Dixon RA, Lamb C (2004) An extracellular aspartic protease functions in Arabidopsis disease resistance signaling. EMBO J 23:980–988PubMedCrossRefGoogle Scholar
  61. Yang JL, Zheng SJ, He YF, Matsumoto H (2005) Aluminum resistance requires resistance to acid stress: a case study with spinach that exudes oxlate rapidly when exposed to Al stress. J Exp Bot 56:1197–1203PubMedCrossRefGoogle Scholar
  62. Zubko E, Adams CJ, Machaelkova I, Malbeck J, Scollan C, Meyer P (2002) Activation tagging identifies a gene from Petunia hybrida responsible for the production of active cytokinins in plants. Plant J 29:797–808PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2006

Authors and Affiliations

  1. 1.Umeå Plant Science Centre, Department of Plant PhysiologyUmeå UniversityUmeåSweden
  2. 2.Botanisches Institut 1University of KarlsruheKarlsruheGermany

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