Narciclasine, a potential allelochemical, affects subcellular trafficking of auxin transporter proteins and actin cytoskeleton dynamics in Arabidopsis roots

Planta

Volumn 242, Issue 6, 2015, Pages 1349-1360

  Hu, Yanfeng ^a,b   Na, Xiaofan ^a   Li, Jiaolong ^a   Yang, Lijing ^a   You, Jia ^c   Liang, Xiaolei ^a   Wang, Jianfeng ^a   Peng, Liang ^a   Bi, Yurong ^a  

^a LANZHOU UNIVERSITY   (China)

^b NORTHEAST INSTITUTE OF GEOGRAPHY AND AGRICULTURAL ECOLOGY   (China)

^c NORTHWEST NORMAL UNIVERSITY   (China)

Author keywords

Actin cytoskeleton; Allelochemical; Auxin; Auxin transport

Indexed keywords

AMARYLLIDACEAE ALKALOID; ARABIDOPSIS PROTEIN; INDOLEACETIC ACID DERIVATIVE; NARCICLASINE; PHENANTHRIDINE DERIVATIVE;

ACTIN FILAMENT; ARABIDOPSIS; GENE EXPRESSION REGULATION; METABOLISM; PLANT ROOT; TRANSPORT AT THE CELLULAR LEVEL;

ACTIN CYTOSKELETON; AMARYLLIDACEAE ALKALOIDS; ARABIDOPSIS; ARABIDOPSIS PROTEINS; BIOLOGICAL TRANSPORT; GENE EXPRESSION REGULATION, PLANT; INDOLEACETIC ACIDS; PHENANTHRIDINES; PLANT ROOTS;

EID: 84944356605     PISSN: 00320935     EISSN: 14322048     Source Type: Journal    
DOI: 10.1007/s00425-015-2373-6     Document Type: Article

References (61)

1. Axelos M, Bardet C, Liboz T, Le Van Thai A, Curie C et al (1989) The gene family encoding the Arabidopsis thaliana translation elongation factor ef-1 alpha: molecular cloning, characterization and expression. Mol Gen Genet 219:106–112
2. Bais HP, Vepachedu R, Gilroy S, Callaway RM, Vivanco JM (2003) Allelopathy and exotic plant invasion: from molecules and genes to species interactions. Science 301:1377–1380
3. Bannigan A, Wiedemeier AM, Williamson RE, Overall RL, Baskin TI (2006) Cortical microtubule arrays lose uniform alignment between cells and are oryzalin resistant in the Arabidopsis mutant, radially swollen 6. Plant Cell Physiol 47:949–958
4. Bastida J, Lavilla R, Viladomat F (2006) Chemical and biological aspects of Narcissus alkaloids. Alkaloids Chem Biol 63:87–179
5. Benková E, Michniewicz M, Sauer M, Teichmann T, Seifertová D et al (2003) Local, efflux-dependent auxin gradients as a common module for plant organ formation. Cell 115:591–602
6. Berkov S, Bastida J, Sidjimova B, Viladomat F, Codina C (2008) Phytochemical differentiation of Galanthus nivalis and Galanthus elwesii (Amaryllidaceae): a case study. Biochem Syst Ecol 36:638–645
7. Bertin C, Yang XH, Weston LA (2003) The role of root exudates and allelochemicals in the rhizosphere. Plant Soil 256:67–83
8. Bi YR, Yung KH, Wong YH (1998) Physiological effects of narciclasine from the mucilage of Narcissus tazetta L. bulbs. Plant Sci 135:103–108
9. Bi YR, Zhang LX, Guo JK, Yung KH, Wong YS (2003) Narciclasine alters chloroplast membrane structure and inhibits 5-aminolevulinic acid and chlorophyll binding protein accumulation in wheat (Triticum aestivum) leaves. N Z J Crop Hortic Sci 31:335–343
10. Blakeslee JJ, Bandyopadhyay A, Lee OR, Mravec J, Titapiwatanakun B et al (2007) Interactions among PIN-FORMED and P-glycoprotein auxin transporters in Arabidopsis. Plant Cell 19:131–147
11. Blum U (2005) Relationships between phenolic acid concentrations, transpiration, water utilization, leaf area expansion, and uptake of phenolic acids: nutrient culture studies. J Chem Ecol 31:1907–1932
12. Bolte S, Talbot C, Boutte Y, CatriceO Read ND et al (2004) Fm-dyes as experimental probes for dissecting vesicle trafficking in living plant cells. J Microsc 214:159–173
13. Ceriotti G (1967) Narciclasine: an antimitotic substance from narcissus bulbs. Nature 213:595–596
14. Cutler SR, Ehrhardt DW, Griffitts JS, Somerville CR (2000) Random GFP:cDNA fusions enable visualization of subcellular structures in cells of Arabidopsis at a high frequency. Proc Nat Acad Sci USA 97:3718–3723
15. +-ATPase activity is required for endocytic and secretory trafficking in Arabidopsis. Plant Cell 18:715–730
16. Dhonukshe P, Aniento F, Hwang I, Robinson D, Mravec J et al (2007) Clathrin-mediated constitutive endocytosis of PIN auxin efflux carriers in Arabidopsis. Curr Biol 17:520–527
17. Dhonukshe P, Grigoriev I, Fischer R, Tominaga M, Robinson DG et al (2008a) Auxin transport inhibitors impair vesicle motility and actin cytoskeleton dynamics in diverse eukaryotes. Proc Nat Acad Sci USA 105:4489–4494
18. Dhonukshe P, Tanaka H, Goh T, Ebine K, Mähönen AP et al (2008b) Generation of cell polarity in plants links endocytosis, auxin distribution and cell fate decisions. Nature 456:962–966
19. Ding L, Qi L, Jing H, Li J, Wang W et al (2008) Phytotoxic effects of leukamenin E (an ent-kaurene diterpenoid) on root growth and root hair development in Lactuca sativa L. seedlings. J Chem Ecol 34:1492–1500
20. Essl D, Dirnberger D, Gomord V, Strasser R, Faye L et al (1999) The N-terminal 77 amino acids from tobacco N-acetylglucosaminyltransferase I are sufficient to retain a reporter protein in the Golgi apparatus of Nicotiana benthamiana cells. FEBS Lett 453:169–173
21. Friml J, Wiśniewska J, Benková E, Mendgen K, Palme K (2002) Lateral relocation of auxin efflux regulator PIN3 mediates tropism in Arabidopsis. Nature 415:806–809
22. Gabrielsen B, Monath TP, Huggins JW, Kefauver DF, Pettit GR et al (1992) Antiviral (RNA) activity of selected Amaryllidaceae isoquinoline constituents and synthesis of related substances. J Nat Prod 55:1569–1581
23. Geldner N, Friml J, Stierhof YD, Jürgens G, Palme K (2001) Auxin transport inhibitors block PIN1 cycling and vesicle trafficking. Nature 413:425–428
24. Geldner N, Anders N, Wolters H, Keicher J, Kornberger W et al (2003) The Arabidopsis GNOM ARF-GEF mediates endosomal recycling, auxin transport, and auxin-dependent plant growth. Cell 112:219–230
25. Geldner N, Hyman DL, Wang X, Schumacher K, Chory J (2007) Endosomal signaling of plant steroid receptor kinase BRI1. Genes Dev 21:1598–1602
26. Graña E, Sotelo T, Díaz-Tielas C, Araniti F, Krasuska U et al (2013) Citral inducesauxin and ethylene-mediated malformations and arrests cell division in Arabidopsis thaliana roots. J Chem Ecol 39:271–282
27. Grieneisen VA, Xu J, Marée AF, Hogeweg P, Scheres B (2007) Auxin transport is sufficient to generate a maximum and gradient guiding root growth. Nature 449:1008–1013
28. Horiuchi J, Badri DV, Kimball BA, Negre F, Dudareva N, Paschke MW, Vivanco JM (2007) The floral volatile, methyl benzoate, from snapdragon (Antirrhinummajus) triggers phytotoxic effects in Arabidopsisthaliana. Planta 226:1–10
29. Hu Y, Yang L, Na X, You J, Hu W et al (2012) Narciclasine inhibits the responses of Arabidopsis roots to auxin. Planta 236:597–612
30. Hu Y, Li J, Yang L, Nan W, Cao X et al (2014) Narciclasine inhibition of root growth is caused by DNA damage-induced cell cycle arrest in lettuce seedlings. Protoplasma 251:1113–1124
31. Hussey PJ, Ketelaar T, Deeks MJ (2006) Control of the actin cytoskeleton in plant cell growth. Annu Rev Plant Biol 57:109–125
32. Inderjit, Duke SO (2003) Ecophysiological aspect of allelopathy. Planta 217:529–539
33. Jaillais Y, Fobis-Loisy I, Miege C, Rollin C, Gaude T (2006) AtSNX1 defines an endosome for auxin-carrier trafficking in Arabidopsis. Nature 443:106–109
34. Kim H, Park M, Kim SJ, Hwang I (2005) Actin filaments play a critical role in vacuolar trafficking at the Golgi complex in plant cells. Plant Cell 17:888–902
35. Kleine-Vehn J, Dhonukshe P, Swarup R, Bennett M, Friml J (2006) Anovel pathway for subcellular trafficking of AUX1 auxin influx carrier. Plant Cell 18:3171–3181
36. Kleine-Vehn J, Dhonukshe P, Sauer M, Brewer P, Wiśniewska J et al (2008) ARF-GEF-dependent transcytosis mechanism for polar delivery of PIN auxin carriers in Arabidopsis. Curr Biol 18:526–531
37. Kornienko A, Evidente A (2008) Chemistry, biology, and medicinal potential of narciclasine and its congeners. Chem Rev 108:1982–2014
38. Kurup S, Runions J, Kohler U, Laplaze L, Hodge S et al (2005) Marking cell lineages in living tissues. Plant J 42:444–453
39. Lallemand S, Kaps M, Einhellig F (2009) Applied allelopathy: effects of Daffodils on other species in sustainable agriculture and the home landscape. Hortscience 44:1164
40. Lefranc F, Sauvage S, Van Goietsenoven G, Mégalizzi V, Lamoral-Theys D et al (2009) Narciclasine, a plant growth modulator, activates Rho and stress fibers in glioblastoma cells. Mol Cancer Ther 8:1739–1750
41. Mullin RD, Machesky LM (2000) Actin assembly mediated by Arp2/3 complex and WASP family proteins. Methods Enzymol 325:214–237
42. Na X, Hu Y, Yue K, Lu H, Jia P et al (2011a) Concentration-dependent effects of narciclasine on cell cycle progression in Arabidopsis root tips. BMC Plant Biol 11:184
43. Na X, Hu Y, Yue K, Lu H, Jia P et al (2011b) Narciclasine modulates polar auxin transport in Arabidopsis roots. J Plant Physiol 168:1149–1156
44. Naramoto S, Otegui MS, Kutsuna N, de Rycke R, Dainobu T, Karampelias M, Fujimoto M, Feraru E, Miki D, Fukuda H, Nakano A, Friml J (2014) Insights into the localization and function of the membrane trafficking regulator GNOM ARF-GEF at the Golgi apparatus in Arabidopsis. Plant Cell 26:3062–3076
45. Nishimura T, Matano N, Morishima T, Kakinuma C, Hayashi K et al (2012) Identification of IAA transport inhibitors including compounds affecting cellular PIN trafficking by two chemical screening approaches using maize coleoptile systems. Plant Cell Physiol 53:1671–1682
46. Ortiz-Zapater E, Soriano-Ortega E, Marcote MJ, Ortiz-Masiá D, Aniento F (2006) Trafficking of the human transferrin receptor in plant cells: effects of tyrphostin A23 and brefeldin A. Plant J 48:757–770
47. Paciorek T, Zazímalová E, Ruthardt N, Petrásek J, Stierhof YD et al (2005) Auxin inhibits endocytosis and promotes its own efflux from cells. Nature 435:1251–1256
48. Piozzi F, Marino ML, Fuganti C, Martino AD (1969) Occurrence of non-basic metabolites in Amaryllidaceae. Phytochemistry 8:1745–1748
49. Rahman A, Bannigan A, Sulaman W, Pechter P, Blancaflor EB et al (2007) Auxin, actin and growth of the Arabidopsis thaliana primary root. Plant J 50:514–528
50. Robert S, Chary SN, Drakakaki G, Li S, Yang Z et al (2008) Endosidin1 defines a compartment involved in endocytosis of the brassinosteroid receptor BRI1 and the auxin transporters PIN2 and AUX1. Proc Nat Acad Sci USA 105:8464–8469
51. Soltys D, Rudzińska-Langwald A, Gniazdowska A, Wiśniewska A, Bogatek R (2012) Inhibition of tomato (Solanum lycopersicum L.) root growth by cyanamide is due to altered cell division, phytohormone balance and expansin gene expression. Planta 236:1629–1638
52. Swarup R, Kargul J, Marchant A, Zadik D, Rahman A et al (2004) Structure-function analysis of the presumptive Arabidopsis auxin permease AUX1. Plant Cell 16:3069–3083
53. Titapiwatanakun B, Murphy AS (2009) Post-transcriptional regulation of auxin transport proteins: cellular trafficking, protein phosphorylation, protein maturation, ubiquitination, and membrane composition. J Exp Bot 60:1093–1107
54. Ueda T, Yamaguch M, Uchimiya H, Nakano A (2001) Ara6, a plant-unique novel tyype Rab GTPpase, functions in the endocytic pathway of Arabidopsis thaliana. EMBO J 20:4370–4741
55. Van Goietsenoven G, Mathieu V, Lefranc F, Kornienko A, Evidente A et al (2012) Narciclasine as well as other Amaryllidaceae isocarbostyrils are promising GTP-ase targeting agents against brain cancers. Med Res Rev 33:439–455
56. Wang YS, Yoo CM, Blancaflor EB (2008) Improved imaging of actin filaments in transgenic Arabidopsis plants expressing a green fluorescent protein fusion to the C- and N-termini of the fimbrin actinbinding domain 2. New Phytol 177:525–536
57. Weir TL, Park SW, Vivanco JM (2004) Biochemical and physiological mechanisms mediated by allelochemicals. Curr Opin Plant Biol 7:472–479
58. Weston LA, Mathesius U (2013) Flavonoids: their structure, biosynthesis and role in the rhizosphere, including allelopathy. J Chem Ecol 39:283–297
59. Wisniewska J, Xu J, Seifertová D, Brewer PB, Ruzicka K et al (2006) Polar PIN localization directs auxin flow in plants. Science 312:883
60. Xu J, Scheres B (2005) Dissection of Arabidopsis ADP-RIBOSYLATIONFACTOR1 function in epidermal cell polarity. Plant Cell 17:525–536
61. Zupkó I, Réthy B, Hohmann J, Molnár J, Ocsovszki I et al (2009) Antitumor activity of alkaloids derived from Amaryllidaceae species. In Vivo 23:41–48