Auxin Influx Carriers Control Vascular Patterning and Xylem Differentiation in
The vascular tissues in the shoot of Arabidopsis thaliana (Arabidopsis) plants are organized in vascular bundles, disposed in a conserved periodic radial pattern. It is known that this pattern emerges due to the accumulation of the phytohormone auxin, which is actively transported by the so-called efflux and the influx carriers. Efflux carriers facilitate polar transport of auxin from inside the cell to the extracellular space, while influx carriers pump auxin from outside the cell to its interior in a non-polar manner. Although a role for auxin efflux carriers in the emergence of this pattern has been recognized, the role of auxin influx carriers has remained hitherto neglected. In this study, we combine theoretical and experimental approaches to unravel the role of the auxin influx carriers in the formation of plant vasculature. Our analysis uncovers primary roles for the auxin influx carriers in vascular patterning, revealing that auxin influx carriers modulate both patterning and the differentiation of the water transporting vascular cells, known as xylem cells.
Vyšlo v časopise:
Auxin Influx Carriers Control Vascular Patterning and Xylem Differentiation in. PLoS Genet 11(4): e32767. doi:10.1371/journal.pgen.1005183
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1005183
Souhrn
The vascular tissues in the shoot of Arabidopsis thaliana (Arabidopsis) plants are organized in vascular bundles, disposed in a conserved periodic radial pattern. It is known that this pattern emerges due to the accumulation of the phytohormone auxin, which is actively transported by the so-called efflux and the influx carriers. Efflux carriers facilitate polar transport of auxin from inside the cell to the extracellular space, while influx carriers pump auxin from outside the cell to its interior in a non-polar manner. Although a role for auxin efflux carriers in the emergence of this pattern has been recognized, the role of auxin influx carriers has remained hitherto neglected. In this study, we combine theoretical and experimental approaches to unravel the role of the auxin influx carriers in the formation of plant vasculature. Our analysis uncovers primary roles for the auxin influx carriers in vascular patterning, revealing that auxin influx carriers modulate both patterning and the differentiation of the water transporting vascular cells, known as xylem cells.
Zdroje
1. Scarpella E, Marcos D, Friml J, Berleth T (2006) Control of leaf vascular patterning by polar auxin transport. Genes & development 20: 1015–1027.
2. Reinhardt D, Pesce ER, Stieger P, Mandel T, Baltensperger K, et al. (2003) Regulation of phyllotaxis by polar auxin transport. Nature 426: 255–260. 14628043
3. Jönsson H, Heisler MG, Shapiro BE, Meyerowitz EM, Mjolsness E (2006) An auxin-driven polarized transport model for phyllotaxis. Proceedings of the National Academy of Sciences of the United States of America 103: 1633–1638. 16415160
4. Smith RS, Guyomarc'h S, Mandel T, Reinhardt D, Kuhlemeier C, et al. (2006) A plausible model of phyllotaxis. Proceedings of the National Academy of Sciences of the United States of America 103: 1301–1306. 16432192
5. Bayer EM, Smith RS, Mandel T, Nakayama N, Sauer M, et al. (2009) Integration of transport-based models for phyllotaxis and midvein formation. Genes & development 23: 373–384.
6. Galweiler L, Guan C, Muller A, Wisman E, Mendgen K, et al. (1998) Regulation of polar auxin transport by AtPIN1 in Arabidopsis vascular tissue. Science 282: 2226–2230. 9856939
7. Ibañes M, Fàbregas N, Chory J, Caño-Delgado AI (2009) Brassinosteroid signaling and auxin transport are required to establish the periodic pattern of Arabidopsis shoot vascular bundles. Proceedings of the National Academy of Sciences of the United States of America 106: 13630–13635. doi: 10.1073/pnas.0906416106 19666540
8. Benkova E, Michniewicz M, Sauer M, Teichmann T, Seifertova D, et al. (2003) Local, efflux-dependent auxin gradients as a common module for plant organ formation. Cell 115: 591–602. 14651850
9. Blilou I, Xu J, Wildwater M, Willemsen V, Paponov I, et al. (2005) The PIN auxin efflux facilitator network controls growth and patterning in Arabidopsis roots. Nature 433: 39–44. 15635403
10. Grieneisen VA, Xu J, Maree AF, Hogeweg P, Scheres B (2007) Auxin transport is sufficient to generate a maximum and gradient guiding root growth. Nature 449: 1008–1013. 17960234
11. Muller A, Guan C, Galweiler L, Tanzler P, Huijser P, et al. (1998) AtPIN2 defines a locus of Arabidopsis for root gravitropism control. The EMBO journal 17: 6903–6911. 9843496
12. Friml J, Wisniewska J, Benkova E, Mendgen K, Palme K (2002) Lateral relocation of auxin efflux regulator PIN3 mediates tropism in Arabidopsis. Nature 415: 806–809. 11845211
13. Abas L, Benjamins R, Malenica N, Paciorek T, Wisniewska J, et al. (2006) Intracellular trafficking and proteolysis of the Arabidopsis auxin-efflux facilitator PIN2 are involved in root gravitropism. Nature cell biology 8: 249–256. 16489343
14. Peret B, Middleton AM, French AP, Larrieu A, Bishopp A, et al. (2013) Sequential induction of auxin efflux and influx carriers regulates lateral root emergence. Molecular systems biology 9: 699. doi: 10.1038/msb.2013.43 24150423
15. Bishopp A, Help H, El-Showk S, Weijers D, Scheres B, et al. (2011) A mutually inhibitory interaction between auxin and cytokinin specifies vascular pattern in roots. Current biology: CB 21: 917–926. doi: 10.1016/j.cub.2011.04.017 21620702
16. Fukuda H, Komamine A (1980) Establishment of an Experimental System for the Study of Tracheary Element Differentiation from Single Cells Isolated from the Mesophyll of Zinnia elegans. Plant physiology 65: 57–60. 16661142
17. Ljung K, Bhalerao RP, Sandberg G (2001) Sites and homeostatic control of auxin biosynthesis in Arabidopsis during vegetative growth. The Plant journal: for cell and molecular biology 28: 465–474. 11737783
18. Rubery PH, Sheldrake AR (1974) Carrier-mediated auxin transport. Planta 118: 101–121. doi: 10.1007/BF00388387 24442257
19. Raven JA (1975) Transport of indoleacetic acid in plant cells in relation to ph and electrical potential gradients, and its significance for polar iaa transport. New Phytologist 74: 163–172.
20. Geisler M, Murphy AS (2006) The ABC of auxin transport: the role of p-glycoproteins in plant development. FEBS letters 580: 1094–1102. 16359667
21. Bandyopadhyay A, Blakeslee JJ, Lee OR, Mravec J, Sauer M, et al. (2007) Interactions of PIN and PGP auxin transport mechanisms. Biochemical Society transactions 35: 137–141. 17233620
22. Mravec J, Kubes M, Bielach A, Gaykova V, Petrasek J, et al. (2008) Interaction of PIN and PGP transport mechanisms in auxin distribution-dependent development. Development 135: 3345–3354. doi: 10.1242/dev.021071 18787070
23. Titapiwatanakun B, Blakeslee JJ, Bandyopadhyay A, Yang H, Mravec J, et al. (2009) ABCB19/PGP19 stabilises PIN1 in membrane microdomains in Arabidopsis. The Plant journal: for cell and molecular biology 57: 27–44. doi: 10.1111/j.1365-313X.2008.03668.x 18774968
24. Bennett MJ, Marchant A, Green HG, May ST, Ward SP, et al. (1996) Arabidopsis AUX1 gene: a permease-like regulator of root gravitropism. Science 273: 948–950. 8688077
25. Peret B, Swarup K, Ferguson A, Seth M, Yang Y, et al. (2012) AUX/LAX genes encode a family of auxin influx transporters that perform distinct functions during Arabidopsis development. The Plant cell 24: 2874–2885. doi: 10.1105/tpc.112.097766 22773749
26. Swarup R, Peret B (2012) AUX/LAX family of auxin influx carriers-an overview. Frontiers in plant science 3: 225. doi: 10.3389/fpls.2012.00225 23087694
27. Kleine-Vehn J, Dhonukshe P, Swarup R, Bennett M, Friml J (2006) Subcellular trafficking of the Arabidopsis auxin influx carrier AUX1 uses a novel pathway distinct from PIN1. The Plant cell 18: 3171–3181. 17114355
28. Smith RS, Bayer EM (2009) Auxin transport-feedback models of patterning in plants. Plant, cell & environment 32: 1258–1271.
29. Novoselova ES, Mironova VV, Omelyanchuk NA, Kazantsev FV, Likhoshvai VA (2013) Mathematical modeling of auxin transport in protoxylem and protophloem of Arabidopsis thaliana root tips. Journal of bioinformatics and computational biology 11: 1340010. doi: 10.1142/S0219720013400106 23427992
30. Stieger PA, Reinhardt D, Kuhlemeier C (2002) The auxin influx carrier is essential for correct leaf positioning. The Plant journal: for cell and molecular biology 32: 509–517. 12445122
31. Bainbridge K, Guyomarc'h S, Bayer E, Swarup R, Bennett M, et al. (2008) Auxin influx carriers stabilize phyllotactic patterning. Genes & development 22: 810–823.
32. Ugartechea-Chirino Y, Swarup R, Swarup K, Peret B, Whitworth M, et al. (2010) The AUX1 LAX family of auxin influx carriers is required for the establishment of embryonic root cell organization in Arabidopsis thaliana. Annals of botany 105: 277–289. doi: 10.1093/aob/mcp287 19952011
33. Swarup R, Friml J, Marchant A, Ljung K, Sandberg G, et al. (2001) Localization of the auxin permease AUX1 suggests two functionally distinct hormone transport pathways operate in the Arabidopsis root apex. Genes & development 15: 2648–2653.
34. Swarup R, Kramer EM, Perry P, Knox K, Leyser HM, et al. (2005) Root gravitropism requires lateral root cap and epidermal cells for transport and response to a mobile auxin signal. Nature cell biology 7: 1057–1065. 16244669
35. Swarup K, Benkova E, Swarup R, Casimiro I, Peret B, et al. (2008) The auxin influx carrier LAX3 promotes lateral root emergence. Nature cell biology 10: 946–954. doi: 10.1038/ncb1754 18622388
36. Marchant A, Bhalerao R, Casimiro I, Eklof J, Casero PJ, et al. (2002) AUX1 promotes lateral root formation by facilitating indole-3-acetic acid distribution between sink and source tissues in the Arabidopsis seedling. The Plant cell 14: 589–597. 11910006
37. Marchant A, Kargul J, May ST, Muller P, Delbarre A, et al. (1999) AUX1 regulates root gravitropism in Arabidopsis by facilitating auxin uptake within root apical tissues. The EMBO journal 18: 2066–2073. 10205161
38. Lampugnani ER, Kilinc A, Smyth DR (2013) Auxin controls petal initiation in Arabidopsis. Development 140: 185–194. doi: 10.1242/dev.084582 23175631
39. Vandenbussche F, Petrasek J, Zadnikova P, Hoyerova K, Pesek B, et al. (2010) The auxin influx carriers AUX1 and LAX3 are involved in auxin-ethylene interactions during apical hook development in Arabidopsis thaliana seedlings. Development 137: 597–606. doi: 10.1242/dev.040790 20110325
40. Heisler MG, Jönsson H (2006) Modeling Auxin Transport and Plant Development. J Plant Growth Regul 25: 302–312.
41. Sahlin P, Soderberg B, Jönsson H (2009) Regulated transport as a mechanism for pattern generation: capabilities for phyllotaxis and beyond. Journal of theoretical biology 258: 60–70. doi: 10.1016/j.jtbi.2009.01.019 19490869
42. Wabnik K, Kleine-Vehn J, Balla J, Sauer M, Naramoto S, et al. (2010) Emergence of tissue polarization from synergy of intracellular and extracellular auxin signaling. Molecular systems biology 6: 447. doi: 10.1038/msb.2010.103 21179019
43. Essau K (1977) Anatomy of Seed Plants. Wiley, New York 2nd Edition.
44. Jurgens G (2001) Apical-basal pattern formation in Arabidopsis embryogenesis. The EMBO journal 20: 3609–3616. 11447101
45. Essau K (1965) Plant Anatomy. Wiley, New York.
46. Fukuda H (2004) Signals that control plant vascular cell differentiation. Nature reviews Molecular cell biology 5: 379–391. 15122351
47. Mahonen AP, ten Tusscher K, Siligato R, Smetana O, Diaz-Trivino S, et al. (2014) PLETHORA gradient formation mechanism separates auxin responses. Nature 515: 125–129. doi: 10.1038/nature13663 25156253
48. Heisler MG, Ohno C, Das P, Sieber P, Reddy GV, et al. (2005) Patterns of auxin transport and gene expression during primordium development revealed by live imaging of the Arabidopsis inflorescence meristem. Current biology: CB 15: 1899–1911. 16271866
49. Robert S, Kleine-Vehn J, Barbez E, Sauer M, Paciorek T, et al. (2010) ABP1 mediates auxin inhibition of clathrin-dependent endocytosis in Arabidopsis. Cell 143: 111–121. doi: 10.1016/j.cell.2010.09.027 20887896
50. Goldsmith MH, Goldsmith TH, Martin MH (1981) Mathematical analysis of the chemosmotic polar diffusion of auxin through plant tissues. Proceedings of the National Academy of Sciences of the United States of America 78: 976–980. 16592983
51. Kramer EM (2004) PIN and AUX/LAX proteins: their role in auxin accumulation. Trends in plant science 9: 578–582. 15564124
52. Kramer EM, Frazer NL, Baskin TI (2007) Measurement of diffusion within the cell wall in living roots of Arabidopsis thaliana. Journal of experimental botany 58: 3005–3015. 17728296
53. Kramer EM (2008) Computer models of auxin transport: a review and commentary. Journal of experimental botany 59: 45–53. 17431022
54. Alim K, Frey E (2010) Quantitative predictions on auxin-induced polar distribution of PIN proteins during vein formation in leaves. The European physical journal E, Soft matter 33: 165–173. doi: 10.1140/epje/i2010-10604-5 20571847
55. van Berkel K, de Boer RJ, Scheres B, ten Tusscher K (2013) Polar auxin transport: models and mechanisms. Development 140: 2253–2268. doi: 10.1242/dev.079111 23674599
56. Zourelidou M, Absmanner B, Weller B, Barbosa IC, Willige BC, et al. (2014) Auxin efflux by PIN-FORMED proteins is activated by two different protein kinases, D6 PROTEIN KINASE and PINOID. eLife 3.
57. Fosket DE, Torrey JG (1969) Hormonal control of cell proliferation and xylem differentiation in cultured tissues of Glycine max var. Biloxi. Plant physiology 44: 871–880. 5816361
58. Sachs T (1981) The Control of the Patterned Differentiation of Vascular Tissues: Academic Press.
59. Perrot-Rechenmann C (2010) Cellular responses to auxin: division versus expansion. Cold Spring Harbor perspectives in biology 2: a001446. doi: 10.1101/cshperspect.a001446 20452959
60. Ulmasov T, Murfett J, Hagen G, Guilfoyle TJ (1997) Aux/IAA proteins repress expression of reporter genes containing natural and highly active synthetic auxin response elements. The Plant cell 9: 1963–1971. 9401121
61. Dharmasiri N, Dharmasiri S, Weijers D, Lechner E, Yamada M, et al. (2005) Plant Development Is Regulated by a Family of Auxin Receptor F Box Proteins. Developmental Cell 9: 109–119. 15992545
62. Muraro D, Mellor N, Pound MP, Help H, Lucas M, et al. (2014) Integration of hormonal signaling networks and mobile microRNAs is required for vascular patterning in Arabidopsis roots. Proceedings of the National Academy of Sciences of the United States of America 111: 857–862. doi: 10.1073/pnas.1221766111 24381155
63. Band LR, Wells DM, Fozard JA, Ghetiu T, French AP, et al. (2014) Systems analysis of auxin transport in the Arabidopsis root apex. The Plant cell 26: 862–875. doi: 10.1105/tpc.113.119495 24632533
64. Kang J, Tang J, Donnelly P, Dengler N (2003) Primary vascular pattern and expression of ATHB-8 in shoots of Arabidopsis. New Phytologist 158: 443–454.
65. Laxmi A, Pan J, Morsy M, Chen R (2008) Light plays an essential role in intracellular distribution of auxin efflux carrier PIN2 in Arabidopsis thaliana. PloS one 3: e1510. doi: 10.1371/journal.pone.0001510 18231596
66. Ding Z, Galvan-Ampudia CS, Demarsy E, Langowski L, Kleine-Vehn J, et al. (2011) Light-mediated polarization of the PIN3 auxin transporter for the phototropic response in Arabidopsis. Nature cell biology 13: 447–452. doi: 10.1038/ncb2208 21394084
67. Xu T, Dai N, Chen J, Nagawa S, Cao M, et al. (2014) Cell surface ABP1-TMK auxin-sensing complex activates ROP GTPase signaling. Science 343: 1025–1028. doi: 10.1126/science.1245125 24578577
68. Gao Y, Zhang Y, Zhang D, Dai X, Estelle M, et al. (2015) Auxin binding protein 1 (ABP1) is not required for either auxin signaling or Arabidopsis development. Proceedings of the National Academy of Sciences of the United States of America 112: 2275–2280. doi: 10.1073/pnas.1500365112 25646447
69. Rutschow HL, Baskin TI, Kramer EM (2011) Regulation of solute flux through plasmodesmata in the root meristem. Plant physiology 155: 1817–1826. doi: 10.1104/pp.110.168187 21325566
70. Press WH, Teukolsky SA, Vetterling WT, Flannery BP (1993) Numerical Recipes in FORTRAN; The Art of Scientific Computing: Cambridge University Press.
71. Cross M, Greenside H (2009) Pattern formation and dynamics in nonequilibrium systems. Cambridge University Press New York.
72. Tursun B, Cochella L, Carrera I, Hobert O (2009) A toolkit and robust pipeline for the generation of fosmid-based reporter genes in C. elegans. PloS one 4: e4625. doi: 10.1371/journal.pone.0004625 19259264
73. Zhou R, Benavente LM, Stepanova AN, Alonso JM (2011) A recombineering-based gene tagging system for Arabidopsis. The Plant journal: for cell and molecular biology 66: 712–723. doi: 10.1111/j.1365-313X.2011.04524.x 21294796
74. Peret B, Swarup R, Jansen L, Devos G, Auguy F, et al. (2007) Auxin influx activity is associated with Frankia infection during actinorhizal nodule formation in Casuarina glauca. Plant physiology 144: 1852–1862. 17556507
75. Mahonen AP, Bonke M, Kauppinen L, Riikonen M, Benfey PN, et al. (2000) A novel two-component hybrid molecule regulates vascular morphogenesis of the Arabidopsis root. Genes & development 14: 2938–2943.
76. Chaffey N, Cholewa E, Regan S, Sundberg B (2002) Secondary xylem development in Arabidopsis: a model for wood formation. Physiologia plantarum 114: 594–600. 11975734
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Genetika Reprodukčná medicínaČlánok vyšiel v časopise
PLOS Genetics
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