A Division in PIN-Mediated Auxin Patterning during Organ Initiation in Grasses

PLoS Computational Biology

Volumn 10, Issue 1, 2014, Pages

  O'Connor, Devin L ^a,b,e   Runions, Adam ^c   Sluis, Aaron ^a,b   Bragg, Jennifer ^d   Vogel, John P ^d   Prusinkiewicz, Przemyslaw ^c   Hake, Sarah ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b U S DEPARTMENT OF AGRICULTURE   (United States)

^c UNIVERSITY OF CALGARY   (Canada)

^d WESTERN REGIONAL RESEARCH CENTER   (United States)

^e UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

HISTOLOGY; PHYLOGENETIC; PLANTS (BOTANY); TISSUE;

ARABIDOPSIS; ARABIDOPSIS THALIANA; AUXIN SIGNALING; BRASSICACEAE; INTERNAL TISSUES; LOCAL MAXIMUM; PHYLOGENETICS; SHOOT APICAL MERISTEMS; SYNTENY ANALYSIS; VASCULATURE;

PROTEINS;

AUXIN; PEPTIDYLPROLYL ISOMERASE PIN1; PIN PROTEIN; PIN1A PROTEIN; PIN1B PROTEIN; SISTER OF PIN1 PROTEIN; UNCLASSIFIED DRUG; VEGETABLE PROTEIN;

ANGIOSPERM; ARABIDOPSIS THALIANA; ARTICLE; BRACHYPODIUM; CLADISTICS; COMPUTER SIMULATION; CONTROLLED STUDY; GRASS; MAIZE; MOLECULAR DYNAMICS; MOLECULAR MODEL; MOLECULAR PHYLOGENY; NONHUMAN; PLANT DEVELOPMENT; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION; SPIKELET;

ALGORITHMS; ARABIDOPSIS; BRACHYPODIUM; COMPUTATIONAL BIOLOGY; COMPUTER SIMULATION; FLOWERS; GENE EXPRESSION REGULATION, PLANT; GENES, REPORTER; IMAGE PROCESSING, COMPUTER-ASSISTED; INDOLEACETIC ACIDS; MERISTEM; PHYLOGENY; PLANT LEAVES; POACEAE; SOFTWARE; ZEA MAYS;

EID: 84896725119     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.1003447     Document Type: Article

References (57)

1. Dettmer J, Friml J, (2011) Cell polarity in plants: when two do the same, it is not the same. Curr Opin Cell Biol 23: 686-696 doi:10.1016/j.ceb.2011.09.006.
2. Leyser OM, (2011) Auxin, self-organisation, and the colonial nature of plants. Current Biology 21: R331-R337 doi:10.1016/j.cub.2011.02.031.
3. Petrásek J, Friml J, (2009) Auxin transport routes in plant development. Development 136: 2675-2688 doi:10.1242/dev.030353.
4. Petrásek J, Mravec J, Bouchard R, Blakeslee JJ, Abas M, et al. (2006) PIN proteins perform a rate-limiting function in cellular auxin efflux. Science 312: 914-918 doi:10.1126/science.1123542.
5. Wisniewska J, Xu J, Seifertová D, Brewer PB, Ruzicka K, et al. (2006) Polar PIN localization directs auxin flow in plants. Science 312: 883 doi:10.1126/science.1121356.
6. Krecek P, Skůpa P, Libus J, Naramoto S, Tejos R, et al. (2009) The PIN-FORMED (PIN) protein family of auxin transporters. Genome Biol 10: 249 doi:10.1186/gb-2009-10-12-249.
7. Viaene T, Delwiche CF, Rensing SA, Friml J, (2012) Origin and evolution of PIN auxin transporters in the green lineage. Trends Plant Sci 18 (1):: 5-10 doi:10.1016/j.tplants.2012.08.009.
8. Mravec J, Skůpa P, Bailly A, Hoyerová K, Krecek P, et al. (2009) Subcellular homeostasis of phytohormone auxin is mediated by the ER-localized PIN5 transporter. Nature 459: 1136-1140 doi:10.1038/nature08066.
9. 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.
10. 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 doi:10.1038/nature03184.
11. Friml J, Vieten A, Sauer M, Weijers D, Schwarz H, et al. (2003) Efflux-dependent auxin gradients establish the apical-basal axis of Arabidopsis. Nature 426: 147-153 doi:10.1038/nature02085.
12. Reinhardt D, Pesce E-R, Stieger P, Mandel T, Baltensperger K, et al. (2003) Regulation of phyllotaxis by polar auxin transport. Nat Cell Biol 426: 255-260 doi:10.1038/nature02081.
13. Scarpella E, Marcos D, Friml J, Berleth T, (2006) Control of leaf vascular patterning by polar auxin transport. Genes Dev 20: 1015-1027 doi:10.1101/gad.1402406.
14. Dhonukshe P, Huang F, Galván-Ampudia CS, Mähönen AP, Kleine-Vehn J, et al. (2010) Plasma membrane-bound AGC3 kinases phosphorylate PIN auxin carriers at TPRXS(N/S) motifs to direct apical PIN recycling. Development 137: 3245-3255 doi:10.1242/dev.052456.
15. Huang F, Zago MK, Abas L, van Marion A, Galván-Ampudia CS, et al. (2010) Phosphorylation of conserved PIN motifs directs Arabidopsis PIN1 polarity and auxin transport. Plant Cell 22: 1129-1142 doi:10.1105/tpc.109.072678.
16. Zhang J, Nodzynski T, Pencík A, Rolcík J, Friml J, (2010) PIN phosphorylation is sufficient to mediate PIN polarity and direct auxin transport. Proc Natl Acad Sci USA 107: 918-922 doi:10.1073/pnas.0909460107.
17. Bilsborough GD, Runions A, Barkoulas M, Jenkins HW, Hasson A, et al. (2011) Model for the regulation of Arabidopsis thaliana leaf margin development. Proc Natl Acad Sci USA 108: 3424-3429 doi:10.1073/pnas.1015162108.
18. Hay A, Barkoulas M, Tsiantis M, (2006) ASYMMETRIC LEAVES1 and auxin activities converge to repress BREVIPEDICELLUS expression and promote leaf development in Arabidopsis. Development 133: 3955-3961 doi:10.1242/dev.02545.
19. Hay A, Tsiantis M, (2006) The genetic basis for differences in leaf form between Arabidopsis thaliana and its wild relative Cardamine hirsuta. Nat Genet 38: 942-947 doi:10.1038/ng1835.
20. Reinhardt D, Mandel T, Kuhlemeier C, (2000) Auxin regulates the initiation and radial position of plant lateral organs. Plant Cell 12: 507-518.
21. Jönsson H, Heisler MG, Shapiro BE, Meyerowitz EM, Mjolsness E, (2006) An auxin-driven polarized transport model for phyllotaxis. Proc Natl Acad Sci USA 103: 1633-1638 doi:10.1073/pnas.0509839103.
22. Smith RS, Guyomarc'h S, Mandel T, Reinhardt D, Kuhlemeier C, et al. (2006) A plausible model of phyllotaxis. Proc Natl Acad Sci USA 103: 1301-1306 doi:10.1073/pnas.0510457103.
23. van Mourik S, Kaufmann K, van Dijk ADJ, Angenent GC, Merks RMH, et al. (2012) Simulation of organ patterning on the floral meristem using a polar auxin transport model. PLoS ONE 7: e28762 doi:10.1371/journal.pone.0028762.
24. Merks RMH, Van de Peer Y, Inzé D, Beemster GTS, (2007) Canalization without flux sensors: a traveling-wave hypothesis. Trends Plant Sci 12: 384-390 doi:10.1016/j.tplants.2007.08.004.
25. Sachs T, (1981) The control of the patterned differentiation of vascular tissues. Adv Bot Res 9: 151-262.
26. Sachs T, (1969) Polarity and induction of organized vascular tissues. Ann Bot-London 33: 263.
27. Mitchison G, (1981) The polar transport of auxin and vein patterns in plants. Philos T Roy Soc B 295: 461-&.
28. Mitchison G, (1980) Model for vein formation in higher-plants. P Roy Soc Lond B Bio 207: 79-109.
29. Rolland-Lagan A-G, Prusinkiewicz P, (2005) Reviewing models of auxin canalization in the context of leaf vein pattern formation in Arabidopsis. Plant J 44: 854-865 doi:10.1111/j.1365-313X.2005.02581.x.
30. Stoma S, Lucas M, Chopard J, Schaedel M, Traas J, et al. (2008) Flux-based transport enhancement as a plausible unifying mechanism for auxin transport in meristem development. PLoS Comput Biol 4: e1000207 doi:10.1371/journal.pcbi.1000207.
31. Feugier FG, Mochizuki A, Iwasa Y, (2005) Self-organization of the vascular system in plant leaves: inter-dependent dynamics of auxin flux and carrier proteins. Journal of Theoretical Biology 236: 366-375 doi:10.1016/j.jtbi.2005.03.017.
32. Bayer EM, Smith RS, Mandel T, Nakayama N, Sauer M, et al. (2009) Integration of transport-based models for phyllotaxis and midvein formation. Genes Dev 23: 373-384 doi:10.1101/gad.497009.
33. Smith RS, Bayer EM, (2009) Auxin transport-feedback models of patterning in plants. Plant Cell Environ 32: 1258-1271 doi:10.1111/j.1365-3040.2009.01997.x.
34. Brooks L, Strable J, Zhang X, Ohtsu K, Zhou R, et al. (2009) Microdissection of shoot meristem functional domains. PLoS Genet 5: e1000476 doi:10.1371/journal.pgen.1000476.
35. Peng J, Chen R, (2011) Auxin efflux transporter MtPIN10 regulates compound leaf and flower development in Medicago truncatula. Plant Signal Behav 6: 1537-1544 doi:10.4161/psb.6.10.17326.
36. Carraro N, Forestan C, Canova S, Traas J, Varotto S, (2006) ZmPIN1a and ZmPIN1b encode two novel putative candidates for polar auxin transport and plant architecture determination of maize. Plant Physiol 142: 254-264 doi:10.1104/pp.106.080119.
37. Gallavotti A, Yang Y, Schmidt R, Jackson D, (2008) The relationship between auxin transport and maize branching. Plant Physiol 147 (4):: 1913-23 doi:10.1104/pp.108.121541.
38. Forestan C, Farinati S, Varotto S, (2012) The maize PIN gene family of auxin transporters. Front Plant Sci 3: 16 doi:10.3389/fpls.2012.00016.
39. Derbyshire P, Byrne M, (2013) MORE SPIKELETS1 is required for spikelet fate in the inflorescence of Brachypodium distachyon. Plant Physiol 161 (3):: 1291-302 doi:10.1104/pp.112.212340.
40. 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. Curr Biol 15: 1899-1911 doi:10.1016/j.cub.2005.09.052.
41. Avsian-Kretchmer O, (2002) Indole acetic acid distribution coincides with vascular differentiation pattern during Arabidopsis leaf ontogeny. Plant Physiol 130: 199-209 doi:10.1104/pp.003228.
42. Medford JI, Behringer FJ, Callos JD, Feldmann KA, (1992) Normal and abnormal development in the Arabidopsis vegetative shoot apex. Plant Cell 4: 631-643 doi:10.1105/tpc.4.6.631.
43. Evans LS, Berg AR, (1972) Early histogenesis and semiquantitative histochemistry of leaf initiation in Triticum aestivum. American Journal of Botany 59: 973-980.
44. Sharman B, (1942) Developmental anatomy of the shoot of Zea mays L. Ann Bot-London 6: 245-282.
45. Rinne PL, van der Schoot C, (1998) Symplasmic fields in the tunica of the shoot apical meristem coordinate morphogenetic events. Development 125: 1477-1485.
46. Bainbridge K, Guyomarc'h S, Bayer E, Swarup R, Bennett M, et al. (2008) Auxin influx carriers stabilize phyllotactic patterning. Genes Dev 22: 810-823 doi:10.1101/gad.462608.
47. Barkoulas M, Hay A, Kougioumoutzi E, Tsiantis M, (2008) A developmental framework for dissected leaf formation in the Arabidopsis relative Cardamine hirsuta. Nat Genet 40: 1136-1141 doi:10.1038/ng.189.
48. Prusinkiewicz P, Runions A, (2012) Computational models of plant development and form. New Phytol 193: 549-569 doi:10.1111/j.1469-8137.2011.04009.x.
49. Kramer EM, (2009) Auxin-regulated cell polarity: an inside job? Trends Plant Sci 14: 242-247 doi:10.1016/j.tplants.2009.02.005.
50. Sauer M, Kleine-Vehn J, (2011) AUXIN BINDING PROTEIN1: The Outsider. Plant Cell 23 (6):: 2033-43 doi:10.1105/tpc.111.087064.
51. Abley K, de Reuille PB, Strutt D, Bangham A, Prusinkiewicz P, et al. (2013) An intracellular partitioning-based framework for tissue cell polarity in plants and animals. Development 140: 2061-2074 doi:10.1242/dev.062984.
52. Wabnik K, Kleine-Vehn J, Govaerts W, Friml J, (2011) Prototype cell-to-cell auxin transport mechanism by intracellular auxin compartmentalization. Trends Plant Sci 16: 468-475 doi:10.1016/j.tplants.2011.05.002.
53. Vogel J, Hill T, (2008) High-efficiency Agrobacterium-mediated transformation of Brachypodium distachyon inbred line Bd21-3. Plant Cell Rep 27: 471-478 doi:10.1007/s00299-007-0472-y.
54. Grandjean O, (2004) In vivo analysis of cell division, cell growth, and differentiation at the shoot apical meristem in Arabidopsis. Plant Cell 16: 74-87 doi:10.1105/tpc.017962.
55. Chuck G, Bortiri E, (2010) The unique relationship between tsh4 and ra2 in patterning floral phytomers. Plant Signal Behav 5: 979-981.
56. Smith C, Prusinkiewicz P, (2004) Simulation modeling of growing tissues. Proceedings of the 4th International Workshop on Functional-Structural Plant Models pp. 365-370.
57. Bremer B, Bremer K, Chase MW, Fay MF, Reveal JL, et al. (2009) An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG III. Bot J Linn Soc 161: 105-121 doi:10.1111/j.1095-8339.2009.00996.x.