Mechanistic insights from a quantitative analysis of pollen tube guidance

BMC Plant Biology

Volumn 10, Issue , 2010, Pages

  Stewman, Shannon F ^a,b,h   Jones Rhoades, Matthew ^f   Bhimalapuram, Prabhakar ^g   Tchernookov, Martin ^a,b   Preuss, Daphne ^c,d,e   Dinner, Aaron R ^a,b,e  

^a UNIVERSITY OF CHICAGO   (United States)

^b UNIVERSITY OF CHICAGO   (United States)

^c THE UNIVERSITY OF CHICAGO   (United States)

^d Chromatin Inc   (United States)

^e UNIVERSITY OF CHICAGO   (United States)

^f KNOX COLLEGE   (United States)

^g INTERNATIONAL INSTITUTE OF INFORMATION TECHNOLOGY   (India)

^h ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA;

ARABIDOPSIS; ARTICLE; BIOLOGICAL MODEL; COMPUTER SIMULATION; CONFOCAL MICROSCOPY; CULTURE MEDIUM; GROWTH, DEVELOPMENT AND AGING; IMAGE PROCESSING; OVULE; POLLEN TUBE;

ARABIDOPSIS; COMPUTER SIMULATION; CULTURE MEDIA; IMAGE PROCESSING, COMPUTER-ASSISTED; MICROSCOPY, CONFOCAL; MODELS, BIOLOGICAL; OVULE; POLLEN TUBE;

EID: 77649287384     PISSN: None     EISSN: 14712229     Source Type: Journal    
DOI: 10.1186/1471-2229-10-32     Document Type: Article

References (73)

1. Lush WM. Whither chemotropism and pollen tube guidance?. Trends Plant Sci 1999, 4:413-418. 10.1016/S1360-1385(99)01473-9, 10498966.
2. Palanivelu R, Preuss D. Pollen tube targeting and axon guidance: parallels in tip growth mechanisms. Trends Cell Biol 2000, 10:517-524. 10.1016/S0962-8924(00)01849-3, 11121743.
3. Johnson MA, Preuss D. Plotting a course: multiple signals guide pollen tubes to their targets. Dev Cell 2002, 2:273-281. 10.1016/S1534-5807(02)00130-2, 11879633.
4. Mascarenhas JP. The biochemistry of angiosperm pollen development. Bot Rev 1975, 41:259-314.
5. Lush WM, Grieser F, Wolter-Arts M. Directional guidance of Nicotiana alata pollen tubes in vitro and on the stigma. Plant Phys 1998, 118:733-741.
6. Kim S, Mollet JC, Dong J, Zhang K, Park SY, Lord EM. Chemocyanin, a small basic protein from the lily stigma, induces pollen tube chemotropism. Proc Natl Acad Sci USA 2003, 100:16125-16130. 10.1073/pnas.2533800100, 307703, 14671326.
7. Palanivelu R, Preuss D. Distinct short-range ovule signals attract or repel Arabidopsis thaliana pollen tubes in vitro. BMC Plant Biol 2006, 6:7. 10.1186/1471-2229-6-7, 1489931, 16595022.
8. Prado AM, Porterfield DM, Feijó JA. Nitric oxide is involved in growth regulation and reorientation of pollen tubes. Development 2004, 131:2707-2714. 10.1242/dev.01153, 15128654.
9. Prado AM, Colaçoa R, Morenoa N, Silvaa AC, Feijó JA. Targeting of pollen tubes to ovules is dependent on nitric oxide (NO) signaling. Mol Plant 2008, 1:703-714. 10.1093/mp/ssn034, 19825574.
10. Okuda S, Tsutsui H, Shiina K, Sprunck S, Takeuchi H, Yui R, Kasahara R, Hamamura Y, Mizukami A, Susaki D, Kawano N, Sakakibara T, Namiki S, Itoh K, Otsuka K, Matsuzaki M, Nozaki H, Kuroiwa T, Nakano A, Kanaoka M, Dresselhaus T, Sasaki N, Higashiyama T. Defensin-like polypeptide LUREs are pollen tube attractants secreted from synergid cells. Nature 2009, 458:357-361. 10.1038/nature07882, 19295610.
11. Higashiyama T, Kuroiwa H, Kawano S, Kuroiwa T. Guidance in vitro of the pollen tube to the naked embryo sac of Torenia fournieri. Plant Cell 1998, 10:2019-2032. 10.1105/tpc.10.12.2019, 143976, 9836742.
12. Willemse MTM, Plyushch TA, Reinders MC. In vitro micropylar penetration of the pollen tube in the ovule of Gasteria verrucosa. Plant Science 1995, 108:201-208.
13. Higashiyama T, Inatsugi R, Sakamoto S, Sasaki N, Mori T, Kuroiwa H, Nakada T, Nozaki H, Kuroiwa T, Nakano A. Species preferentiality of the pollen tube attractant derived from the synergid cell of Torenia fournieri. Plant Physiol 2006, 142:481-491. 10.1104/pp.106.083832, 1586061, 16935992.
14. Higashiyama T, Yabe S, Sasaki N, Nishimura Y, Miyagishima S, Kuroiwa H, Kuroiwa T. Pollen tube attraction by the synergid cell. Science 2001, 293:1480-1483. 10.1126/science.1062429, 11520985.
15. Hill NA, Hader DP. A biased random walk model for the trajectories of swimming micro-organisms. J Theor Biol 1997, 186:503-526. 10.1006/jtbi.1997.0421, 11536821.
16. Dieterich P, Klages R, Preuss R, Schwab A. Anomalous dynamics of cell migration. Proc Natl Acad Sci USA 2008, 105:459-463. 10.1073/pnas.0707603105, 2206558, 18182493.
17. Selmeczi D, Mosler S, Hagedorn PH, Larsen NB, Flyvbjerg H. Cell motility as persistent random motion: theories from experiments. Biophys J 2006, 89:912-931. 10.1529/biophysj.105.061150, 1366641, 15951372.
18. Shenoy VB, Tambe DT, Prasad A, Theriot JA. A kinematic description of the trajectories of Listeria monocytogenes propelled by actin comet tails. Proc Natl Acad Sci USA 2007, 104:8229-8234. 10.1073/pnas.0702454104, 1895934, 17485664.
19. Nossal R, Zigmond SH. Chemotropism indices for polymorphonuclear leukocytes. Biophys J 1976, 16:1171-1182. 10.1016/S0006-3495(76)85766-9, 1334931, 963197.
20. Tranquillo RT, Lauffenburger DA. Stochastic model of leukocyte chemosensory movement. J Math Biol 1987, 25:229-262. 10.1007/BF00276435, 3625051.
21. Tranquillo RT, Lauffenburger DA, Zigmond SH. A stochastic model for leukocyte random motility and chemotaxis based on receptor binding fluctuations. J Cell Biol 1988, 106:303-309. 10.1083/jcb.106.2.303, 2114982, 3339093.
22. Shimizu KK, Okada K. Attractive and repulsive interactions between female and male gametophytes in Arabidopsis pollen tube guidance. Development 2000, 127:4511-4518.
23. Huck N, Moore JM, Federer M, Grossniklaus U. The Arabidopsis mutant feronia disrupts the female gametophytic control of pollen tube reception. Development 2003, 130:2149-2159. 10.1242/dev.00458, 12668629.
24. Rotman N, Rozier F, Boavida L, Dumas C, Berger F, Faure J. Female control of male gamete delivery during fertilization in Arabidopsis thaliana. Curr Biol 2003, 13:432-436. 10.1016/S0960-9822(03)00093-9, 12620194.
25. Escobar-Restrepo J, Huck N, Kessler S, Gagliardini V, Gheyselinck J, Yang W, Grossniklaus U. The FERONIA receptor-like kinase mediates male-female interactions during pollen tube reception. Science 2007, 317:656-660. 10.1126/science.1143562, 17673660.
26. Mardia KV. Statistics of directional data 1972, London and New York: Academic Press.
27. Fisher NI. Statistical analysis of circular data 1993, Cambridge (UK) and New York: Cambridge University Press.
28. Devreotes P, Janetopoulos C. Eukaryotic chemotaxis: distinctions between directional sensing and polarization. J Biol Chem 2003, 278:20445-20448. 10.1074/jbc.R300010200, 12672811.
29. Lin Y, Wang Y, Zhu J, Yang Z. Localization of a Rho GTPase implies a role in tip growth and movement of the generative cell in pollen tubes. Plant Cell 1996, 8:293-303. 10.1105/tpc.8.2.293, 161099, 12239385.
30. Hwang JU, Gu Y, Lee YJ, Yang Z. Oscillatory ROP GTPase activation leads the oscillatory polarized growth of pollen tubes. Mol Biol Cell 2005, 16:5385-5399. 10.1091/mbc.E05-05-0409, 1266434, 16148045.
31. Hepler PK, Vidali L, Cheung AY. Polarized cell growth in higher plants. Annu Rev Cell Dev Biol 2001, 17:159-187. 10.1146/annurev.cellbio.17.1.159, 11687487.
32. Feijó JA, Sainhas J, Holdaway-Clarke T, Cordeiro MS, Kunkel JG, Hepler PK. Cellular oscillations and the regulation of growth: the pollen tube paradigm. Bioessays 2001, 23:86-94. 10.1002/1521-1878(200101)23:1<86::AID-BIES1011>3.0.CO;2-D, 11135313.
33. Feijó JA, Costa SS, Prado AM, Becker JD, Certal AC. Signalling by tips. Curr Opin Plant Biol 2004, 7:589-598. 10.1016/j.pbi.2004.07.014, 15337103.
34. Certal AC, Almeida RB, Carvalho LM, Wong E, Moreno N, Michard E, Carneiro J, Rodriguéz-Léon J, Wu HM, Cheung AY, Feijó JA. Exclusion of a proton ATPase from the apical membrane is associated with cell polarity and tip growth in Nicotiana tabacum pollen tubes. Plant Cell 2008, 20:614-634. 10.1105/tpc.106.047423, 2329945, 18364468.
35. Macnab RM, Koshland DE. The gradient-sensing mechanism in bacterial chemotaxis. Proc Natl Acad Sci USA 1972, 69:2509-2512. 10.1073/pnas.69.9.2509, 426976, 4560688.
36. Berg HC, Tedesco PM. Transient response to chemotactic stimuli in Escherichia coli. Proc Natl Acad Sci USA 1975, 72:3235-3239. 10.1073/pnas.72.8.3235, 432957, 1103143.
37. Berg HC, Purcell EM. Physics of chemoreception. Biophys J 1977, 20:193-219. 10.1016/S0006-3495(77)85544-6, 1473391, 911982.
38. Vergassola M, Villermaux E, Shraiman BI. 'Infotaxis' as a strategy for searching without gradients. Nature 2007, 445:406-409. 10.1038/nature05464, 17251974.
39. Reinhardt M. Das wachstum der pilzhyphen. Ein beitrag zur kenntniss des flachenwachstums vegetabilischer zellmembranen. Jahrb Wiss Bot 1892, 23:479-566.
40. de Ricci DR, Kendrick B. Computer modeling of hyphal tip growth in fungi. Can J Bot 1972, 50:2455-2462.
41. Goriely A, Tabor M. Biomechanical models of hyphal growth in actinomycetes. J Theor Biol 2003, 222:211-218. 10.1016/S0022-5193(03)00029-8, 12727456.
42. Dumais J, Shaw S, Steele C, Long S, Ray P. An anisotropic-viscoplastic model of plant cell morphogenesis by tip growth. Int J Dev Biol 2006, 50:209-222. 10.1387/ijdb.052066jd, 16479489.
43. Bolduc JF, Lewis LJ, Aubin C, Geitmann A. Finite-element analysis of geometrical factors in micro-indentation of pollen tubes. Biomechan Model Mechanobiol 2006, 5:227-236.
44. Kroeger JH, Geitmann A, Grant M. Model for calcium dependent oscillatory growth in pollen tubes. J Theor Biol 2008, 253:363-374. 10.1016/j.jtbi.2008.02.042, 18471831.
45. Crick F. Diffusion in embryogenesis. Nature 1970, 225:420-422. 10.1038/225420a0, 5411117.
46. Eichele G, Thaller C. Characterization of concentration gradients of a morphogenetically active retinoid in the chick limb bud. J Cell Biol 1987, 105:1917-1923. 10.1083/jcb.105.4.1917, 2114645, 3667700.
47. Goodhill GJ. Diffusion in axon guidance. Eur J Neurosci 1997, 9:1414-1421. 10.1111/j.1460-9568.1997.tb01496.x, 9240399.
48. Altieri AS, Hinton DP, Byrd RA. Association of biomolecular systems via pulsed field gradient NMR self-diffusion measurements. J Am Chem Soc 1995, 117:7566-7567.
49. Hülskamp M, Schneitz K, Pruitt R. Genetic evidence for a long-range activity that directs pollen tube guidance in Arabidopsis. Plant Cell 1995, 7:57-64. 10.1105/tpc.7.1.57, 160764, 12242351.
50. Crawford BCW, Ditta G, Yanofsky MF. The NTT gene is required for transmitting-tract development in carpels of Arabidopsis thaliana. Curr Biol 2007, 17:1101-1108. 10.1016/j.cub.2007.05.079, 17600712.
51. Zigmond SH. Chemotropism indices for polymorphonuclear leukocytes. Nature 1974, 249:450-452. 10.1038/249450a0, 4834231.
52. Samadani A, Mettetal J, van Oudenaarden A. Cellular asymmetry and individuality in directional sensing. Proc Natl Acad Sci USA 2006, 103:11549-11554. 10.1073/pnas.0601909103, 1544207, 16864788.
53. Mortimer D, Feldner J, Vaughan T, Vetter I, Pujic Z, Rosoff WJ, Burrage K, Dayan P, Richards LJ, Goodhill GJ. A Bayesian model predicts the response of axons to molecular gradients. Proc Natl Acad Sci 2009, 106:10296-10301. 10.1073/pnas.0900715106, 2700145,2700145, 19541606.
54. Zheng ZL, Yang Z. The Rop GTPase switch turns on polar growth in pollen. Trends Plant Sci 2000, 5:298-303. 10.1016/S1360-1385(00)01654-X, 10871902.
55. Adler J. Chemotaxis in bacteria. Annu Rev Biochem 1975, 44:341-356. 10.1146/annurev.bi.44.070175.002013, 1094913.
56. DeLisi C, Marchetti F, Grosso GD. A theory of measurement error and its implications for spatial and temporal gradient sensing during chemotaxis. Cell Biophys 1982, 4:211-229.
57. Ray SM, Park SS, Ray A. Pollen tube guidance by the female gametophyte. Development 1997, 124:2489-2498.
58. Kasahara RD, Portereiko MF, Sandaklie-Nikolova L, Rabiger DS, Drews GN. MYB98 is required for pollen tube guidance and synergid cell differentiation in Arabidopsis. Plant Cell 2005, 17:2981-2992. 10.1105/tpc.105.034603, 1276024, 16214903.
59. Chen YH, Li HJ, Shi DQ, Yuan L, Liu J, Sreenivasan R, Baskar R, Grossniklaus U, Yang WC. The central cell plays a critical role in pollen tube guidance in Arabidopsis. Plant Cell 2007, 19:3563-3577. 10.1105/tpc.107.053967, 2174880, 18055609.
60. Punwani JA, Rabiger DS, Drews GN. MYB98 positively regulates a battery of synergid-expressed genes encoding filiform apparatus localized proteins. Plant Cell 2007, 19:2557-2568. 10.1105/tpc.107.052076, 2002610, 17693534.
61. Bowman JL. Arabidopsis: an atlas of morphology and development 1994, New York: Springer-Verlag.
62. Kandasamy MK, Nasrallah JB, Nasrallah ME. Pollen-pistil interactions and developmental regulation of pollen tube growth in Arabidopsis. Development 1994, 120:3405-3418., http://dev.biologists.org/content/120/12/3405.abstract
63. Hollander M, Wolfe D. Nonparametric statistical methods 1999, New York: John Wiley & Sons, 2.
64. R Development Core Team R: A Language and Environment for Statistical Computing, version 2.8.1. R Development Core Team., http://www.R-project.org
65. Efron B, Tibshirani RJ. An introduction to the bootstrap 1993, New York: Chapman & Hall.
66. Canty A, Ripley B. boot: Bootstrap R (S-Plus) Functions. R package version 1.2-34. , http://cran.r-project.org/web/packages/boot/index.html
67. Davison AC, Hinkley DV. Bootstrap methods and their applications 1997, Cambridge (UK): Cambridge University Press.
68. QuantumSoft, Inc. pro Fit 6.1 User Manual. QuantumSoft, Inc.., http://quansoft.com/manual/proFit_61_Handbook.pdf
69. van Kampen NG. Stochastic processes in physics and chemistry 1992, Amsterdam: Elsevier, 2.
70. Abramowitz M, Stegun IA. Handbook of mathematical functions with formulas, graphs, and mathematical tables, ninth Dover printing, tenth GPO printing 1964, New York: Dover.
71. Press WH, Flannery BP, Teukolsky SA, Vetterling WT. Numerical Recipes: The art of scientific computing 2007, Cambridge (UK) and New York: Cambridge University Press, 3.
72. Moré JJ, Garbow BS, Hillstrom KE. User Guide for MINPACK-1. Tech. Rep. ANL-80-74 1980, Argonne, IL, USA Argonne National Laboratory.
73. Jones E, Oliphant T, Peterson P, et al. SciPy: Open source scientific tools for Python. , http://www.scipy.org