Geometric parameters of the apical meristem and the quality of phyllotactic patterns in Magnolia flowers

• Autorzy: Wiss D. , Zagorska-Marek B.
• Języki publikacji: EN

Abstrakty

EN

The ratio of primordium size to the meristem size (P/M ratio) is regarded by some geometrical models of phyllotaxis as the parameter, which determines the quality of spiral and whorled patterns of lateral organ arrangement. This assumption was tested on floral meristems in four genets representing four Magnolia taxa: M. × salicifolia, M. stellata, M. denudata and M. acuminata. In successive zones of Magnolia flower, lateral organs are initiated in specific phyllotactic patterns and at specific values of the meristem and primordia sizes. The elements of perianth, usually positioned in three trimerous whorls, are initiated as large primordia on relatively small meristem. The switch in the identity of primordia, from tepals to stamens is accompanied by an abrupt increase in the size of the meristem and decrease in the primordia size. Small values of P/M ratio and frequent occurrence of qualitative transformations of phyllotaxis contribute to the exceptionally rich spectrum of spiral patterns in androecium zone. New spiral patterns emerge when bigger primordia of carpels are initiated on the meristem, which at the same time starts diminishing in size either abruptly (M. × salicifolia, M. stellata, M. acuminata) or slowly (M. denudata). Spiral patterns identified in gynoecia have lower numbers of parastichies than the patterns of androecia and occur in frequencies specific for the genet. Although noted ranges of the meristem and primordia sizes, justify the occurrence of phyllotactic patterns observed in successive zones of Magnolia flower, they do not explain genet-specific frequencies of the patterns observed in gynoecium zone. The lack of straightforward relationship between frequency of the patterns and P/M ratio in gynoecium suggests that more complex geometrical factors or factors of non-geometrical nature are engaged in determination of Magnolia floral phyllotaxis.

Słowa kluczowe

EN

geometrical parameter; apical meristem; quality; phyllotactic pattern; Magnolia; flower; phyllotaxis; plant development; primordium; meristem

• Wydawca: -
• Czasopismo: Acta Societatis Botanicorum Poloniae
• Rocznik: 2012
• Tom: 81
• Numer: 3
• Opis fizyczny: p.203-216,fig.,ref.

Twórcy

autor

Wiss D.

• Institute of Experimental Biology, Wroclaw University, Kanonia 6/8, 50-328 Wroclaw, Poland

autor

Zagorska-Marek B.

Bibliografia

• 1. Church AH. On the relation of phyllotaxis to mechanical laws. London: Williams & Norgate; 1904.
• 2. Richards FJ. The geometry of phyllotaxis and its origin.Symp Soc Exper Biol. 1948;2:217–245.
• 3. Richards FJ. Phyllotaxis: its quantitative expression and relation to growth in the apex. Phil Trans R Soc B. 1951;235(629):509–564. http://dx.doi.org/10.1098/ rstb.1951.0007
• 4. Richards FJ. Spatial and temporal correlations involved in leaf pattern production at the apex. In: Milthrope FL, editor. The growth of leaves. London: Butterworths; 1956. p. 66–76.
• 5. Erickson RO. The geometry in phyllotaxis. In: Dale JE, Milthorpe FL, editors. The growth and functioning of leaves: proceedings of a symposium held prior to the thirteenth International Botanical Congress at the University of Sydney, 18–20 August 1981. Cambridge: CambridgeUniversity Press; 1983. p. 53–88.
• 6. Larson PR. Development and organization of the primary vascular system in Populus deltoides according to phyllotaxy. Am J Bot. 1975;62(10):1084–1099. http://dx.doi. org/10.2307/2442125
• 7. Larson PR. Phyllotactic transitions in the vascular system of Populus deltoides Bartr. as determined by 14C labeling. Planta. 1977;134(3):241–249. http://dx.doi.org/10.1007/ BF00384188
• 8. Banasiak A, Zagórska-Marek B. Signals flowing from mature tissues to SAM determine the phyllotactic continuity in successive annual increments of the conifer shoot. Acta Soc Bot Pol. 2006;75(2):113–121.
• 9. Banasiak A. Putative dual pathway of auxin transport in organogenesis of Arabidopsis. Planta. 2011;233(1):49–61. http://dx.doi.org/10.1007/s00425-010-1280-0
• 10. Zagórska-Marek B. Phyllotactic patterns and transitions in Abies balsamea. Can J Bot. 1985;63(10):1844–1854. http:// dx.doi.org/10.1139/b85-259
• 11. Szymanowska-Pułka M. Phyllotactic patterns in capitula of Carlina acaulis L. Acta Soc Bot Pol. 1994;65(3–4):229–245. http://dx.doi.org/10.5586/asbp.2011.043
• 12. Zagórska-Marek B. Phyllotaxic diversity in Magnolia flowers. Acta Soc Bot Pol. 1994;63(2):117–137.
• 13. Endress P. Floral phyllotaxis and floral evolution. Bot Jahrb Syst. 1987;108(2–3):417–438. http://dx.doi.org/10.1016/j. pbi.2006.11.007
• 14. Tucker SC. Phyllotaxis and vascular organization of the carpels in Michelia fuscata. Am J Bot. 1961;48(1):60. http:// dx.doi.org/10.2307/2439596
• 15. Doust AN. The developmental basis of floral variation in Drimys winteri (Winteraceae). Int J Plant Sci. 2001;164(4):697–717.
• 16. Zagórska-Marek B. Phyllotaxis triangular unit: phyllotactic transitions as the consequence of apical wedge disclinations in a crystal-like pattern of the units. Acta Soc Bot Pol. 1987;56(2):229–255.
• 17. Meicenheimer RD, Zagórska-Marek B. Consideration of the geometry of the phyllotaxic triangular unit and discontinuous phyllotactic transitions. J Theor Biol. 1989;139(3):359– 368. http://dx.doi.org/10.1016/S0022-5193(89)80214-0
• 18. Gomez-Campo C. Phyllotactic patterns in Bryophyllum tubiflorum Harv. Bot Gaz. 1974;135(1):49–58.
• 19. Gola EM. Phyllotaxis diversity in Lycopodium clavatum L. and Lycopodium annotinum L. Acta Soc Bot Pol. 1996;65(3–4):235–247.
• 20. Kwiatkowska D. Intraspecific variation of phyllotaxis stability in Anagallis arvensis. Acta Soc Bot Pol. 1997;66(3–4):259–271.
• 21. Stieger PA, Reinhardt D, Kuhlemeier C. The auxin influx carrier is essential for correct leaf positioning. Plant J. 2002;32(4):509–517. http://dx.doi. org/10.1046/j.1365-313X.2002.01448.x
• 22. Reinhardt D, Pesce ER, Stieger P, Mandel T, Baltensperger K, Bennett M, et al. Regulation of phyllotaxis by polar auxin transport. Nature. 2003;426(6964):255–260. http://dx.doi. org/10.1038/nature02081
• 23. Bainbridge K, Guyomarc'h S, Bayer E, Swarup R, Bennett M, Mandel T, et al. Auxin influx carriers stabilize phyllotactic patterning. Genes Dev. 2008;22(6):810–823. http:// dx.doi.org/10.1101/gad.462608
• 24. Veen AH, Lindenmayer A. Diffusion mechanism for phyllotaxis: theoretical physico-chemical and computer study. Plant Physiol. 1977;60(1):127–139. http://dx.doi. org/10.1104/pp.60.1.127
• 25. Williams RF, Brittain EG. A geometrical model of phyllotaxis. Aust J Bot. 1984;32(1):43. http://dx.doi.org/10.1071/ BT9840043
• 26. Douady S, Couder Y. Phyllotaxis as a dynamical self organizing process part I: the spiral modes resulting from time-periodic iterations. J Theor Biol. 1996;178(3):255–273. http://dx.doi.org/10.1006/jtbi.1996.0024
• 27. Douady S, Couder Y. Phyllotaxis as a dynamical self organizing process part II: the spontaneous formation of a periodicity and the coexistence of spiral and whorled patterns. J Theor Biol. 1996;178(3):275–294. http://dx.doi. org/10.1006/jtbi.1996.0025
• 28. Douady S, Couder Y. Phyllotaxis as a dynamical self organizing process part III: the simulation of the transient regimes of ontogeny. J Theor Biol. 1996;178(3):295–312. http://dx.doi.org/10.1006/jtbi.1996.0026
• 29. Jonsson H, Heisler MG, Shapiro BE, Meyerowitz EM, Mjolsness E. An auxin-driven polarized transport model for phyllotaxis. Proc Natl Acad Sci USA. 2006;103(5):1633– 1638. http://dx.doi.org/10.1073/pnas.0509839103
• 30. Smith RS, Guyomarc'h S, Mandel T, Reinhardt D, Kuhlemeier C, Prusinkiewicz P. A plausible model of phyllotaxis. Proc Natl Acad Sci USA. 2006;103(5):1301–1306. http:// dx.doi.org/10.1073/pnas.0510457103
• 31. Zagórska-Marek B, Szpak M. Virtual phyllotaxis and real plant model cases. Funct Plant Biol. 2008;35(10):1025– 1033. http://dx.doi.org/10.1071/FP08076
• 32. Snow M, Snow R. Auxin and leaf formation. New Phytol. 1937;36(1):1–18. http://dx.doi. org/10.1111/j.1469-8137.1937.tb06899.x
• 33. Snow M, Snow R. Minimum areas and leaf determination. Proc R Soc B. 1952;139(897):545–566. http://dx.doi. org/10.1098/rspb.1952.0034
• 34. Snow M, Snow R. Regulation of sizes of leaf primordia by growing-point of stem apex. Proc R Soc B.1955;144(915):222–229. http://dx.doi.org/10.1098/ rspb.1955.0053
• 35. Lenhard M, Laux T. Stem cell homeostasis in the Arabidopsis shoot meristem is regulated by intercellular movement of CLAVATA3 and its sequestration by CLAVATA1. Development. 2003;130:3163–3173. http://dx.doi.org/10.1242/dev.00525
• 36. Sharma VK, Carles CC, Fletcher JC. Maintenance of stem cell populations in plants. Proc Natl Acad Sci USA. 2003;100(90001):11823–11829. http://dx.doi.org/10.1073/ pnas.1834206100
• 37. Zhao Y, Medrano L, Ohashi K, Fletcher JC, Yu H, Sakai H, et al. HANABA TARANU is a GATA transcription factor that regulates shoot apical meristem and flower development in Arabidopsis. Plant Cell. 2004;16(10):2586–2600. http://dx.doi.org/10.1105/tpc.104.024869
• 38. Hu Y, Xie Q, Chua NH. The Arabidopsis auxin-inducible gene ARGOS controls lateral organ size. Plant Cell. 2003;15(9):1951–1961. http://dx.doi.org/10.1105/ tpc.013557
• 39. Ori N, Eshed Y, Chuck G, Bowman JL, Hake S. Mechanisms that control knox gene expression in the Arabidopsis shoot. Development. 2000;127(24):5523–5532.
• 40. Semiarti E, Ueno Y, Tsukaya H, Iwakawa H, Machida C, Machida Y. The ASYMMETRIC LEAVES2 gene of Arabidopsis thaliana regulates formation of a symmetric lamina, establishment of venation and repression of meristem-related homeobox genes in leaves. Development.2001;128(10):1771–1783.
• 41. Autran D, Jonak C, Belcram K, Beemster GTS, Kronenberger J, Grandjean O, et al. Cell numbers and leaf development in Arabidopsis: a functional analysis of the STRUWWELPETER gene. EMBO J. 2002;21(22):6036–6049. http://dx.doi.org/10.1093/emboj/cdf614
• 42. Clay NK, Nelson T. The recessive epigenetic swellmap mutation affects the expression of two step II splicing factors required for the transcription of the cell proliferation gene STRUWWELPETER and for the timing of cell cycle arrest in the Arabidopsis leaf. Plant Cell. 2005;17(7):1994–2008.http://dx.doi.org/10.1105/tpc.105.032771
• 43. Running MP, Fletcher JC, Meyerowitz EM. The WIGGUM gene is required for proper regulation of floral meristem size in Arabidopsis. Development. 1998;125(14):2545–2553.
• 44. Song JY, Leung T, Ehler LK, Wang C, Liu Z. Regulation of meristem organization and cell division by TSO1, an Arabidopsis gene with cysteine-rich repeats. Development. 2000;127(10):2207–2217.
• 45. Hauser BA, He JQ, Park SO, Gasser CS. TSO1 is a novel protein that modulates cytokinesis and cell expansion in Arabidopsis. Development. 2000;127(10):2219–2226.
• 46. Dornelas MC, van Lammeren AA, Kreis M. Arabidopsis thaliana SHAGGY-related protein kinases (AtSK11 and 12) function in perianth and gynoecium development. Plant J. 2000;21(5):419–429. http://dx.doi. org/10.1046/j.1365-313x.2000.00691.x
• 47. Leyser HMO, Furner IJ. Characterisation of three shoot apical meristem mutants of Arabidopsis thaliana. Development. 1992;116(2):397–403.
• 48. Laufs P, Dockx J, Kronenberger J, Traas J. MGOUN1 and MGOUN2: two genes required for primordium initiation at the shoot apical and floral meristems in Arabidopsis thaliana. Development. 1998;125(7):1253–1260.
• 49. Para A, Sundås-Larsson A. The pleiotropic mutation dar1 affects plant architecture in Arabidopsis thaliana. Dev Biol. 2003;254(2):215–225. http://dx.doi.org/10.1016/ S0012-1606(02)00035-0
• 50. Xu FX. Floral ontogeny of two species in Magnolia L. J Integr Plant Biol. 2006;48(10):1197–1203. http://dx.doi. org/10.1111/j.1744-7909.2006.00341.x
• 51. Xu F, Rudall PJ. Comparative floral anatomy and ontogeny in Magnoliaceae. Plant Syst Evol. 2006;258(1–2):1–15. http://dx.doi.org/10.1007/s00606-005-0361-1
• 52. Johansen DA. Plant microtechnique. New York: McGraw- Hill Book Co.; 1940.
• 53. Leins P, Erbar C. Floral developmental studies: some old and new questions. Int J Plant Sci. 1997;158(6 suppl):3–12. http://dx.doi.org/10.1086/297504
• 54. Tucker SC. Ontogeny of the floral apex of Michelia fuscata. Am J Bot. 1960;47(4):266. http://dx.doi. org/10.2307/2439606
• 55. Lyndon RF. Phyllotaxis and the initiation of primordia during flower development in Silene. Ann Bot. 1978;42:1349–1360.
• 56. Meicenheimer RD. Relationships between shoot growth and changing phyllotaxy of Ranunculus. Am J Bot. 1979;66(5):557. http://dx.doi.org/10.2307/2442505
• 57. Uhl NW, Moore HE. Androecial development in six polyandrous genera representing five major groups of palms. Ann Bot. 1980;45(1):57–75.
• 58. Kirchoff BK. Shape matters: Hofmeister's rule, primordium shape, and flower orientation. Int J Plant Sci. 2003;164(4):505–517. http://dx.doi.org/10.1086/375421
• 59. Zagórska-Marek B, Wiss D. Dislocations in the repetitive unit patterns of biological systems. In: Nation JB, editor. Formal descriptions of developing systems. Manoa: Kluwer Academic Publishers; 2003. p. 99–117.
• 60. Zagórska-Marek B. Magnolia flower – the living crystal. Magnolia. 2011;89:11–21.
• 61. Erbar C, Leins P. Zur Spirale in Magnolien-Blüten. Beitr Biol Pflanzen. 1982;56:225–241.
• 62. Jean RV. Phyllotaxis: a systemic study in plant morphogenesis. Cambridge: Cambridge University Press; 1994.
• 63. Vakarelov I. Changes in phyllotactic pattern structure in Pinus L. due to changes in altitude. In: Jean RV, Barabé D, editors. Symmetry in plants. Singapore: World Scientific; 1998. p. 213–230.
• 64. Gola EM. Phyllotactic spectra in cacti: Mammillaria species and some genera from Rebutia group. Acta Soc Bot Pol. 1997;66(3–4):237–257.
• 65. Szpak M, Zagórska-Marek B. Phyllotaxis instability – exploring the depths of first available space. Acta Soc Bot Pol. 2011;80(4):279–284. http://dx.doi.org/10.5586/ asbp.2011.043
• 66. McCully ME, Dale HM. Variations in leaf number in Hippuris. A study of whorled phyllotaxis. Can J Bot. 1961;39(3):611–625. http://dx.doi.org/10.1139/b61-050
• 67. Bierhorst DW. Symmetry in Equisetum. Am J Bot. 1959;46(3):170. http://dx.doi.org/10.2307/2439274
• 68. Kwiatkowska D, Florek-Marwitz J. Ontogenetic variation of phyllotaxis and apex geometry in vegetative shoots of Sedum maximum (L.) Hoffm. Acta Soc Bot Pol. 1999;68(2):85–95.
• 69. Greyson RI, Walden DB. The ABPHYL syndrome in Zea mays. I. Arrangement, number and size of leaves. Am J Bot. 1972;59(5):466–472. http://dx.doi.org/10.2307/2441527
• 70. Greyson RI, Walden DB, Hume JA, Erickson RO. TheABPHYL syndrome in Zea mays. II. Patterns of leaf initiation and the shape of the shoot meristem. Can J Bot. 1978;56(13):1545–1550. http://dx.doi.org/10.1139/b78-183
• 71. Jackson D, Hake S. Control of phyllotaxy in maize by the abphyl1 gene. Development. 1999;126(2):315–323.
• 72. Lyndon RF. The shoot apical meristem: its growth and development. Cambridge: Cambridge University Press; 1998.
• 73. Carles CC, Fletcher JC. Shoot apical meristem maintenance: the art of a dynamic balance. Trends Plant Sci. 2003;8(8):394–401. http://dx.doi.org/10.1016/ S1360-1385(03)00164-X
• 74. Hernandez LF, Palmer JH. Regeneration of the sunflower capitulum after cylindrical wounding of the receptacle. Am J Bot. 1988;75(9):1253. http://dx.doi.org/10.2307/2444447
• 75. Endress P. Chaotic floral phyllotaxis and reduced perianth in Achlys (Berberidaceae). Bot Acta. 1989;102:159–163.
• 76. Lehmann NL, Sattler R. Irregular floral development in Calla palustris (Araceae) and the concept of homeosis. Am J Bot. 1992;79(10):1145. http://dx.doi.org/10.2307/2445214
• 77. Kwiatkowska D. The relationships between the primary vascular system and phyllotactic patterns of Anagallis arvensis (Primulaceae). Am J Bot. 1992;79(8):904. http://dx.doi.org/10.2307/2445001
• 78. Zagórska-Marek B, Banasiak A. Related to phyllotaxis interlocked systems of vascular sympodia and cortical resin canals in Abies and Picea shoots. Acta Soc Bot Pol. 2000;69(3):165–172.