Acacia (wattle) and Cananga (ylang-ylang): from spiral to whorled and irregular (chaotic) phyllotactic patterns - a pictorial report

• Autorzy: Rutishauser R.
• Języki publikacji: EN

Abstrakty

EN

Phyllotaxis, i.e., the arrangement of leaves around the stem and leaf-like organs inside flowers is regular in most vascular plants. Thus, developmental models usually explain regular phyllotactic patterns such as Fibonacci spirals and decussate/whorled patterns that obey Hofmeister’s rule: primordia form as far away as possible from previously initiated primordia. However, flowering plants showing at first Fibonacci spirals or whorled phyllotaxes may switch to other patterns that lack an obvious order and thus may be called irregular or even chaotic. Vegetative shoot tips of various Australian wattles (Acacia spp., Leguminosae in eudicots) and flower buds of ylang-ylang (Cananga odorata) and other Annonaceae (basal angiosperms) provide examples of irregular patterning. This pictorial report provides food for thought for scientists interested in phyllotaxis patterns beyond the usual spiral and whorled patterns. Emphasis is given on irregular phyllotaxes that occur in wild-type plants, mainly correlated with geometrical parameters such as leaf and stamen primordia that are very small as compared to the size of their apical meristems. They call for additional explanatory models, combining auxin-driven development with geometrical constraints and biophysical processes.

• Wydawca: -
• Czasopismo: Acta Societatis Botanicorum Poloniae
• Rocznik: 2016
• Tom: 85
• Numer: 4
• Opis fizyczny: Article 3531 [15p.], fig.,ref.

Twórcy

autor

Rutishauser R.

• Institute of Systematic and Evolutionary Botany (ISEB), University of Zurich, Zollikerstrasse 107, 8008 Zurich, Switzerland

Bibliografia

• 1. Reinhardt D, Pesce ER, Stieger P, Mandel T, Baltensperger K, Bennett M, et al. Regulation of phyllotaxis by polar auxin transport. Nature. 2003;426:255–260. https://doi.org/10.1038/nature02081
• 2. Smith RS, Kuhlemeier C, Prusinkiewicz P. Inhibition fields for phyllotactic pattern formation: a simulation study. Can J Bot. 2006;84:1635–1649. https://doi.org/10.1139/b06-133
• 3. Lee B, Johnston R, Yang Y, Gallavotti A, Kojima M, Travençolo BAN, et al. Studies of aberrant phyllotaxy1 mutants of maize indicate complex interactions between auxin and cytokinin signaling in the shoot apical meristem. Plant Physiol. 2009;150:205–216. https://doi.org/10.1104/pp.109.137034
• 4. Bainbridge K, Guyomarc’h S, Bayer E, Swarup R, Bennett M, Mandel T, et al. Auxin influx carriers stabilize phyllotactic patterning. Genes Dev. 2008;22:810–823. https://doi.org/10.1101/gad.462608
• 5. Richards FJ. Phyllotaxis: its quantitative expression and relation to growth in the apex. Philos Trans R Soc Lond B Biol Sci. 1951;235:509–563. https://doi.org/10.1098/rstb.1951.0007
• 6. Williams RF. The shoot apex and leaf growth: a study in quantitative biology. Cambridge: Cambridge University Press; 1975. https://doi.org/10.1017/CBO9780511753404
• 7. Rutishauser R. Plastochrone ratio and leaf arc as parameters of a quantitative phyllotaxis analysis in vascular plants. In: Jean RV, Barabé D, editors. Symmetry in plants. Singapore: World Scientific Press; 1998. p. 171–212. https://doi.org/10.1142/9789814261074_0008
• 8. Endress PK. Angiosperm floral evolution: morphological developmental framework. In: Soltis DE, Leebens-Mack JH, Soltis PS, editors. Developmental genetics of the flower. Amsterdam: Elsevier; 2006. p. 2–62. (Advances in Botanical Research; vol 44). https://doi.org/10.1016/s0065-2296(06)44001-5
• 9. Endress PK, Doyle JA. Floral phyllotaxis in basal angiosperms: development and evolution. Curr Opin Plant Biol. 2007;10:52–57. https://doi.org/10.1016/j.pbi.2006.11.007
• 10. Endress PK, Armstrong JE. Floral development and floral phyllotaxis in Anaxagorea (Annonaceae). Ann Bot. 2011;108:835–845. https://doi.org/10.1093/aob/mcr201
• 11. Rutishauser R, Sattler R. Architecture and development of the phyllode-stipule whorls in Acacia longipedunculata: controversial interpretations and continuum approach. Can J Bot. 1986;64:1987–2019. https://doi.org/10.1139/b86-263
• 12. Sattler R, Luckert D, Rutishauser R. Symmetry in plants: phyllode and stipule development in Acacia longipedunculata. Can J Bot. 1988;66:1270–1284. https://doi.org/10.1139/b88-182
• 13. Rutishauser R. Polymerous leaf whorls in vascular plants: developmental morphology and fuzziness or organ identities. Int J Plant Sci. 1999;160(6 suppl):S81–S103. https://doi.org/10.1086/314221
• 14. Rutishauser R, Isler B. Fuzzy Arberian morphology: Utricularia, developmental mosaics, partial shoot hypothesis of the leaf and other FAMous ideas of Agnes Arber (1879–1960) on vascular plant bauplans. Ann Bot. 2001;88:1173–1202. https://doi.org/10.1006/anbo.2001.1498
• 15. Rutishauser R, Grob V, Pfeifer E. Plants are used to having identity crises. In: Minelli A, Fusco G, editors. Evolving pathways: key themes in evolutionary developmental biology. Cambridge: Cambridge University Press; 2008. p. 194–213. https://doi.org/10.1017/CBO9780511541582.015
• 16. Rutishauser R. Phyllotactic patterns in phyllodinous acacias (Acacia subg. Heterophyllum): promising aspects for systematics. Bulletin of the International Group for the Study of Mimosoideae. 1986;14:77–108.
• 17. Maslin BR. Synoptic overview of Acacia sensu lato (Leguminosae: Mimosoideae) in East and Southeast Asia. Gardens’ Bulletin Singapore. 2015;67:231–250. https://doi.org/10.3850/S2382581215000186
• 18. Murphy DJ, Brown GK, Miller JT, Ladiges PY. Molecular phylogeny of Acacia Mill. (Mimosoideae: Leguminosae): evidence for major clades and informal classification. Taxon. 2010;59(1):7–19.
• 19. Kaplan DR. Heteroblastic leaf development in Acacia: morphological and morphogenetic implications. Cellule. 1980;73:135–203.
• 20. Hatt C, Mankessi F, Durand JB, Boudon F, Montes F, Lartaud M, et al. Characteristics of Acacia mangium shoot apical meristems in natural and in vitro conditions in relation to heteroblasty. Trees. 2012;26(3):1031–1044. https://doi.org/10.1007/s00468-012-0680-0
• 21. Kaplan DR. The concept of homology and its central role in the elucidation of plant systematic relationships. In: Duncan T, Stuessy TF, editors. Cladistics: perspectives on the reconstruction of evolutionary history. New York, NY: Columbia University Press; 1984. p. 51–70.
• 22. Simmons M. Acacias of Australia. Melbourne: Nelson; 1981.
• 23. Gardner S, Drinnan A, Newbigin E, Ladiges P. Leaf ontogeny and morphology in Acacia Mill. Muelleria. 2008;26:43–50.
• 24. World Wide Wattle. Species gallery [Internet]. 2016 [cited 2016 Dec 26]. Available from: http://worldwidewattle.com/speciesgallery
• 25. Pedley L. A revision of Acacia lycopodiifolia A. Cunn. ex Hook. and its allies. Contributions from the Queensland Herbarium. 1972;11:1–23.
• 26. Kirchoff BK. Shape matters: Hofmeister’s rule, primordium shape, and flower orientation. Int J Plant Sci. 2003;164(4):505–517. https://doi.org/10.1086/375421
• 27. Goebel K. Organographie der Pflanzen, insbesondere der Archegoniaten und Samenpflanzen. Vol. 1. 3rd ed. Jena: Fischer; 1928.
• 28. Braun A. Vergleichende Untersuchung über die Ordnung der Schuppen an den Tannenzapfen. Nova acta Academiae Caesareae Leopoldino-Carolinae. 1831;15:195–402. https://doi.org/10.5962/bhl.title.69200
• 29. Hofmeister W. Allgemeine Morphologie der Gewächse. Leipzig: W. Engelmann; 1868.
• 30. Dormer KJ. Some examples of correlation between stipules and lateral leaf traces. New Phytol. 1944;43:151–153. https://doi.org/10.1111/j.1469-8137.1944.tb05010.x
• 31. Pedley L. A revision of Acacia Mill. in Queensland. Austrobaileya. 1978;1(2):75–234.
• 32. Pedley L. A revision of Acacia Mill. in Queensland. Austrobaileya 1979;1(3):235–337.
• 33. Mishler BD, Knerr N, González-Orozco CE, Thornhill AH, Laffan SW, Miller JT. Phylogenetic measures of biodiversity and neo- and paleo-endemism in Australian Acacia. Nature Commun. 2014;5:4473. https://doi.org/10.1038/ncomms5473
• 34. Thiv M, Ghogue JP, Grob V, Huber K, Pfeifer E, Rutishauser R. How to get off the mismatch at the generic rank in African Podostemaceae? Plant Syst Evol. 2009;283:57–77. https://doi.org/10.1007/s00606-009-0214-4
• 35. Leins P, Erbar C. Early floral developmental studies in Annonaceae. Biosystematics and Ecology Series. 1996;10:1–27.
• 36. Erbar C, Leins P. Flowers in Magnoliidae and the origin of flowers in other subclasses of the angiosperms. I. The relationships between flowers of Magnoliidae and Alismatidae. Plant Syst Evol. 1994;8(suppl):193–208. https://doi.org/10.1007/978-3-7091-6910-0_12
• 37. Endress PK. The flowers in extant basal angiosperms and inferences on ancestral flowers. Int J Plant Sci. 2001;162(5):1111–1140. https://doi.org/10.1086/321919
• 38. Ronse Decraene LP, Smets E. The floral development of Popowia whitei (Annonaceae). Nord J Bot. 1990;10:411–420. https://doi.org/10.1111/j.1756-1051.1990.tb01781.x
• 39. Ronse Decraene LP, Smets E. Correction. Nord J Bot. 1991;11:420. https://doi.org/10.1111/j.1756-1051.1991.tb01238.x
• 40. Ronse Decraene LP, Smets E. The distribution and systematic relevance of the androecial character polymery. Bot J Linn Soc. 1993;113:285–350. https://doi.org/10.1111/j.1095-8339.1993.tb00341.x
• 41. Zagórska-Marek B. Phyllotaxic diversity in Magnolia flowers. Acta Soc Bot Pol. 1994;63:117–137. https://doi.org/10.5586/asbp.1994.017
• 42. Zagórska-Marek B, Szpak M. Virtual phyllotaxis and real plant model cases. Funct Plant Biol. 2008;35(10):1025–1033. https://doi.org/10.1071/FP08076
• 43. Wiss D, Zagórska-Marek B. Geometric parameters of the apical meristem and the quality of phyllotactic patterns in Magnolia flowers. Acta Soc Bot Pol. 2012;81:203–216. https://doi.org/10.5586/asbp.2012.029
• 44. Staedler YM, Endress PK. Diversity and lability of floral phyllotaxis in the pluricarpellate families of core Laurales (Gomortegaceae, Atherospermataceae, Siparunaceae, Monimiaceae). Int J Plant Sci. 2009;170:522–550. https://doi.org/10.1086/597272
• 45. Staedler YM, Weston PH, Endress PK. Floral phyllotaxis and floral architecture in Calycanthaceae. Int J Plant Sci. 2007;168(3):285–306. https://doi.org/10.1086/510417
• 46. Endress PK. Floral phyllotaxis and floral evolution. Botanische Jahrbücher für Systematik. 1987;108:417–438.
• 47. Endress PK. Chaotic floral phyllotaxis and reduced perianth in Achlys (Berberidaceae). Bot Acta. 1989;102:159–163. https://doi.org/10.1111/j.1438-8677.1989.tb00085.x
• 48. Besnard F, Refahi Y, Morin V, Marteaux B, Brunoud G, Chambrier P. et al. Cytokinin signalling inhibitory fields provide robustness to phyllotaxis. Nature. 2014;505:417–421. https://doi.org/10.1038/nature12791
• 49. Newell AC, Shipman PD, Sun Z. Phyllotaxis as an example of the symbiosis of mechanical forces and biochemical processes in living tissue. Plant Signal Behav. 2008;3(8):586–589. https://doi.org/10.4161/psb.3.8.6223
• 50. Runions A, Smith RS, Prusinkiewicz P. Computational models of auxin-driven development [Internet]. 2014 [cited 2016 Dec 26]. Available from: http://algorithmicbotany.org/papers/auxin.ARPD2014.pdf

Identyfikatory

DOI

10.5586/asbp.3531