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Phyllotaxis: from classical knowledge to molecular genetics

Abstract

Plant organs are repetitively generated at the shoot apical meristem (SAM) in recognizable patterns. This phenomenon, known as phyllotaxis, has long fascinated scientists from different disciplines. While we have an enriched body of knowledge on phyllotactic patterns, parameters, and transitions, only in the past 20 years, however, have we started to identify genes and elucidate genetic pathways that involved in phyllotaxis. In this review, I first summarize the classical knowledge of phyllotaxis from a morphological perspective. I then discuss recent advances in the regulation of phyllotaxis, from a molecular genetics perspective. I show that the morphological beauty of phyllotaxis we appreciate is the manifestation of many regulators, in addition to the critical role of auxin as a patterning signal, exerting their respective effects in a coordinated fashion either directly or indirectly in the SAM.

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Fig. 4

Modified from Douady and Couder (1996b) with permission from Elsevier. d divergence angle formed by primordia 1 and 2, R0 radius of the shoot apical meristem (SAM), r1 distance from primordium 1 to the center of the SAM, r2: distance from primordium 2 to the center of the SAM, ψ/2 half conic angle

Fig. 5
Fig. 6

Modified from Reinhardt et al. (2003) with permission from Springer Nature. c Auxin distribution in Arabidopsis inflorescence meristem visualized by DII-VENUS (green, absence of auxin). Inset: overlay with autofluorescence signal (red). Reprinted from Vernoux et al. (2011). d Simulated SAM exhibiting a spiral pattern. Higher to lower auxin concentration is indicated by brighter to darker green. PIN1 localization is indicated by red. Reprinted from Smith et al. (2006), copyright (2006) National Academy of Sciences. e, f Conceptual model of polar auxin transport determining the position of organ formation. Auxin is transported acropetally toward the SAM (e) and accumulates in young primordia (f) under the guidance of polarly localized PIN1 (light blue). Polar auxin transport is indicated by blue arrows. Auxin transport from inner cells to the epidermal cells is indicated by green arrows. Auxin gradient is indicated by red. Insets: depicted area in the SAM. Modified from Reinhardt (2005) with permission from Elsevier. I incipient primordia, P visible primordia, SAM shoot apical meristem

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Acknowledgements

I thank Prof. Denis Barabé, Prof. Jun-Ichi Itoh, Prof. Christian Lacroix, Prof. Munetaka Sugiyama, Dr. Teva Vernoux, and two anonymous reviewers for their valuable comments and suggestions. I also thank Prof. Christian Lacroix, Prof. Kiyotaka Okada, Prof. Beata Zagórska-Marek, and Dr. Teng Zhang for providing figures and Prof. Hirokazu Tsukaya for plant identification.

Funding

This work is supported by Japan Society for the Promotion of Science Postdoctoral Fellowship for Research in Japan (Grant No. P19085).

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Xiaofeng Yin is a co-organizer of the JPR International Symposium “Beyond Fibonacci patterns and the golden angle: phyllotactic variations and their cellular origin” held during the 83th Annual Meeting of Botanical Society of Japan.

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Yin, X. Phyllotaxis: from classical knowledge to molecular genetics. J Plant Res 134, 373–401 (2021). https://doi.org/10.1007/s10265-020-01247-3

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Keywords

  • Auxin
  • Divergence angle
  • Pattern formation
  • Phyllotaxis
  • Plastochron
  • Shoot apical meristem (SAM)