Cytokinin signalling inhibitory fields provide robustness to phyllotaxis

Besnard, Fabrice; Refahi, Yassin; Morin, Valérie; Marteaux, Benjamin; Brunoud, Géraldine; Chambrier, Pierre; Rozier, Frédérique; Mirabet, Vincent; Legrand, Jonathan; Lainé, Stéphanie; Thévenon, Emmanuel; Farcot, Etienne; Cellier, Coralie; Das, Pradeep; Bishopp, Anthony; Dumas, Renaud; Parcy, François; Helariutta, Yrjö; Boudaoud, Arezki; Godin, Christophe; Traas, Jan; Guédon, Yann; Vernoux, Teva

doi:10.1038/nature12791

Cited by 235 publications

(298 citation statements)

References 54 publications

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“…S9, and Table S1) (32). Similar to leaf polarity, a recent report found that not one, but two, independent signaling mechanisms define phyllotaxis, the spatiotemporal pattern of leaves initiation at the meristem, leading to increased precision (46).…”

Section: Discussionmentioning

confidence: 92%

Auxin depletion from leaf primordia contributes to organ patterning

Wang

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

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107

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Stem cells are responsible for organogenesis, but it is largely unknown whether and how information from stem cells acts to direct organ patterning after organ primordia are formed. It has long been proposed that the stem cells at the plant shoot apex produce a signal, which promotes leaf adaxial-abaxial (dorsoventral) patterning. Here we show the existence of a transient low auxin zone in the adaxial domain of early leaf primordia. We also demonstrate that this adaxial low auxin domain contributes to leaf adaxial-abaxial patterning. The auxin signal is mediated by the auxin-responsive transcription factor MONOPTEROS (MP), whose constitutive activation in the adaxial domain promotes abaxial cell fate. Furthermore, we show that auxin flow from emerging leaf primordia to the shoot apical meristem establishes the low auxin zone, and that this auxin flow contributes to leaf polarity. Our results provide an explanation for the hypothetical meristem-derived leaf polarity signal. Opposite to the original proposal, instead of a signal derived from the meristem, we show that a signaling molecule is departing from the primordium to the meristem to promote robustness in leaf patterning. Extensive molecular genetic studies of more than a decade have identified a transcriptional regulatory network containing several adaxially or abaxially expressed leaf abaxial-and adaxialpromoting genes (1-6). These genes encode transcription factors and small RNAs, and their domain-specific expression patterns are required for adaxial-abaxial asymmetric cell differentiation and lamina expansion. Regulatory genes expressed in the abaxial domain suppress those expressed in the adaxial domain and vice versa. MicroRNAs 165 and 166 (MiR165/166) and transcription factor-encoding KANADI (KAN) genes are expressed in the abaxial domain and restrict the expression of class III homeo-

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Section: Discussionmentioning

confidence: 92%

Auxin depletion from leaf primordia contributes to organ patterning

Wang

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

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107

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“…The consequence of the auxin model [53,54] is that the new primordium at the shoot apex is initiated where the auxin concentration is sufficiently high. The possibility of modulating auxin concentrations by cytokinins and controlled expression of the genes such as PLETHORA or INDETERMINATE DOMAIN involved in auxin biosynthesis, transport and degradation is now being intensely studied [50,[66][67][68][69]. The area between adjacent inhibitory fields corresponds to Snow and Snow's first available space.…”

Section: Discussionmentioning

confidence: 99%

“…Ongoing quest for the mechanisms of robustness in phyllotaxis in experimental plant biology [49,50] is heavily affected by the fact of relative stability of the main Fibonacci in a model plant Arabidopsis thaliana. The major challenge then is to find out the level of noise that guarantees maintenance of the pattern.…”

Section: Discussionmentioning

confidence: 99%

The significance of γ-and λ-dislocations in transient states of phyllotaxis: how to get more from less – sometimes!

Zagórska‐Marek

Szpak

2016

Acta Soc Bot Pol

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In some plants, developmental changes of phyllotaxis are so frequent that the whole spectrum of phyllotactic patterns becomes available for investigation and thus many unknown subtleties of phyllotaxis come to light. Among these, Magnolia acuminata is the most prominent. In a series of experiments performed in silico with application of a simple geometric model of phyllotaxis, we were able to confront the empirical data on phyllotactic transitions occurring in magnolia flowers with the results of computer simulations. They revealed that in addition to the ratio between the sizes of plant organs, the history of developing pattern was also important, especially for the direction of ontogenetic changes. The parameters of size tolerance and vertical tolerance in positioning a new element in the first available space, brought the effects of simulations closer to the real patterns. They helped especially to resolve the enigma of multiplication of parastichies (γ-dislocations) observed sometimes during determined growth of magnolia floral axes. We conclude that ontogenetic changes in phyllotaxis result mainly from changing sizes of organs in the course of development and that the changes do not always occur with mathematical accuracy.

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“…Cytokinin signaling peaks in two bisymmetric procambial cell files, where it regulates the localization of PINFORMED (PIN) auxin efflux carriers and creates an auxin maximum in the adjacent xylem axis. Auxin signaling in turn promotes the expression of the negative regulator of cytokinin signaling AHP6 by ARF5 (Besnard et al, 2014). This mutually exclusive pattern of cytokinin and auxin is required for the specification of the bisymmetric vascular pattern (Bishopp et al, 2011).…”

Section: Mutually Exclusive Distribution Pattern Of Cytokinin and Auxmentioning

confidence: 99%

Type-B ARABIDOPSIS RESPONSE REGULATORs Specify the Shoot Stem Cell Niche by Dual Regulation of WUSCHEL

et al. 2017

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ORCID IDs: 0000-0003-3103-8629 (W.J.M.); 0000-0002-3129-5206 (X.S.Z.)Plants are known for their capacity to regenerate the whole body through de novo formation of apical meristems from a mass of proliferating cells named callus. Exogenous cytokinin and auxin determine cell fate for the establishment of the stem cell niche, which is the vital step of shoot regeneration, but the underlying mechanisms remain unclear. Here, we show that type-B ARABIDOPSIS RESPONSE REGULATORs (ARRs), critical components of cytokinin signaling, activate the transcription of WUSCHEL (WUS), which encodes a key regulator for maintaining stem cells. In parallel, type-B ARRs inhibit auxin accumulation by repressing the expression of YUCCAs, which encode a key enzyme for auxin biosynthesis, indirectly promoting WUS induction. Both pathways are essential for de novo regeneration of the shoot stem cell niche. In addition, the dual regulation of type-B ARRs on WUS transcription is required for the maintenance of the shoot apical meristem in planta. Thus, our results reveal a long-standing missing link between cytokinin signaling and WUS regulator, and the findings provide critical information for understanding cell fate specification.

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Cytokinin signalling inhibitory fields provide robustness to phyllotaxis

Cited by 235 publications

References 54 publications

Auxin depletion from leaf primordia contributes to organ patterning

Auxin depletion from leaf primordia contributes to organ patterning

The significance of γ-and λ-dislocations in transient states of phyllotaxis: how to get more from less – sometimes!

Type-B ARABIDOPSIS RESPONSE REGULATORs Specify the Shoot Stem Cell Niche by Dual Regulation of WUSCHEL

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