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Auxin export from proximal fruits drives arrest in temporally competent inflorescences

Nature Plants volume 6, pages 699–707 (2020)Cite this article

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Abstract

A well-defined set of regulatory pathways control entry into the reproductive phase in flowering plants, but little is known about the mechanistic control of the end-of-flowering despite this being a critical process for optimization of fruit and seed production. Complete fruit removal, or lack of fertile fruit-set, prevents timely inflorescence arrest in Arabidopsis, leading to a previous proposal that a cumulative fruit/seed-derived signal causes simultaneous ‘global proliferative arrest’. Recent studies have suggested that inflorescence arrest involves gene expression changes in the inflorescence meristem that are, at least in part, controlled by the FRUITFULL–APETALA2 pathway; however, there is limited understanding of how this process is coordinated at the whole-plant level. Here, we provide a framework for the communication previously inferred in the global proliferative arrest model. We show that the end-of-flowering in Arabidopsis is not ‘global’ and does not occur synchronously between branches, but rather that the arrest of each inflorescence is a local process, driven by auxin export from fruit proximal to the inflorescence apex. Furthermore, we show that inflorescences are competent for arrest only once they reach a certain developmental age. Understanding the regulation of inflorescence arrest will be of major importance to extending and maximizing crop yields.

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Fig. 1: Inflorescence arrest is a temporally regulated process.
Fig. 2: Inflorescence arrest is locally regulated by fruit presence.
Fig. 3: Inflorescence duration is extended by global fruit absence.
Fig. 4: Small numbers of fruit are sufficient for local inflorescence arrest.
Fig. 5: Proximal fruit drive arrest in competent inflorescences.
Fig. 6: Auxin export from fruit triggers inflorescence arrest.

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All figures in this manuscript are associated with raw data. All data will be made available upon request.

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Acknowledgements

A.W. was supported by BBSRC DTP grant no. BB/M008770/1. K.L. and J.S. are supported by the Knut and Alice Wallenberg Foundation, the Swedish Governmental Agency for Innovation Systems and the Swedish Research Council. We thank R. Granbom for technical assistance and the Swedish Metabolomics Centre (http://www.swedishmetabolomicscentre.se/) for access to instrumentation.

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Author notes

  1. These authors contributed equally: Alexander Ware, Catriona H. Walker.

Authors and Affiliations

  1. School of Biosciences, University of Nottingham, Loughborough, UK

    Alexander Ware, Anthony Bishopp & Zoe A. Wilson

  2. School of Biology, Faculty of Biological Sciences, University of Leeds, Leeds, UK

    Catriona H. Walker, Pablo González-Suárez & Tom Bennett

  3. Department of Forest Genetics and Plant Physiology, Umeå Plant Science Centre, Swedish University of Agricultural Sciences, Umeå, Sweden

    Jan Šimura & Karin Ljung

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  1. Alexander Ware
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Contributions

C.H.W., A.W., P.G.-S., J.S. and K.L. performed experiments and analysed the data. T.B., A.B. and Z.A.W. designed the study. All authors contributed to writing the manuscript.

Corresponding authors

Correspondence to Zoe A. Wilson or Tom Bennett.

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The authors declare no competing interests.

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Peer review information Nature Plants thanks Remko Offringa and the other, anonymous, reviewers for their contribution to the peer review of this work.

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Extended data

Extended Data Fig. 1 Role of auxin transport in floral arrest.

a, Weight in milligrams of 5 fertile (Ler) or sterile (ms1-1) fruits harvested at six days post anthesis. The upper and lower confines of the box indicate the interquartile range, the central line indicates the median, and the whiskers represent the maximum and minimum values. Bars with the same letter are not statistically different from each other (two-tailed T-test, p < 0.001). b, Temporal production of flowers by the PI of male-sterile ams plants upon application of either 5 mg/g NAA in lanolin, or a mock treatment consisting of lanolin and DMSO, to the de-fruited pedicels of the top 10 fruit in ams at 23 dpa; any further fruit which were produced were also treated in the same manner. n = 12 biologically independent samples, bars indicate s.e.m. Asterisks indicate significance. c, Effect of the auxin transport mutants pin3-3 pin4-3 pin7-1 (pin347), aux1 lax1 lax2 lax3 (aux1 lax123) and smxl6-4 smxl7-1 smxl8-1 (smxl678) on primary inflorescence (PI) duration, relative to Col-0 wild-type. n = 9-12 (Col-0 n = 9, pin347 n = 10, aux1 lax123 n = 12, smxl678 n = 11). The upper and lower confines of the box indicate the interquartile range, the central line indicates the median, and the whiskers represent the maximum and minimum values. Bars with the same letter are not statistically different from each other (ANOVA, Tukey HSD test). d, Effect of subapical NPA treatment on temporal flower production in the PI of the male-sterile line ams. An approximately 1 cm region directly below the apex of the PI was either treated with NPA (0.1 mg/g) in lanolin or a mock at 12 dpa. n = 5 biologically independent samples, bars indicate s.e.m. Asterisks indicate significance as determined by Sidak’s multiple comparisons following fitting of a mixed-effects model; * = <0.05; ** = <0.01; *** = 0.001; **** = 0.0001. e, Effect of the strigolactone mutants max4-5 and d14-1 on primary inflorescence (PI) duration, relative to Col-0 wild-type. n = 8-11 biologically independent samples (Col-0 n = 8, max4-5 n = 11, d14-1 n = 8). The upper and lower confines of the box indicate the interquartile range, the central line indicates the median, and the whiskers represent the maximum and minimum values. Bars with the same letter are not statistically different from each other (ANOVA, Tukey HSD test).

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Ware, A., Walker, C.H., Šimura, J. et al. Auxin export from proximal fruits drives arrest in temporally competent inflorescences. Nat. Plants 6, 699–707 (2020). https://doi.org/10.1038/s41477-020-0661-z

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