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Arabidopsis floral buds are locked through stress-induced sepal tip curving

Nature Plants volume 10, pages 1258–1266 (2024)Cite this article

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Abstract

In most plant species, sepals—the outermost floral organs—provide a protective shield for reproductive organs. How the floral bud becomes sealed is unknown. In Arabidopsis, we identified a small region at the sepal tip that is markedly curved inward early on and remains curved even after anthesis. Through modelling and quantitative growth analysis, we find that this hook emerges from growth arrest at the tip at a stage when cortical microtubules align with growth-derived tensile stress. Depolymerizing microtubules specifically at young sepal tips hindered hook formation and resulted in open floral buds. Mutants with defective growth pattern at the tip failed to curve inwards, whereas mutants with enhanced alignment of cortical microtubules at the tip exhibited a stronger hook. We propose that floral buds are locked due to a stress-derived growth arrest event curving the sepal tip and forming a rigid hook early on during flower development.

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Fig. 1: Changes in sepal curvature during flower development.
Fig. 2: Regional growth conflict at the sepal tip promotes inward tip curvature.
Fig. 3: Expression pattern of pWOX1::sYFP2-PHS1ΔP and the impacts on cell growth.
Fig. 4: Altered growth pattern at the sepal tip in pWOX1:sYFP2-PHS1ΔP correlates with reduced tip curvature.

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Acknowledgements

We thank F. Zhao for the pWOX1 promoter and T. Hashimoto for the PHS1deltaP plasmid; our collaborators (A. Boudaoud, A. Roeder, D. Kwiatkowska and J. Traas) for their comments and help in this project. This work was supported by the European Research Council (ERC, Grant Agreement No. 101019515, ‘Musix’), CEFIPRA (grant 6103-1), and the French National Research Agency through a European ERA-NET Coordinating Action in Plant Sciences (ERA-CAPS) grant (Grant No. ANR-17-CAPS-0002-01). R.S.S. was supported by a Biotechnological and Biological Sciences Research Council Institute Strategic Programme Grant to the John Innes Centre (BB/X01102X/1).

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Authors and Affiliations

  1. Laboratoire de Reproduction et Développement des Plantes, Université de Lyon, ENS de Lyon, UCBL, INRAE, CNRS, Lyon, France

    Duy-Chi Trinh, Isaty Melogno, Marjolaine Martin, Christophe Trehin & Olivier Hamant

  2. University of Science and Technology of Hanoi, Vietnam Academy of Science and Technology (VAST), Cau Giay, Vietnam

    Duy-Chi Trinh

  3. Department of Computational and Systems Biology, John Innes Centre, Norwich, UK

    Richard S. Smith

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Contributions

D.-C.T. and O.H. conceptualized the project. D.-C.T. and O.H. devised the methodology. D.-C.T., R.S.S. and I.M. conducted the investigation. D.-C.T. and M.M. created the materials. D.-C.T. and R.S.S. created the figures. O.H. acquired the funding. O.H. administered the project. O.H. and C.T. supervised the project. D.-C.T. and O.H. wrote the original draft of the paper. All authors read, contributed to the revision and approved the final version of the paper.

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Correspondence to Duy-Chi Trinh or Olivier Hamant.

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Extended data

Extended Data Fig. 1 Sepal arrangement, growth and rationale for using the curving score.

(A) Four sepals of the same flower, the abaxial is the largest, followed by the adaxial, and the lateral sepals are smaller. (B) Sepal arrangement seals the flower bud. The adaxial sepal overlaps with one side of the lateral sepal, and the abaxial overlaps with the other side. The highly curved, dome-shaped tip of the abaxial covers the tip of the three other sepals. (C) Images illustrating the temporal sequence of sepal emergence (from confocal stack maximal projection of pUBQ10:Lti6b- TdTomato flowers). The abaxial sepal initiates first, followed by the adaxial, then by the two lateral ones. (D) Rationale for the curving score, defined as the aspect ratio of the bounding box, as a proxy for sepal curvature. In scenario #1, the shapes are simply homothetic deformations from the original shape. In scenario #2, axial growth is larger than lateral growth. In scenario #3, axial growth is lower than lateral growth. Scenario #4 mixes periods where axial and lateral growth dominate alternatively. The bounding box of the curved shape is illustrated in #1, with a red rectangle. Measured curvature and curving score on these artificial templates are plotted in panels (E) and (F). (E) Average curvature k of artificial shapes at stages 1 to 8 in the four scenarios, measured as k = 1/R, with R being the radius of a circle that best fit the shape contour. k does not reflect drastic differences in curvature, despite the obvious differences in shape (panel D), especially at early stage. Therefore, we did not use this parameter to characterize changes in sepal curving. (F) Curving score (aspect ratio width/length of the box bounding the artificial shapes) at stages 1 to 8 in the four scenarios. This parameter better captures and discriminates the changes in curvature. The differences when the shapes become more curved or flatter are evident, in contrast to (E). (G) Average curvature k = 1/R of the abaxial sepals for all 39 flower buds from a representative inflorescence from young to old. As the sepals grow, the radius R of the best fit circle keeps increasing, hence the curvature keeps decreasing. (H) Curving scores of abaxial sepals of all floral buds of another inflorescence. Note the transient increase in the score during early floral development.

Extended Data Fig. 2 Analyses of sepal curvature on WT sepals.

(A) An example of a WT sepals growing over seven days. Top panel: correct sepal lengths. Bottom panel: the sepals are normalized so that they all have the same length of 500 µm (arbitrary length). (B-D) Measurement of curvature defined as 1/R (µm-1), with R being the radius of the best fit circle, for normal sepals (B), or normalized sepals (C), and measurement of the curving score defined as the width/length ratio of the box bounding the sepal (D). Top panel: for individual samples; bottom panel: the average. Data are presented as mean values ± SD. 2-sided Student’s t-test. (E) Similar to Figure B, top panel, but the sepal curvature is plotted against the sepal length.

Extended Data Fig. 3 Relative cell wall stiffness revealed by osmotic treatment and sepal phenotype of the kanatin mutant.

(A) A WT sepal before and after 30 min of treatment with 0.4 M NaCl solution (hyperosmotic treatment); propidium iodide staining. The treatment induced tissue shrinkage. Note that some cells of the adaxial sepals are visible but are not taken into account for the analysis. Scale bar = 20 µm. (B) Side view of the sepal in (A) to show that this sepal is similar to those about to experience a significant increase in sepal curving, as in Day3-Day4 in Extended Data Fig. 2d. Scale bar = 20 µm. (C) Heat map showing relative reduction in area of regions of cells in the sepal in (A) after treated with salt solution. Higher values mean greater reduction in area, indicating softer cell walls, and vice versa. Scale bar = 10 µm. (D) Data in (C) plotted as a function of cell distance relative to the tip end, showing that cell regions near the tip experienced less reduction in area after hyperosmotic treatment, hence stiffer cell walls. (E) Statistical test of reduction in area of four group of cell regions along the sepal proximo-distal axis: from 20-40% (near the base), 40-60%, 60-80% and 80-100% (tip). It confirms that the tip region (80-100%) experienced less reduction in area after hyperosmotic treatment compared to other regions. Boxplot centres depict the median while the bottom and top box limits depict the 25th and 75th percentile, respectively. Whiskers represent minima and maxima. 2-sided Student’s t-test. (F-G) Heatmaps similar to (E) but for two other sepals, both showing that the tip is stiffer than other regions. (H) Flower and sepal phenotype of the katanin mutant (mad5). The flowers open early and the sepals are not highly curved at the tip to form the sepal hook. Scale bars = 0.1 mm.

Extended Data Fig. 4 Impacts of pWOX1::sYFP2-PHS1ΔP on cell growth in the sepal.

(A) Images of a WT sepal growing over three days, showing both the microtubule reporter (pPDF1:mCitrin-MBD in green) and membrane marker (UBQ10:Lti6b-tdTomato in magenta). (B) Same as (A), but for pWOX1::sYFP2-PHS1ΔP. The arrows indicate cells without cortical microtubules, and they become larger. (C-D) Close-up image of the WT and mutant tips showing that microtubules are present in WT cells but completely depolymerized in some mutant cells (arrow). (E) Growth rate (time) of cells in the WT sepal over three days. Note that cells at the tip grow at similar rates. (F) Growth rate (time) of cells in the mutant sepal over three days. Note that cells without cortical microtubules at the tip (arrows; the same cells in Extended Data Fig. 4b) grow at much higher rates than their neighbors, especially at Day2-3. (G) Cell area (μm2) of the WT sepal (shown in (A) over 3 days. Note that cells at the tip are among the smallest. (H) Same as (G), but for the pWOX1::sYFP2-PHS1ΔP sepal (shown in (B)). Note that cells at the tip are among the largest (arrows; the same cells in Extended Data Fig. 4b,f).

Extended Data Fig. 5 Mapping cell growth rate along the base-tip axis.

(A) Heat map showing growth rate (times) of the WT sepal from Fig. 4a, Day5-6. (B) Heat map showing the distance in µm of all the cells in the sepal in (A), Day5-6, starting from the base. (C) From (A) and (B), growth rate of all the cells can be mapped according to their distance relative to the tip. A cell with a distance ~ 100% means that it is near the tip of the sepal. Focusing on the tip, it illustrates that in the period of Day5-6, cells at the tip of the pWOX1::sYFP2-PHS1ΔP grew faster than those in the WT.

Extended Data Fig. 6 Impacts of pWOX1::sYFP2-PHS1ΔP on cell growth along the margin and in the inner (adaxial) side.

(A-B; the middle row) Confocal images of the inner side of a WT and a pWOX1::sYFP2-PHS1ΔP sepal. (C-D) Close-up of the areas in green in A-B to show cells along the margin. One cell in D is lager, probably due to the impact of PHS1ΔP there (green arrow). (E-F) Close-up images of the areas in yellow containing the sepal tip and adjacent regions. In pWOX1::sYFP2-PHS1ΔP sepals, giant cells appear only at the tip (yellow arrows).

Extended Data Fig. 7 The impacts of pWOX1::sYFP2-PHS1ΔP to final sepal phenotype and the early development of xxt1 xxt2 sepals.

(A) Mature sepals of WT, pWOX1::sYFP2-PHS1ΔP line #1 and #2, and of the double mutant xxt1 xxt2. (B) Sepal length, width and aspect ratio W/L (width/length) of the four genotypes. pWOX1::sYFP2-PHS1ΔP sepals are slightly shorter (~ 15%) and wider (< 5%). They and xxt1 xxt2 plants prodce sepals with a similar increase in the aspect ratio W/L. n = 20, 30, 30, 20 sepals for WT, PHS1dP #1, #2 and xxt1 xxt2, respectively. Boxplot centres depict the median while the bottom and top box limits depict the 25th and 75th percentile, respectively. Whiskers represent minima and maxima. 2-sided Student’s t-test. NS: not significant. (C) xxt1 xxt2 sepals can form the hook, similar to WT ones (compare to Fig. 2a). (D) Correlating growth pattern and curving of xxt1 xxt2 sepals, similar to Fig. 2d and Fig. 4a. The increase in inward curving of the sepal is also associated with a drop in growth rate at the tip. A similar pattern of growth and curving was observed in 3 independent sepals.

Extended Data Fig. 8 Enhanced microtubule dynamics in the spiral 2 (spr2) mutant strengthens floral closure.

(A) Side view of a WT flower at anthesis. (B) Side view of a spr2 flower at anthesis. Note that the sepals are still linked together while the inner organs are strongly deformed as they grow under such steric constraint. (C) Top view of spr2 flower from panel (B) showing the interlocked sepal tip. (D) Another spr2 flower with comparable phenotype to (B). The arrows point to the deformed siliques. These two flowers were observed in 11 plants. We never observed a flower with such phenotype in the WT. (E) spr2 floral buds at earlier stages (yellow stars): note how petals start to grow out of the floral bud, while the sepals remain interlocked. Note that we never observed sepal twisting in spr2 in our growth conditions. Yet, we cannot exclude a minor contribution of twisting to floral closure in other growth conditions.

Extended Data Fig. 9 Sepals of the mutant vip3-1 with defective growth pattern show weak inward curving.

(A) Correlating growth pattern and sepal curving in WT sepals. The same images as in Fig. 2d, reproducing here as a control for the mutant. Note that when the tip stops growing but the sepal body grows fast, there is a jump in sepal curving. Adapted from1. (B) The same as (A), but for two vip3-1 sepals. Note that from Day3-Day6, there is not a sharp difference in growth rate between the tip and the body, and in Day6-7 the tip of the mutant sepals does not stop growing properly, and the sepals do not significantly curve inwards. The two vip3-1 sepal examples are different (overall shape, jagged vs. not jagged tip), but they exhibit comparable defect in their growth pattern (late reactivation of tip growth). (C) Quantification of the curving score (aspect ratio width/length of the box bounding the sepal contour as viewed from the side) in the WT. (D) The same as (C) but for vip3-1 sepals. (E) The average of (C) and (D) showing the difference in sepal curving scores between WT and the mutant. nWT = 4, nvip3-1 = 5 independent sepals. Data are presented as mean values ± SD. Asterisks indicate level of statistical significance: ** p ≤ 0.01, *** p ≤ 0.001. 2-sided Student’s t-test.

Supplementary information

Supplementary Information

Supplementary Fig. 1, Material and Methods, and references.

Reporting Summary

Supplementary Video 1

We generated a finite element method (FEM) simulation of a growing, curved sepal experiencing growth arrest at the tip. Simulations were performed in the MorphoMechanX simulation framework26. We started with a section of a sphere to approximate the shape and size of a sepal at stage 3. This was then extruded to create volumetric wedge (6 node) elements, to which we assigned isotropic, uniform material properties. Anisotropic growth was assigned to be three times greater in the longitudinal direction versus the transverse direction. Growth arrest was simulated by reducing the growth rate by half on a selection of elements at the tip, representing the arrest zone seen in planta. The template was then grown, and the conflict caused by reduced growth at the tip caused it to bend inwards as seen experimentally.

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Trinh, DC., Melogno, I., Martin, M. et al. Arabidopsis floral buds are locked through stress-induced sepal tip curving. Nat. Plants 10, 1258–1266 (2024). https://doi.org/10.1038/s41477-024-01760-6

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