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Giant fluctuations in strain rate as part of normal leaf growth

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Abstract

We report the effects of abrupt transitions of light intensity on the growth patterns and mechanical properties of young tobacco leaves. Changes in light intensity induce large variations in the leaf strain rate, which can be an order of magnitude larger than the average growth rates, and include both tissue expansion and shrinkage. These are accompanied by large changes in the tissue’s mechanical properties. Similar effects are observed in response to wind. We show evidence supporting the hypothesis that these effects originate from hydraulic mechanisms, i.e., variations in turgor pressure. In the context of growth patterns and growth regulation, we show giant fluctuations in strain rate to be a normal part of the growth process of leaves, which should be taken into account as a means for redistributing the stresses accumulated during the process of growth.

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References

  1. J. Elsner, M. Michalski, D. Kwiatkowska, Spatiotemporal variation of leaf epidermal cell growth: a quantitative analysis of Arabidopsis thaliana wild-type and triple cyclinD3 mutant plants. Ann. Bot. 109(5), 897–910 (2012)

    Article  Google Scholar 

  2. L. Hong et al., Heterogeneity and robustness in plant morphogenesis: from cells to organs. Annu. Rev. Plant Biol. 69(1), 469–495 (2018)

    Article  Google Scholar 

  3. M. Sahaf, E. Sharon, The rheology of a growing leaf: stress-induced changes in the mechanical properties of leaves. J. Exp. Bot. 67(18), 5509–5515 (2016)

    Article  Google Scholar 

  4. N. Hervieux et al., A mechanical feedback restricts sepal growth and shape in arabidopsis. Curr. Biol. 26(8), 1019–1028 (2016)

    Article  Google Scholar 

  5. H. Salah, F. Tardieu, Control of leaf expansion rate of droughted maize plants under fluctuating evaporative demand (a superposition of hydraulic and chemical messages?). Plant Physiol. 114(3), 893–900 (1997)

    Article  Google Scholar 

  6. J.S. Boyer, Relationship of water potential to growth of leaves. Plant Physiol. 43(7), 1056–1062 (1968)

    Article  Google Scholar 

  7. G.P. Findlay, Membranes and the electrophysiology of turgor regulation. Aust. J. Plant Physiol. 28(7), 617–634 (2001)

    Google Scholar 

  8. J.A. Lockhart, An analysis of irreversible plant cell elongation. J. Theor. Biol. 8(2), 264–275 (1965)

    Article  Google Scholar 

  9. J.H. Kroeger, R. Zerzour, A. Geitmann, Regulator or driving force? the role of Turgor pressure in oscillatory plant cell growth. PLoS ONE 6(4), e18549 (2011)

    Article  ADS  Google Scholar 

  10. J. Passioura, S. Fry, Turgor and cell expansion: beyond the Lockhart equation. Funct. Plant Biol. 19(5), 565 (1992)

    Article  Google Scholar 

  11. G.C. Whitelam, K.J. Halliday, Light and Plant Development (Blackwell Pub, Hoboken, 2007)

    Book  Google Scholar 

  12. M.L. Molas, J.Z. Kiss, Chapter 1 phototropism and gravitropism in plants. Adv. Bot. Res 49, 1–34 (2009)

    Article  Google Scholar 

  13. P.D. Cerdán, J. Chory, Regulation of flowering time by light quality. Nature 423(6942), 881–885 (2003)

    Article  ADS  Google Scholar 

  14. D. Vince-Prue, Photocontrol of stem elongation in light-grown plants of Fuchsia hybrida. Planta 133(2), 149–156 (1977)

    Article  Google Scholar 

  15. R.E. Kendrick, G.H.M. Kronenberg, Photomorphogenesis in Plants, vol. 56 (Springer, Berlin, 1994), p. 5

    Book  Google Scholar 

  16. E. de Langre, Effects of wind on plants. Annu. Rev. Fluid Mech. 40(1), 141–168 (2008)

    Article  ADS  MathSciNet  MATH  Google Scholar 

  17. M.C. Marchetti et al., Hydrodynamics of soft active matter. Rev. Mod. Phys. 85(3), 1143–1189 (2013)

    Article  ADS  Google Scholar 

  18. H. Poorter et al., A meta-analysis of plant responses to light intensity for 70 traits ranging from molecules to whole plant performance. New Phytol. 223(3), 1073–1105 (2019)

    Article  Google Scholar 

  19. Y. Onoda, F. Schieving, N.P.R. Anten, A novel method of measuring leaf epidermis and mesophyll stiffness shows the ubiquitous nature of the sandwich structure of leaf laminas in broad-leaved angiosperm species. J. Exp. Bot. 66(9), 2487–2499 (2015)

    Article  Google Scholar 

  20. C. Scoffoni, A. Pou, K. Aasamaa, L. Sack, The rapid light response of leaf hydraulic conductance: new evidence from two experimental methods. Plant, Cell Environ. 31(12), 1803–1812 (2008)

    Article  Google Scholar 

  21. W.G. Allaway, T.A. Mansfield, Stomatal responses to changes in carbon dioxide concentration in leaves treated with 3-(4-chlorophenyl)-1, 1-dimethylurea. New Phytol. 66(1), 57–63 (1967)

    Article  Google Scholar 

  22. T.D. Sharkey, K. Raschke, Effect of light quality on stomatal opening in leaves of Xanthium strumarium L. Plant Physiol. 68(5), 1170–1174 (1981)

    Article  Google Scholar 

  23. J.T.M. Elzenga, H.B.A. Prins, E. Van Volkenburgh, Light-induced membrane potential changes of epidermal and mesophyll cells in growing leaves of Pisum sativum. Planta 197(1), 127–134 (1995)

    Article  Google Scholar 

  24. M. Samejima, T. Sibaoka, Changes in the extracellular ion concentration in the main pulvinus of Mimosa pudica during rapid movement and recovery. Plant Cell Physiol. 21(3), 467–479 (1980)

    Google Scholar 

  25. K. Raschke, R. Hedrich, Simultaneous and independent effects of abscisic acid on stomata and the photosynthetic apparatus in whole leaves. Planta 163(1), 105–118 (1985)

    Article  Google Scholar 

  26. W.R. Cummins, H. Kende, K. Raschke, Specificity and reversibility of the rapid stomatal response to abscisic acid. Planta 99(4), 347–351 (1971)

    Article  Google Scholar 

  27. R.J. Jones, T.A. Mansfield, Suppression of stomatal opening in leaves treated with abscisic acid. J. Exp. Bot. 21(3), 714–719 (1970)

    Article  Google Scholar 

  28. S.M. Assmann, K.-I. Shimazaki, The multisensory guard cell. Stomatal responses to blue light and abscisic acid. Plant Physiol. 119(3), 809–816 (1999)

    Article  Google Scholar 

  29. K.A. Mott, P.J. Franks, The role of epidermal turgor in stomatal interactions following a local perturbation in humidity. Plant, Cell Environ. 24(6), 657–662 (2001)

    Article  Google Scholar 

  30. F. Darwin, Observations on stomata. Proc. R. Soc. London 63(1), 413–417 (1898)

    Google Scholar 

  31. D. Büssis, U. von Groll, J. Fisahn, T. Altmann, Stomatal aperture can compensate altered stomatal density in Arabidopsis thaliana at growth light conditions. Funct. Plant Biol. 33(11), 1037 (2006)

    Article  Google Scholar 

  32. J. Eckstein, W. Beyschlag, K.A. Mott, R.J. Ryel, Changes in photon flux can induce stomatal patchiness. Plant, Cell Environ. 19(9), 1066–1074 (1996)

    Article  Google Scholar 

  33. Y. Fu, Y. Gu, Z. Zheng, G. Wasteneys, Z. Yang, Arabidopsis interdigitating cell growth requires two antagonistic pathways with opposing action on cell morphogenesis. Cell 120(5), 687–700 (2005)

    Article  Google Scholar 

  34. A. Sapala et al., Why plants make puzzle cells, and how their shape emerges. Elife 7, e32794 (2018)

    Article  Google Scholar 

Download references

Acknowledgements

The authors would like to thank Prof. Amnon Schwartz for his enlightening comments on stomatal behavior and the “wrong way” mechanism.

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Authors and Affiliations

  1. The Racah Institute of Physics, The Hebrew University of Jerusalem, Jerusalem, Israel

    Michal Sahaf & Eran Sharon

Authors
  1. Michal Sahaf
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  2. Eran Sharon
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Corresponding author

Correspondence to Eran Sharon.

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Figure.

 1: Additional examples of light-induced changes in growth rate, shown in Fig. 2 of the main text. Three examples of the growth rate of different leaves in response to the dark–light transition (morning). Three examples of the growth rate of different leaves in response to the light–dark transition (evening). (EPS 10013 kb)

Figure.

 2: Additional examples of changes in Young’s modulus, induced by the dark–light transition, shown in Fig. 4 of the main text. (EPS 12 kb)

Figure.

 3: Histograms showing the variability of several parameters characterizing the leaf’s response to changes in light. A. Time for recovery of Young’s modulus in the dark-to-light transition. Includes 77 measurements. This is the time from the beginning of the transition and until Young’s modulus reached a steady value. B. Minimal normalized Young’s modulus during the dark-to-light transition. Decrease shown in  % of the initial value. Includes 77 measurements. This is the smallest value observed during the peak of the transition. C. Time for recovery of the negative strain rate (shrinking) during the dark-to-light transition. Includes 24 measurements. This is the time from the beginning of the response and until strain rate reached a positive value. C. Time for recovery of the increased strain rate (shrinking) during the light-to-dark transition. Includes 24 measurements. This is the time from the beginning of the transition and until the strain rate reached a steady value. (EPS 49 kb)

Figure.

 4: Additional examples of wind-induced changes in Young’s modulus, shown in Fig. 8C of the main text. (EPS 8416 kb)

Figure.

 5: The change in young’s modulus (top) and stress–strain phase (bottom) in response to dark-to-light transition follows the time in which the light was switched on. The measurement was taken on the same leaf on two subsequent days, with a 3-hour difference in the time the light was switched on. On day 1 (red open diamonds), the artificial light was switched on at ~ 20 min, synchronized with the sunrise. That was also the case on previous days (not shown). On day 2 (blue circles), the light was switched on 3 h later. In addition to the main response which occurred at ~ 200 min, a small response can be seen at ~ 60 min. This may be a circadian response, but is more likely to be a result of some natural light coming through, since the room was not completely sealed. (EPS 18 kb)

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Sahaf, M., Sharon, E. Giant fluctuations in strain rate as part of normal leaf growth. Eur. Phys. J. Plus 135, 836 (2020). https://doi.org/10.1140/epjp/s13360-020-00813-x

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