Plant Growth Regulation

, Volume 81, Issue 1, pp 63–70 | Cite as

Stomatal distribution patterns change according to leaf development and leaf water status in Salix miyabeana

  • Mario Fontana
  • Michel Labrecque
  • Alexandre Collin
  • Nicolas BélangerEmail author
Original paper


Salix is a pioneer woody plant genus characterized by a strong plasticity in leaf morphology. The aims of this paper were to determine stomatal distribution (1) in mature leaves in response to environmental conditions, and (2) during leaf development. Stomata of abaxial and adaxial faces of mature leaves of Salix miyabeana SX67 (cultivated in short rotation coppice) were analyzed at the end of summer 2012 and 2013 at six locations in Quebec, Canada. Within each site and across the two growing seasons, stomatal density of abaxial faces was diluted by an increase in area of mature leaves due to higher rainfall. For shrubs with more than one growing season, stomatal density of abaxial faces was affected by annual rainfall, independently of site, whereas leaf area was predominantly influenced by site but was also modulated in part by rainfall. The number of stomata per leaf was site-specific, independently of rainfall. These leaves were mainly hypostomatic, although those collected on shrubs during their first growing season after coppicing (i.e. with a high root:shoot ratio) were amphistomatic. Similarly, at early development stages (surface area <2.8 cm2), leaves were amphistomatic, whereas stomata on adaxial faces of larger leaves were occluded. Nevertheless, stomatal conductance of abaxial faces increased with leaf area, whereas stomatal density was best described by a quadratic relationship. This strategy allows for a maximum uptake of carbon while limiting water loss during leaf development and to adapt the morphology of mature leaves depending on moisture and site conditions.


Amphistomy Hypostomy Leaf area Conductance Stomatal density Willow 



We gratefully thank Jacinthe Ricard-Piché for her help in the field and laboratory. We also thank Youssef Chebli and Louise Pelletier for their support to acquire microscope images. Financial support for this project was provided by the Fonds de recherche du Québec—Nature et technologies—Programme de recherche en partenariat contribuant à la réduction et à la séquestration des gaz à effet de serre (2011-GZ-138839).


  1. Abbruzzese G, Beritognolo I, Muleo R, Piazzai M, Sabatti M, Scarascia Mugnozza G, Kuzminsky E (2009) Leaf morphological plasticity and stomatal conductance in three Populus alba L. genotypes subjected to salt stress. Environ Exp Bot 66:381–388CrossRefGoogle Scholar
  2. Barton MK (2007) Making holes in leaves: promoting cell state transitions in stomatal development. Plant Cell 19:1140–1143CrossRefPubMedPubMedCentralGoogle Scholar
  3. Bondada BR, Oosterhuis DM (2000) Comparative epidermal ultrastructure of cotton (Gossypium hirsutum L.) leaf, bract and capsule wall. Ann Bot 86:1143–1152CrossRefGoogle Scholar
  4. Boratyńska K, Jasińska AK, Ciepłuch E (2008) Effect of tree age on needle morphology and anatomy of Pinus uliginosa and Pinus silvestris—species-specific character separation during ontogenesis. Flora 203:617–626CrossRefGoogle Scholar
  5. Carins Murphy MR, Jordan GJ, Brodribb TJ (2014) Acclimation to humidity modifies the link between leaf size and the density of veins and stomata. Plant Cell Environ 37:124–131CrossRefPubMedGoogle Scholar
  6. Ceulemans R, Impens I, Steenackers V (1987) Variations in photosynthetic, anatomical, and enzymatic leaf traits and correlations with growth in recently selected Populus hybrids. Can J For Res 17:273–283CrossRefGoogle Scholar
  7. Chen J-H, Sun H, Yang Y-P (2008) Comparative morphology of leaf epidermis of Salix (Salicaceae) with special emphasis on sections Lindleyanae and Retusae. Bot J Lin Soc 157:311–322CrossRefGoogle Scholar
  8. Cooper RL, Cass DD (2003) A comparative epidermis study of the Athabasca sand dune willows (Salix; Salicaceae) and their putative progenitors. Can J Bot 81:749–754CrossRefGoogle Scholar
  9. England J, Attiwill P (2006) Changes in leaf morphology and anatomy with tree age and height in the broadleaved evergreen species, Eucalyptus regnans F. Muell. Trees 20:79–90CrossRefGoogle Scholar
  10. Fontana M, Lafleur B, Labrecque M, Courchesne F, Bélanger N. (2016) Maximum annual potential yields of Salix miyabeana SX67 in southern Quebec and effects of coppicing and stool age. Bioenerg Res. doi: 10.1007/s12155-016-9752-0 Google Scholar
  11. Franich RA, Wells LG, Barnet JR (1977) Variation with tee age of needle cuticle topography and stomatal structure in Pinus radiate D. Don. Ann Bot 41:621–626Google Scholar
  12. Furukawa A (1992) Ontogenetic changes in stomatal size and conductance of sunflowers. Ecol Res 7:147–153CrossRefGoogle Scholar
  13. Ghahremaninejad F, Khalili Z, Maassoumi AA, Mirzaie-Nodoushan H, Riahi M (2012) Leaf epidermal features of Salix species (Salicaceae) and their systematic significance. Am J Bot 99:769–777CrossRefPubMedGoogle Scholar
  14. Guidi Nissim W, Pitre FE, Teodorescu TI, Labrecque M (2013) Long-term biomass productivity of willow bioenergy plantations maintained in southern Quebec, Canada. Biomass Bioenerg 56:361–369CrossRefGoogle Scholar
  15. James SA, Bell DT (2000) Influence of light availability on leaf structure and growth of two Eucalyptus globulus ssp. provenances. Tree Physiol 20:1007–1018CrossRefPubMedGoogle Scholar
  16. Kouwenberg LL, Kürschner W, Visscher H (2004) Changes in stomatal frequency and size during elongation of Tsuga heterophylla needles. Ann Bot 94:561–569CrossRefPubMedPubMedCentralGoogle Scholar
  17. Labrecque M, Teodorescu IT (2003) High biomass yield achieved by Salix clones in SRIC following two 3-year coppice rotations on abandoned farmland in southern Quebec, Canada. Biomass Bioenerg 25:135–146CrossRefGoogle Scholar
  18. Labrecque M, Teodorescu IT (2005) Field performance and biomass production of 12 willow and poplar clones in short-rotation coppice in southern Quebec (Canada). Biomass Bioenerg 29:1–9CrossRefGoogle Scholar
  19. Lake JA, Woodward FI, Quick WP (2002) Long-distance CO2 signalling in plants. J Exp Bot 53:183–193CrossRefPubMedGoogle Scholar
  20. Lawson T, Blatt MR (2014) Stomatal size, speed, and responsiveness impact on photosynthesis and water use efficiency. Plant Physiol 164:1556–1570CrossRefPubMedPubMedCentralGoogle Scholar
  21. Maňkovská B, Percy K, Karnosky D (2005) Impacts of greenhouse gases on epicuticular waxes of Populus tremuloides Michx.: results from an open-air exposure and a natural O3 gradient. Environ Pollu 137:580–586CrossRefGoogle Scholar
  22. Marcysiak K (2012) Variation of leaf shape of Salix herbacea in Europe. Plant Syst Evol 298:1597–1607CrossRefGoogle Scholar
  23. Mott KA, Michaelson O (1991) Amphistomy as an adaptation to high light intensity in Ambrosia cordifolia (Compositae). Am J Bot 78:76–79CrossRefGoogle Scholar
  24. Mott KA, Gibson AC, O’Leary JW (1982) The adaptive significance of amphistomatic leaves. Plant Cell Environ 5:455–460CrossRefGoogle Scholar
  25. Naz N, Hameed M, Ashraf M, Al-Qurainy F, Arshad M (2010) Relationships between gaz-exchange characteristics and stomatal structural modifications in some desert grasses under high salinity. Photosynthetica 48:446–456CrossRefGoogle Scholar
  26. Pallardy S, Kozlowski T (1980) Cuticle development in the stomatal region of Populus clones. New Phytol 85:363–368CrossRefGoogle Scholar
  27. Pantin F, Simonneau T, Muller B (2012) Coming of leaf age: control of growth by hydraulics and metabolics during leaf ontogeny. New Phytol 196:349–366CrossRefPubMedGoogle Scholar
  28. Quarrie SA, Jones HG (1977) Effects of abscisic acid and water stress on development and morphology of wheat. J Exp Bot 28:192–203CrossRefGoogle Scholar
  29. Raven JA (2002) Selection pressures on stomatal evolution. New Phytol 153:371–386CrossRefGoogle Scholar
  30. Régnière J (1996) Generalized approach to landscape-wide seasonal forecasting with temperature-driven simulation models. Environ Entomol 25:869–881CrossRefGoogle Scholar
  31. Royer D (2001) Stomatal density and stomatal index as indicators of paleoatmospheric CO2 concentration. Rev Palaeobot Palynol 114:1–28CrossRefPubMedGoogle Scholar
  32. Rudall PJ, Hilton J, Bateman RM (2013) Several developmental and morphogenetic factors govern the evolution of stomatal patterning in land plants. New Phytol 200:598–614CrossRefPubMedGoogle Scholar
  33. Stojnić S, Orlović S, Trudić B, Živković U, von Wuehlisch G, Miljković D (2015) Phenotypic plasticity of European beech (Fagus sylvatica L.) stomatal features under water deficit assessed in provenance trial. Dendrobiology 73:163–173CrossRefGoogle Scholar
  34. Trimbacher C, Egkmullner O (1997) A method for quantifying changes in the epicuticular wax structure of Norway spruce needles. Eur J For Path 27:83–93CrossRefGoogle Scholar
  35. Voleníková M, Tichá I (2001) Insertion profiles in stomatal density and sizes in Nicotiana tabacum L. plantlets. Biol Plantarum 44:161–165CrossRefGoogle Scholar
  36. Woodward F (1986) Ecophysiological studies on the shrub Vaccinium myrtillus L. taken from a wide altitudinal range. Oecologia 70:580–586CrossRefGoogle Scholar
  37. Xu Z, Zhou G (2008) Responses of leaf stomatal density to water status and its relationship with photosynthesis in a grass. J Exp Bot 59:3317–3325CrossRefPubMedPubMedCentralGoogle Scholar
  38. Zhang Y, Wang Z, Wu Y, Zhang X (2006) Stomatal characteristics of different green organs in wheat under different irrigation regimes. Acta Agr Sin 32:70–75Google Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2016

Authors and Affiliations

  • Mario Fontana
    • 1
    • 2
  • Michel Labrecque
    • 2
  • Alexandre Collin
    • 1
  • Nicolas Bélanger
    • 1
    • 3
    Email author
  1. 1.Centre d’étude de la forêtUniversité du Québec à MontréalMontréalCanada
  2. 2.Institut de recherche en biologie végétale, Jardin botanique de MontréalMontréalCanada
  3. 3.Département Science et technologieUniversité du QuébecMontréalCanada

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