Abstract
Ferns flourish in many habitats, from epiphytic to terrestrial and from sunny to shady, and such varied conditions require contrasting photosynthetic strategies to cope with drought. Four species of temperate ferns from different habitats were subjected to drought by withholding irrigation in order to investigate their photosynthetic responses. Lepisorus thunbergianus (epiphytic) had low stomatal density and showed high water-use efficiency (WUE) retaining photosynthetic activity with low relative frond water content under drought stress, which suggested their high adaptation to drought. On the other hand, low WUE with low light-saturated photosynthetic rate in Adiantum pedatum (terrestrial, shady environment) was associated with much lower photosynthesis than in the other species under drought stress, suggesting lower adaptation to drought-prone habitats. Morphological stomatal traits such as stomatal density and photosynthetic response to drought in ferns involved species-specific adaptation to survive and grow in their natural habitats with different levels of drought.
Similar content being viewed by others
Abbreviations
- C i :
-
internal CO2 concentration
- DM:
-
dry mass of frond
- FM:
-
fresh mass of frond
- FWC:
-
frond water content
- g s :
-
stomatal conductance
- J :
-
electron transport rate
- LMA:
-
leaf mass per area
- P max :
-
light-saturated photosynthetic rate
- P N :
-
net photosynthetic rate
- WUE (P max/g s):
-
photosynthetic water-use efficiency
- RFWC:
-
relative frond water content
- SWC:
-
relative soil water contents
- TM:
-
turgid mass of frond
- V cmax :
-
maximum carboxylation rate
- VPD:
-
vapor pressure deficit
- δ13C:
-
carbon isotope ratio
References
Brodribb T.J., Holbrook N.M.: Stomatal protection against hydraulic failure: a comparison of coexisting ferns and angiosperms. — New Phytol. 162: 663–670, 2004.
Brodribb T.J., McAdam S.A.M.: Passive origins of stomatal control in vascular plants. — Science 331: 582–585, 2011.
Brodribb T.J., McAdam S. A. M.: Unique responsiveness of angiosperm stomata to elevated CO2 explained by calcium signalling. — PLoS ONE 8: e82057, 2013.
Brodribb T.J., McAdam S.A.M., Jordan G.J. et al.: Evolution of stomatal responsiveness to CO2 and optimization of water-use efficiency among land plants. — New Phytol. 183: 839–847, 2009.
Chaves M.M., Flexas J., Pinheiro C.: Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell. — Ann. Bot.-London 103: 551–560, 2009.
Doi M., Kitagawa Y., Shimazaki K.: Stomatal blue light response is present in early vascular plants. — Plant Physiol. 169: 1205–1213, 2015.
Doi M., Shimazaki K.: The stomata of the fern Adiantum capillus-veneris do not respond to CO2 in the dark and open by photosynthesis in guard cells. — Plant Physiol. 147: 922–930, 2008.
Doi M., Wada M., Shimazaki K.: The fern Adiantum capillus-veneris lacks stomatal responses to blue light. — Plant Cell Physiol. 47: 748–755, 2006.
Durand L.Z., Goldstein G.: Photosynthesis, photoinhibition, and nitrogen use efficiency in native and invasive tree ferns in Hawaii. — Oecologia 126: 345–354, 2001.
Ethier G.J., Livingston N.J.: On the need to incorporate sensitivity to CO2 transfer conductance into the Farquhar-von Caemmerer-Berry leaf photosynthesis model. — Plant Cell Environ. 27: 137–153, 2004.
Flexas J., Bota J., Loreto F. et al.: Diffusive and metabolic limitations to photosynthesis under drought and salinity in C3 plants. — Plant Biol. 6: 269–279, 2004.
Flexas J., Medrano H.: Drought-inhibition of photosynthesis in C3 plants: Stomatal and non-stomatal limitations revisited. — Ann. Bot-London 89: 183–189, 2002.
Galán J.M.G., Prada C., Rolleri C.H. et al.: Biometry of stomata in Blechnum species (Blechnaceae) with some taxonomic and ecological implications for the ferns. — Rev. Biol. Trop. 59: 403–415, 2011.
Galmés J., Flexas J., Savé R. et al.: Water relations and stomatal characteristics of Mediterranean plants with different growth forms and leaf habits: responses to water stress and recovery. — Plant Soil 290: 139–155, 2007.
Gulías J., Flexas J., Mus M. et al.: Relationship between maximum leaf photosynthesis, nitrogen content and specific leaf area in Balearic endemic and non-endemic mediterranean species. — Ann. Bot.-London 92: 215–222, 2003.
Gordon C., Woodin S.J., Mullins C. et al.: Effects of environmental change, including drought, on water use by competing Calluna vulgaris (heather) and Pteridium aquilinum (bracken). — Funct. Ecol. 13: 96–106, 1999.
Hanba Y.T., Kogami H., Terashima I.: The effect of internal CO2 conductance on leaf carbon isotope ratio. — Isot. Environ. Health Stud. 39: 5–13, 2003.
Hetherington A.M., Woodward F.I.: The role of stomata in sensing and driving environmental change. — Nature 424: 901–908, 2003.
Hietz P., Briones O.: Correlation between water relations and within-canopy distribution of epiphytic ferns in a Mexican cloud forest. — Oecologia 114: 305–316, 1998.
Hunt M.A., Davidson N.J., Unwin G.L. et al. Ecophysiology of the soft tree fern, Dicksonia antarctica Labill.–Austral. Ecol. 27: 360–368, 2002.
Kawase M., Hanba Y.T., Katsuhara M.: The photosynthetic response of tobacco plants overexpressing ice plant aquaporin McMIPB to a soil water deficit and high vapor pressure deficit. — J. Plant Res. 126: 517–527, 2013.
Kessler M., Siorak Y., Wunderlich M. et al.: Patterns of morphological leaf traits among pteridophytes along humidity and temperature gradients in the Bolivian Andes. — Funct. Plant Biol. 34: 963–971, 2007.
Kanda Y.: Investigation of the freely available easy-to-use software ‘EZR’for medical statistics. — Bone Marrow Transpl. 48: 452–458, 2013.
Kursar T.A., Coley P.D.: Delayed development of the photosynthetic apparatus in tropical rain forest species. — Funct. Ecol. 6: 411–422, 1992.
McAdam S.A.M., Brodribb T.J.: Ancestral stomatal control results in a canalization of fern and lycophyte adaptation to drought. — New Phytol. 198: 429–441, 2013.
Medrano H., Flexas J., Galmés J.: Variability in water use efficiency at the leaf level among Mediterranean plants with different growth forms. — Plant Soil 317: 17–29, 2009.
Nishida K., Kodama N., Yonemura S. et al.: Rapid response of leaf photosynthesis in two fern species Pteridium aquilinum and Thelypteris dentata to changes in CO2 measured by tunable diode laser absorption spectroscopy. — J. Plant Res. 128: 777–789, 2015.
Nobel P.S.: Mierohabitat, water relations, and photosynthesis of a desert fern, Notholaena parryi. — Oecologia 31: 293–309, 1978.
Pittermann J., Limm E., Rico C. et al.: Structure-function constraints of tracheid-based xylem: a comparison of conifers and ferns. — New Phytol. 192: 449–461, 2011.
Prange R.K., Ormod D.P., Proctor J.T.A.: Effect of water stress on gas exchange in fronds of the ostrich fern (Matteuccia struthiopteris (L.) Todaro). — J. Exp. Bot. 34: 1108–1116, 1983.
Pryer K.M., Schuettpelz E., Wolf P.G. et al.: Phylogeny and evolution of ferns (monilophytes) with a focus on the early leptosporangiate divergences. — Am. J. Bot. 91: 1582–1598, 2004.
Royo A.A., Carson W.P.: On the formation of dense understory layers in forests worldwide: consequences and implications for forest dynamics, biodiversity, and succession. — Can. J. Forest Res. 36: 1345–1362, 2006.
Saldanã A., Gianoli E., Lusk C.H.: Ecophysiological responses to light availability in three Blechnum species (Pteridophyta, Blechnaceae) of different ecological breadth. — Oecologia 145: 252–257, 2005.
Scartazza A., Lauteri M. Guido M.C. et al.: Carbon isotope discrimination in leaf and stem sugars, water-use efficiency and mesophyll conductance during different developmental stages in rice subjected to drought. — Aust. J. Plant Physiol. 25: 489–498, 1998.
Schneider H., Schuettpelz E., Pryer K.M. et al.: Ferns diversified in the shadow of angiosperms. — Nature 428: 553–557, 2004.
Smith A.R., Pryer K.M., Schuettpelz E. et al.: A classification for extant ferns. — Taxon 55: 705–731, 2006.
Tayasu I., Hirasawa R., Ogawa N. et al.: New organic reference materials for carbon- and nitrogen-stable isotope ratio measurements provided by Center for Ecological Research, Kyoto University, and Institute of Biogeosciences, Japan Agency for Marine-Earth Science and Technology. — Limnology 12: 261–266, 2011.
Tosens T., Nishida K., Gago J. et al.: The photosynthetic capacity in 35 ferns and fern allies: mesophyll CO2 diffusion as a key trait. — New Phytol. 209: 1576–1590, 2016.
Watkins J.E.Jr, Rundel W.R., Cardelús C.L.: The influence of life form on carbon and nitrogen relationships in tropical rainforest ferns. — Oecologia 153: 225–232, 2007.
Woodward F.I.: Stomatal numbers are sensitive to increases in CO2 from pre-industrial levels. — Nature 327: 617–618, 1987.
Woodhouse R.M., Nobel P.S.: Stipe anatomy, water potentials, and xylem conductances in seven species of ferns (Filicopsida). — Am. J. Bot. 69: 135–140, 1982.
Zhang Q., Chen J.W., Li B.G. et al.: The effect of drought on photosynthesis in two epiphytic and two terrestrial tropical fern species. — Photosynthetica 47: 128–132, 2009.
Zotz G.: Vascular epiphytes in the temperate zones–a review. — Plant Ecol. 176: 173–183, 2005.
Author information
Authors and Affiliations
Corresponding author
Additional information
Acknowledgements: We would like to thank Dr. Jiro Tatsumi for supporting our study. We thank Dr. Sakihito Kitajima for helpful comments on the manuscript. The carbon isotope ratio was measured at the Center for Ecological Research, Kyoto University, and we thank Drs. Tayasu Ichiro and Riyo Hirasawa for their assistance in making these measurements. This work was supported by a Research Grant for Young Scientists in Kyoto Institute of Technology in 2012 2013, and 2015 (K. Nishida).
Rights and permissions
About this article
Cite this article
Nishida, K., Hanba, Y.T. Photosynthetic response of four fern species from different habitats to drought stress: relationship between morpho-anatomical and physiological traits. Photosynthetica 55, 689–697 (2017). https://doi.org/10.1007/s11099-017-0694-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11099-017-0694-3