Photosynthetica 2023, 61(2):225-235 | DOI: 10.32615/ps.2023.017

Variation in leaf mesophyll anatomy of fern species imposes significant effects on leaf gas exchange, light capture, and leaf hydraulic conductance

S. FUJII1, K. NISHIDA1, T.K. AKITSU2, A. KUME3, Y.T. HANBA1
1 Kyoto Institute of Technology, Matsugasaki, Sakyo-ku, 606-8585 Kyoto, Japan
2 Earth Observation Research Center, Japan Aerospace Exploration Agency, 2-1-1 Sengen, 305-8505 Tsukuba, Japan
3 Faculty of Agriculture, Kyushu University, 744 Motooka, Nishi-ku, 819-0395 Fukuoka, Japan

The mesophyll anatomical traits are essential factors for efficient light capture, CO2 diffusion, and hydraulics in leaves. At the same time, leaf hydraulics are governed by the xylem anatomical traits. Thus, simultaneous analyses of the mesophyll and xylem anatomy will clarify the links among light capture, CO2 capture, and water use. However, such simultaneous analyses have been scarcely performed, particularly on non-seed plants. Using seven fern species, we first showed that fern species with a large mesophyll thickness had a high photosynthetic rate related to high light capture, high drought tolerance, and low leaf hydraulic conductance. The chloroplast surface area (Sc) per mesophyll thickness significantly decreased with an increase in mesophyll thickness, which may increase light diffusion and absorption efficiency in each chloroplast. The photosynthetic rate per Sc was almost constant with mesophyll thickness, which suggests that ferns enhance their light capture ability via the regulation of chloroplast density.

Additional key words: bryophyte; fern; leaf water relations; light absorptance; mesophyll anatomy; stomatal conductance.

Received: February 5, 2023; Revised: March 26, 2023; Accepted: April 13, 2023; Prepublished online: May 4, 2023; Published: June 6, 2023  Show citation

ACS AIP APA ASA Harvard Chicago Chicago Notes IEEE ISO690 MLA NLM Turabian Vancouver
FUJII, S., NISHIDA, K., AKITSU, T.K., KUME, A., & HANBA, Y.T. (2023). Variation in leaf mesophyll anatomy of fern species imposes significant effects on leaf gas exchange, light capture, and leaf hydraulic conductance. Photosynthetica61(SPECIAL ISSUE 2023/1), 225-235. doi: 10.32615/ps.2023.017
Download citation

Supplementary files

Download fileFujii_3001_supplement.docx

File size: 16.17 kB

References

  1. Aasamaa K., Sõber A., Rahi M.: Leaf anatomical characteristics associated with shoot hydraulic conductance, stomatal conductance and stomatal sensitivity to changes of leaf water status in temperate deciduous trees. - Funct. Plant Biol. 28: 765-774, 2001. Go to original source...
  2. Baltzer J.L., Thomas S.C.: Leaf optical responses to light and soil nutrient availability in temperate deciduous trees. - Am. J. Bot. 92: 214-223, 2005. Go to original source...
  3. Bartlett M.K., Scoffoni C., Sack L.: The determinants of leaf turgor loss point and prediction of drought tolerance of species and biomes: a global meta-analysis. - Ecol. Lett. 15: 393-405, 2012. Go to original source...
  4. Brodribb T.J., Feild T.S., Jordan G.J.: Leaf maximum photosynthetic rate and venation are linked by hydraulics. - Plant Physiol. 144: 1890-1898, 2007. Go to original source...
  5. Brodribb T.J., Holbrook N.M., Zwieniecki M.A., Palma B.: Leaf hydraulic capacity in ferns, conifers and angiosperms: Impacts on photosynthetic maxima. - New Phytol. 165: 839-846, 2005. Go to original source...
  6. Campany C.E., Pittermann J., Baer A. et al.: Leaf water relations in epiphytic ferns are driven by drought avoidance rather than tolerance mechanisms. - Plant Cell Environ. 44: 1741-1755, 2021. Go to original source...
  7. Carriquí M., Roig-Oliver M., Brodribb T.J. et al.: Anatomical constraints to nonstomatal diffusion conductance and photosynthesis in lycophytes and bryophytes. - New Phytol. 222: 1256-1270, 2019. Go to original source...
  8. Cui M., Vogelmann T.C., Smith W.K.: Chlorophyll and light gradients in sun and shade leaves of Spinacia oleracea. - Plant Cell Environ. 14: 493-500, 1991. Go to original source...
  9. Ebihara A.: [The Standard of Ferns and Lycophytes in Japan.] Gakken Plus, Tokyo 2018. [In Japanese]
  10. 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. Go to original source...
  11. Fini A., Loreto F., Tattini M. et al.: Mesophyll conductance plays a central role in leaf functioning of Oleaceae species exposed to contrasting sunlight irradiance. - Physiol. Plantarum 157: 54-68, 2016. Go to original source...
  12. Gago J., Carriquí M., Nadal M. et al.: Photosynthesis optimized across land plant phylogeny. - Trends Plant Sci. 24: 947-958, 2019. Go to original source...
  13. Hanba Y.T., Kogami H., Terashima I.: The effect of growth irradiance on leaf anatomy and photosynthesis in Acer species differing in light demand. - Plant Cell Environ. 25: 1021-1030, 2002. Go to original source...
  14. Hanba Y.T., Miyazawa S.-I., Terashima I.: The influence of leaf thickness on the CO2 transfer conductance and leaf stable carbon isotope ratio for some evergreen tree species in Japanese warm-temperate forests. - Funct. Ecol. 13: 632-639, 1999. Go to original source...
  15. Hanba Y.T., Nishida K., Tsutsui Y. et al.: Leaf optical properties and photosynthesis of fern species with wide range of divergence time in relation to the mesophyll anatomy. - Ann. Bot.-London 131: 437-450, 2023. Go to original source...
  16. Hu W., Lu Z., Meng F. et al.: The reduction in leaf area precedes that in photosynthesis under potassium deficiency: the importance of leaf anatomy. - New Phytol. 227: 1749-1763, 2020. Go to original source...
  17. Kanda Y.: Investigation of the freely available easy-to-use software 'EZR' for medical statistics. - Bone Marrow Transplant. 48: 452-458, 2013. Go to original source...
  18. Koide R.T., Robichaux R.H., Morse S.R., Smith C.M.: Plant water status, hydraulic resistance and capacitance. - In: Pearcy R.W., Ehleringer J.R., Mooney H.A., Rundel P.W. (ed.): Plant Physiological Ecology. Pp. 161-183. Springer, Dordrecht 1989. Go to original source...
  19. Kume A., Akitsu T., Nasahara K.N.: Why is chlorophyll b only used in light-harvesting systems? - J. Plant Res. 131: 961-972, 2018. Go to original source...
  20. Kume A.: Importance of the green color, absorption gradient, and spectral absorption of chloroplasts for the radiative energy balance of leaves. - J. Plant Res. 130: 501-514, 2017. Go to original source...
  21. Lambers H., Oliveira R.S.: Plant Physiological Ecology. Pp. 736. Springer, Cham 2019. Go to original source...
  22. Maréchaux I., Bartlett M.K., Sack L. et al.: Drought tolerance as predicted by leaf water potential at turgor loss point varies strongly across species within an Amazonian forest. - Funct. Ecol. 29: 1268-1277, 2015. Go to original source...
  23. Matos F.S., Wolfgramm R., Gonçalves F.V. et al.: Phenotypic plasticity in response to light in the coffee tree. - Environ. Exp. Bot. 67: 421-427, 2009. Go to original source...
  24. Mizokami Y., Oguchi R., Sugiura D. et al.: Cost-benefit analysis of mesophyll conductance: diversities of anatomical, biochemical and environmental determinants. - Ann. Bot.-London 130: 265-283, 2022. Go to original source...
  25. Nishida K., Kodama N., Yonemura S., Hanba Y.T.: 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. Go to original source...
  26. Noda H.M., Motohka T., Murakami K. et al.: Accurate measurement of optical properties of narrow leaves and conifer needles with a typical integrating sphere and spectroradiometer. - Plant Cell Environ. 36: 1903-1909, 2013. Go to original source...
  27. Oguchi R., Hikosaka K., Hirose T.: Leaf anatomy as a constraint for photosynthetic acclimation: Differential responses in leaf anatomy to increasing growth irradiance among three deciduous trees. - Plant Cell Environ. 28: 916-927, 2005. Go to original source...
  28. Perera-Castro A.V., Waterman M.J., Robinson S.A., Flexas J.: Limitations to photosynthesis in bryophytes: certainties and uncertainties regarding methodology. - J. Exp. Bot. 73: 4592-4604, 2022. Go to original source...
  29. Pittermann J., Limm E., Rico C., Christman M.A.: Structure-function constraints of tracheid-based xylem: a comparison of conifers and ferns. - New Phytol. 192: 449-461, 2011. Go to original source...
  30. 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. Go to original source...
  31. R Core Team: R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Available at: https://www.R-project.org/, 2022.
  32. Ren T., Weraduwage S.M., Sharkey T.D.: Prospects for enhancing leaf photosynthetic capacity by manipulating mesophyll cell morphology. - J. Exp. Bot. 70: 1153-1165, 2019. Go to original source...
  33. 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. Go to original source...
  34. Sack L., Scoffoni C., John G.P. et al.: How do leaf veins influence the worldwide leaf economic spectrum? Review and synthesis. - J. Exp. Bot. 64: 4053-4080, 2013. Go to original source...
  35. Sack L., Scoffoni C., Johnson D.M. et al.: The anatomical determinants of leaf hydraulic function. - In: Hacke U. (ed.): Functional and Ecological Xylem Anatomy. Pp. 255-271. Springer, Cham 2015. Go to original source...
  36. Schneider C.A., Rasband W.S., Eliceiri K.W.: NIH Image to ImageJ: 25 years of image analysis. - Nat. Methods 9: 671-675, 2012. Go to original source...
  37. Schuettpelz E., Pryer K.M.: Evidence for a Cenozoic radiation of ferns in an angiosperm-dominated canopy. - PNAS 106: 11200-11205, 2009. Go to original source...
  38. Solovchenko A.: Screening pigments: General questions. - In: Photoprotection in Plants. Springer Series in Biophysics. Vol. 14. Pp. 9-31. Springer, Berlin-Heidelberg 2010. Go to original source...
  39. Takemura K., Kamachi H., Kume A. et al.: A hypergravity environment increases chloroplast sizes, photosynthesis and plant growth of the moss Physcomitrella patens. - J. Plant Res. 130: 181-192, 2017. Go to original source...
  40. Terashima I., Fujita T., Inoue T. et al.: Green light drives leaf photosynthesis more efficiently than red light in strong white light: Revisiting the enigmatic question of why leaves are green. - Plant Cell Physiol. 50: 684-697, 2009. Go to original source...
  41. Terashima I., Hanba Y.T., Tholen D., Niinemets Ü.: Leaf functional anatomy in relation to photosynthesis. - Plant Physiol. 155: 108-116, 2011. Go to original source...
  42. Testo W., Field A., Barrington D.: Overcoming among-lineage rate heterogeneity to infer the divergence times and biogeography of the clubmoss family Lycopodiaceae. - J. Biogeogr. 45: 1929-1941, 2018. Go to original source...
  43. Thain J.F.: Curvature correction factors in the measurement of cell surface areas in plant tissues. - J. Exp. Bot. 34: 87-94, 1983. Go to original source...
  44. Thornley J.H.M., Johnson I.R.: Plant and Crop Modelling: A Mathematical Approach to Plant and Crop Physiology. Pp. 669. The Blackburn Press, New Jersey 1990.
  45. Tosens T., Niinemets Ü., Vislap V. et al.: Developmental changes in mesophyll diffusion conductance and photosynthetic capacity under different light and water availabilities in Populus tremula: how structure constrains function. - Plant Cell Environ. 35: 839-856, 2012. Go to original source...
  46. 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. Go to original source...
  47. Watkins J.E., Holbrook N.M., Zwieniecki M.A.: Hydraulic properties of fern sporophytes: consequences for ecological and evolutionary diversification. - Am. J. Bot. 97: 2007-2019, 2010. Go to original source...
  48. Zanne A.E., Westoby M., Falster D.S. et al.: Angiosperm wood structure: Global patterns in vessel anatomy and their relation to wood density and potential conductivity. - Am. J. Bot. 97: 207-215, 2010. Go to original source...
  49. Zhang S.-B., Sun M., Cao K.-F. et al.: Leaf photosynthetic rate of tropical ferns is evolutionarily linked to water transport capacity. - PLoS ONE 9: e84682, 2014. Go to original source...