Diffusional limitations explain the lower photosynthetic capacity of ferns as compared with angiosperms in a common garden study

Abstract

Ferns are thought to have lower photosynthetic rates than angiosperms and they lack fine stomatal regulation. However, no study has directly compared photosynthesis in plants of both groups grown under optimal conditions in a common environment. We present a common garden comparison of seven angiosperms and seven ferns paired by habitat preference, with the aims of (1) confirming that ferns do have lower photosynthesis capacity than angiosperms and quantifying these differences; (2) determining the importance of diffusional versus biochemical limitations; and (3) analysing the potential implication of leaf anatomical traits in setting the photosynthesis capacity in both groups. On average, the photosynthetic rate of ferns was about half that of angiosperms, and they exhibited lower stomatal and mesophyll conductance to CO2 (gm ), maximum velocity of carboxylation and electron transport rate. A quantitative limitation analysis revealed that stomatal and mesophyll conductances were co-responsible for the lower photosynthesis of ferns as compared with angiosperms. However, gm alone was the most constraining factor for photosynthesis in ferns. Consistently, leaf anatomy showed important differences between angiosperms and ferns, especially in cell wall thickness and the surface of chloroplasts exposed to intercellular air spaces.

Relationships of Leaf Net Photosynthesis, Stomatal Conductance, and Mesophyll Conductance to Primary Metabolism: A Multispecies Meta-Analysis Approach

“…These approaches comprise (1) the "Harley" method, combining chlorophyll fluorescence and gasexchange data (Harley et al, 1992); (2) the "Ethier" curve-fitting method (Ethier and Livingston, 2004); and (3) the "Evans" method, employing an online carbon isotope discrimination methodology (Evans et al, 1986). There is another approach to estimate g m in a manner based on leaf anatomical properties, which agrees with in vivo approaches in several angiosperms as well as in several fern species (Tosens et al, 2012;Tomás et al, 2013;Carriquí et al, 2015). However, several concerns were recently published about the reliability and uncertainties of the different in vivo methodologies (Tholen et al, 2012;Sun et al, 2014).…”

“…It is well known that cell wall composition can strongly differ between plant species and groups, especially in those from the Graminaceae family, ferns, and equisetums (Fry et al, 2008;Franková and Fry, 2013). Additionally, it has been described pooling together 61 different species that the cell wall thickness shows a negative significant relationship with g m (Tosens et al, 2012;Tomás et al, 2013;Carriquí et al, 2015).…”

The Sclerophyllous Eucalyptus camaldulensis and Herbaceous Nicotiana tabacum Have Different Mechanisms to Maintain High Rates of Photosynthesis

“…Photosynthetic limitations in E. camaldulensis and N. tabacum were assessed according to the method of Grassi and Magnani (2005) and Carriqui et al (2015). The values for stomatal ( l s ), mesophyll conductance ( l mc ), and biochemical ( l b ) limitations represented measures of the relative importance of stomatal diffusion, mesophyll diffusion, and photosynthetic biochemistry in setting the observed value of A n .…”

“…The values for stomatal ( l s ), mesophyll conductance ( l mc ), and biochemical ( l b ) limitations represented measures of the relative importance of stomatal diffusion, mesophyll diffusion, and photosynthetic biochemistry in setting the observed value of A n . Relative photosynthetic limitations were calculated as follows (Grassi and Magnani, 2005; Carriqui et al, 2015): $\begin{array}{ccc}left{l}_s& =& \frac{{\mathrm{\text{g}}}_{\mathrm{\text{tot}}}/{\mathrm{\text{g}}}_{\mathrm{\text{s}}}\times \partial A_{\mathrm{\text{n}}}/\partial C_{\mathrm{\text{c}}}}{{\mathrm{\text{g}}}_{\mathrm{\text{tot}}}+\partial A_{\mathrm{\text{n}}}/\partial C_{\mathrm{\text{c}}}}\\ l_{mc}& =& \frac{{\mathrm{\text{g}}}_{\mathrm{\text{tot}}}/{\mathrm{\text{g}}}_{\mathrm{\text{m}}}\times \partial A_{\mathrm{\text{n}}}/\partial C_{\mathrm{\text{c}}}}{{\mathrm{\text{g}}}_{\mathrm{\text{tot}}}+\partial A_{\mathrm{\text{n}}}/\partial C_{\mathrm{\text{c}}}}\\ l_b& =& \frac{{\mathrm{\text{g}}}_{\mathrm{\text{tot}}}}{{\mathrm{\text{g}}}_{\mathrm{\text{tot}}}+\partial A_{\mathrm{\text{n}}}/\partial C_{\mathrm{\text{c}}}}\end{array}$ where g tot was total conductance to CO 2 between the leaf surface and carboxylation sites (calculated as 1/ g tot = 1/ g s + 1/ g m ).…”

“…Mesophyll conductance plays an important role in determining the rate of photosynthesis in C 3 plants (Flexas et al, 2008; Carriqui et al, 2015). A low g m value increases the resistance of CO 2 conductance to the chloroplasts, leading to a decline in the chloroplast CO 2 concentration ( C c ) and, thus, restricted CO 2 assimilation (Loreto et al, 1992; Hanba et al, 2002; Flexas et al, 2012; Gago et al, 2013; Carriqui et al, 2015). Therefore, for the sclerophyllous E. camaldulensis , other mechanisms favoring CO 2 diffusion must be used to increase C c because it is essential for the maintenance of high CO 2 assimilation.…”