Growth of the C4 dicot Flaveria bidentis: photosynthetic acclimation to low light through shifts in leaf anatomy and biochemistry

Abstract

In C(4) plants, acclimation to growth at low irradiance by means of anatomical and biochemical changes to leaf tissue is considered to be limited by the need for a close interaction and coordination between bundle sheath and mesophyll cells. Here differences in relative growth rate (RGR), gas exchange, carbon isotope discrimination, photosynthetic enzyme activity, and leaf anatomy in the C(4) dicot Flaveria bidentis grown at a low (LI; 150 micromol quanta m(2) s(-1)) and medium (MI; 500 micromol quanta m(2) s(-1)) irradiance and with a 12 h photoperiod over 36 d were examined. RGRs measured using a 3D non-destructive imaging technique were consistently higher in MI plants. Rates of CO(2) assimilation per leaf area measured at 1500 micromol quanta m(2) s(-1) were higher for MI than LI plants but did not differ on a mass basis. LI plants had lower Rubisco and phosphoenolpyruvate carboxylase activities and chlorophyll content on a leaf area basis. Bundle sheath leakiness of CO(2) (phi) calculated from real-time carbon isotope discrimination was similar for MI and LI plants at high irradiance. phi increased at lower irradiances, but more so in MI plants, reflecting acclimation to low growth irradiance. Leaf thickness and vein density were greater in MI plants, and mesophyll surface area exposed to intercellular airspace (S(m)) and bundle sheath surface area per unit leaf area (S(b)) measured from leaf cross-sections were also both significantly greater in MI compared with LI leaves. Both mesophyll and bundle sheath conductance to CO(2) diffusion were greater in MI compared with LI plants. Despite being a C(4) species, F. bidentis is very plastic with respect to growth irradiance.

Fig. 1.

Top and side images of the Flaveria bidentis wild type grown at MI taken over a 36 d period with a 3D growth imaging system (Scanalyser, Lemnatech). Image backgrounds have been removed by the software analysis grid, leaving 2D pictures that are subsequently expressed as a plant area.

Fig. 2.

Comparison between growth measurements derived from image analysis or destructive harvest. Biomass over 36 d using (a) imaging volumes and (b) shoot dry mass. Cumulative relative growth rates from (c) imaging and (d) shoot dry mass. Points indicate the average of 5–10 plants. Correlation between computed volumes from imaging and (e) leaf area and (f) shoot dry mass. Plants grown at an irradiance of 150 μmol quanta m⁻² s⁻¹ (LI) and 500 μmol quanta m⁻² s⁻¹ (MI) are represented by filled and open circles, respectively. In (e) dashed (y=870.77x–803.48) and dotted (y=947.92x–1562.4) lines represent the linear regression for LI and MI irradiance treatments, respectively. In (f) dashed (y=341.91x–850.79) and dotted (y=288.24x–803.47) lines represent the linear regression for LI and MI irradiance treatments, respectively.

Fig. 3.

CO₂ assimilation rate as a function of intercellular pCO₂ (C_i) in Flaveria bidentis plants grown at 500 μmol quanta m⁻² s⁻¹ (a, b open symbols) and 150 μmol quanta m⁻² s⁻¹ (c, d filled symbols). Graphs (b) and (d) expand the scale at low C_i to highlight the difference between growth irradiance treatments. Gas exchange measurements were made at three irradiances, 150 (triangle), 500 (square), and 1500 (circle) μmol quanta m⁻² s⁻¹, and a leaf temperature of 25 °C.

Fig. 4.

CO₂ assimilation rate, A (a), stomatal conductance, g_s (b), carbon isotope discrimination, Δ (c), the ratio of intercellular to ambient pCO₂, C_i/C_a (d), bundle sheath leakiness, ϕ (e), and ξ (f), as a function of irradiance, in Flaveria bidentis grown at 150 μmol quanta m⁻² s⁻¹ (filled circles) and 500 μmol quanta m⁻² s⁻¹ (open circles) irradiance. Measurements were made at an ambient pCO₂ of ∼360 μbar, and a leaf temperature of 25 °C.

Fig. 5.

(a) Diagram representing regions of interest (ROIs) in cross-sections of Flaveria bidentis leaves. ROIs include bundle sheath cells (BS), palisade mesophyll cells (PM), spongy mesophyll cells (SM), and total vascular tissue (VT) which were manually outlined and measured to give area and perimeter data. Interveinal distances (IVD) were measured between two adjacent vascular bundles. Leaf mesophyll thickness (LMT) was measured between epidermal layers at four points in each cross-section. Intercellular airspaces (IA) within the interveinal distance were individually outlined and combined to give a total length of mesophyll cells exposed to intercellular airspace (S_m). Black stripes represent the perimeter of the bundle sheath tissue within the interveinal zone (S_b). Representative light microscope images (×400 magnification) of leaf sections of plants grown at 150 μmol quanta m⁻² s⁻¹ (b) and 500 μmol quanta m⁻² s⁻¹ (c). (This figure is available in colour at JXB online.)