Variation in photosynthetic induction between rice accessions and its potential for improving productivity

Abstract

Photosynthetic induction describes the transient increase in leaf CO₂ uptake with an increase in light. During induction, efficiency is lower than at steady state. Under field conditions of fluctuating light, this lower efficiency during induction may cost > 20% of potential crop assimilation. Accelerating induction would boost photosynthetic and resource-use efficiencies. Variation between rice accessions and potential for accelerating induction was analysed by gas exchange. Induction during shade to sun transitions of 14 accessions representing five subpopulations from the 3000 Rice Genome Project Panel (3K RGP) was analysed. Differences of 109% occurred in the CO₂ fixed during the first 300 s of induction, 117% in the half-time to completion of induction, and 65% in intrinsic water-use efficiency during induction, between the highest and lowest performing accessions. Induction in three accessions with contrasting responses (AUS 278, NCS 771 A and IR64-21) was compared for a range of [CO₂ ] to analyse limitations. This showed in vivo capacity for carboxylation at Rubisco (V_c,max ), and not stomata, as the primary limitation to induction, with significant differences between accessions. Variation in nonsteady-state efficiency greatly exceeded that at steady state, suggesting a new and more promising opportunity for selection of greater crop photosynthetic efficiency in this key food crop.

Keywords: Rubisco activase; dynamic photosynthesis; food security; photosynthesis; photosynthetic induction; rice; stomata; water-use efficiency.

Figure 1

(a) Net leaf CO₂ uptake A, (b) stomatal conductance g _s, (c) intrinsic water use efficiency iWUE = A/g _s, and (d) intercellular [CO₂] C _i with time t of induction on transfer at 0 s from low to high light (50–1700 µmol m⁻² s⁻¹) in rice (Oryza sativa). The ‘induction period’, characterized by a steep increase in A, is demarked with the grey box and lasted up to 300 s. The three accessions that were selected for further study of induction at varied [CO₂] were AUS 278 (red), NCS 771 A (blue) and IR64‐21 (black). The other three accessions in grey are Du Gen Chuan, K2 C45 and Malogbana. For ease of visualization, only six accessions are included, but the data for all 14 accessions are available in Table 1 and Fig. 2.

Figure 2

Mean and variation for all rice (Oryza sativa) accessions for average leaf CO₂ uptake during the first 300 s of induction (${\overline{A}}_{300}$), average A stomatal conductance during the first 300 s of induction (g _s avg), average intrinsic water‐use efficiency (${\text{iWUE}}_{\text{avg}}={\overline{A}}_{300}/g_{\text{s avg}}$), average intercellular CO₂ concentration during the first 300 s (C _i avg), and time that A reached 50% and 90% of A ₃₀₀ (IT₅₀ and IT₉₀, respectively). The accessions are ranked by increasing mean for each parameter. Different letters represent statistically significant differences (P < 0.05) between different accessions.

Figure 3

(a) Pearson correlation R ² of all measured dynamic and steady‐state (*) photosynthetic traits measured in rice (Oryza sativa). Negative correlations (red) and positive (blue). Traits are as follows: ${\overline{A}}_{300}$ and ${\overline{A}}_{700}$, average A during the first 300 s an 700 s of induction, respectively; A _sat, light‐saturated leaf CO₂ uptake; g _s, stomatal conductance; C _i, intercellular [CO₂] at steady state; iWUE, intrinsic water‐use efficiency (iWUE = A/g _s); g _s avg, average stomatal conductance during the first 300 s of induction; iWUE_avg, average intrinsic water‐use efficiency ($\text{iWUE}={\overline{A}}_{300}/g_{\text{s avg}}$); C _i avg, average intercellular [CO₂] during the first 300 s; A ₃₀₀, A at 300 s into induction; A _Max, maximum rate of CO₂ uptake across the entire induction period; IT₅₀ and IT₉₀, time that A reached 50% and 90%, respectively, of A ₃₀₀; IT₉₀  − IT₅₀, the difference between IT₉₀ and IT₅₀; ${\text{C Loss}}_{300}=(A-{\overline{A}}_{300})\times 300$, the difference between the total uptake that would have occurred over the first 300 , if A had risen instantaneously to A ₃₀₀ less the integral of the actual A over the first 300 s; ${\text{C Loss}}_{700}=(A-{\overline{A}}_{700})\times 700$. (b–e) Individual measures, regression line, correlation coefficient R ², confidence interval (95%), and P‐value for (b) ${\overline{A}}_{300}$ vs IT₅₀, (c) ${\overline{A}}_{300}$ vs IT₉₀, (d) A _Max vs IT₅₀, and (e) A _Max vs IT₉₀.

Figure 4

Induction of leaf CO₂ uptake A and stomatal conductance g _s at [CO₂] = 100, 200, 300, 400, 600 and 800 µmol mol⁻¹ for three rice (Oryza sativa) cultivars. Each point is the mean (± SE) of four plants. The dashed vertical line at 360 s represents the point of transition from low to high photosynthetic photon flux density (50–1700 µmol m⁻² s⁻¹); that is, the start of induction.

Figure 5

The responses of leaf CO₂ uptake A to intercellular [CO₂] C _i at steady state (dark blue), and at 60 s (orange), 180 s (grey), 360 s (yellow), and 700 s (light blue) from the start of induction and replotted from Fig. 4. The operating point of each curve at 400 µmol mol⁻¹ atmospheric [CO₂] C _a is indicated with a black arrow. Each point is the mean (± SE) of four plants of each rice (Oryza sativa) accession.

Figure 6

Nonstomatal (open squares) and stomatal (closed triangles) limitations with leaf CO₂ uptake A (closed circles) vs time over the first 300 s of induction for the three selected rice (Oryza sativa) accessions. Nonstomatal and stomatal limitations during induction were calculated relative to the near‐steady‐state value obtained at 300 s. Each point represents the mean (± SE) of four individual plants measured at ambient [CO₂].

Figure 7

Apparent maximum rate of carboxylation V _c,max with time through induction calculated from the response of leaf CO₂ uptake A to intercellular [CO₂] C _i derived from inductions made at different [CO₂], as in Fig. 4. Induction began at 360 s. Significance of difference between the three rice (Oryza sativa) accessions is based on a repeated measures (time) one‐way ANOVA. Each point represents the mean (± SE) of four individual plants.