Demonstration of a relationship between state transitions and photosynthetic efficiency in a higher plant

Abstract

A consequence of the series configuration of PSI and PSII is that imbalanced excitation of the photosystems leads to a reduction in linear electron transport and a drop in photosynthetic efficiency. Achieving balanced excitation is complicated by the distinct nature of the photosystems, which differ in composition, absorption spectra, and intrinsic efficiency, and by a spectrally variable natural environment. The existence of long- and short-term mechanisms that tune the photosynthetic apparatus and redistribute excitation energy between the photosystems highlights the importance of maintaining balanced excitation. In the short term, state transitions help restore balance through adjustments which, though not fully characterised, are observable using fluorescence techniques. Upon initiation of a state transition in algae and cyanobacteria, increases in photosynthetic efficiency are observable. However, while higher plants show fluorescence signatures associated with state transitions, no correlation between a state transition and photosynthetic efficiency has been demonstrated. In the present study, state 1 and state 2 were alternately induced in tomato leaves by illuminating leaves produced under artificial sun and shade spectra with a sequence of irradiances extreme in terms of PSI or PSII overexcitation. Light-use efficiency increased in both leaf types during transition from one state to the other with remarkably similar kinetics to that of F'm/Fm, F'o/Fo, and, during the PSII-overexciting irradiance, ΦPSII and qP. We have provided compelling evidence for the first time of a correlation between photosynthetic efficiency and state transitions in a higher plant. The importance of this relationship in natural ecophysiological contexts remains to be elucidated.

Keywords: light-use efficiency; photosynthesis; photosystems; state transitions.

Figure 1.. Spectra of growth and measurement light.

Relative quantum flux and spectral distribution of (A; thin solid line) artificial daylight spectrum, (B; dotted line) artificial shade spectrum, (C; left thick line) filtered 480 nm (nominal) irradiance (peak wavelength 478, 10 nm FWHP), and (D; right thick line) 700 nm (nominal) irradiance (peak wavelength 695, 10 nm FWHM). The broadband spectra were used as growth irradiance treatments and the narrowband spectra were applied separately as actinic irradiance during gas exchange measurements.

Figure 2.. Assimilation rates during a PSII/PSI light regime.

Rates of assimilation for SUN (red) and SHADE (blue) leaves during a PSII/PSI light regime. Absorbed irradiance was 40 µmol m⁻²s⁻¹ for each irradiance type. Letters ‘A’, ‘B’, and ‘C’ are references for Figure 3. Error bars shown represent the SEM (n = 3).

Figure 3.. Detailed view of assimilation rates upon light switching.

(A–C): Detailed view of assimilation rate in SUN (red) and SHADE (blue) leaves during (A) switching from PSII to PSI light, (B) switching from PSI to PSII light, and (C) second switching from PSII to PSI light. Letters correspond with data segments by ‘A’ and ‘B’ in Figure 2. Error bars shown represent the SEM (n = 3). The set of error bars to the right of the dotted line correspond with local minima after switching.

Figure 4.. Response of assimilation to the doubling of intensity of PSI and PSII light.

Rate of assimilation for a SUN leaf initially exposed to PSII light at an absorbed irradiance of ∼20 µmol m⁻²s⁻¹ followed by the subsequent doubling of intensity. PSII light was followed in the same manner by PSI light.

Figure 5.. Leaf light transmission, reflectance and absorptance.

Leaf light transmission determined in situ on intact SUN (open circles) and SHADE (closed circles) leaves together with estimated reflection (based on transmission) and calculated absorption values. Error bars shown represent the SEM (n = 3).

Figure 6.. Φ_CO2 traces during a PSII/PSI light regime.

Φ_CO2 calculated for SUN (red) and SHADE (blue) leaves using (A) leaf absorption determined from leaf discs directly after gas exchange measurements or (B) calculated leaf absorption determined in situ on intact leaves during gas exchange measurements. Error bars shown represent the SEM (n = 3).

Figure 7.. Fluorescence yield associated with transitions between state 1 and state 2.

Segment of fluorescence yield trace obtained with a SUN leaf and bearing classical hallmarks of a state transition. Fluorescence yield changes abruptly upon light switching and subsequent increases or decreases to a new steady state as a state transition proceeds.

Figure 8.. Responses of selected fluorescence parameters to a PSII/PSI light regime in SUN leaves, superimposed over corresponding scaled Φ_CO2 responses.

Measurements of ΦPSII, q_P, F′m/Fm, F′o/Fo, F′v/F′m, and NPQ (open circles) for SUN leaves, superimposed on light-limited Φ_CO2 traces for SUN leaves. Error bars shown represent the SEM (n = 3).

Figure 9.. Responses of selected fluorescence parameters to a PSII/PSI light regime in SHADE leaves, superimposed over corresponding scaled Φ_CO2 responses.

Measurements of ΦPSII, q_P, F′m/Fm, F′o/Fo, F′v/F′m, and NPQ (open circles) for SHADE leaves, superimposed on light-limited Φ_CO2 traces for SUN leaves. Error bars shown represent the SEM (n = 3).

Figure 10.. Relationship between selected fluorescence parameters and Φ_CO2 during exposure of SUN and SHADE leaves to PSI (700 nm) or PSII (480 nm) light.

Relationship between Φ_CO2 and ΦPSII, q_P, F′v/Fm, and F′o/Fo, F′m/Fm for SUN (open triangles) and SHADE leaves (closed circles) presented with 480 and 700 nm irradiance (n = 3).