Potential mechanisms of low-temperature tolerance of C₄ photosynthesis in Miscanthus × giganteus: an in vivo analysis

Abstract

Miscanthus × giganteus (Greef & Deuter ex Hodkinson & Renvoize) is unique among C₄ species in its remarkable ability to maintain high photosynthetic productivity at low temperature, by contrast to the related C₄ NADP-malic enzyme-type species Zea mays L. In order to determine the in vivo physiological basis of this difference in photosynthesis, water vapor and CO₂ exchange and modulated chlorophyll fluorescence were simultaneously monitored on attached leaf segments from plants grown and measured at 25/20°C or 14/11°C (day/night temperature). Analysis of the response of photosynthesis to internal CO₂ concentration suggested that ribulose bisphosphate carboxylase/oxygenase (Rubisco) and/or pyruvate orthophosphate dikinase (PPDK) play a more important role in determining the response to low temperature than does phosphoenolpyruvate carboxylase (PEPc). For both species at both temperatures, the linear relationship between operating efficiency of whole-chain electron transport through photosystem II (Φ_PSII) and the efficiency of CO₂ assimilation (Φ_CO2) was unchanged and had a zero intercept, suggesting the absence of non-photosynthetic electron sinks. The major limitation at low temperature could not be solely at Rubisco or at any other point in the Calvin cycle, since this would have increased leakage of CO₂ to the mesophyll and increased Φ_PSII/Φ_CO2. This in vivo analysis suggested that maintenance of high photosynthetic rates in M. × giganteus at low temperature, in contrast to Z. mays, is most likely the result of different properties of Rubisco and/or PPDK, reduced susceptibility to photoinhibition, and the ability to maintain high levels of leaf absorptance during growth at low temperature.

Appendix

List of symbols and abbreviations used

A :

CO₂ uptake (photosynthesis; μmol m⁻² s⁻¹)

A _21% :

Photosynthesis at ambient O₂ (μmol m⁻² s⁻¹)

A _1% :

Photosynthesis at low O₂ (μmol m⁻² s⁻¹)

A _sat :

Light-saturated photosynthesis (μmol m⁻² s⁻¹)

A/C_i:

Curve of photosynthetic response to C_i

A/Q_abs:

Curve of photosynthetic response to Q_abs

α:

Leaf absorptance

C _a :

Ambient/external [CO₂] (μl l⁻¹)

C _i :

Internal [CO₂] (μl l⁻¹)

C _{i, 370} :

Operating point of photosynthesis (μmol m⁻² s⁻¹)

CE:

Carboxylation efficiency of PEPc

[CO₂]:

CO₂ concentration (μl l⁻¹)

ETR:

Electron transport rate (μmol m⁻² s⁻¹)

F _o :

Dark-adapted minimal fluorescence

F_o′:

Minimal fluorescence after the light period

F _m :

Dark-adapted maximal fluorescence

F_m′:

Maximal fluorescence during the saturating pulse

F _s :

Steady-state fluorescence in the light

F _v :

Dark-adapted variable fluorescence

F_v′:

Variable fluorescence in the light

(F_m′−F_s)/F_v′:

Efficiency of open PSII centers

F_v′/F_m′:

Maximum quantum efficiency of PSII

f :

Fraction of absorbed quanta used by PSII

Φ_PSII:

Operating efficiency of whole-chain electron transport through PSII

Φ_CO2:

Efficiency of CO₂ assimilation

Φ_{CO2, max}:

Maximum quantum yield

g _s :

Stomatal conductance to water vapor (mol m⁻² s⁻¹)

LED:

Light-emitting diode

l _s :

Stomatal limitation to photosynthesis (%)

ME:

Malic enzyme

NPQ:

Non-photochemical quenching

PEPc:

Phosphoenolpyruvate carboxylase

PPDK:

Pyruvate orthophosphate dikinase

PSI:

Photosystem I

PSII:

Photosystem II

Q :

Incident light (photosynthetic photon flux density; μmol m⁻² s⁻¹)

Q _abs :

Absorbed light (photosynthetic photon flux density; μmol m⁻² s⁻¹)

R :

Leaf reflectance

R _d :

Dark respiration rate (μmol m⁻² s⁻¹)

Rubisco:

Ribulose bisphosphate carboxylase/oxygenase

τ:

Leaf transmittance

θ:

Convexity coefficient of A/Q_abs curve

V _pr :

CO₂-saturated rate of photosynthesis (μmol m⁻² s⁻¹)