Overexpression of thioredoxin m in tobacco chloroplasts inhibits the protein kinase STN7 and alters photosynthetic performance.

María Ancín,Iker Aranjuelo,Jon Veramendi,Luis Larraya,Fermín Morales,Inmaculada Farran,Alicia Fernández-San Millán

doi:10.1093/jxb/ery415

Abstract

The activity of the protein kinase STN7, involved in phosphorylation of the light-harvesting complex II (LHCII) proteins, has been reported as being co-operatively regulated by the redox state of the plastoquinone pool and the ferredoxin-thioredoxin (Trx) system. The present study aims to investigate the role of plastid Trxs in STN7 regulation and their impact on photosynthesis. For this purpose, tobacco plants overexpressing Trx f or m from the plastid genome were characterized, demonstrating that only Trx m overexpression was associated with a complete loss of LHCII phosphorylation that did not correlate with decreased STN7 levels. The absence of phosphorylation in Trx m-overexpressing plants impeded migration of LHCII from PSII to PSI, with the concomitant loss of PSI-LHCII complex formation. Consequently, the thylakoid ultrastructure was altered, showing reduced grana stacking. Moreover, the electron transport rate was negatively affected, showing an impact on energy-demanding processes such as the Rubisco maximum carboxylation capacity and ribulose 1,5-bisphosphate regeneration rate values, which caused a strong depletion in net photosynthetic rates. Finally, tobacco plants overexpressing a Trx m mutant lacking the reactive redox site showed equivalent physiological performance to the wild type, indicating that the overexpressed Trx m deactivates STN7 in a redox-dependent way.

Highlights

The gathering of light energy and its later transformation into chemical energy is a central process for the proper functioning of photosynthetic machinery and plant performance
Recent studies in Arabidopsis have demonstrated that S and M trimers still remain associated with PSII upon phosphorylation (Wientjes et al, 2013a; Crepin and Caffarri, 2015), and that phosphorylated L trimers may serve as an antenna for PSI in most natural light conditions (Wientjes et al, 2013b), suggesting that association of phosphorylated LHCII (pLHCII) with PSI in higher plants may represent a long-term response against changes in light intensity under most natural light conditions
light-harvesting complex II (LHCII) phosphorylation, which is predominantly mediated by STN7, was detected in Wt and o/exTrxf plants, whereas it was completely lacking in o/exTrxm plants

Summary

Introduction

The gathering of light energy and its later transformation into chemical energy is a central process for the proper functioning of photosynthetic machinery and plant performance. Light energy is captured by a set of lightharvesting complexes (LHCs) that constitute, together with their associated reaction centers and electron donors/acceptors, the PSI and PSII photosystems. Under light conditions favoring PSI excitation, the kinase is deactivated and the pLHCII becomes dephosphorylated and relocated to PSII, increasing its cross-section and balancing the energy towards PSII (reversion to state 1).This rebalancing process, called state transitions, has been described as a fast post-translational acclimation mechanism operating in photosynthetic organisms under limiting light intensities (Allen, 1992, 2003; Lemeille and Rochaix, 2010; Tikkanen et al, 2011). LHCII comprises different homo- and heterotrimers of Lhcb, Lhcb, and Lhcb apoproteins (Galka et al, 2012) According to their affinity for binding to the PSII core, LHCII trimers can be classified into at least three different types: S (strong), M (moderate), and L (loose) (Dekker and Boekema, 2005). Recent studies in Arabidopsis have demonstrated that S and M trimers still remain associated with PSII upon phosphorylation (Wientjes et al, 2013a; Crepin and Caffarri, 2015), and that phosphorylated L trimers may serve as an antenna for PSI in most natural light conditions (Wientjes et al, 2013b), suggesting that association of pLHCII with PSI in higher plants may represent a long-term response against changes in light intensity under most natural light conditions

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Discussion

Conclusion