Fine-Tuning of Photosynthesis Requires CURVATURE THYLAKOID1-Mediated Thylakoid Plasticity

Abstract

The thylakoid membrane system of higher plant chloroplasts consists of interconnected subdomains of appressed and nonappressed membrane bilayers, known as grana and stroma lamellae, respectively. CURVATURE THYLAKOID1 (CURT1) protein complexes mediate the shape of grana stacks in a dosage-dependent manner and facilitate membrane curvature at the grana margins, the interface between grana and stroma lamellae. Although grana stacks are highly conserved among land plants, the functional relevance of grana stacking remains unclear. Here, we show that inhibiting CURT1-mediated alteration of thylakoid ultrastructure in Arabidopsis () reduces photosynthetic efficiency and plant fitness under adverse, controlled, and natural light conditions. Plants that lack CURT1 show less adjustment of grana diameter, which compromises regulatory mechanisms like the photosystem II repair cycle and state transitions. Interestingly, CURT1A suffices to induce thylakoid membrane curvature in planta and thylakoid hyperbending in plants overexpressing CURT1A. We suggest that CURT1 oligomerization is regulated at the posttranslational level in a light-dependent fashion and that CURT1-mediated thylakoid plasticity plays an important role in fine-tuning photosynthesis and plant fitness during challenging growth conditions.

Thylakoid proteome modulation in pea plants grown at different irradiances: quantitative proteomic profiling in a non‐model organism aided by transcriptomic data integration

“…CURT1 is a protein located in the grana margins that is involved in shaping the extent of thylakoid layers per granum (Armbruster et al, 2013). Upon HL exposure, Arabidopsis knockout mutants for CURT1 showed enlarged grana with fewer layers and reduced fitness (Armbruster et al, 2013;Pribil et al, 2018); conversely lines overexpressing CURT1 increased the number of layers per granum at the expense of the diameter, while maintaining a photosynthetic performance similar to that of the wild type (Armbruster et al, 2013;Pribil et al, 2018). RIQ1 is a protein located in the grana whose absence causes an increase in the number of thylakoids per granum and a looser association of LHCII with the PSII core (Yokoyama et al, 2016).…”

“…Under low light intensities, some LHCIIs can migrate from PSII to PSI to increase the absorption capacity of PSI in a process called 'state transition' (Allen and Forsberg, 2001). The overall ultrastructure of the thylakoid membranes hence requires dynamic architectural switches for tuning the interplay between PSs in response to light cues (Anderson et al, 2008;Kirchhoff, 2014b;Schumann et al, 2017;Pribil et al, 2018).…”

The Role of Phosphorylation Dynamics of CURVATURE THYLAKOID 1B in Plant Thylakoid Membranes

“…Indeed, the repulsive forces exerted by increased CURT1B phosphorylation in the edges of grana margins might locally increase the grana partition gaps and thus facilitate the de-stacking of grana edges necessary to accommodate the PSII repair machinery (Yamamoto et al, 2013;Tikkanen and Aro, 2014;Yoshioka-Nishimura et al, 2014). However, the fact that a certain percentage of CURT1B is acetylated, but not phosphorylated, and that this subpopulation of CURT1B is apparently not responsive to light changes, suggests that CURT1 proteins might have additional functions in conditions other than those studied so far (Armbruster et al, 2013;Pribil et al, 2018).…”

“…Recently, members of a family of membrane-integral thylakoid proteins named CURVATURE THYLAKOID1 (CURT1) have been proposed as new key components in shaping grana dimensions in response to changes in light quality and quantity (Armbruster et al, 2013;Pribil et al, 2018). One of them, CURT1B, formerly known as TMP14 or PSAP (At2g4682), was originally described as a PSI subunit interacting with PsaL/PsaH/PsaO (Khrouchtchova et al, 2005;Yu et al, 2008).…”

Antimicrobial solid media for screening non-sterile Arabidopsis thaliana seeds

“…2) except in the case of the psaL mutant, where the inclusion of timentin may have impaired germination in 7 % of seeds (at 168 h: 96 % of untreated seeds had germinated versus 89 % of seeds sown on timentin plus terbinafine). Carbenicillin (500 mg/L) inhibited normal root development in all lines examined and delayed germination in all cases except for the curt1abcd quadruple mutant, which exhibits slower germination than the wild-type ecotypes examined here and naturally produces a lower proportion of viable seeds [22]. The combination of terbinafine (1 µM) and timentin (200 mg/L) prevented microbial contamination for five days in 100 % of cases, and for seven days in 90 % of cases (Fig.…”