Dynamic Acclimation to High Light in Arabidopsis thaliana Involves Widespread Reengineering of the Leaf Proteome

Abstract

Leaves of Arabidopsis thaliana transferred from low to high light increase their capacity for photosynthesis, a process of dynamic acclimation. A mutant, gpt2, lacking a chloroplast glucose-6-phosphate/phosphate translocator, is deficient in its ability to acclimate to increased light. Here, we have used a label-free proteomics approach, to perform relative quantitation of 1993 proteins from Arabidopsis wild type and gpt2 leaves exposed to increased light. Data are available via ProteomeXchange with identifier PXD006598. Acclimation to light is shown to involve increases in electron transport and carbon metabolism but no change in the abundance of photosynthetic reaction centers. The gpt2 mutant shows a similar increase in total protein content to wild type but differences in the extent of change of certain proteins, including in the relative abundance of the cytochrome b6f complex and plastocyanin, the thylakoid ATPase and selected Benson-Calvin cycle enzymes. Changes in leaf metabolite content as plants acclimate can be explained by changes in the abundance of enzymes involved in metabolism, which were reduced in gpt2 in some cases. Plants of gpt2 invest more in stress-related proteins, suggesting that their reduced ability to acclimate photosynthetic capacity results in increased stress.

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

“…When comparing HL with LL plants the Lhcb4.2 isoform displayed a decreasing rate similar to Lhcb6; conversely, Lhcb4.3 showed a remarkable 4.6‐fold increase (Figure , Table S4), in accordance with the threefold accumulation observed by Miller et al . () in A. thaliana exposed to HL, though less extreme. Interestingly, here we observed a more than twofold increase of Lhcb4.3 already in ML with respect to LL plants (Figure , Table S4), suggesting that the transcriptional control of this protein (Floris et al ., ), and its accumulation within the PSII–LHCIIsc (Albanese et al ., ), are already enhanced by moderate growth irradiances.…”

“…As the P. sativum genome is not yet fully sequenced, we used a custom protein database inferred from transcriptomic data to complement the Viridiplantae protein database, which resulted in a remarkably increased number of quantifiable proteins (194 versus 63; see Methods S8, Tables S2 and S3). From the proteomic quantification, the relative variation of abundance of PSI and PSII core proteins, and thus their relative ratio, was not significantly affected by growth irradiance (Figure ), in accordance with the 77‐K fluorescence measurements (Figure c) and with other recent proteomic evidence in A. thaliana (acclimated from 100 to 400 μE for 1 week; Miller et al ., ). The proteomic quantification, however, does not reflect the integrity of PS as a complex.…”

“…The amount of Lhcb3, which is a M‐trimer constituent, and of Lhcb6, which functions as linker for this trimer to the PSII core (Su et al ., ), decreased simultaneously (Figure ), confirming the major role of these two subunits in modulating the PSII–LHCIIsc functional antenna size in response to variation of growth irradiance (Albanese et al ., ). The Lhcb4 subunit, which occupies a pivotal position for bridging either S‐ or M‐trimers to the PSII core, is present in A. thaliana in three isoforms, Lhcb4.1, Lhcb4.2 and Lhcb4.3 (Jansson, ; Miller et al ., ). To date only two isoforms have been found in P. sativum at the protein level, either as part of the PSII–LHCIIsc (Albanese et al ., ) or within the thylakoids (this work); they are now named according to their corresponding entries in the transcriptome as Lhcb4.2 and Lhcb4.3 (Table S3a).…”

“…The amount of VDE and ZEP further increased in HL, although to a minor extent (Table S4), probably because of the reduction of the overall LHCII pool (Figure ), the functional interactors of VDE and ZEP. Interestingly, PsbS, the other major contributor to qE, accumulated only in HL (Figure ), probably acting as a constitutive promoter of a dissipative state in LHCII upon high irradiation (Albanese et al ., ; Miller et al ., ) activating NPQ (Betterle et al ., ; Johnson et al ., ). Even though it is still unclear where PsbS specifically associates with PSII (Gerotto et al ., ; Correa‐Galvis et al ., ), a role in controlling the PSII macro‐organization has been proposed (Kereïche et al ., ).…”

Structural and functional differentiation of the light‐harvesting protein Lhcb4 during land plant diversification

“…In some flowering plants, as the model organism A. thaliana , this subunit differentiated in up to three isoforms, Lhcb4.1, Lhcb4.2 and Lhcb4.3. Contrarily to LHCB4.1 and LHCB4.2 , the LHCB4.3 gene is strongly upregulated in moderate and high light, as attested at level of transcription (Alboresi et al ), translation (Floris et al ) and protein expression (Albanese et al , Miller et al , Albanese et al ). The increased accumulation of the Lhcb4.3 subunit observed in PSII‐LHCIIsc of plants acclimated to increasing intensity of light (Albanese et al ), induced us to investigate whether this isoform has a preferential localization in a specific PSII‐LHCIIsc conformation that might explain a light‐regulated function for this protein.…”