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

• Published in: The Plant journal : for cell and molecular biology 2018-11, Vol.96 (4), p.786-800
• Main Authors: Albanese, Pascal, Manfredi, Marcello, Re, Angela, Marengo, Emilio, Saracco, Guido, Pagliano, Cristina
• Format: Article
• Language: English
• Subjects: Acclimation; Acclimatization; Accumulation; ATP synthase; Carotenoids - metabolism; Chlorophyll; Chlorophyll - metabolism; Data integration; Drug Combinations; Electron Transport; Environmental changes; Environmental conditions; Fluorescence; Gene Expression Profiling; Gene Expression Regulation, Plant; Isoforms; Kinetics; Light; light acclimation; Light intensity; Luminous intensity; Membrane proteins; Membrane trafficking; Membranes; omics data integration; Photosystem I Protein Complex - metabolism; Photosystem II; Photosystem II Protein Complex - metabolism; Pisum sativum; Plant Extracts - metabolism; Plant Proteins - metabolism; Protein Biosynthesis; Protein synthesis; Protein transport; Proteins; Proteome - metabolism; Proteomes; Proteomics; quantitative proteomics; Relative abundance; Stress, Physiological - genetics; SWATH analysis; thylakoid membrane; Thylakoid membranes; Thylakoids - metabolism; Transcriptome; Xanthophylls
• ISSN: 0960-7412; 1365-313X
• DOI: 10.1111/tpj.14068

Summary Plant thylakoid membranes contain hundreds of proteins that closely interact to cope with ever‐changing environmental conditions. We investigated how Pisum sativum L. (pea) grown at different irradiances optimizes light‐use efficiency through the differential accumulation of thylakoid proteins. Thylakoid membranes from plants grown under low (LL), moderate (ML) and high (HL) light intensity were characterized by combining chlorophyll fluorescence measurements with quantitative label‐free proteomic analysis. Protein sequences retrieved from available transcriptomic data considerably improved thylakoid proteome profiling, increasing the quantifiable proteins from 63 to 194. The experimental approach used also demonstrates that this integrative omics strategy is powerful for unravelling protein isoforms and functions that are still unknown in non‐model organisms. We found that the different growth irradiances affect the electron transport kinetics but not the relative abundance of photosystems (PS) I and II. Two acclimation strategies were evident. The behaviour of plants acclimated to LL was compared at higher irradiances: (i) in ML, plants turn on photoprotective responses mostly modulating the PSII light‐harvesting capacity, either accumulating Lhcb4.3 or favouring the xanthophyll cycle; (ii) in HL, plants reduce the pool of light‐harvesting complex II and enhance the PSII repair cycle. When growing at ML and HL, plants accumulate ATP synthase, boosting both cyclic and linear electron transport by finely tuning the ΔpH across the membrane and optimizing protein trafficking by adjusting the thylakoid architecture. Our results provide a quantitative snapshot of how plants coordinate light harvesting, electron transport and protein synthesis by adjusting the thylakoid membrane proteome in a light‐dependent manner. Significance Statement The thylakoid membrane proteome carries out the photosynthetic light reactions needed to store solar energy in biologically available carbon‐based compounds. As plants face ever‐changing light conditions, we quantitatively assessed the proteome adjustments that occur in the thylakoid membranes of pea plants grown at different light intensities, highlighting the complexity of the highly coordinated mechanisms underlying light‐dependent proteome modulation.