TIP family aquaporins play role in chloroplast osmoregulation and photosynthesis

Abstract

SUMMARYPhotosynthetic oxygen evolution by photosystem II requires water supply into the chloroplast to reach the thylakoid lumen. A rapid water flow is also required into the chloroplast for optimal oxygen evolution and to overcome osmotic stress. The mechanisms governing water transport in chloroplasts are largely unexplored. Previous proteomics indicated the presence of three aquaporins from the tonoplast intrinsic protein (TIP) family, TIP1;1, TIP1;2 and TIP2;1, in chloroplast membranes of Arabidopsis thaliana. Here we revisited their location and studied their role in chloroplasts. Localization experiments indicated that TIP2;1 resides in the thylakoid, whereas TIP1;2 is present in both thylakoid and envelope membranes. Mutants lacking TIP1;2 and/or TIP2;1 did not display a macroscopic phenotype when grown under standard conditions. The mutant chloroplasts and thylakoids underwent less volume changes than the corresponding wild type preparations upon osmotic treatment and in the light. Significantly reduced rates of photosynthetic electron transport were obtained in the mutant leaves, with implications on the CO2 fixation rates. However, electron transport rates did not significantly differ between mutants and wild type when isolated thylakoids were examined. Less acidification of the thylakoid lumen was measured in mutants thylakoids, resulting in a slower induction of delta pH-dependent photoprotective mechanisms. These results identify TIP1;2 and TIP2;1 as chloroplast proteins and highlight their importance for osmoregulation and optimal photosynthesis. A third aquaporin, TIP1;1, is present in the chloroplast envelope, and may play role in photosynthesis under excessive light conditions, as based on the weak photosynthetic phenotype of its mutant.

Comparative Analysis of Re-Annotated Genes Provides Insight into Evolutionary Divergence and Expressions of Aquaporin Family in Pepper

“…Specifically, many plants use osmotic adjustment and ion transport through AQP [ 16 ] to adapt to stress, and the finding that anion and organic substance transport-related GO terms were enriched in the salt cluster 5 ( Figure 5 C) supports this suggestion. Moreover, enrichment of GO terms related to the thylakoid membrane in cold cluster 5 were consistent with previous studies, which showed that the TIP genes in Arabidopsis control the volume of the thylakoid lumen during water or light stress, thereby creating an optimal photosynthetic environment [ 17 ]. Our results suggest that the pepper AQP genes also have an important role in molecular responses to changing conditions and act in concert with other pepper genes.…”

The Passage of H2O2 from Chloroplasts to Their Associated Nucleus during Retrograde Signalling: Reflections on the Role of the Nuclear Envelope

“…Of the 35 AQPs in Arabidopsis [71], up to 5 may be present in the chloroplast. Of these, at least two isoforms of the tonoplast intrinsic protein (TIP1;1 and TIP1;2) AQP family and one of the plasma membrane intrinsic proteins, PIP2a, may span the inner chloroplast envelope membrane [72][73][74]. Therefore, the current evidence strongly suggests that AQPs are the exit route out of the chloroplast for H 2 O 2 .…”

Significance of solute specificity, expression, and gating mechanism of tonoplast intrinsic protein during development and stress response in plants

“…Apart from vacuoles, some of the TIP homologs were also localized in other subcellular locations such as plasma membrane, chloroplast, and mitochondria (Figure 2). AtTIP1;1 and AtTIP2;1 were localized in the chloroplast envelope; however, their distinct localization pattern should be confirmed in different plant species (Beebo et al, 2020; Ferro et al, 2003; Maurel et al, 2015). Proteomic analysis in Arabidopsis suggests the presence of TIPs in the thylakoid membrane of chloroplast (Ferro et al, 2010).…”