Role of callose synthases in transfer cell wall development in tocopherol deficient Arabidopsis mutants

Hiroshi Maeda,Wan Song,Dean Dellapenna,Tammy Sage

doi:10.3389/fpls.2014.00046

Hiroshi Maeda, Wan Song + Show 2 more

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https://doi.org/10.3389/fpls.2014.00046

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Abstract

Tocopherols (vitamin E) are lipid-soluble antioxidants produced by all plants and algae, and many cyanobacteria, yet their functions in these photosynthetic organisms are still not fully understood. We have previously reported that the vitamin E deficient 2 (vte2) mutant of Arabidopsis thaliana is sensitive to low temperature (LT) due to impaired transfer cell wall (TCW) development and photoassimilate export associated with massive callose deposition in transfer cells of the phloem. To further understand the roles of tocopherols in LT induced TCW development we compared the global transcript profiles of vte2 and wild-type leaves during LT treatment. Tocopherol deficiency had no significant impact on global gene expression in permissive conditions, but significantly affected expression of 77 genes after 48 h of LT treatment. In vte2 relative to wild type, genes associated with solute transport were repressed, while those involved in various pathogen responses and cell wall modifications, including two members of callose synthase gene family, GLUCAN SYNTHASE LIKE 4 (GSL4) and GSL11, were induced. However, introduction of gsl4 or gsl11 mutations individually into the vte2 background did not suppress callose deposition or the overall LT-induced phenotypes of vte2. Intriguingly, introduction of a mutation disrupting GSL5, the major GSL responsible for pathogen-induced callose deposition, into vte2 substantially reduced vascular callose deposition at LT, but again had no effect on the photoassimilate export phenotype of LT-treated vte2. These results suggest that GSL5 plays a major role in TCW callose deposition in LT-treated vte2 but that this GSL5-dependent callose deposition is not the primary cause of the impaired photoassimilate export phenotype.

Highlights

Tocopherols are essential nutrients in mammals and, together with tocotrienols, are collectively known as vitamin E (Evans and Bishop, 1922; Bramley et al, 2000; Schneider, 2005)
TOCOPHEROL DEFICIENCY HAS LITTLE IMPACT ON GLOBAL GENE EXPRESSION AT PERMISSIVE CONDITIONS To identify changes in gene expression that might be related to the absence of tocopherols, global transcript profiles were compared between vte2 and Col plants grown under permissive conditions for 4 weeks, when they are physiologically and biochemically indistinguishable, and at two time points of low temperature (LT) treatment (48 and 120 h) selected based on our previous timecourse study of the physiological and biochemical changes of vte2 and Col during LT treatment (Maeda et al, 2006)
Immunolabeling of www.frontiersin.org callose was sometimes present but mostly rare to absent in all cell types of Col and gsl5 (Figures 6E,F). These results indicate that GSL5 is responsible for the bulk of detectable callose deposition in LT treated vte2 (Figure 5A), callose synthase(s) other than GSL5 initiate the LT-induced callose deposition in transfer cells of vte2 that may associate with the inhibition of photoassimilate export capacity in vte2

Summary

Introduction

Tocopherols are essential nutrients in mammals and, together with tocotrienols, are collectively known as vitamin E (Evans and Bishop, 1922; Bramley et al, 2000; Schneider, 2005). The tocopherol-deficient vte (vitamin e 2) mutant of Arabidopsis thaliana is defective in homogentisate phytyl transferase (HPT), the first committed enzyme of the pathway, and lacks all tocopherols and pathway intermediates (Collakova and DellaPenna, 2001; Savidge et al, 2002; Sattler et al, 2004; Mene-Saffrane et al, 2010). The vte mutants exhibit reduced seed viability and defective seedling development associated with elevated lipid peroxidation (Sattler et al, 2004; Mene-Saffrane et al, 2010; DellaPenna and Mene-Saffrane, 2011), demonstrating that a primary role of tocopherols is to limit non-enzymatic lipid oxidation of polyunsaturated fatty acids (PUFAs), especially during seed desiccation and seedling germination. Transcript profiling studies further confirmed the importance of non-enzymatic lipid oxidation in triggering the oxidative and defense responses in germinating seeds of vte (Sattler et al, 2006)

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