Defense-Related Transcriptional Reprogramming in Vitamin E-Deficient Arabidopsis Mutants Exposed to Contrasting Phosphate Availability

Abstract

Vitamin E inhibits the propagation of lipid peroxidation and helps protecting photosystem II from photoinhibition, but little is known about its possible role in plant response to Pi availability. Here, we aimed at examining the effect of vitamin E deficiency in Arabidopsis thaliana vte mutants on phytohormone contents and the expression of transcription factors in plants exposed to contrasting Pi availability. Plants were subjected to two doses of Pi, either unprimed (controls) or previously exposed to low Pi (primed). In the wild type, α-tocopherol contents increased significantly in response to repeated periods of low Pi, which was paralleled by increased growth, indicative of a priming effect. This growth-stimulating effect was, however, abolished in vte mutants. Hormonal profiling revealed significant effects of Pi availability, priming and genotype on the contents of jasmonates and salicylates; remarkably, vte mutants showed enhanced accumulation of both hormones under low Pi. Furthermore, expression profiling of 1,880 transcription factors by qRT-PCR revealed a pronounced effect of priming on the transcript levels of 45 transcription factors mainly associated with growth and stress in wild-type plants in response to low Pi availability; while distinct differences in the transcriptional response were detected in vte mutants. We conclude that α-tocopherol plays a major role in the response of plants to Pi availability not only by protecting plants from photo-oxidative stress, but also by exerting a control over growth- and defense-related transcriptional reprogramming and hormonal modulation.

An altered tocopherol composition in chloroplasts reduces plant resistance to Botrytis cinerea

“…Interestingly, previous studies have shown that the vte4 mutant is also more sensitive to abiotic stress than the vte1 mutant and that the former generally responds with an enhanced stress sensitivity than the latter (Cela et al, 2011;Allu et al, 2017).…”

The Chloroplast Reactive Oxygen Species-Redox System in Plant Immunity and Disease

“…The importance of the NTRC in plant immunity is shown by elevated JA signaling and enhanced susceptibility of the ntrc Arabidopsis mutant to non-host pathogens Ishiga et al, 2016 Thioredoxin Trx-h NtTRXh3 protein localized in chloroplasts is involved in tobacco resistance to viruses by contributing to ROS scavenging and cellular reducing conditions. The redox status of thioredoxins affects nuclear gene expression by modifying chloroplasts retrograde signaling Rintamäki et al, 2009;Sun et al, 2010 Tocopherols Involved in the antioxidant protection of chloroplast membranes and in the transfer of stress signals outside the chloroplast via plastid-endoplasmic reticulum contact sites Tocopherols content and composition modulate nuclear gene expression, the profiles of defense hormones and PUFA-derived defense products Mehrshahi et al, 2014;Müller and Munné-Bosch, 2015;Allu et al, 2017;Cela et al, 2018 Apocarotenoids Chloroplast-generated signaling molecules produced by carotenoid cleavage link chloroplast activity and nuclear gene expression. They interfere with SA signaling by regulating the localization of NPR1, a redox-sensitive transcription co-activator, in the nucleus Bobik and Burch-Smith, 2015;Brunkard et al, 2015;Hou et al, 2016 Polyunsaturated fatty acids (PUFA)…”

“…Under stress, changes in the content and composition of tocopherols modulate nuclear gene expression, the profiles of SA, JA, ABA, and ET as well as the formation of defense-related lipid peroxidation products. A link between redox and hormone signaling mediated, respectively, by γ-tocopherol and Ethylene Response Factors (ERFs) which integrates ABA, JA, and ET response to infection, found in vitamin E-deficient Arabidopsis mutant, likely represents a mechanism of chloroplast to nucleus retrograde signaling ( Müller and Munné-Bosch, 2015 ; Allu et al, 2017 ). Altered tocopherol composition in chloroplasts negatively influenced Arabidopsis response to B. cinerea through enhanced lipid peroxidation and delayed defense activation ( Cela et al, 2018 ).…”

Tocopherols modulate leaf vein arrangement and composition without impacting photosynthesis

“…The majority of foliar tocopherols is -tocopherol localized in the chloroplast (Mène-Saffrané and DellaPenna 2010), and the chloroplast provides significant input into cellular redox signaling networks (Foyer and Noctor 2013). Tocopherols might directly modulate regulators such as plant hormones involved in vascular differentiation or, alternatively, interact with transcription factors that control regulators of leaf development (see Allu et al 2017). Cellular redox state regulates the activity of phytohormones such as auxins (Foyer and Noctor 2013) that are involved in vascular differentiation (Mattsson et al 2003, Scarpella andMeijer 2004).…”

“…While current efforts to limit crop losses under extreme environmental conditions (e.g., drought and unfavorable temperatures) include overexpression of antioxidant systems (for a review of efforts, see Logan et al 2006), it has been cautioned that plant response to the environment relies on oxidative signaling (Foyer and Noctor 2009; see also Demmig- Adams et al 2013,b, Kurepin et al 2013. For example, Allu et al (2017) recently reported differences in hormonal and transcriptional responses to soil phosphate availability between the vte1 mutant and wild-type A. thaliana. Additional information is, therefore, needed to understand how altered leaf antioxidant contents affect plant development and to identify possible tradeoffs in adjustments to contrasting environments.…”