Ethylene signaling triggered by low concentrations of ascorbic acid regulates biomass accumulation in Arabidopsis thaliana
Introduction
Ascorbic acid (AA) participates of many physiological processes in plants. It has a central function in plant antioxidant defenses, in the elongation and cell division and in the optimization of photosynthesis [1]. The concentration of AA changes during plant development presenting high levels in young and actively growing tissues and declining during senescence [2]. Since Homo sapiens like other primates has lost the capacity to synthesize AA, the accumulation of this antioxidant to high levels in edible plant organs is of paramount interest to human nutrition [3].
Glucose is the primary precursor for AA synthesis in different organisms [4]. However, l-galactose is considered the first metabolite exclusively committed to this pathway in plants [5]. GDP-L-galactose phosphorylase (VTC2/VTC5) catalyzes the formation of L-galactose from GDP-L-galactose. Mutant plants deficient in VTC2 still have an active homologue VTC5 protein. The reduced activity of VTC5 leads to a small contribution to this pathway and consequently vtc2 plants have very low concentration of AA [6]. Mutants with low activity of VTC2/VTC5 are very useful to study the specific role of AA in plant biology.
Phenotype modifications due to low AA were analyzed in a collection of Arabidopsis deficient mutants [7]. AA-deficient mutants are highly susceptible to the oxidative stress caused by ozone [8] but show a high level of pathogen resistance [8], [9]. In addition these AA-deficient mutants have a smaller rosette size than the wild type, altered root architecture and gravitropism and flowering time [10], [11]. AA deficient plants also show alterations in hormone metabolism and/or signaling. Higher concentrations of abscisic acid were observed in vtc mutant leaves [12]. Furthermore, an increased expression of genes associated with abscisic acid signaling was reported in AA-deficient mutants [13], together with altered expression of salicylic acid [14] and ethylene-associated genes [12]. Ethylene is an important stress hormone in plants, which inhibits growth and promotes senescence in different organs [15], [16]. While it has been suggested that the reduced growth observed in vtc2-1 mutants might segregate independently of the vtc2-1 mutation [17], this has not been substantiated in other studies using different growing conditions. Consequently, redox-dependent changes in phytohormone pathways may be responsible for some of the characteristics of vtc2 phenotype, especially those leading to slower plant growth. In the following studies, we investigated how low redox buffering capacity in two independent vtc2 mutant lines that have very low AA contents interacts with ethylene signaling to regulate photosynthesis and rosette development.
Section snippets
Plant material and treatments
Experiments were carried out with wild type Arabidopsis thaliana (L.) Heynh. (Ecotype Columbia 0, wt) and AA deficient plants (vtc2-1 and vtc2-4). Seeds of the wt and vtc2-4 T-DNA were obtained from the Nottingham Arabidopsis Stock Centre and vtc2-1 EMS from Dr Robert Last [18]. Plants were grown in a chamber under a PPFD of 120 µmol m−2 s−1, at 23 °C and a photoperiod of 10/14 h light/dark, respectively. After one month, plants were transferred to another chamber with similar conditions but
Ethylene production in plants with low concentration of AA
Both vtc2 mutants produce higher amounts of ethylene than wt plants (Fig. 1). This high level of volatile hormone production coincides with the increased levels of transcripts encoding proteins associated with ethylene signaling [12]. The synthesis of ethylene is an autocatalytic process occurring at the last stages of plant growth in order to accelerate plant senescence [15]. The increased synthesis of this hormone during the early stages (i.e. plant growth before flowering) may affect
Conclusions
The results presented here demonstrate that AA deficiency modulates ethylene emissions and signaling leading to alterations in gas diffusion and photosynthesis in vtc2 leaves (Fig. 7). Taking in consideration that 1-MCP does not substantially affect AA concentration, ethylene effects on leaf conductance is exerted by non-dependent AA-mechanisms. Since AA is a major cellular antioxidant the findings reported here are entirely consistent with the hypothesis that oxidative signals and ethylene
Acknowledgments
GGG and CGB are researchers of CONICET. Authors are thankful to Agencia Nacional de Promoción Científica y Tecnológica (PICT 2012-0809) and Consejo Nacional de Investigaciones Científicas y Técnicas (PIP 2012 – 0483) for the grants supporting our research.
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