When exposed to unfavorable environmental conditions, plants can absorb light energy in excess of their photosynthetic capacities, with the surplus energy leading to the production of reactive oxygen species and photooxidative stress. Subsequent lipid peroxidation generates toxic reactive carbonyl species whose accumulation culminates in cell death. β-Cyclocitral, an oxidized by-product of β-carotene generated in the chloroplasts, mediates a protective retrograde response that lowers the levels of toxic peroxides and carbonyls, limiting damage to intracellular components. In this study, we elucidate the molecular mechanism induced by β-cyclocitral in Arabidopsis thaliana and show that the xenobiotic detoxification response is involved in the tolerance to excess light energy. The involvement of the xenobiotic response suggests a possible origin for this pathway. Furthermore, we establish the hierarchical structure of this pathway that is mediated by the β-cyclocitralinducible GRAS protein SCARECROW LIKE14 (SCL14) and involves ANAC102 as a pivotal component upstream of other ANAC transcription factors and of many enzymes of the xenobiotic detoxification response. Finally, the SCL14-dependent protective mechanism is also involved in the low sensitivity of young leaf tissues to high-light stress.
Singlet oxygen ( O ) signalling in plants is essential to trigger both acclimatory mechanisms and programmed cell death under high light stress. However, because of its chemical features, O requires mediators, and the players involved in this pathway are largely unknown. The β-carotene oxidation product, β-cyclocitral, is one such mediator. Produced in the chloroplast, β-cyclocitral induces changes in nuclear gene expression leading to photoacclimation. Recently, the METHYLENE BLUE SENSITIVITY protein MBS has been identified as a key player in O signalling leading to tolerance to high light. Here, we provide evidence that MBS1 is essential for acclimation to O and cross-talks with β-cyclocitral to mediate transfer of the O signal to the nucleus, leading to photoacclimation. The presented results position MBS1 downstream of β-cyclocitral in O signalling and suggest an additional role for MBS1 in the regulation of plant growth and development under chronic O production.
Summary β-Cyclocitral (β-CC) is a volatile compound deriving from 1 O 2 oxidation of β-carotene in plant leaves. β-CC elicits a retrograde signal, modulating 1 O 2 -responsive genes and enhancing tolerance to photooxidative stress. Here, we show that β-CC is converted into water-soluble β-cyclocitric acid (β-CCA) in leaves. This metabolite is a signal that enhances plant tolerance to drought by a mechanism different from known responses such as stomatal closure, osmotic potential adjustment, and jasmonate signaling. This action of β-CCA is a conserved mechanism, being observed in various plant species, and it does not fully overlap with the β-CC-dependent signaling, indicating that β-CCA induces only a branch of β-CC signaling. Overexpressing SCARECROW-LIKE14 (SCL14, a regulator of xenobiotic detoxification) increased drought tolerance and potentiated the protective effect of β-CCA, showing the involvement of the SCL14-dependent detoxification in the phenomenon. β-CCA is a bioactive apocarotenoid that could potentially be used to protect crop plants against drought.
Stressful environmental conditions lead to the production of reactive oxygen species in the chloroplasts, due to limited photosynthesis and enhanced excitation pressure on the photosystems. Among these reactive species, singlet oxygen ( 1 O 2 ), which is generated at the level of the PSII reaction center, is very reactive, readily oxidizing macromolecules in its immediate surroundings, and it has been identified as the principal cause of photooxidative damage in plant leaves. The two b-carotene molecules present in the PSII reaction center are prime targets of 1 O 2 oxidation, leading to the formation of various oxidized derivatives. Plants have evolved sensing mechanisms for those PSII-generated metabolites, which regulate gene expression, putting in place defense mechanisms and alleviating the effects of PSII-damaging conditions. A new picture is thus emerging which places PSII as a sensor and transducer in plant stress resilience through its capacity to generate signaling metabolites under excess light energy. This review summarizes new advances in the characterization of the apocarotenoids involved in the PSIImediated stress response and of the pathways elicited by these molecules, among which is the xenobiotic detoxification.
Distinct ROS signaling pathways initiated by singlet oxygen ( 1 O 2 ) or superoxide and hydrogen peroxide have been attributed to either cell death or acclimation, respectively. Recent studies have revealed that more complex antagonistic and synergistic relationships exist within and between these pathways. As specific chloroplastic ROS signals are difficult to study, rapid systemic signaling experiments using localized high light (HL) stress or ROS treatments were used in this study to uncouple signals required for direct HL and ROS perception and distal systemic acquired acclimation (SAA). A qPCR approach was chosen to determine local perception and distal signal reception. Analysis of a thylakoidal ascorbate peroxidase mutant (tapx), the 1 O 2 -retrograde signaling double mutant (ex1/ex2), and an apoplastic signaling double mutant (rbohD/F) revealed that tAPX and EXECUTER 1 are required for both HL and systemic acclimation stress perception. Apoplastic membrane-localized RBOHs were required for systemic spread of the signal but not for local signal induction in directly stressed tissues. Endogenous ROS treatments revealed a very strong systemic response induced by a localized 1 h induction of 1 O 2 using the conditional flu mutant. A qPCR time course of 1 O 2 induced systemic marker genes in directly and indirectly connected leaves revealed a direct vascular connection component of both immediate and longer term SAA signaling responses. These results reveal the importance of an EXECUTER-dependent 1 O 2 retrograde signal for both local and long distance RBOH-dependent acclimation signaling that is distinct from other HL signaling pathways, and that direct vascular connections have a role in spatial-temporal SAA induction.
Capturing light intensities exceeding the capacity of photosynthesis can lead to cell death in plant leaves. In this review, we summarize recent findings on the mechanisms mediating light-induced cell death, highlighting the role of reactive carbonyl species, of the endoplasmic reticulum and of phytohormones in the adoption of phototolerance versus cell death pathways.
We investigated the potential plant growth-promoting traits of 377 culturable endophytic bacteria, isolated from Vitis vinifera cv. Glera, as good biofertilizer candidates in vineyard management. Endophyte ability in promoting plant growth was assessed in vitro by testing ammonia production, phosphate solubilization, indole-3-acetic acid (IAA) and IAA-like molecule biosynthesis, siderophore and lytic enzyme secretion. Many of the isolates were able to mobilize phosphate (33%), release ammonium (39%), secrete siderophores (38%) and a limited part of them synthetized IAA and IAA-like molecules (5%). Effects of each of the 377 grapevine beneficial bacteria on Arabidopsis thaliana root development were also analyzed to discern plant growth-promoting abilities (PGP) of the different strains, that often exhibit more than one PGP trait. A supervised model-based clustering analysis highlighted six different classes of PGP effects on root architecture. A. thaliana DR5::GUS plantlets, inoculated with IAA-producing endophytes, resulted in altered root growth and enhanced auxin response. Overall, the results indicate that the Glera PGP endospheric culturable microbiome could contribute, by structural root changes, to obtain water and nutrients increasing plant adaptation and survival. From the complete cultivable collection, twelve promising endophytes mainly belonging to the Bacillus but also to Micrococcus and Pantoea genera, were selected for further investigations in the grapevine host plants towards future application in sustainable management of vineyards.
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