For more than 200 years, the plant hormone salicylic acid (SA) has been studied for its medicinal use in humans. However, its extensive signaling role in plants, particularly in defense against pathogens, has only become evident during the past 20 years. This review surveys how SA in plants regulates both local disease resistance mechanisms, including host cell death and defense gene expression, and systemic acquired resistance (SAR). Genetic studies reveal an increasingly complex network of proteins required for SA-mediated defense signaling, and this process is amplified by several regulatory feedback loops. The interaction between the SA signaling pathway and those regulated by other plant hormones and/or defense signals is also discussed.

Salicylic Acid, a multifaceted hormone to combat disease.

ROS signaling: the new wave?

Reactive oxygen species (ROS) play an integral role as signalling molecules in the regulation of numerous biological processes such as growth, development, and responses to biotic and/or abiotic stimuli in plants. To some extent, various functions of ROS signalling are attributed to differences in the regulatory mechanisms of respiratory burst oxidase homologues (RBOHs) that are involved in a multitude of different signal transduction pathways activated in assorted tissue and cell types under fluctuating environmental conditions. Recent findings revealed that stress responses in plants are mediated by a temporal-spatial coordination between ROS and other signals that rely on production of stress-specific chemicals, compounds, and hormones. In this review we will provide an update of recent findings related to the integration of ROS signals with an array of signalling pathways aimed at regulating different responses in plants. In particular, we will address signals that confer systemic acquired resistance (SAR) or systemic acquired acclimation (SAA) in plants.

ROS as key players in plant stress signalling

The redox state of the chloroplast and mitochondria, the two main powerhouses of photosynthesizing eukaryotes, is maintained by a delicate balance between energy production and consumption, and affected by the need to avoid increased production of reactive oxygen species (ROS). These demands are especially critical during exposure to extreme environmental conditions, such as high light (HL) intensity, heat, drought or a combination of different environmental stresses. Under these conditions, ROS and redox cues, generated in the chloroplast and mitochondria, are essential for maintaining normal energy and metabolic fluxes, optimizing different cell functions, activating acclimation responses through retrograde signalling, and controlling whole-plant systemic signalling pathways. Regulation of the multiple redox and ROS signals in plants requires a high degree of coordination and balance between signalling and metabolic pathways in different cellular compartments. In this review, we provide an update on ROS and redox signalling in the context of abiotic stress responses, while addressing their role in retrograde regulation, systemic acquired acclimation and cellular coordination in plants.

https://onlinelibrary.wiley.com/doi/pdf/10.1111/j.1365-3040.2011.02336.x

ROS and redox signalling in the response of plants to abiotic stress

Reactive oxygen species (ROS) have multifaceted roles in the orchestration of plant gene expression and gene-product regulation. Cellular redox homeostasis is considered to be an “integrator” of information from metabolism and the environment controlling plant growth and acclimation responses, as well as cell suicide events. The different ROS forms influence gene expression in specific and sometimes antagonistic ways. Low molecular antioxidants (e.g., ascorbate, glutathione) serve not only to limit the lifetime of the ROS signals but also to participate in an extensive range of other redox signaling and regulatory functions. In contrast to the low molecular weight antioxidants, the “redox” states of components involved in photosynthesis such as plastoquinone show rapid and often transient shifts in response to changes in light and other environmental signals. Whereas both types of “redox regulation” are intimately linked through the thioredoxin, peroxiredoxin, and pyridine nucleotide pools, they ...

Redox Regulation in Photosynthetic Organisms: Signaling, Acclimation, and Practical Implications

Plants are simultaneously exposed to abiotic and biotic hazards. Here, we show that local and systemic acclimation in Arabidopsis thaliana leaves in response to excess excitation energy (EEE) is associated with cell death and is regulated by specific redox changes of the plastoquinone (PQ) pool. These redox changes cause a rapid decrease of stomatal conductance, global induction of ASCORBATE PEROXIDASE2 and PATHOGEN RESISTANCE1, and increased production of reactive oxygen species (ROS) and ethylene that signals through ETHYLENE INSENSITIVE2 (EIN2). We provide evidence that multiple hormonal/ROS signaling pathways regulate the plant's response to EEE and that EEE stimulates systemic acquired resistance and basal defenses to virulent biotrophic bacteria. In the Arabidopsis LESION SIMULATING DISEASE1 (lsd1) null mutant that is deregulated for EEE acclimation responses, propagation of EEE-induced programmed cell death depends on the plant defense regulators ENHANCED DISEASE SUSCEPTIBILITY1 (EDS1) and PHYTOALEXIN DEFICIENT4 (PAD4). We find that EDS1 and PAD4 operate upstream of ethylene and ROS production in the EEE response. The data suggest that the balanced activities of LSD1, EDS1, PAD4, and EIN2 regulate signaling of programmed cell death, light acclimation, and holistic defense responses that are initiated, at least in part, by redox changes of the PQ pool.

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Chloroplast Signaling and LESION SIMULATING DISEASE1 Regulate Crosstalk between Light Acclimation and Immunity in Arabidopsis

Aerenchyma tissues form gas-conducting tubes that provide roots with oxygen under hypoxic conditions. Although aerenchyma have received considerable attention in Zea mays, the signaling events and genes controlling aerenchyma induction remain elusive. Here, we show that Arabidopsis thaliana hypocotyls form lysigenous aerenchyma in response to hypoxia and that this process involves H2O2 and ethylene signaling. By studyingArabidopsis mutants that are deregulated for excess light acclimation, cell death, and defense responses, we find that the formation of lysigenous aerenchyma depends on the plant defense regulators LESIONSIMULATINGDISEASE1 (LSD1),ENHANCEDDISEASESUSCEPTIBILITY1 (EDS1), andPHYTOALEXINDEFICIENT4 (PAD4) that operate upstream of ethylene and reactive oxygen species production. The obtained results indicate that programmed cell death of lysigenous aerenchyma in hypocotyls occurs in a similar but independent manner from the foliar programmed cell death. Thus, the induction of aerenchyma is subject to a genetic and tissue-specific program. The data lead us to conclude that the balanced activities of LSD1, EDS1, and PAD4 regulate lysigenous aerenchyma formation in response to hypoxia.

Lysigenous aerenchyma formation in Arabidopsis is controlled by LESION SIMULATING DISEASE1.

Actinorhizal root nodule symbioses are very diverse, and the symbiosis of Datisca glomerata has previously been shown to have many unusual aspects. In order to gain molecular information on the infection mechanism, nodule development and nodule metabolism, we compared the transcriptomes of D. glomerata roots and nodules. Root and nodule libraries representing the 3′-ends of cDNAs were subjected to high-throughput parallel 454 sequencing. To identify the corresponding genes and to improve the assembly, Illumina sequencing of the nodule transcriptome was performed as well. The evaluation revealed 406 differentially regulated genes, 295 of which (72.7%) could be assigned a function based on homology. Analysis of the nodule transcriptome showed that genes encoding components of the common symbiosis signaling pathway were present in nodules of D. glomerata, which in combination with the previously established function of SymRK in D. glomerata nodulation suggests that this pathway is also active in actinorhizal Cucurbitales. Furthermore, comparison of the D. glomerata nodule transcriptome with nodule transcriptomes from actinorhizal Fagales revealed a new subgroup of nodule-specific defensins that might play a role specific to actinorhizal symbioses. The D. glomerata members of this defensin subgroup contain an acidic C-terminal domain that was never found in plant defensins before.

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Comparison of the nodule vs. root transcriptome of the actinorhizal plant Datisca glomerata: actinorhizal nodules contain a specific class of defensins.

Marian Plaszczyca

Papers

Chloroplast Signaling and LESION SIMULATING DISEASE1 Regulate Crosstalk between Light Acclimation and Immunity in Arabidopsis

Lysigenous aerenchyma formation in Arabidopsis is controlled by LESION SIMULATING DISEASE1.

Comparison of the nodule vs. root transcriptome of the actinorhizal plant Datisca glomerata: actinorhizal nodules contain a specific class of defensins.