**3. Photosynthesis under biotic stress: How is it regulated?**

#### **3.1 Integration of metabolic, hormonal and environmental signals in stress acclimation and retrograde signaling**

Plants are able to integrate and evaluate a diversity of input signals to optimize acclimation responses to stressful environmental growth conditions and to ensure plant survival. Frequently observed adaptation responses are growth retardation, reduced metabolism and photosynthesis, reallocation of metabolic resources and increased antioxidant capacity. Cumulative evidence showing strong stress-related effects on ROS and auxin levels, coupled with the stress-induced morphogenetic changes often produced during adaptation, indicate that these physiologically active metabolites play a prominent role in the integration of the stress-regulatory networks, acting through mechanisms that remain poorly understood (Tognetti et al., 2011). The elaborate ROS signaling network is also known to act in concert with other hormonal networks and with plastid signaling to regulate developmental

signaling pathways that are active under low or high light. These can lead to rapid state transitions, involving reversible association of the mobile pool of LHCII to PSI or PSII, or LTR. Qo (red oval) represents the docking site where plastoquinol binds to the cytochrome *b6f* complex. Both processes are dependent on the redox-regulated activity of the STN7 kinase (possibly in conjunction with STN8; purple letters). The TAP38 phosphatase (in red letters) regulates state transitions by specifically dephosphorylating LHCII. On the other hand, LTR involves chloroplast and nuclear gene expression (purple arrows). LTRdependent plastid gene expression is believed to be regulated by the *Chloroplast Sensor Kinase* (CSK, in purple letters), while nuclear gene expression might require a putative LTR signal (in purple box). LTR-dependent changes in gene expression and protein accumulation

can also lead to the establishment of two distinct metabolic states (purple letters, in

from Kleine et al., 2009, Pfannschmidt et al., 2009, and Pesaresi et al., 2010).

**3.1 Integration of metabolic, hormonal and environmental signals in stress** 

Plants are able to integrate and evaluate a diversity of input signals to optimize acclimation responses to stressful environmental growth conditions and to ensure plant survival. Frequently observed adaptation responses are growth retardation, reduced metabolism and photosynthesis, reallocation of metabolic resources and increased antioxidant capacity. Cumulative evidence showing strong stress-related effects on ROS and auxin levels, coupled with the stress-induced morphogenetic changes often produced during adaptation, indicate that these physiologically active metabolites play a prominent role in the integration of the stress-regulatory networks, acting through mechanisms that remain poorly understood (Tognetti et al., 2011). The elaborate ROS signaling network is also known to act in concert with other hormonal networks and with plastid signaling to regulate developmental

**3. Photosynthesis under biotic stress: How is it regulated?** 

**acclimation and retrograde signaling** 

*cytoplasm*) derived from the exposure to either PSI or PSII light (yellow letters and arrows). ROS are generated by transfer of electrons from PSI or reduced ferredoxin (Fd) to oxygengenerating superoxide (O2-, in black letters). This is detoxified by superoxide dismutase (SOD, in black letters) to hydrogen peroxide (H2O2; in black letters). Un-scavenged H2O2 might able to diffuse freely across the chloroplast envelope or through water channels (or aquaporins, A; blue letter in blue circle) and is thought to start MAP kinase cascades in the cytosol. Singlet oxygen (1O2; in black letters), is generated at PSII. Its high reactivity and short half-life require additional signaling components, such as Executer 1 and 2 (EX1, EX2, in black letters), although evidence in green algae suggests that 1O2 might be able to diffuse out of the chloroplast*. Metabolic* plastid signaling has been proposed to require the activity of the malate/oxaloacetate (MOT; in green letters) and triosephosphate (TPT; in green letters) translocators needed for the export of excess reducing power and ATP from the chloroplast. Alternatively, metabolite concentration changes (e.g., glucose originated from the Calvin cycle; green letters) could be sensed by cytosolic or nuclear receptors (i.e. hexokinase; HK, green letters in yellow circle) to modify nuclear gene expression. Abscisic acid (ABA, in orange letters) whose synthesis is derived from ROS-sensitive xanthophyll precursors (XP, in orange letters) in the chloroplast, has also been proposed to act as a signal relying information on the chloroplast status to the nucleus. Dotted arrows represent pathways mediated by unknown components that have not been entirely elucidated. Tetrapyrrole and ROS-scavenging-associated signaling pathways are not shown (Adapted

processes, in addition to abiotic and biotic stress tolerance responses (Kleine et al., 2009; Tognetti et al., 2011). For instance, the local and systemic acclimation in Arabidopsis leaves in response to excess excitation energy associated with cell death and regulated by specific redox changes of the PQ pool, also caused a rapid decrease of stomatal conductance, global induction of genes involved in ROS scavenging and pathogen resistance, increased ROS production and enhanced ethylene signaling. In addition, evidence was provided which showed that multiple hormonal/ROS signaling pathways not only regulate the plant's response to excess excitation energy, but also control induced systemic acquired resistance and basal defenses to virulent bacterial pathogens. The balanced activity of the disease resistance and signaling-related proteins coded by the *LSD1*, *EDS1*, *PAD4*, and *EIN2* genes was found to be necessary to regulate the steps leading to programmed cell death, light acclimation, and defense responses that are initiated, at least in part, by redox changes of the PQ pool (Mühlenbock et al., 2008). Further evidence coupling chloroplast-controlled disease resistance with ROS accumulation was obtained with the Arabidopsis mutant *rph1* (for *resistance to Phytophthora 1*), which was found to be susceptible to the pathogen *Phytophthora brassicae* as a consequence of a reduced oxidative burst, a runaway cell-death response, and failure to properly activate the expression of defense-related genes. The finding that the *RPH1* gene encodes an evolutionary highly conserved chloroplast protein was in accordance with a prominent chloroplast-dependent role in the activation of immune responses to *Phytophthora*, not only in Arabidopsis but in potato, as well (Belhaj et al., 2009).

In addition, signal integration at the level of transcription factor (TF) activation appears to be majorly controlled by the family of APETALA 2/ ethylene response element binding protein (AP2/EREBP) TFs, which are abundantly represented in Arabidopsis, poplar and rice (Dietz et al., 2010). By dint of their activation of different innervating pathways, or their ability to bind to multiple target elements, AP2/EREBP TFs are known to integrate several signaling inputs. A couple of examples are the ERF1 TF, which is controlled by ethylene and JA (Lorenzo et al., 2004), and the dehydration-responsive element binding TF TINY, that connects abiotic stress signaling via DRE-dependent regulation to biotic stress signaling via ethylene response elements (Sun et al., 2008). It is considered that combinatorial target gene regulation by different signals may involve different mechanisms, including: (i) cross-talk in the signaling pathways; (ii) stimuli-dependent TF activation, e.g. by homo- or heterotypic dimer and oligomer formation, respectively; (iii) competition for the same or binding to different cis elements; and (iv) amplification cascades that can be modulated by interfering signals (Dietz et al., 2010).
