**1. Introduction**

Photosynthesis is a central process for the survival of plants, providing essential elements for growth and reproduction. As its name implies, the excitation of chlorophyll by photons, initiates an electron current that results in the generation of NADPH and ATP, which are subsequently used by the plant to sustain growth and development. However, precise and challenging energy equilibrium between the synthesis of NADPH and ATP and the downstream reactions that consume them must be maintained to ensure that the photosynthetic process runs efficiently. This balancing act is not trivial considering the necessity to integrate extremely rapid, temperature-independent photochemical reactions with relatively slow, temperature-dependent biochemical reactions. In addition, the equilibrium can be perturbed with relative ease when plants face adverse ambient conditions, including biotic stresses, leading to negative effects on the photosynthetic apparatus and concomitant disruption of the orderly transfer of electrons to their proper final acceptors. To avoid or minimize damage, plants have developed several strategies to maintain stability, the details of which will be explored in this chapter.

Together with many other biotic stresses, insect herbivory is known to alter photosynthetic activity and/or photosynthetic gene expression levels in affected plants. The effects are predominantly negative, although compensatory responses are not uncommon. Both positive and negative effects can be detected in injured and adjacent, intact, plant tissue, which may include, in some species, photosynthetically active stems in addition to leaves. Indirect effects on photosynthesis have been clearly demonstrated with the use of fluorescence and thermal imaging system techniques. The negative insect herbivory-derived effects on photosynthesis are frequently explained by a theoretical framework constructed on the argument that the resource-rich photosynthetic apparatus is sacrificed to provide the metabolic precursors and energy needed for the proper deployment of the resource-

Friend or Foe? Exploring the Factors that Determine the Difference

2009; Mubarakshina et al., 2010).

**2.1.1 State transitions** 

**2.1 Short-term acclimation mechanisms** 

Between Positive and Negative Effects on Photosynthesis in Response to Insect Herbivory 157

molecular short-term and long-term acclimation mechanisms are deployed by photosynthetic organisms (predominantly green algae and land plants) to maintain or restore photosynthetic efficiency under adverse conditions and counteract stresses (Öquist & Huner, 2003; Ensminger et al., 2006). On a time scale of minutes, organisms can reduce the efficiency of energy transfer to PSII either by redistributing light energy to PSI at the expense of PSII through state transitions or by dissipating excess energy as heat by nonphotochemical quenching associated with the light-harvesting complex (LHC) antenna (Hüner et al., 1998; Szyszka et al., 2007). Alternatively, it has also been proposed that quenching of excess energy may occur at the reaction centers, in addition to zeaxanthindependent antenna quenching (Krause & Weis, 1991; Bukhov et al., 2001; Matsubara & Chow, 2004; Ivanov et al., 2006). Long-term acclimation responses include alterations in light harvesting antenna size and adjustments of PSI: PSII stoichiometry that balance the excitation light energy absorbed by the two photosystems (Yamazaki et al., 2005; Ozaki et al., 2007, Solanke & Sharma, 2008; Muramatsu et al., 2009). A significant body of experimental evidence indicates that redox signals from photosynthetic electron transport and reactive oxygen species (ROS) or ROS-scavenging molecules play a central role in the regulation of acclimation and stress responses (Foyer & Noctor, 2009; Pfannschmidt et al.,

State transitions represent a short-term response, occurring within a time-frame of seconds to minutes, required to balance the light excitation energy between the antennae systems of PSII and PSI which preferentially absorb 650 and 700 nm light, respectively. Because of these differences in light absorption properties, changes in light conditions, such as those happening under shaded or light-limiting conditions, or as a consequence of shifts in the spectral filtering properties of leaf canopies, can lead to unequal excitation of the two photosystems (Allen & Forsberg, 2001; Haldrup et al., 2001; Wollman, 2001; Dietzel et al., 2008; Pesaresi et al., 2010). Preferential excitation of PSI leads to the oxidation of the plastoquinone (PQ) pool and to state 1. In state 1 the mobile light-harvesting antenna is bound to PSII and the photosynthetic electron transport chain acts mostly in a linear mode generating NADPH and ATP. Preferential excitation of PSII relative to PSI leads to a reduced state of the PQ pool and thus to the docking of plastoquinol to the Qo site of the cytochrome *b6f* complex. It is the PQ redox state only, acting independently of photoreceptors (Fey et al., 2005), that then activates the so-called redox-sensitive thylakoid LHCII kinase needed to phosphorylate the peripheral LHCII "mobile pool", which then migrates laterally, as a consequence of charge repulsion, from PSII to PSI (state 2) (Lunde et al., 2000). Chemical cross-linking and RNA interference approaches performed in Arabidopsis plants maintained in state 2 have provided evidence for an association of LHCII polypeptides to a specific PSI docking domain composed of subunits PsaL, PsaH and PsaO (Lunde et al., 2000; Zhang et al., 2004; Pesaresi et al., 2010), whereas a gentle mechanical fractionation of the thylakoid membranes showed that the lateral movement of phosphorylated LHCII might be confined to a very limited portion of the thylakoid membranes, more precisely to the grana margins (Tikkanen et al., 2008). Regardless of the mechanism, the re-distribution of the light-harvesting chlorophyll to PSI at the expense of

demanding defense responses, although the concept of a down-regulated photosynthetic apparatus as a protective measure against oxidative damage has also been proposed. Jasmonic acid (JA), frequently interacting with ethylene, is recognized as the primary regulator of the defense response against defoliating insects and is strongly associated with the down-regulation of photosynthesis genes. Conversely, the mechanism(s) responsible for the compensatory photosynthetic activity that allows increased plant growth or fitness after insect herbivory are not well understood. Experimental evidence gathered to date suggests that the onset of compensatory photosynthesis may be dependent on many factors. The timing of herbivory injury, which also influences the plant's source/sink relationships along its phenology, is important. Also influential are the type of tissue damaged, the type and extension of damage, which in turn may be influenced by highly specific factors such as the composition of the herbivore´s saliva and the type of endosimbiotic bacteria colonizing the insect´s gut, the development stage of the herbivore, its feeding guild and even differences within guilds. Finally, the tolerance capacity of the plant to injury, the environmental conditions surrounding the plant, and the type of defense produced, if any, in response to herbivory, will also define whether a given assault on the plant leads to compensatory responses. The suggested role for phytochrome as a regulator of resource allocation between plant growth and anti-herbivore defense also implies its participation as a signaling element in herbivory-dependent changes in photosynthesis. Moreover, emerging data suggest that stress acclimation and chloroplast-to-nucleus signaling is mediated by phytohormones acting via AP2/EREBP transcription factors, which are believed to play a major and diversified role in environmental signal integration.

The overall perspective on the varying factors that influence the effect that insect herbivory may have on photosynthesis is that of complexity. This chapter will also concentrate on the description of these multiple factors, including emerging data that have shed light on the poorly understood mechanisms that regulate photosynthesis-related gene expression or that define how herbivore damage is interpreted by the plant, either as a "friendly" jolt to increase photosynthesis and stimulate growth and promote fitness or as an "act of war" leading to austerity measures to privilege a defense effort.
