The redox state of the apoplast influences the acclimation of photosynthesis and leaf metabolism to changing irradiance

Abstract

The redox state of the apoplast is largely determined by ascorbate oxidase (AO) activity. The influence of AO activity on leaf acclimation to changing irradiance was explored in wild‐type (WT) and transgenic tobacco (Nicotiana tobaccum) lines containing either high [pumpkin AO (PAO)] or low [tobacco AO (TAO)] AO activity at low [low light (LL); 250 μmol m−2 s−1] and high [high light (HL); 1600 μmol m−2 s−1] irradiance and following the transition from HL to LL. AO activities changed over the photoperiod, particularly in the PAO plants. AO activity had little effect on leaf ascorbate, which was significantly higher under HL than under LL. Apoplastic ascorbate/dehydroascorbate (DHA) ratios and threonate levels were modified by AO activity. Despite decreased levels of transcripts encoding ascorbate synthesis enzymes, leaf ascorbate increased over the first photoperiod following the transition from HL to LL, to much higher levels than LL‐grown plants. Photosynthesis rates were significantly higher in the TAO leaves than in WT or PAO plants grown under HL but not under LL. Sub‐sets of amino acids and fatty acids were lower in TAO and WT leaves than in the PAO plants under HL, and following the transition to LL. Light acclimation processes are therefore influenced by the apoplastic as well as chloroplastic redox state.

Redox Control of Aphid Resistance through Altered Cell Wall Composition and Nutritional Quality

“…A twoway ANOVA was used to identify transcripts that were altered significantly in abundance in relation to genotype or as a result of aphid infestation. Only a relatively small number of transcripts (132) showed differential regulation with regard to genotype, in agreement with our previous report (Karpinska et al, 2017;Supplemental Table S1). In contrast, aphid infestation had a greater influence on the leaf transcriptome, with more than 1,100 transcripts exhibiting significantly different abundance in response to aphid infestation (Supplemental Table S2).…”

“…Discrete changes in the ascorbate-DHA ratios of the apoplast/cell wall compartment were facilitated by alterations in the levels of AO activity without any significant effects on the whole-leaf ascorbate pool, as shown previously (Pignocchi et al, , 2006Karpinska et al, 2017). The relative abundance of a small number of leaf transcripts, such as those involved in amino acid metabolism, and metabolites such as oxalate were changed in response to changes in AO activity.…”

“…Changes in photosynthetic gene expression are an almost universal plant response to insect attack (Kerchev et al, 2012b); however, little is known regarding how specific changes may influence plantinsect interactions. The data presented here suggest that the redox state of the apoplast exerts an influence over photosynthetic gene expression in response to aphid perception, as has been observed in response to light (Karpinska et al, 2017).…”

“…We have discussed the details of the transcript changes related to AO activity previously (Karpinska et al, 2017;Supplemental Table S1), so we will not discuss these features in detail here, except to mention that RBOHF and a calcium channel protein associated with plant defenses to fungal pathogens were differentially expressed in relation to AO activity (Pignocchi et al, 2006). We have shown previously that, while the leaves of the PAO lines show constitutive activation of the MAPK signaling coupled to the decreased expression of the calcium channel NtTPC1B, which encodes a voltageoperated calcium channel that is activated by hydrogen peroxide, the TAO line lower expression showed increased resistance to a virulent strain of Pseudomonas syringae (Pignocchi et al, 2006).…”

“…In the following studies, the level of oxidation of the apoplast was changed by altering the level of AO and, hence, the availability of ascorbate in the apoplast. Transgenic tobacco (Nicotiana tabacum) plants that either express a tobacco AO gene in the antisense (TAO) orientation and therefore have low AO activity or that express a pumpkin (Cucurbita maxima) AO gene (PAO) and thus have high levels of AO compared with the wild type Karpinska et al, 2017) were used to determine whether the apoplastic redox state plays a specific role in limiting infestation by the generalist aphid Myzus persicae. We have shown previously that the differences in maximal extractable leaf AO activities in PAO and TAO leaves result in large changes in the ascorbate and dehydroascorabte (DHA) contents of the apoplast without having any significant effects on the total ascorbate pool of the whole leaf ascorbate or leaf ascorbate-DHA ratios Karpinska et al, 2017).…”