Light acclimation, retrograde signalling, cell death and immune defences in plants

Karpiński, Stanisław; Szechyńska‐Hebda, Magdalena; Wituszyńska, Weronika; Burdiak, Paweł

doi:10.1111/pce.12018

Cited by 161 publications

(178 citation statements)

References 68 publications

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“…One possibility is that CEF may be at least partly regulated by H 2 O 2 (26), which is produced by the light reactions of photosynthesis and already known to regulate other cellular processes such as plant growth, development, and defense (30)(31)(32). Based on in vitro studies, it was previously proposed that H 2 O 2 could activate CEF or chlororespiration by modifying the NDH complex (27).…”

Section: Significancementioning

confidence: 99%

Activation of cyclic electron flow by hydrogen peroxide in vivo

Strand

Livingston

Satoh-Cruz

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

124

116

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Cyclic electron flow (CEF) around photosystem I is thought to balance the ATP/NADPH energy budget of photosynthesis, requiring that its rate be finely regulated. The mechanisms of this regulation are not well understood. We observed that mutants that exhibited constitutively high rates of CEF also showed elevated production of H 2 O 2 . We thus tested the hypothesis that CEF can be activated by H 2 O 2 in vivo. CEF was strongly increased by H 2 O 2 both by infiltration or in situ production by chloroplastlocalized glycolate oxidase, implying that H 2 O 2 can activate CEF either directly by redox modulation of key enzymes, or indirectly by affecting other photosynthetic processes. CEF appeared with a half time of about 20 min after exposure to H 2 O 2 , suggesting activation of previously expressed CEF-related machinery. H 2 O 2 -dependent CEF was not sensitive to antimycin A or loss of PGR5, indicating that increased CEF probably does not involve the PGR5-PGRL1 associated pathway. In contrast, the rise in CEF was not observed in a mutant deficient in the chloroplast NADPH:PQ reductase (NDH), supporting the involvement of this complex in CEF activated by H 2 O 2 . We propose that H 2 O 2 is a missing link between environmental stress, metabolism, and redox regulation of CEF in higher plants. I n oxygenic photosynthesis, linear electron flow (LEF) is the process by which light energy is captured to drive the extraction of electrons and protons from water and transfer them through a system of electron carriers to reduce NADPH. LEF is coupled to proton translocation into the thylakoid lumen, generating an electrochemical gradient of protons ðΔμ H +Þ or proton motive force (pmf). The pmf drives the synthesis of ATP to power the reactions of the Calvin-Benson-Bassham (CBB) cycle and other essential metabolic processes in the chloroplast. The pmf is also a key regulator of photosynthesis in that it activates the photoprotective q E response to dissipate excess light energy and downregulates electron transfer by controlling the rate of oxidation of plastoquinol at the cytochrome b 6 f complex (b 6 f), thus preventing the buildup of reduced intermediates (1, 2).LEF results in the transfer or deposition into the lumen of three protons for each electron transferred through PSII, plastoquinone (PQ), b 6 f, plastocyanin, and photosystem I (PSI) to ferredoxin (Fd). The synthesis of one ATP is thought to require the passage of 4.67 protons through the ATP synthase, so that LEF should produce a ratio of ATP/NADPH of about 1.33; this ratio is too low to sustain the CBB cycle or supply ATP required for translation, protein transport, or other ATP-dependent processes (3). In addition, the relative demands for ATP and NADPH can change dramatically depending on environmental, developmental, and other factors, leading to rapid energy imbalances that require dynamical regulation of ATP/NADPH balance.Several alternative electron flow pathways in the chloroplast have been proposed to augment ATP production, thus balancing the ATP/NADPH ...

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Section: Significancementioning

confidence: 99%

Activation of cyclic electron flow by hydrogen peroxide in vivo

Strand

Livingston

Satoh-Cruz

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

124

116

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“…Thus, PsbS inversely regulates plant biomass production and susceptibility to herbivore attack. Plant exposure to HL causes a reduction in the photosynthetic electron transport chain components, and overproduction of ROS in the chloroplast, cytoplasm, and apoplast (Karpiński et al 2013). Such imbalances in the photosynthetic apparatus promote the formation of not only ROS but also induce an array of defence related genes.…”

Section: Discussionmentioning

confidence: 99%

Cross-talk between high light stress and plant defence to the two-spotted spider mite in Arabidopsis thaliana

et al. 2017

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Little is known about how plants deal with arthropod herbivores under the fluctuating light intensity and spectra which occur in natural environments. Moreover, the role of simultaneous stress such as excess light (EL) in the regulation of plant responses to herbivores is poorly characterized. In the current study, we focused on a mite-herbivore, specifically, the two-spotted spider mite (TSSM), which is one of the major agricultural pests worldwide. Our results showed that TSSM-induced leaf damage (visualized by trypan blue staining) and oviposition rate (measured as daily female fecundity) decreased after EL pre-treatment in wild-type Arabidopsis plants, but the observed responses were not wavelength specific. Thus, we established that EL pre-treatment reduced Arabidopsis susceptibility to TSSM infestation. Due to the fact that a portion of EL energy is dissipated by plants as heat in the mechanism known as non-photochemical quenching (NPQ) of chlorophyll fluorescence, we tested an Arabidopsis npq4-1 mutant impaired in NPQ. We showed that npq4-1 plants are significantly less susceptible to TSSM feeding activity, and this result was not dependent on light pre-treatment. Therefore, our findings strongly support the role of light in plant defence against TSSM, pointing to a key role for a photoprotective mechanism such as NPQ in this regulation. We hypothesize that plants impaired in NPQ are constantly primed to mite attack, as this seems to be a universal evolutionarily conserved mechanism for herbivores.

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“…Within this context, the redox states of the plastoquinone (PQ) pool and the cytochrome b 6 ,f complex are important in the short-term control of electron transport and in the longer-term adjustments of membrane protein content and composition through the regulation of gene expression [5,31]. The protein kinase STN7 is associated with the cytochrome b 6 ,f complex.…”

Section: (A) Chloroplast Redox Signalsmentioning

confidence: 99%

“…Cross-tolerance phenomena are often associated with the accumulation of reactive oxygen species (ROS) and altered redox and phytohormone signalling, particularly through ethylene (ET), salicylic acid (SA), abscisic acid (ABA) and jasmonate (JA)-mediated pathways [11][12][13][14]. Chloroplasts play an important role in redox signalling events linking light acclimation responses to immunity to pathogens as well as in the synthesis of important plant hormones such as ABA, JA and strigolactones [5][6][7][8][9][10][11][15][16][17]. Moreover, chloroplasts play an important role in systemic as well as local signals, facilitating a whole plant response to the high light experienced by a single leaf, a process that is called systemic acquired acclimation or systemic acquired resistance (SAR) [6,7].…”

Section: Introductionmentioning

confidence: 99%

“…Chloroplast-to-nucleus retrograde signalling is important for acclimation and defence responses [6,7,15,[18][19][20][21][22][23][24][25][26]. Many metabolites such as intermediates of tetrapyrrole biosynthesis such as Mg-ProtoIX, haem, 3 0 -phosphoadenosine 5 0 -phosphate (PAP); b-cyclocitral, ROS and methylerythritol cyclodiphosphate are considered to act as signalling molecules involved in the transmission of signals to the nucleus [18][19][20][21][22][23][24][25][26].…”

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

The functions of WHIRLY1 and REDOX-RESPONSIVE TRANSCRIPTION FACTOR 1 in cross tolerance responses in plants: a hypothesis

Foyer

Karpińska

Krupinska

2014

Phil. Trans. R. Soc. B

121

112

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Chloroplasts are important sensors of environment change, fulfilling key roles in the regulation of plant growth and development in relation to environmental cues. Photosynthesis produces a repertoire of reductive and oxidative (redox) signals that provide information to the nucleus facilitating appropriate acclimation to a changing light environment. Redox signals are also recognized by the cellular innate immune system allowing activation of non-specific, stress-responsive pathways that underpin cross tolerance to biotic–abiotic stresses. While these pathways have been intensively studied in recent years, little is known about the different components that mediate chloroplast-to-nucleus signalling and facilitate cross tolerance phenomena. Here, we consider the properties of the WHIRLY family of proteins and the REDOX-RESPONSIVE TRANSCRIPTION FACTOR 1 (RRTF1) in relation to chloroplast redox signals that facilitate the synergistic co-activation of gene expression pathways and confer cross tolerance to abiotic and biotic stresses. We propose a new hypothesis for the role of WHIRLY1 as a redox sensor in chloroplast-to-nucleus retrograde signalling leading to cross tolerance, including acclimation and immunity responses. By virtue of its association with chloroplast nucleoids and with nuclear DNA, WHIRLY1 is an attractive candidate coordinator of the expression of photosynthetic genes in the nucleus and chloroplasts. We propose that the redox state of the photosynthetic electron transport chain triggers the movement of WHIRLY1 from the chloroplasts to the nucleus, and draw parallels with the regulation of NONEXPRESSOR OF PATHOGENESIS-RELATED GENES 1 (NPR1).

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Light acclimation, retrograde signalling, cell death and immune defences in plants

Cited by 161 publications

References 68 publications

Activation of cyclic electron flow by hydrogen peroxide in vivo

Activation of cyclic electron flow by hydrogen peroxide in vivo

Cross-talk between high light stress and plant defence to the two-spotted spider mite in Arabidopsis thaliana

The functions of WHIRLY1 and REDOX-RESPONSIVE TRANSCRIPTION FACTOR 1 in cross tolerance responses in plants: a hypothesis

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