Photosynthetic acclimation, vernalization, crop productivity and 'the grand design of photosynthesis'.

Daniel Arnon first proposed the notion of a 'grand design of photosynthesis' in 1982 to illustrate the central role of photosynthesis as the primary energy transformer for all life on Earth. However, we suggest that this concept can be extended to the broad impact of photosynthesis not only in global energy transformation but also in the regulation of plant growth, development, survival and crop productivity through chloroplast redox signalling. We compare and contrast the role of chloroplast redox imbalance, measured as excitation pressure, in governing acclimation to abiotic stress and phenotypic plasticity. Although all photoautrophs sense excessive excitation energy through changes in excitation pressure, the response to this chloroplast redox signal is species dependent. Due to a limited capacity to adjust metabolic sinks, cyanobacteria and green algae induce photoprotective mechanisms which dissipate excess excitation energy at a cost of decreased photosynthetic performance. In contrast, terrestrial, cold tolerant plants such as wheat enhance metabolic sink capacity which leads to enhanced photosynthetic performance and biomass accumulation with minimal dependence on photoprotection. We suggest that the family of nuclear C-repeat binding transcription factors (CBFs) associated with the frost resistance locus, FR2, contiguous with the vernalization locus,VRN1, and mapped to chromosome 5A of wheat, may be critical components that link leaf chloroplast redox regulation to enhanced photosynthetic performance, the accumulation of growth-active gibberellins and the dwarf phenotype during cold acclimation prior to the vegetative to reproductive transition controlled by vernalization in winter cereals. Further genetic, molecular and biochemical research to confirm these links and to elucidate the molecular mechanism by which chloroplast redox modulation of CBF expression leads to enhanced photosynthetic performance is required. Because of the superior abiotic stress tolerance of cold tolerant winter wheat and seed yields that historically exceed those of spring wheat by 30-40%, we discuss the potential to exploit winter cereals for the maintenance or perhaps even the enhancement of cereal productivity under future climate change scenarios that will be required to feed a growing human population.

Global transcriptome analyses provide evidence that chloroplast redox state contributes to intracellular as well as long-distance signalling in response to stress and acclimation in Arabidopsis.

Global transcriptome analyses were used to assess the interactive effects of short-term stress versus long-term acclimation to high light (HL), low temperature (LT) and excitation pressure in Arabidopsis. Microarray analyses indicated that exposure to stress resulted in two times as many modulated transcripts in both, high-light-treated and low-temperature-treated plants, compared to plants that were fully acclimated to either one of these conditions. We showed that 10.9 % of all transcripts were regulated in the same way by both stress conditions, and hence, were categorized as excitation pressure regulated, rather than regulated by either high-light or low-temperature stress per se. This group of chloroplast redox-sensitive genes included various photosynthetic genes as well as genes known to be associated with cold acclimation (cbf3, cor15A, cor15B) and gibberellic acid (GA) metabolism and signalling (ga2ox1, gai). Chemical inhibition of the photosynthetic electron transport by either DCMU or DBMIB indicated that although the plastoquinone pool contributes significantly to redox regulation of the transcriptome (8.6 %), it appears that PSI represents the major source of redox signals (89 %), whereas PSII appears to contribute only 3.1 %. A comparison of the gene expression profiles between stress and acclimated plants indicated that 10 % of the genes induced by a short, 1-h stress were also associated with long-term acclimation to high excitation pressure. This included the APETALA2/ETHYLENE-RESPONSIVE-BINDING PROTEIN family, the MYB domain- and MYB-related transcription factor family as well as the GRAS transcription factor family important in GA signalling confirming that acclimation to stress is a time-nested phenomenon. We suggest that acclimation to photosynthetic redox imbalance extends beyond the chloroplast and the leaf cell to systemic ROS signalling. This is discussed in terms of the control of plant phenotype through regulation of the nuclear encoded cbf regulon and GA metabolism.

Secreted fungal effector lipase releases free fatty acids to inhibit innate immunity-related callose formation during wheat head infection.

The deposition of the (1,3)-ß-glucan cell wall polymer callose at sites of attempted penetration is a common plant defense response to intruding pathogens and part of the plant's innate immunity. Infection of the Fusarium graminearum disruption mutant Δfgl1, which lacks the effector lipase FGL1, is restricted to inoculated wheat (Triticum aestivum) spikelets, whereas the wild-type strain colonized the whole wheat spike. Our studies here were aimed at analyzing the role of FGL1 in establishing full F. graminearum virulence. Confocal laser-scanning microscopy revealed that the Δfgl1 mutant strongly induced the deposition of spot-like callose patches in vascular bundles of directly inoculated spikelets, while these callose deposits were not observed in infections by the wild type. Elevated concentrations of the polyunsaturated free fatty acids (FFAs) linoleic and α-linolenic acid, which we detected in F. graminearum wild type-infected wheat spike tissue compared with Δfgl1-infected tissue, provided clear evidence for a suggested function of FGL1 in suppressing callose biosynthesis. These FFAs not only inhibited plant callose biosynthesis in vitro and in planta but also partially restored virulence to the Δfgl1 mutant when applied during infection of wheat spikelets. Additional FFA analysis confirmed that the purified effector lipase FGL1 was sufficient to release linoleic and α-linolenic acids from wheat spike tissue. We concluded that these two FFAs have a major function in the suppression of the innate immunity-related callose biosynthesis and, hence, the progress of F. graminearum wheat infection.

Role of CBFs as integrators of chloroplast redox, phytochrome and plant hormone signaling during cold acclimation.

Cold acclimation of winter cereals and other winter hardy species is a prerequisite to increase subsequent freezing tolerance. Low temperatures upregulate the expression of C-repeat/dehydration-responsive element binding transcription factors (CBF/DREB1) which in turn induce the expression of COLD-REGULATED (COR) genes. We summarize evidence which indicates that the integration of these interactions is responsible for the dwarf phenotype and enhanced photosynthetic performance associated with cold-acclimated and CBF-overexpressing plants. Plants overexpressing CBFs but grown at warm temperatures mimic the cold-tolerant, dwarf, compact phenotype; increased photosynthetic performance; and biomass accumulation typically associated with cold-acclimated plants. In this review, we propose a model whereby the cold acclimation signal is perceived by plants through an integration of low temperature and changes in light intensity, as well as changes in light quality. Such integration leads to the activation of the CBF-regulon and subsequent upregulation of COR gene and GA 2-oxidase (GA2ox) expression which results in a dwarf phenotype coupled with increased freezing tolerance and enhanced photosynthetic performance. We conclude that, due to their photoautotrophic nature, plants do not rely on a single low temperature sensor, but integrate changes in light intensity, light quality, and membrane viscosity in order to establish the cold-acclimated state. CBFs appear to act as master regulators of these interconnecting sensing/signaling pathways.

Chloroplast redox imbalance governs phenotypic plasticity: the "grand design of photosynthesis" revisited.

Sunlight, the ultimate energy source for life on our planet, enters the biosphere as a direct consequence of the evolution of photoautotrophy. Photoautotrophs must balance the light energy absorbed and trapped through extremely fast, temperature-insensitive photochemistry with energy consumed through much slower, temperature-dependent biochemistry and metabolism. The attainment of such a balance in cellular energy flow between chloroplasts, mitochondria and the cytosol is called photostasis. Photoautotrophs sense cellular energy imbalances through modulation of excitation pressure which is a measure of the relative redox state of Q(A), the first stable quinone electron acceptor of photosystem II reaction centers. High excitation pressure constitutes a potential stress condition that can be caused either by exposure to an irradiance that exceeds the capacity of C, N, and S assimilation to utilize the electrons generated from the absorbed energy or by low temperature or any stress that decreases the capacity of the metabolic pathways downstream of photochemistry to utilize photosynthetically generated reductants. The similarities and differences in the phenotypic responses between cyanobacteria, green algae, crop plants, and variegation mutants of Arabidopsis thaliana as a function of cold acclimation and photoacclimation are reconciled in terms of differential responses to excitation pressure and the predisposition of photoautotrophs to maintain photostasis. The various acclimation strategies associated with green algae and cyanobacteria versus winter cereals and A. thaliana are discussed in terms of retrograde regulation and the "grand design of photosynthesis" originally proposed by Arnon (1982).

Flexibility in photosynthetic electron transport: the physiological role of plastoquinol terminal oxidase (PTOX).

Oxygenic photosynthesis depends on a highly conserved electron transport system, which must be particularly dynamic in its response to environmental and physiological changes, in order to avoid an excess of excitation energy and subsequent oxidative damage. Apart from cyclic electron flow around PSII and around PSI, several alternative electron transport pathways exist including a plastoquinol terminal oxidase (PTOX) that mediates electron flow from plastoquinol to O(2). The existence of PTOX was first hypothesized in 1982 and this was verified years later based on the discovery of a non-heme, di-iron carboxylate protein localized to thylakoid membranes that displayed sequence similarity to the mitochondrial alternative oxidase. The absence of this protein renders higher plants susceptible to excitation pressure dependant variegation combined with impaired carotenoid synthesis. Chloroplasts, as well as other plastids (i.e. etioplasts, amyloplasts and chromoplasts), fail to assemble organized internal membrane structures correctly, when exposed to high excitation pressure early in development. While the role of PTOX in plastid development is established, its physiological role under stress conditions remains equivocal and we postulate that it serves as an alternative electron sink under conditions where the acceptor side of PSI is limited. The aim of this review is to provide an overview of the past achievements in this field and to offer directions for future investigative efforts. Plastoquinol terminal oxidase (PTOX) is involved in an alternative electron transport pathway that mediates electron flow from plastoquinol to O(2). This article is part of a Special Issue entitled: Regulation of Electron Transport in Chloroplasts.

Photosynthetic redox imbalance governs leaf sectoring in the Arabidopsis thaliana variegation mutants immutans, spotty, var1, and var2.

We hypothesized that chloroplast energy imbalance sensed through alterations in the redox state of the photosynthetic electron transport chain, measured as excitation pressure, governs the extent of variegation in the immutans mutant of Arabidopsis thaliana. To test this hypothesis, we developed a nondestructive imaging technique and used it to quantify the extent of variegation in vivo as a function of growth temperature and irradiance. The extent of variegation was positively correlated (R(2) = 0.750) with an increase in excitation pressure irrespective of whether high light, low temperature, or continuous illumination was used to induce increased excitation pressure. Similar trends were observed with the variegated mutants spotty, var1, and var2. Measurements of greening of etiolated wild-type and immutans cotyledons indicated that the absence of IMMUTANS increased excitation pressure twofold during the first 6 to 12 h of greening, which led to impaired biogenesis of thylakoid membranes. In contrast with IMMUTANS, the expression of its mitochondrial analog, AOX1a, was transiently upregulated in the wild type but permanently upregulated in immutans, indicating that the effects of excitation pressure during greening were also detectable in mitochondria. We conclude that mutations involving components of the photosynthetic electron transport chain, such as those present in immutans, spotty, var1, and var2, predispose Arabidopsis chloroplasts to photooxidation under high excitation pressure, resulting in the variegated phenotype.