Short-term acclimation of the photosynthetic electron transfer chain to changing light: a mathematical model

Photosynthetic eukaryotes house two photosystems with distinct light absorption spectra. Natural fluctuations in light quality and quantity can lead to unbalanced or excess excitation, compromising photosynthetic efficiency and causing photodamage. Consequently, these organisms have acquired several distinct adaptive mechanisms, collectively referred to as non-photochemical quenching (NPQ) of chlorophyll fluorescence, which modulates the organization and function of the photosynthetic apparatus. The ability to monitor NPQ processes fluorometrically has led to substantial progress in elucidating the underlying molecular mechanisms. However, the relative contribution of distinct NPQ mechanisms to variable light conditions in different photosynthetic eukaryotes remains unclear. Here, we present a mathematical model of the dynamic regulation of eukaryotic photosynthesis using ordinary differential equations. We demonstrate that, for Chlamydomonas, our model recapitulates the basic fluorescence features of short-term light acclimation known as state transitions and discuss how the model can be iteratively refined by comparison with physiological experiments to further our understanding of light acclimation in different species.     

Non‐invasive,whole‐plant imaging of chloroplast movement and chlorophyll fluorescence reveals photosynthetic phenotypes independent of chloroplast photorelocation defects in chloroplast division mutants

Leaf chloroplast movement is thought to optimize light capture and to minimize photodamage. To better understand the impact of chloroplast movement on photosynthesis, we developed a technique based on the imaging of reflectance from leaf surfaces that enables continuous, high‐sensitivity, non‐invasive measurements of chloroplast movement in multiple intact plants under white actinic light. We validated the method by measuring photorelocation responses in Arabidopsis chloroplast division mutants with drastically enlarged chloroplasts, and in phototropin mutants with impaired photorelocation but normal chloroplast morphology, under different light regimes. Additionally, we expanded our platform to permit simultaneous image‐based measurements of chlorophyll fluorescence and chloroplast movement. We show that chloroplast division mutants with enlarged, less‐mobile chloroplasts exhibit greater photosystem II photodamage than is observed in the wild type, particularly under fluctuating high levels of light. Comparison between division mutants and the severe photorelocation mutant phot1‐5 phot2‐1 showed that these effects are not entirely attributable to diminished photorelocation responses, as previously hypothesized, implying that altered chloroplast morphology affects other photosynthetic processes. Our dual‐imaging platform also allowed us to develop a straightforward approach to correct non‐photochemical quenching (NPQ) calculations for interference from chloroplast movement. This correction method should be generally useful when fluorescence and reflectance are measured in the same experiments. The corrected data indicate that the energy‐dependent (qE) and photoinhibitory (qI) components of NPQ contribute differentially to the NPQ phenotypes of the chloroplast division and photorelocation mutants. This imaging technology thus provides a platform for analyzing the contributions of chloroplast movement, chloroplast morphology and other phenotypic attributes to the overall photosynthetic performance of higher plants.     

SubChlo: Predicting protein subchloroplast locations with pseudo-amino acid composition and the evidence-theoretic K-nearest neighbor (ET-KNN) algorithm

The chloroplast is a type of plant specific subcellular organelle. It is of central importance in several biological processes like photosynthesis and amino acid biosynthesis. Thus, understanding the function of chloroplast proteins is of significant value. Since the function of chloroplast proteins correlates with their subchloroplast locations, the knowledge of their subchloroplast locations can be very helpful in understanding their role in the biological processes. In the current paper, by introducing the evidence-theoretic K-nearest neighbor (ET-KNN) algorithm, we developed a method for predicting the protein subchloroplast locations. This is the first algorithm for predicting the protein subchloroplast locations. We have implemented our algorithm as an online service, SubChlo (http://bioinfo.au.tsinghua.edu.cn/subchlo). This service may be useful to the chloroplast proteome research.     

NPQ(T): a chlorophyll fluorescence parameter for rapid estimation and imaging of non‐photochemical quenching of excitons in photosystem‐II‐associated antenna complexes

In photosynthesis, light energy is absorbed by light‐harvesting complexes and used to drive photochemistry. However, a fraction of absorbed light is lost to non‐photochemical quenching (NPQ) that reflects several important photosynthetic processes to dissipate excess energy. Currently, estimates of NPQ and its individual components (q_E, q_I, q_Z and q_T) are measured from pulse‐amplitude‐modulation (PAM) measurements of chlorophyll fluorescence yield and require measurements of the maximal yield of fluorescence in fully dark‐adapted material (F_m), when NPQ is assumed to be negligible. Unfortunately, this approach requires extensive dark acclimation, often precluding widespread or high‐throughput use, particularly under field conditions or in imaging applications, while introducing artefacts when F_m is measured in the presence of residual photodamaged centres. To address these limitations, we derived and characterized a new set of parameters, NPQ_(T), and its components that can be (1) measured in a few seconds, allowing for high‐throughput and field applications; (2) does not require full relaxation of quenching processes and thus can be applied to photoinhibited materials; (3) can distinguish between NPQ and chloroplast movements; and (4) can be used to image NPQ in plants with large leaf movements. We discuss the applications benefits and caveats of both approaches.     

Gibberellin indirectly promotes chloroplast biogenesis as a means to maintain the chloroplast population of expanded cells

Chloroplast biogenesis needs to be well coordinated with cell division and cell expansion during plant growth and development to achieve optimal photosynthesis rates. Previous studies showed that gibberellins (GAs) regulate many important plant developmental processes, including cell division and cell expansion. However, the relationship between chloroplast biogenesis with cell division and cell expansion, and how GA coordinately regulates these processes, remains poorly understood. In this study, we showed that chloroplast division was significantly reduced in the GA‐deficient mutants of Arabidopsis (ga1‐3) and Oryza sativa (d18‐AD), accompanied by the reduced expression of several chloroplast division‐related genes. However, the chloroplasts of both mutants exhibited increased grana stacking compared with their respective wild‐type plants, suggesting that there might be a compensation mechanism linking chloroplast division and grana stacking. A time‐course analysis showed that cell expansion‐related genes tended to be upregulated earlier and more significantly than the genes related to chloroplast division and cell division in GA‐treated ga1‐3 leaves, suggesting the possibility that GA may promote chloroplast division indirectly through impacting leaf mesophyll cell expansion. Furthermore, our cellular and molecular analysis of the GA‐response signaling mutants suggest that RGA and GAI are the major repressors regulating GA‐induced chloroplast division, but other DELLA proteins (RGL1, RGL2 and RGL3) also play a role in repressing chloroplast division in Arabidopsis. Taken together, our data show that GA plays a critical role in controlling and coordinating cell division, cell expansion and chloroplast biogenesis through influencing the DELLA protein family in both dicot and monocot plant species.     

A bestrophin‐like protein modulates the proton motive force across the thylakoid membrane in Arabidopsis

During photosynthesis, photosynthetic electron transport generates a proton motive force(pmf) across the thylakoid membrane, which is used for ATP biosynthesis via ATP synthase in the chloroplast. The pmf is composed of an electric potential(△Ψ) and an osmotic component(△pH).Partitioning between these components in chloroplasts is strictly regulated in response to fluctuating environments.However, our knowledge of the molecular mechanisms that regulate pmf partitioning is limited. Here, we report a bestrophin-like protein(At Best), which is critical for pmf partitioning. While the Dp H component was slightly reduced in atbest, the △Ψ component was much greater in this mutant than in the wild type, resulting in less efficient activation of nonphotochemical quenching(NPQ) upon both illumination and a shift from low light to high light. Although no visible phenotype was observed in the atbest mutant in the greenhouse, this mutant exhibited stronger photoinhibition than the wild type when grown in the field. At Best belongs to the bestrophin family proteins, which are believed to function as chloride(Cl~-) channels. Thus, our findings reveal an Researimportant Cl~- channel required for ion transport and homeostasis across the thylakoid membrane in higher plants. These processes are essential for fine-tuning photosynthesis under fluctuating environmental conditions.     

Imaging viral infection: studies on Nicotiana benthamiana plants infected with the pepper mild mottle tobamovirus

We have studied by kinetic Chl-fluorescence imaging (Chl-FI) Nicotiana benthamiana plants infected with the Italian strain of the pepper mild mottle tobamovirus (PMMoV-I). We have mapped leaf photosynthesis at different points of the fluorescence induction curve as well as at different post-infection times. Images of different fluorescence parameters were obtained to investigate which one could discriminate control from infected leaves in the absence of symptoms. The non-photochemical quenching (NPQ) of excess energy in photosystem II (PSII) seems to be the most adequate chlorophyll fluorescence parameter to assess the effect of tobamoviral infection on the chloroplast. Non-symptomatic mature leaves from inoculated plants displayed a very characteristic time-varying NPQ pattern. In addition, a correlation between NPQ amplification and virus localization by tissue-print was found, suggesting that an increase in the local NPQ values is associated with the areas invaded by the pathogen. Changes in chloroplast ultrastructure in non-symptomatic leaf areas showing different NPQ levels were also investigated. A gradient of ultrastructural modifications was observed among the different areas. The paper is dedicated to the memory of Prof. Dr López Gorgé (1935–2004)     

Dynamic flexibility in the structure and function of photosystem II in higher plant thylakoid membranes: the grana enigma

Grana are not essential for photosynthesis, yet they are ubiquitous in higher plants and in the recently evolved Charaphyta algae; hence grana role and its need is still an intriguing enigma. This article discusses how the grana provide integrated and multifaceted functional advantages, by facilitating mechanisms that fine-tune the dynamics of the photosynthetic apparatus, with particular implications for photosystem II (PSII). This dynamic flexibility of photosynthetic membranes is advantageous in plants responding to ever-changing environmental conditions, from darkness or limiting light to saturating light and sustained or intermittent high light. The thylakoid dynamics are brought about by structural and organizational changes at the level of the overall height and number of granal stacks per chloroplast, molecular dynamics within the membrane itself, the partition gap between appressed membranes within stacks, the aqueous lumen encased by the continuous thylakoid membrane network, and even the stroma bathing the thylakoids. The structural and organizational changes of grana stacks in turn are driven by physicochemical forces, including entropy, at work in the chloroplast. In response to light, attractive van der Waals interactions and screening of electrostatic repulsion between appressed grana thylakoids across the partition gap and most probably direct protein interactions across the granal lumen (PSII extrinsic proteins OEEp-OEEp, particularly PsbQ-PsbQ) contribute to the integrity of grana stacks. We propose that both the light-induced contraction of the partition gap and the granal lumen elicit maximisation of entropy in the chloroplast stroma, thereby enhancing carbon fixation and chloroplast protein synthesizing capacity. This spatiotemporal dynamic flexibility in the structure and function of active and inactive PSIIs within grana stacks in higher plant chloroplasts is vital for the optimization of photosynthesis under a wide range of environmental and developmental conditions.     

Instantaneous switching between different modes of non-photochemical quenching in plants. Consequences for increasing biomass production

Photosynthetic productivity usually saturates far below the maximum solar light intensity, meaning that in those conditions many absorbed photons and the resulting electronic excitations of the pigment molecules can no longer be utilized for photosynthesis. To avoid photodamage, various protection mechanisms are induced that dissipate excess excitations, which otherwise could lead to the formation of harmful molecular species like singlet oxygen. This Non-Photochemical Quenching (NPQ) of excitations can be monitored via a decrease of the chlorophyll fluorescence. There is consensus that in plants 1) there are at least two major NPQ (sub)processes and 2) NPQ (de)activation occurs on various time scales, ranging from (tens of) seconds to minutes. This relatively slow switching has a negative effect on photosynthetic efficiency, and Kromdijk et al. demonstrated in 2016 (Science 354, 857) that faster switching rates can lead to increased crop productivity. Very recently, we were involved in the discovery of a new NPQ process that switches off well within a millisecond (Farooq et al. (2018) Nat. Plants 4, 225). Here we describe the current level of knowledge regarding this process and discuss its implications.     

Chloroplast: the Trojan horse in plant–virus interaction

The chloroplast is one of the most dynamic organelles of a plant cell. It carries out photosynthesis, synthesizes major phytohormones, plays an active part in the defence response and is crucial for interorganelle signalling. Viruses, on the other hand, are extremely strategic in manipulating the internal environment of the host cell. The chloroplast, a prime target for viruses, undergoes enormous structural and functional damage during viral infection. Indeed, large proportions of affected gene products in a virus‐infected plant are closely associated with the chloroplast and the process of photosynthesis. Although the chloroplast is deficient in gene silencing machinery, it elicits the effector‐triggered immune response against viral pathogens. Virus infection induces the organelle to produce an extensive network of stromules which are involved in both viral propagation and antiviral defence. From studies over the last few decades, the involvement of the chloroplast in the regulation of plant–virus interaction has become increasingly evident. This review presents an exhaustive account of these facts, with their implications for pathogenicity. We have attempted to highlight the intricacies of chloroplast–virus interactions and to explain the existing gaps in our current knowledge, which will enable virologists to utilize chloroplast genome‐based antiviral resistance in economically important crops.     

RUS家族对植物生长发育的调控作用

叶绿体基因组编码许多参与光合作用和其他代谢过程的关键蛋白质,在叶绿体中合成的代谢物对于植物正常的生长发育至关重要。根对紫外线-B辐射敏感[Root-UVB (ultraviolet radiation B)-sensitive, RUS]蛋白属于叶绿体蛋白,由高度保守的DUF647结构域组成,在参与植物形态发生、物质运输和能量代谢等多种生命活动的调控中发挥作用。本文就近年来关于RUS家族在植物的胚胎发育、光形态建成、维生素B6稳态、生长素转运和花药发育等生长发育过程中的相关研究进行回顾和总结,为深入研究其在植物生长发育中的分子调控机制提供了参考。     

植物水孔蛋白研究进展

水孔蛋白是植物重要的膜功能蛋白,不仅介导植物各组织间水分的高效转运,还参与植物体内其他物质的跨膜转运,同时在植物光合作用、生长发育、免疫应答以及信号转导等生理过程中也发挥重要作用。本文主要综述了植物水孔蛋白结构特征和分类,多种生理功能,以及其转录水平和转录后水平活性调节等方面的最新研究进展,并就如何系统全面地开展水孔蛋白参与植物生长发育过程的分子调控机制研究提出展望。植物水孔蛋白的深入研究有助于阐明植物体内物质转运的分子机理及其生理作用机制,对指导农业生产中作物的生长发育调控有重要理论意义。     

Chloroplast photorelocation movement mediated by phototropin family proteins in green plants

Chloroplasts gather in areas irradiated with weak light to maximize photosynthesis (the accumulation response). They move away from areas irradiated with strong light to minimize damage of the photosynthetic apparatus (the avoidance response). The processes underlying these chloroplast movements can be divided into three parts: photoperception, signal transduction, and chloroplast movement. Photoreceptors for chloroplast movement have been identified recently in various plant species. A blue light receptor phototropin (phot) mediates chloroplast photorelocation movement in the seed plant Arabidopsis thaliana, the fern Adiantum capillus-veneris, the moss Physcomitrella patens and possibly the green alga Mougeotia scalaris. A chimeric photoreceptor between phytochrome and phototropin, neochrome (neo), was found in some advanced ferns and in the green alga M. scalaris. While the mechanism of chloroplast movement is not well understood, it is known that actin filaments play an important role in this process. To understand the molecular mechanisms associated with chloroplast movement, several mutants were isolated in A. thaliana (jac1 and chup1) and the corresponding genes were cloned. In this review, recent progress in photoreceptor research into chloroplast movement in various plant species and the possible factors functioning in signal transduction or the regulation of actin filaments identified in A. thaliana is discussed.     

A kaleidoscope of photosynthetic antenna proteins and their emerging roles

Photosynthetic light-harvesting antennae are pigment-binding proteins that perform one of the most fundamental tasks on Earth, capturing light and transferring energy that enables life in our biosphere. Adaptation to different light environments led to the evolution of an astonishing diversity of light-harvesting systems. At the same time, several strategies have been developed to optimize the light energy input into photosynthetic membranes in response to fluctuating conditions. The basic feature of these prompt responses is the dynamic nature of antenna complexes, whose function readily adapts to the light available. High-resolution microscopy and spectroscopic studies on membrane dynamics demonstrate the crosstalk between antennae and other thylakoid membrane components. With the increased understanding of light-harvesting mechanisms and their regulation, efforts are focusing on the development of sustainable processes for effective conversion of sunlight into functional bio-products. The major challenge in this approach lies in the application of fundamental discoveries in light-harvesting systems for the improvement of plant or algal photosynthesis. Here, we underline some of the latest fundamental discoveries on the molecular mechanisms and regulation of light harvesting that can potentially be exploited for the optimization of photosynthesis.

The latest fundamental knowledge obtained on the light-harvesting mechanisms of the antenna proteins can be bridged to biotechnical optimization of photosynthesis.     

Comparative anatomy, morphology, and molecular phylogenetics of the African genus Satanocrater (Acanthaceae)

? Premise of the study: Anatomical and morphological features of Satanocrater were studied to test hypotheses of xeric adaptations in the genus, which is endemic to arid tropical Africa. These features, together with molecular data, were used to test the phylogenetic placement of Satanocrater within the large plant family Acanthaceae. ? Methods: We undertook a comparative study of four species of Satanocrater. Carbon isotope ratios were generated to test a hypothesis of C(4) photosynthesis. Molecular data from chloroplast (trnG-trnS, trnG-trnR, psbA-trnH) and nuclear (Eif3E) loci were used to test the placement of Satanocrater within Acanthaceae. ? Key results: Anatomical features reflecting xeric adaptations of species of Satanocrater included a thick-walled epidermis, thick cuticle, abundant trichomes and glandular scales, stomata overarched by subsidiary cells, tightly packed mesophyll cells, and well-developed palisade parenchyma on both leaf surfaces. Although two species had enlarged bundle sheath cells, a feature often implicated in C(4) photosynthesis, isotope ratios indicated all species of Satanocrater use the C(3) pathway. Molecular data resolved Satanocrater within tribe Ruellieae with strong support. Within Ruellieae, our data suggest that pollen morphology of Satanocrater may represent an intermediate stage in a transition series. ? Conclusions: Anatomical and morphological features of Satanocrater reflect adaptation to xeric environments and add new information about the biology of xerophytes. Morphological and molecular data place Satanocrater in the tribe Ruellieae with confidence. This study adds to our capacity to test hypotheses of broad evolutionary and ecological interest in a diverse and important family of flowering plants.     

Functional genomics of plant photosynthesis in the fast lane using Chlamydomonas reinhardtii

Oxygenic photosynthesis by algae and plants supports much of life on Earth. Several model organisms are used to study this vital process, but the unicellular green alga Chlamydomonas reinhardtii offers significant advantages for the genetic dissection of photosynthesis. Recent experiments with Chlamydomonas have substantially advanced our understanding of several aspects of photosynthesis, including chloroplast biogenesis, structure-function relationships in photosynthetic complexes, and environmental regulation. Chlamydomonas is therefore the organism of choice for elucidating detailed functions of the hundreds of genes involved in plant photosynthesis.