Functional Plant Biology
Volume 45 Numbers 1 & 2 2018
Plant Signalling: From Molecules to Behaviour
FP17085Unravelling the plant signalling machinery: an update on the cellular and genetic basis of plant signal transduction
Signalling is a central phenomenon in biology. It is crucial to all aspects of plant physiology including growth, development and interactions with the environment. Here, novel hypotheses and experimental data regarding signalling hubs, second messengers, programmed cell death and autophagy are presented from the Fourth Plant Signalling and Behaviour Symposium in Saint Petersburg, Russia, June 2016).
FP16420Mechanisms of cytosolic calcium elevation in plants: the role of ion channels, calcium extrusion systems and NADPH oxidase-mediated 'ROS-Ca2+ Hub'
Transient elevation of cytosolic Ca2+, also referred to as a Ca2+signal, is a central phenomenon of plant signalling. Plants evolved sophisticated systems to initiate, amplify and terminate Ca2+ signals. Structure and properties of these systems, including Ca2+-permeable ion channels, Ca2+-ATPases, Ca2+/H+ exchangers and ‘ROS-Ca2+ hub’ are discussed here. They provide a fine-tuned mechanism for encoding diverse external and internal stimuli.
FP16380The role of ion disequilibrium in induction of root cell death and autophagy by environmental stresses
Environmental stresses are main causes for low agricultural productivity. At the cellular level, stresses induce generation of reactive oxygen species (ROS), ion disequilibrium, autophagy and programmed cell death (PCD). Here we propose that these processes interact and that ROS and ion disequilibrium are triggers of autophagy and PCD. Overall, presented data contribute to understanding plant stress physiology.
Rhizobium bacteria, which live within the root nodules of legumes, allow plants to capture nitrogen gas from the atmosphere and use it for their own growth. Central to this symbiosis is an intracellular structure, called the symbiosome, in which nitrogen-fixing bacterial cells exchange components with the host cells that harbor them. Recent research on the differentiation of symbiosomes and of the infected cells that accommodate them has helped to decipher some general molecular mechanisms of cell differentiation.
Melatonin is an important hormone and signalling molecule in all forms of life including humans, plants and bacteria. Recent plant physiology and genomic experiments have described the redirection of plant growth and metabolism, and demonstrated a diversity of genes involved in response to melatonin, however, the exact metabolic cascades that translate melatonin signals into physiological responses is not fully understood. This review provides an overview of melatonin mediated signalling manifested as behaviours and its roles in basic and industrial research.
FP16279Molecular mechanisms accompanying nitric oxide signalling through tyrosine nitration and S-nitrosylation of proteins in plants
Understanding the molecular mechanisms of plant development constitutes an important field of investigations in the current era of plant biology research. Nitric oxide signalling regulates a variety of biochemical processes in plants. This review provides an in-depth analysis of our current understanding on the subject, particularly with reference to plant growth under stress conditions.
Large conductance SV/TPC1 channels are ubiquitously and abundantly expressed in the vacuolar membranes of higher plants. They are unique established Ca2+-permeable channels in vacuoles, but their activity is strongly negatively controlled, so that they were believed to be inactive or to act only locally. Recent evidence suggests the key role of SV/TPC1 channels in the long-distance Ca2+ signalling.
Cyclic GMP (cGMP) signalling in plants is crucial for many physiological processes. Recent analytical and genomic developments now allow detailed studies into the biochemistry and physiological role of cGMP in plants, and the latest findings are reviewed in this article.
FP16322Formation mechanisms of superoxide radical and hydrogen peroxide in chloroplasts, and factors determining the signalling by hydrogen peroxide
Photosynthetic electron transport chain is not the only source of ATP and NADPH for photosynthesis; it is a sensor, informing adaptation systems of plant about environmental changes. An important transmitter of this information is hydrogen peroxide whose mechanisms of formation are presented, laying special emphasis on the formation outside and within thylakoid membrane. It is discussed, that the formation place can ensure definite signal about the specific environmental change.
Clarifying herbivory-induced plant cellular signalling is a critical step to push the research of plant-herbivore interaction forward. We review the role of ion channels/transporters in modulating herbivory-induced early signalling events and rapid systemic signal transmission in plants. This work provides a comprehensive source of information about plant defensive strategies upon attack.
FP16339Electrical signalling in Nitellopsis obtusa: potential biomarkers of biologically active compounds
The electrophysiological response pattern of Nitellopsis obtusa cell can be assessed to evaluate the effect of many biologically active compounds. We illustrate a variety of electrophysiological approaches for the investigations of electrical signaling after chemical treatment in vivo. The insights about the Characean model system are likely to hold for plants in general and even deepen the understanding of the plant evolution.
FP16242Rapid changes in root HvPIP2;2 aquaporins abundance and ABA concentration are required to enhance root hydraulic conductivity and maintain leaf water potential in response to increased evaporative demand
The ABA-deficient barley mutant Az34 and wild type (WT) were exposed to air warming. Although transpiration rate of both genotypes increased, leaf water potential decreased in the mutant but was maintained in WT plants. Only WT plants showed increased root ABA accumulation, which increased root hydraulic conductivity and aquaporin abundance, which seems important in maintaining leaf hydration.
FP16261Two native types of phytochrome A, phyAʹ and phyAʺ, differ by the state of phosphorylation at the N-terminus as revealed by fluorescence investigations of the Ser/Ala mutant of rice phyA expressed in transgenic Arabidopsis
Plants adapt to environmental light conditions with the use of the sophisticated phytochrome system. In this work, polymorphism of its major component – phytochrome A– was investigated. With the use of transgenic Arabidopsis and fluorescence technique, it was shown that two molecular types of the photoreceptor differ by the state of phosphorylation and their existence accounts for its complex functions.
FP16342Parameters of electrical signals and photosynthetic responses induced by them in pea seedlings depend on the nature of stimulus
Plants, like animals, produce electrical signals in response to various external influences. In this study we raised a question whether the electrical signals transmit information about the nature of the stimulus, and found out that different stimuli induce signals of varied parameters. The obtained results explain how plants adapt to changing environment.
Although plant proteases of the phytaspase family are important contributors to stress-induced plant cell death, phytaspase of a classical model plant Arabidopsis thaliana has escaped identification thus far. We identified the Arabidopsis phytaspase-encoding gene and characterised the recombinant enzyme. Substrate specificity and properties of the Arabidopsis phytaspase display both important similarities with and distinctions from the already characterised phytaspases.
FP16347Spatial distribution of organelles in leaf cells and soybean root nodules revealed by focused ion beam-scanning electron microscopy
Focussed ion bean scanning electron microscopy (FIB-SEM) is a technique that can be used to generate 3D renderings of cells and their contents. Although FIB-SEM has been regularly used to investigate animal cells and tissues, it has rarely been deployed to study plant structures. Here we demonstrate that FIB-SEM can easily be used to study plant samples and have discovered previously unknown arrangements of organelles and membranes in those samples.
FP16292Studies of cytokinin receptor–phosphotransmitter interaction provide evidences for the initiation of cytokinin signalling in the endoplasmic reticulum
Cytokinin is an important plant hormone and its mode of action has been extensively studied; however, to date, the subcellular localisation of cytokinin perception and signal transduction remains a matter of debate. This study describes cytokinin receptor–phosphotransmitter interaction and its subcellular localisation in living plant cells and it provides several experimental evidences for receptor activity at the endoplasmic reticulum (ER) membrane. It is concluded that intracellular cytokinins within the ER lumen may play an important role in cytokinin signalling, at least in some cell types.
Plant fibres with a tertiary cell wall (G-layer) may function as plant ‘muscles’. Large-scale transcriptome profiling of isolated flax phloem fibres permitted to identify the major players and regulatory elements that operate during graviresponce specifically in the fibres of the pulling stem side. The suggested mechanisms of phloem fibre involvement in tropisms may considerably renew the concept of herbaceous plant behaviour upon gravistimulation.
FP16340Cytokinins regulate root growth through its action on meristematic cell proliferation but not on the transition to differentiation
Root growth is controlled by phytohormones, but what cellular processes are regulated and how it occurs is still an open question. Here it is shown that cytokinin affects root growth mainly through its effect on cell proliferation, and does not initiate the transition of cells to differentiation as previously thought. Cellular analysis performed could be applied for the analysis of how any plant hormone influences developmental processes in plant roots.
Memristors, or resistors with memory, exist in vivo as components of plasma membranes in plants, fruits, roots and seeds. Authors found memristors in an androecium, spur, petals and pedicel in Sunpatiens flowers. The discovery of memristors in Sunpatiens (Impatiens spp.) creates a new direction in the modelling and understanding of electrophysiological phenomena and memory elements in flowers.
FP16379Photochemical activity changes accompanying the embryogenesis of pea (Pisum sativum) with yellow and green cotyledons
We studied the dynamics of photochemical activity in seed coats and cotyledons during development of yellow- and green-seeded pea cultivars by using the pulse amplitude modulation fluorometric analysis. The fast transients of the chlorophyll a fluorescence revealed higher photochemical activity in the coats of yellow-seeded cultivar at the early- and middle cotyledon stages of seed development in comparison to those observed in the green-seeded ones. Photochemical activity in the cotyledons of both cultivars could not be any more detected at the late cotyledon stage. This process was triggered by dehydration of seed tissues.
Intracellular communications in plant cells of large dimensions rely primarily on cytoplasmic streaming, because diffusion is too slow for the transport on mm-scale distances. Illumination of a small cell spot at various distances from the point of chlorophyll fluorescence measurements revealed the wave-like propagation of the fluorescence response along the cell length. The results show that the photosynthetic function of immobile chloroplasts under constant light can be affected by long-distance transmission of a photosynthetically active metabolite from the remote cell parts.
FP16418The levels of peroxisomal catalase protein and activity modulate the onset of cell death in tobacco BY-2 cells via reactive oxygen species levels and autophagy
Peroxisomes balance the cellular levels of reactive oxygen species (ROS) and therefore should modulate ROS-regulated programs like autophagy or cell death. We used tobacco suspension cultures to show that degradation of peroxisomes via autophagy was a prerequisite for cell death and depended on the levels of the major peroxisomal protein, catalase. This suggests a role of plant catalase in the regulation of peroxisome turnover and autophagic cell death.
FP17116Myotubularins, PtdIns5P, and ROS in ABA-mediated stomatal movements in dehydrated Arabidopsis seedlings
Arabidopsis myotubularins AtMTM1 and AtMTM2 control stomata movements via reactive oxygen species (ROS) homeostasis under drought stress. Acting as a secondary messenger in the ABA-induced ROS production in guard cells, PtdIns5P emerges as an evolutionarily conserved signalling molecule downstream of AtMTMs calibrating cellular ROS levels under stress. AtMTM1 and AtMTM2 activities balance ABA-induced ROS and cellular homeostasis under dehydration stress.
FP16324Molecular insights into the functional role of nitric oxide (NO) as a signal for plant responses in chickpea
Although many studies established nitric oxide (NO) as a signaling molecule in plants, the identification of target molecules of NO has remained elusive due to the lack of in depth molecular studies. Our quantitative proteome analysis suggests the differential regulation of 248 proteins and dynamic regulation of metabolic pathways by exogenous NO donor in chickpea. This is the first report in legumes pointing at the potential candidates that attribute the reported functions of NO in plants.
FP17151Endoplasmic reticulum stress regulates glutathione metabolism and activities of glutathione related enzymes in Arabidopsis
Prolonged endoplasmic reticulum (ER) stress oxidises the cellular glutathione pool. To elucidate the role of glutathione during ER stress, biosynthesis and degradation of glutathione and activities of related enzymes were evaluated. Our data demonstrated that glutathione biosynthesis and an apoplastic but not cytoplasmic catabolic pathway was induced. In addition, the activities of enzymes that use glutathione as a substrate were increased by ER stress.
The peer-reviewed and edited version of record published online before inclusion in an issue
FP17195Wheat pre-anthesis development as affected by photoperiod sensitivity genes (Ppd-1) under contrasting photoperiods
The duration of phases leading to wheat anthesis date, and hence yield potential, are regulated by daylength (photoperiod). Genes controlling the response to photoperiod (Ppd-1): (i) provided varying magnitudes of insensitivity; (ii) were not particularly associated to duration – photoperiod sensitivity – of any specific phase; and (iii) showed no additive effect when stacked. Further investigation with different allelic variants should be conducted to tailor time to anthesis and duration of each particular phase to improve wheat yield potential facing climate change.
FP17162Antioxidant capacity along the leaf blade of the C3-CAM facultative bromeliad Guzmania monostachia under water deficit conditions
Guzmania monostachia is an epiphytic, tank-forming bromeliad that displays variable degrees of crassulacean acid metabolism (CAM) along the leaf blade under water deficit conditions. The hypothesis that the most intense CAM found in the apex portion is related to reduced oxidative burden was not confirmed. However, G. monostachia was able to keep reactive oxygen species under tolerable levels under water deficit conditions by increasing the antioxidant capacity in the apex, which is the leaf portion most exposed to light.
FP17147XopR TTSS-effector regulates in planta growth, virulence of Indian strain of Xanthomonas oryzae pv. oryzae via suppressing reactive oxygen species production and cell wall-associated rice immune responses during blight induction
Bacterial pathogens secret effectors to modulate plant immunity, enabling unlimited pathogen growth inside host, and causing disease. Xanthomonas oryzae pv. oryzae executes XopR effector to suppress immune responses in rice for its growth and subsequent blight disease. This finding provides insights into understanding the key weapon used by the pathogen, and will help to identify the novel targets for disease management.
FP17199Seasonal variations of leaf chlorophyll–protein complexes in the wintergreen herbaceous plant Ajuga reptans L.
In the perennial herbaceous wintergreen plant Ajuga reptans (bugle), the photosynthetic apparatus (PSA) is reorganised during winter. The aim of this work was to examine the structural changes in the pigment–protein complexes of PSA. Changes in aggregation of the thylakoid protein complexes were observed including a restructuring of the PSI–PSII megacomplex and the PSII–LHCII supercomplex parallel to changes in the zeaxanthin-dependent protective mechanism.
FP17303Integrated genomics, physiology and breeding approaches for improving nitrogen use efficiency in potato: translating knowledge from other crops
Potato is a high nitrogen-responsive crop, hence improving nitrogen use efficiency (NUE) of plant is important to reduce production cost and minimize environmental loss. Potato is a less studied crop especially at plant level with enhanced NUE. This review highlights translation of advanced NUE research from other plants like Arabidopsis, rice, wheat and maize applying integrated genomics, physiology and breeding approaches.
Root properties impact strongly on plant performance, but high-throughput methods for non-invasive and quantitative root trait assessment are rarely available. We developed and tested a root phenotyping concept, which involves NIR imaging of roots grown along surfaces of transparent culture vessels using visible light blocking long pass filters. We reveal the viability of the concept and its suitability for simultaneous root and shoot phenotyping.
FP17226Constitutive expression of CaHSP22.5 enhances chilling tolerance in transgenic tobacco by promoting the activity of antioxidative enzymes
Chilling stress limits the productivity and geographical distribution of many plants throughout the world. Accumulation of the endoplasmic reticulum-located small heat shock protein CaHSP22.5 enhanced photochemical activity and oxidation resistance and alleviated endoplasmic reticulum stress caused by chilling stress in transgenic tobacco plants. CaHSP22.5 could be useful for improving the tolerance of chilling-sensitive plant types.
Understanding the mechanism of high-temperature stress (heat) tolerance during the plant reproductive phase is important for developing heat tolerant cultivars in lentil. We found a higher reduction in pollen viability and lower photosynthetic electron transport rate in heat sensitive genotypes and a functional marker amplified only in heat tolerant ones. We conclude that these traits and the associated functional markers will be useful in lentil breeding.
FP17288Identification of MdDof genes in apple and analysis of their response to biotic or abiotic stress
In the study presented we identified MdDof genes in apple and analysed their response to biotic/abiotic stress. The aim of the work was to give references to understand the function of MdDof genes generally and serve as a reference for studies of Dof zinc finger genes in other plants. Finally, we fit the original images into the software Photoshop 6.0 for bigger pictures.
FP17233Impact of hemlock woolly adelgid (Adelges tsugae) infestation on xylem structure and function and leaf physiology in eastern hemlock (Tsuga canadensis)
Hemlock woolly adelgid (HWA) is an invasive insect that feeds upon the foliage of eastern hemlock trees leading to a decline in health and mortality. During early infestation, HWA-induced decline in the health of eastern hemlock is not initially caused by compromised water transport or needle loss. Our results contribute to efforts to understand the mechanisms leading to the demise of eastern hemlocks.
FP17212Structural and functional characterisation of two novel durum wheat annexin genes in response to abiotic stress
Abiotic stress reduces the grain yield of cereal crops. Here, we show that the two durum wheat annexin genes, TdAnn6 and TdAnn12, are induced by different abiotic stresses and heterologous expression in yeast improves tolerance to different stresses. These results show that the two annexins are potentially useful candidate genes for engineering abiotic stress tolerance in cultivated plants.
FP17274Hydrogen sulfide may function downstream of hydrogen peroxide in mediating darkness-induced stomatal closure in Vicia faba
We proved for the first time the effects of H2S, a novel gasotransmitter, on darkness-induced stomatal closure and the relationship with H2O2 in Vicia faba. Here we found that H2S mediated darkness-induced stomatal closure in Vicia faba and it acted downstream of H2O2 in this process. This work enriches the signalling network during darkness-regulated stomatal movement and provides evidence for further research.
FP17265Biochemical and transcriptomic analysis of maize diversity to elucidate drivers of leaf carbon isotope composition
Leaf carbon isotope composition (δ13C) has been used to screen for water-use efficiency in C3 plants, but gaps in the understanding of factors influencing δ13C have limited its application in C4 species. This study exploited maize genetic diversity to explore biochemical and post-photosynthetic factors that may influence δ13C. Our findings indicate that the observed variation in leaf carbon isotope composition across diverse maize lines is likely driven by differences in stomatal and mesophyll conductance and not photosynthetic or respiratory metabolism.
Sustaining plant productivity under microgravity conditions is a prerequisite for successful colonisation of space by humans. Therefore, we address the effects of simulated microgravity on seed germination and the first steps of seedling development at the total proteome level. This study complements a large body of transcriptomic data and gives an insight into gravity-related changes in early plant ontogenesis.
FP17180The regulator of G-protein signalling protein mediates D-glucose-induced stomatal closure via triggering hydrogen peroxide and nitric oxide production in Arabidopsis
Stomatal guard cells sense and respond to sugar, but the means by which they do so have not been fully elucidated. Our study showed that RGS1, a putative receptor for D-glucose, mediates D-glucose-induced H2O2 and NO production in guard cells and subsequent stomatal closure. The data suggest that photosynthetic product D-glucose, as an integrative signal, coordinates plant CO2 uptake with water loss.
FP16393Role of the antioxidant system in the regulation of the chlorophyll biosynthesis pathway in the vascular plant Cucumis sativus
Fine tuning the flow of chlorophyll biosynthesis pathway is crucial for the growth and development of the plants. Antioxidant systems were found to influence this pathway through maintaining the specific concentration of H2O2. This finding provides insights into understanding the antioxidant-mediated regulation of chlorophyll biosynthesis in detail, and will help in the development of oxidative stress-resistant plants.
Many environmental stresses are periodic and predictable. Plants have adapted to these by temporally organising their stress responses to maximise efficiency and efficacy. We review current evidence for temporal regulation of responses to the environment and environmental impacts on the plant circadian clock. Better understanding of the reciprocal interactions between the plant circadian clock and environmental stresses may aid in identifying mechanisms to improve plant growth and increase food security.
FP17203The involvement of programmed cell death in inflated leaf petiole morphogenesis in Trapa pseudoincisa
The inflated leaf petiole of Trapa pseudoincisa undergoes a developmental process from solid to hollow phase. Schizo-lysigenous aerenchyma was developed via the mechanism of programmed cell death (PCD) during the process of inflated leaf petiole morphogenesis. Thus, a trans-disciplinary systems approach that recognizes the need for integration of cytological and molecular characteristics for identification of aerenchyma type in aquatic plant is required.
FP17095Involvement of signalling molecules NO, H2O2 and H2S in modification of plasma membrane proton pump in cucumber roots subjected to salt or low temperature stress
Cascades by which signalling molecules participate in plant responses to changes in environmental conditions are still under intensive study. Our aim was to explain the role of NO, H2O2 and H2S in adaptation of cucumber seedlings to both salt and low temperature stress. Results show that signalling molecules are important for understanding the mechanisms of modification of the activity of the plasma membrane proton pump, which is a key enzyme in abiotic stress conditions.
Chlorophyll b is the major regulator of photosynthetic antennae in land plants. Its absence diminishes light harvesting, photoprotection and ultimately photosynthesis. We show that barley mutants lacking chl b display impaired stomatal control, which can be restored by temporal shading of the plants. Thus the effects of this mutation extend beyond chloroplast metabolism.
Global demand for agricultural product is predicted to surpass our production capacity in the near future, and enhancing plant photosynthesis may be a solution for crop yield improvement. To accelerate enhancement we need to know which target(s) should be manipulated for greatest impact, therefore, a modelling tool has been developed. The tool will be able to improve our understanding of photosynthetic manipulation impacts on crop biomass accumulation, which ultimately affects crop yield.
FP17202The LmSAP gene isolated from the halotolerant Lobularia maritima improves salt and ionic tolerance in transgenic tobacco lines
Abiotic stresses pose serious threats to growth and productivity of crop plants worldwide. We describe the isolation of a novel gene, designated LmSAP, from Lobularia maritime to exploit the potential of this halophyte as a genetic resource to improve salt and ionic tolerance in plants and, particularly, in cereals. These results show that LmSAP is a potentially useful candidate gene for engineering salt and ionic tolerance in cultivated plants.
Reproductive growth is very important for plant survival and population establishment under salinity. It remains unknown whether the reproductive process of Suaeda salsa is affected by salinity. NaCl markedly increased the reproductive growth of S. salsa by increasing flower number and fertility. Unravelling the mechanisms of plant salt tolerance will be helpful for improving agricultural production.
Ethylene-induced abscission of young cotton fruits is a major lint yield limiting factor in cotton crop production under stressed environments. Extreme weather events such as long-term soil waterlogging and elevated CO2 can increase fruit loss caused by ethylene production in cotton. Our study showed that the physiological and yield performance of cotton crops under future environments can potentially be improved by mitigating ethylene action.
FP17167Co-inoculation of maize with Azospirillum brasilense and Rhizobium tropici as a strategy to mitigate salinity stress
Salinity is a major factor affecting crop production worldwide. We identified enzymatic and genetic mechanisms in maize that confer tolerance against abiotic stresses when inoculated with plant growth-promoting bacteria. Inoculation with the elite strains identified in this study, of Azospirillum brasilense (Ab-V6) and Rhizobium tropici (CIAT 899) might represent a valuable and sustainable strategy to mitigate salinity stress.
FP16444Aquaporin AtTIP5;1 as an essential target of gibberellins promotes hypocotyl cell elongation in Arabidopsis thaliana under excess boron stress
Gibberellins (GAs) promote hypocotyl elongation by controlling the expression of many genes in plants. However, only a few target genes of GAs have been identified to date. The paper provides strong evidence that tonoplast aquaporin AtTIP5;1 mediates GA-stimulated hypocotyl cell elongation under excess boron condition in Arabidopsis. The finding highlights the essential roles of vacuoles and boron in GA signalling in plants.
By 2015 genetically modified (GM) crops had been commercialised for 20 years. This technology ranks amongst the most rapidly accepted by farmers, but are there downsides to these introductions? This review considers the advantages and potential disadvantages of GM crops.
FP17201Modelling seasonal changes in the temperature-dependency of CO2 photosynthetic responses in two Vitis vinifera cultivars
Interspecific differences in photosynthetic attributes of Chardonnay and Merlot grapevines have been established. The cause of such differences were attributed to a higher carboxylation and regeneration capacity in the Merlot leaves, especially at high temperatures and cultivar differences were exacerbated as the season progressed. Differences in biochemical processes related to assimilation at high temperatures were measured between the cultivars, and these may relate to inherent differences in temperature tolerance between these closely related cultivars.
These articles have been peer reviewed and accepted for publication. They are still in production and have not been edited, so may differ from the final published form.
Pearl millet [Pennisetum glaucum (L.) R. Br.] contrasting for the transpiration response to vapour pressure deficit also differ in their dependence on the symplastic and apoplastic water transport pathways
Dynamic analysis of the impact of free-air CO2 enrichment (FACE) on biomass and N uptake in two contrasting genotypes of rice
Structural and functional disorder in the photosynthetic apparatus of radish plants under magnesium deficiency
Improving nitrogen use efficiency in plants: Effective phenotyping in conjunction with agronomic and genetic approaches
MeBIK1, a novel cassava receptor-like cytoplasmic kinase, regulates PTI response of transgenic Arabidopsis
S-Nitrosocysteine-responsive genes modulate diverse regulatory pathways in Oryza sativa: A transcriptome profiling study
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