Stress-Induced Cell Reprogramming. A Role for Global Genome Regulation?

Stress adaptation in crops is an important and timely topic in basic and applied biology. Interest in the issue is ambiguous. On the one hand, it is fascinating to understand interaction between plants and environment. On the other hand and in view of the needs of human life, we want to create crop plants that are able to confront successfully unfavorable natural conditions. The main goal in plant breeding is to obtain plants that combine high yields and reliable yield stability over years and locations. Simultaneously, plant products must have a high quality in terms of nutritional value, if used as food or feed, and/or of other characteristics of commercial interests. However, in addition to biotic stress factors, disturbances of extreme or even mild abiotic stress are supposed to account for a high amount of unachieved potential in plant production all over the world. Diverse forms of abiotic stress may occur, including drought, heat, cold and freezing, salinity, nutrient deficiency, toxic concentration of heavy metals, oxidative stress as well as oxygen shortage, and mechanical stress. Although it is known that diverse environmental stress factors never act alone, experimental study of plant responses on abiotic stress is normally restricted to plant reactions on isolated stress factors. However, it has to be considered that stress always occurs as a complex of various interacting environmental factors that contribute in varying degrees to the overall stress. Consequently, plants always respond to a unique complex of growth conditions. Stress inducers from the abiotic as well as biotic world have some common signal and response pathways in plants and thereby have the potential to modulate the effect of each other through cross-talking. Further, plants, as sessile organisms, have to get along with the dynamics of transiently changing environmental conditions, and this has to be achieved at the various stages of plant development (see Amzallag, 2001, for the meaning of developmental windows in stress adaptation). Virtual experimentation is currently thought to offer the best potential for future research on stress adaptation because the complexity of plant reactions and stress factors may be taken into account simultaneously. Therefore, a global, multidisciplinary initiative to establish systems biology in plant sciences is very promising. Systems biology aims to collect and manage the huge amount of data available at any level of plant life to enable modeling of an artificial plant organism, the in silico plant. Confronting the artificial plant by computer simulation with real-life obstacles, such as abiotic stress through nutrient depletion or water deficit, will help to improve our understanding of how plants work and how to improve the capacity of plants in terms of increased “fitness for stress.” Combining computational skill and interest in natural sciences to the benefit of humanity, environment, and remunerative intersectorial applications covers the most fascinating areas for younger researchers in biology and has the potential to attract students to a scientific career. Therefore, the field of systems plant biology will especially promote the potential of young scientists and promises to advance science a significant step forward. However, crucial to the success of this challenging idea of in silico experimental studies on stress adaptation will be the quality and completeness of the data used. Modeling the potential of plants requires a maximum of input of regulatory networks working in plants to cover the high adaptability of plants to environmental conditions and the plasticity of plant reactions. Therefore, it is of outstanding importance to understand all levels of regulatory mechanisms. This includes sequence analysis of genes and non-gene DNA, and studies of transcriptomes and posttranscriptional regulation, of proteomes and posttranslational regulation, as well as of metabolomes. Besides, profound knowledge on the functioning of regulatory genes, like transcription factors, seems to be critical to understanding general and specific expression control mechanisms in plant responses. But of equal importance for future progress will be our understanding of the details of chromatin and nuclear organization. In medicinal research and research on plant development, global mechanisms to organize genome structure and nuclear territories are discussed as superimposed instruments for the regulation of concerted gene activities. Nevertheless, in plant research on stress adaptation, the significance of this kind of global regulation of expression is still more or less ignored. This article will first illustrate how plants can adapt in a complex and coordinated manner to transient changes of abiotic environmental conditions and why cellular reprogramming is considered as a key process in stress adaptation. As an example, recent knowledge on both physiological and molecular adaptive reactions by plants to phosphorus (P) deficiency will be pointed out. Then, the factors involved in global genome regulation will be presented, and their possible contribution for adaptive reprogramming in target cells will be brought to attention. Nutrient deficiency may seriously interfere with normal plant growth and development. Nutrient efficiency is therefore thought to be an important goal in plant breeding. This might refer to macronutrients, such as nitrogen and P, and/or microelements, such as iron or zinc. Phosphorus is especially critical in terms of crop productivity. Access to this nutrient may be hampered by soil characteristics and water availability. Bioavailable anionic phosphate may be excluded from soil solutions and, thus, from mobility in the soil by the strong tendency of P to form insoluble inorganic compounds or to convert to organic forms. Adaptation to abiotic stress. The figure emphasizes typical phenotypic and epigenetic changes at the whole-plant as well as the cell level in response to phosphate deficiency (A) and indicates factors involved in global genome regulation (B). For details, refer to the text. The amount of P taken up into the root system is about proportional to the percentage of root hairs (Jungk, 2001). Therefore, root hairs are discussed as a breeding trait for high nutrient efficiency in crop plants. Taking into account that induction of root hairs by environmental conditions demands redifferentiation of existing root epidermal cells to trichoblasts, it was recommended by Michael (2001) to calculate this trait in studies of environmental effects on plants as “percentage of hair-forming cells in the rhizodermis” rather than “hair density per unit root length” (p. 118), as it is used for studies on mineral uptake. Another kind of significant cell redifferentiation response to P deficiency is typically observed in the rhizodermis near the root apex next to the zone of differentiation, where root hair initiation takes place. Here, so-called transfer cells are formed. These cells rarely occur under ordinary conditions and demonstrate two outstanding characteristics: strong enlargement of the cell surface due to ingrowths of secondary cell wall material extending into the cell lumina and a high increase in the number of mitochondria pointing to a high turnover of energy and carbon. Although the specific function of transfer cells in the rhizodermis remains to be further elucidated, in general they are thought to strengthen the flux of solutes at the boundaries of symplast and apoplast. Along with these environmentally induced changes in cell differentiation during adaptation, the rhizosphere of P-depleted plants is found to be enriched by plant excretion products, including protons and organic acids such as citrate and malate. Excreted acidic phosphatases as well as ribonucleases are also reported to occur due to P deficiency. These compounds are appropriate to initiate the conversion of immobile P in the soil to bioavailable forms by chemical and biochemical reactions or promotion of the proliferation of associating microorganisms and fungi, including also mycorrhizae. Taken together, adaptive phenotypic expression as response on P deficiency is primarily directed to avoid or minimize forthcoming stress by increasing P uptake. This is achieved by different strategies: (1) through the enlargement of the surface of the root system to reach a wider area of the environment; (2) by intensifying excretion of plant compounds to influence the bioavailability of the nutrient actively; and (3) by enhancing the potential of the uptake system. To realize these adaptive reactions to low amounts of bioavailable P, interaction of organs and targeting of tissues and cells for differential regulation is required. Highly efficient methods are available now to study complex alterations at the level of transcripts, proteins, and metabolism, completing our current knowledge due to genomics. A wealth of data has been recorded recently for changes caused by various abiotic stress inducers and is ready to be analyzed by bioinformatics. All these data show that numerous genes and pre- as well as posttranscriptional and/or -translational factors and processes are involved to achieve appropriate plant responses to environmental circumstances, including mechanisms for stress avoidance as well as tolerance. Related to P depletion, for example, Wu et al. (2003) performed microarray studies in shoots and roots of Arabidopsis that covered transcription analysis of 6,172 genes. About 30% of these genes, i.e. 1,835 genes, have been transiently up- or down-regulated by 2-fold or more within the first 72 h under P deprivation. These genes cover a wide range of functions, including more than 100 genes each for transcription factors as well as cell signaling proteins. In the roots, 296 genes were specifically repressed and 141 specifically up-regulated. In the shoot, the number of differentially regulated genes was significantly higher and accounts for 617 down-regulated and 488 up-regulated genes. A further 293 genes were found to be up- or - down-regulated in the shoot as well as in the roots. It is noteworthy that adaptive reprogramming obviously requires a higher number of down-regulated genes than up-regulated genes. Alteration of complex expression patterns needs to be coordinated at the cell level. During recent years, a driving force to gain new insights in basic knowledge on how plants function at cellular levels has been the powerful search for transgenes that might enable efficient molecular breeding on abiotic stress tolerance. Three levels in cell biology have been mainly envisaged as tools for analyses and manipulation: (1) the level of target proteins, which are involved directly in metabolism or structure; (2) the level of regulatory proteins, namely the transcription factors and their target sequences to affect gene activity; and, evidently, (3) the level of signal transduction, including e.g. calcium and activated oxygens as signals, as well as signal cascades like the mitogen-activated protein kinase system. However, regulation of gene expression also requires superimposed organizational structures to realize coordinated transient access to the binding sites of regulating factors. In eukaryotes, accessibility of DNA sequences to the transcription machinery is crucially determined by the degree of packaging of the DNA into condensed and open chromatin domains. Additionally, recent studies have been undertaken to unravel the role of nonrandomly positioning of genes in the nucleus for gene expression during the interphase of the cell cycle. Global genome regulation refers to the structural and compositional organization of chromatin in the nucleus that defines coordinated accessibility to the DNA. The importance of factors involved in global genome regulation is currently highly acknowledged as critical for genetic as well as epigenetic programming in plant development. Environmentally induced reprogramming of cells during adaptation points to developmental plasticity as a typical characteristic of plants. This suggests a significant role of global genome regulation also in adaptive plant cell biology. Linear DNA is packaged into a condensed higher-order structure, the chromatin. Organization to a first-order condensation is achieved by wrapping the DNA around a globular octamer of histone proteins in a 1.8 turn according to 146 bp. The octamer consists of two tetramers of the histones H2A, H2B, H3, and H4. The DNA/protein complexes are called nucleosomes. Nucleosomes are linked to each other by a linear DNA stretch of 20 to 200 bp, giving the impression of beads on a string in electron microscopy. This 10-nm-diameter fiber is referred to as decondensed or open chromatin, which is ready to get directly into contact with regulatory factors, e.g. of the transcription or replication machinery. A higher degree of condensation will render access to the DNA more difficult or even impossible, leading finally to the silencing of underlying sequences. To further condense the 10-nm-diameter fiber to a solenoid structure, histone H1 links coils consisting of 6 nucleosomes to the famous 30-nm-diameter fiber. These chromatin structures are typically addressed to the fraction of euchromatic domains, whereas heterochromatic domains demonstrate highly compact structures that are generally inaccessible to DNA-binding factors and transcriptionally silent. Heterochromatic regions are thought to have an important impact on the realization of cell programs during development and differentiation and, hence, are of high interest related to future research on plant stress responses. Large heterochromatic domains are found at the centromeric and telomeric regions of the chromosomes and contribute to proper chromatid cohesion and chromosome segregation. However, additional smaller heterochromatic domains are distributed throughout the chromosomes. Current studies reveal that many factors and processes are involved in the assembly of heterochromatin, including, most importantly, the targeting of initiation sites by help of repetitive sequences or silencers as well as the posttranslational modifications of histones (see Grewal and Moazed, 2003). A flux from a decondensed to a more condensed state and vice versa is crucial for all kinds of cellular differentiation. This flexibility in chromatin structure is termed chromatin remodeling and may be defined as “any event that alters the nuclease sensitivity of a region of chromatin” (Aalfs and Kingston, 2000, p. 548). 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