Colloids and Surfaces B: Biointerfaces 54 (2007) 3745

Review

Understanding molecular mechanism of higher plant plasticity under abiotic stress

Hong-Bo Shao a,b,c, , Qing-Jie Guo c , Li-Ye Chu c , Xi-Ning Zhao b, , Zhong-Liang Su c , Ya-Chen Hu d , Jiang-Feng Cheng c
a

Molecular Biology Laboratory, Bio-informatics College, Chongqing University of Posts & Telecom, Chongqing 400065, Peoples Republic of China b Center of National Water-saving and Irrigation at Yangling, Centre of Soil and Water Conservation and Eco-environmental Research, The Chinese Academy of Sciences and Northwest A&F University, Yangling 712100, Peoples Republic of China c College of Molecular and Chemical Engineering, Qingdao University of Science and Technology, Qingdao 266042, Peoples Republic of China d Teaching Affairs Department, Jilin Normal University, Siping 136000, Jilin, Peoples Republic of China Received 23 May 2006; received in revised form 2 July 2006; accepted 7 July 2006 Available online 10 July 2006

Abstract Higher plants play the most important role in keeping a stable environment on the earth, which regulate global circumstances in many ways in terms of different levels (molecular, individual, community, and so on), but the nature of the mechanism is gene expression and control temporally and spatially at the molecular level. In persistently changing environment, there are many adverse stress conditions such as cold, drought, salinity and UV-B (280320 mm), which inuence plant growth and crop production greatly. Plants differ from animals in many aspects, but the important may be that plants are more easily inuenced by environment than animals. Plants have a series of ne mechanisms for responding to environmental changes, which has been established during their long-period evolution and articial domestication. These mechanisms are involved in many aspects of anatomy, physiology, biochemistry, genetics, development, evolution and molecular biology, in which the adaptive machinery related to molecular biology is the most important. The elucidation of it will extremely and purposefully promote the sustainable utilization of plant resources and make the best use of its current potential under different scales. This molecular mechanism at least include environmental signal recognition (input), signal transduction (many cascade biochemical reactions are involved in this process), signal output, signal responses and phenotype realization, which is a multi-dimensional network system and contain many levels of gene expression and regulation. We will focus on the molecular adaptive machinery of higher plant plasticity under abiotic stresses. 2006 Published by Elsevier B.V.
Keywords: Plant gene regulatory network system; Abiotic stress; Signal; Biointerfaces; Physiological mechanisms; Biological water-saving; Agricultural sustainable development

Contents
1. 2. 3. 4. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . A general model for stress signal transduction pathway in higher plants . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Plant physiological function performance under abiotic stress . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Aspects of plant gene regulatory network system . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.1. Environmental stress-responsive transcriptional elements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.2. Complexity of plant gene regulatory network system: specicity and cross-talk . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Concluding remarks and perspective . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Acknowledgement . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 38 38 40 40 40 41 41 43 43

5.

Corresponding author. Tel.: +86 23 62477654. Corresponding author. E-mail addresses: zxnsbs@yahoo.com.cn (X.-N. Zhao), shaohongbochu@126.com, shaohongbochu@hotmail.com (H.-B. Shao).

0927-7765/$ see front matter 2006 Published by Elsevier B.V. doi:10.1016/j.colsurfb.2006.07.002

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1. Introduction Unlike animals, higher plants, which are sessile, cannot escape from the surroundings, but adapt themselves to the changing environments by forming a series of molecular responses to copying with these problems. The physiological processing basis for these molecular responses is the integration of many transduced events into a comprehensive network of signaling pathways. Higher plant hormones occupy a central place in this transduction network, frequently acting in conjunction with other signals, to co-ordinately regulate cellular processes such as division, elongation and differentiation, which are the fundamental basis for higher plant development and related character expressions [119]. In a word, it is at the molecular level-gene expression and control in time and space that we can bring out the mystery of living organisms and explore the nature of environmental changes [2029]. Ecological science is the fused and ramied eld between natural sciences and social sciences where the frontier is molecular ecology and very important to conducting the practice of vegetation restoration and reconstruction and crop production on the globe. It is obvious that molecular biology is the purposeful basis for improving diverse types of eco-environment [3037]. The common stress factors mentioned above are those important ecological factors inuencing environment, which are general environmental stimuli and cues to higher plants [2439]. Molecular responses to such common environmental stresses have been studied intensively over the last few years, in which there is an intricate network of signaling pathways controlling perception of these environmental stress signals, the generation of second messengers, signal transduction, and therefore, deeper understanding of these molecular processes is even vital to the agricultural production in the arid and semiarid area of the world. In this review, updated progresses were introduced in terms of functional analysis of signaling components and problems with respect to agricultural eco-environment, and a probable general network of stress-responsive gene expression-control model were summarized, with an emphasis on the integration between stress signal transduction pathways and agricultural eco-environment. The viewpoint is that the molecular information from higher plant cells, tissues, and organs should be efciently popularized to levels of individuals, community, and ecosystem, which can play a greater role, and which is also one of the greatest challenges for plant systems biology during the 21st century. Human being has stepped into glorious 21th century, during which sustainablehealthy utilization for environment and resources and its own health concerns are the most important issue. This issue is tightly linked with agriculture (food) and eco-environment, in which biology, in particular plant biology plays the greatest role, because plants offer the globe its only renewable resource of food, building material and energy and plant biology is the most powerful tool to reasonably use natural resources [15]. In the broad eld of plant biology, its core is the study for life activities at molecular level (mainly, DNA and protein macromolecules), whose interactions at various biointerfaces at different scales are quite important to keep a steady state between plants and changing environment, espe-

cially adverse surroundings [619]. So, adaptation in plants is an important and timely topic in basic and applied biology [2028]. On the one hand, it is very interesting to understand interaction between plants and their environment. On the other hand and in view of the needs for human life, we more want to create crop plants that are able to confront successfully unfavorable natural conditions [2949]. The main aim in plant breeding is to obtain plants that combine higher yields, reliable yield stability, better quality and obvious characters resisting stresses (abiotic and biotic) over years and locations [2,4,7,9,5057]. 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 globe [58,59,118]. Diverse forms of abiotic stresses may occur, including drought, cold and freezing, heat, salinity, nutrient deciency, toxic heavy metals, oxidative stress as well as oxygen shortage, and mechanical stress [6072,118]. Although it is accepted that diverse environmental stress factors never act alone, experimental study of plant responses to abiotic stress is normally restricted to plant reactions on isolated stress factors [7377,115]. 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 stressed phenotype [72,73,7887,102,103,114]. Consequently, plants usually respond to a unique complex of growth conditions [33,34,55,56,88,89,104]. Stress inducers from the abiotic as well as biotic world have some common signal and responding pathways in plants [4,8,10,12,9095,104,115] and thereby have the potential to moderate the effect of each other through cross-talking [6075,96,104]. Further, plants, as sessile organisms, have to get alone with the dynamics of transiently changing environmental conditions and have the exibility for responding to these complicated changes [9,10,12,17,19,21,2830,32,38,49,55,57,104], and this has to be achieved at the various stages of plant development [4,6,11,21,22,57,59,6976,77,84,90,105]. 2. A general model for stress signal transduction pathway in higher plants Animals perceive their local environments by complex signal transduction processes. Intelligent responses are computed, and tness is increased by behavioral changes that commonly involve movement. Movement is a fundamental part of the animal lifestyle that aroses in evolution from the requirements to nd food and to mate. The same case happens on higher plants and sessile higher plants must also change behavior to increase tness as the local environment uctuates. The ubiquitous distribution of light has never provided evolutionary pressure to develop movement; instead, behavioral changes are exemplied by phenotypic plasticity. But the need for detailed environmental stimuli, accurate sensing, assessment, and intelligent computation are just strong [106129]. A stronger spatial dimension network underlies signal transduction; for instance, and higher plants must be able to detect gradients in signals (such as light) and resources (such as nitrate and water). Higher plant development itself also is decidedly polar. The spatial dimension

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Fig. 1. A common framework model for the signal transduction of abiotic stress in higher plants.

is satised in many ways. Higher plant cells place receptors, channels, G proteins, and kinases, in specic membranes. Some signaling protein complexes are permanent, such as relatively stable and perhaps hardwired COP9 signalosome. Other signaling protein complexes are likely to be ephemeral and formed immediately as a result of signaling. There are at least 600 receptor kinases in Arabidopsis, and most of them are membrane bound. Incompatibility and disease defense signal transduction use receptor kinases. After ligand binding and autophosphorylation, such kinases may act as nucleation sites for the construction of ephemeral signaling complexes that contain many proteins [130]. Although there are some differences in different higher plants, a common signal model for stress transduction pathways exist in higher plant (Fig. 1). This model begins with the perception of signals from environments, followed by the generation of second messengers (such as inositol phosphates and reactive oxygen species). Second messengers can modulate intracellular Ca2+ levels, often initiating a protein phosphorylation cascade that nally targets proteins directly involved in cellular protection or transcription factors controlling specic sets of stress-regulated genes. The products of these genes may participate in the production of regulatory molecules like the plant hormones abscisic acid (ABA), ethylene, and salicylic acid (SA). Some of these regulatory molecules can, in turn, initiate a second round of circulation. More and more facts from different disciplines of natural sciences and social sciences have clearly shown that molecular biology is the leading during the 21st century, by which many issues may get a eventual resolution to. It is the time that we should take much care about our environment on the basis of considering a vast amount of data involved in biology, physiology, pedology, environmental stress and molecular biology. How to integrate this information available, how to analyze the data completely, how to establish a tied relationship among different data obtained at different levels and accuracy are the main challenges confronted in front of us, which are the key points for us to improve our environment and conduct sustainable development on purpose. We are facing a

uctuating world, in which the surrounding is worse and worse and the resource is more and more limited, our nal goal just being to adapt ourselves to such circumstance and utilize it best and to have the optimium survival space through our knowledge. A recent Floral Genome Project, an ambitious undertaking linking phylogenetic, genomic, and developmental perspectives on plant reproduction, funded by the National Science Foundation of USA from October 2001 through 2006 will provide us with more comprehensive knowledge about the origin, conservation, and diversication of the genetic architecture of owers, which will also give us insights into the global changes [131]. Rossel et al. used microarray techniques and Arabidopsis as experimental materials to explore the relationship between global changes and gene expression, enforcing and further bearing out the multiplicity and universality that higher plants are adapted to changing environment from the starting point of gene expression. Much research is needed in this frontier and overlapped eld. Advances in our understanding of the integration of higher plant signaling processes at the transcription level have relied, rely and will continue to rely heavily on the application of genetic approaches in the model plant Arabidopsis thaliana. Such studies have helped, in the rst instance, to identify important components of hormone and other stress signaling pathways. An integrative signaling function has often been elucidated through the pleiotropic hormone response phytotype of the null mutation or by subsequent second-sited mutation screens. At the protein level, novel interactions between newly discovered components from nominally discrete signaling pathways will be detected through the application of two-hybrid proteomic-based approaches or the use of high-throughput protein chip-based technologies. No doubt, microarray based expression analysis represents the genomic technology most (likely to have an immediate impact on this area of research). The ability to prole the entire Arabidopsis genome opens up unprecedented opportunities to study different environmental stress signals at the level of gene expression. However, great care must be taken in experimental design to ensure that meaningful results are obtained. For

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instance, the researcher, must ensure that comparisons are made between materials at equivalent developmental stages when proling a hormone mutant versus wild type. Equally importantly, validation of initial expression proling results must be obtained with either independent alleles or related hormone mutants. Remember, these results should be compared with those obtained from other higher plants as possible as researchers can. It is very clear that signal transduction processes are very much complicated, requiring the suitable, spatial and temporal coordination of all signaling molecules involved in the transduction process. Therefore, there are some molecules that take part in the modicaton, delivery, or assembly of signaling components, but do not directly relay the signal. They are very critical for the precise transmission of stress signals. These proteins include protein modiers (e.g., enzymes for protein lipidation, methylation, glycosylation, and ubiquitination), scaffolds, and adaptors. 3. Plant physiological function performance under abiotic stress Plants live in soil-plant-atmosphere continuum (SPAC) environment, and they have to coordinate the mechanisms of diverse types to respond to the above changing environment at any time for sustainable survival [96100,104,112,115]. Plant production realization is obtained eventually through physiological pathways at least at the level of individual and community [52,56,89,90]. One molecule, one kind of tissue or an organ cannot produce any economic yield in terms of the need for human being [76,77,95]. Under the condition of ensuring plant survival, plants can produce corresponding yield. Water is one of key factors inuencing plant production and many reports have proved this clearly [10,20,2426,33,45,59,62,85,94,95,104118]. Loss of water in soil will lead to great reduction in plant production, which has been reected from total grain yield of many countries in the world [81,114,115]. Water is the important material for photosynthetic reactions that plants depend on to nish accumulation of photosynthetic products, which are impacted greatly by physiological pathways and environmental factor (such as soil water supply) [96100]. So, different soil water supplying will result in quite different physiological pathways, which directly determine the ability for plants to make photosynthetic products [9,18,20,29,47,52,56,81,95,107,114,115]. Water decits in soil environment also inuence solute transport (ion and nutrient uptake of plants) to larger extent, which effects on photosynthetic reactions in plant chloroplasts in many ways [28,29,36,52,54,55,58,59,8891,95,93108]. This is the reason that ion homeostasis and redox state have been brought to attention [15,18,34,37,40,58,63,66,67,8588,103,104]. The series of the above reactions and processes occurring at different biointerfaces is regulated and controlled by plant gene regulatory network system spatially and temporally on the basis of responding to plant developmental cue, through which plants can elegantly respond to the changing environment [10,70,71,104]. This network system has been formed by the interaction between plants and environment for a long time of

evolution, which will continue to evolve with environmental succession [12,21,30,105]. From the angle of individual plant development, Plant Growth Periodicity curve can reect and show the above trend [21,90,104,105]. Besides, plant responses to soil water decits take a slow-fast-slow shaped curve in terms of main physio-biochemical indices change and this is in agreement with Plant Growth Periodicity, which also illustrates this fact and wide plasticity for plants [69,105]. Surely, concerted expression of corresponding genes in plant gene regulatory network system makes it possible that we can see the phenotype and phenotype change under given temporalspatial condition [22,95,104,105,114,123,124]. 4. Aspects of plant gene regulatory network system Recent progress in molecular biology (especially, DNA microarray), genomics, proteomics and metabolomics has obtained insight into plant gene regulatory network system, which is mainly composed of inducible-genes (environmental factors and developmental cues), their expression programming and regulatory element (cis-element and trans-element), corresponding biochemical pathways and diverse signal factors [96,101103]. Under the condition of soil water decits, related stress factors always result in overlapping responses, including anatomical, physiological, biochemical, molecular biological changes, which make plant gene regulatory network system more complicated and difcult to explore [95100,102,113]. Much information with respect to this topic is from the model plant, Arabidopsis thaliana. Main aspects will be illustrated below. 4.1. Environmental stress-responsive transcriptional elements Plants can sense, process, respond to environmental stress and activate related-gene expression to increase their resistance to stress [103113]. Environmental stress-inducible genes can be mainly divided into two types in terms of their protein products: one type of genes, whose coding products directly confer the function of plant cells to resist to environmental stress such as LEA protein, anti-freezing protein, osmotic regulatory protein, enzymes for synthesizing betaine, proline and other osmoregulators; the other type of genes, whose coding products play an important role in regulating gene expression and signal transduction such as the transcriptional elements for sensing and transducing the protein kinases of MAP and CDP, bZIP, MYB and others [30,32,33,45,75,104]. Transcriptional elements are dened as the protein combining with the specialized DNA sequence of eukaryotic promoters or the protein having structural characteristics of known DNA-combining region, whose main function is to activate or suppress transcriptional effect of corresponding genes [4,5,13,37,51]. Up to now, hundreds of transcriptional elements of environmental stress-responsive genes in higher plants have been isolated, which regulate and control the stress reaction related to drought, salinity, cold, pathogen and heat [30,32,70,71,85,104]. In the genome of Arabidopsis and rice, they have about 13001500 genes for coding

H.-B. Shao et al. / Colloids and Surfaces B: Biointerfaces 54 (2007) 3745 Table 1 Some of identied transcriptional elements in higher plants Plant materials Arabidopsis thaliana A. thaliana A. thaliana A. thaliana A. thaliana A. thaliana A. thaliana A. thaliana A. thaliana Oryza Zea mays Triticum Avena Helianthus Phaseolus Phaseolus Craterestinma Daucus Populus Factors ABI5/AtDPBF AtDPBF2 AtDPBF4 ABF1 ABF2/AREB5 ABF4/AREB2 GBF3 AB53 ATHB6 OsVPI VP1 EmBP-1 AtVPI DPBF5,-2,-3 ROM2(repressor) PIARF Cpvp1 C-ABI3 PtABI3 Binding sites/factor types ABA response element (ABREs)/bZIP ABA response element (ABREs)/bZIP ABA response element (ABREs)/bZIP ABA response element (ABREs)/bZIP ABA response element (ABREs)/bZIP ABA response element (ABREs)/bZIP ABA response element (ABREs)/bZIP RY/sph elements/B3 domain proteins HD-Zip RY/sph elements/B3 domain proteins MYB ABA response element (ABREs)/bZIP RY/sph elements/B3 domain proteins ABA response element (ABREs)/Bzip ABA response element (ABREs)/Bzip RY/sph elements/B3 domain proteins RY/sph elements/B3 domain proteins RY/sph elements/B3 domain proteins RY/sph elements/B3 domain proteins

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transcriptional elements, most of which have not been identied functionally [4,27,29,37,64,67,74,75]. Recent study has shown that the transcriptional elements involved in plant stress responses mainly include four kinds: APETALA2/EREBP, bZIP, WRKY, and MYB [40,47,50,51,75,104,117]. Typical transcriptional elements have been summarized in Table 1 for reference. 4.2. Complexity of plant gene regulatory network system: specicity and cross-talk Many transcriptional element families participate in plant stress responses, each of which has many members with *highly conservative DNA-binding domain, composing a complicated, temporalspatial network system for plant gene expression and regulation [4,70]. Different members of TGA/OBF families have different DNA-binding specicity, proteinprotein interaction and expressing proles. Chromatin immunoprecipitation techniques indicated that tobacco TGA1a in vivo combined with xenobiotic-responsive promoters, but could not combine with PR promoter with as-1 cis-element [78,104,119]. Arabidopsis TGA2 could be responsive to SA signal, but not be

responsive to xenobiotic stress signals [1,3,104,120]. Much analysis of genomic expression proling by DNA microarray indicates that the mRNA coding transcriptional element genes in many plants are usually induced to express and accumulated [14,17,19,113120]. Most transcriptional element genes involved in plant stress responses have not only completely different expression proles, but also some overlapping expression proles, showing the complexity, specicity and cross-talk of plant gene regulatory network system [4,70,71,115]. In other words, one kind of stress may simultaneously activate many transcriptional elements and one transcriptional element may be activated by many types of plant stress responses [75,104]. For instance, CBF3/DREB1a can be responsive rapidly to cold, at the same time, regulated by circadian clock [75,121], which reects the functional complement between plant coldresponsive pathway and circadian clock-regulated circle in terms of CBF3/DREB1a functions. Shinozaki et al. [70,71] thought that four signal pathways were involved in plant drought, cold and salinity responses, in which two were ABA-dependent (I and II), and two were non-ABA-dependent (III and IV). The process of stress signal sensing and transducing, transcriptional regulating, and functional expressing was existent in these pathways. It is obvious that transcriptional elements play a central role in the process [75,115123]. Zhu [85] concluded that molecular mechanism of plant stress response (drought and salinity)included three main steps, i.e., stress signal input, transducing process, and regulatory product output through the study of Arabidopsis drought and salinity for many years. Results of many genetic mutants and key intermediate molecules from his lab supported his view powerfully. Recent related anti-drought data (dynamic change of anti-oxidative enzymes and soil water stress threshold) from my lab also proved the point [7577,105111]. From plant developmental context, plant responses to environmental stresses have a universal law, which has been reected completely by Plant Growth Periodicity curve [69]. Our study on dynamic changing of wheat anti-oxidative enzymes under soil water decit have indicated that wheat with different genotypes responded to soil water stress by taking a slow-rapid-slow characteristic curve during wheat life cycle [105,114]. This is the physiological basis for water-saving agriculture and dry land farming, which also provides substantial evidence for the above viewpoint [9,10,90,112,114,115]. 5. Concluding remarks and perspective Plants are different from animals in many aspects. The most important difference is that plants are more easily inuenced by environmental factors than animals [49,104,105]. So, plants have more rene mechanisms to regulate themselves from molecular level to ecosystem to respond to environmental changing. For instance, there are many coding-protein genes downstream only for osmotic regulation in abiotic stress resistance (Table 2) [6,8,16,19,24,43,47,75,78,98,104,117,130]. By contrast, animals are more active and have the ability to escape from environmental stresses in most cases [49]. Under the above background, plants are quite different animals in their gene regu-

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Fig. 2. The basic draft for plant gene regulatory network system.

latory network system [49,60,82,131,132]. Nerve system-based or nerve system-like-based structure and hormones are composed of the body for gene expression in animal network system, leading to animal activeness [82,126130]. In addition, developmental programming cannot be easily effected by environmental cues [49,104]. Plants are always in the state of passiveness for confronting environmental succession and the related issue is more complicated, which is the main cause that plants are behind animals in the study of most elds [127,128,131].
Table 2 Some examples of the osmotic regulating genes downstream in abiotic resistance Components ROS scavenging Chaperones Fructan Trehalose Glycine betaine Proline Ectoine K+ -transporters K+ -channels H2 O channel proteins Metabolic functions Increase in ROS scavenging enzymes Heat-/cold-/salt-shock proteins; protein folding Osmoprotection Osmoprotection Protein protection and carbon sink Substrate for mitochondrial respiration; redox control Osmoprotectant High afnity K+ uptake Low afnity or dual afnity K+ uptake Membrane cycling control Gene/proteins GP, PHGPX Hsp, Csp, Ssp, DnaJ SacB Tps; Tpp, trehalase codA P5CS/P5CR EctA, BC Hkt1, Hak1 Akt1, Akt TIP

Charting plant gene regulatory network system under soil water decits is a great challenge. Nowadays, there are indeed many favorable conditions for charting this blueprint, including much available data from Arabidopsis, rice, grass, yeast and fruit y, but the range of tested plants is very much limited, many stress-responsive genes have not been unied in terms of their rene functions, and many genes participating in environmental stresses are interacted and overlapped, which have led to incorrect placing of key gene (gene effectors) and signal molecules in the whole plant gene regulatory network system [95,115,128]. Besides, much data are from under condition of one type of stresses. It is a fact that plants always confront more than two kinds of individual environmental stresses or their combination simultaneously in eld [43,71,94,104,115,130,131]. Although drawing this dimensional plant gene regulatory network system with great details and complete pathways is impossible currently, the basic draft for this blueprint could be summarized in Fig. 2. This draft was established in combination with recent advance in this hot topic and from the context of development, which will provide instructions for further investigation and insights into understanding of plant rene plasticity for abiotic environmental stresses [127132]. In a word, precise elucidation of plant gene regulatory network system under abiotic stresses is of importance to molecularly engineering plant resistance, because of which many excellent scientists world-wide have been engaged in this frontier eld, resulting in a long-step progress [104,105,113,128132].

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There are also many issues remained to be solved and needed to make efforts. Scope of tested plants needs to be extended; comprehensive study on a combination of environmental stress factors in laboratories and in eld should be given much attention; system development viewpoint and computer simulation analysis method should be also applied. With accumulation of data from being extended plant range, the molecular mechanism of higher plant plasticity, i.e., plant gene regulatory network system under environmental stresses will be clearer and clearer. Acknowledgement Shao HB is grateful for the support from Initiation Foundation of Chongqing University of Post & Telecom (2005A-92), Qingdao University of Science and Technolog (0022221), Natural Science Foundation of Shandong Province, and Taishan Scholar Construction Project of Shandong Province (JS200510036). References
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