Colloids and Surfaces B: Biointerfaces 54 (2007) 37–45

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, People’s 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, People’s Republic of China
c College of Molecular and Chemical Engineering, Qingdao University of Science and Technology, Qingdao 266042, People’s Republic of China
d Teaching Affairs Department, Jilin Normal University, Siping 136000, Jilin, People’s 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 (280–320 mm), which influence plant growth and crop production greatly. Plants differ from animals in many aspects, but the important may
be that plants are more easily influenced by environment than animals. Plants have a series of fine mechanisms for responding to environmental
changes, which has been established during their long-period evolution and artificial 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. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 38
2. A general model for stress signal transduction pathway in higher plants . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 38
3. Plant physiological function performance under abiotic stress . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 40
4. Aspects of plant gene regulatory network system . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 40
4.1. Environmental stress-responsive transcriptional elements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 40
4.2. Complexity of plant gene regulatory network system: specificity and cross-talk . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 41
5. Concluding remarks and perspective . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 41
Acknowledgement . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 43
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 43

∗ 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
38 H.-B. Shao et al. / Colloids and Surfaces B: Biointerfaces 54 (2007) 37–45
1. Introduction
Unlike animals, higher plants, which are sessile, cannot
escape from the surroundings, but adapt themselves to the chang-
ing 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 funda-
mental basis for higher plant development and related character
expressions [1–19]. 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 [20–29]. Ecological science is the fused
and ramified field between natural sciences and social sciences
where the frontier is molecular ecology and very important to
conducting the practice of vegetation restoration and recon-
struction and crop production on the globe. It is obvious that
molecular biology is the purposeful basis for improving diverse
types of eco-environment [30–37]. The common stress factors
mentioned above are those important ecological factors influ-
encing environment, which are general environmental stimuli
and cues to higher plants [24–39]. 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 environ-
mental stress signals, the generation of second messengers, sig-
nal 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, up-
dated progresses were introduced in terms of functional analysis
of signaling components and problems with respect to agri-
cultural eco-environment, and a probable general network of
stress-responsive gene expression-control model were summa-
rized, 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 efficiently popularized to lev-
els 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, dur-
ing which sustainable—healthy 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 nat-
ural resources [1–5]. In the broad field of plant biology, its
core is the study for life activities at molecular level (mainly,
DNA and protein macromolecules), whose interactions at vari-
ous biointerfaces at different scales are quite important to keep
a steady state between plants and changing environment, espe-
cially adverse surroundings [6–19]. So, adaptation in plants is an
important and timely topic in basic and applied biology [20–28].
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 [29–49]. The main aim in plant breeding is
to obtain plants that combine higher yields, reliable yield sta-
bility, better quality and obvious characters resisting stresses
(abiotic and biotic) over years and locations [2,4,7,9,50–57].
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, salin-
ity, nutrient deficiency, toxic heavy metals, oxidative stress as
well as oxygen shortage, and mechanical stress [60–72,118].
Although it is accepted that diverse environmental stress factors
never act alone, experimental study of plant responses to abi-
otic stress is normally restricted to plant reactions on isolated
stress factors [73–77,115]. 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 [72,73,78–87,102,103,114]. Conse-
quently, 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 [4,8,10,12,90–95,104,115]
and thereby have the potential to moderate the effect of each
other through cross-talking [60–75,96,104]. Further, plants,
as sessile organisms, have to get alone with the dynamics
of transiently changing environmental conditions and have
the flexibility for responding to these complicated changes
[9,10,12,17,19,21,28–30,32,38,49,55,57,104], and this has to
be achieved at the various stages of plant development
[4,6,11,21,22,57,59,69–76,77,84,90,105].
2. A general model for stress signal transduction
pathway in higher plants
Animals perceive their local environments by complex sig-
nal transduction processes. Intelligent responses are computed,
and fitness is increased by behavioral changes that commonly
involve movement. Movement is a fundamental part of the ani-
mal lifestyle that aroses in evolution from the requirements to
find food and to mate. The same case happens on higher plants
and sessile higher plants must also change behavior to increase
fitness as the local environment fluctuates. The ubiquitous dis-
tribution of light has never provided evolutionary pressure to
develop movement; instead, behavioral changes are exemplified
by phenotypic plasticity. But the need for detailed environmental
stimuli, accurate sensing, assessment, and intelligent compu-
tation are just strong [106–129]. 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 devel-
opment itself also is decidedly polar. The spatial dimension
 H.-B. Shao et al. / Colloids and Surfaces B: Biointerfaces 54 (2007) 37–45
Fig. 1. A common framework model for the signal transduction of abiotic stress in higher plants.
is satisfied in many ways. Higher plant cells place receptors,
channels, G proteins, and kinases, in specific membranes. Some
signaling protein complexes are permanent, such as relatively
stable and perhaps hardwired COP9 signalosome. Other sig-
naling protein complexes are likely to be ephemeral and formed
immediately as a result of signaling. There are at least 600 recep-
tor kinases in Arabidopsis, and most of them are membrane
bound. Incompatibility and disease defense signal transduction
use receptor kinases. After ligand binding and autophosphoryla-
tion, 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 path-
ways 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 phosphory-
lation cascade that finally targets proteins directly involved in
cellular protection or transcription factors controlling specific
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 dif-
ferent 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 reso-
lution 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
39
fluctuating world, in which the surrounding is worse and worse
and the resource is more and more limited, our final 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 link-
ing 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 diversification of the genetic architecture of flowers, 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 multiplic-
ity 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 field.
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 stud-
ies have helped, in the first instance, to identify important com-
ponents of hormone and other stress signaling pathways. An
integrative signaling function has often been elucidated through
the pleiotropic hormone response phytotype of the null muta-
tion or by subsequent second-sited mutation screens. At the
protein level, novel interactions between newly discovered com-
ponents 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 imme-
diate impact on this area of research). The ability to profile the
entire Arabidopsis genome opens up unprecedented opportuni-
ties to study different environmental stress signals at the level of
gene expression. However, great care must be taken in experi-
mental design to ensure that meaningful results are obtained. For
40 H.-B. Shao et al. / Colloids and Surfaces B: Biointerfaces 54 (2007) 37–45
instance, the researcher, must ensure that comparisons are made
between materials at equivalent developmental stages when
profiling a hormone mutant versus wild type. Equally impor-
tantly, validation of initial expression profiling 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 transduc-
tion process. Therefore, there are some molecules that take part
in the modificaton, delivery, or assembly of signaling compo-
nents, but do not directly relay the signal. They are very critical
for the precise transmission of stress signals. These proteins
include protein modifiers (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) envi-
ronment, and they have to coordinate the mechanisms of diverse
types to respond to the above changing environment at any
time for sustainable survival [96–100,104,112,115]. Plant pro-
duction 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 can-
not 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 fac-
tors influencing plant production and many reports have proved
this clearly [10,20,24–26,33,45,59,62,85,94,95,104–118]. Loss
of water in soil will lead to great reduction in plant produc-
tion, which has been reflected from total grain yield of many
countries in the world [81,114,115]. Water is the important mate-
rial for photosynthetic reactions that plants depend on to finish
accumulation of photosynthetic products, which are impacted
greatly by physiological pathways and environmental factor
(such as soil water supply) [96–100]. So, different soil water
supplying will result in quite different physiological pathways,
which directly determine the ability for plants to make pho-
tosynthetic products [9,18,20,29,47,52,56,81,95,107,114,115].
Water deficits in soil environment also influence solute trans-
port (ion and nutrient uptake of plants) to larger extent, which
effects on photosynthetic reactions in plant chloroplasts in many
ways [28,29,36,52,54,55,58,59,88–91,95,93–108]. This is the
reason that ion homeostasis and redox state have been brought
to attention [15,18,34,37,40,58,63,66,67,85–88,103,104]. The
series of the above reactions and processes occurring at dif-
ferent 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 reflect and
show the above trend [21,90,104,105]. Besides, plant responses
to soil water deficits 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 illus-
trates this fact and wide plasticity for plants [69,105]. Surely,
concerted expression of corresponding genes in plant gene reg-
ulatory network system makes it possible that we can see the
phenotype and phenotype change under given temporal–spatial
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), cor-
responding biochemical pathways and diverse signal factors
[96,101–103]. Under the condition of soil water deficits, 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 difficult to explore [95–100,102,113].
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 [103–113]. Environmental stress-inducible genes can
be mainly divided into two types in terms of their protein prod-
ucts: 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 osmoregu-
lators; the other type of genes, whose coding products play an
important role in regulating gene expression and signal trans-
duction 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
defined as the protein combining with the specialized DNA
sequence of eukaryotic promoters or the protein having struc-
tural 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 Ara-
bidopsis and rice, they have about 1300–1500 genes for coding
 H.-B. Shao et al. / Colloids and Surfaces B: Biointerfaces 54 (2007) 37–45 41

Table 1 responsive to xenobiotic stress signals [1,3,104,120]. Much

Some of identified transcriptional elements in higher plants analysis of genomic expression profiling by DNA microarray
Plant materials Factors Binding sites/factor types indicates that the mRNA coding transcriptional element genes
Arabidopsis thaliana ABI5/AtDPBF ABA response element
in many plants are usually induced to express and accumu-
(ABREs)/bZIP lated [14,17,19,113–120]. Most transcriptional element genes
A. thaliana AtDPBF2 ABA response element involved in plant stress responses have not only completely dif-
(ABREs)/bZIP ferent expression profiles, but also some overlapping expression
A. thaliana AtDPBF4 ABA response element profiles, showing the complexity, specificity and cross-talk of
(ABREs)/bZIP
A. thaliana ABF1 ABA response element
plant gene regulatory network system [4,70,71,115]. In other
(ABREs)/bZIP words, one kind of stress may simultaneously activate many
A. thaliana ABF2/AREB5 ABA response element transcriptional elements and one transcriptional element may
(ABREs)/bZIP be activated by many types of plant stress responses [75,104].
A. thaliana ABF4/AREB2 ABA response element For instance, CBF3/DREB1a can be responsive rapidly to
(ABREs)/bZIP
A. thaliana GBF3 ABA response element
cold, at the same time, regulated by circadian clock [75,121],
(ABREs)/bZIP which reflects the functional complement between plant cold-
A. thaliana AB53 RY/sph elements/B3 responsive pathway and circadian clock-regulated circle in terms
domain proteins of CBF3/DREB1a functions.
A. thaliana ATHB6 HD-Zip Shinozaki et al. [70,71] thought that four signal pathways
Oryza OsVPI RY/sph elements/B3
domain proteins
were involved in plant drought, cold and salinity responses,
Zea mays VP1 MYB in which two were ABA-dependent (I and II), and two were
Triticum EmBP-1 ABA response element non-ABA-dependent (III and IV). The process of stress signal
(ABREs)/bZIP sensing and transducing, transcriptional regulating, and func-
Avena AtVPI RY/sph elements/B3 tional expressing was existent in these pathways. It is obvious
domain proteins
Helianthus DPBF5,-2,-3 ABA response element
that transcriptional elements play a central role in the process
(ABREs)/Bzip [75,115–123]. Zhu [85] concluded that molecular mechanism of
Phaseolus ROM2(repressor) ABA response element plant stress response (drought and salinity)included three main
(ABREs)/Bzip steps, i.e., stress signal input, transducing process, and regula-
Phaseolus PIARF RY/sph elements/B3 tory product output through the study of Arabidopsis drought
domain proteins
Craterestinma Cpvp1 RY/sph elements/B3
and salinity for many years. Results of many genetic mutants
domain proteins and key intermediate molecules from his lab supported his view
Daucus C-ABI3 RY/sph elements/B3 powerfully. Recent related anti-drought data (dynamic change of
domain proteins anti-oxidative enzymes and soil water stress threshold) from my
Populus PtABI3 RY/sph elements/B3 lab also proved the point [75–77,105–111]. From plant develop-
domain proteins
mental context, plant responses to environmental stresses have
a universal law, which has been reflected completely by Plant
Growth Periodicity curve [69]. Our study on dynamic chang-
transcriptional elements, most of which have not been iden- ing of wheat anti-oxidative enzymes under soil water deficit
tified functionally [4,27,29,37,64,67,74,75]. Recent study has have indicated that wheat with different genotypes responded
shown that the transcriptional elements involved in plant stress to soil water stress by taking a “slow-rapid-slow” characteristic
responses mainly include four kinds: APETALA2/EREBP, bZIP, curve during wheat life cycle [105,114]. This is the physiolog-
WRKY, and MYB [40,47,50,51,75,104,117]. Typical transcrip- ical basis for water-saving agriculture and dry land farming,
tional elements have been summarized in Table 1 for reference. which also provides substantial evidence for the above view-
point [9,10,90,112,114,115].
4.2. Complexity of plant gene regulatory network system:
specificity and cross-talk 5. Concluding remarks and perspective

Many transcriptional element families participate in plant
stress responses, each of which has many members with *highly
conservative DNA-binding domain, composing a complicated,
temporal–spatial network system for plant gene expression and
regulation [4,70]. Different members of TGA/OBF families
have different DNA-binding specificity, protein–protein inter-
action and expressing profiles. 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]. Ara-
bidopsis TGA2 could be responsive to SA signal, but not be
Plants are different from animals in many aspects. The
most important difference is that plants are more easily influ-
enced by environmental factors than animals [49,104,105]. So,
plants have more refine mechanisms to regulate themselves
from molecular level to ecosystem to respond to environmen-
tal changing. For instance, there are many coding-protein genes
downstream only for osmotic regulation in abiotic stress resis-
tance (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-
42 H.-B. Shao et al. / Colloids and Surfaces B: Biointerfaces 54 (2007) 37–45

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

latory network system [49,60,82,131,132]. Nerve system-based Charting plant gene regulatory network system under soil
or nerve system-like-based structure and hormones are com- water deficits is a great challenge. Nowadays, there are indeed
posed of the body for gene expression in animal network system, many favorable conditions for charting this blueprint, includ-
leading to animal activeness [82,126–130]. In addition, develop- ing much available data from Arabidopsis, rice, grass, yeast and
mental programming cannot be easily effected by environmental fruit fly, but the range of tested plants is very much limited, many
cues [49,104]. Plants are always in the state of passiveness for stress-responsive genes have not been unified in terms of their
confronting environmental succession and the related issue is refine functions, and many genes participating in environmental
more complicated, which is the main cause that plants are behind stresses are interacted and overlapped, which have led to incor-
animals in the study of most fields [127,128,131]. rect placing of key gene (gene effectors) and signal molecules in
the whole plant gene regulatory network system [95,115,128].
Table 2
Besides, much data are from under condition of one type of
Some examples of the osmotic regulating genes downstream in abiotic resistance stresses. It is a fact that plants always confront more than two
kinds of individual environmental stresses or their combination
Components Metabolic functions Gene/proteins
simultaneously in field [43,71,94,104,115,130,131]. Although
ROS scavenging Increase in ROS scavenging GP, PHGPX drawing this dimensional plant gene regulatory network system
enzymes with great details and complete pathways is impossible currently,
Chaperones Heat-/cold-/salt-shock Hsp, Csp, Ssp, DnaJ
proteins; protein folding
the basic draft for this blueprint could be summarized in Fig. 2.
Fructan Osmoprotection SacB This draft was established in combination with recent advance
Trehalose Osmoprotection Tps; Tpp, trehalase in this hot topic and from the context of development, which
Glycine betaine Protein protection and carbon codA will provide instructions for further investigation and insights
sink into understanding of plant refine plasticity for abiotic environ-
Proline Substrate for mitochondrial P5CS/P5CR
respiration; redox control
mental stresses [127–132].
Ectoine Osmoprotectant EctA, BC In a word, precise elucidation of plant gene regulatory net-
K+ -transporters High affinity K+ uptake Hkt1, Hak1 work system under abiotic stresses is of importance to molecu-
K+ -channels Low affinity or dual affinity Akt1, Akt larly engineering plant resistance, because of which many excel-
K+ uptake lent scientists world-wide have been engaged in this frontier
H2 O channel proteins Membrane cycling control TIP
field, resulting in a long-step progress [104,105,113,128–132].
 H.-B. Shao et al. / Colloids and Surfaces B: Biointerfaces 54 (2007) 37–45
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 field should be given much atten-
tion; system development viewpoint and computer simulation
analysis method should be also applied. With accumulation of
data from being extended plant range, the molecular mecha-
nism of higher plant plasticity, i.e., plant gene regulatory net-
work 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), Qing-
dao University of Science and Technolog (0022221), Natural
Science Foundation of Shandong Province, and Taishan Scholar
Construction Project of Shandong Province (JS200510036).
References
[1] N. Agraval, P.V.N. Dasaradhi, A. Mohmmed, et al., RNA interference:
biology, mechanism, and application, Microbiol. Mol. Biol. Rev. 67 (4)
(2003) 657–685.
[2] A. Anand, H.N. Trick, B.S. Gill, et al., Stable transgene expression
and random gene silencing in wheat, Plant Biotechnol. J. 1 (4) (2003)
241–254.
[3] V. Ambros, B. Bartel, D.P. Bartel, et al., A uniform system for microRNA
annotation, RNA 9 (2003) 277–279.
[4] E.A. Bray, Genes commonly regulated by water-deficit stress in Ara-
bidopsis thaliana, J. Exp. Bot. 55 (407) (2004) 2331–2341.
[5] M.A. Beer, S. Tavazoie, Predicting gene expression from sequence, Cell
117 (2004) 185–198.
[6] E.M. Brill, J.M. Watson, Ectopic expression of a Eucalyptus grandis SVP
orthologue alters the flowering time of Arabidopsis thaliana, Funct. Plant
Biol. 31 (2004) 217–224.
[7] R. Bonniem, S. Schwartzman, M. Oppenheimer, et al., Counting the cost
of deforestation, Science, 288 (5472) 1763–1764.
[8] V. Chinnusamy, K. Schumaker, J.K. Zhu, Molecular genetic perspectives
on cross-talk and specificity in abiotic stress signaling in plants, J. Exp.
Bot. 55 (395) (2004) 225–236.
[9] M.M. Chaves, M.M. Oliveira, Mechanisms underlying plant resilience
to water deficits: prospects for water-saving agriculture, J. Exp. Bot. 55
(407) (2004) 2365–2384.
[10] M.M. Chaves, J. Maroco, J. Pereira, Understanding plant responses to
drought—from genes to the whole plant, Funct. Plant Biol. 30 (2003)
239–2647.
[11] X.M. Chen, J. Liu, Y.L. Cheng, et al., HEN1 functions pleiotropically in
Arabidopsis development and acts in C function in the flower, Develop-
ment 129 (2002) 1085–1094.
[12] D. Charlesworth, B. Charlesworth, G.A. McVean, Genome sequences
and evolutionary biology, a two-way interaction, Trends Ecol. Evol. 16
(5) (2001) 235–242.
[13] L.A. Castle, D.L. Siehl, R. Gorton, et al., Discovery and directed evolution
of a glyphosate tolerance gene, Science 304 (5674) (2004) 1151–1154.
[14] R.E. Casu, C.M. Dimmock, S.C. Chapman, et al., Identification of
differentially expressed transcripts from maturing stem of sugarcane
by in silico analysis of stem expressed sequence tags and gene
expression profiling, Plant Mol. Biol. 51 (2004) 1–15 (uncorrected
proof).
[15] A. Costa, A. Carpaneto, S. Varotto, et al., Potassium and carrot embryo-
genesis: are K+ channels necessary for development? Plant Mol. Biol. 51
(2004) 1–16 (uncorrected proof).
43
[16] T. Capell, L. Bassie, P. Christou, Modulation of the polyamine biosyn-
thetic pathway in transgenic rice confers tolerance to drought stress,
PNAS 101 (26) (2004) 9909–9914.
[17] P. Casati, V. Walbot, Rapid transcriptome responses of maiz (Zea mays) to
UV-B irradiated and shielded tissues, Genome Biol. 5 (2004) R16–R28.
[18] Z. Chen, D.R. Gallie, The Ascorbic acid redox state controls guard cell
signaling and stomatal movement, Plant Cell 16 (2004) 1143–1162.
[19] J. Doebley, L. Lukens, Transcriptional regulators and the evolution of
plant form, Plant Cell 10 (1998) 1075–1082.
[20] J.A. De Ronde, R.N. Laurie, T. Caetano, et al., Comparative study between
transgenic and non-transgenic soybean lines proved transgenic lines to be
more drought tolerant, Euphytica 138 (2) (2004) 123–132.
[21] A.M. Dufty Jr., J. Clobert, A.P. Moller, Hormones, developmental plas-
ticity and adaptation, Trends Ecol. Evol. 17 (4) (2002) 190–196.
[22] C. Delessert, T.W. Wilson, D. Van Der Straeten, et al., Spatial and temporal
analysis of the local response to wounding in Arabidopsis leaves, Plant
Mol. Biol. 51 (2004) 1–18 (uncorrected proof).
[23] H.W. Doelle, Biotechnology and human development in developing coun-
tries, EJB Electron. J. Biotechnol. 2 (2002) 1–10.
[24] E.A. Eckardt, H.-T. Cho, R.M. Perrin, Plant biology, Plant Cell 2001 13
(2001) 2165–2173.
[25] Editor’s Choice, The National plant genomics initiative: objectives for
2003–2008, Plant Physiol. 130 (2004) 1741–1744.
[26] European Commission, Plants for the future: a European Vision for
Plant Genomics and Biotechnology Towards 2025, 2004 (see the web
http://site.www.europabio.org/).
[27] K.S. Fischer, J. Barton, G.S. Khush, et al., Collaborations in rice, Science
290 (5490) (2000) 279–280.
[28] O. Fiehn, Metabolomics-the link between genotypes and phenotypes,
Plant Mol. Biol. 48 (2002) 155–171.
[29] R.W. Gesch, I.H. Kang, M. Gallo-Meagher, et al., Rubisco expression
in rice leaves is related to genotypic variation of photosynthesis under
elevated growth CO2 and temperature, Plant, Cell Environ. 26 (12) (2002)
98–107.
[30] C. Glombitza, P.H. Dubuis, O. Thulke, et al., Crosstalk and differential
response to abiotic and biotic stressors reflected at the transcriptional level
of effector genes from secondary metabolism, Plant Mol. Biol. 51 (2004)
1–19 (uncorrected proof).
[31] P.R. Graves, T.A.J. Haystead, Molecular biologist’s guide to proteomics,
Microbiol. Mol. Biol. Rev. 66 (1) (2002) 39–63.
[32] G.P. Hao, Z.Y. Wu, M.S. Chen, et al., ATHK1 gene regulates signal trans-
duction of osmotic stress in Arabidopsis thaliana, J. Plant Physiol. Mol.
Biol. 30 (5) (2004) 553–560.
[33] H.P. Harding, Y.H. Zhang, H.Q. Zeng, et al., An integrated stress response
regulates amino acid metabolism for resistance to oxidative stress, Mol.
Cell 11 (2004) 619–633.
[34] J.A. Hernandez, C. Escobar, G. Creissen, et al., Role of hydrogen peroxide
and the redox state of ascorbate in the induction of antioxidant enzymes in
pea leaves under excess light stress, Funct. Plant Biol. 31 (2004) 359–368.
[35] M. Higuchi, M.S. Pischke, A.P. Mahonen, et al., In planta functions
of the Arabidopsis cytokinin receptor family, PNAS 101 (23) (2004)
8821–8826.
[36] N.G. Halford, M. Paul, Carbon metabolite sensing and signaling, Plant
Biotechnol. J. 1 (2003) 381–398.
[37] M.Y. Hiral, M. Yano, D.B. Goodenowe, et al., Integration of transcrip-
tomics and metabolomics for understanding of global responses to nutri-
tional stresses in Arabidopsis thaliana, PNAS 101 (26) (2004) 1–6.
[38] M.Y. Jiang, J.H. Zhang, Abscisic acid and antioxidant defense in plant
cells, Acta Bot. Sin. 46 (1) (2004) 1–9.
[39] G.C. Kennedy, I.W. Wilson, Plant functional genomics:opportunities in
microarray databases and data mining, Funct. Plant Biol. 31 (2004)
295–314.
[40] T.H. Kim, B.R. Lee, W.J. Jung, et al., De novo protein synthesis in relation
to ammonia and proline accumulation in water stressed white clover,
Funct. Plant Biol. 31 (2004) 847–855.
[41] Y.W. Kwon, D.S. Kim, Herbicide-resistant genetically-modified crop:its
risks with an emphasis on gene flow, Weed Biol. Manage. 1 (1) (2001)
42–49.
44 H.-B. Shao et al. / Colloids and Surfaces B: Biointerfaces 54 (2007) 37–45
[42] M. Kasuga, Q. Liu, S. Miura, et al., Improving plant drought, alt, and
freezing tolerance by gene transfer of a single-inducible transcription
factor, Nat Biotech. 17 (3) (1999) 287–291.
[43] J.A. Kreps, Y.J. Wu, H.S. Chang, et al., Transcriptome changes for Ara-
bidopsis in response to salt, osmotic, and cold stress, Plant Physiol. 130
(2002) 2129–2141.
[44] S.D. Lokhandle, K. Ogawa, A. Tanaka, et al., Effect of temperature on
ascorbate peroxidase activity and flowering of Arabidopsis thaliana eco-
types under different light conditions, J. Plant Physiol. 160 (2003) 57–
64.
[45] Q. Liu, Y. Zhang, S.Y. Chen, Plant protein kinase genes induced by
drought, high salt and cold stresses, Chin. Sci. Bull. 45 (13) (2000)
1153–1157.
[46] M.H. Lu, J.F. Chen, Genetic engineering of plant for cold tolerance, Acta
Bot. Boreal-Occident Sin 24 (10) (2004) 1953–1958 (in Chinese with
English abstract).
[47] X.N. Liu, Baird Wm Vance, Identification of a novel gene, AABRC5, rom
Helianthus annuu (Asteraceae) that is upregulated in response to drought,
salinity, and abscisic acid, Am. J. Bot. 91 (2004) 184–191.
[48] Y.S. Liu, S. Roof, Z.B. Ye, et al., Manipulation of light signal transduction
as a means of modifying fruit nutritional quality in tomato, PNAS 101
(26) (2004) 9897–9902.
[49] E.M. Meyerowitz, Plants compared to animals: the broadest comparative
study of development, Science 295 (5559) (2002) 1482–1485.
[50] X. Manival, L. Ghisolfi-Nieto, G. Joseph, et al., RNA-binding strategies
common to cold-shock domain-and RNA recognition motif-containing
proteins, Nucl. Acids Res. 29 (11) (2001) 2223–2233.
[51] M.F. Mette, J. van der Winden, M. Matzke, et al., Short RNAs can iden-
tify new candidate transposable element families in Arabidopsis, Plant
Physiol. 130 (2002) 6–9.
[52] M. Miyao, Molecular evolution and genetic engineering of C4 photosyn-
thetic enzymes, J. Exp. Bot. 54 (381) (2003) 179–189.
[53] S. Munne-Bosch, L. Alegre, Die and let live: leaf senescence contributes
to plant survival under drought stress, Funct. Plant Biol. 31 (2004) 203–
216.
[54] L.O. Medict, R.A. Azevedo, R.J. Smith, et al., The influence of nitrogen
supply on antioxidant enzymes in plant roots, Funct. Plant Biol. 31 (2004)
1–9.
[55] J.F. Ma, Role of silicon in enhancing the resistance of plants to biotic and
abiotic stresses, Soil Sci. Plant Nutr. 50 (1) (2004) 11–18.
[56] R. Munns, Comparative physiology of salt and water stress, Plant, Cell
Environ. 25 (2) (2003) 239–256.
[57] C. Mlot, Plant biology in the genome era, Science 281 (5375) (1998)
331–332.
[58] G. Noctor, L. Gomez, H. Vanacker, et al., Interactions between biosynthe-
sis, compartmentation and transport in the control of glutathione home-
ostasis and signaling, J. Exp. Bot. 53 (372) (2002) 1283–1304.
[59] P. Neumann, Salinity resistance and plant growth revisited, Plant, Cell
Environ. 20 (1997) 1193–1198.
[60] R.S. Poethig, Life with 25,000 genes, Genome Res. 11 (3) (2001)
313–316.
[61] A. Pellegrineschi, J.M. Ribaut, R. Trethowan, Progress in the genetic engi-
neering of wheat for water-limited conditions, JIRCAS Working Report,
2002, pp. 55-60.
[62] T. Puhakainen, M.W. Hess, P. Makela, et al., Overexpression of multiple
dehydrin genes enhances tolerance to freezing stress in Arabidopsis, Plant
Mol. Biol. 51 (2004) 1–11 (uncorrected proof).
[63] A.L. Rae, J.M. Jarmey, S.R. Mudge, et al., Over-expression of a high-
affinity phosphate transporter in transgenic barley plants does not enhance
phosphate uptake rates, Funct. Plant Biol. 31 (2004) 141–148.
[64] A.A. Rosenberg, M.J. Fogarty, M.P. Sissenwine, et al., Achieving sus-
tainable use of renewable resources, Science 262 (1993) 828–829.
[65] J.L. Riechmann, J. Heard, G. Martin, et al., Arabidopsis transcription
factors: genome-wide comparative analysis among eukaryotes, Science
290 (5499) (2000) 2105–2110.
[66] S. Shigeoka, T. Ishikawa, M. Tamoi, et al., Regulation and function
of ascorbate peroxidase isoenzymes, J. Exp. Bot. 53 (372) (2002)
1305–1319.
[67] K. Samis, S. Bowley, B. McKersie, Pyramiding Mn-superoxide dismutase
transgenes to improve persistence and biomass production in alfalfa, J.
Exp. Bot. 53 (372) (2002) 1343–1350.
[68] D.E. Soltis, P.S. Soltis, The role of phylogenetics in comparative genetics,
Plant Physiol. 132 (2003) 1790–1800.
[69] C.D. Schlighting, Phenotypic plasticity in plants, Plant Spec. Biol. 17
(2002) 85–88.
[70] K. Shinozaki, K. Yamaguchi-Shinozaki, M. Seki, Regulatory network of
gene expression in the drought and cold stress responses, Curr. Opin.
Plant Biol. 6 (5) (2003) 410–4178.
[71] K. Shinozaki, E.S. Dennis, Cell signaling and gene regulation global
analyses of signal transduction and gene expression profiles, Curr. Opin.
Plant Biol. 6 (5) (2003) 405–409.
[72] C. Somerville, J. Dangl, Plant Biology in 2010, Science 290 (4599) (2000)
2077–2078.
[73] H.B. Shao, Z.S. Liang, M.A. Shao, et al., Impacts of PEG-6000 pretreat-
ment for barley (Hordeum vulgare L.) seeds on the effect of their mature
embryo in vitro culture and primary investigation on its physiological
mechanism, Biointerfaces 41 (1) (2005) 7–13.
[74] H.B. Shao, Z.S. Liang, M.A. Shao, LEA protein: structure, functions and
gene expression, Biointerfaces 45 (3/4) (2005) 131–135.
[75] H.B. Shao, Z.S. Liang, M.A. Shao, Roles of ABA signal transduction
during higher plant seed maturation and germination, Forest. Stud. China
5 (4) (2003) 42–51.
[76] H.B. Shao, Z.S. Liang, M.A. Shao, et al., Changes of some physiological
and biochemical indices for soil water deficits among 10 wheat genotypes
at seedling stage, Biointerfaces 41 (2) (2005) 107–113.
[77] H.B. Shao, Z.S. Liang, M.A. Shao, Changes of some anti-oxidative phys-
iological indices under soil water deficits among 10 wheat genotypes at
tillering stage, J. Sci. Food Agric. 86, in press.
[78] J.E. Taylor, M.R. McAinsh, Signaling crosstalk in plants: emerging issues,
J. Exp. Bot. 55 (395) (2004) 147–149.
[79] E. Vranova, D. Inze, Breusegem Frank Van, Signal transduction during
oxidative stress, J. Exp. Bot. 53 (3720) (2002) 1227–1236.
[80] H. Wang, Z.J. Huang, Q. Chen, et al., Ectopic overexpression of tomato
JERF3 in tobacco activates downstream gene expression and enhances
salt tolerance, Plant Mol. Biol. 51 (2004) 1–10 (uncorrected proof).
[81] W.X. Wang, B. Vinocur, A. Altman, Plant responses to drought, salinity
and extreme temperatures: towards genetic engineering for stress toler-
ance, Planta 218 (2003) 1–14.
[82] G.H. Wei, D.P. Liu, C.C. Liang, Charting gene regulatory networks: strate-
gies, challenges and perspectives, Biochem. J. 381 (2004) 1–12.
[83] S. Winichayakul, R.L. Moyle, D.J. Ryan, et al., Distinct cis-elements
in the Asparagus officinalis asparagines synthetase promoter respond to
carbohydrate and senescence signals, Funct. Plant Biol. 31 (2004) 573–
582.
[84] W.D. Yong, Y.Y. Xu, W.Z. Xu, et al., Vernalization-induced flowering in
wheat is mediated by a lectin-like gene VER2, Planta 217 (2003) 261–270.
[85] J.K. Zhu, Salt and drought stress signal transduction in plants, Annu. Rev.
Plant Biol. 53 (2002) 247–273.
[86] J.H. Zhu, H.Z. Shi, B.H. Lee, et al., An Arabidopsis homeodomain
transcription factor gene, OS9, mediates cold tolerance through a CBF-
independent pathway, PNAS 101 (26) (2004) 9873–9878.
[87] T. Zhu, Global analysis of gene expression using GeneChip microarrays,
Curr. Opin. Plant Biol. 6 (5) (2003) 418–425.
[88] J.K. Zhu, Regulation of ion homeostasis under salt stress, Curr. Opin.
Plant Biol. 6 (5) (2003) 441–445.
[89] J.C. Yang, J.H. Zhang, Grain filling of cereals under soil drying, New
Phytol. 169 (2006) 223–236.
[90] H.S. Liu, F.M. Li, Photosynthesis, root respiration, and grain yield of
spring wheat in response to surface soil drying, Plant Growth Regul. 45
(2005) 149–154.
[91] D.B. Andrew, M. Uribelarrea, A. Elizabeth, et al., Photosynthesis, pro-
ductivity and yield of maize are not affected by open-air elevation of
CO2 concentration in the absence of drought, Plant Physiol. 140 (2006)
779–790.
[92] M.W. Humphreys, R.S. Yadav, A.J. Cairns, et al., A change climate for
grassland research, New Phytol. 169 (2006) 9–26.
 H.-B. Shao et al. / Colloids and Surfaces B: Biointerfaces 54 (2007) 37–45
[93] H. Philippe, R.G. George, J.G. Peter, et al., Rhizosphere geometry and het-
erogeneity arising from root-mediated physical and chemical processes,
New Phytol. 168 (2005) 293–303.
[94] H. Angela, The plastic plant: root responses to heterogeneous supplies of
nutrients, New Phytol. 162 (2004) 9–24.
[95] R. Munns, Genes and salt tolerance:bringing them together, New Phytol.
167 (2005) 645–663.
[96] E. De la Barrera, J.L. Andrade, Challenges to plant megadiversity:how
environmental physiology can help, New Phytol. 167 (2005) 5–8.
[97] L.J. David, H. Angela, K. Yahov, Plant and mycorrhizal regulation of
rhizodeposition, New Phytol. 163 (2004) 459–480.
[98] T. Mark, B. Antony, Abiotic stress tolerance in grasses. From model plants
to crop plants, Plant Physiol. 137 (2005) 791–793.
[99] G.F. Brian, F.H. Jeff, L. Kochian, Focus on plant nutrition, Plant Physiol.
136 (2004) 2437.
[100] S.W. Travis, P.B. Harsh, G. Erich, et al., Root exudation and rhizosphere
biology, Plant Physiol. 132 (2003) 44–51.
[101] M. Gregory, G. Pascal, J.A. Christian, et al., Transcription factor net-
works. Pathways to the knowledge of root development, Plant Physiol.
136 (2004) 3478–3485.
[102] J.C. Yang, E.H. Chang, W.J. Zhang, et al., Relationship between chemical
signals of root system and rice quality, Agric. Sci. China 39 (1) (2006)
38–47 (in Chinese with English abstract).
[103] X.A. Liu, D.R. Bush, Expression and transcriptional regulation of amino
acid transporters in plants, Amino Acids (1) (2006) 1–8.
[104] H.B. Shao, Z.S. Liang, M.A. Shao, Molecular mechanisms of higher plant
adaptation to environment, Acta Ecol. Sin 25 (7) (2005) 1772–1781.
[105] H.B. Shao, Z.S. Liang, M.A. Shao, Dynamic change of anti-oxidative
enzymes for 10 wheat genotypes at soil water deficits through their life
circle, Biointerfaces 42 (3–4) (2005) 187–195.
[106] H.B. Shao, M.A. Shao, Z.S. Liang, Change of protective enzymes and
MDA for 10 wheat genotypes at soil water deficits at maturation stage,
Biointerfaces 45 (1) (2005) 7–13.
[107] H.B. Shao, Z.S. Liang, M.A. Shao, S.M. Sun, Z.M. Hu, Investigation on
dynamic changes of photosynthetic characteristics of 10 wheat (Triticum
aestivum L.) genotypes during two vegetative-growth stages at water
deficits, Biointerfaces 43 (3–4) (2005) 221–227.
[108] H.B. Shao, M.A. Shao, Z.S. Liang, Osmotic adjustment comparison of
10 wheat (Triticum aestivum L.) genotypes at soil water deficits, Bioint-
erfaces 47 (2) (2006) 132–139.
[109] Y. Tan, Z.S. Liang, H.B. Shao, Effect of water deficits on the activity of
anti-oxidative enzymes and osmoregulation among 3 different genotypes
of Radix Astragali at seeding stage, Biointerfaces 49 (1) (2006) 60–65.
[110] L.Y. Chu, H.B. Shao, M.Y. Li, Molecular biological mechanisms of pho-
tochrome signal transduction, Biointerfaces 45 (3/4) (2005) 154–161.
[111] G.R. Sun, Y.Z. Peng, H.B. Shao, L.Y. Chu, Does Puccinelia tenuiflora
have the ability of salt exudation? Biointerfaces 45 (5) (2005) 207–213.
[112] H.B. Shao, Z.S. Liang, M.A. Shao, New considerations for improving
eco-environment: take advantage of information timely and efficiently
from molecular biology and biotechnology, J Chongqing Uni Posts &
Teleco (Nat. Sci. Ed.) 16 (4) (2004) 95–99.
45
[113] H.B. Shao, L.Y. Chu, Plant molecular biology in China: opportunities and
challenges, Plant Mol. Biol. Rep. 23 (4) (2005) 345–358.
[114] H.B. Shao, L.Y. Chu, M.A. Shao, Some advances in plant stress physi-
ology and their implications in the systems biology era, Biointerfaces 52
(1), in press.
[115] H.B. Shao, L.Y. Chu, M.A. Shao, X.A. Liu, Response to Mittler Ron:
the greatest challenge for plant physiologists and molecular biologists:
feeding the increasing world population under global climate change and
multi-stress environment, Trends in Plant Science 11 (6), in press.
[116] F.A. Bazzaz, Plant biology in the future, PNAS 98 (10) (2001) 5441–5445.
[117] W. Tang, L. Harris, R.J. Newton, Molecular mechanism of salinity stress
and biotechnological strategies for engineering salt tolerance in plants,
Forest. Stud. China 5 (2) (2003) 52–62.
[118] B. Arnholdt-Schmitt, Stress-induced cell reprogramming. A role for
global genome regulation? Plant Physiol. 136 (2004) 2579–2586.
[119] C. Johson, E. Boden, M. Desal, et al., In vivo target promoter-binding
activities of a xenobiotic stress-activated TGA factor, Plant J. 28 (2001)
237–243.
[120] J.M. Zhou, Y. Trifa, H. Silva, et al., NPR1 differentially interacts with
members of the TGA/OBF family of transcription factors that bind an
element of PR-1 gene required for induction by salicylic acid, Mol. Plant-
Microb. Interact. 13 (2000) 191–202.
[121] S.L. Harmer, J.B. Hogenesch, M. Straume, et al., Orchestrated transcrip-
tion of key pathways in Arabidopsis by the circadian clock, Science 290
(2000) 2110–2113.
[122] V. Chinnusamy, K. Schumaker, J.K. Zhu, Molecular gegetic perspectives
on cross-talk and specificity in abiotic stress signaling in plants, J. Exp.
Bot. 55 (2004) 225–236.
[123] A.K. Grennan, Abiotic stress in rice. An “omic” approach, Plant Physiol.
140 (2006) 1139–1141.
[124] M. Ashraf, M.R. Foolad, Roles of glycine betaine and praline in improving
plant abiotic stress, Environ. Exp. Bot. 55, in press.
[125] A. Soltani, M. Gholipoor, E. Zeinali, Seed reserve utilization and seedling
growth of wheat as affected by drought and salinity, Environ. Exp. Bot.
55 (2006) 195–200.
[126] Z.V. Avramova, Heterochromatin in animals and plants. Similarities and
differences, Plant Physiol. 129 (2002) 40–49.
[127] D.E. Salt, Update on plant ionomics, Plant Physiol. 136 (2004)
2451–2456.
[128] A.H. Millar, V. Mittova, G. Kiddle, et al., Control of ascorbate synthesis
by respiration and its implications for stress responses, Plant Physiol. 133
(2003) 443–447.
[129] J. Leon, E. Rojo, J.J. Sanchez-Serrano, Wound signaling in plants, J. Exp.
Bot. 52 (2001) 1–9.
[130] J.B. Rossel, I.W. Wilson, B.J. Pogson, Global changes in gene expres-
sion in response to high light in Arabidopsis, Plant Physiol. 130 (2002)
1109–1120.
[131] A. Trewavas, Plant cell signal transduction: the emerging phenotye, Plant
Cell, S3–S4.
[132] S.G. Moller, P.J. Ingles, G.C. Whiteham, The cell biology of phytochrome
signalling, New Phytol. 154 (2002) 553–590.