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Plant Physiol, January 2001, Vol. 125, pp. 89-93
So What's New in the Field of Plant Cold Acclimation?
Lots!
Michael F.
Thomashow*
Department of Crop and Soil Sciences, Michigan State University,
East Lansing, Michigan 48824-1325
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INTRODUCTION |
Due to its intrinsically interesting
nature and importance to agriculture, considerable effort has been
directed at understanding the phenomenon of "cold acclimation," the
process whereby certain plants increase in freezing tolerance upon
exposure to low temperature. By 1980, thousands of research articles
had been published on the topic and significant insights had been
gained, including the following: Freezing tolerance is a multigenic
trait, freezing injury in most plants and tissues results largely from
the severe cellular dehydration that occurs upon ice formation, and the
cellular membrane systems are a primary site of freeze-induced injury. What was lacking, however, was a consensus regarding the mechanistic basis of freezing tolerance. Moreover, specific genes with functional roles in freezing tolerance had not been identified and their modes of
action had not been determined, critical deficiencies in regard to both
a basic understanding of cold acclimation and practical efforts to
improve the stress tolerance of agronomic plants.
Now, 20 years later, the cold acclimation research landscape has
dramatically changed. Largely through bringing molecular genetic
and mutational approaches to bear on the topic, along with the
development of Arabidopsis as a model to study the phenomenon, genes
with roles in cold acclimation have begun to be identified and their
modes of action determined. In addition, low-temperature signaling and
regulatory pathways involved in activating the cold acclimation
response have begun to be described and the insights gained are
beginning to suggest novel approaches to improve the environmental
stress tolerance of plants. My objective here is to highlight some of
these exciting advances.
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THE CBF/DREB1 TRANSCRIPTIONAL ACTIVATORS: REGULATORS OF COLD
ACCLIMATION |
In 1985, Guy et al. (4) established that changes in gene
expression occur with cold acclimation and so opened a floodgate of
effort by investigators to identify and characterize cold-responsive genes (22). The underlying hypothesis was that some of these genes were
likely to be involved in freezing tolerance and that studies of their
regulation and function would provide new insights into the cold
acclimation process. Studies on cold-regulated gene expression in
Arabidopsis have resulted in the discovery of a family of
transcriptional activators, the CBF/DREB1 proteins, that have a key
role in cold acclimation.
The CBF/DREB1 Proteins Regulate Expression of Freezing Tolerance
Genes
Initial studies on cold-regulated gene expression established that
the promoters of certain cold-responsive genes are activated in
response to low temperature and dehydration stress (22). Further analysis in Arabidopsis led to the identification of a DNA regulatory element, the C-repeat (CRT) dehydration responsive element
(DRE), which has a conserved core sequence of CCGAC, that imparts
responsiveness to low temperature and dehydration (24).
Transcriptional activators that bind to the CRT/DRE, designated either
CBF1, CBF2, and CBF3 (3, 20) or DREB1b, DREB1c, and DREB1a (14),
respectively, were subsequently identified. The proteins, which contain
the AP2/EREBP-DNA-binding domain, have nearly identical amino acid
sequences and are encoded by genes located on chromosome 4 in tandem
array (3, 14, 18, 20). Constitutive overexpression of the
CBF1/DREB1b (6) or CBF3/DREB1a (9, 14) genes
in transgenic Arabidopsis plants induces the expression of
multiple cold-responsive CRT/DRE-containing genes without a low-temperature stimulus (Fig. 1).
Moreover, nonacclimated transgenic plants overexpressing either
CBF1/DREB1b (6) or CBF3/DREB1a (9, 14) are
more freezing tolerant than nonacclimated control plants. Thus, it has
been concluded that the "CBF regulon" (CRT/DRE-containing genes
that are induced by the CBF/DREB1 transcription factors) includes genes
with roles in cold acclimation.
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Figure 1.
Model of the Arabidopsis CBF cold acclimation
pathway. Low temperature leads to rapid induction of the
CBF/DREB1 genes that in turn results in expression of the
CBF regulon of CRT/DRE-regulated genes. Action of the CBF regulon,
which includes COR, ERD, and presumably yet to be
discovered ("XYZ") cold-regulated genes,
results in an increase in plant freezing tolerance. Cold-induced
expression of the CBF/DREB1 genes has been proposed (3) to
involve the action of a regulatory protein present at warm temperature
designated ICE (inducer of CBF expression). Low temperature is
envisioned to either activate the ICE protein or other protein(s) with
which it interacts (3). Such activation may involve alterations in
protein phosphorylation caused by a cold-induced influx of calcium (see
text). The SFR6 protein appears to act between CBF/DREB1
transcription and induction of the CRT/DRE-regulated genes (11) whereas
HOS1 appears to act upstream of CBF transcription (13).
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Given that the CBF/DREB1 proteins can induce transcription of
cold-regulated CRT/DRE-containing target genes without a
low-temperature stimulus, why aren't the CRT/DRE-regulated genes
normally expressed at warm temperatures? The simple answer is that the
CBF/DREB1 genes themselves are cold regulated (3, 14).
Within 15 min of transfer to low temperature, CBF/DREB1 transcripts
begin to accumulate, followed at 1 to 2 h by accumulation of
transcripts for the target CRT/DRE-regulated genes. The mechanism
whereby the CBF/DREB1 genes are activated by low temperature
is not yet known, but appears to involve the action of cold-responsive
promoters (18) that are not subject to autoregulation (3). Thus,
Gilmour et al. (3) have hypothesized the existence of a transcription
factor, designated ICE, that acts at the CBF/DREB1 promoters (Fig. 1).
As envisioned, the protein would be present at normal growth
temperature, but be in an inactive state. Upon exposing plants to low
temperature, ICE (or a protein that it interacts with) is proposed to
become activated and stimulate transcription of the
CBF/DREB1 genes followed by induction of the CBF regulon
(Fig. 1).
Role of the CBF Regulon in Dehydration Stress Tolerance
As temperatures drop below freezing, ice formation is generally
initiated in the extracellular spaces of plants and, because the
chemical potential of ice is less than that of liquid water, there is
movement of unfrozen water from inside the cell to the extracellular spaces where it freezes. This process
continues until an equilibrium in chemical potential is achieved.
If the freezing temperature is  10°C, the unfrozen liquid will have
an osmolarity of about 5 and typically greater than 90% of the
osmotically active water will have moved out of the cell. It is clear,
then, that freezing tolerance must include tolerance to severe
dehydration stress. Given this, it is not unreasonable to think that
the mechanisms of freezing and drought tolerance might include the
action of common genes. Shinozaki and Yamaguchi-Shinozaki and coworkers (9, 14) have shown that Arabidopsis plants overexpressing
CBF3/DREB1a, and consequently the CBF regulon, are not only
more freezing tolerant than control plants, but are also more tolerant
of dehydration stress caused by either drought or high salinity. Thus,
the "biological rationale" for why the CRT/DRE imparts
responsiveness to both low temperature and dehydration stress is
obvious. However, the genes encoding the CBF/DREB1 activators are not
responsive to dehydration stress (14). So what accounts for the
dehydration responsiveness of CRT/DRE regulatory element? The Shinozaki
labs have provided an explanation for this apparent "paradox" (14). They have identified a gene, DREB2a, that encodes an
AP2/EREBP domain protein that binds to the CRT/DRE and is induced in
response to drought and high salinity.
Functions of the CBF Regulon
The results summarized above indicate that a fundamental function
of the CBF regulon is to protect cells against freezing and other
stresses involving dehydration. How does the CBF regulon accomplish
this? At present, our knowledge in this area is scant as only six
CRT/DRE-controlled genes have been identified (KIN1, COR6.6/KIN2, COR15a, COR47/RD17,
COR78/RD29a, and ERD10; 6, 9) and direct evidence
for the mode of action of only one, COR15a, is available (1, 19). Overexpression of COR15a, which encodes a
polypeptide that is targeted to the stromal compartment of the chloroplasts, increases the freezing tolerance of chloroplasts in
nonacclimated Arabidopsis plants by 1°C to 2°C (1). This effect appears to result from the mature COR15a-encoded
polypeptide, COR15am, decreasing the propensity of membranes to form
deleterious hexagonal II phase lipids upon freeze-induced dehydration
(19). Whether other CRT/DRE-controlled genes encode proteins
that participate in stabilizing membranes remains to be determined. The
function of the CBF regulon, however, does not appear to be
"limited" to the action of membrane-stabilizing proteins.
Arabidopsis plants overexpressing CBF3 not only have
elevated levels of COR proteins, but also have elevated levels of Pro
and total sugars (2). Increased levels of Pro and sugars occur with
cold acclimation in a wide variety of plants and are thought to
contribute to the enhancement of freezing tolerance, in part, through
stabilizing membranes. Thus, the CBF/DREB1 regulatory proteins appear
to be "master switches" that integrate activation of multiple
components of the cold acclimation response.
Use of CBF/DREB1 Genes to Improve Environmental Stress
Tolerance
A major challenge in coming years will be keeping food production
in pace with increasing world population. Developing crops with
increased environmental stress tolerance will greatly help in this
regard as abiotic stresses limit the geographical locations where crops
can be grown and cause significant losses in plant productivity on an
annual basis. The results described above suggest the possibility of
using the Arabidopsis CBF/DREB1 genes, or homologs from
other plants, to optimize expression of CBF regulons in agronomic crops
and thereby enhance freezing, drought, and salt tolerance. There is
preliminary evidence that overexpression of the Arabidopsis CBF genes in canola (Brassica napus) results in
expression of target CRT/DRE-regulated genes and increases freezing
tolerance in both nonacclimated and cold-acclimated plants (7). Whether the "CBF cold acclimation pathway" is operative in more distantly related plants remains to be determined. In addition, the best strategy
to optimize CBF/DREB1 expression is not yet certain. Placing
the CBF/DREB1 genes under control of a strong constitutive promoter may not be the best approach as overexpression of
CBF3/DREB1a in Arabidopsis using the cauliflower mosaic
virus 35S promoter can cause a severely stunted phenotype
(2, 14). Using stress-inducible (9) or other conditional promoters may
be a better approach to improve stress tolerance without causing
negative agronomic effects.
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THE SFR AND ESKIMO1 FREEZING TOLERANCE
GENES |
Warren and colleagues (15) have used chemical mutagenesis to
identify seven Arabidopsis genes, designated SFR
(sensitivity to freezing), that affect cold acclimation. Mutant alleles
of five of these genes (sfr1, 2, 4,
5-1, 5-2, and 6) have no
obvious adverse effects on the ability of plants to cope with low
nonfreezing temperatures, but decrease the level of freezing tolerance
that plants attain with cold acclimation. The identities of the
SFR genes are not known. However, SFR6 has a role
in regulating expression of the CBF regulon (11). To be
specific, transcripts for multiple CRT/DRE-regulated genes do
not accumulate to normal levels during cold acclimation in
sfr6 plants. This finding offers a simple explanation for
why sfr6 plants are defective in cold acclimation. However,
the reason why accumulation of transcripts for CRT/DRE-regulated genes
is impaired in sfr6 plants is not known. It is significant that it does not result from a defect in cold responsiveness of the CBF genes because transcripts for CBF1,
2, and 3 accumulate normally in the
sfr6 mutant in response to low temperature (11). Thus, the
SFR6 protein appears to act somewhere between CBF transcription and
induction of the CBF regulon (Fig. 1).
Xin and Browse (23) have used chemical mutagenesis to isolate
cold acclimation "constitutive" mutants. One mutation,
eskimo1 (esk1), results in increased freezing
tolerance in both nonacclimated and cold-acclimated plants.
Nonacclimated esk1 mutant plants have a 30-fold higher level
of Pro than nonacclimated wild-type plants; a 2-fold higher level of
total soluble sugars; and a 3-fold higher level of transcripts for
RAB18, a cold-responsive gene encoding a dehydrin protein.
It is presumed that the increases in Pro and sugars, and potentially
the RAB18 protein, contribute to the enhancement of freezing tolerance.
It is significant that the esk1 mutation does not affect
expression of four CRT/DRE-regulated cold-responsive genes tested.
Thus, Xin and Browse (23) proposed that there are parallel or
branched signaling pathways that activate "distinct suites" of cold
acclimation responses and that activation of one pathway can bring
about considerable freezing tolerance without support from other
components. Because esk1 plants do not overexpress CRT/DRE-regulated cold-responsive genes, they proposed that
esk1 defines a cold acclimation signaling pathway that is
distinct from the CBF cold acclimation pathway. The mechanism of
ESK1 action is not known, but the fact that the two
available esk1 alleles are recessive suggests that
ESK1 may act as a negative regulator of cold acclimation.
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COLD ACCLIMATION SIGNAL TRANSDUCTION |
There is mounting evidence that calcium is an important second
messenger involved in activating the cold acclimation response. In both
Arabidopsis (10) and alfalfa (Medicago sativa; 16),
cytoplasmic calcium levels increase rapidly in response to low
temperature due in part to an influx of calcium from extracellular
stores. This increase in calcium is required for plants to fully cold acclimate and for maximal cold induction of at least some
CRT/DRE-regulated genes (10, 21). Little is known about the steps
between calcium influx and the activation of gene expression, but it
appears that protein phosphorylation may be involved (17); transcript
levels of the alfalfa cold-responsive cas15 gene increase at
normal growth temperatures in plants treated with the protein
phosphatase inhibitor okadaic acid and do not accumulate to normal
levels upon low-temperature treatment in plants treated with the
protein kinase inhibitor staurosporine. Moreover, low temperature
causes a rapid and dramatic decrease in protein phosphatase 2A activity
that is dependent on calcium influx (17). Thus, low temperature may
lead to an influx in calcium that inhibits phosphatase 2A activity
that, in turn, leads to the phosphorylation of one or more proteins
involved in inducing genes involved in cold acclimation. The protein
kinase(s) responsible for inducing cold-regulated genes and activating
freezing tolerance mechanisms is not known, but there are
interesting candidates (22) including an alfalfa mitogen-activated
protein kinase, designated p44mmk4, that becomes
activated within 10 min of alfalfa plants being exposed to low
temperature (8).
Zhu and colleagues (5, 12) have identified two genes, HOS1
and HOS2 (high expression of osmotically responsive
genes), that appear to encode negative regulators of low-temperature
signal transduction. Mutations in these genes result in
"superinduction" of COR78/RD29a and certain other
CRT/DRE-regulated genes in response to low temperature. The
HOS1 gene has recently been identified by positional cloning
and shown to encode a protein with a RING-finger motif (13). The
precise function of HOS1 is not known, but transcription of the
CBF/DREB1 genes was found to be superinduced in
hos-1 plants. Thus, Zhu and colleagues (13) have proposed
that HOS1 is a negative regulator that functions upstream of
CBF/DREB1 transcription (Fig. 1).
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CONCLUDING REMARKS |
Cold acclimation research, in my view, has entered a "golden
age." Tremendous advances have been made in our understanding of cold acclimation in the past two decades and there is every reason
to believe that the next 20 years will bring even more spectacular and
meaningful insights. Through a blending of classical genetics and
biochemistry with the powerful new approaches of proteomics and
structural, functional, and comparative genomics, I think it is likely
that a core set of "first principles" will soon emerge that will
allow for the rational design of plants with increased environmental
stress tolerance. Such knowledge will not only be exciting and a
profound scientific achievement, but will greatly aid efforts in
agriculture to continue providing food to feed the world.
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ACKNOWLEDGMENTS |
I thank Suzanne Thomashow, Eric Stockinger, and members of
my laboratory for comments on how to improve this
manuscript. Our research was supported by grants from the U.S.
Department of Agriculture (to M.F.T.), the National Science Foundation,
Mendel Biotechnology, Inc., and the Michigan Agricultural Experiment Station.
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FOOTNOTES |
*
E-mail thomash6{at}pilot.msu.edu; fax 517-353-5174.
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LITERATURE CITED |
-
Artus NN, Uemura M, Steponkus PL, Gilmour SJ, Lin CT, Thomashow MF
(1996)
Proc Natl Acad Sci USA
93: 13404-13409
[Abstract/Free Full Text]
-
Gilmour SJ, Sebolt AM, Salazar MP, Everard JD, Thomashow MF
(2000)
Plant Physiol
124: 1854-1865
[Abstract/Free Full Text]
-
Gilmour SJ, Zarka DG, Stockinger EJ, Salazar MP, Houghton JM, Thomashow MF
(1998)
Plant J
16: 433-442
[CrossRef][Web of Science][Medline]
-
Guy CL, Niemi KJ, Brambl R
(1985)
Proc Natl Acad Sci USA
82: 3673-3677
[Abstract/Free Full Text]
-
Ishitani M, Xiong L, Lee H, Stevenson B, Zhu J-K
(1998)
Plant Cell
10: 1151-1161
[Abstract/Free Full Text]
-
Jaglo-Ottosen KR, Gilmour SJ, Zarka DG, Schabenberger O, Thomashow MF
(1998)
Science
280: 104-106
[Abstract/Free Full Text]
-
Jaglo-Ottosen KR, Kleff S, Salazar MP, Thomashow MF
(2000) (Abs # 452;
http://ww.rycomusa.com/aspp2000/public/P33/0652.html), ASPP Annual
Meeting, Plant Biology 2000, 15-19 July, 2000, San Diego,
CA
-
Jonak C, Kiegerl S, Ligterink W, Barker PJ, Huskisson NS, Hirt H
(1996)
Proc Natl Acad Sci USA
93: 11274-11279
[Abstract/Free Full Text]
-
Kasuga M, Liu Q, Miura S, Yamaguchi-Shinozaki K, Shinozaki K
(1999)
Nat Biotechnol
17: 287-291
[CrossRef][Web of Science][Medline]
-
Knight H, Trewavas AJ, Knight MR
(1996)
Plant Cell
8: 489-503
[Abstract]
-
Knight H, Veale EL, Warren GJ, Knight MR
(1999)
Plant Cell
11: 875-886
[Abstract/Free Full Text]
-
Lee H, Xiong L, Ishitani M, Stevenson B, Zhu J-K
(1999)
Plant J
17: 301-308
[CrossRef][Web of Science][Medline]
-
Lee H, Xiong L, Ishitani M, Stevenson B, Zhu J-K
(2000)
(abstract no. 107). 11th International Conference on Arabidopsis Research, http://www.wisc.edu/union/info/conf/arabidopsis/Arab_abs.pdf, pp 54
-
Liu Q, Kasuga M, Sakuma Y, Abe H, Miura S, Yamaguchi-Shinozaki K, Shinozaki K
(1998)
Plant Cell
10: 1391-1406
[Abstract/Free Full Text]
-
McKown R, Kuroki G, Warren G
(1996)
J Exp Bot
47: 1919-1925
-
Monroy AF, Dhindsa RS
(1995)
Plant Cell
7: 321-331
[Abstract]
-
Monroy AF, Sangwan V, Dhindsa RS
(1998)
Plant J
13: 653-660
[CrossRef][Web of Science]
-
Shinwari ZK, Nakashima K, Miura S, Kasuga M, Seki M, Yamaguchi-Shinozaki K, Shinozaki K
(1998)
Biochem Biophys Res Commun
250: 161-170
[CrossRef][Web of Science][Medline]
-
Steponkus PL, Uemura M, Joseph RA, Gilmour SJ, Thomashow MF
(1998)
Proc Natl Acad Sci USA
95: 14570-14575
[Abstract/Free Full Text]
-
Stockinger EJ, Gilmour SJ, Thomashow MF
(1997)
Proc Natl Acad Sci USA
94: 1035-1040
[Abstract/Free Full Text]
-
Tähtiharju S, Sangwan V, Monroy AF, Dhindsa RS, Borg M
(1997)
Planta
203: 442-447
[CrossRef][Web of Science][Medline]
-
Thomashow MF
(1999)
Annu Rev Plant Physiol Plant Mol Biol
50: 571-599
[CrossRef][Web of Science]
-
Xin Z, Browse J
(1998)
Proc Natl Acad Sci USA
95: 7799-7804
[Abstract/Free Full Text]
-
Yamaguchi-Shinozaki K, Shinozaki K
(1994)
Plant Cell
6: 251-264
[Abstract]
© 2001 American Society of Plant Physiologists
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[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
I. M. Scott, S. M. Clarke, J. E. Wood, and L. A.J. Mur
Salicylate Accumulation Inhibits Growth at Chilling Temperature in Arabidopsis
Plant Physiology,
June 1, 2004;
135(2):
1040 - 1049.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
F. Novillo, J. M. Alonso, J. R. Ecker, and J. Salinas
CBF2/DREB1C is a negative regulator of CBF1/DREB1B and CBF3/DREB1A expression and plays a central role in stress tolerance in Arabidopsis
PNAS,
March 16, 2004;
101(11):
3985 - 3990.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
H. Shou, P. Bordallo, J.-B. Fan, J. M. Yeakley, M. Bibikova, J. Sheen, and K. Wang
From The Cover: Expression of an active tobacco mitogen-activated protein kinase kinase kinase enhances freezing tolerance in transgenic maize
PNAS,
March 2, 2004;
101(9):
3298 - 3303.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
F. T.S. Nogueira, V. E. De Rosa Jr., M. Menossi, E. C. Ulian, and P. Arruda
RNA Expression Profiles and Data Mining of Sugarcane Response to Low Temperature
Plant Physiology,
August 1, 2003;
132(4):
1811 - 1824.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
A. Abdrakhamanova, Q. Y. Wang, L. Khokhlova, and P. Nick
Is Microtubule Disassembly a Trigger for Cold Acclimation?
Plant Cell Physiol.,
July 15, 2003;
44(7):
676 - 686.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
N. J. Provart, P. Gil, W. Chen, B. Han, H.-S. Chang, X. Wang, and T. Zhu
Gene Expression Phenotypes of Arabidopsis Associated with Sensitivity to Low Temperatures
Plant Physiology,
June 1, 2003;
132(2):
893 - 906.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
B. Downie, S. Gurusinghe, P. Dahal, R. R. Thacker, J. C. Snyder, H. Nonogaki, K. Yim, K. Fukanaga, V. Alvarado, and K. J. Bradford
Expression of a GALACTINOL SYNTHASE Gene in Tomato Seeds Is Up-Regulated before Maturation Desiccation and Again after Imbibition whenever Radicle Protrusion Is Prevented
Plant Physiology,
March 1, 2003;
131(3):
1347 - 1359.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
R. DOLFERUS, E. J. KLOK, C. DELESSERT, S. WILSON, K. P. ISMOND, A. G. GOOD, W. J. PEACOCK, and E. S. DENNIS
Enhancing the Anaerobic Response
Ann. Bot.,
January 2, 2003;
91(2):
111 - 117.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
D. Garwe, J. A. Thomson, and S. G. Mundree
Molecular characterization of XVSAP1, a stress-responsive gene from the resurrection plant Xerophyta viscosa Baker1
J. Exp. Bot.,
January 2, 2003;
54(381):
191 - 201.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
J. W. White and G. Hoogenboom
Gene-Based Approaches to Crop Simulation: Past Experiences and Future Opportunities
Agron. J.,
January 1, 2003;
95(1):
52 - 64.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
J. A. Kreps, Y. Wu, H.-S. Chang, T. Zhu, X. Wang, and J. F. Harper
Transcriptome Changes for Arabidopsis in Response to Salt, Osmotic, and Cold Stress
Plant Physiology,
December 1, 2002;
130(4):
2129 - 2141.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
T.-H. Hsieh, J.-t. Lee, Y.-y. Charng, and M.-T. Chan
Tomato Plants Ectopically Expressing Arabidopsis CBF1 Show Enhanced Resistance to Water Deficit Stress
Plant Physiology,
October 1, 2002;
130(2):
618 - 626.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
E. Ruelland, C. Cantrel, M. Gawer, J.-C. Kader, and A. Zachowski
Activation of Phospholipases C and D Is an Early Response to a Cold Exposure in Arabidopsis Suspension Cells
Plant Physiology,
October 1, 2002;
130(2):
999 - 1007.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
M. C. Falk, B. M. Chassy, S. K. Harlander, T. J. Hoban IV, M. N. McGloughlin, and A. R. Akhlaghi
Food Biotechnology: Benefits and Concerns
J. Nutr.,
June 1, 2002;
132(6):
1384 - 1390.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
M. Vermel, B. Guermann, L. Delage, J.-M. Grienenberger, L. Marechal-Drouard, and J. M. Gualberto
A family of RRM-type RNA-binding proteins specific to plant mitochondria
PNAS,
April 30, 2002;
99(9):
5866 - 5871.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
D. N. Thomas and G. S. Dieckmann
Antarctic Sea Ice--a Habitat for Extremophiles
Science,
January 25, 2002;
295(5555):
641 - 644.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
K. R. Jaglo, S. Kleff, K. L. Amundsen, X. Zhang, V. Haake, J. Z. Zhang, T. Deits, and M. F. Thomashow
Components of the Arabidopsis C-Repeat/Dehydration-Responsive Element Binding Factor Cold-Response Pathway Are Conserved in Brassica napus and Other Plant Species
Plant Physiology,
November 1, 2001;
127(3):
910 - 917.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
M. Vermel, B. Guermann, L. Delage, J.-M. Grienenberger, L. Marechal-Drouard, and J. M. Gualberto
A family of RRM-type RNA-binding proteins specific to plant mitochondria
PNAS,
April 30, 2002;
99(9):
5866 - 5871.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
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TOP
INTRODUCTION
THE CBF/DREB1 TRANSCRIPTIONAL...