from freezing to scorching, transcriptional responses to temperature variations in plants

Available online at www.sciencedirect.com

From freezing to scorching, transcriptional responses totemperature variations in plantsJian Hua

Plants are capable of adapting to a wide range of temperatures

by reprogramming their transcriptome, proteome, and

metabolome. Early investigations uncovered a regulatory

network containing the CBF–COR pathway in freezing

tolerance and the HSF–HSP pathway in thermotolerance.

Recent studies have identified additional signaling components

for extreme temperature tolerance and new regulators of plant

form in response to temperature variation within the

nonextreme range. Some common regulators are shared

between temperature responses and other environmental and

developmental responses. These discoveries further reveal the

complexity and sophistication of molecular mechanisms

underlying plants’ adaptation to their environment.

Address

Department of Plant Biology, Cornell University, Ithaca, NY 14853,

United States

Corresponding author: Hua, Jian ([email protected])

Current Opinion in Plant Biology 2009, 12:568–573

This review comes from a themed issue on

Cell signalling and gene regulation

Edited by Jan U. Lohmann and Jennifer L. Nemhauser

Available online 26th August 2009

1369-5266/$ – see front matter

# 2009 Elsevier Ltd. All rights reserved.

DOI 10.1016/j.pbi.2009.07.012

IntroductionTemperature is one of the most important environmental

factors that regulate plant growth and development [1,2�].Plants perceive various characteristics of temperature

including the absolute temperature, temperature

changes, and the accumulation of temperature values

over time. The effect of temperature response can be

manifest immediately or at a much later stage. Tremen-

dous advances have been made in the past two decades to

identify important components in cold and heat acclim-

ation as well as in vernalization. More recent studies are

beginning to reveal the molecular events in plants’

responses to nonextreme temperature and the cross-talk

between temperature and other environmental/develop-

mental signals. A number of excellent reviews have

covered cold acclimation [3�,4,5], vernalization [6], ther-

motolerance [5,7,8�], and temperature interaction with

light and the circadian clock [9�,10]. This review intends


to update the progress of the past two years in under-

standing freezing tolerance, thermotolerance, and the

regulation of plant form by temperature, especially at

the level of transcriptional regulation.

Regulation of the CBF pathwayCold acclimation is an adaptive response where plants

acquire an increase in freezing tolerance upon a prior low

nonfreezing temperature treatment [11]. Extensive tran-

scriptional reprogramming occurs during cold acclimation

to induce cold-regulated (COR) genes, some of which are

responsible for producing cryoprotective molecules. Cen-

tral to this transcriptional regulation are the CBF [C-repeat(CRT)/dehydration responsive element (DRE)-binding factor]

genes that encode AP2/ERF family transcription factors

[11]. Three CBF genes (CBF1–3) in Arabidopsis are

induced by cold and confer increased freezing tolerance

when overexpressed. These three genes have different

expression patterns and do not regulate an identical set of

genes, suggesting a fine-tuned regulatory system for

optimal adaptation to cold [12�]. The CBF proteins bind

to the (CRT/DRE) motif (CCGAC) present in the pro-

moters of a number of COR genes named the CBFregulon. The importance of the CBF pathway in cold

tolerance has been observed in both monocots and dicots

[13]. Natural variations in the CBF family also support a

regulatory function of these genes. Compared to Arabi-

dopsis accessions in the North, those in the Southern

range have a higher nucleotide polymorphism in both

coding and regulatory regions of the CBF family. Relaxed

selection on the CBF genes in Southern accessions results

in compromised transcriptional activation during cold

acclimation [14].

The CBF3/DREB1A gene is activated by the MYC

bHLH transcription factor ICE1 (Inducer of CBF Expres-sion 1) and its interacting protein AtMYB15 [15,16]. ICE1

binds to the canonical MYC element CANNTG in the

promoter of CBF3. ICE2, an ICE1 homolog, is also

involved in cold acclimation, probably through regulating

the CBF1 gene [17]. ICE1 itself is negatively regulated by

HOS1 (High Expression of Osmotically Responsive

Genes 1), a E3 ubiquitin ligase responsible for the ubi-

quitination and degradation of ICE1 [18]. SIZ1, a SUMO

E3 ligase, is a positive regulator of ICE1 [19�]. The siz1mutant is defective in cold induction of the CBF and CORgenes and is chilling and freezing sensitive. SIZ1 may

increase CBF induction by sumoylating ICE1 to antagon-

ize ubiquitination mediated by HOS1. Indeed, SIZ1

expression led to both moderately increased sumolyation

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http://dx.doi.org/10.1016/j.pbi.2009.07.012

Transcriptional responses to temperature variations Hua 569

and decreased polyubiquitination of ICE1 in in vitrostudies. Further, a sumoylation-defective mutant of

ICE1 repressed cold induction of CBF3 and was freezing

sensitive.

Both ICE1 and SIZ1 have broader roles than regulating

CBF expression. Surprisingly, ICE1 was re-isolated as

SCREAM, whose gain-of-function mutant exhibited con-

stitutive stomata differentiation in the epidermis [20].

ICE1 therefore appears to perform permissive roles in

stomata development while other tissue-specific bHLHgenes play more instructive roles. SIZ1, being the only

SUMO E3 ligase in Arabidopsis, is found to regulate

thermotolerance, drought resistance, salicylic acid (SA)

accumulation, and flowering time, indicating a broad role

of sumoylation regulation in plant growth and develop-

ment [21].

The CBF2 gene is activated by members of calmodulin-

binding transcription activators, CAMTA [22��]. A CM2

element responsible for the induction of CBF2 matches

the CG-1 element (CGCG) that is recognized and bound

by the CG-1 domain present in the CAMTA proteins.

The camta3 mutant in Arabidopsis had reduced cold

induction of CBF2 and other early cold-induced genes;

and the camta1 camta3 double mutant had compromised

freezing tolerance. Induction of calcium spike is an early

event in cold response, and this study reveals a potential

connection of calcium signaling and cold-regulated gene

expression. Both ICE1 and CAMTA binding sites are

found in the promoter of CBF2. It will be interesting to

see how these two transcription factors interact to

regulate CBF genes and contribute to COR induction.

Cold acclimation independent of CBFtranscript inductionFreezing tolerance is regulated at multiple levels in

addition to the induction of CBF genes. Loss of function

of the transcription factors HOS9 and HOS10 has stronger

or earlier induction of CBF regulon without affecting

CBF expression, suggesting they might have a general

role in repressing COR genes [3�]. Another regulator of the

COR genes, but not CBF induction, is SFR6 (SENSITIVETO FREEZING 6) [23]. The sfr6 mutant fails to undergo

cold acclimation because of a defect in upregulating the

CBF regulon. SFR6 functions downstream of the CBFs as

it is required for the induction of COR genes by CBF1 and

CBF2 overexpression. The sfr6 mutant has other defects

including late flowering and a sucrose-dependent long-

period phenotype [24]. The SFR6 gene encodes a novel

protein that is localized in the nucleus, suggesting that it

may modulate gene expression directly to influence

multiple responses.

The esk1 (eskimo1) mutant can withstand a much lower

freezing temperature than the wild-type. It encodes a

novel plant-specific protein in a large protein family with


unknown functions in Arabidopsis [25]. The esk1 mutant

also has increased drought tolerance as a result of better

water usage efficiency and salt resistance [26]. These

phenotypes are not related to the upregulation of the

CBF regulon, but might be associated with the upregula-

tion of some stress-responsive genes.

The complexity in freezing tolerance is further suggested

by natural variations in Arabidopsis. The expression levels

of CBF and COR genes do not totally correlate with

freezing tolerance in a set of 50 accessions [27], suggesting

that multiple components could be under adaptive selec-

tion.

Triggering the CBF pathway by signals otherthan low temperatureThe CBF pathway is also stimulated by signals other than

cold (48C). A progressive decrease of temperature from

208C to 17, 14, 12, 10, or 88C induced similar responses at

the level of transcripts, enzyme activities, and metab-

olites, with increasing amplitude as temperature

decreased [28�]. Interestingly, these small decreases

in temperature at the nonextreme range trigger the

expression of most of the genes induced robustly by

cold. Another study revealed that two COR genes

were induced by a temperature decrease from 28 to

228C through the CBF genes and the CRT elements

[29]. Thus the CBF pathway is adopted in response to

small decreases in temperature, which might be an

adaptive strategy to prepare plants for extreme tempera-

tures.

More intriguingly, the CBF regulon is controlled by light

quality [30��]. A low red to far-red (R:FR) ratio upregu-

lated the CBF genes and their downstream COR genes at

16 but not 228C. Remarkably, this low R:FR-induced

increase in CBF expression was sufficient to confer freez-

ing tolerance at 168C. The combination of low R:FR ratio

with a relatively low temperature might mimic autumn.

This connection between light quality and cold response

suggests that plants could integrate multiple environmen-

tal signals to anticipate seasonal changes and turn on

adaptive responses.

Thermotolerance via HSF and HSPPlants can acquire better thermotolerance by a prior high

temperature treatment. This heat acclimation involves

the accumulation of heat-shock proteins (HSPs) that are

molecular chaperones [31,32]. HSPs are induced by

heat-stress transcription factors (HSFs) that bind to

the heat-shock element (HSE) ‘GAANNTTC’ in the

promoters of HSPs [7]. There are 44 HSP genes in four

families and 21 HSF genes in Arabidopsis [33]. In

addition to heat, these genes can be induced by various

abiotic and biotic stresses [33], suggesting that they may

represent interaction points between multiple stress

response pathways.


570 Cell signalling and gene regulation

There is a continuing effort to determine if these genes

play a role in thermotolerance. Although knocking out

one single HSP, HSF, or heat-induced genes had little

impact on thermotolerance in most cases; a role of

HSP101I, Hsa32, and HSFA2 in Arabidopsis, and HSFA1ain tomato has been identified in thermotolerance by

mutant analysis [34–36]. Recent studies revealed that

Hsp110, HSFA7a, and HSFA3 also play critical roles in

this process [37�,38,39]. Interestingly, the TMS1 (Thermo-sensitive Male Sterile 1) gene was identified as an Hsp40homolog and is important for pollen tube thermotolerance

[40]. This suggests that HSF and HSP genes could

acquire specialized functions, which might be revealed

by more sensitive and specific assays for their mutants.

The activities of HSFs can be modified post-transcrip-

tionally. An interacting protein of HSFA1a was found to

be a CaM-binding protein kinase (CBK) [41]. The knock-

out lines of this AtCBK3 gene had impaired basal thermo-

tolerance and were defective in the transcription of HSPgenes. AtCBK3 might control the binding activity of

HSFs to HSEs by phosphorylating AtHSFA1a. Similar

to CAMTA for cold induction, CBK3 is a potential

connection of calcium signaling and heat-induced tran-

scription.

Some HSFs are themselves induced by heat. The heat

induction of HSFA3 is directly regulated by the transcrip-

tion factor DREB2A (DRE Binding 2A), which was

known to regulate drought-stress responses [42]. Heat-

inducible DREB2A can bind to the DRE element in the

promoter of HSFA3 under heat shock to induce HSFA3

and further activate HSP expression [38,39]. The DRE

element is present in the promoters of a cluster of heat-

induced genes [37�], which might be DREB2A targets in

heat response.

Thermotolerance via heat-inducibletranscription factorsAdditional heat-inducible transcription factors are found

to contribute to thermotolerance. The NF-X1 (NuclearTranscription Factor X-box binding 1) gene has a heat

induction pattern similar to the cluster of genes with a

DRE element in the promoter. It promotes both acquired

thermotolerance and salt tolerance [37�]. The transcrip-

tional coactivator MBF1c (Multiprotein Bridging Factor

1c) involved in multiple stress responses, accumulates

rapidly during heat stress and is localized to the nucleus.

It appears to function in thermotolerance upstream to SA,

trehalose, and ethylene, but is not required for the

expression of HSFA2 and different HSPs [43]. The

dual/multifunction of DREB2A, MBF1c, and NF-X1further supports the connection of heat acclimation

response with other stress responses.

A novel transcriptional activation mechanism in thermo-

tolerance was revealed by a putative membrane-tethered


transcription factor bZIP28 [44�]. It has a transmembrane

domain and is localized to the endoplasmic reticulum

under nonheat conditions. Upon heat treatment, the

transcript is increased and the protein undergoes proteol-

ysis to release the predicted transcription factor domain to

the nucleus to activate transcription. Its direct transcrip-

tional targets are unknown, although heat induction of

Bip2 and HSP26.5-P is affected in its null mutant. It will

be interesting to see if and how this transcription factor

works with HSF to regulate HSP induction.

Thermotolerance independent of HSPsThermotolerance involves multiple HSP-independent

pathways mediated by abscisic acid (ABA), SA, hydrogen

peroxide, and ethylene [45]. The nonprotein amino acid

beta-aminobutyric acid (BABA) was recently added to

this list. It enhances acquired but not basal thermotoler-

ance, probably through upregulating HSP101 and the

ABA pathway [46].

The cloning of the HOT5 (Sensitive to Hot Temperature 5)

gene also indicates the involvement of nitric oxide (NO)

homeostasis in thermotolerance [47�]. The hot5 null

mutants have multiple defects, including failing to

heat-acclimate as light-grown plants. HOT5 encodes an

S-nitrosoglutathione reductase (GSNOR), which metab-

olizes the NO adduct S-nitrosoglutathione. The hot5 null

mutants exhibit heat sensitivity associated with increased

NO species, indicating NO homeostasis is important to

heat-stress tolerance.

Temperature on plant growth and architecturePlants modulate their size and architecture in response to

ambient temperature. Generally, low temperature inhi-

bits plant growth, not simply as a passive metabolic con-

sequence but a regulated process involving hormone

signaling. Low temperature inhibits the expression of

gibberellin (GA) biosynthetic genes and inducing GA-

catabolizing genes, thus reducing accumulation of GA

and limiting plant growth [2�]. The antagonistic inter-

action between cold and GA is further revealed in CBFoverexpression lines that exhibit growth retardation at

normal temperature. This dwarf phenotype is rescued by

GA application or constitutive GA-signaling della mutant

[48��]. Further, cold-induced root inhibition can also be

reduced by della mutants. These data indicate that the

GA and DELLA pathway is utilized for growth inhi-

bition, triggered by CBF genes and cold.

SA is also involved in inhibiting plant growth at low

temperature. More SA accumulates at 5 than at 238C,

and SA-deficient mutants are larger than the wild-type at

58C [49]. SA is a major signaling molecule for plant

disease resistance, and a number of mutants with con-

stitutive defense response accumulate high levels of SA

and have a dwarf phenotype. High temperature could

inhibit defense responses, resulting in a recovery of



Figure 1

Schematic diagram of temperature-signaling events in cold acclimation, thermotolerance, and plant form regulation. The approximate ranges of

temperature triggering the corresponding responses are shown as filled rounded rectangles. The CBF genes play important roles in cold acclimation

and are regulated by multiple pathways. Thermotolerance involves induction of HSP genes, which are regulated by multiple transcription factors.

Regulation of plant form by ambient temperature involves hormone signaling. Major components mentioned in the text are shown, with emphasis on

transcriptional regulation. Not all known regulators are shown. Regulators that integrate multiple signals are indicated by shaded ovals. Arrow in red

indicates a stronger activation at a higher temperature; arrow in blue indicates a stronger activation at a lower temperature; and arrow with dotted line

indicates a higher activation by a larger temperature change. Transcription factors are colored in purple.

normal growth in these mutants [50]. Consistently, tran-

scription profiling found that heat treatment decreases

transcripts involved in programmed cell death, basic

metabolism, and biotic stress responses [37�]. The mol-

ecular basis of temperature regulation of SA accumulation

and plant defense responses is unknown.

High temperature induces architecture changes in-

cluding elongation of hypocotyls and petioles. These

morphological responses are reminiscent of shade avoid-

ance, and indeed auxin has been identified as involved in

both responses [51,52]. PIF4 (PHYTOCHROME INTER-ACTING FACTOR 4) was recently identified as a

mediator of the morphological responses to high

temperature [53��]. PIF4 is a bHLH protein with

growth-promoting activities in both light and GA sig-

naling. PIF4 affects the high temperature induction of

the auxin-responsive gene IAA29, which also mediates

auxin-regulated shade avoidance. As pif4 is responsive to

high temperature in floral induction, PIF4 is not a or the

only temperature-perception component but rather

mediates growth regulation by light and temperature.

PIF4 and its homology PIF5 are regulated by clock and

light and promote stem growth at the end of the night

[54]. Thus, PIF4 acts as an integrator of environmental

signals including light, clock, and temperature, poten-

tially allowing plants to time growth with optimal growth

conditions.


Other transcription factors function in integrating tempera-

ture and other signals. SPT (SPATULA) is involved in

responding to light and low temperature to regulate ger-

mination, with an additional role in floral organ develop-

ment [55]. ICE1 regulates cold acclimation and stomata

differentiation [15,20]. RPP7 and RPP9 appear to receive

both light and temperature signals to regulate the circadian

clock [2�]. FLC, FLM, and SVP could mediate both light

and temperature in flowering time control [9�]. Thus plants

employ an array of transcription factors to integrate

multiple signals to regulate growth and development.

ConclusionsWith the power of genetics and genomics, more players

are being identified for transcriptional control in tempera-

ture responses. They form a fine-tuned network to trans-

duce and integrate multiple signals (Figure 1). The

challenge ahead is to reveal temperature-perception mol-

ecules, identify internodes of multiple responses, and

integrate regulation at transcriptome, proteome, and

metabolome levels. All these will lead to a system un-

derstanding of adaptive strategies that plants use to cope

with environmental changes.

AcknowledgementsWork in the Hua laboratory was supported by grants from the NationalScience Foundation (IOS-0642289) and US Department of Agriculture(2005-35100-16044).


572 Cell signalling and gene regulation

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45. Larkindale J, Hall JD, Knight MR, Vierling E: Heat stressphenotypes of Arabidopsis mutants implicate multiplesignaling pathways in the acquisition of thermotolerance.Plant Physiol 2005, 138:882-897.

46. Zimmerli L, Hou BH, Tsai CH, Jakab G, Mauch-Mani B,Somerville S: The xenobiotic beta-aminobutyric acid enhancesArabidopsis thermotolerance. Plant J 2008, 53:144-156.

47.�

Lee U, Wie C, Fernandez BO, Feelisch M, Vierling E: Modulation ofnitrosative stress by S-nitrosoglutathione reductase is criticalfor thermotolerance and plant growth in Arabidopsis. Plant Cell2008, 20:786-802.

The hot5 mutant is defective in heat acclimation. In this study, HOT5 isfound to encode a S-nitrosoglutathione reductase (GSNOR) that meta-bolizes the NO adduct S-nitrosoglutathione. NO homeostasis is found tobe critical for heat-stress response and plant development.

48.��

Achard P, Gong F, Cheminant S, Alioua M, Hedden P, Genschik P:The cold-inducible CBF1 factor-dependent signaling pathwaymodulates the accumulation of the growth-repressing DELLAproteins via its effect on gibberellin metabolism. Plant Cell2008, 20:2117-2129.

This study shows that CBF1 inhibits plant growth through GA/DELLApathway. Overexpression of CBF1 or cold could decrease GA amountand enhance the accumulation of the growth-inhibiting DELLA proteins.

49. Scott IM, Clarke SM, Wood JE, Mur LA: Salicylate accumulationinhibits growth at chilling temperature in Arabidopsis. PlantPhysiol 2004, 135:1040-1049.

50. Yang S, Yang H, Grisafi P, Sanchatjate S, Fink GR, Sun Q, Hua J:The BON/CPN gene family represses cell death and promotescell growth in Arabidopsis. Plant J 2006, 45:166-179.

51. Gray WM, Ostin A, Sandberg G, Romano CP, Estelle M: Hightemperature promotes auxin-mediated hypocotyl elongationin Arabidopsis. Proc Natl Acad Sci U S A 1998, 95:7197-7202.

52. Tao Y, Ferrer JL, Ljung K, Pojer F, Hong F, Long JA, Li L,Moreno JE, Bowman ME, Ivans LJ et al.: Rapid synthesis of auxinvia a new tryptophan-dependent pathway is required forshade avoidance in plants. Cell 2008, 133:164-176.

53.��

Koini MA, Alvey L, Allen T, Tilley CA, Harberd NP, Whitelam GC,Franklin KA: High temperature-mediated adaptations in plantarchitecture require the bHLH transcription factor PIF4. CurrBiol 2009, 19:408-413.

This study demonstrates that PIF4 mediates the morphological responsesto high temperature (288C). It does so probably through inducing auxin-responsive genes but independent of phytochrome or DELLA proteins.

54. Nozue K, Covington MF, Duek PD, Lorrain S, Fankhauser C,Harmer SL, Maloof JN: Rhythmic growth explained bycoincidence between internal and external cues. Nature 2007,448:358-361.

55. Penfield S, Josse EM, Kannangara R, Gilday AD, Halliday KJ,Graham IA: Cold and light control seed germination throughthe bHLH transcription factor SPATULA. Curr Biol 2005,15:1998-2006.


from freezing to scorching, transcriptional responses to temperature variations in plants

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