A cold night can follow a hot day, and because they cannot move, plants subjected to such temperature fluctuations must acclimate on the basis mainly of pre-existing proteins. Zhang et al. report in a paper in BMC Plant Biology, however, that heat-induced cell death results from transcriptional activation of a kinase related to disease resistance factors and leading to a localized hypersensitive response. This specialized response reflects the failure of adaptations that normally enable plants to survive over a remarkable temperature range, by mechanisms that are not fully understood

CB Osmond

DA Hoisington

FW Went

H Shimono

H Zhang

S Sato

SD Smith

Virginia Walbot

English

PubMed

Abstract A cold night can follow a hot day, and because they cannot move, plants subjected to such temperature fluctuations must acclimate on the basis mainly of pre-existing proteins. Zhang et al. report in a paper in BMC Plant Biology, however, that heat-induced cell death results from transcriptional activation of a kinase related to disease resistance factors and leading to a localized hypersensitive response. This specialized response reflects the failure of adaptations that normally enable plants to survive over a remarkable temperature range, by mechanisms that are not fully understood.</p

Walbot Virginia

Directory of Open Access Journals

BMC Biology

How plants cope with temperature stress

Springer - Publisher Connector

How plants cope with temperature stress
Virginia Walbot
Walbot BMC Biology 2011, 9:79 
http://www.biomedcentral.com/1741-7007/9/79 (17 November 2011)
When you camp out in the high deserts of Southern 
California, it freezes at night. As you huddle in your 
sleeping bag waiting for the coffee water to boil, the sun 
rises and plants begin to photosynthesize using the first 
photons in the cool dawn. Later that day while you are 
shedding clothing and gulping water in 45°C heat, the 
same plants conduct photosynthesis under a blazing sun. 
It is remarkable that plants adapted to high deserts thrive 
despite approximately 50°C daily temperature swings [1]. 
Transcription, translation, membrane properties, mito­
chon drial respiration, microtubule and microfilament­
mediated processes, plastids, and all other essential cell 
functions retain activity over a broad temperature range, 
and furthermore, all of these processes remain in balance 
[2]. How can plant cells, tissues and organs sustain 
homeo stasis despite temperature fluctuations? Of course, 
for temperate and tropical zone plants and crops, the 
fluctuations are less extreme over a typical day, but 
nonetheless changes of 10 to 15°C over a day or a week 
are readily accommodated. Only when some process fails 
as a result of heat or cold does the local temperature 
regime set the limits of plant distribution [3]. Zhang et al. 
[4] provide an example of failure, with evidence that 
exceeding the homeostatic limits for managing reactive 
oxygen species at high temperature results in localized 
cell death.
Efficiency versus adaptability
At the level of individual proteins, there must be a com­
pro mise between peak efficiency at constant temperature ­ 
the route taken by mammals ­ and sufficiency over a 
broad temperature range (Figure  1). To state it another 
way, mammalian enzymes and constituent processes fail 
outside a narrow window of optimal temperatures, and 
such failure is catastrophic for the organism, whereas 
plants can maintain and coordinate cellular processes 
over a broad temperature range.
When coordination between key cellular processes 
fails, cell death can result. This can occur in plant cells as 
part of a localized hypersensitive response to pathogen 
attack, a strategy to restrict the growth of the invader. 
Similar localized cell death lesions can result from failure 
of homeostatic processes at the non­permissive tempera­
ture in plant mutants with specific sensitivity to either 
heat or cold. In both cases this reflects an inability to 
manage reactive oxygen and its consequences. In the case 
reported by Zhang et al. [4] high temperature is non­
permissive (Figure  2). In contrast, the dominant Lesion 
mimic1 (Les1) maize mutant is entirely normal at high 
temperature but at 22°C or lower, extensive necrotic leaf 
lesions develop [5]. Wounding leaves with pins or 
painting leaves with low molecular weight organic 
compounds (the sort found in marking pens used to 
write on maize leaves) can trigger lesion symptoms at any 
temperature. The observations of Zhang et al. suggest 
that pathways activated in pathogen defense may also play 
a part in integrating responses to the abiotic challenges of 
substantial temperature fluctuations. It remains mys­
terious, however, how plants generally manage to maintain 
homeostasis in the face of such fluctuations.
Is the solution to temperature fluctuation 
duplication or stabilization of proteins?
Varying by plant species, alleles of duplicated genes in 
tetraploid plants could be selected to contribute to 
Abstract
A cold night can follow a hot day, and because they 
cannot move, plants subjected to such temperature 
fluctuations must acclimate on the basis mainly of pre-
existing proteins. Zhang et al. report in a paper in BMC 
Plant Biology, however, that heat-induced cell death 
results from transcriptional activation of a kinase related 
to disease resistance factors and leading to a localized 
hypersensitive response. This specialized response 
reflects the failure of adaptations that normally enable 
plants to survive over a remarkable temperature range, 
by mechanisms that are not fully understood.
How plants cope with temperature stress
Virginia Walbot*
See research article: http://www.biomedcentral.com/1471-2229/11/160/abstract
CO M M E N TA RY  Open Access
*Correspondence: walbot@stanford.edu 
Department of Biology MC5020, 385 Serra Mall, Stanford University, Stanford, 
CA 94305-5020, USA
© 2011 Walbot; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons 
Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any 
medium, provided the original work is properly cited.
Walbot BMC Biology 2011, 9:79 
http://www.biomedcentral.com/1741-7007/9/79
temperature buffering; but only the most recent 
tetraploid possibly retains all duplicated genes, so this 
cannot account for adaptability in the majority of plants. 
If subfunctionalized loci are necessary for temperature 
adaptation, gene loss and allele fixation at single loci 
could be a recipe for disaster in a fluctuating environ­
ment, because they would result in numerous processes 
vulnerable to high and low temperatures. I predict 
instead that much of the buffering against temperature 
perturbation in protein complexes and in process 
coordination will require an extra, perhaps novel and 
plant­specific, suite of stabilizing proteins.
To me, the retention of fidelity in nucleic acid­based 
processes is the most striking. Empirical laboratory 
evidence amply demonstrates that interactions of 
proteins, such as transcription factor binding to short 
DNA motifs or charged tRNAs with three bases in 
mRNA, are stable over a very narrow temperature range. 
In vivo, chromatin structure could stabilize protein­DNA 
interaction to regulate transcription initiation, and the 
ribosome similarly provides a special niche for trans­
lation. In plants, I anticipate that proteins will be identi­
fied that stabilize specific, local chromatin configurations 
within the normal temperature range for a given habitat. 
Similarly, I predict that there will be proteins to stabilize 
the ribosome to permit the otherwise tenuous inter­
actions within the molecular complexes to continue with 
high fidelity and efficiency. These stability factors would 
prevent both disassociation of factors that act together 
and persistence of interactions between proteins whose 
disassembly is required for normal regulation of cellular 
processes. I imagine that the various molecular com­
plexes defined in laboratory yeast and in mammals will 
have accessory proteins. I predict that these will be more 
likely to be defined by biochemistry than genetic 
approaches, because under optimal conditions they may 
be dispensable.
Continuous development as a strategy for organ 
acclimation
The plant life strategy of continuous development also 
contributes to maintenance of function in a fluctuating 
environment. Plants acclimate to current conditions by 
integrating environmental information with develop­
mental programs for leaf and stem or root initiation from 
meristems and subsequent growth and differentiation. 
An example of acclimation to light conditions is exploited 
by the nursery industry to entice you to purchase plants. 
By starving plants for photons in dim light, horticulturists 
generate plants with larger, darker green leaves. After you 
have bought the plant and installed it in a sunny window, 
all of the luxuriant shade leaves senesce precociously and 
smaller, paler sun leaves emerge that are more suited to 
the high­light environment. Zebra­stripe mutants of 
maize mirror the alternation of cool dark nights with 
warmer bright days through failure to stabilize chloro­
phyll content (Figure 3) for half of each 24­hour period in 
response to non­permissive light or temperature 
conditions, with the consequence that crosswise strips of 
pale tissue alternate with normal green tissue throughout 
Figure 1. Schematic representation of the temperature tolerance 
of plant and animal processes. Plant proteins (black line) will show 
a broad range of activity and stability relative to temperature in 
comparison to mammalian proteins (red line) with a peak narrowly 
centered on body temperature.
Low                High
Temperature
Protein
Activity &
Stability
Figure 2. Necrotic lesions on leaves grown at non-permissive 
temperature. Rice leaves overexpressing NRKe, a gene encoding 
a kinase related to known disease-resistance kinases that induce 
necrosis in response to infection, are grown for 10 days at 24°C (the 
two blades on the left) and then for 3 days at 35°C (the two blades 
on the right). At 35°C, the non-permissive temperature, the leaves 
develop necrotic lesions. Taken from Figure 2b of Zhang et al. [4].
Walbot BMC Biology 2011, 9:79 
http://www.biomedcentral.com/1741-7007/9/79
Page 2 of 4
the 10­day period of blade development. In many grasses, 
defective stripes are not restored to wild­type phenotype 
but remain a report on temperature fluctuations beyond 
the optimal range over the course of leaf growth.
Key stages when temperature tolerance really 
matters
Germination in flowering plants is the irreversible 
growth of a plant embryo out of the protective seed coat, 
fueled by stored nutrient reserves. As germination 
proceeds, there is a race between the rate of reserve 
consumption and the establishment of an independent, 
photosynthetically competent seedling able to acquire 
water and mineral nutrients from the soil. Germination is 
highly sensitive to temperature in many species. First, 
many species are triggered to germinate by either a high 
or low temperature period that destroys germination 
inhibitors, an adaptation allowing the plant to measure 
the end of winter for spring emergence or end of summer 
for fall germination. Second, water spurs imbibition, 
making growth possible, but a subsequent drop in 
temperature can freeze the tender seedling stem, while 
high heat will crisp the unfurling preformed leaves 
beyond repair, under conditions that can be tolerated by 
a well established plant.
Flowering represents another one­way commitment in 
the lifecycle, as an apical meristem previously generating 
leaves and stems switches to the floral program and is 
entirely consumed in making a flower. Although heat and 
cold can adversely affect the showy floral parts, the most 
serious impact is primarily on the developing haploid 
pollen and its nutritive diploid support tissue, the 
tapetum. The parallel with germination is that pollen is 
sealed off from the vegetative plant shortly after meiosis 
by a thick coat and must survive with a fixed nutrient 
store throughout maturation, dispersal, and the initial 
stages of pollen tube growth prior to fertilization. 
Nutrients in pollen pass through the tapetal layer and the 
quality of this single­cell­thick tissue ring is thus also 
paramount. In tomato, slight temperature elevation that 
did not affect plant biomass, number of flowers, or 
meiosis greatly affected the number of functional pollen 
grains and hence fruit yield [6]. In rice, low temperature 
limits cool season production because of the negative 
impact on male reproductive fitness [7]. The literature on 
male fitness abounds with examples of the negative 
impact of temperature extremes tolerated by the 
vegetative plant.
Considering both vegetative (leaf phenotype) cases and 
male sterility, it is clear that temperatures just beyond the 
acclimation range can greatly affect both survival and 
reproduction. These cases show that plants can thrive 
across a broad temperature range, but that temperatures 
beyond genotypic thresholds evoke consequences such as 
cell death ­ as demonstrated by Zhang et al. ­ poor 
greening, and male sterility. These deleterious pheno­
types are the starting point for unraveling the mecha­
nisms underpinning temperature tolerance, with the 
hypothesis that the first process to fail at either high or 
low temperature defines a key component of plant life.
Acknowledgements
Supported by a grant from the National Science Foundation (PGRP 07-01880).
Published: 17 November 2011
References
1. Smith SD, Monson RK, Anderson JE: Physiological Ecology of North American 
Desert plants. New York: Springer; 1997.
2. Went FW: The effect of temperature on plant growth. Annu Rev Plant Physiol 
1953, 4:347-362.
3. Osmond CB, Austin MP, Berry JA, Billings WD, Boyer JS, Dacey JWH, Nobel PS, 
Smith SD, Winner WE: Stress physiology and the distribution of plants. 
Bioscience 1987, 37:38-48.
4. Zhang H, Cao Y, Zhao J, Li H, Xiao J, Wang S: A pair of orthologs of a 
Figure 3. Zebra striping in a fully mature corn plant grown 
on Moloka’I, Hawaii in winter 2011. All of the adult leaves were 
marked by crosswise normal dark green and chlorotic (yellow green) 
bands. It takes about 10 days for an adult leaf to develop, and pairs 
of green and yellow-green bands are inferred to represent a 24-hour 
period of leaf development. Without further tests it is not possible to 
pinpoint whether normal chloroplast development or stability is heat 
or cold sensitive. Ambient day temperatures were 23 to 27°C, just 
slightly elevated over night temperatures of 17 to 21°C. Zebra striping 
is highly persistent in maize because zones of poor differentiation 
are not repaired during growth at the permissive temperature. 
Photograph courtesy of Tim Kelliher, Stanford University.
Walbot BMC Biology 2011, 9:79 
http://www.biomedcentral.com/1741-7007/9/79
Page 3 of 4
leucine-rich repeat receptor kinase-like disease resistance gene family 
regulates rice response to raised temperature. BMC Plant Biol 2011, 11: 160.
5. Hoisington DA, Neuffer MG, Walbot V: Disease lesion mimics in maize. I. 
Effect of genetic background, temperature, developmental age, and 
wounding on necrotic spot formation with Les1. Dev Biol 1982, 93:381-388.
6. Sato S, Kamiyama M, Iwata T, Makita N, Furukawa H, Ikeda H: Moderate 
increase of mean daily temperature adversely affects fruit set of 
Lycopersicon esculentum by disrupting specific physiological processes in 
male reproductive development. Ann Bot 2006, 97:731-738.
7. Shimono H, Hasegawa T, Moriyama M, Fumimura S, Nagata T: Modeling 
spikelet sterility induced by low temperature in rice. Agronomy J 2005, 
97:1524-1536.
doi:10.1186/1741-7007-9-79
Cite this article as: Walbot V: How plants cope with temperature stress. BMC 
Biology 2011, 9:79.
Walbot BMC Biology 2011, 9:79 
http://www.biomedcentral.com/1741-7007/9/79
Page 4 of 4


Crossref

JE: Physiological Ecology of North American Desert plants.

S: A pair of orthologs of a

The effect of temperature on plant growth. Annu Rev Plant Physiol

WE: Stress physiology and the distribution of plants. Bioscience

http://doaj.org/search?source=%7B%22query%22%3A%7B%22bool%22%3A%7B%22must%22%3A%5B%7B%22term%22%3A%7B%22id%22%3A%222ca734ae18d24012bfc19830155c9575%22%7D%7D%5D%7D%7D%7D

How plants cope with temperature stress

Abstract

Similar works

Full text

Available Versions

Directory of Open Access Journals

Springer - Publisher Connector

Crossref