How plants cope with temperature stress
© Walbot; licensee BioMed Central Ltd. 2011
Received: 22 October 2011
Accepted: 11 November 2011
Published: 17 November 2011
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.
See research article http://www.biomedcentral.com/1471-2229/11/160
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 . Transcription, translation, membrane properties, mitochondrial 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 . How can plant cells, tissues and organs sustain homeostasis 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 . Zhang et al.  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
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 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 environment, 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 plant-specific, suite of stabilizing proteins.
To me, the retention of fidelity in nucleic acid-based 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 protein-DNA interaction to regulate transcription initiation, and the ribosome similarly provides a special niche for translation. In plants, I anticipate that proteins will be identified 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 interactions 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 complexes 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
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 one-way 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 single-cell-thick 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 . In rice, low temperature limits cool season production because of the negative impact on male reproductive fitness . 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 phenotypes are the starting point for unraveling the mechanisms 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.
Supported by a grant from the National Science Foundation (PGRP 07-01880).
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