Plant strategies for survival in changing environment
Article first published online: 21 NOV 2012
Copyright © Physiologia Plantarum 2012
Special Issue: Abiotic Stress
Volume 147, Issue 1, pages 1–3, January 2013
How to Cite
Uemura, M. and Hausman, J.-F. (2013), Plant strategies for survival in changing environment. Physiologia Plantarum, 147: 1–3. doi: 10.1111/ppl.12004
- Issue published online: 17 DEC 2012
- Article first published online: 21 NOV 2012
- Manuscript Received: 5 NOV 2012
- Manuscript Accepted: 5 NOV 2012
From summer to fall, one of the most thrilling experiences for people who live close to the Arctic Circle is the quick changes in day-length and temperature. The day-length can shorten by 10 min or more every day and the temperature can drop suddenly (even to subzero degrees in August) with a swift change in the weather – from the cloudless azure sky to heavy snow fall.
Being immobile, plants stay outside however cold and dark it gets. How do they survive the winters with freezing temperatures that can go down to −40°C or even lower? Plants have evolved very clever and fascinating adaptive mechanisms, collectively referred to as ‘cold acclimation’. This interesting phenomenon has been intensively studied and the results of this research have been applied to improve the adaptability of crops to non-optimum growth temperatures.
The mechanisms plants use to survive at freezing temperatures vary greatly depending on plant species and, in some cases, the particular tissues/organs that are exposed to freezing (Levitt 1980, Sakai and Larcher 1987, Fujikawa et al. 2009). The majority of herbaceous plants, including many important crops (e.g. wheat, barley and rye) and vegetables (e.g., spinach, cabbage and turnip), tolerate freezing by a mechanism called ‘extracellular freezing’. In extracellular freezing, ice formation occurs in the extracellular spaces of the plant tissues and intracellular water is absorbed at the surface of extracellular ice crystals due to differences in the chemical potential between ice and water at subzero temperatures. For flower and leaf buds of many woody plants, ‘extraorgan freezing’ is observed in which ice crystals form outside of the organ (e.g. in the scale and other outer parts of the bud) and water inside the bud moves out to the place where ice crystals are formed. Another mechanism used by plants to survive at freezing temperatures is ‘deep supercooling’, which can be found in specialized tissues of plants such as ray parenchyma cells in woody plants. Deep supercooling is not accompanied by the movement of water from one place to another, which is very different from the other two mechanisms adopted by plants at freezing temperatures. Thus, plants have evolved complex strategies for survival at freezing temperatures, and researchers have been attempting to understand why these different mechanisms have evolved and how they provide the different plant species with specific selective advantages under freezing conditions.
To survive at freezing temperatures, plants start preparing themselves as early as the late summer or early fall (Guy et al. 2008). They may alter both their overall structure and macromolecular components considerably during cold acclimation. The cold-induced synthesis of specific compounds helps to stabilize complex components within cells; including membranes, proteins and nucleic acids. The increase of osmotic concentrations in cells due to the accumulation of cellular substances prevents water from freezing at subzero temperatures, which also keeps complex cellular components intact. In addition, plants strictly control the biosynthesis of compounds to regulate ice formation in tissues (such as ice-nucleating and antifreeze compounds). Another noticeable change that occurs in plant cells preparing for winter survival are changes in membrane compositions and to membrane function in order to maintain cellular reactions at freezing temperatures (Uemura et al. 2006). Plant membranes, specifically the plasma membrane which is the primary site of freezing injury, significantly and actively change their composition from late summer to autumn. As a whole, these changes result in protection against dehydration, oxidative damage and other stresses imposed at freezing temperatures.
How then do these changes in protein, lipid and metabolite composition result in increased freezing tolerance and help plants survive severe winters? With the rapid advances in plant genomics research in recent years, very fundamental knowledge of the responds of plants to cold (and shortening day-length) has become available (Thomashow 2010, Qin et al. 2011). The complete decoding of the genome sequences of several plant species, in addition to the subsequent bioinformatics and gene expression analyses, gives us a large amount of information on plant responses to environmental stimuli. Phenotypic responses of plants to cold seem to be genetically regulated in a tight and sophisticated way. Several independent and cross-talking pathways contribute to adaptation of plants to tolerate winter conditions (such as soluble compound accumulation and membrane changes described above). One group of master genes involved in plant survival during winter is the C-repeat binding factor/dehydration-responsive element binding factor (CBF/DREB) family of transcription factors that regulate a number of downstream target genes and cellular acclimation processes in response to exposure to low temperatures. We now know that in several plant species, overexpression of CBF/DREB transcription factors by gene transformation techniques results in a significant increase in their freezing tolerance as well as tolerance to other environmental stresses such as dehydration and salinity stresses. This means that when molecular aspects of cold adaptation are further elucidated, a wider range of applications will become available to improve plant performance under severe stressful conditions.
Researchers studying plant stress responses are now facing to a new challenge. There is no longer any doubt that changes are occurring to the global climate, but the direction and significance of the changes are not predictable. For example, global temperatures in general have been increasing over the last 100 years or so, but this does not mean that the temperatures are increasing in a uniform way in every corner of the globe. Sudden drops of temperature, unexpectedly early arrival of winter following an unusually warm fall, and a very late frost just after bud break of fruit trees in spring have been reported in various places of the world. For plants to survive in such unpredictable and unprecedented conditions they have to be equipped with specific mechanisms to protect themselves. That can happen as a result of natural selection in a time scale of evolution. But the invisible hand of nature may not work fast enough this time if we are to leave a sound environment for the generations to come. That is the new challenge for the study of plant stress responses. More studies are needed and the results must be shared among those involved in this research field.
In summer 2011, we were fortunate to have two conferences dedicated to sharing the newest knowledge on the plasticity of plant adaptation, providing focal points for discussing the best ways to develop research programs to further our understanding. One was the ninth International Plant Cold Hardiness Seminar (IPCHS), which was held for 6 days in Luxembourg, Luxembourg. Since 1977 when the first IPCHS was held, we have witnessed the development of new technologies in the area of molecular biology, genomics, proteomics and metabolomics; developments that have impacted our understanding of plant cold hardiness. The ninth IPCHS focused on how plants perceive cold signals, how genes are involved in cold acclimation, what the mechanisms are to control expression of these ‘cold-regulated’ genes and how we can improve the cold hardiness of plants by new techniques and had two sessions entitled ‘cellular responses to low temperature’ and ‘genetic adaptations of plants to cold’. All these advances have provided the opportunity to re-explore and better understand the physiology of cold tolerance, avoidance and acclimation in plants. This special issue on plant abiotic stress adaptation collected six papers from the ninth IPCHS (Castonguay et al. 2013, Crosatti et al. 2013, Gusta and Wisniewski 2013, Neuner et al. 2013, Pagter and Arora 2013, Tanino et al. 2013).
The second meeting was a 1-day Japan-Scandinavia Colloquium on ‘abiotic stress from genes to biosphere’ sponsored by the Japan Society for the Promotion of Science, held in Stavanger, Norway as a pre-conference meeting of the Scandinavian Plant Physiology Society bi-annual meeting. The Colloquium intended to serve as a basis for further understanding of plant adaptability to the changing environment and contribute to mitigating the adverse effects of the human-induced climate change on plants and in turn non-plant organisms. This special issue collected four papers from the Colloquium (Begum et al. 2013, Fujita et al. 2013, Rahman 2013, Ursache et al. 2013).
Our journey to understand how plants maintain their life at freezing temperatures in a changing world still continues and we need new, effective means to step up to a new stage of our research. This issue collects a total of 10 papers from these two exciting conferences, and we sincerely hope that readers can gain insight into the current understanding of how plants respond to freezing temperatures and in which directions future research will take to further our understanding of plant behavior under adverse growth conditions, extending our knowledge to the practical world.
- 2013) Regulation of cambial activity in relation to environmental conditions: understanding the role of temperature in wood formation of trees. Physiol Plant 147: 46–54 , , , , (
- 2013) Molecular physiology and breeding at the crossroads of cold hardiness improvement. Physiol Plant 147: 64–74 , , , , , (
- 2013) Harden the chloroplast to protect the plant. Physiol Plant 147: 55–63 , , , , (
- 2009) Factors related to change of deep supercooling capability in xylem parenchyma cells of trees. In: Gusta LV, Wisniewski ME, Tanino KK (eds) Plant Cold Hardiness from the Laboratory to the Field. CABI Press, Wallingford, pp 29–42 , , , (
- 2013) Pivotal role of the AREB/ABF-SnRK2 pathway in ABRE-mediated transcription in response to osmotic stress in plants. Physiol Plant 147: 15–27 , , (
- 2013) Understanding plant cold hardiness: an opinion. Physiol Plant 147: 4–14 , (
- 2008) Metabolomics of temperature stress. Physiol Plant 132: 220–235 , , , , (
- 1980) Reponses of Plants to Environmental Stresses, 2nd Edn, Vol. 1. Academic Press, New York (
- 2013) Frost resistance of reproductive tissues during various stages of development in high-mountain plants. Physiol Plant 147: 88–100 , , , , (
- 2013) Winter-survival and deacclimation of perennials under warming climate: physiological perspectives. Physiol Plant 147: 75–87 , (
- 2011) Achievements and challenges in understanding plant abiotic stress responses and tolerance. Plant Cell Physiol 52: 1569–1582 , , (
- 2013) Auxin: a regulator of cold stress response. Physiol Plant 147: 28–35 (
- 1987) Frost Survival of Plants: Responses and Adaptation to Freezing Stress. Springer-Verlag, Berlin , (
- 2013) Allium fistulosum as a novel system to investigate mechanisms of freezing resistance. Physiol Plant 147: 101–111 , , , , , , , , , , , (
- 2010) Molecular basis of plant cold acclimation: insights gained from studying the CBF cold response pathway. Plant Physiol 154: 571–577 (
- 2006) Responses of the plasma membrane to low temperatures. Physiol Plant 126: 81–89 , , , , , (
- 2013) Genetic and hormonal regulation of cambial development. Physiol Plant 147: 36–45 , , (