A special issue in memory of Dr Marilyn Griffith
Plant cold and abiotic stress gets hot*
Article first published online: 16 JAN 2006
Volume 126, Issue 1, pages 1–4, January 2006
How to Cite
Guy, C., Porat, R. and Hurry, V. (2006), Plant cold and abiotic stress gets hot. Physiologia Plantarum, 126: 1–4. doi: 10.1111/j.1399-3054.2006.00628.x
- Issue published online: 16 JAN 2006
- Article first published online: 16 JAN 2006
Since the dawn of agriculture, farmers have fought an ongoing battle to protect their crops against the elements. While the first farmers struggled with few tools at their disposal to protect the precious harvest that was necessary for their day-to-day survival, today's farmers have many more tools to turn to in their efforts to protect their crops, which are now more important for economic survival than for the farmers' life or death existence.
Over the past 45 years, farmers have increased food production at a rate that has more than kept pace with the expanding human population. By 1990, farmers worldwide were able to produce enough food to theoretically provide every human with nearly 4000 calories per day, which was substantially greater than that estimated in 1961 (Bender 1997). However, if the world population does increase, as predicted, to approximately 9 billion by 2050 (Anonymous 2003), then to maintain the status quo of 1990, world food production will need to rise by approximately 70%.
This dramatic and sustained increase in demand for food production will need to be achieved at a time when world agriculture faces the new challenge of global climate change. It is thought that global climate change will begin to have a profound effect on food production around the world during the 21st century, leading to famine in some regions but additional wealth in others. Recent assessments suggest that global climate change will increase crop yields at high and mid-latitudes where temperatures will be more favourable and growing seasons longer (Parry et al. 2003). Increases may be greatest in North America and China, where rainfall and environmental conditions are predicted to be more favourable. In contrast, increased abiotic stress and evaporation of moisture from soils could reduce yields in lower latitudes – where food shortages are already chronic and predicted population growth rates may be greatest. Studies single out Africa as likely to suffer the greatest yield reductions, with up to 70 million more people at risk of hunger (Parry et al. 2003). A prediction of special concern within the climate change paradigm is that the effects of subzero temperatures at times of year that are mistimed or abnormal can cause physiological consequences for sensitive parts of indigenous plants such as flower buds, ovaries and leaves leading to a potential loss of sexual reproduction that can have long-lasting effects on the demography of annuals as well as long-lived perennials (Inouye 2000). Thus, short-term negative effects of unseasonable frosts and freezes may lead to longer-term benefits through lowered populations of seed predators, but may also have dramatic consequences for herbivores, even causing local extinctions. Thus, such ill-timed frosts may cause local extinctions and influence the geographical distribution of many local plants and animal species (Inouye 2000). While the potential for global climate change to influence the frequency and distribution of subzero temperature events remains uncertain, it is considered likely that frost and freezes may become more frequent in some areas and less frequent in others creating both windfalls and challenges for agriculture and the natural flora and fauna.
Part of the solution to meet the challenges of nourishing a growing human population in an era of global climate change may emanate from the natural abilities of plants to cope with unfavourable environmental conditions. During the course of evolution, plants have acquired an array of coping and defensive strategies to minimize the deleterious effects of unfavourable environmental conditions. Nevertheless, environmental conditions during crop growth and development exact a significant toll on the inherent genetic potential of crop plants for maximum yield. Boyer (1982) in a classic study made a comparison of the record yields and the average yields for many crop plants and found that most of the time crop plants were reaching only about 20% of their genetic potential for yield. While such yield reductions could be attributed to several biotic categories: disease, insect and weeds, the major diminution in yield resulted from abiotic stresses. Therefore, improving cold and abiotic stress tolerance of crop plants could significantly contribute to yield increases towards the 70% predicted to meet population growth requirements.
In Memory of Dr Marilyn Griffith
Naturally, cold stress has profound impacts on agricultural practices and production on an annual basis contributing to significant economic losses worldwide. This special issue on Cold and Abiotic Stress is an effort to bring together a collection of minireviews with a major focus on recent advancements and developing technologies to study plant cold and abiotic stress. However, this special issue is not just about a journey into the frontiers of plant cold and abiotic stress research, but a commemoration and recognition of Dr Marilyn Griffith's journey during a scientific career as professor, researcher, colleague and friend in the field of plant environmental stress research particularly with respect to freezing stress.
Marilyn was a faculty member of the Department of Biology at the University of Waterloo from 1987 until she passed away 21 February, 2005. She was also a member of the editorial board of Physiologia Plantarum serving as an editor and subject editor. As a plant biologist, she wanted to understand how plants function. Specifically, she wanted to know how plants survive winter and, in particular, freezing and thawing. Apparently, Marilyn's inquisitiveness with plants harkened back to her childhood in rural Massachusetts, where a neighbour's interest in gardening and plant taxonomy sparked her fascination in plants (Daily Bulletin 2005). She would earn a Master's degree at the Yale School of Forestry and Environmental Studies and come to understand that environmental stresses were major limiting factors of plant productivity. Marilyn went on to the University of Minnesota for a PhD where she explored the freezing tolerance of winter rye. At Minnesota, Marilyn met and worked with Dr Norm Huner. They would become long-term collaborators and life-long friends. After postdoctoral training, and as a member of the faculty at the University of Alaska, Marilyn moved to the University of Waterloo. It is there that Marilyn's laboratory began to characterize plant antifreeze proteins (Moffatt et al. 2006). Later she would say, ‘People used to think that plants freeze because it's cold.' What she and colleagues have shown is that plants control their freezing by producing ice nucleators which initiate the freezing process that allows freezing to take place in intercellular spaces. Then antifreeze proteins interact directly with ice in planta and reduce freezing injury by slowing the growth and recrystallization of ice (Moffatt et al. 2006). In her scientific journey, Marilyn would become widely recognized for her work with plant antifreeze proteins. Perhaps, the pinnacle of Marilyn's professional journey may have occurred in 2003 when she was named a Killam Research Fellow. With her passing, the journey into understanding how plants function and how they survive freezing and thawing will not end but continue onward in laboratories all around the world.
Special Issue Papers
This special issue with 12 review articles on abiotic stress is focused with a major emphasis on cold stress in memory of Marilyn Griffith. The fascinating perspective by Moffatt et al. (2006) discusses the scientific contributions made by Dr Griffith and colleagues as a historical recap and then outlines the latest findings and ideas of how plant antifreeze proteins function in ice binding as part of a mechanism that acts to control in planta freezing and recrystalization processes. Reviews by Murata and Los (2006), Ensminger et al. (2006) and Suzuki and Mittler (2006) examine different biochemical and physiological possibilities that could be important in sensing and signalling cold stress or the consequences of low temperatures on cellular processes. Using Synechocystis as a model photosynthetic organism and taking a global mutagenesis approach to the genome complement of histidine kinases and their cognate response regulators, Murata and Los describe efforts aimed at identifying a primary or early sensor that initiates low temperature perception and signalling. Similarly, in the photosynthetic cells and organs of higher plants, there is a need to integrate and regulate light energy harvesting with energy consumption in response to changing environmental conditions. Ensminger et al. (2006) outline reasons why it is important to maintain proper balance between energy harvesting and energy consumption and explain why sensing the balance as a function of the redox status of photosynthesis could be an important signalling mechanism especially during cold stress. Failure to maintain proper balance in processes like photosynthesis can have deleterious consequences. It is generally accepted that abiotic stress can lead to the production of reactive oxygen species (ROS). The review of Suzuki and Mittler (2006) discusses the role of ROS in plant sensing and signalling mechanisms in relation to temperature stress and highlights reasons why maintaining or controlling the levels of ROS is critical to prevent adverse consequences.
Once the stress condition has been perceived, and signal transduction has been activated, downstream genes involved in response and tolerance mechanisms become activated. Three reviews by Chinnusamy et al. (2006), Nakashima and Yamaguchi-Shinozaki (2006) and Van Buskirk and Thomashow (2006) are focused on the regulation of gene expression in response to cold and other abiotic stresses. Together, these three articles provide a comprehensive overview of the state of the field in regulating gene expression during cold, osmotic and salt stress. Chinnusamy et al. (2006) provide an examination of cold sensing and signalling, second messengers and then delve into regulation of downstream genes by transcription factors and post-transcriptional processes. Nakashima and Yamaguchi-Shinozaki (2006) focus on transcriptional regulation of downstream genes, and the mechanisms involved in osmotic and cold stress responsive gene expression, including crosstalk that acts to control gene expression. The review by Van Buskirk and Thomashow (2006) initially focuses on the CBF/DREB1 cold response pathway in plants but then introduces additional cold response regulatory pathways associated with cold acclimation. Together, these three papers outline many of the new key advances regarding differential gene expression in response to cold and related abiotic stresses and highlight new and emerging topics for future research endeavours.
A second theme of this special issue is the application of global, genomic-scale or profiling technologies in the study of cold-stress responses of plants, along with transcriptome profiling that has already helped pioneer new understanding about differential gene expression and helped to delimit gene inventories of stress-related regulons (Chinnusamy et al. 2006, Ensminger et al. 2006, Murata and Los 2006, Nakashima and Yamaguchi-Shinozaki 2006, Van Buskirk and Thomashow 2006, Suzuki and Mittler 2006). Reviews by Uemura et al. (2006), Wang et al. (2006), Renaut et al. (2006) and de la Fuente van Bentem et al. (2006) focus on research advances and different technologies that involve proteomics of the plasma membrane or whole cells (Renaut et al. 2006, Uemura et al. 2006), lipid profiling of the plasma membrane and whole cells (Uemura et al. 2006, Wang et al. 2006) and the newly developing field of phosphoproteomics (de la Fuente van Bentem et al. 2006). As research on cold and abiotic stresses over the past 20 years has revealed amazing levels of complexity in signalling, regulation and tolerance mechanisms, it has become ever more clear that robust approaches able to uncover global responses are necessary to sort out the key events, players and processes in stress responses. Focusing on what is considered to be the primary site of freezing injury, the plasma membrane, Uemura et al. (2006) describe studies that employ lipid profiling and proteomic approaches to understand the dynamics of changes that occur during acclimation and freezing. Similarly, Wang et al. (2006) describe the use and the value of a wide-scale lipidomics approach to delving into the consequences of low temperature acclimation and stress on plant membranes. On a larger scale, the minireview by Renaut et al. (2006) demonstrates the power of using proteomics to understand the protein dynamics during cold acclimation in woody species. They show that many of the proteins whose abundance of changes during cold acclimation are those that have already been identified through gene expression studies. Ideally and perhaps necessarily, having information about sensing, signalling, genic content, regulation of gene expression, protein dynamics and now post-translational regulatory control of protein and enzymatic function will all help in the quest to know and understand stress responses and tolerance mechanisms. The minireview by de la Fuente van Bentem et al. (2006) outlines an exciting new omics approach to study phosphoprotein dynamics in response to stress situations that is certain to reveal important new insights regarding post-translational regulatory mechanisms of plants.
The last minireview by Kaplan et al. (2006) comes full circle in that from the global omics approaches come vast amounts of information about genes, RNAs, proteins, lipids and metabolism. The minireview by Kaplan et al. (2006) delves into the function of a specific gene, β-amylase, that has been linked with cold stress responses in a variety of transcriptome studies dealing with cold and temperature stress. They show how complexity even within a single-gene family must be factored into the overall understanding of plant responses to cold and abiotic stresses.
Together, it is our hope that this special issue will provide readers an enhanced understanding of the state of the art in the field of cold and abiotic stress, and that it will help to advance our common journey to understand how plants function and survive unfavourable temperature and abiotic factor conditions.
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