Key molecular and metabolic processes used for genetic engineering to improve freezing tolerance in cereals.

It has been estimated recently that cereals are harvested on 700 million hectares (Mha) worldwide (Dunwell, 2014), and also that, due to low temperature damage, worldwide losses in crop production amount to about US$2 billion each year (Sanghera et al., 2011). In spite of the urgent need for more coldor frost-tolerant cereal varieties, classical breeding programmes have shown limited progress in improving freezing tolerance (Thomashow, 1999). This lack of success is due mainly to the fact that the physiological process, i.e. the cold acclimation that leads to the development of freezing tolerance, is quite a complex quantitative trait. However, the deeper insight provided by different ‘omics’ technologies has made possible knowledge-based engineering of more stress-resistant plants; while the recent developments in cereal transformation methodology offer the technology to realize these aims. Since many recently published book chapters and reviews summarize our current knowledge on plant abiotic stress tolerance, this chapter focuses particularly on freezing tolerance, especially in cereals.

[1]  M. Saadalla BREEDING FOR DROUGHT TOLERANCE IN CEREALS : AN OVERVIEW , 2015 .

[2]  K. Kosová,et al.  Dynamics of cold acclimation and complex phytohormone responses in Triticum monococcum lines G3116 and DV92 differing in vernalization and frost tolerance level , 2014 .

[3]  Jim M. Dunwell,et al.  Transgenic cereals: Current status and future prospects , 2014 .

[4]  D. Livingston,et al.  Metabolic Changes in Avena sativa Crowns Recovering from Freezing , 2014, PloS one.

[5]  Jean-Benoît Charron,et al.  Comparative analysis of the cold acclimation and freezing tolerance capacities of seven diploid Brachypodium distachyon accessions , 2013, Annals of botany.

[6]  R. Vaňková,et al.  Redox control of plant growth and development. , 2013, Plant science : an international journal of experimental plant biology.

[7]  Taniya Dhillon,et al.  Hv-CBF2A overexpression in barley accelerates COR gene transcript accumulation and acquisition of freezing tolerance during cold acclimation , 2013, Plant Molecular Biology.

[8]  V. Hurry,et al.  Role of CBFs as Integrators of Chloroplast Redox, Phytochrome and Plant Hormone Signaling during Cold Acclimation , 2013, International journal of molecular sciences.

[9]  F. Locatelli,et al.  The OsMyb4 gene family: stress response and transcriptional auto-regulation mechanisms , 2013, Biologia Plantarum.

[10]  Wendy Harwood,et al.  Transgenic barley lines prove the involvement of TaCBF14 and TaCBF15 in the cold acclimation process and in frost tolerance , 2013, Journal of experimental botany.

[11]  Z. Bánfalvi,et al.  Hormones, NO, Antioxidants and Metabolites as Key Players in Plant Cold Acclimation , 2013 .

[12]  Midori Yoshida,et al.  Molecular Analysis of Fructan Metabolism Associated with Freezing Tolerance and Snow Mold Resistance of Winter Wheat , 2013 .

[13]  R. Bode Effects of Excitation Pressure on Variegation and Global Gene Expression in Arabidopsis thaliana , 2013 .

[14]  A. Katiyar,et al.  Genome-wide classification and expression analysis of MYB transcription factor families in rice and Arabidopsis , 2012, BMC Genomics.

[15]  D. Hincha,et al.  Clinal variation in the non-acclimated and cold-acclimated freezing tolerance of Arabidopsis thaliana accessions. , 2012, Plant, cell & environment.

[16]  Denis Gaudet,et al.  Carbohydrate profiling in seeds and seedlings of transgenic triticale modified in the expression of sucrose:sucrose-1-fructosyltransferase (1-SST) and sucrose:fructan-6-fructosyltransferase (6-SFT). , 2012, Journal of bioscience and bioengineering.

[17]  M. Thomashow,et al.  Photoperiodic regulation of the C-repeat binding factor (CBF) cold acclimation pathway and freezing tolerance in Arabidopsis thaliana , 2012, Proceedings of the National Academy of Sciences.

[18]  D. Hincha,et al.  Comparison of freezing tolerance, compatible solutes and polyamines in geographically diverse collections of Thellungiella sp. and Arabidopsis thaliana accessions , 2012, BMC Plant Biology.

[19]  K. Kosová,et al.  Complex phytohormone responses during the cold acclimation of two wheat cultivars differing in cold tolerance, winter Samanta and spring Sandra. , 2012, Journal of plant physiology.

[20]  K. Shinozaki,et al.  AP2/ERF family transcription factors in plant abiotic stress responses. , 2012, Biochimica et biophysica acta.

[21]  Jasbir Singh,et al.  The effects of phenotypic plasticity on photosynthetic performance in winter rye, winter wheat and Brassica napus. , 2012, Physiologia plantarum.

[22]  Luigi Cattivelli,et al.  The rice Osmyb4 gene enhances tolerance to frost and improves germination under unfavourable conditions in transgenic barley plants , 2012, Journal of Applied Genetics.

[23]  D. Ankerst,et al.  Association analysis of frost tolerance in rye using candidate genes and phenotypic data from controlled, semi-controlled, and field phenotyping platforms , 2011, BMC Plant Biology.

[24]  B. Fowler,et al.  Genome-wide gene expression analysis supports a developmental model of low temperature tolerance gene regulation in wheat (Triticum aestivum L.) , 2011, BMC Genomics.

[25]  M. Zhou,et al.  CBF-dependent signaling pathway: A key responder to low temperature stress in plants , 2011, Critical reviews in biotechnology.

[26]  S. Oliver,et al.  Transcriptome Analysis of the Vernalization Response in Barley (Hordeum vulgare) Seedlings , 2011, PloS one.

[27]  S. H. Wani,et al.  Engineering Cold Stress Tolerance in Crop Plants , 2011, Current genomics.

[28]  G. Galiba,et al.  Differential effects of cold acclimation and abscisic acid on free amino acid composition in wheat. , 2011, Plant science : an international journal of experimental plant biology.

[29]  V. Bajic,et al.  Supra-optimal expression of the cold-regulated OsMyb4 transcription factor in transgenic rice changes the complexity of transcriptional network with major effects on stress tolerance and panicle development. , 2010, Plant, cell & environment.

[30]  Lothar Willmitzer,et al.  Interaction with Diurnal and Circadian Regulation Results in Dynamic Metabolic and Transcriptional Changes during Cold Acclimation in Arabidopsis , 2010, PloS one.

[31]  M. Thomashow Molecular Basis of Plant Cold Acclimation: Insights Gained from Studying the CBF Cold Response Pathway1 , 2010, Plant Physiology.

[32]  T. Tammaru,et al.  Pathogen resistance in the moth Orgyia antiqua: direct influence of host plant dominates over the effects of individual condition , 2010, Bulletin of Entomological Research.

[33]  F. Guo,et al.  Overexpression of Arabidopsis CBF1 gene in transgenic tobacco alleviates photoinhibition of PSII and PSI during chilling stress under low irradiance. , 2010, Journal of plant physiology.

[34]  A. Savouré,et al.  Proline: a multifunctional amino acid. , 2010, Trends in plant science.

[35]  Ning Li,et al.  Over-expression of TsCBF1 gene confers improved drought tolerance in transgenic maize , 2010, Molecular Breeding.

[36]  A. Stella,et al.  Genetic variants of HvCbf14 are statistically associated with frost tolerance in a European germplasm collection of Hordeum vulgare , 2009, Theoretical and Applied Genetics.

[37]  C. Pozniak,et al.  Comparative expression of Cbf genes in the Triticeae under different acclimation induction temperatures , 2009, Molecular Genetics and Genomics.

[38]  D. Hincha,et al.  Fructan and its relationship to abiotic stress tolerance in plants , 2009, Cellular and Molecular Life Sciences.

[39]  K. Franklin Light and temperature signal crosstalk in plant development. , 2009, Current opinion in plant biology.

[40]  Ding-Geng Chen,et al.  Cbf genes of the Fr-A2 allele are differentially regulated between long-term cold acclimated crown tissue of freeze-resistant and – susceptible, winter wheat mutant lines , 2009, BMC Plant Biology.

[41]  P. Vítámvás,et al.  WCS120 protein family and frost tolerance during cold acclimation, deacclimation and reacclimation of winter wheat. , 2008, Plant physiology and biochemistry : PPB.

[42]  Elena Baldoni,et al.  Osmyb4 expression improves adaptive responses to drought and cold stress in transgenic apples , 2008, Plant Cell Reports.

[43]  P. Hedden,et al.  The Cold-Inducible CBF1 Factor–Dependent Signaling Pathway Modulates the Accumulation of the Growth-Repressing DELLA Proteins via Its Effect on Gibberellin Metabolism[W] , 2008, The Plant Cell Online.

[44]  M. Folling,et al.  Improved fructan accumulation in perennial ryegrass transformed with the onion fructosyltransferase genes 1-SST and 6G-FFT. , 2008, Journal of plant physiology.

[45]  D. Fowler,et al.  Cold Acclimation Threshold Induction Temperatures in Cereals , 2008 .

[46]  E. Stockinger,et al.  Identification of candidate CBF genes for the frost tolerance locus Fr-Am2 in Triticummonococcum , 2008, Plant Molecular Biology.

[47]  Yutaka Sato,et al.  Genetic engineering of rice capable of synthesizing fructans and enhancing chilling tolerance. , 2008, Journal of experimental botany.

[48]  S. Takumi,et al.  Increased freezing tolerance through up-regulation of downstream genes via the wheat CBF gene in transgenic tobacco. , 2008, Plant physiology and biochemistry : PPB.

[49]  Joachim Selbig,et al.  Metabolomics of temperature stress. , 2007, Physiologia plantarum.

[50]  G. Whitelam,et al.  Light-quality regulation of freezing tolerance in Arabidopsis thaliana , 2007, Nature Genetics.

[51]  C. A. Scapim,et al.  Stress-induced synthesis of proline confers tolerance to water deficit in transgenic wheat. , 2007, Journal of plant physiology.

[52]  S. Song,et al.  Expression of barley HvCBF4 enhances tolerance to abiotic stress in transgenic rice. , 2007, Plant biotechnology journal.

[53]  E. Stockinger,et al.  Fine mapping of a HvCBF gene cluster at the frost resistance locus Fr-H2 in barley , 2007, Theoretical and Applied Genetics.

[54]  Jianhua Zhu,et al.  Interplay between cold-responsive gene regulation, metabolism and RNA processing during plant cold acclimation. , 2007, Current opinion in plant biology.

[55]  N. Tuteja Abscisic Acid and Abiotic Stress Signaling , 2007, Plant signaling & behavior.

[56]  A. J. Cairns,et al.  Fructan in temperate forage grasses; agronomy, physiology, and molecular biology. , 2007 .

[57]  F. Sarhan,et al.  The CBF gene family in hexaploid wheat and its relationship to the phylogenetic complexity of cereal CBFs , 2007, Molecular Genetics and Genomics.

[58]  M. Iriti,et al.  The ectopic expression of the rice Osmyb4 gene in Arabidopsis increases tolerance to abiotic, environmental and biotic stresses , 2006 .

[59]  R. Chibbar,et al.  Identification of quantitative trait loci and associated candidate genes for low-temperature tolerance in cold-hardy winter wheat , 2006, Functional & Integrative Genomics.

[60]  J. Dubcovsky,et al.  A cluster of 11 CBF transcription factors is located at the frost tolerance locus Fr-Am2 in Triticum monococcum , 2006, Molecular Genetics and Genomics.

[61]  E. Stockinger,et al.  Mapping regulatory genes as candidates for cold and drought stress tolerance in barley , 2006, Theoretical and Applied Genetics.

[62]  E. Stockinger,et al.  Structural, Functional, and Phylogenetic Characterization of a Large CBF Gene Family in Barley , 2005, Plant Molecular Biology.

[63]  C. Vannini,et al.  Overexpression of Osmyb4 enhances compatible solute accumulation and increases stress tolerance of Arabidopsis thaliana , 2005 .

[64]  J. Dubcovsky,et al.  The expression of several Cbf genes at the Fr-A2 locus is linked to frost resistance in wheat , 2005, Molecular Genetics and Genomics.

[65]  K. Shinozaki,et al.  The effect of overexpression of two Brassica CBF/DREB1-like transcription factors on photosynthetic capacity and freezing tolerance in Brassica napus. , 2005, Plant & cell physiology.

[66]  Doug Heath,et al.  A global reorganization of the metabolome in Arabidopsis during cold acclimation is revealed by metabolic fingerprinting , 2005 .

[67]  G. Perrotta,et al.  Large scale analysis of transcripts abundance in barley subjected to several single and combined abiotic stress conditions , 2004 .

[68]  Oliver Fiehn,et al.  A prominent role for the CBF cold response pathway in configuring the low-temperature metabolome of Arabidopsis. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[69]  Toshihiko Yamada,et al.  Transgenic perennial ryegrass plants expressing wheat fructosyltransferase genes accumulate increased amounts of fructan and acquire increased tolerance on a cellular level to freezing , 2004 .

[70]  M. Uemura,et al.  Solute accumulation in heat seedlings during cold acclimation: contribution to increased freezing tolerance. , 2004, Cryo letters.

[71]  R. Pearce Adaptation of Higher Plants to Freezing , 2004 .

[72]  V. Rai Role of Amino Acids in Plant Responses to Stresses , 2002, Biologia Plantarum.

[73]  F. Kaplan,et al.  Exploring the Temperature-Stress Metabolome of Arabidopsis , 2004 .

[74]  D. Djilianov,et al.  Transgenic tobacco plants accumulating osmolytes show reduced oxidative damage under freezing stress. , 2004, Plant physiology and biochemistry : PPB.

[75]  C. Vannini,et al.  Overexpression of the rice Osmyb4 gene increases chilling and freezing tolerance of Arabidopsis thaliana plants. , 2004, The Plant journal : for cell and molecular biology.

[76]  J. Dubcovsky,et al.  The cold-regulated transcriptional activator Cbf3 is linked to the frost-tolerance locus Fr-A2 on wheat chromosome 5A , 2003, Molecular Genetics and Genomics.

[77]  Mark Stitt,et al.  A plant for all seasons: alterations in photosynthetic carbon metabolism during cold acclimation in Arabidopsis. , 2002, Current opinion in plant biology.

[78]  Midori Yoshida,et al.  Molecular Characterization of Sucrose:Sucrose 1-Fructosyltransferase and Sucrose:Fructan 6-Fructosyltransferase Associated with Fructan Accumulation in Winter Wheat during Cold Hardening , 2002, Bioscience, biotechnology, and biochemistry.

[79]  V. Hurry,et al.  Susceptibility to low‐temperature photoinhibition and the acquisition of freezing tolerance in winter and spring wheat: The role of growth temperature and irradiance , 2001 .

[80]  M. Thomashow,et al.  Components of the Arabidopsis C-repeat/dehydration-responsive element binding factor cold-response pathway are conserved in Brassica napus and other plant species. , 2001, Plant physiology.

[81]  K. Shinozaki,et al.  Antisense suppression of proline degradation improves tolerance to freezing and salinity in Arabidopsis thaliana , 1999, FEBS letters.

[82]  G. Galiba,et al.  Frost hardiness depending on carbohydrate changes during cold acclimation in wheat , 1999 .

[83]  Michael F. Thomashow,et al.  PLANT COLD ACCLIMATION: Freezing Tolerance Genes and Regulatory Mechanisms. , 1999, Annual review of plant physiology and plant molecular biology.

[84]  G. Öquist,et al.  Energy balance and acclimation to light and cold , 1998 .

[85]  J. Snape,et al.  Location of a gene regulating cold-induced carbohydrate production on chromosome 5A of wheat , 1997, Theoretical and Applied Genetics.

[86]  A. Ivanov,et al.  Photosystem II Excitation Pressure and Development of Resistance to Photoinhibition (II. Adjustment of Photosynthetic Capacity in Winter Wheat and Winter Rye) , 1996, Plant physiology.

[87]  V. Hurry,et al.  Cold Hardening of Spring and Winter Wheat and Rape Results in Differential Effects on Growth, Carbon Metabolism, and Carbohydrate Content , 1995, Plant physiology.

[88]  R. Tuberosa,et al.  Involvement of Chromosomes 5A and 5D in Cold‐Induced Abscisic Acid Accumulation in and Frost Tolerance of Wheat Calli , 1993 .

[89]  V. Hurry,et al.  Low-Temperature Effects on Photosynthesis and Correlation with Freezing Tolerance in Spring and Winter Cultivars of Wheat and Rye , 1993, Plant physiology.

[90]  C. R. Olien,et al.  Changes in Soluble Carbohydrate Composition of Barley, Wheat, and Rye during Winter , 1993 .

[91]  S. Schulenburg,et al.  Abscisic acid and proline levels in cold hardened winter wheat leaves in relation to variety-specific differences in freezing resistance , 1990 .

[92]  M. Crespi,et al.  Sucrose and fructan metabolism of different wheat cultivars at chilling temperatures , 1990 .

[93]  J. Krekule,et al.  Levels of ethylene, ACC, MACC, ABA and proline as indicators of cold hardening and frost resistance in winter wheat , 1989 .

[94]  E. Jacobsen,et al.  Effect of cold hardening, wilting and exogenously applied proline on leaf proline content and frost tolerance of several genotypes of Solanum , 1985 .

[95]  G. Yelenosky Accumulation of Free Proline in Citrus Leaves during Cold Hardening of Young Trees in Controlled Temperature Regimes. , 1979, Plant physiology.