ReviewMolecular mechanisms underlying frost tolerance in perennial grasses adapted to cold climates
Introduction
Plants in cold climates are frequently exposed to sub-zero temperatures in the autumn, winter, and spring seasons. Exposure to sub-zero temperatures requires a battery of molecular and physiological adaptations to minimize frost related injuries which potentially can be fatal. Cold acclimation (CA) is a process whereby plants in response to low but non-freezing temperatures undergo a range of biological changes in order to increase their frost tolerance (FT) and prepare for the winter season [1]. The process of CA encompasses biological modifications on many levels, e.g. modulation of gene expression levels [2], accumulation and degradation of proteins [3], [4], [5] changes in sugar content [6], and changes in the photosynthetic machinery [7].
A large part of the research concerning plant cold stress response and FT has been carried out using the model species, Arabidopsis thaliana (named herein as Arabidopsis) and Oryza sativa (rice) [1]. As a consequence, the research on low-temperature stress responses in non-model species has focussed on genetic mechanisms, which originally were identified in the model species and have been conserved between plant lineages over hundreds of millions of years. In many cases a direct inference of gene function based on homology between model dicot plants and agriculturally important species is elusive. Moreover, neither Arabidopsis nor rice is adapted to a perennial life in extreme winter climates. This is important because adaptation to a perennial life history in harsh winter climates must have required changes at the genetic level which cannot be studied using an annual model species. Hence if we only use model plant species to investigate the molecular basis of cold and frost stress response this might provide limited insights into the genetic mechanisms underlying these traits in important agricultural species.
The Pooideae grasses (temperate grasses) is a large and economically important sub-family including cereals (Triticeae tribe) and forage grasses (Poaeae tribe). Divergence of temperate grasses from the most recent common ancestor shared with rice is thought to have happened ∼46–42 million years ago (Mya) [8], [9]. Parallel to the origin and early evolution of the Pooideae group the global climate became gradually cooler [10]. As opposed to rice, which is adapted to warm and humid environments, Pooideae grasses radiated in cooler environments [11]. This is reflected by the present distribution of Pooideae species which is extremely skewed towards cooler environments [12]. Thus evolution of cold and frost stress responses, either through fine tuning of ancient abiotic stress responses or evolution of novel adaptations to cold environments must have been central for the Pooideae sub-family.
The evolutionary history of temperate grasses makes them an excellent model system for studying adaptations to cold and frost stress. During the last decade several research groups have focussed their research on understanding the cold and freezing stress responses in forage grass species (Poeae tribe), mainly Lolium and Festuca species, and recently also Phleum pratense L. Species of the Poeae tribe are excellent models for plant adaptations to cold environment because of their adaptation to habitats in the northernmost part of the Northern hemisphere, i.e. the circumpolar arctic region. The research on the Poeae species includes mapping of quantitative trait loci (QTL), transcriptomics, proteomics, and functional gene studies, and plant physiology research of low-temperature (CA) response and FT. We do not intend for this review to serve as an elaborate review of every aspect of CA and FT but aim to summarize the progress in CA and FT research on forage grasses from the past decade. We will start by highlighting results from studies at the -omics level, and then focus on three specific mechanisms involved in CA and FT where research performed on forage grasses has made significant contributions; (1) photoinhibition, (2) ice interacting proteins, and (3) fructan synthesis.
Section snippets
QTL mapping and genomics
Winter survival (WS) is a very complex trait determined by combinations of frost, desiccation, water logging, ice-encasement, anoxia, and snow cover. However, FT is the single component that generally explains most of the variation in WS [13]. There are few reports of Quantitative Trait Locus (QTL) mapping of FT and WS in forage grass species. Mapping of frost and drought tolerance QTLs using regrowth tests, and WS QTLs based on field survival, in the ‘B14/16 × HF2/7’ full-sib family of meadow
Transcriptomics of cold acclimation and frost tolerance
Comprehensive research on transcriptional modulation during CA has been carried out in Arabidopsis using different microarray technologies and different statistical criteria. These studies have estimated the number of Arabidopsis genes being regulated by CA to be in the order of 2–13% [31], [32], [33], [34]. Recently, CA transcriptional responses have also been investigated in cold tolerant Pooideae species such as winter and spring wheat (Triticum aestivum) cultivars [35], [36], barley (H.
Frost tolerance and proteomics
Even though there is a hierarchical, and to some extent deterministic, relationship between the transcriptome and the proteome response, gene expression levels and protein levels are in many cases not strictly correlated (e.g. [42]). Hence, genome-wide transcription analyses do not offer the complete picture of plant molecular responses during CA and cold stress. It is therefore important to complement gene expression studies with studies of proteomic changes under CA and investigate how
Photoinhibition avoidance in cold and freezing tolerance
Photoinhibition is the process whereby light energy absorbed in the photosynthetic light processes exceeds energy demand of the dark processes which leads to PSII over-reduction and subsequent inhibition of the photosynthetic capacity (Fig. 1). This can result not only in destruction of the photosynthetic apparatus but also to damage of whole cells due to production of reactive oxygen species accompanying PSII over-reduction [58]. Under low temperatures in winter and spring, the photosynthetic
Pooideae lineage specific genes: ice interacting proteins and fructan metabolism
Several gene families, or sub-classes of gene families, are known to be lineage specific for the Pooideae grasses, for example sub-clades of the CBF-transcription factor family [72], the fructocyl transferase (FST) gene family [73], and one Pooideae-specific ice re-crystalization inhibition protein coding gene family [9]. It has been speculated if these Pooideae-specific gene family expansions have been important for adaptation of a common Pooideae ancestor to cold climates and subsequently
Concluding remarks
Perennial forage grasses are essential elements of sustainable and multifunctional farming systems providing both feed for ruminants and ecosystem services, e.g. carbon sequestration, soil formation and protection, nutrient cycling, and aesthetic landscape values. This is especially the case in high-latitude and high-altitude temperate regions where perennial grasses make up a very large part of the agricultural land. Climate changes are predicted to give more unpredictable and unstable winter
References (104)
- 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
Plant Sci.
(2004) - et al.
Molecular responses to dehydration and low temperature: differences and cross-talk between two stress signaling pathways
Curr. Opin. Plant Biol.
(2000) Updating the ‘crop circles’
Curr. Opin. Plant Biol.
(2005)- et al.
Identification of genes associated with cold acclimation in perennial ryegrass
J. Plant Physiol.
(2009) - et al.
Chilling stress-induced proteomic changes in rice roots
J. Plant Physiol.
(2009) - et al.
Comparative proteomic analysis provides new insights into chilling stress responses in rice
Mol. Cell. Proteom.
(2006) - et al.
WCS120 protein family and proteins soluble upon boiling in cold-acclimated winter wheat
J. Plant Physiol.
(2007) - et al.
How do environmental stresses accelerate photoinhibition?
Trends Plant Sci.
(2008) - et al.
Regulatory genes involved in the determination of frost tolerance in temperate cereals
Plant Sci.
(2009) - et al.
Antifreeze proteins in overwintering plants: a tale of two activities
Trends Plant Sci.
(2004)
Characterization of a family of ice-active proteins from the ryegrass, Lolium perenne
Cryobiology
A theoretical model of a plant antifreeze protein from lolium perenne
Biophys. J.
Identification of the ice-binding face of a plant antifreeze protein
FEBS Lett.
Fructans interact strongly with model membranes
Biochim. Biophys. Acta (BBA) – Biomemb.
Fructans insert between the headgroups of phospholipids
Biochim. Biophys. Acta (BBA) – Biomemb.
Plant cold acclimation: freezing tolerance genes and regulatory mechanisms
Annu. Rev. Plant Physiol. Plant Mol. Biol.
Low temperature regulation of the Arabidopsis CBF family of AP2 transcriptional activators as an early step in cold-induced COR gene expression
Plant J.
Cold acclimation and freezing stress tolerance: role of protein metabolism
Annu. Rev. Plant Physiol. Plant Mol. Biol.
Identification of leaf proteins differentially accumulated during cold acclimation between Festuca pratensis plants with distinct levels of frost tolerance
J. Exp. Bot.
The effects of cold acclimation on photosynthetic apparatus and the expression of COR14b in four genotypes of barley (Hordeum vulgare) contrasting in their tolerance to freezing and high-light treatment in cold conditions
Ann. Bot.
Evolutionary dynamics of grass genomes
New Phytol.
Tracking the evolution of a cold stress associated gene family in cold tolerant grasses
BMC Evol. Biol.
Trends, rhythms, and aberrations in global climate 65 Ma to present
Science
Phylogeny and subfamilial classification of the grasses (Poaceae)
Ann. Mo. Bot. Gard.
Studies on the origin, evolution, and distribution of the gramineae. V. The subfamily Festucoideae
Aust. J. Bot.
Development and Evaluation of laboratory Testing Methods for Winterhardiness Breeding
RFLP mapping of the vernalization (Vrn1) and frost resistance (Fr1) genes on chromosome 5A of wheat
TAG Theor. Appl. Genet.
The cold-regulated transcriptional activator Cbf3 is linked to the frost-tolerance locus Fr-A2 on wheat chromosome 5A
Mol. Genet. Genom.
Quantitative trait loci controlling vernalisation requirement, heading time and number of panicles in meadow fescue (Festuca pratensis Huds.)
TAG Theor. Appl. Genet.
Developmental traits affecting low-temperature tolerance response in near-isogenic lines for the vernalization locus Vrn-A1 in wheat (Triticum aestivum L. em Thell)
Ann. Bot.
Regulation of freezing tolerance and flowering in temperate cereals: the VRN-1 connection
Plant Physiol.
QTL analysis of morphological, developmental, and winter hardiness-associated traits in perennial ryegrass
Crop Sci.
Identification of quantitative trait loci controlling winter hardiness in an annual × perennial ryegrass interspesific hybrid population
Mol. Breed.
Fine mapping of a Hv CBF gene cluster at the frost resistance locus Fr-H2 in barley
TAG Theor. Appl. Genet.
Mapping of barley homologs to genes that regulate low temperature tolerance in Arabidopsis
TAG Theor. Appl. Genet.
A cluster of 11 CBF transcription factors is located at the frost tolerance locus Fr-A m 2 in Triticum monococcum
Mol. Genet. Genom.
A perennial ryegrass CBF gene cluster is located in a region predicted by conserved synteny between Poaceae species
TAG Theor. Appl. Genet.
Functional and phylogenetic analysis of a DREB/CBF-like gene in perennial ryegrass (Lolium perenne L.)
Planta
A linkage map of meadow fescue (Festuca pratensis Huds.) and comparative mapping with other Poaceae species
TAG Theor. Appl. Genet.
Chromosomal rearrangements differentiating the ryegrass genome from the Triticeae, oat, and rice genomes using common heterologous RFLP probes
TAG Theor. Appl. Genet.
Arabidopsis transcriptome profiling indicates that multiple regulatory pathways are activated during cold acclimation in addition to the CBF cold response pathway
Plant Cell
A global survey of gene regulation during cold acclimation in Arabidopsis thaliana
PLoS Genet.
Roles of the CBF2 and ZAT12 transcription factors in configuring the low temperature transcriptome of Arabidopsis
Plant J.
The Arabidopsis cold-responsive transcriptome and its regulation by ICE1
Plant Cell
Regulatory gene candidates and gene expression analysis of cold acclimation in winter and spring wheat
Plant Mol. Biol.
Plant responses to cold: transcriptome analysis of wheat
Plant Biotechnol. J.
Transcriptome analysis of cold acclimation in barley albina and xantha mutants
Plant Physiol.
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2021, Acta Ecologica SinicaCitation Excerpt :All of mentioned effects can ultimately result in reduced leaf expansion, wilting and yellow leaves, chlorosis, necrosis, weak germination, stunned seedling and damages to reproductive organs [80,145]. Plants respond to cold stress through different mechanisms: a) The expression of genes related to cold acclimation are up-regulated, such as genes encoding dehydrins (DHN), chloroplast-targeted cold regulated (ct-COR) proteins, ice recrystallization inhibition proteins (IRIP), fructosyl transferase (FST), and C-repeat binding factors (CBF) [113], b) Increase in cell membrane stability with accumulating sugars and antifreeze proteins like dehydrins [111] and modifying lipid composition to increase the unsaturated to saturated ratio [52], c) Elevation of some phytohormones such as SA, JA, ET, and ABA [135], d) Increasing the activity of antioxidants [58,119], e) Accumulation of compatible solutes like amino acids, sugars, carbohydrates, proline and glycine betaine (low molecular weight nitrogen compounds) as osmotic adjustments [52,157], f) Change in nutritive elements amount [141,142], g) Increase in secondary metabolites (SMs) production [114]. In this review we summarize (i) the biosynthesis of phytohormones under cold stress in medicinal plants, (ii) secondary metabolites elicitation under cold stress in those plants (iii) growth, physiological and nutritional responses in medicinal plants under cold stress condition.
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2020, Journal of Plant PhysiologyCitation Excerpt :Plant adaptive response triggered mostly by a gradual decrease in temperature during late autumn, called cold acclimation or hardening, leads to a series of biochemical changes that enhance the cold resistance of sensitive tissues (Pecchioni et al., 2012). Cold acclimation is crucial for induction of genetic mechanisms responsible for FT (Sandve et al., 2011; van der Schoot and Rinne, 2011). From a genetic point of view, FT is a polygenic trait affected by several genes with different chromosome locations (Vágújfalvi et al., 2012).