Elsevier

Plant Science

Volume 180, Issue 1, January 2011, Pages 69-77
Plant Science

Review
Molecular mechanisms underlying frost tolerance in perennial grasses adapted to cold climates

https://doi.org/10.1016/j.plantsci.2010.07.011Get rights and content

Abstract

We review recent progress in understanding cold and freezing stress responses in forage grass species, notably Lolium and Festuca species. The chromosomal positions of important frost tolerance and winter survival QTLs on Festuca and Lolium chromosomes 4 and 5 are most likely orthologs of QTLs on Triticeae chromosome 5 which correspond to a cluster of CBF-genes and the major vernalization gene. Gene expression and protein accumulation analyses after cold acclimation shed light on general responses to cold stress. These responses involve modulation of transcription levels of genes encoding proteins involved in cell signalling, cellular transport and proteins associated with the cell membrane. Also, abundance levels of proteins directly involved in photosynthesis were found to be different between genotypes of differing frost tolerance levels, stressing the importance of the link between the function of the photosynthetic apparatus under cold stress and frost tolerance levels. The significance of the ability to undergo photosynthetic acclimation and avoid photoinhibition is also evident from numerous studies in forage grasses. Other interesting candidate mechanisms for freezing tolerance in forage grasses are molecular responses to cold stress which have evolved after the divergence of temperate grasses. This includes metabolic machinery for synthesis of fructans and novel ice-binding proteins.

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

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