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. 2013 Jun 3:4:167.
doi: 10.3389/fpls.2013.00167. eCollection 2013.

Adaptation to seasonality and the winter freeze

Jill C Preston  1 , Simen R Sandve
Affiliations

Adaptation to seasonality and the winter freeze

Jill C Preston et al. Front Plant Sci. .

Abstract

Flowering plants initially diversified during the Mesozoic era at least 140 million years ago in regions of the world where temperate seasonal environments were not encountered. Since then several cooling events resulted in the contraction of warm and wet environments and the establishment of novel temperate zones in both hemispheres. In response, less than half of modern angiosperm families have members that evolved specific adaptations to cold seasonal climates, including cold acclimation, freezing tolerance, endodormancy, and vernalization responsiveness. Despite compelling evidence for multiple independent origins, the level of genetic constraint on the evolution of adaptations to seasonal cold is not well understood. However, the recent increase in molecular genetic studies examining the response of model and crop species to seasonal cold offers new insight into the evolutionary lability of these traits. This insight has major implications for our understanding of complex trait evolution, and the potential role of local adaptation in response to past and future climate change. In this review, we discuss the biochemical, morphological, and developmental basis of adaptations to seasonal cold, and synthesize recent literature on the genetic basis of these traits in a phylogenomic context. We find evidence for multiple genetic links between distinct physiological responses to cold, possibly reinforcing the coordinated expression of these traits. Furthermore, repeated recruitment of the same or similar ancestral pathways suggests that land plants might be somewhat pre-adapted to dealing with temperature stress, perhaps making inducible cold traits relatively easy to evolve.

Keywords: cold acclimation; endodormancy; freezing tolerance; plant adaptation; seasonality; vernalization responsiveness.

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Figures

FIGURE 1
FIGURE 1
Evolution of cold adaptive traits in seed plants. Relationships among major seed plant orders are inferred using representative taxa from Smith et al. (2011) in phylomatic (Webb and Donoghue, 2005). Orders are color-coded as primarily temperate (blue), broadly distributed, or primarily tropical (red) based on the APG website (Stevens, 2001 onward). Blue stars indicate orders where trees are primarily temperate based on Ricklefs (2005). Evidence for endodormancy (E), cold acclimation/freezing tolerance (A), and vernalization responsiveness (V) are denoted for each order with example species. Since most species have not been tested for cold adaptations, absence of data does not necessarily indicate absence of traits. However, since cold climates arose after major radiations in seed plants, presence data (based on Krug, 1991; De la Rosa et al., 2000; Kawamata et al., 2002; Wilson et al., 2002; Karlson et al., 2004; Streck and Schuh, 2005; Lopez and Runkle, 2006; Fausey and Cameron, 2007; Kalberer et al., 2007; Mewes and Pank, 2007; Rohwer and Heins, 2007; Svendsen et al., 2007; Padhye and Cameron, 2008, 2009; Pietsch et al., 2009; Zlesak and Anderson, 2009; Biasi et al., 2010; Byard et al., 2010; Ghelardini et al., 2010; Kaymak and Guvenc, 2010; Kubota et al., 2010; Lenahan et al., 2010; Rantasen and Palonen, 2010; Caffarra et al., 2011; Cave et al., 2011; Charrier et al., 2011; Dogramaci et al., 2011; Lin et al., 2011; Adhikari et al., 2012; Andreini et al., 2012; Bilavcik et al., 2012; Diaz-Riquelme et al., 2012; Nishitani et al., 2012; Sanchez-Perez et al., 2012; Whitman and Runkle, 2012; Alessandro et al., 2013; Guzy-Wrobelska et al., 2013; Jones et al., 2013; Mojtahedi et al., 2013) indicates multiple origins of cold adaptive traits across the phylogeny.
FIGURE 2
FIGURE 2
Effect of cold on plant phenotype. In herbaceous plants (left) such as A. thaliana and wheat, cool autumnal temperatures induce cold acclimation mostly in young leaves, and the acquisition of floral competency in the shoot apical meristem. In A. thaliana, cold acclimation is also induced by short days, and results in a decrease in growth rate through the gibberellic acid pathway, and an increase in freezing tolerance within cells (middle). In woody plants (right) such as pines and birch, endodormancy can be induced as early as late summer and results in the complete cessation of meristematic mitosis. As in herbaceous plants, cool temperatures lead to cold acclimation and a gradual increase in freezing tolerance, sometimes (e.g., deciduous trees) but not always (e.g., evergreen trees) resulting in a reduction in whole-plant growth. At the cellular level, freezing tolerance results from the ability of cells to deal with dehydration, ice crystal formation, biomolecule instability, and disruption to photosynthesis. At the whole-plant level, some freezing tolerant woody plants are able to deal with the increased likelihood of embolism resulting from bubbles formed when dissolved gases are released from frozen xylem sap. Asterisk denotes species-level differences in growth responses to cold acclimation. VR, vernalization responsiveness.
FIGURE 3
FIGURE 3
Hypothetical model showing possible genetic links between cold-regulated growth and reproduction in temperate plants. Expression levels of FT- and SOC1-like flowering integrator genes are maintained at moderate levels in summer by the antagonistic action of long day and warm temperature-regulated genes (A). During cooler temperatures of the autumn, the ICE-CBF-COR cold acclimation pathway is initiated, resulting in a high level of flowering repressors, such as FLC- and SVP-like genes. Although SVP-like gene transcription is dampened by the negative action of FCA- and FVE-like proteins, levels are high enough to work with FLC to repress FT-like and SOC1-like genes, resulting in endodormancy in woody perennials (B). Freezing winter temperatures negatively regulate FRI- and FLC-like genes, or functional equivalents, resulting in the derepression of FT- and SOC1-like genes, and the subsequent negative regulation of cold acclimation genes (C). However, despite up-regulation of FT-like genes in leaves, callus plugs in the shoot apices hinder the floral transition. During warm conditions of the spring, the combination of callus plug decay and long day regulation of FT-like genes results in bud flush and the induction of flowering (D). Unbroken and broken lines represent strong and weak interactions, respectively.
FIGURE 4
FIGURE 4
Importance of gene duplications for the functional evolution of vernalization responsive genes. (A) Simplified phylogeny of the APETALA1/FRUITFULL (AP1/FUL) gene family showing the grass-specific duplication that gave rise to VRN1 based on Litt and Irish (2003) and Preston and Kellogg (2006). (B) Simplified phylogeny of the CCT zinc-finger gene family showing the pooid-specific duplication that gave rise to ZCCT1 and ZCCT2 based on Yan et al. (2004). (C) Simplified phylogeny of the FLOWERING LOCUS C (FLC) gene family showing the Brassicaceae-specific duplication that gave rise to FLC and MAF genes based on Becker and Theissen (2003). Inferred ancestral functions are stated at the base of each tree. Stars denote important duplication events for the evolution of VR. Pooid clades are red, grass clades are purple, monocot clades are orange, Brassicaceae clades are blue, eudicot clades are green, and angiosperm clades are yellow.
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