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Alpine habitats are shaped by harsh abiotic conditions and cold climates. Temperature stress can affect phenotypic plasticity, reproduction, and epigenetic profiles, which may affect acclimation and adaptation. Distribution patterns suggest that polyploidy seems to be advantageous under cold conditions. Nevertheless, whether temperature stress can induce gene expression changes in different cytotypes, and how the response is initialized through gene set pathways and epigenetic control remain vague for non-model plants. The perennial alpine plant Ranunculus kuepferi was used to investigate the effect of cold stress on gene expression profiles. Diploid and autotetraploid individuals were exposed to cold and warm conditions in climate growth chambers and analyzed via transcriptome sequencing and qRT-PCR. Overall, cold stress changed gene expression profiles of both cytotypes and induced cold acclimation. Diploids changed more gene set pathways than tetraploids, and suppressed pathways involved in ion/cation homeostasis. Tetraploids mostly activated gene set pathways related to cell wall and plasma membrane. An epigenetic background for gene regulation in response to temperature conditions is indicated. Results suggest that perennial alpine plants can respond to temperature extremes via altered gene expression. Tetraploids are better acclimated to cold conditions, enabling them to colonize colder climatic areas in the Alps. [ABSTRACT FROM AUTHOR]

Simple Summary: Environmental abiotic stimuli, e.g., temperature stress conditions, can influence the phenotype, reproduction, and epigenetics of plants. How a plant responds to cold temperature stress regarding these aspects, together with the interactions between them and the ploidy level, is still not intensively explored. Herein, we test such effects under experimental cold stress conditions on the species Ranunculus kuepferi, an alpine perennial herb, which mainly occurs in two cytotypes. Results suggest that diploid individuals grow better under warm conditions, while tetraploids prefer cold conditions. Moreover, phenotypic characteristics seem to correlate with the epigenetic patterns. Furthermore, cold stress conditions seem to reduce the reproductive fitness of both cytotypes. We propose that results illustrate that phenotypic plasticity, i.e., the ability of an organism, as a single genotype, to differentially respond to environmental stimuli, may affect the potential of the two cytotypes to tolerate cold stress. Finally, our study follows the geographical distribution of the species, i.e., the phenomenon that asexual taxa occupy larger geographical ranges than their sexual progenitors and extend further toward cold environments at high altitudes, which was previously observed for the natural population of the species in the European Alps. Plant life in alpine habitats is shaped by harsh abiotic conditions and cold climates. Phenotypic variation of morphological characters and reproduction can be influenced by temperature stress. Nevertheless, little is known about the performance of different cytotypes under cold stress and how epigenetic patterns could relate to phenotypic variation. Ranunculus kuepferi, a perennial alpine plant, served as a model system for testing the effect of cold stress on phenotypic plasticity, reproduction mode, and epigenetic variation. Diploid and autotetraploid individuals were placed in climate growth cabinets under warm and cold conditions. Morphological traits (height, leaves and flowers) and the proportion of well-developed seeds were measured as fitness indicators, while flow cytometric seed screening (FCSS) was utilized to determine the reproduction mode. Subsequently, comparisons with patterns of methylation-sensitive amplified fragment-length polymorphisms (AFLPs) were conducted. Diploids grew better under warm conditions, while tetraploids performed better in cold treatments. Epigenetic patterns were correlated with the expressed morphological traits. Cold stress reduced the reproduction fitness but did not induce apomixis in diploids. Overall, our study underlines the potential of phenotypic plasticity for acclimation under environmental conditions and confirms the different niche preferences of cytotypes in natural populations. Results help to understand the pattern of geographical parthenogenesis in the species. [ABSTRACT FROM AUTHOR]

Polyploidization and the shift to apomictic reproduction are connected to changes in DNA cytosine-methylation. Cytosine-methylation is further sensitive to environmental conditions. We, therefore, hypothesize that DNA methylation patterns would differentiate within species with geographical parthenogenesis, i.e., when diploid sexual and polyploid apomictic populations exhibit different spatial distributions. On natural populations of the alpine plant Ranunculus kuepferi, we tested differences in methylation patterns across two cytotypes (diploid, tetraploid) and three reproduction modes (sexual, mixed, apomictic), and their correlation to environmental data and geographical distributions. We used methylation-sensitive amplified fragment-length polymorphism (methylation-sensitive AFLPs) and scored three types of epiloci. Methylation patterns differed independently between cytotypes versus modes of reproduction and separated three distinct combined groups (2x sexual + mixed, 4x mixed, and 4x apomictic), with differentiation of 4x apomicts in all epiloci. We found no global spatial autocorrelation, but instead correlations to elevation and temperature gradients in 22 and 36 epiloci, respectively. Results suggest that methylation patterns in R. kuepferi were altered by cold conditions during postglacial recolonization of the Alps, and by the concomitant shift to facultative apomixis, and by polyploidization. Obligate apomictic tetraploids at the highest elevations established a distinct methylation profile. Methylation patterns reflect an ecological gradient rather than the geographical differentiation. [ABSTRACT FROM AUTHOR]