| Abstract: | Alpine dwarfism is widely observed in alpine plant populations and often considered a high-altitude adaptation, yet its molecular basis and ecological relevance remain unclear. In this study, we used map-based cloning and field transplant experiments to investigate dwarfism in natural Arabidopsis (Arabidopsis thaliana) accessions collected from the Swiss Alps. A loss-of-function mutation due to a single nucleotide deletion in gibberellin20-oxidase1 (GA5) was identified as the cause of dwarfism in an alpine accession. The mutated allele, ga5-184, was found in two natural Arabidopsis populations collected from one geographic region at high altitude, but was different from all other reported ga5 null alleles, suggesting that this allele has evolved locally. In field transplant experiments, the dwarf accession with ga5-184 exhibited a fitness pattern consistent with adaptation to high altitude. Across a wider array of accessions from the Swiss Alps, plant height decreased with altitude of origin, but fitness patterns in the transplant experiments were variable and general altitudinal adaptation was not evident. In general, our study provides new insights into molecular basis and possible ecological roles of alpine dwarfism, and demonstrates the importance of the GA-signaling pathway for the generation of ecologically relevant variation in higher plants.Adaptation to environmental conditions is one of the evolutionary processes that can lead to lineage divergence and the generation of biodiversity (Savolainen et al., 2013). Local adaptation within species may evolve in spatially heterogeneous environments if the strength of divergent selection among populations overrides other evolutionary forces (e.g. genetic drift, gene flow), and is manifested in an increased fitness of local genotypes in the local habitat when compared with foreign genotypes in the local habitat and when compared with fitness of the local genotypes in foreign habitats (Kawecki and Ebert, 2004; Savolainen et al., 2013). It is often a challenge for classic studies of local adaptation to identify traits mediating local adaptation and the underlying genetic architectures. To date, our knowledge on the molecular basis of local adaptation remains remarkably limited, even though this topic has been extensively studied in recent decades (Bergelson and Roux, 2010; Barrett and Hoekstra, 2011). A particular difficulty in studying the molecular basis of local adaptation comes from the need to combine meaningful field experiments together with relevant molecular studies to provide solid evidence on the adaptive value of phenotypes and associated genotypes. Therefore, a complete study of molecular mechanisms of adaptation ideally requires (1) identifying candidate traits under natural selection or relevant for adaptation, (2) isolating genes/loci that influence candidate traits, and (3) quantifying the fitness (adaptive value) conferred by different alleles under natural conditions (Bergelson and Roux, 2010). In the model plant Arabidopsis (Arabidopsis thaliana) and its relatives, as well as in several animal systems, great advances in detecting the molecular basis of adaptation have been made (e.g. Linnen et al., 2009; Fournier-Level et al., 2011; Hancock et al., 2011). Nevertheless, discussions on adaptionist storytelling or of producing molecular spandrels have been recurrent (for review, see Barrett and Hoekstra, 2011).Alpine habitats are characterized by a fine mosaic of heterogeneous and often extreme environmental conditions (Körner, 2003; Byars et al., 2007; Pico, 2012). Along altitudinal gradients, changes in environmental conditions are often steep, and plants growing in alpine areas have developed a variety of morphological and physiological adaptations that allow them to cope with extreme conditions. Alpine plant dwarfism, that is, reduced plant stature with increasing altitude, is one of the most common characteristics observed in plant populations originating from high altitudes (Clausen et al., 1948; Körner, 2003). Alpine dwarfism is thought to help alpine plants take advantage of the higher ambient temperature close to the soil surface, allocate more resources to reproduction, decrease damage from strong wind, and reduce evaporation (Turesson, 1922; Körner, 2003). Therefore, alpine dwarfism is widely considered as adaptive in plants (Turesson, 1922; Clausen et al., 1948; Körner, 2003; Byars et al., 2007; Gonzalo-Turpin and Hazard, 2009). However, whether alpine dwarfism is indeed adaptive and how it is genetically controlled remain unknown in many species. This may be partially attributable to the limited genomic resources that are available for alpine plant species, which are usually nonmodel organisms. Hence, studying the molecular basis of this ecologically important trait in model organisms such as Arabidopsis can give much-needed insights (Bergelson and Roux, 2010).Dwarfism and semidwarfism are important and well-studied traits in agriculture because they help overcome lodging and thus substantially contributed to the green revolution in the last century, the unprecedented increase in crop yields due to the adoption of genetically improved crop varieties (Peng et al., 1999; Khush, 2001). It has repeatedly been found in a diversity of plants that dwarfism and semidwarfism were due to deficiencies in either signaling or biosynthesis of GA (e.g. Spray et al., 1996; Peng et al., 1999; Monna et al., 2002). Dwarfism and dwarfing alleles have also been reported in natural Arabidopsis accessions (Barboza et al., 2013), and other recent studies have shown evidence of population differentiation and climatic adaptation along altitudinal gradients in this model plant (Montesinos et al., 2009; Méndez-Vigo et al., 2011, 2013; Montesinos-Navarro et al., 2011; Pico, 2012; Suter et al., 2014; Luo et al., 2015). In this study, we have investigated plant dwarfism in natural Arabidopsis accessions collected in the Swiss Alps (Supplemental Table S1) and identified a loss-of-function mutation in gibberellin20-oxidase1 (GA5, also called GA20ox1) as the cause of dwarfism in an Arabidopsis accession collected from high altitude (2,012 m above sea level [a.s.l.]). In field transplant experiments, this accession displayed fitness patterns consistent with altitudinal adaptation. Across a larger set of regional accessions, including 10 further accessions without the dwarfing mutation, plant height decreased with altitude of origin; however, this pattern could not be tied to adaptive differentiation along altitude. |
