| Abstract: | Understanding the genetic bases of natural variation for developmental and stress-related traits is a major goal of current plant biology. Variation in plant hormone levels and signaling might underlie such phenotypic variation occurring even within the same species. Here we report the genetic and molecular basis of semidwarf individuals found in natural Arabidopsis thaliana populations. Allelism tests demonstrate that independent loss-of-function mutations at GA locus 5 (GA5), which encodes gibberellin 20-oxidase 1 (GA20ox1) involved in the last steps of gibberellin biosynthesis, are found in different populations from southern, western, and northern Europe; central Asia; and Japan. Sequencing of GA5 identified 21 different loss-of-function alleles causing semidwarfness without any obvious general tradeoff affecting plant performance traits. GA5 shows signatures of purifying selection, whereas GA5 loss-of-function alleles can also exhibit patterns of positive selection in specific populations as shown by Fay and Wu’s H statistics. These results suggest that antagonistic pleiotropy might underlie the occurrence of GA5 loss-of-function mutations in nature. Furthermore, because GA5 is the ortholog of rice SD1 and barley Sdw1/Denso green revolution genes, this study illustrates the occurrence of conserved adaptive evolution between wild A.thaliana and domesticated plants.Bioactive gibberellins (GAs) are plant growth regulators involved in important traits such as seed germination, flowering time, flower development, and elongation growth (1). GA biosynthesis and signaling pathways are well defined (1, 2) and have been targeted in crop breeding. Modification of GA pathways was crucial in the green revolution because it conferred semidwarfness, thus reducing lodging and increasing crop yields (3–6). Green revolution semidwarf varieties in wheat are due to mutations in DELLA genes, whereas many short straw rice varieties carry a mutation in the Semi-Dwarf-1 (SD1) locus. This locus codes for GA 20-oxidase-2, a GA biosynthesis gene that is also mutated in most modern barley varieties in which the gene was called Denso or Semi-dwarf 1 (Sdw1) (7).GA 20-oxidases are involved in the later steps of GA biosynthesis and belong to the group of 2-oxoglutarate–dependent dioxygenases that, together with GA 3-oxidases, form biologically active GA (8). Arabidopsis thaliana has five GA20ox paralogous genes. AtGA20ox-1, AtGA20ox-2, AtGA20ox-3, and AtGA20ox-4 can catalyze the in vitro conversion of GA12 to GA9. Therefore, GA20ox paralogs might have partial redundant functions (9). However, among paralog genes, only AtGA20ox-1 (GA5), which was cloned on the basis of the ga5 mutant (10), affected plant height (8).Natural variation for GA biosynthesis has been previously described in A. thaliana because the Bur-0 accession carries a loss-of-function allele at GA20ox4 (9), which does not result in a semidwarf phenotype. In addition, genetic variation in GA1 has been associated with variation in floral morphology (11). Furthermore, the semidwarf phenotype (here defined as a plant height shorter than half the size of genetically related individuals) observed in the Kas-2 accession is due to a recessive allele at the GA5 locus (12). The latter finding led to the questions of whether green revolution alleles, artificially selected in cereals, could also occur in natural populations of the wild species A. thaliana, and if so, how many different GA5 loss-of-function alleles exist, how they are distributed, and why they occur in some populations. |
