Drought-induced proline accumulation is widely observed in plants but its regulation and adaptive value are not as well understood. Proline accumulation of the Arabidopsis accession Shakdara (Sha) was threefold less than that of Landsberg erecta (Ler) and quantitative trait loci mapping identified a reduced function allele of the proline synthesis enzyme Δ 1 -pyrroline-5-carboxylate synthetase1 (P5CS1) as a basis for the lower proline of Sha. Sha P5CS1 had additional TA repeats in intron 2 and a G-to-T transversion in intron 3 that were sufficient to promote alternative splicing and production of a nonfunctional transcript lacking exon 3 (exon 3-skip P5CS1). In Sha, and additional accessions with the same intron polymorphisms, the nonfunctional exon 3-skip P5CS1 splice variant constituted as much as half of the total P5CS1 transcript. In a larger panel of Arabidopsis accessions, low water potential-induced proline accumulation varied by 10-fold and variable production of exon 3-skip P5CS1 among accessions was an important, but not the sole, factor underlying variation in proline accumulation. Population genetic analyses suggest that P5CS1 may have evolved under positive selection, and more extensive correlation of exon 3-skip P5CS1 production than proline abundance with climate conditions of natural accessions also suggest a role of P5CS1 in local adaptation to the environment. These data identify a unique source of alternative splicing in plants, demonstrate a role of exon 3-skip P5CS1 in natural variation of proline metabolism, and suggest an association of P5CS1 and its alternative splicing with environmental adaptation.amino acid metabolism | drought adaptation | stress gene expression | osmoprotectant | compatible solute P roline acts as an osmoprotectant and cryoprotectant in organisms as diverse as bacteria, plants, and insects (1, 2). Many plants accumulate proline in response to low water potential (ψ w ) and dehydration caused by drought or freezing. The mechanisms by which proline may promote drought resistance include osmoprotectant functions, as well as newly emerging functions of proline metabolism in NADP/NADPH balance and transfer or storage of energy and reducing potential (1-3). However, the overall importance of proline in drought adaptation is not as firmly established. In Arabidopsis thaliana, transcriptional up-regulation of Δ 1 -pyrroline-5-carboxylate synthetase1 (P5CS1) is essential for low ψ w -induced proline accumulation, and proline accumulation of p5cs1 mutants is only 15-20% of the wild-type level (4-6). Additional regulation of proline metabolism is likely but not understood. The timing and duration of water limitation, as well as other environmental variables, all influence drought-adaptation strategies used by plants. Thus, we may expect substantial natural variation of these traits within a widely distributed species, such as Arabidopsis (7-10), with many of these differences related to the local conditions to which a particular accession has adapted (11-13). Several studies ha...
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