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A natural variant of NAL1, selected in high-yield rice breeding programs, pleiotropically increases photosynthesis rate.

Takai T, Adachi S, Taguchi-Shiobara F, Sanoh-Arai Y, Iwasawa N, Yoshinaga S, Hirose S, Taniguchi Y, Yamanouchi U, Wu J, Matsumoto T, Sugimoto K, Kondo K, Ikka T, Ando T, Kono I, Ito S, Shomura A, Ookawa T, Hirasawa T, Yano M, Kondo M, Yamamoto T - Sci Rep (2013)

Bottom Line: The high-photosynthesis allele of GPS was found to be a partial loss-of-function allele of NAL1.Furthermore, pedigree analysis suggested that rice breeders have repeatedly selected the high-photosynthesis allele in high-yield breeding programs.The identification and utilization of NAL1 (GPS) can enhance future high-yield breeding and provides a new strategy for increasing rice productivity.

View Article: PubMed Central - PubMed

Affiliation: 1] NARO Institute of Crop Science, Tsukuba, Ibaraki 305-8508, Japan [2] National Institute of Agrobiological Sciences, Tsukuba, Ibaraki 305-8602, Japan [3].

ABSTRACT
Improvement of leaf photosynthesis is an important strategy for greater crop productivity. Here we show that the quantitative trait locus GPS (GREEN FOR PHOTOSYNTHESIS) in rice (Oryza sativa L.) controls photosynthesis rate by regulating carboxylation efficiency. Map-based cloning revealed that GPS is identical to NAL1 (NARROW LEAF1), a gene previously reported to control lateral leaf growth. The high-photosynthesis allele of GPS was found to be a partial loss-of-function allele of NAL1. This allele increased mesophyll cell number between vascular bundles, which led to thickened leaves, and it pleiotropically enhanced photosynthesis rate without the detrimental side effects observed in previously identified nal1 mutants, such as dwarf plant stature. Furthermore, pedigree analysis suggested that rice breeders have repeatedly selected the high-photosynthesis allele in high-yield breeding programs. The identification and utilization of NAL1 (GPS) can enhance future high-yield breeding and provides a new strategy for increasing rice productivity.

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Molecular cloning of GPS.(a, b) High-resolution linkage map of GPS region produced with 8308 F2 plants in the Koshihikari background (a) and 2784 F2 plants in the Takanari background (b). Populations were produced by crossing each cultivar with the corresponding NIL-GPS. The number of recombinants between molecular markers is indicated below the second line in each figure part. Yellow-green shading, regions homozygous for alleles from Koshihikari; dark green, Takanari. Each purple bar in the photosynthesis rate graphs represents the mean ± s.d. (n = 6) of the adjacent genotype. ***P < 0.001; **P < 0.01; n.s., not significant within pairs of recombinant lines (Student's t-test). (c) Gene structure and mutation sites of NAL1 in Koshihikari, Takanari, and nal1 mutant line in Taichung 65 genetic background (T65-nal1). Light blue bars represent exons; white bars represent 5′ and 3′ untranslated regions.
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f4: Molecular cloning of GPS.(a, b) High-resolution linkage map of GPS region produced with 8308 F2 plants in the Koshihikari background (a) and 2784 F2 plants in the Takanari background (b). Populations were produced by crossing each cultivar with the corresponding NIL-GPS. The number of recombinants between molecular markers is indicated below the second line in each figure part. Yellow-green shading, regions homozygous for alleles from Koshihikari; dark green, Takanari. Each purple bar in the photosynthesis rate graphs represents the mean ± s.d. (n = 6) of the adjacent genotype. ***P < 0.001; **P < 0.01; n.s., not significant within pairs of recombinant lines (Student's t-test). (c) Gene structure and mutation sites of NAL1 in Koshihikari, Takanari, and nal1 mutant line in Taichung 65 genetic background (T65-nal1). Light blue bars represent exons; white bars represent 5′ and 3′ untranslated regions.

Mentions: For map-based cloning of GPS, we first used 142 F2 plants derived from Koshihikari × Koshihikari NIL-GPS and 143 from Takanari × Takanari NIL-GPS. GPS was coarsely mapped near the simple sequence repeat (SSR) molecular marker RM3534 in both populations (Fig. 4a, b). For further high-resolution mapping, another 8308 and 2784 F2 plants were used to select plants with recombination near RM3534 through marker-assisted selection in the Koshihikari and Takanari genetic backgrounds, respectively. From this selection, we obtained 26 and 24 plants, respectively. Analysis of recombinant homozygous F3 lines narrowed the candidate region down to the 23.5-kb region between the markers InDel_4_135 and InDel_4_105 in both genetic backgrounds (Fig. 4a, b). The photosynthesis rates in lines carrying the Takanari allele in this region were higher than in those carrying the Koshihikari allele (Fig. 4a, b). The Rice Annotation Project Database (RAP-DB)30 predicts three genes in this region. A bacterial artificial chromosome (BAC) clone containing the candidate genomic region (Taka03G22; Fig. 4b) was obtained by screening a genomic library of Takanari. We determined the sequence of the candidate region in Takanari by using this BAC clone and compared it with the corresponding sequence in Koshihikari, for which the whole genome sequence is now available31. Among the three genes annotated in RAP-DB, we found polymorphisms in the coding region for only one gene, at Os04g0615000. This gene was previously reported as NARROW LEAF1 (NAL1), encoding a plant-specific protein which may be involved in polar auxin transport32. There were ten single-nucleotide polymorphisms (SNPs), three of which encoded amino acid substitutions, in NAL1 between Koshihikari and Takanari (Fig. 4c). A 5895-bp retrotransposon insertion was also found in the second exon of NAL1 in the Koshihikari genome (Fig. 4c).


A natural variant of NAL1, selected in high-yield rice breeding programs, pleiotropically increases photosynthesis rate.

Takai T, Adachi S, Taguchi-Shiobara F, Sanoh-Arai Y, Iwasawa N, Yoshinaga S, Hirose S, Taniguchi Y, Yamanouchi U, Wu J, Matsumoto T, Sugimoto K, Kondo K, Ikka T, Ando T, Kono I, Ito S, Shomura A, Ookawa T, Hirasawa T, Yano M, Kondo M, Yamamoto T - Sci Rep (2013)

Molecular cloning of GPS.(a, b) High-resolution linkage map of GPS region produced with 8308 F2 plants in the Koshihikari background (a) and 2784 F2 plants in the Takanari background (b). Populations were produced by crossing each cultivar with the corresponding NIL-GPS. The number of recombinants between molecular markers is indicated below the second line in each figure part. Yellow-green shading, regions homozygous for alleles from Koshihikari; dark green, Takanari. Each purple bar in the photosynthesis rate graphs represents the mean ± s.d. (n = 6) of the adjacent genotype. ***P < 0.001; **P < 0.01; n.s., not significant within pairs of recombinant lines (Student's t-test). (c) Gene structure and mutation sites of NAL1 in Koshihikari, Takanari, and nal1 mutant line in Taichung 65 genetic background (T65-nal1). Light blue bars represent exons; white bars represent 5′ and 3′ untranslated regions.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3756344&req=5

f4: Molecular cloning of GPS.(a, b) High-resolution linkage map of GPS region produced with 8308 F2 plants in the Koshihikari background (a) and 2784 F2 plants in the Takanari background (b). Populations were produced by crossing each cultivar with the corresponding NIL-GPS. The number of recombinants between molecular markers is indicated below the second line in each figure part. Yellow-green shading, regions homozygous for alleles from Koshihikari; dark green, Takanari. Each purple bar in the photosynthesis rate graphs represents the mean ± s.d. (n = 6) of the adjacent genotype. ***P < 0.001; **P < 0.01; n.s., not significant within pairs of recombinant lines (Student's t-test). (c) Gene structure and mutation sites of NAL1 in Koshihikari, Takanari, and nal1 mutant line in Taichung 65 genetic background (T65-nal1). Light blue bars represent exons; white bars represent 5′ and 3′ untranslated regions.
Mentions: For map-based cloning of GPS, we first used 142 F2 plants derived from Koshihikari × Koshihikari NIL-GPS and 143 from Takanari × Takanari NIL-GPS. GPS was coarsely mapped near the simple sequence repeat (SSR) molecular marker RM3534 in both populations (Fig. 4a, b). For further high-resolution mapping, another 8308 and 2784 F2 plants were used to select plants with recombination near RM3534 through marker-assisted selection in the Koshihikari and Takanari genetic backgrounds, respectively. From this selection, we obtained 26 and 24 plants, respectively. Analysis of recombinant homozygous F3 lines narrowed the candidate region down to the 23.5-kb region between the markers InDel_4_135 and InDel_4_105 in both genetic backgrounds (Fig. 4a, b). The photosynthesis rates in lines carrying the Takanari allele in this region were higher than in those carrying the Koshihikari allele (Fig. 4a, b). The Rice Annotation Project Database (RAP-DB)30 predicts three genes in this region. A bacterial artificial chromosome (BAC) clone containing the candidate genomic region (Taka03G22; Fig. 4b) was obtained by screening a genomic library of Takanari. We determined the sequence of the candidate region in Takanari by using this BAC clone and compared it with the corresponding sequence in Koshihikari, for which the whole genome sequence is now available31. Among the three genes annotated in RAP-DB, we found polymorphisms in the coding region for only one gene, at Os04g0615000. This gene was previously reported as NARROW LEAF1 (NAL1), encoding a plant-specific protein which may be involved in polar auxin transport32. There were ten single-nucleotide polymorphisms (SNPs), three of which encoded amino acid substitutions, in NAL1 between Koshihikari and Takanari (Fig. 4c). A 5895-bp retrotransposon insertion was also found in the second exon of NAL1 in the Koshihikari genome (Fig. 4c).

Bottom Line: The high-photosynthesis allele of GPS was found to be a partial loss-of-function allele of NAL1.Furthermore, pedigree analysis suggested that rice breeders have repeatedly selected the high-photosynthesis allele in high-yield breeding programs.The identification and utilization of NAL1 (GPS) can enhance future high-yield breeding and provides a new strategy for increasing rice productivity.

View Article: PubMed Central - PubMed

Affiliation: 1] NARO Institute of Crop Science, Tsukuba, Ibaraki 305-8508, Japan [2] National Institute of Agrobiological Sciences, Tsukuba, Ibaraki 305-8602, Japan [3].

ABSTRACT
Improvement of leaf photosynthesis is an important strategy for greater crop productivity. Here we show that the quantitative trait locus GPS (GREEN FOR PHOTOSYNTHESIS) in rice (Oryza sativa L.) controls photosynthesis rate by regulating carboxylation efficiency. Map-based cloning revealed that GPS is identical to NAL1 (NARROW LEAF1), a gene previously reported to control lateral leaf growth. The high-photosynthesis allele of GPS was found to be a partial loss-of-function allele of NAL1. This allele increased mesophyll cell number between vascular bundles, which led to thickened leaves, and it pleiotropically enhanced photosynthesis rate without the detrimental side effects observed in previously identified nal1 mutants, such as dwarf plant stature. Furthermore, pedigree analysis suggested that rice breeders have repeatedly selected the high-photosynthesis allele in high-yield breeding programs. The identification and utilization of NAL1 (GPS) can enhance future high-yield breeding and provides a new strategy for increasing rice productivity.

Show MeSH
Related in: MedlinePlus