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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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Expression and protein differences between GPS alleles in Koshihikari and Takanari.(a) Flag leaves in Koshihikari, Koshihikari NIL-GPS, Takanari, and Takanari NIL-GPS. (b) Expression analysis by quantitative real-time PCR of NAL1 in flag leaves at three developmental stages. DBH, days before heading. Each symbol represents mean ± s.d. (n = 4); n.s., not significant between Koshihikari and Takanari (Student's t-test). (c) Western blot analysis of NAL1 protein extracted from flag leaves. Molecular weight marker and samples were run on the same gel and were electro-transferred onto the same membranes. Each column in the graph represents mean ± s.d. (n = 3). *P < 0.05 versus Koshihikari (Student's t-test).
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f6: Expression and protein differences between GPS alleles in Koshihikari and Takanari.(a) Flag leaves in Koshihikari, Koshihikari NIL-GPS, Takanari, and Takanari NIL-GPS. (b) Expression analysis by quantitative real-time PCR of NAL1 in flag leaves at three developmental stages. DBH, days before heading. Each symbol represents mean ± s.d. (n = 4); n.s., not significant between Koshihikari and Takanari (Student's t-test). (c) Western blot analysis of NAL1 protein extracted from flag leaves. Molecular weight marker and samples were run on the same gel and were electro-transferred onto the same membranes. Each column in the graph represents mean ± s.d. (n = 3). *P < 0.05 versus Koshihikari (Student's t-test).

Mentions: When we compared the flag leaf shapes and culm lengths of Koshihikari, Takanari, the reciprocal NILs-GPS, T65-nal1, and RNAi-NAL1, flag leaf width and length in Koshihikari NIL-GPS were decreased compared with Koshihikari (Fig. 6a, Supplementary Fig. S5i, j), but the reduction was less severe than in T65-nal1 and RNAi-NAL1 (Supplementary Fig. S5a, b, e, f, i, j). No difference was observed in culm length between each parental cultivar and the corresponding NIL-GPS (Supplementary Fig. S5k). On the basis of these results, we considered that the Takanari GPS allele might be functional but weaker than the Koshihikari allele. On the other hand, the presence of a retrotransposon insertion in the coding region of Koshihikari (Fig. 4c) might reduce the function relative to the Takanari allele. Therefore, we compared the expression level of NAL1 in the flag leaves of Koshihikari and Takanari at several developmental stages. Quantitative real-time PCR (qRT-PCR) detected the expression of NAL1 in both Koshihikari and Takanari, with no significant difference at any flag leaf developmental stage (Fig. 6b). Further investigation of NAL1 transcripts found that about 20% of the Koshihikari transcripts sequenced contained no retrotransposon insertion, whereas many other transcripts sequenced contained insertion of the full, or partial retrotransposon (Supplementary Fig. S6). Takanari also had many splice variants in NAL1 transcripts (Supplementary Fig. S7). Although a recent study reported several kinds of splice variants for NAL1 transcripts only in an indica cultivar33, our results revealed many splice variants for NAL1 transcripts in both a japonica cultivar, Koshihikari, and an indica cultivar, Takanari. These results indicate that NAL1 expression mechanism is too complicated to explain the cause of the two alleles of GPS by the expression or transcription level of NAL1.


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)

Expression and protein differences between GPS alleles in Koshihikari and Takanari.(a) Flag leaves in Koshihikari, Koshihikari NIL-GPS, Takanari, and Takanari NIL-GPS. (b) Expression analysis by quantitative real-time PCR of NAL1 in flag leaves at three developmental stages. DBH, days before heading. Each symbol represents mean ± s.d. (n = 4); n.s., not significant between Koshihikari and Takanari (Student's t-test). (c) Western blot analysis of NAL1 protein extracted from flag leaves. Molecular weight marker and samples were run on the same gel and were electro-transferred onto the same membranes. Each column in the graph represents mean ± s.d. (n = 3). *P < 0.05 versus Koshihikari (Student's t-test).
© Copyright Policy - open-access
Related In: Results  -  Collection

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

f6: Expression and protein differences between GPS alleles in Koshihikari and Takanari.(a) Flag leaves in Koshihikari, Koshihikari NIL-GPS, Takanari, and Takanari NIL-GPS. (b) Expression analysis by quantitative real-time PCR of NAL1 in flag leaves at three developmental stages. DBH, days before heading. Each symbol represents mean ± s.d. (n = 4); n.s., not significant between Koshihikari and Takanari (Student's t-test). (c) Western blot analysis of NAL1 protein extracted from flag leaves. Molecular weight marker and samples were run on the same gel and were electro-transferred onto the same membranes. Each column in the graph represents mean ± s.d. (n = 3). *P < 0.05 versus Koshihikari (Student's t-test).
Mentions: When we compared the flag leaf shapes and culm lengths of Koshihikari, Takanari, the reciprocal NILs-GPS, T65-nal1, and RNAi-NAL1, flag leaf width and length in Koshihikari NIL-GPS were decreased compared with Koshihikari (Fig. 6a, Supplementary Fig. S5i, j), but the reduction was less severe than in T65-nal1 and RNAi-NAL1 (Supplementary Fig. S5a, b, e, f, i, j). No difference was observed in culm length between each parental cultivar and the corresponding NIL-GPS (Supplementary Fig. S5k). On the basis of these results, we considered that the Takanari GPS allele might be functional but weaker than the Koshihikari allele. On the other hand, the presence of a retrotransposon insertion in the coding region of Koshihikari (Fig. 4c) might reduce the function relative to the Takanari allele. Therefore, we compared the expression level of NAL1 in the flag leaves of Koshihikari and Takanari at several developmental stages. Quantitative real-time PCR (qRT-PCR) detected the expression of NAL1 in both Koshihikari and Takanari, with no significant difference at any flag leaf developmental stage (Fig. 6b). Further investigation of NAL1 transcripts found that about 20% of the Koshihikari transcripts sequenced contained no retrotransposon insertion, whereas many other transcripts sequenced contained insertion of the full, or partial retrotransposon (Supplementary Fig. S6). Takanari also had many splice variants in NAL1 transcripts (Supplementary Fig. S7). Although a recent study reported several kinds of splice variants for NAL1 transcripts only in an indica cultivar33, our results revealed many splice variants for NAL1 transcripts in both a japonica cultivar, Koshihikari, and an indica cultivar, Takanari. These results indicate that NAL1 expression mechanism is too complicated to explain the cause of the two alleles of GPS by the expression or transcription level of NAL1.

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