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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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Plant morphology and photosynthesis rate in mutant and transgenic plants with differing expression of NAL1.(a, b) Plant morphology (a) and flag leaves (b) of Taichung 65 (T65) and nal1 mutant line in T65 genetic background (T65-nal1). (c–e) Comparison of N content per unit leaf area (c), N content per unit dry mass (d), and photosynthesis rate (e) of flag leaves at full heading stage between T65 and T65-nal1. Each column represents mean ± s.d. (n = 10); ***P < 0.001 versus T65 (Student's t-test). (f) Plant morphology of Koshihikari and transgenic plants with RNAi-induced suppression of NAL1 in the Koshihikari genetic background (RNAi-NAL1). (g) Relationship between expression level of NAL1 and photosynthesis rate of flag leaves at full heading stage in Koshihikari and RNAi-NAL1 T0 plants. Each circle represents an individual Koshihikari or T0 plant. (h, i) Comparison of N content per unit leaf area (h) and per unit dry mass (i) between Koshihikari and RNAi-NAL1. Each column represents mean ± s.d. (n = 25 for RNAi-NAL1, n = 5 for Koshihikari); ***P < 0.001 versus Koshihikari (Student's t-test).
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f5: Plant morphology and photosynthesis rate in mutant and transgenic plants with differing expression of NAL1.(a, b) Plant morphology (a) and flag leaves (b) of Taichung 65 (T65) and nal1 mutant line in T65 genetic background (T65-nal1). (c–e) Comparison of N content per unit leaf area (c), N content per unit dry mass (d), and photosynthesis rate (e) of flag leaves at full heading stage between T65 and T65-nal1. Each column represents mean ± s.d. (n = 10); ***P < 0.001 versus T65 (Student's t-test). (f) Plant morphology of Koshihikari and transgenic plants with RNAi-induced suppression of NAL1 in the Koshihikari genetic background (RNAi-NAL1). (g) Relationship between expression level of NAL1 and photosynthesis rate of flag leaves at full heading stage in Koshihikari and RNAi-NAL1 T0 plants. Each circle represents an individual Koshihikari or T0 plant. (h, i) Comparison of N content per unit leaf area (h) and per unit dry mass (i) between Koshihikari and RNAi-NAL1. Each column represents mean ± s.d. (n = 25 for RNAi-NAL1, n = 5 for Koshihikari); ***P < 0.001 versus Koshihikari (Student's t-test).

Mentions: The previously identified nal1 mutation affected plant height as well as lateral leaf growth32. However, the relationship between NAL1 and leaf photosynthesis was not examined in that study. To clarify the effect of NAL1 on leaf photosynthesis, we analysed a nal1 mutant in the Taichung 65 genetic background (T65-nal1), which has the same deletion of 30-bp in the fourth exon as previously reported32 (Fig. 4c). T65-nal1 showed severe dwarf plant stature and remarkably smaller and narrower flag leaves than T65 (Fig. 5a, b, Supplementary Fig. S5a–c). However, T65-nal1 had higher flag leaf N content both per unit leaf area and per unit dry weight at full heading than T65 (Fig. 5c, d) and a higher photosynthesis rate than T65 (Fig. 5e). These results suggest that reduction or loss-of-function of NAL1 increased photosynthesis rate.


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)

Plant morphology and photosynthesis rate in mutant and transgenic plants with differing expression of NAL1.(a, b) Plant morphology (a) and flag leaves (b) of Taichung 65 (T65) and nal1 mutant line in T65 genetic background (T65-nal1). (c–e) Comparison of N content per unit leaf area (c), N content per unit dry mass (d), and photosynthesis rate (e) of flag leaves at full heading stage between T65 and T65-nal1. Each column represents mean ± s.d. (n = 10); ***P < 0.001 versus T65 (Student's t-test). (f) Plant morphology of Koshihikari and transgenic plants with RNAi-induced suppression of NAL1 in the Koshihikari genetic background (RNAi-NAL1). (g) Relationship between expression level of NAL1 and photosynthesis rate of flag leaves at full heading stage in Koshihikari and RNAi-NAL1 T0 plants. Each circle represents an individual Koshihikari or T0 plant. (h, i) Comparison of N content per unit leaf area (h) and per unit dry mass (i) between Koshihikari and RNAi-NAL1. Each column represents mean ± s.d. (n = 25 for RNAi-NAL1, n = 5 for Koshihikari); ***P < 0.001 versus Koshihikari (Student's t-test).
© Copyright Policy - open-access
Related In: Results  -  Collection

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

f5: Plant morphology and photosynthesis rate in mutant and transgenic plants with differing expression of NAL1.(a, b) Plant morphology (a) and flag leaves (b) of Taichung 65 (T65) and nal1 mutant line in T65 genetic background (T65-nal1). (c–e) Comparison of N content per unit leaf area (c), N content per unit dry mass (d), and photosynthesis rate (e) of flag leaves at full heading stage between T65 and T65-nal1. Each column represents mean ± s.d. (n = 10); ***P < 0.001 versus T65 (Student's t-test). (f) Plant morphology of Koshihikari and transgenic plants with RNAi-induced suppression of NAL1 in the Koshihikari genetic background (RNAi-NAL1). (g) Relationship between expression level of NAL1 and photosynthesis rate of flag leaves at full heading stage in Koshihikari and RNAi-NAL1 T0 plants. Each circle represents an individual Koshihikari or T0 plant. (h, i) Comparison of N content per unit leaf area (h) and per unit dry mass (i) between Koshihikari and RNAi-NAL1. Each column represents mean ± s.d. (n = 25 for RNAi-NAL1, n = 5 for Koshihikari); ***P < 0.001 versus Koshihikari (Student's t-test).
Mentions: The previously identified nal1 mutation affected plant height as well as lateral leaf growth32. However, the relationship between NAL1 and leaf photosynthesis was not examined in that study. To clarify the effect of NAL1 on leaf photosynthesis, we analysed a nal1 mutant in the Taichung 65 genetic background (T65-nal1), which has the same deletion of 30-bp in the fourth exon as previously reported32 (Fig. 4c). T65-nal1 showed severe dwarf plant stature and remarkably smaller and narrower flag leaves than T65 (Fig. 5a, b, Supplementary Fig. S5a–c). However, T65-nal1 had higher flag leaf N content both per unit leaf area and per unit dry weight at full heading than T65 (Fig. 5c, d) and a higher photosynthesis rate than T65 (Fig. 5e). These results suggest that reduction or loss-of-function of NAL1 increased photosynthesis rate.

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