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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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Leaf anatomical characteristics controlled by GPS.(a, b) Comparison of specific leaf area (SLA) (a) and thickness (b) of flag leaves in Koshihikari, Koshihikari NIL-GPS, Takanari, and Takanari NIL-GPS. LVB, large vascular bundle, SVB, small vascular bundle. (c–f) Cross-sections of flag leaves stained with toluidine blue in Koshihikari (c), Koshihikari NIL-GPS (d), Takanari (e), and Takanari NIL-GPS (f). (g–j) Comparisons of mesophyll cell number (g), mean mesophyll cell size (h), total mesophyll area of cross-section (i), and interveinal distance (j) between LVB and SVB and between SVBs in the four genotypes. Each column represents mean ± s.d. (n = 9). Different letters indicate significant difference at the 5% level (Tukey-Kramer HSD test).
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f7: Leaf anatomical characteristics controlled by GPS.(a, b) Comparison of specific leaf area (SLA) (a) and thickness (b) of flag leaves in Koshihikari, Koshihikari NIL-GPS, Takanari, and Takanari NIL-GPS. LVB, large vascular bundle, SVB, small vascular bundle. (c–f) Cross-sections of flag leaves stained with toluidine blue in Koshihikari (c), Koshihikari NIL-GPS (d), Takanari (e), and Takanari NIL-GPS (f). (g–j) Comparisons of mesophyll cell number (g), mean mesophyll cell size (h), total mesophyll area of cross-section (i), and interveinal distance (j) between LVB and SVB and between SVBs in the four genotypes. Each column represents mean ± s.d. (n = 9). Different letters indicate significant difference at the 5% level (Tukey-Kramer HSD test).

Mentions: The finding that GPS and NAL1 are the same gene suggests that leaf morphological changes affect the photosynthesis rate. Previous studies have shown that leaf anatomical changes can affect leaf photosynthesis3435. We examined specific leaf area (SLA), which is inversely related to leaf thickness36, of flag leaves in Koshihikari, Takanari, and the reciprocal NILs-GPS, and found that the Takanari allele of GPS decreased SLA (Fig. 7a). Both T65-nal1 mutant plants and RNAi-NAL1 transgenic plants also showed lower SLA than either wild-type cultivar (Supplementary Fig. S5d, h). We next observed cross-sections of the central parts of flag leaves in Koshihikari, Takanari, and the reciprocal NILs-GPS, and confirmed that the Takanari allele increased leaf thickness at both large and small vascular bundles (LVB and SVB, respectively; Fig. 7b–f). Because the majority of rice leaf tissue consists of mesophyll cells, we examined mesophyll cell number and size in cross-sections of flag leaves. Although mean mesophyll cell size did not differ between each parental cultivar and the corresponding NIL-GPS, the Takanari allele increased mesophyll cell number between the vascular bundles (Fig. 7g, h), and consequently enlarged the total mesophyll area between the vascular bundles in the cross-sections (Fig. 7i). The Takanari allele did not increase the distance between vascular bundles and in some cases decreased it slightly (Fig. 7j). Taken together, these results suggest that increased mesophyll cell number produced thicker flag leaves and ultimately led to higher photosynthesis rate per unit leaf area in plants with the Takanari allele.


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)

Leaf anatomical characteristics controlled by GPS.(a, b) Comparison of specific leaf area (SLA) (a) and thickness (b) of flag leaves in Koshihikari, Koshihikari NIL-GPS, Takanari, and Takanari NIL-GPS. LVB, large vascular bundle, SVB, small vascular bundle. (c–f) Cross-sections of flag leaves stained with toluidine blue in Koshihikari (c), Koshihikari NIL-GPS (d), Takanari (e), and Takanari NIL-GPS (f). (g–j) Comparisons of mesophyll cell number (g), mean mesophyll cell size (h), total mesophyll area of cross-section (i), and interveinal distance (j) between LVB and SVB and between SVBs in the four genotypes. Each column represents mean ± s.d. (n = 9). Different letters indicate significant difference at the 5% level (Tukey-Kramer HSD test).
© Copyright Policy - open-access
Related In: Results  -  Collection

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

f7: Leaf anatomical characteristics controlled by GPS.(a, b) Comparison of specific leaf area (SLA) (a) and thickness (b) of flag leaves in Koshihikari, Koshihikari NIL-GPS, Takanari, and Takanari NIL-GPS. LVB, large vascular bundle, SVB, small vascular bundle. (c–f) Cross-sections of flag leaves stained with toluidine blue in Koshihikari (c), Koshihikari NIL-GPS (d), Takanari (e), and Takanari NIL-GPS (f). (g–j) Comparisons of mesophyll cell number (g), mean mesophyll cell size (h), total mesophyll area of cross-section (i), and interveinal distance (j) between LVB and SVB and between SVBs in the four genotypes. Each column represents mean ± s.d. (n = 9). Different letters indicate significant difference at the 5% level (Tukey-Kramer HSD test).
Mentions: The finding that GPS and NAL1 are the same gene suggests that leaf morphological changes affect the photosynthesis rate. Previous studies have shown that leaf anatomical changes can affect leaf photosynthesis3435. We examined specific leaf area (SLA), which is inversely related to leaf thickness36, of flag leaves in Koshihikari, Takanari, and the reciprocal NILs-GPS, and found that the Takanari allele of GPS decreased SLA (Fig. 7a). Both T65-nal1 mutant plants and RNAi-NAL1 transgenic plants also showed lower SLA than either wild-type cultivar (Supplementary Fig. S5d, h). We next observed cross-sections of the central parts of flag leaves in Koshihikari, Takanari, and the reciprocal NILs-GPS, and confirmed that the Takanari allele increased leaf thickness at both large and small vascular bundles (LVB and SVB, respectively; Fig. 7b–f). Because the majority of rice leaf tissue consists of mesophyll cells, we examined mesophyll cell number and size in cross-sections of flag leaves. Although mean mesophyll cell size did not differ between each parental cultivar and the corresponding NIL-GPS, the Takanari allele increased mesophyll cell number between the vascular bundles (Fig. 7g, h), and consequently enlarged the total mesophyll area between the vascular bundles in the cross-sections (Fig. 7i). The Takanari allele did not increase the distance between vascular bundles and in some cases decreased it slightly (Fig. 7j). Taken together, these results suggest that increased mesophyll cell number produced thicker flag leaves and ultimately led to higher photosynthesis rate per unit leaf area in plants with the Takanari allele.

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